The Ecology and Behavior of Chickadees and Titmice

This page intentionally left blank

The Ecology and
Behavior of
Chickadees and
Titmice

An integrated approach
EDITED BY

Ken A. Otter

1
3
Great Clarendon Street, Oxford OX2 6DP
Oxford University Press is a department of the University of Oxford.
It furthers the Universitys objective of excellence in research, scholarship,
and education by publishing worldwide in
Oxford New York
Auckland Cape Town Dar es Salaam Hong Kong Karachi
Kuala Lumpur Madrid Melbourne Mexico City Nairobi
New Delhi Shanghai Taipei Toronto
With offices in
Argentina Austria Brazil Chile Czech Republic France Greece
Guatemala Hungary Italy Japan Poland Portugal Singapore
South Korea Switzerland Thailand Turkey Ukraine Vietnam
Oxford is a registered trade mark of Oxford University Press
in the UK and in certain other countries
Published in the United States
by Oxford University Press Inc., New York
Oxford University Press, 2007
The moral rights of the author have been asserted
Database right Oxford University Press (maker)
First published 2007
All rights reserved. No part of this publication may be reproduced,
stored in a retrieval system, or transmitted, in any form or by any means,
without the prior permission in writing of Oxford University Press,
or as expressly permitted by law, or under terms agreed with the appropriate
reprographics rights organization. Enquiries concerning reproduction
outside the scope of the above should be sent to the Rights Department,
Oxford University Press, at the address above
You must not circulate this book in any other binding or cover
and you must impose the same condition on any acquirer
British Library Cataloguing in Publication Data
Data available
Library of Congress Cataloging in Publication Data
Data available
Typeset by Newgen Imaging Systems (P) Ltd., Chennai, India
Printed in Great Britain
on acid-free paper by
Antony Rowe Ltd., Chippenham, Wiltshire

ISBN 9780198569992

10 9 8 7 6 5 4 3 2 1
 Preface
Who cares about chickadees?
This is a fairly common saying of one of my
colleagues, mainly as a means of antagonizing my
students, who have often been talking about their
research during previous moments (to be fair, this
colleague often says the same thing about his
own study species). It is, however, a very good
questionwho does care about chickadees? Having
worked on species in the Paridae family for nearly
15 years, I have always been amazed at the number
of peopleresearchers and non-researchers alike
who do.
I feel there are two primary reasons for the gen-
eral affinity toward this family. First and foremost,
these birds will closely approach humans. The
birds in the Paridae family (Parids) are primarily
non-migratory, and commonly use bird feeders and
nest in suburban environments, which often bring
them into contact with people. Few people in North
America, regardless of their knowledge of birds,
cant count a chickadee or titmouse among the
wildlife that they recognize. This familiarity brings
with it a natural curiosity on the part of the average
person about these birds. Second, they are cute. A
testament to this fact is the number of paintings of
chickadees one sees on various ornamentsan
artist who lived less than a km from where I grew
up made a career of painting stylized watercolors
of fledgling chickadees, which I have seen adorning
coffee mugs all across North America. This factor
shouldnt be underestimated in why people appear
to have a stronger affinity to chickadees than to
other common suburban birds.
But why are these birds so popular with
researchers? The answer is most likely associated
with the first reason indicated above. Parids,
especially the best studied species, tend to tolerate
very close approach by researchers compared to
other species. If one stands still while working on
chickadees, it isnt uncommon for birds to
approach closely enough so as to allow reading the
color-combination of their leg bands with the naked
eye. Such disregard allows researchers to easily
monitor the behavior of their subjects. The result is
greater insight into the subtle aspects of communi-
cation, survival strategies, and social organization
that have resulted in a proliferation of research in
animal behavior, physiology, and experimental
psychology. Further, many species of Eurasian
Parids take readily to nestboxes, and the ease
associated with working on such species has
resulted in some of the longest-term ecological
studies on any bird species (see Chapter 18).
Finally, Parids appear to take readily to aviaries,
allowing for studies and observations that would
be difficult to conduct in field settings.
My own start on studying Parids was
accidentalI had originally started a Masters on
northern saw-whet owls (Aegolius acadicus), but a
fortuitous crash in the owl population forced me to
switch to my supervisors study species, the black-
capped chickadee. Once I began research on these
birds, I discovered the advantages of working with
a species that allowed the detailed behavioral
research I was interested in, coupled with extensive
knowledge on the species upon which to build (my
work on chickadees began the year that Susan
Smith published The Black-Capped Chickadee [Smith
1991]). Chickadees (and titmice) appeared to lend
themselves to a myriad of research avenues, which
I soon found were already being pursued by many
labs around the continent.
It was the fact that so many labs working in so
many disparate fields in evolution, psychology,
neuroethology, ecology, and animal behavior used
chickadees and titmice as study subjects that
became the impetus for this book. Parids are
v
vi P R E FA C E
probably one of the most studied groups of birds
globally, yet some features of the North American
Parids differed markedly from the more exten-
sively studied Eurasian birds. The goal was to
assemble people studying various aspects of
ecology and behavior who used North American
Parids as the primary focal species in their
research. The chapters of this book address particu-
lar topics, rather than address the life histories of
individual species (for excellent life history
accounts, the American Ornithologist Union
Species Accounts are an invaluable supplement
see Table 1). Our goal was to compare research on
North American Parids with their Eurasian
counterparts, and to show how both groups have
contributed to greater understanding of many
disparate fields in biology.
Contributions, workshop and synopses
With the number of studies conducted on North
American chickadees and titmice, it was a difficult
task determining who should be asked to con-
tribute to this work. I assembled prospective con-
tributors by both scanning the literature for groups
that had repeatedly published work on North
American chickadees and titmice in the preceding
5 years, and by contacting those groups that I knew
to be working on various aspects of ecology or
behavior in the family. No such effort can be per-
fectly inclusive, and mine has definitely missed a
couple of people that have added significantly to
the literature on this group over the past year or so.
Nevertheless, this project has succeeded in assem-
bling a very strong cohort of researchers from
Canada and the United States.
Contributors submitted first drafts of chapters in
July 2005. These chapters grouped into the four sec-
tions of the book. Section I focuses on extrinsic and
intrinsic mechanisms controlling various behav-
iors, such as scatter-hoarding and recovery of seeds
in wintering Parids and the control of circannual
and finer-scale aspects of behavior. Section II
groups chapters relating to interspecific and
intraspecific influences on evolution, breeding
and/or social behavior in the North American
Parids. The complexity of vocalizations in this
group has made chickadees a well-studied group in
animal communication, and Section III is devoted
to this aspect of their biology. Finally, recent work
on Parids in North America has begun to focus on
landscape ecology issues relating to dispersal,
adaptation and breeding, which comprise the three
chapters in Section IV of the book. Susan Smith
introduces the North American Parids and the con-
tributions to this volume (Chapter 1), highlighting
the advances in our knowledge of this group since
the publication of her original book on the black-
capped chickadee (Smith 1991). Andr Dhondt
(Chapter 18) concludes the book by comparing the
focus of research efforts between Eurasian and
North American Parid researchers, and surmises
that the different focuses might reflect differences
in the life history patterns of favorite study species
on the two continents.
In August 2005, contributors gathered for the
first North American Parid Workshop in Snowbird,
Utah (Fig. 1). During 2 days, we spent half of our
time individually presenting chapters, and the
other half engaged in discussions about the syner-
gies that could be gained by integrating advances
made by different groups working on parallel (or
sometimes even diverse) topics. The result of this
workshop was the synopses chapters for each of the
four sections of the book. These synopses identify
how the individual chapter contributions comple-
ment to further our understanding of complex eco-
logical or behavioral processes, but as importantly,
also identify where unanswered questions remain
that will provide the impetus for research avenues
over the next decade or more.
Global distributions of the Paridae and
major taxonomic distinctions
Harrap and Quinn (1995) published a thorough
account of the Paridae in their Chickadees, Tits,
Nuthatches and Treecreepers, in which true tits within
the Paridae accounted for 55 species world-wide
subdivided into 10 subgenera (Table 1). These
species occur in largely discrete distributions on
three continental land masses: North America,
Eurasia, and sub-Saharan Africa (Fig. 2). North
American species include members of the Poecile
black- and brown-capped chickadees and tits
and the Baeolophus titmice. Inclusive areas occupied

Figure 1 Participants of the first North American Parid Workshop, standing under an appropriately named ski chair-lift at Snowbird, Utah.
by the various Parid species covers almost the
entire continent from central Mexico to the
Canadian/ Alaskan tundra (see maps in Harrap
and Quinn 1995, or in the species accounts listed
in Table 1).
Eurasia contains groups that span both Europe
and Asia (e.g. the Parus, Cyanistes, Periparus, Poecile,
and Lophophanes groups) and some groups
restricted to Asia (Sittiparus, Parduliparus, and
Machlophus). The combined range of these groups
covers almost the entire Eurasian continent with
the exception of desert regions in the Middle East
and Mongolia. Several Eurasian species occupy the
Northern coastal areas of Africa bordering the
Mediterranean, but a large group of endemic
African species (all in the Melaniparus, a name likely
influenced by the African black-tits) jointly occupy
most of the continent south of the Sahara.
This book focuses predominantly on the North
American Parids, the chickadees in the Poecile and
P R E FA C E vii
the titmice in the Baeolophus groups. Chickadees
occupy a broader expanse of the continent, the var-
ious species occupying a range from the northern
boreal forests of Canada and Alaska to central
Mexico, whereas the titmice have a more southerly
distribution from the northeastern US and Canada
to central Mexico.
Nomenclatural debates and the
potential for resolution
One fly in the Parid ointment has been a disagree-
ment over systematic nomenclature between North
America and Eurasian regulating bodies, which
thankfully appears to be near resolution. In 1998, the
American Ornithologists Union Check-list of North
American Birds (7th Ed) elevated the subgeneric
names to generic level in renaming its Parid species.
This decision was based on work done by Slikas et al.
(1996) on DNA-DNA hybridization that indicated
 viii
P R E FA C E
Table 1 Groupings, distribution, and scientific names of species within the true titsthe family Paridae.

Family Paridae
Subgenera/Genera Common name Genus species Distribution AOU account
Groupings (English)

Poecile Marsh tit Poecile palustris Eurasia

black-capped tits Sombre tit Poecile lugubris Eurasia
Willow tit Poecile montana* Eurasia
White-browed tit Poecile superciliosa Eurasia
Pre Davids tit Poecile davidi Eurasia
Black-capped chickadee Poecile atricapillus North America Smith (1993)
Carolina chickadee Poecile carolinensis North America Mostrom et al. (2002)
Mountain chickadee Poecile gambeli North America McCallum et al. (1999)
Mexican chickadee Poecile sclateri North America Ficken and Nocedal (1992)
brown-capped tits Siberian tit/grey-headed Poecile cincta Eurasia/ Hailman and Haftorn (1995)
chickadee North America
Boreal chickadee Poecile hudsonica North America Ficken et al. (1996)
Chestnut-backed chickadee Poecile rufescens North America Dahlsten et al. (2002)
Varied tit Poecile varia Eurasia
Periparus Coal tit Periparus ater Eurasia
coal tit and allies Spot-winged tit Periparus melanolophus Eurasia
Rufous-vented tit Periparus rubidiventris Eurasia
Rufous-naped tit Periparus rufonuchalis Eurasia
Pardaliparus Elegant tit Periparus elegans Eurasia
Asian tits Palawan tit Periparus amabilis Eurasia
Yellow-bellied tit Periparus venustulus Eurasia
Lophophanes Crested tit Lophophanes cristatus Eurasia
Eurasian crested tits Grey-crested tit Lophophanes dichrous Eurasia
Melaniparus Dusky tit Parus funereus Africa
African tits Carps black tit Parus carpi Africa
Southern black tit Parus niger Africa
White-winged black tit Parus leucomelas Africa
White-shouldered black tit Parus guineensis Africa
 White-bellied black tit Parus albiventris Africa
White-backed black tit Parus leuconotus Africa
Rufous-bellied tit Parus rufiventris Africa
Cinnamon-breasted tit Parus pallidiventris Africa
Red-throated tit Parus fringillinus Africa
Stripe-breasted tit Parus fasciiventer Africa
Acacia tit Parus thruppi Africa
Miombo tit Parus griseiventris Africa
Ashy tit Parus cinerascens Africa
Southern grey tit Parus afer Africa
Parus Great tit Parus major Eurasia
great tit and allies Black-lored tit Parus xanthogenys Eurasia
Turkestan tit Parus bokharensis Eurasia
White-naped tit Parus nuchalis Eurasia
Green-backed tit Parus monticolus Eurasia
Yellow-cheeked tit Parus spilonotus Eurasia
Groundpecker Parus humilis Eurasia
Machlolophus Yellow tit Parus holsti Taiwan
Sittiparus White-fronted tit Parus semilarvatus Eurasia
Cyanistes Blue tit Cyanistes caeruleus Eurasia
blue tit and allies Azure tit Cyanistes cyanus Eurasia
Baeolophus Tufted titmouse Baeolophus bicolor North America Grubb and Pravasudov (1994)
North American titmice Black-crested titmouse Baeolophus atricristatus North America Grubb and Pravasudov (1994)
Oak titmouse Baeolophus inornatus North America Cicero 2000
Juniper titmouse Baeolophus ridgwayi North America Cicero 2000
Bridled titmouse Baeolophus wollweberi North America Nocedal and Ficken (1998)
Related species Sultan tit Melanochlora sultana Eurasia
Yellow-browed tit Sylviparus modestus Eurasia

Nomenclatural conventions are based on the proposed nomenclature from Gill et al. (2005), which has been adopted formally by the American Ornithologists Union (1998,
2000; Banks et al. 2002, 2003) and the British Onithologists Union (Sangster et al. 2005) and advocated by the International Ornithological Congress (Gill and Wright 2006).
Groupings in the first column are divisions (generic/subgeneric) based on Harrap and Quinn (1995)
*Although the masculine species name for the Willow titmontanuswas recommended for adoption by the BOU (Sangster et al. 2005), Poecile is a feminine noun and
the adjectival species names should also be feminized (e.g. montana rather than montanus) as appears in Gill and Wright (2006). The same convention should apply to
P. cincta, P. hudsonica, P. superciliosa. The exception to this rule is P. atricapillus (Banks et al. 2003): this is based on capillus being a noun cap in Latin, and the adjective

P R E FA C E
atri (black) being applied to the noun makes atricapillus a noun string. As such, it does not have to follow the same convention as species names that are adjectives, and the
ending should not be changed to follow gender of the generic name (F. Gill and D. Donsker, personal communication).

ix
x P R E FA C E
Figure 2 Inclusive ranges of the various members of the family Paridae, in global distribution. Members of this family occupy much of the area
of North America, Eurasia, and sub-Saharan Africa. For distributions of individual species, see Harrap and Quinn 1995.
the divisions between subgenera in this family were
as genetically divergent as the distinction between
genera in other families. The result was North
American chickadees being categorized by the
genus Poecile and North American titmice being cat-
egorized by the genus Baeolophus. Further species
divisions were created in North America with the
splitting of the plain titmouse (Parus inornatus) into
two distinct species, the oak and the juniper tit-
mouse (Baeolophus inornatus and B. ridgwayi, respec-
tivelyCicero 2000), as well as the split of the
black-crested titmouse (Baeolophus atricristatus) from
the tufted titmouse (Baeolophus bicolor) into which it
had formerly been placed (Banks et al. 2002).
This nomenclatural elevation of subgeneric
names, however, also assumed that the Eurasian
species would correspondingly be categorized
under the genera, Poecile (black-capped and brown-
capped clades), Cyanistes for the blue tit, Periparus
for the coal tit and its allies, Lophophanes for the
Eurasian crested tits, and the retention of Parus for
the great tit, allies and African tits. A problem arose,
however, as the various governing bodies in Eurasia
did not adopt the suggested nomenclatural changes.
The most egregious division was in the one species
that occurs on both continentsthe Siberian tit (tra-
ditionally Parus cinctus). The race of this species that
occurs in Alaska and the Yukon was officially
renamed the grey-headed chickadee, Poecile cincta,
adopting the newer generic name, and a feminized
version of the species name, despite these not being
recognized as two distinct species.
This resulted in a fair amount of confusion (see
also Chapter 2). The black-capped chickadee has
officially had its names changed from Parus atri-
capillus to Poecile atricapillus (AOU 1998), then to
Poecile atricapilla (AOU 2000); Poecile was a feminine
noun and atricapillus was a masculine adjective. At
the same time, other masculinized species names
were also changede.g. Poecile hudsonica and Poecile
cincta. However, capillus is a Latin noun, and adding
the adjectival suffix atri makes this species name a
noun string, which do not have to follow the same
gender matching consideration as purely adjectival
species names (D. Donsker, IOC Taxonomic Editor,
personal communication). Thus, a later ruling

changed the black-capped chickadee back to Poecile
atricapillus (Banks et al. 2003), as an exception to the
rule. The failure of new generic name adoption
worldwide, however, created additional problems,
as it was not uncommon when publishing in
European journals for the names to be changed back
to Parus from either Poecile or Baeolophus.
The genetic relationship between the various
groups is now well established (Gill et al. 2005
the most recent cladogram is reprinted in
Figure 2.1), and has been relatively consistent across
several genetic techniques (Gill et al. 1993; Slikas
et al. 1996). North American titmice consistently fall
out as a separate taxonomic unit, while North
American chickadees are closely allied with the
Eurasian species of Poecile. Further, the remaining
Eurasian Parids fall into four additional mono-
phyletic groupsParus, which includes birds in
Harrap and Quinns (1995) Parus, Melaniparus and
Machlolophus groups; Cyanistes for the blue tits
and allies; Lophophanes for the Eurasian crested tits;
and Periparus for the coal tit and allies (Gill et al.
2005). The American Ornithologists Union (1998,
2000) and the British Ornithologists Union
(Sangster et al. 2005) have officially adopted these
generic groupings as suggested by Gill et al. (2005).
Further, these listings have been supported by the
International Ornithological Congress (IOC) in Gill
and Wrights (2006) Birds of the World:Recommended
English Names. We have adopted the new nomencla-
ture in the listing of species in Table 1, and all the
contributors of this book urge the international use
of a single naming classification for species world-
wide, so as to maintain the integrity of the concept
of single scientific names. A check of the Inter-
national Commission on Zoological Nomenclatures
(ICZN) official website in Oct 2006, however, still
lists all Eurasian species under Parus, yet strangely
also lists all North American species at least twice,
once under their former Parus designation and also
under their Poecile/Baeolophus designations.
Certain discrepancies remain, primarily around
the gender endings for Eurasian species in the
Poecile group. The BOU officially adopted the name
of the Willow tit as Poecile montanus, although this
species should follow the feminized naming con-
vention (P. montana) used for P. cincta and P. hud-
sonica to be technically accurate (as adopted by Gill
P R E FA C E xi
and Wright 2006). We also urge the immediate
adoption of the feminized versions of P. superciliosa
for the white-browed tit. By the widespread adop-
tion of these naming conventions in all remaining
jurisdictions, we may be able to finally put an end
to this period in the history of the Paridae.
For the remainder of the book, the common
names of the species in the Paridae will be used
without restating the scientific name. Further, refer-
ence to the birds in the family Paridae, will be
referred to as Parids.
Problem of under-represented groups
Upon reading this book, most readers will realize
that we should have titled the book: The Ecology and
Behavior of CHICKADEES and titmice. As with the
Eurasian species, work on North American Parids
has largely focused on a small number of species
(Chapter 18), most notably the black-capped
chickadee. In addition to documenting what is
known about chickadee and titmice, chapters focus
on identifying knowledge gaps that arise from both
understudied aspects of North American Parids
compared to Eurasian Parids, and whether studies
on the black-capped or Carolina chickadee transfer
to other chickadees or the titmice species. The
reader will find that such reflections are a recurrent
focus of chapters throughout this book, which we
make unapologetically as a means of identifying
goals to drive Parid research in the future.
On a global scale, the work presented in this
book highlights where North American Parids dif-
fer or concur with work conducted on Eurasian
species. One of the largest knowledge gaps in our
understanding of Parid ecology and behavior is the
obvious lack of research on the sub-Saharan African
and endemic south-east Asian species. It is our
hope that by identifying these various knowledge
gaps, we ourselves, or a new generation of
researchers, will take up the call and begin parallel
research on less-represented species and groups.
References
American Ornithologists Union (1998). Check-list of North
American Birds, 7th edn. American Ornithologists
Union, Washington, DC.
xii P R E FA C E
American Ornithologists Union. (2000). Forty-second
supplement to the American Ornithologists Union
Check-list of North American Birds. Auk, 117, 847858.
Banks, R. C., Cicero, C., Dunn, J. L., Kratter, A. W.,
Rasmussen, P. C., Remsen, J. V., Rising, J. D., and Stotz,
D. F. (2002). Forty-third supplement to the American
Ornithologists Union Check-list of North American
Birds. Auk, 119, 897906.
Banks, R. C., Cicero, C., Dunn, J. L., Kratter, A. W.,
Rasmussen, P. C., Remsen, J. V., Rising, J. D., and Stotz,
D. F. (2003). Forty-fourth supplement to the American
Ornithologists Union Check-list of North American
Birds. Auk, 120, 923931.
Cicero, C. (2000). Oak titmouse (Baeolophus inornatus) and
Juniper titmouse (Baeolophus ridgwayi). In: Pool, A. and
Gill, F. eds. The Birds of North America, no. 485. The Birds
of North America, Inc., Philadelphia.
Dahlsten, D. L., Brennan, L. A., McCallum, D. A., and
Gaunt, S. L. L. (2002). Chestnut-backed chickadee
(Poecile rufescens). In: Pool, A. and Gill, F., eds. The Birds
of North America, no. 689. The Birds of North America,
Inc., Philadelphia.
Ficken, M. S., McLaren, M. A., and Hailman, J. P. (1996).
Boreal chickadee (Parus hudsonicus). In: Pool, A. and
Gill, F., eds. The Birds of North America, no. 254. The
Academy of Natural Sciences, Washington, D.C.;
The American Ornithologists Union, Philadelphia.
Ficken, M. S. and Nocedal, J. (1992) Mexican chickadee
(Parus sclateri). In: Poole, A., Stettenheim, P., and Gill, F.,
eds. The Birds of North America, no. 8. The Academy of
Natural Sciences, Washington, DC; The American
Ornithologists Union, Philadelphia
Gill, F. B., Mostrom, A. M., and Mack, A. L. (1993).
Speciation in North American chickadees: I. Patterns of
mtDNA genetic divergence. Evolution, 47, 195212.
Gill, F. B., Slikas, B., and Sheldon, F. H. (2005). Phylogeny
of titmice (Paridae): II. Species relationships based on
sequences of the mitochondrial cytochrome-B gene.
Auk, 122, 121143.
Grubb, T. C. Jr and Pravasudov, V. V. (1994). Tufted
titmouse (Parus bicolor). In: Pool, A., and Gill, F., eds.
The Birds of North America, no. 86. The Academy of
Natural Sciences, Washington, DC; The American
Ornithologists Union, Philadelphia.
Gill, F. and Wright, M. (2006) Birds of the World:
Recommended English Names. Princeton University Press,
New Jersey.
Hailman, J. P. and Haftorn, S. (1995). Siberian Tit (Parus
cinctus). In: Pool, A. and Gill, F. eds. The Birds of North
America, no. 196. The Academy of Natural Sciences,
Washington, DC; The American Ornithologists Union,
Philadelphia.
Harrap, S. and Quinn, D. (1995). Chickadees, Tits,
Nuthatches and Treecreepers. Princeton University Press,
Princeton, New Jersey, 464 pp.
McCallum, D. A., Grundel, R., and Dahlsten, D. L. (1999).
Mountain chickadee (Poecile gambeli). In: Pool, A. and
Gill, F. eds. The Birds of North America, no. 453. The Birds
of North America, Inc., Philadelphia.
Mostrom, A. M., Curry, R. L., and Lohr, B. (2002). Carolina
chickadee (Poecile carolinensis). In: Pool, A. and Gill, F.,
eds. The Birds of North America, no. 636. The Birds of
North America, Inc., Philadelphia.
Nocedal, J. and Ficken, M. S. (1998). Bridled titmouse
(Baeolophus wollweberi). In: Pool, A. and Gill, F., eds. The
Birds of North America, no. 375. The Birds of North
America, Inc., Philadelphia.
Sangster, G. Collinson, J. M., Helbig, A. J., Knox, A. G., and
Parkin, D. T. (2005) Taxonomic recommendations for
British birds: third report. Ibis 147, 821826.
Slikas, B., Sheldon, F. H., and Gill, F. B. (1996). Phylogeny
of titmice (Paridae): I. Estimate of relationships among
subgenera based on DNA-DNA hybridization. Journal
of Avian Biology, 27, 7082.
Smith, S. M. (1991). The Black-Capped Chickadee: Behavioral
Ecology and Natural History. Cornell University Press,
Ithaca, New York.
Smith, S. M. (1993). Black-capped chickadee (Parus atri-
capillus). In: Poole, A., Stettenheim, P. and Gill, F., eds.
The Birds of North America, no. 39 The Academy of
Natural Sciences, Washington, DC; The American
Ornithologists Union, Philadelphia.
Ken A. Otter
Ecosystem Science and Management Program
University of Northern British Columbia
Canada
 Acknowledgements
This book would not have been possible without
the enthusiastic contribution of the various authors.
Throughout the process of assembling the work-
shop, acquiring, and cross-reviewing chapters, and
preparing collaborative synopses, everyone
involved has been positive and tolerant of my con-
stant prodding. For this, I thank everyone.
Hosting of the first North American Parid
Workshop at Snowbird, Utah was funded by a
publication grant provided by the University of
Northern British Columbia. For his support on this,
I would like to thank our Vice President of
Research, Max Blouw, for his unfailing efforts to
promote and enhance the research productivity of
people at our institution. Emily Jones, the small
meetings manager, and the staff at Snowbird Resort
were instrumental in organizing the details that
made the workshop a success.
The editorial staff at Oxford University Press, Ian
Sherman, Abbie Headon, Christine Rode and
Stefanie Gehrig, have all been very encouraging
during the effort to put this book together. They
replied quickly and decisively to all queries I put to
them, and have been extremely helpful throughout
this process.
This is the typical place where the author
explains their life-long love of birds has been the
impetus for taking on the task of editing a book. In
actuality, I was much more fascinated by snakes
and lizards as a youth, and I thank my parents,
Alan and Millie Otter, for allowing me to indulge in
this obsession with the purchase of pet lizards,
provision of books on reptiles and putting up with
me bringing home garter snakes whenever possible
(our lab. mascots are still a pair of Anole lizards). I
came to appreciate birds in University through the
mentoring of Dick Cannings and Jamie Smith at
UBC, and to both I am indebted for pointing and
encouraging me on what would become a career
path. During my early work on chickadees, I bene-
fited from interactions with numerous well-estab-
lished Parid researchers whose enthusiasm,
encouragement-and willingness to share these with
an unheard-of grad student-made a lasting impres-
sion; most notable of these were Laurene Ratcliffe,
Susan Smith, Jack Hailman, Andr Dhondt, Peter
McGregor, and Torben Dabelsteen. I had the for-
tune to work on Parids in Europe with the latter
two, and I am thrilled to list the first four as con-
tributors to this book.
The dedication of this book, however, goes to my
wife, Barbara, and my son, Devon. Barbara had to
put up with my being away from home up to
6 months of the year during graduate studies and
postdoctoral work, and has followed me around the
globe during my studies on this family of birds. This
is even more remarkable considering that Barbara is
not a biologist, and exhibits very little enthusiasm
for the grubbiness and bugs typically associated
with field work. Devon (3 years old at the writing of
this) has had to put up with Daddy being gone for
large stretches during the winter and spring, but I
am starting him earlyhe can already identify
black-capped chickadees by both song and call.
xiii
This page intentionally left blank
 Contents

Preface v
Acknowledgements xiii
List of contributors xxiii

1 Introduction to the North American Paridae 1

Susan M. Smith

Section I Proximate mechanisms in behavior and evolution 7

2 Neurobiology of spatial behavior 9

David F. Sherry and Jennifer S. Hoshooley

2.1 Introduction 9
2.2 Food storing in the Paridae 9
2.2.1 Food storing in the wild 9
2.2.2 Memory for cache sites 11
2.2.3 Memory for caches versus other spatial locations 11
2.2.4 Spatial memory in food-storing versus non-storing birds 12
2.3 The hippocampus 14
2.3.1 Comparative studies of the hippocampus 16
2.3.2 Neural processing of spatial information 16
2.3.3 Neurogenesis in the hippocampus of the adult black-capped chickadee 18
2.4 Summary and conclusions 20

3 The relationship between environment, corticosterone, food caching, spatial memory, and
the hippocampus in chickadees 25
Vladimir V. Pravosudov

3.1 Introduction 25
3.2 Inter- and intraspecific differences in caching, spatial memory, and the hippocampus 25
3.2.1 Interspecific differences 25
3.2.2 Intraspecific differences 26
3.3 Unpredictable food, corticosterone, spatial memory, and the hippocampus 29
3.3.1 Seasonality in food caching and spatial memory 29
3.3.2 Seasonal variation in hippocampus volume, neuron number, and neurogenesis rates 29
3.3.3 Photoperiod 30
3.3.4 Unpredictable food supply 31
3.4 Corticosterone, food caching, spatial memory, and the hippocampus 32
3.4.1 Corticosterone in Alaskan and Colorado chickadees 34

xv
xvi CONTENTS

3.5 Dominance, corticosterone, spatial memory, and the hippocampus 35

3.6 Conclusions 38

4 Photoperiodism and the annual cycle of black-capped chickadees 43

Leslie S. Phillmore and Scott A. MacDougall-Shackleton

4.1 Introduction 43
4.1.1 Seasonality 43
4.1.2 Photoperiodism and seasonal reproduction 44
4.1.3 Seasonal neural plasticity 44
4.2 Annual cycle of black-capped chickadees 45
4.2.1 Overview 45
4.3 Photoperiodism and reproduction in black-capped chickadees 46
4.3.1 Comparison with other species 46
4.3.2 Photoperiodism in black-capped chickadees 47
4.4 Seasonal changes in song and the song-control system 48
4.5 Seasonal changes in food storing and the hippocampus 49
4.5.1 Food storing 49
4.5.2 Hippocampus 50
4.6 Future directions 51

5 Fine-scale variation in the timing of reproduction in titmice and chickadees 55

Scott M. Ramsay and Ken A. Otter

5.1 Introduction 55
5.2 The history of research on reproductive timing: Lack 1966 56
5.3 Causes of fine-scale variation in timing among individuals 57
5.3.1 Intrinsic factors 57
5.3.1.1 Female age/genetics 57
5.3.2 Extrinsic factors 57
5.3.2.1 Photoperiod 57
5.3.2.2 Temperature 58
5.3.2.3 Food/energy limitation 58
5.3.3 Population adaptations to local habitat 59
5.4 Effects of fine-scale variation in timing 60
5.4.1 Offspring production and recruitment 60
5.4.1.1 Clutch size 60
5.4.1.2 Synchronization with offspring food supply 60
5.4.1.3 Hatching/fledging success 61
5.4.1.4 Recruitment 61
5.4.2 Future effects on adult fitness components 62
5.4.2.1 Survivorship 62
5.4.2.2 Future breeding costs 62
5.5 Consequences of long-term climatic variation on reproductive timing 63
5.5.1 Cyclical climatic variation 63
5.5.2 Directional climatic variation 64
5.6 Reproductive timing in males 65
5.6.1 Questions/predictions 65
5.7 Conclusions 66
 CONTENTS xvii

Synopsis I Proximate mechanisms in behavior and evolution 71

David F. Sherry, Vladimir V. Pravosudov, Scott A. MacDougall-Shackleton,
Jennifer S. Hoshooley, and Leslie S. Phillmore

Section II Reproductive ecology, evolution, and behavior 75

6 Phylogeography of chestnut-backed chickadees in western North America 77

Theresa M. Burg

6.1 Introduction 77
6.2 Chestnut-backed chickadees 78
6.2.1 Origin 78
6.2.2 Biogeography 78
6.3 Patterns of contemporary population structure 79
6.3.1 Chestnut-backed chickadee 79
6.3.1.1 Interior and coastal populations 81
6.3.1.2 Central, coastal Alaska 82
6.3.1.3 Queen Charlotte Islands 82
6.3.1.4 Private alleles 83
6.3.1.5 Recolonization patterns 85
6.3.2 Comparison to other Parids 86
6.3.2.1 North American chickadees 86
6.3.2.2 Eurasian Parids 86
6.4 Factors influencing population genetics of Parids 88
6.4.1 Postglacial colonization and glacial refugia 89
6.4.2 Disjunct populations 90
6.4.2.1 Mainland populations 90
6.4.2.2 Island populations 90
6.4.3 Limited dispersal within continuous habitat and peripheral populations 90
6.5 Conclusions and perspectives 90

7 Behavioral aspects of chickadee hybridization 95

Robert L. Curry, Lindsay M. Rossano, and Matthew W. Reudink

7.1 Introduction 95
7.2 Background and methods 96
7.2.1 Study sites 96
7.2.2 Field methods 96
7.2.3 Genetic methods 97
7.2.4 Hybrid index scores 97
7.2.5 Song and call recordings 98
7.2.6 Sound analysis 98
7.3 Results 98
7.3.1 Genetic composition of study populations 98
7.3.2 Song patterns beyond and within hybrid zone 99
7.3.3 Chick-a-dee calls beyond and within hybrid zone 101
7.3.4 Lack of congruence between songs and calls 102
7.3.5 Relationships between behavior and genetics 102
7.4 Discussion 103
7.4.1 Hybridization in south-eastern Pennsylvania 103
7.4.2 Song patterns in the Pennsylvania contact zone 103
xviii CONTENTS

7.4.3 Chick-a-dee calls across the hybrid zone 104

7.4.4 Potentially confounding variables in analysis of vocal patterns 104
7.4.5 Completing the behavioral picture of chickadee hybridization 105
7.5 Hybridization throughout the Paridae 105
7.5.1 Other examples in North America 105
7.5.2 Hybridization among Eurasian Parids 106
7.6 Future directions 107

8 Life in the small-bodied cavity-nester guild: Demography of sympatric mountain and

black-capped chickadees within nest web communities under changing habitat conditions 111
Kathy Martin and Andrea R. Norris

8.1 Introduction 111

8.1.1 Parids as members of the nest web 111
8.1.1.1 Mountain chickadees 112
8.1.1.2 Black-capped chickadees 112
8.1.1.3 Possible competitors of chickadees 112
8.1.2 Facilitators of small-bodied cavity-nesters 115
8.1.3 Predators of small-bodied cavity-nesters 115
8.1.4 Interspecific interactions among small-bodied cavity-nesters 115
8.2 Study area and habitat change 116
8.3 Data analysis 117
8.3.1 Population growth models 118
8.3.2 Excavation history, nest tree, and cavity characteristics 118
8.3.3 Site level changes in mountain chickadee populations using population
growth models 120
8.3.3.1 Population size 120
8.3.3.2 Nest density 121

9 Social dominance and fitness in black-capped chickadees 131

Laurene Ratcliffe, Daniel J. Mennill, and Kristin A. Schubert

9.1 Introduction 131

9.2 General methods 132
9.2.1 Winter field methods 132
9.2.2 Spring field methods 133
9.3 Correlates of social rank 133
9.3.1 Age 134
9.3.2 Sex 135
9.3.3 Seniority 135
9.3.4 Size and condition 135
9.3.5 Plumage 136
9.3.6 Vocalizations 137
9.4 Hierarchy formation and maintenance 137
9.4.1 Consistency in dominance relationships between sites 139
9.5 Variation in rank acquisition 139
9.6 Rank, survival, and lifetime reproductive success 140
9.6.1 Survival 140
9.6.2 Reproductive success 141
9.7 Future research 143
 CONTENTS xix

Synopsis II Parid reproductive behavior 147

Daniel J. Mennill, Theresa M. Burg, Robert L. Curry, Kathy Martin, Andrea R. Norris,
Laurene Ratcliffe, Matthew W. Reudink, Lindsay M. Rossano, and Kristin A. Schubert

Section III Vocal communication 151

10 Chickadee vocal production and perception: An integrative approach to understanding

acoustic communication 153
Christopher B. Sturdy, Laurie L. Bloomfield, Isabelle Charrier, and Tiffany T.-Y. Lee

10.1 Introduction 153

10.2 Song production and perception 153
10.2.1 Song production 153
10.2.2 Song perception 155
10.2.2.1 Playback experiments of song perception 156
10.2.2.2 Operant conditioning experiments of song perception 157
10.3 Call production and perception 159
10.3.1 Call production 159
10.3.2 Call perception 161
10.3.2.1 Playback studies of call perception 161
10.3.2.2 Operant conditioning studies of call perception 162
10.4 Summary and future directions 164

11 The gargle call of black-capped chickadees: ontogeny, acoustic structure, population

patterns, function, and processes leading to sharing of call characteristics 167
Myron C. Baker and David E. Gammon

11.1 Introduction 167

11.2 The gargle 168
11.2.1 Brief description of the call 168
11.2.2 Ontogeny of the call 168
11.3 Features of the call and population patterns 171
11.3.1 Persistence and change in gargle calls over time 174
11.3.2 Year-to-year changes in repertoires of individuals 174
11.4 Contexts of use of the call 174
11.5 Interactive playback experiment I 175
11.6 Aviary experiments on gargle changes 175
11.7 Interactive playback experiment II 177
11.8 Combined analysis of interactive playback tests 177
11.9 Synthesis of theory and empirical results 178

12 How postdispersal social environment may influence acoustic variation in birdsong 183
David E. Gammon

12.1 Introduction 183

12.2 Description of model and hypothesis 184
12.3 Description of study system 185
12.4 Acoustic variation before and after the bottleneck 187
12.4.1 Sampling procedure 187
xx CONTENTS

12.4.2 Analysis of data 188

12.4.3 Effect of the bottleneck 189
12.5 Comparison of acoustic variation in Fort Collins 2004 and Islands North 190
12.6 Acoustic variation within juveniles 191
12.7 Ages of singing adults in 2004 191
12.8 Synthesis of empirical results 191
12.8.1 Potential explanations 192
12.8.2 How postdispersal social environment may affect song development 192
12.8.3 Future studies needed 193
12.9 On the origin and maintenance of acoustic variation in birdsong 194
12.9.1 Acoustic variation across space and time in Parids 194
12.9.2 Development of song in Parids 194
12.9.3 Does the possession of novel song material affect reproductive fitness? 194
12.9.4 Implications for the origin and maintenance of dialects and repertoires 195

13 Information and the chick-a-dee call: Communicating with a complex vocal system 199
Jeffrey R. Lucas and Todd M. Freeberg

13.1 Introduction 199

13.2 Information and the chick-a-dee call 200
13.2.1 Basic note types of chick-a-dee calls 200
13.2.2 Variability in note types 200
13.2.3 Signal redundancy 204
13.2.4 Identity 204
13.2.5 Syntactical information 205
13.2.5.1 Syntax 205
13.2.5.2 Context 207
13.2.5.3 Playback studies 209
13.3 Conclusions, concessions, and a call for comparative work 209

14 Status signaling and communication networks in chickadees: Complex communication

with a simple song 215
Daniel J. Mennill and Ken A. Otter

14.1 Introduction 215

14.2 The fee-bee song: Variation on a two-note theme 215
14.3 Context of singing in chickadees 217
14.3.1 Singing context 1: Diurnal countersinging interactions 217
14.3.1.1 Variation in song frequency during countersinging interactions 218
14.3.1.2 Variation in song timing during countersinging interactions 219
14.3.2 Singing context 2: The dawn chorus 220
14.4 Communication networks 222
14.4.1 Male eavesdropping in black-capped chickadees 222
14.4.2 Female eavesdropping in black-capped chickadees 224
14.4.3 Nest cavities and male singing behavior 227
14.5 Singing behavior in other North American Parids 229
14.6 Summary and future studies 230
 CONTENTS xxi

Synopsis III Complexities in vocal communication 235

Todd M. Freeberg, Myron C. Baker, Laurie L. Bloomfield, Isabelle Charrier,
David E. Gammon, Jack P. Hailman, Tiffany T.-Y. Lee, Jeffrey R. Lucas, Daniel J. Mennill,
and Christopher B. Sturdy

Overview 235
Vocal complexity of chickadees and titmice 235
The song versus call distinction and social complexity 236
Methodological advances 237
What is to be done? 237

Section IV Landscape ecology, behavior, and conservation issues 241

15 Edge, patch, and landscape effects on Parid distribution and movements 243
Andr Desrochers and Marc Blisle

15.1 Introduction 243

15.2 Response to edges by Parids 243
15.2.1 Food abundance 244
15.2.2 Microclimate 244
15.2.3 Predator avoidance 245
15.2.4 Movement corridors 245
15.3 Responses to patches 247
15.4 Beyond the patch: response to landscapes 248
15.5 Parids as leaders of other forest birds 257
15.6 Conclusions 258

16 Winter adaptations in chickadees and titmice and the added effect of habitat
fragmentation 263
Jennifer R. Olson and Thomas C. Grubb, Jr

16.1 Introduction 263

16.2 Physiological adaptations to winter conditions 263
16.2.1 Nocturnal hypothermia and seasonal metabolic adjustments 263
16.2.2 Thermogenesis by shivering 265
16.3 Behavioral modifications and ecological adaptations to winter conditions 266
16.3.1 Over-wintering in heterospecific flocks 266
16.3.2 Foraging behavior and food caching 268
16.3.3 Cavity roosting 268
16.4 Responses to habitat fragmentation 269
16.4.1 Species richness and density 270
16.4.2 Woodlot edge effect 270
16.5 Effects of fragmentation on wintering permanent resident birds 270
16.5.1 Survivorship 270
16.5.2 Effects of wind and temperature on isolated woodlots 271
16.5.3 Woodlot connectivity and interpatch movement 273
xxii CONTENTS

17 Habitat quality and reproductive behavior in chickadees and tits: Potential for habitat
matrix use in forest generalists 277
Ken A. Otter, Harry van Oort, and Kevin T. Fort

17.1 Introduction 277

17.2 Fragmentation, the matrix, and halo effects 278
17.3 Habitat variation and reproductive success in the Paridae 280
17.3.1 Matrix of similar age or structure but dissimilar species composition 280
17.3.1.1 Blue tits in evergreen versus deciduous oak forests 280
17.3.1.2 Comparison of blue tits to greats tits and other study sites 282
17.3.2 Matrix: Habitat of similar species but dissimilar age 282
17.3.2.1 Chickadees breeding in mature versus young forestssettlement 283
17.3.2.2 Habitat quality and reproductive success in chickadees 284
17.3.2.3 Habitat quality and condition-dependent behaviors in chickadees 285
17.4 Parids and insight into the use of matrix in conservation planning 288

Synopsis IV Landscape ecology, behavior, and conservation issues 293

Andr Desrochers, Ken A. Otter, Marc Blisle, and Jennifer R. Olson

Introduction 293
Focus on the Parids 293
Global perspective 293
Dispersal 294
Habitat selection at the individual level 295
Parids as a model group 296

18 What drives differences between North American and Eurasian tit studies? 299
Andr A. Dhondt

18.1 Introduction 299

18.2 Natural history traits determine the ease of study and the questions asked 299
18.3 The value of long-term studies: Providing answers to questions not yet asked 302
18.3.1 Spring phenology 302
18.3.2 Dispersal and local adaptation 303
18.3.3 Effects of habitat fragmentation 303
18.4 Winter group territoriality: A derived trait that leads to winter limitation 305
18.5 Studies of hybrid zones 307
18.6 Conclusions 307

Index 311
 Contributors
Myron C. Baker, Professor Emeritus, Department
of Biology, Colorado State University, Fort
Collins, Colorado 80523, USA.
mcbaker@lamar.colostate.edu
Marc Blisle, Assistant Professor, Dpartement de
Biologie, Universit de Sherbrooke, 2500 boul. de
lUniversit Sherbrooke, Qubec J1K 2R1, Canada.
marc.m.belisle@usherbrooke.ca
Laurie L. Bloomfield, Doctoral Student,
Department of Psychology and Centre for
Neuroscience, P-217 Biological Sciences
Building, University of Alberta, Edmonton,
Alberta T6G 2E9, Canada.
laurie.bloomfield@ualberta.ca
Theresa M. Burg, Assistant Professor,
Department of Biological Sciences,
University of Lethbridge, 4401 University Drive,
Lethbridge, Alberta, T1K 3M4, Canada.
theresa.burg@uleth.ca
Isabelle Charrier, Postdoctoral Fellow, Department
of Psychology and Centre for Neuroscience, P-
217 Biological Sciences Building, University of
Alberta, Edmonton, Alberta T6G 2E9, Canada.
isabelle.charrier@ibaic.u-psud.fr
Robert L. Curry, Associate Professor, Department
of Biology, Villanova University, 800 Lancaster
Ave., Villanova, Pennsylvania 19085, USA.
robert.curry@villanova.edu
Andr Desrochers, Director, Centre dtude de la
fort, Facult de foresterie and gomatique,
Universit Laval, Qubec City, Qubec G1K 7P4,
Canada.
andre.desrochers@sbf.ulaval.ca
Andr A. Dhondt, Edwin H. Morgens Professor of
Ornithology and Director of Bird Population
Studies, Department of Ecology and
Evolutionary Biology, Cornell Laboratory of
Ornithology, 159 Sapsucker Woods Road,
Cornell University Ithaca, NY 14850, USA.
aad4@cornell.edu
Kevin T. Fort, Species at Risk Biologist, Canadian
Wildlife Service, Pacific Wildlife Research
Centre, 5421 Robertson Rd. RR#1, Delta, BC V4K
3N2, Canada.
Kevin.Fort@ec.gc.ca
Todd M. Freeberg, Assistant Professor,
Department of Psychology, Austin Peay Building
303A, University of Tennessee, Knoxville, TN
37996, USA. tfreeber@utk.edu
David E. Gammon, Assistant Professor, Campus Box
2625, Elon University Elon, NC 27244-2010, USA.
dgammon@elon.edu
Thomas C. Grubb Jr, Professor of Evolution,
Ecology, and Organismal Biology, Ohio State
University, 318 West 12th, Columbus, Ohio
43210-1293, USA.
grubb.1@osu.edu
Jack P. Hailman, Professor Emeritus, Zoology,
University of Wisconsin, Madison and Research
Associate, Archbold Biological Station, Old SR 8
(County 17), Venus, FL 33960, USA.
JHailman@Wisc.edu
Jennifer S. Hoshooley, Doctoral Student,
Department of Psychology and Program in
Neuroscience, University of Western Ontario,
London, Ontario N6A 5C2, Canada.
jmckay4@uwo.ca
Tiffany T-Y. Lee, Doctoral Student, Department of
Psychology and Centre for Neuroscience, P-217
Biological Sciences Building, University of
Alberta, Edmonton, Alberta T6G 2E9, Canada.
ttylee@gmail.com
Jeffrey R. Lucas, Professor, Dept of Biological
Sciences, Purdue University, West Lafayette, IN
47907, USA.
jlucas@bilbo.bio.purdue.edu
xxiii
xxiv C O N T R I B U TO R S
Scott A. MacDougall-Shackleton, Associate
Professor, Department of Psychology, University
of Western Ontario, London, Ontario N6A 5C2,
Canada.
smacdou2@uwo.ca
Kathy J. Martin, Professor, Centre for Applied
Conservation Research, Forest Sciences
Department, University of British Columbia,
Vancouver, BC V6T 1Z4, Canada.
kmartin@interchange.ubc.ca
Daniel J. Mennill, Assistant Professor, Department
of Biological Sciences, University of Windsor,
Windsor, Ontario N9B 3P4, Canada.
dmennill@uwindsor.ca
Andrea R. Norris, Masters Student, Centre for
Applied Conservation Research, Forest Sciences
Department, University of British Columbia,
Vancouver, BC V6T 1Z4, Canada.
arnorris@interchange.ubc.ca
Jennifer R. Olson, Doctoral Student, Department
of Evolution, Ecology, and Organismal Biology,
Ohio State University, 356 Aronoff Laboratory
318 West 12th, Columbus, Ohio 43210-1293, USA.
olson.133@osu.edu
Ken A. Otter, Associate Professor (Biology)
Ecosystem Science and Management Program,
University of Northern British Columbia, 3333
University Way, Prince George, British Columbia
V2N 4Z9, Canada.
otterk@unbc.ca
Leslie S. Phillmore, Assistant Professor
Department of Psychology, Dalhousie
University, Life Sciences Centre, 1355 Oxford
Street Halifax, Nova Scotia B3H 4J1, Canada
leslie.phillmore@dal.ca
Vladimir V. Pravosudov, Assistant Professor,
Department of Biology, University of Nevada,
Reno M/S 314 Reno, NV 89557, USA.
vpravosu@unr.edu
Scott M. Ramsay, Assistant Professor,
Dept of Biology, Wilfrid Laurier University,
Waterloo, Ontario N2L 3C5, Canada.
sramsay@wlu.ca
Laurene M. Ratcliffe, Professor and Associate
Dean of Arts and Sciences, Department of
Biology, Queens University, Kingston,
Ontario K7L 3N6, Canada.
ratcliff@biology.queensu.ca
Matthew W. Reudink, Doctoral Student,
Department of Biology, Queens University,
Kingston, Ontario K7L 3N6, Canada.
reudinkm@biology.queensu.ca
Lindsay M. Rossano, Biologist, Mid-Atlantic
Associates, Inc., Colmar, PA 18951, USA.
lindsay.rossano@villanova.edu
Kristin A. Schubert, Doctoral Student, Behavioral
Biology Research Group, University of
Groningen, P.O. Box 14, 9750 NN Haren, The
Netherlands.
k.a.schubert@rug.nl
David F. Sherry, Professor, Department of
Psychology and Program in Neuroscience,
University of Western Ontario, London, Ontario
N6A 5C2, Canada.
sherry@uwo.ca
Susan M. Smith, Norma Wait Harris and
Emma Gale Harris Foundation Professor of
Biological Sciences, Department of
Biological Sciences, Mount Holyoke College,
50 College Street, South Hadley, MA 01075,
USA.
ssmith@mtholyoke.edu
Christopher B. Sturdy, Assistant Professor and
Alberta Ingenuity Researcher, Department of
Psychology, University of Alberta, P217
Biological Sciences Building, Edmonton, Alberta
T6G ZE9, Canada.
csturdy@ualberta.ca
Harry van Oort, Biologist, Kingbird Biological
Consulting P.O. Box 8617, Revelstoke, B.C. VOE
2S2, Canada.
hvanoort@gmail.com
 CHAPTER 1
Introduction to the North
American Paridae
Susan M. Smith
An amazing amount of new information has been
discovered since I published my first book on
chickadees (Smith 1991). Among the most funda-
mental of these advances is the work of Frank Gill
and his colleagues on the genetic relationships
within the Family Paridae. Working with mito-
chondrial DNA, in particular the mitochondrial
cytochrome-B gene, Gill et al. (2005) have arrived at
an overview of the degree of relatedness among the
members of this avian family. Evidently there have
been two independent invasions of North America
by Parids. The first of these is estimated to have
occurred approximately 4 million years ago (mya),
and led to the present species of crested titmice in
this continent. The second invasion, about 3.5 mya,
led to the chickadees (Gill et al. 2005).
It is unfortunate that there has been a general lack
of agreement as to whether the distinct lineages
among Parids world-wide, as described by Gill and
his colleagues, should be considered as distinct,
separate genera (as adopted by the American
Ornithologist Union in North America in the 1990s),
or whether these should be merely subgenera (the
prevalent view until recently on the other side of the
Atlantic see Preface). This disagreement between
North American and European editors led to the
rather confusing situation in which the species I
work with, the black-capped chickadee, remains
Parus atricapillus in European journals, while having
undergone the unfortunate and convoluted journey
through Poecile atricapilla to Poecile atricapillus in
North American journals. Be that as it may, the
important thing is that this work has clarified which
species belong in which lineages, and how closely
each of these lineages is to the others. All North
American crested titmice are in the same lineage,
which is closest to, but distinct from, that of the
Eurasian crested tits. By contrast, while all of the
North American chickadees are in the same basic
group, they have not diverged sufficiently from cer-
tain Eurasian relatives (e.g. willow and marsh tits,
among others) to be considered a separate lineage
from those species. The recent adoption of the new
generic names by the British Ornithologists Union
and International Ornithological Congress for all
tits world-wide appears to be finally resolving this
issue (see Preface).
North American chickadees can be further
divided into two phenotypically distinct groups:
those with black caps and whistled songs (the black-
capped, Carolina, mountain and Mexican chicka-
dees); and those with brown or grey caps, which
typically lack whistled songs (the chestnut-backed,
boreal chickadees, and Siberian tits). In general, a lot
more work has been done on the first four species; it
is therefore particularly welcome to have a chapter
in this book exploring the phylogeography of chest-
nut-backed chickadees (Chapter 6). Although three
subspecies of chestnut-backed chickadees are recog-
nized, microsatellite analysis indicates that there are
actually four genetically distinct populations now
alive: two in British Columbia (Queen Charlotte
Islands, and south-eastern B.C.); one confined
to Alaska (central Alaska); and a large coastal
group. Burg set out to discover how this particular
distribution has arisen. In particular, she was
exploring the effect of Pleistocene glaciations on the
evolution of these four lineages. Based on careful
analysis of the genetic differences and similarities
between and among these four groups, Burg has
1
2 I N T R O D U C T I O N TO T H E N O RT H A M E R I C A N PA R I D A E
concluded that the current distribution and lineages
of chestnut-backed chickadees is the result of
colonization (after glaciation) from multiple refugia,
rather than having either a single northern or single
southern source.
Another chapter using molecular biological tech-
niques is that of Curry et al. (Chapter 7), working
with black-capped and Carolina chickadees. These
two species, while evidently not each others closest
relatives (Gill et al. 1993, 2005), are nevertheless the
two chickadee species that interbreed most regularly,
along a quite long and broad hybrid zone. Curry and
his colleagues work on this hybrid zone reveals a
dynamic situation in which the Carolina genes
appear to be pushing northward into what was for-
merly purely black-capped chickadee populations.
This is rather horrifying information to people like
me who count on knowing what species they are
working on! In the broad zone of interbreeding,
Curry documents that an individual birds morpho-
logical characteristics might suggest it is purely one
species, while its vocalizations might be very typic-
ally the other speciesand genetically it might be
anywhere along a continuum from either pure
species. As Curry and his colleagues point out, mor-
phological features such as feather edgings or bib size
might be genetically based, but at least some aspects
of vocalizations, in particular whistled songs, must
be learned; hence even a purely Carolina chickadee
might sing a black-capped chickadee song, and vice
versa. And now Curry and his colleagues are finding
a trend for increasing numbers of bilingual birds in
their study areas. This applies not only to whistled
songs, but also to some true calls (especially the dee
calls of the chick-a-dee call complex). And just to make
it even more confusing, a given birds calls similarity
to one of the pure species has no particular correl-
ation with the same individuals songs similarity:
that is, an individual might give a black-capped
chickadee whistled song, but have the shorter dee
notes of a Carolina chickadee in its chick-a-dee call
notes. And now Curry et al. have shown that birds
giving more Carolina-like calls had more black-
capped-like hybrid index scores. I pity the poor
female attempting to make a suitable mate choice in
a situation like this! Actually, Curry et al. conclude
that vocal patterns may be less important than other
aspects of the birds mating systems. Nevertheless, it
is clear that a lot of mistakes are made, as the hybrid
zone is broad and pushing rapidly northward.
One of the rather startling findings of Gill and his
colleagues is that, despite this broad and dynamic
hybrid zone, it is the mountain chickadee, rather
than the Carolina, that is the species most closely
related to black-capped chickadees. Martin and
Norris (Chapter 8) have explored some ecological
aspects of an area in the interior of British Columbia
where these two species are sympatric. One
important difference between the two is that
black-capped chickadees typically excavate their
own nest cavities, while mountain chickadees must
depend on cavities created by other birds.
Martin and Norris work in an area with fluctuat-
ing food supply for nesting chickadees. One of the
really interesting findings they have is that in years
with a high insect food supply, mountain chicka-
dees were able to increase their nest density far
more strongly than could the rarer, but dominant,
black-capped chickadees. It would be really inter-
esting to follow up their suggestion and attempt to
measure the actual cost of nest site excavation.
Another factor to investigate is whether the
black-capped chickadees might respond to increas-
ing food levels not by varying their breeding
density but rather by increasing their clutch size.
Ratcliffe, Mennill, and Schubert (Chapter 9)
examine factors affecting winter social rank and
fitness in black-capped chickadees. Their work has
documented a variety of factors that can influence a
given birds position in its winter flock (I might
remind the reader that the relative rank between
members of a breeding pair typically reverses in the
breeding season, with females becoming dominant
over their mates, Smith 1980).
The effects of age and of sex are both well known.
Ratcliffe et al. have gone well beyond these (while
further clarifying and quantifying the effects of
both). Some of the correlates with dominance
that they have found include body condition:
high-ranked chickadees of each sex are leaner than
lower-ranking birds (thus making them more
maneuverable in predator escape situations).
Ratcliffes group has also shown that plumage
characteristics, like the darkness of the cap and bib,
and brighter white, is correlated with rank, at least
in males. They have also shown that higher-ranked
 I N T R O D U C T I O N TO T H E N O RT H A M E R I C A N PA R I D A E
unpaired males are selected faster by females (Otter
and Ratcliffe 1996).
How is initial rank achieved and maintained?
Ratcliffe et al. have found, at least for males, that the
suppression hypothesis, which states that domin-
ant individuals condition their subordinates to lose
through ongoing attacks, best fits the observed
behavior in the field. Finally, they found, again just
for males, that males that lived longer (and thus
achieved higher rank) did indeed have greater fit-
ness, as measured by lifetime reproductive success;
nevertheless this seemed to be a reflection simply of
whether or not the males reproduced at all, rather
than showing any finer-scale difference between
individuals.
Another area in which an enormous amount of
work has been done since 1991 is physiology, includ-
ing (especially) neurophysiology. One of the major
areas of advance concerns neurophysiological
aspects of food storage, or caching behavior. Black-
capped chickadees, and other members of the Poecile
group, are scatter-hoarders: they can store hundreds
and often thousands of seeds, each in a different
place. There is now abundant evidence, especially for
black-capped chickadees, that the birds can remem-
ber precisely where they stored particular items, and
then can go back and retrieve the stored food.
Exploration of this behavior has proceeded along
several lines. One is purely behavioral. In a
particularly elegant experiment (Brodbeck 1994)
showed that black-capped chickadees used a
hierarchy of cues to return to the location of a
particular food item. Rather amazingly, overall
location within the aviary was most important,
relative position within an array of boxes in the
aviary was second, and color of the box was third
most important for the chickadees. Clearly their
spatial capabilities are exceptional, and we need to
explore the neural basis for these abilities.
And so we come to the hippocampus. Although
the hippocampus in birds is homologous to that in
mammals, the avian structure is more accessible for
investigation, being not as buried within the brain
tissue (Sherry and Hoshooley, Chapter 2). As in
mammals, this structure is strongly associated with
spatial ability. In the last few years, our knowledge
about the avian hippocampus, and especially that of
Parids, has increased enormously. We now know
3
several factors that can affect the size of this structure.
One of these is geographic location of the population.
For example, Pravosudov (Chapter 3) has shown that
black-capped chickadees in Alaska have significantly
larger hippocampi than do Colorado chickadees. The
rather more startling continental difference, with
European birds across many avian families having
significantly larger hippocampi than their North
American counterparts, has yet to be fully explained,
although, as Sherry and Hoshooley point out, the
difference seems not explicable as merely an artifact
of differing laboratory procedures, but actually a
genuine phenomenon. Clearly this puzzling differ-
ence in hippocampus size is both a necessary and a
promising area for future research on both sides of
the Atlantic.
Another facet of hippocampal research is in adult
neurogenesis. A great deal of controversy exists
here, and the data are not easily interpreted. Sherry
and Hoshooley suggest that neurogenesis in many
Parids may, in fact, be relatively constant through-
out the year, but the attrition rate of old cells may
vary with the season.
Actually a number of factors affect the size of the
hippocampus, and also the ability of a bird to per-
form spatial tasks. One of these is stress, especially as
measured by levels of corticosterone. Pravosudov
(Chapter 3) has shown that moderate levels enhance
spatial memory tasks in mountain chickadees,
although exactly how this affects the hippocampus is
not yet known. Dominance rank is also important,
with dominant birds performing memory tasks
significantly better than subordinates. Pravosudov
found no rank difference in either hippocampus size
or number of neurons in the hippocampus, but the
difference may be related to cell turnover: his findings
suggest that cell proliferation rates in subordinate
birds were significantly lower than in dominants.
One factor that seemingly may affect the hippo-
campus, at least directly, is photoperiod (Phillmore
and MacDougall-Shackleton, Chapter 4), although,
frustratingly, data on free-living birds do not seem
to agree with data taken on birds in captivity. Any
photoperiod effect may be mediated by a number of
factors present in field conditions but not available
in the artificial simplicity of the lab.
Clearly photoperiod has an enormous effect on
reproductive physiology. Black-capped chickadees,
4 I N T R O D U C T I O N TO T H E N O RT H A M E R I C A N PA R I D A E
like most songbirds, are absolutely photorefractory
(Chapter 4). But, as Ramsay and Otter (Chapter 5)
point out, photoperiod does not explain year-to-year
variations in reproductive timing. For that, one
needs to look at look at population and individual
differences. For example, variations in sensitivity to
photoperiodic changes can explain population dif-
ferences in onset of breeding in blue tits (Lambrechts
et al. 1997). Individual females also are remarkably
consistent from year to year as to when they begin
laying eggs (Chapter 5). Other factors, such as food
levels, temperature, and parasite loads, may also
affect female timing; now we are beginning to look
at the effects of more global factors, such as the
North Atlantic Oscillation, and global warming, on
clutch initiation dates.
The last three chapters in this book deal with
conservation and habitat management. This is a
welcome addition to the subjects I attempted to
cover in my first book. Parids are relatively seden-
tary, and not particularly good long-distance flyers.
They will go long distances around an open area,
rather than attempt to cross the open space
(Desrochers and Blisle, Chapter 15). Habitat frag-
mentation can have a big impact on their ability to
move from place to place. Even for relatively large
Parids, such as tufted titmice, movements from
patch to patch are greatly enhanced if those patches
are connected by wooded corridors (Olson and
Grubb, Chapter 16). Certainly in these days of
increasing human population, habitat fragmenta-
tion will only increase, and it is important for us to
understand the impact of factors, such as patch size
of blocks of forest, and the importance of connect-
ing links, on the local bird populations. Otter et al.
(Chapter 17) touch on a particularly important area.
In forest management, matrix (intervening habitat
that connects patches of relatively undisturbed
habitat), has been claimed to provide alternative
breeding habitat for a number of species. While this
management technique does provide cover and
enhances movements between patches of relatively
undisturbed habitats, Otter et al. has shown that the
matrix often is largely unsuitable for successful
breeding among the birds it appears to retain.
Careful studies of this nature and quality are
absolutely essential to assess popular management
techniques.
Finally, one of the areas where the greatest recent
progress has been made is the field of vocal commu-
nication. The three most complex vocalizations: the
whistled fee-bee song (Chapters 10 and 14), the gargle
call, which some have argued might be considered
to share some of the functions of a song (Chapters 11
and 12), and the chick-a-dee call complex, with its syn-
tax and incredible complexities (Chapters 10 and 13),
are all addressed in detail in this volume.
Nevertheless, while an enormous amount is now
known about Parid (and in particular chickadee)
communication, enormous gaps in our knowledge
remain. It is unfortunate that the work on both
whistled songs and gargles has been done almost
exclusively on males (with females considered,
when at all, primarily as recipients of male-
produced signals). Yet females produce both of
these vocalizations. The function of these notes,
and how recipients of either sex respond to them, is
as yet largely uninvestigated.
The other, truly enormous hole in our under-
standing of communication in Parids is in the area
of visual signals. One approach to the study of
visual signals is to investigate variation and func-
tion of plumage patches (e.g. Otter and Ratcliffe
1999; Mennill et al. 2003; Doucet et al. 2004;
Woodcock et al. 2005). Black-capped chickadees,
which appear superficially to human eyes as mono-
chromatic, are actually sexually dichromatic
(Chapter 9). Males have brighter whites and greys
and blacker blacks than females; patch sizes vary
consistently too. Remarkably, these subtle plumage
variations reflect not only sex but also rank
(Mennill et al. 2003; Doucet et al. 2004), and are
correlated with female mate choice (Doucet et al.
2004; Woodcock et al. 2005). Similar functions of
plumage patch variation have been found in other
Parids as well (e.g. Ferns and Hinsley 2004).
But where we still know surprisingly little is in the
area of postural signals. Susan T. Smith (1972) gave
brief descriptions of the postural signal repertoire of
Carolina chickadees. Black-capped chickadees give
many similar signals; I attempted to illustrate some
of these in my more recent book (Smith 1997). A few
displays, such as body-ruffling (Piaskowski et al.
1991) and single wing flick (Smith 1996) have been
described, but nobody has attempted a comprehen-
sive overview of visual displays that might balance
 I N T R O D U C T I O N TO T H E N O RT H A M E R I C A N PA R I D A E
the vocal repertoire papers of Ficken et al. (1978) for
black-capped chickadees, and Ficken (1990a, 1990b)
for Mexican chickadees. Indeed, surprisingly little is
known about visual signals in most other North
American Parids. One can argue that the software
technology exists for the study of vocal signals, but
not for visual signals; I suspect that had the pressure
been stronger to develop visual signal software, that
might have been produced first. One can also argue
that vocal signals are a lot easier to study, and I
agree. I am not sure I agree with Smith (1972) when
she suggested that visual signals merely back up
vocalizations. Certainly we need to obtain data to
test this hypothesis. With the state of video technol-
ogy today, both descriptive and manipulative
experiments are possible, even with fast-moving
species such as chickadees (e.g. Baker et al. 1996).
Titmice, being somewhat slower, might make even
better subjects for a thorough examination of the role
of visual signals. Their crests make them particularly
good subjects for such a study. Grubb (1998) refers to
the crest of the tufted titmouse as a semaphore
signal (Grubb 1998:16), where raised crests signal
excitement or aggression, with flattened crests sig-
naling the opposite (passivity and subordination).
Quantitative data on such a role should be relatively
easily obtained. Rigorous study on Parid visual com-
munication is sorely needed, especially here in
North America. This surely is a wide open area for
future research.
References
Baker, M. C., Tracy, T. T., and Miyasato, L. E. (1996). Gargle
vocalizations of black-capped chickadees: test of reper-
toire and video stimuli. Animal Behaviour, 52, 11711175.
Brodbeck, D. R. (1994). Memory for spatial and local cues:
a comparison of a storing and a non-storing species.
Animal Learning and Behavior, 22, 119133.
Doucet, S. M., Mennill, D. J., Montgomerie, R., Boag, P.,
and Ratcliffe, L. M. (2004). Achromatic plumage
reflectance predicts reproductive success in male black-
capped chickadees. Behavioral Ecology, 16, 218222.
Ferns, P. N. and Hinsley, S. A. (2004). Immaculate tits:
head plumage pattern as an indicator of quality in
birds. Animal Behaviour, 67, 261272.
Ficken, M. S. (1990a). Vocal repertoire of the Mexican
chickadee. I. Calls. Journal of Field Ornithology, 61,
380387.
5
Ficken, M. S. (1990b). Vocal repertoire of the Mexican
chickadee. II. Song and song-like vocalizations. Journal
of Field Ornithology, 61, 388395.
Ficken, M. S., Ficken, R. W., and Witkin, S. R. (1978). Vocal
repertoire of the black-capped Chickadee. Auk, 95,
3448.
Gill, F. B., Mostrom, A. M., Mack, A. L. (1993). Speciation
in North American chickadees: I. Patterns of mtDNA
genetic divergence. Evolution, 47, 195212.
Gill, F. B., Slikas, B., and Sheldon, F. H. (2005). Phylogeny
of titmice (Paridae):II. Species relationships based on
sequences of the mitochondrial cytochrome-B gene.
Auk, 122, 121143.
Grubb, T. C. (1998). Wild Bird Guides: Tufted Titmouse.
Stackpole Books, Mechanicsburg.
Lambrechts, M. M., Blondel, J., Maistre, M., and Perret, P.
(1997). A single response mechanism is responsible for
evolutionary adaptive variation in a birds laying date.
Proceedings of the National Academy of Science USA, 94,
51535155.
Mennill, D. J., Doucet, S. M., Montgomerie, R., and
Ratcliffe, L. M. (2003). Achromatic color variation in
black-capped chickadees, Poecile atricapilla: black and
white signals of sex and rank. Behavioral Ecology and
Sociobiology, 53, 350357.
Otter, K. and Ratcliffe, L. (1996). Female initiated divorce
in a monogamous songbird: abandoning mates for
males of higher quality. Proceedings of the Royal Society of
London Series B, Biology, 263, 351354.
Otter, K. and Ratcliffe, L. M. (1999). Relationship of bib
size to age and sex in the black-capped chickadee.
Journal of Field Ornithology, 70, 567577.
Piaskowski, V. D., Weise, C. M., and Ficken, M. S. (1991).
The body-ruffling display of the black-capped chicka-
dee. Wilson Bulletin, 103, 426434
Smith, S. M. (1980). Henpecked males: the general pattern
in monogamy? Journal of Field Ornithology, 51, 5564.
Smith, S. M. (1991). The Black-Capped Chickadee: Behavioral
Ecology and Natural History. Cornell University Press,
Ithaca, New York.
Smith, S. M. (1996). The single wing-flick display of the
black-capped chickadee (Parus atricapillus). Condor, 98,
885887.
Smith, S. M. (1997). Wild Bird Guides: Black-capped
Chickadee. Stackpole Books, Mechanicsburg, PA.
Smith, S. T. (1972). Communication and other social
behavior in Parus carolinensis. Publications of the Nuttall
Ornithological Club, 11, 1125.
Woodcock, E. A., Rathburn, M. K., and Ratcliffe, L. M.
(2005). Achromatic plumage reflectance, social domin-
ance and female mate preference in black-capped
chickadees (Poecile atricapillus). Ethology, 111, 891900.
This page intentionally left blank
 SECTION I
Proximate mechanisms in behavior
and evolution
Extrinsic and intrinsic factors influence the behav-
ior and ecology of all animals, and are inextricably
linked with the content presented in every chapter
of this book. In most of the chapters, there is at least
some emphasis on the factors that regulate the
behaviors being discussed. But while some research
emphasizes the ultimate outcome that exhibiting
certain behavior patterns has on an individuals
reproductive success, others focus upon under-
standing the underlying proximate mechanisms
the external abiotic/biotic conditions or internal
physiologythat regulate the behaviors we see. It
is this focus, which has formed a large component
of Parid research, that forms the relationship for
chapters in this section of the book.
Parids exhibit some specialized traits that make
them prime subjects for the neuroethological and
physiological studies of controlling mechanisms of
behavior. For example, the remarkable ability of
many speciesand notably the two Parid groups
occupying North Americato both cache and
recover enormous numbers of food items over the
course of a winter. In Chapter 2, Sherry and
Hoshooley investigate the structural aspects of the
avian brain, and how this can influence spatial
memory. Using cross-species comparisons within
the Paridae and comparing Parids to other species,
Sherry and Hoshooley review general spatial
abilities of chickadees in food-storing and other
contexts; they then relate the ability to form spatial
memories to the structure, gene expression, and
neurogenesis within the hippocampus. Pravosudov
(Chapter 3) extends this topic by comparing differ-
ences in the spatial abilities across disparate popu-
lations within the same species. In particular, this
research compares populations in circumstances
that vary in food limitation, and how this influ-
ences the propensity for food caching and may
result from physiological differences in the hippo-
campus and hormone regulation between these
same populations.
While enhanced spatial memory may be selected
in over-wintering Parids and this ability might be
more specialized within some avian lineages, other
behaviors and their regulating factors are more
general in nature. The factors that control the cir-
cannual rhythms of the life-history traits, such as
the controlling the timing of seasonal patterns
in reproduction and wintering behavior, occur in
migratory and non-migratory species alike. In
Chapter 4, Phillmore and MacDougall-Shackleton
assess the influence of photoperiod as a mechanism
of regulating annual cycles. In particular, Phillmore
and MacDougall-Shackleton review the interactive
influence of changing light levels on regulating the
annual hormone cycles that influence the develop-
ment of gonads (breeding regulation) and neural
structures associated with both food caching and
7
8 B E H AV I O R A N D E V O L U T I O N
song control. Ramsay and Otter (Chapter 5) focus
on the fine-scale regulation of one of these
behaviorsthe timing of clutch initiation and
fertility in Parids. This topic, which is the subject of
long-term research programs on Eurasian tits and,
recently, North American chickadees, considers the
interaction between annual variation in weather
patterns and food availability in regulating
seasonal and individual variation in nest timing.
As mentioned, all aspects of a species behavior
and ecology are influenced by external abiotic and
internal physiological variables, and several other
chapters in this book could be easily included in
this section (for example, Chapter 10). Chapters
within this section (Chapter 5) might also have
found a home in the next section of the book on
reproductive ecology and behavior of Parids, and
its position as the last chapter in the section pro-
vides the bridge to Section II. Within the present
section, the chapters represent clear situations
where the primary focus of the research is to under-
stand the underlying proximate mechanisms that
control behavioral variation seen in Parids, and to
relate this to how Parids have been used as model
organisms to elicit a greater understanding of
behavior and ecology in general.
 CHAPTER 2
Neurobiology of spatial
behavior
David F. Sherry and Jennifer S. Hoshooley
2.1 Introduction
Chickadees and tits seem unlikely subjects for
research on the neurobiology of spatial behavior.
Most species are sedentary and there appears to be
little about the Parid brain that would recommend
it as a model system for neurobiology. Chickadees
and tits, along with Corvids, have, however, been at
the centre of recent research on spatial ability and a
brain region crucially involved in spatial ability, the
hippocampus. Two basic discoveries focused atten-
tion on chickadees and tits. The first was that chicka-
dees and tits that store food remember the spatial
locations of their caches. These birds are scatter
hoarders and place very large numbers of food
items in sites dispersed through their winter home
range. They can store hundreds of items in a single
day and put each cache in a different place, never
reusing the same site. Remembering the locations
of these caches is a formidable problem and there is
now a great deal of experimental evidence showing
that the birds successfully solve it. The second dis-
covery was that despite appearances, the Parid
brain is unusual. Food-storing chickadees and tits,
along with food-storing jays and nuthatches, have a
larger hippocampus than is found in species that do
not store food. The hippocampus is involved in a
variety of cognitive processes but one that has been
consistently identified in birds and mammals
(including humans) is spatial ability. In this chapter
we will describe what has been learned from
chickadees and tits about the neurobiology of
spatial ability. Review of a parallel research
program on food-storing Corvids can be found in
Balda et al. (1997).
2.2 Food storing in the Paridae
All of the North American chickadees and titmice
store food, as do most of the well-known Eurasian
species (Hampton and Sherry 1992; Sherry 1989).
Figure 2.1 shows the phylogenetic distribution of
food-storing in the Paridae. The behavior is practic-
ally universal in the Poecile group and the two
crested tit groups Lophophanes and Baeolophus. The
only exceptions are three little-known, high-altitude
species endemic to China and the Himalayas for
which it remains unknown whether or not they
store food. Food storing is known not to occur in the
great tit, and although it has been reported for the
blue tit (Hinde 1952; Southern 1946) it is probably
rare, if it occurs at all (Haftorn 1956; Healy et al.
1994; Richards 1958). For the many species of the
Periparus and Parus groups found in China, Nepal,
the Philippines, and Africa there is not enough
information to be certain whether they store food or
not. Food storing has not been observed in the wild
or in captivity in the groundpecker (Parus humilis;
Gebauer, personal communication) a very unusual
bird (formerly Humes ground jay) recently
assigned to the Paridae on the basis of molecular
and biochemical characteristics (Gebauer et al. 2004;
James et al. 2003) and placed near the root of the
Parid phylogeny proposed by Gill et al. (2005).
2.2.1 Food storing in the wild
Food storing has a strong seasonal component in
Parids, beginning in autumn and continuing
through the winter into early spring (Brodin 1994;
Haftorn 1956; Ludescher 1980; Nakamura and
9
10 B E H AV I O R A N D E V O L U T I O N

100 atricapillus
100 gambeli gambeli
82
gambeli baileyi
85 sclateri
rufescens
87
100 hudsonicus
100
cinctus
100 carolinensis extimus Poecile
90 carolinensis carolinensis
100 palustris brevirostris
palustris palustris
93 montanus borealis
davidi
99 superciliosus
varius
lugubris
100 cristatus
Lophophanes
97 dichrous
100 wollweberi
79 100 inornatus Baeolophus
bicolor
ater aemodius
100
melanolophus
97
ater ater
87 Periparus
rubidiventris
100
rufonuchalis
elegans elegans
100 amabilis
elegans mindanensis
100 major
monticolus
92
holsti
100
100 spilonotus
xanthogenys
71 afer Parus
89 albiventris
100
100 niger niger
86
niger niger
73 funereus
95 rufiventris
fasciiventer
Parus humilis
100 Parus caeruleus Cyanistes
Parus cyanus
100 Melanochlora s. sultanea
Melanochlora s. gayeti
Sylviparus modestus

Figure 2.1 The distribution of food-storing in the Paridae, shown on a phylogeny proposed by Gill et al. (2005). Dark shaded boxes show
species known to store, light shaded boxes show species that do not store, or in the case of Parus caeruleus, rarely do so. One species not shown
in this phylogeny, Parus venustulus, is thought to be closely related to Parus ater and has been reported to store food (Harrap and Quinn 1996).
Although there appears to be a phylogenetic pattern to the occurrence of food-storing, there is no information on the presence or absence of the
behavior for most species in the Periparus and Parus groups. Arrows show hypothesized invasions of North America by the Poecile and
Baeolophus groups in the late Tertiary, 3.5 and 4.0 mya, respectively. Branch numbers in this maximum likelihood phylogram show posterior
probabilities greater than 70% (reprinted with permission from Gill et al. 2005).

Wako 1988; Pravosudov 1985). Chickadees and tits
cache all of the foods they normally eat, including
seeds, nuts, fat from animal carcasses, spiders, and
insects, which they sometimes prepare by remov-
ing the head and viscera. Any small crevice or
cavity will do as a storage site, and food is also
stored in moss, lichen, dry leaves, or pushed into
soft ground. Field studies of European marsh tits
(Cowie et al. 1981; Stevens and Krebs 1986) and wil-
low tits (Brodin 1992), in which researchers located
cache sites in the wild, found that most food is
retrieved very soon after it is stored, often by the
end of the same day and generally within a few
days at most. Studies in which ingestion of radio-
labeled stored seeds produced a radio-labeled
growth bar on growing rectrices of willow tits
found some food was also retrieved and eaten at
much longer intervals ranging from six to 40 days
(Brodin and Ekman 1994). The radio labeling
method cannot detect cache recovery after shorter
intervals because of the time required to initiate
growth of a replacement rectrix, or after longer
intervals because replacement of the feather is com-
plete by about 6 weeks. This result shows, never-
theless, that caches are sometimes left in place for
long periods of time before retrieval, or that stored
food is sometimes retrieved and recached multiple
times (Brodin 1994). On the Japanese island of
Miyake, Higuchi (1977) observed nuts of the
Japanese chinquapin Castanopsis cuspidata are
among the food brought by varied tits to their
young. Because these nuts had not been available
on trees since the previous winter, Higuchi con-
cluded the birds were likely feeding their young
from caches made at least several months earlier.
2.2.2 Memory for cache sites
Early field studies of cache retrieval by marsh tits,
willow tits, and Siberian tits (also known as the
gray-headed chickadee and the only Parid to occur
in both the Palearctic and the Nearctic) confirmed
by a variety of methods, including direct observa-
tion, that birds that cache food later return to collect
it (Cowie et al. 1981; Pravosudov 1986; Stevens and
Krebs 1986). Laboratory studies showed that mem-
ory for the spatial locations of caches is the means
of cache retrieval, rather than chance encounter, use
N E U R O B I O L O G Y O F S PAT I A L B E H AV I O R 11
of preferred site types, use of a preferred route, or
marking of cache sites. These experiments deter-
mined the rate of successful cache recovery by cap-
tive birds and found that chickadees and tits
perform much better than expected by either
chance or site preference alone (Sherry 1984; Sherry
et al. 1981; Shettleworth and Krebs 1986; Shettleworth
and Krebs 1982). Memory for cache sites can persist
for up to 4 weeks in black-capped chickadees in
captivity and this is probably an underestimate of
how long food-storing Parids can remember the
locations of their caches (Hitchcock and Sherry 1990).
But knowing that chickadees remember where they
placed their cachesremarkable as that feat of
memory may beonly opens up new questions
about spatial cognition in these little birds. What is
remembered about a cache site and what makes up
a spatial location for a chickadee?
2.2.3 Memory for caches versus other
spatial locations
Experiments with black-capped chickadees, marsh
tits, and coal tits in captivity show that they are
equally good at remembering the locations of food
they have stored and food they have encountered
but not collected in the course of normal foraging
(Shettleworth and Krebs 1986; Shettleworth et al.
1990). Even after an interval of 26 h, the birds return
with equal probability to both kinds of site.
Analyses of interference in memory between sites
where food was stored and sites where food was
encountered give no indication that the two types of
spatial locations are remembered in different ways
(Shettleworth et al. 1990), although the duration of
memory for cache sites may be longer than for sites
where food was encountered (Brodbeck et al. 1992).
Black-capped chickadees memory for spatial
locations where they have found food shows some
of the same properties found in other research on
animal memory using more conventional tasks.
Locations and features that are unique, for
example, are remembered better than locations and
features that are repeated within successive experi-
mental trials (Brodbeck et al. 1992). This may
make cache sites, which are unique in the wild,
easier to remember than stimuli that are repeated
on successive trials in laboratory experiments.
12 B E H AV I O R A N D E V O L U T I O N

Black-capped chickadees memory for sites where occupied the location on the wall formerly occu-
they have found food also shows a serial position pied by the rewarded feeder (Fig. 2.2). There was
effectbetter memory for items at the beginning and also no food in any of the blocks. By dissociating
the end of a sequence compared to the middle very cues in this way and placing them in conflict it was
similar to serial position effects found in animal and possible to determine whether the bird chose the
human memory for lists and series of events correct position on the wall, the correct position in
(Crystal and Shettleworth 1994). the array, or the correct color and pattern. Brodbeck
(1994) found that black-capped chickadees
returned preferentially to the block that was in the
2.2.4 Spatial memory in food-storing versus
correct position on the wall. This result suggested
non-storing birds
that the place where the bird had found food was
To compare spatial ability in storing and non-stor- remembered as a location with respect to the larger
ing birds it is obviously necessary to observe features of the aviary, not the arrangement of blocks
behavior other than food storing. Research on in the array or the distinctive colors and patterns on
memory in chickadees and tits, described above, the block. When the birds failed to find food at this
provides a number of non-storing tasks in which block, however, their second choice was most often
chickadees and tits perform about as well as they to the feeder in the correct position in the array, and
do when retrieving caches, and these tasks can be when they failed to find food there, their third
used to compare performance in storing and non-
storing species.
Krebs et al. (1990) compared memory in food-stor-
ing coal tits and non-storing great tits for sites where (a)
food had previously been encountered. In an experi-
ment that required remembering which of seven
previously encountered sites contained food, coal
tits relocated the site after fewer attempts than great
tits, but in an experiment that required remember-
ing which seven sites out of a possible 60 contained
food, both species did equally well. In the latter
experiment, great tits tended to return to all of the
sites they had previously visited whether they con- (b)
tained food or not, while coal tits tended to return
more selectively to sites that had contained food.
Brodbeck (1994) developed a very interesting
task that makes it possible to determine what
aspects of a spatial location are remembered by
food-storing birds. Birds found food in one of four
distinctively colored and patterned blocks of wood
placed in an array on the wall of an aviary. Once a
Figure 2.2 Chickadees searched until they discovered which of
chickadee had found which block contained food
four blocks arranged in an array on the wall of an aviary contained
the bird was removed from the aviary. When it food, indicated in (a) by the white triangle (Brodbeck 1994). The bird
returned the arrangement of the wood blocks had then left the aviary and the array of blocks was modified, as shown in
been changed. The array was displaced on the wall (b). The array has been shifted to the right in this illustration and the
of the aviary while preserving the relative position feeder formerly baited has been exchanged with another. The bird
then returned to the aviary to search for food. This manipulation
of the blocks to one another. In addition, the
dissociates choice of the matching position on the wall, choice for
rewarded block had been switched with another the matching position in the array, and choice for the matching
block in the array. The displacement was done in colors and patterns of the blocks. Redrawn with permission from
such a way that a different feeder in the array now Brodbeck (1994).

choice was to the feeder with the colors and pattern
that matched the block that was originally baited.
This result shows that chickadees treat spatial loca-
tion with respect to surrounding landmarks as pri-
mary, but also remember smaller-scale spatial
relations and the local features of sites where they
have found food.
Dark-eyed juncos (Junco hyemalis) in Brodbecks
(1994) experiment also remembered which feeder
had been baited but on test trials with cues placed
in conflict showed no preference among cues. Their
first, second, and third choices were equally likely
to be to the correct position on the wall, the correct
position in the array, or the correct colors and
pattern.
Brodbeck and Shettleworth (1995) modified this
procedure for the presentation of stimuli on a com-
puter touch screen. Birds pecked stimuli on the
screen that corresponded to the wood blocks in
Brodbecks original experiment in order to obtain a
food reward. In the touch screen version of the task
the absolute position of the array on the screen was
not manipulated. Comparison of food-storing
black-capped chickadees and non-storing dark-
eyed juncos showed that while chickadees chose
first the stimulus in the correct relative position in
the array and rarely the stimulus of the correct color,
juncos did not differ in their choice of position or
color. Chickadees had a strong tendency to match
spatial location of the rewarded stimulus, not its
color, while juncos matched location and color
equally often. A subsequent experiment showed
that when chickadees were required to choose on
the basis of location alone or color alone, their
responses were over 80% correct for location but no
better than chance for color. Juncos, in contrast, per-
formed equally well and above chance for both loca-
tion and color stimuli (Brodbeck and Shettleworth
1995). These results show that food-storing chicka-
dees either fail to attend to or fail to remember the
color of stimuli in these experiments, in contrast to
the spatial location of stimuli, while non-storing
juncos have no such bias for location over color.
Food-storing chickadees do not necessarily per-
form better than non-storing birds on memory tasks.
Hampton et al. (1998) compared the effects of
proactive interference on memory in black-capped
chickadees and dark-eyed juncos. Proactive
N E U R O B I O L O G Y O F S PAT I A L B E H AV I O R 13
interference is the disruptive effect on memory of
material presented before something that is to be
remembered. A phone number in the middle of a list,
for example, is more difficult to remember than a
number early in the list because of proactive inter-
ference by earlier numbers. Proactive interference
contributes to the serial position effects described
earlier. In Hampton et al.s (1998) experiment,
chickadees and juncos were required to remember
the last in a series of one, two, or three stimuli
presented on a touch screen. Hampton et al. (1998)
reasoned that food-storing chickadees might be
more resistant to proactive interference because of
the large number of cache sites they remember in the
wild. Greater resistance to proactive interference had
been previously reported for food-storing birds by
Clayton and Krebs (1994). Chickadee performance
declined, however, in a linear fashion as the number
of stimuli in the series increaseda clear effect of
proactive interference. The performance of juncos
showed no effect of proactive interference; their
behavior was unaffected by the number of stimuli in
the series. Interestingly, in a second experiment by
Hampton et al. (1998) a seemingly minor change in
procedure resulted in proactive interference in both
chickadees and juncos, with superior performance
by chickadees on series of all three lengths. The
procedural change was to refrain from providing a
food reward for pecking the final stimulus in the
series. Hampton et al. (1998) suggest that the differ-
ence between their two experiments occurs because
juncos are more affected than chickadees by the
recent reward history of stimuli. When the last item
in a series is associated with a food reward, juncos
consistently choose that item independent of the
number of items that preceded it, while chickadees
do not. When juncos are not provided with food
reward associated with the final item, both species
show proactive interference and the performance of
chickadees is consistently better than that of juncos.
Whether this explanation is correct or not, this study
shows that the relative performance of food-storing
and non-storing birds during laboratory memory
tests is not necessarily what one would predict from
food-storing birds reliance upon memory to recover
caches of food. Furthermore, seemingly minor
changes in experimental procedure can be of major
significance to the birds.
14 B E H AV I O R A N D E V O L U T I O N
Shettleworth and Westwood (2002) subsequently
conducted similar experiments comparing the per-
formance of chickadees and juncos on touch screen
tasks using location and color stimuli. They found,
however, that both chickadees and juncos per-
formed better on location stimuli than on color
stimuli, and this was the case whether location and
color items were presented independently or as
parts of a compound stimulus. Shettleworth and
Westwood (2002) also carefully varied the retention
interval over which chickadees and juncos were
required to remember location and color stimuli.
Food-storing chickadees consistently did much bet-
ter with spatial information than they did with
color information, while juncos performed only
slightly better, or no better, with location stimuli
compared to color stimuli. Both species performed
better than chance with both kinds of stimuli and
food-storing birds did not necessarily perform bet-
ter than non-storing birds with spatial stimuli.
Monkey
CA3
DG
CA3
CA1
Figure 2.3 The hippocampus of the cynomolgus monkey (Macaca fascicularis), rat, and pigeon. Two interfolded structures, the dentate gyrus
(DG) and Ammons horn, or cornu ammonis (CA), make up the mammalian hippocampus. Scale bars equal 2 mm. APH area parahippocampalis;
CA1, CA3 cells fields of the cornu ammonis; DG dentate gyrus; HP hippocampus. Modified from Colombo and Broadbent (2000).
A multidimensional scaling analysis of responses
showed, for example, that chickadees did not make
finer or more orderly spatial discriminations than
juncos did for stimuli on a touch screen
(Shettleworth and Westwood 2002). This pattern of
results neatly characterizes many of the apparently
contradictory observations made in the course of
research comparing memory in food-storing and
non-storing birds. Food-storing birds may, in fact,
not excel at spatial tasks compared to other birds,
but spatial tasks are what food-storing birds do
best, at least in experiments that involve pecking
colored shapes on a touch screen.
2.3 The hippocampus
Having discovered the capacity of food-storing
chickadees and tits to relocate cache sites and the
cognitive means by which they do this, researchers
turned to the neural mechanisms behind the birds
Rat Pigeon
APH
CA1
HP
DG

spatial ability. The structure that has received the
most attention has been the hippocampus. In
mammals the importance of the hippocampus for
spatial behavior has been well-documented. The
neuroanatomical region designated as hippo-
campus in the avian brain is found in a very differ-
ent location from that of the hippocampus of the
mammalian brain (Fig. 2.3). In birds, the hippo-
campus lies on the dorsal surface of the brain just
above the ventricles (Karten and Hodos 1967; Stokes
et al. 1974) whereas in mammals the hippocampus is
embedded in overlying neural tissue. The internal
structure of the hippocampus also appears quite
different in birds and mammals. In mammals, dis-
crete divisions are apparent in histologically stained
tissue. The interfolded CA1 and CA3 cell fields of
Ammons horn and the dentate gyrus give the
hippocampus its distinctive appearance. Although
the avian hippocampus lacks such clear cellular
organization, it has structural features that resemble
those found in the mammalian brain. The avian
hippocampus is composed of two regionsthe
hippocampus proper and the area parahippo-
campalis. The hippocampus proper is a V-shaped
band of darkly stained tissue running along the
most medial and the most ventral edges of the
APH
HP
Figure 2.4 The black-capped chickadee hippocampus, made up of
the hippocampus proper (HP) and the area parahippocampalis (APH).
Neurons immunoreactive for the neuronal nuclei specific protein
(NeuN) are shown labeled with diaminobenzidine (DAB) at
5 objective magnification. Arrows indicate the change in cell
density marking the lateral boundary of the hippocampus. V-shaped
line shows the cell density-defined boundary between the
hippocampus proper and the area parahippocampalis.
N E U R O B I O L O G Y O F S PAT I A L B E H AV I O R 15
structure (Fig. 2.4). Neurons in this region are
heterogeneous in size and packed closely together.
The area parahippocampalis is adjacent to the
hippocampus proper and extends laterally to a
boundary marked by a distinct change in cell
density (Krebs et al. 1989). The area parahippo-
campalis is characterized by decreased cell density
(in comparison to the hippocampus proper) and is
comprised of uniformly large neurons. Based on the
results of connectivity and electrophysiology
studies, it has been suggested that the V-shaped
hippocampus proper may be homologous to
Ammons horn and that the dorsomedial region of
the hippocampus may be homologous to the
dentate gyrus (Siegel et al. 2002; Szekely 1999).
Despite these differences in anatomy, many lines
of evidence indicate homology between the avian
and mammalian hippocampus. Developmentally,
the hippocampus arises from the same neural pre-
cursor tissue in birds and mammals (Klln 1962;
Kuhlenbeck 1938). Connectivity studies have also
shown homology between birds and mammals,
both for connections within the hippocampus
and for connections between the hippocampus and
other brain regions (Casini et al. 1986; Krayniak and
Siegel 1978). Neurochemical comparisons have
shown similar distributions of neurotransmitters
and neuropeptides in the mammalian and avian
hippocampus (Erichsen et al. 1991; Krebs et al.
1991). Two phenomena characteristic of the mam-
malian hippocampus, long-term potentiation (LTP)
and place cells, have been described in the avian
hippocampus (Margrie et al. 1998; Siegel et al. 2005).
LTP is a phenomenon in which a few seconds of
electrical stimulation can cause neurons to become
more sensitive to stimulation for days or weeks
afterward. Long-term potentiation may mimic
processes involved in learning and the formation of
memory. Place cells are neurons that are most
electrically active whenever the animal enters a
particular place in its environment. Lesion studies
of pigeons and zebra finches have also shown the
importance of the hippocampus for processing
spatial information (Colombo and Broadbent 2000;
Patel et al. 1997; Watanabe and Bischof 2004). These
converging lines of evidence strongly suggest
that the avian hippocampus and the mammalian
hippocampus are indeed homologous structures,
16 B E H AV I O R A N D E V O L U T I O N
derived with modification from a structure or struc-
tures in the dorso-medial forebrain of their most
recent common ancestor.
Early work exploring the neural basis of food-
storing spatial behavior took a lesion approach. The
first study to examine the effects of hippocampal
ablation showed that Eurasian nutcrackers
(Nucifraga caryocatactes) could not find their
cachesthough they continued to make caches and
search for themfollowing removal of the hippo-
campus (Krushinskaya 1966). Similarly, an intact
hippocampus is necessary for black-capped chicka-
dees to accurately retrieve stored food (Sherry and
Vaccarino 1989). Chickadees with hippocampal
lesions continued to store food (in tree branches
arranged in an indoor aviary) but the accuracy of
retrieval was reduced to a level no better than
expected by chance encounter. Using a different
approach Hampton and Shettleworth (1996a,
1996b) compared the effects of hippocampal lesions
in chickadees and non-storing dark-eyed juncos by
assessing performance on some of the cognitive
tasks described earlier. The results showed that the
hippocampus is necessary in both chickadees and
juncos for tasks that require memory for spatial
information. In their first study the hippocampus
was found to be necessary for memory of the
spatial location of a stimulus but was not necessary
for memory of the color of the stimulus (Hampton
and Shettleworth 1996a). In their second study,
hippocampal lesions were found to impair
performance by both species on an operant spatial
non-matching-to-sample task. These results show
that the chickadee hippocampus plays an essential
role in memory for spatial locations and is involved
in memory for cache sites.
2.3.1 Comparative studies of the hippocampus
The hippocampus of food-storing birds such as
chickadees, nuthatches, and jays is consistently
larger than the hippocampus of non-storing birds
such as thrushes, blackbirds, sparrows, and warb-
lers, after correcting for overall differences in brain
size (Garamszegi and Eens 2004; Krebs et al. 1989;
Sherry et al. 1989). This general pattern also holds
within food-storing families of birds such as the
Paridae. The hippocampus is larger, relative to
overall brain size, in the food-storing marsh tit, for
example, than in the non-storing great tit (Krebs
et al. 1989). Black-capped chickadees, which store
food more intensively than either Mexican chicka-
dees or bridled titmice, have a larger hippocampus
relative to overall brain size than the other two
species (Hampton et al. 1995).
Brodin and Lundborg (2003) carried out a meta-
analysis of available data on hippocampal size in
food-storing Parids and Corvids and concluded
that, in general, there is no relation between relative
hippocampal size and the degree of caching behav-
ior in either of these groups of food-storing birds.
This data set has, in turn, been reanalyzed by Lucas
et al. (2004) who found that the results of Brodin
and Lundborgs earlier analysis were affected by an
unexpected confound: the relative size of the
hippocampus is greater in European birds than in
North American birds. After correcting statistically
for this difference between Eurasian and North
American birds, Lucas et al. (2004) showed that
birds that store food to a greater degree do indeed
have a relatively larger hippocampus. The contin-
ent effect they found has subsequently been shown
to occur in both food-storing and non-storing birds
(Garamszegi and Lucas 2005). The cause of this
difference in hippocampal size between European
and North American birds is not entirely
clear. Garamszegi and Lucas (2005) suggest it is not
likely to be a result of differences in the latitudinal
distribution of European and North American
species and favor instead a continental difference
in avian ecology and life historyyet to be
identifiedas the evolutionary explanation for the
differences in hippocampal size they found.
2.3.2 Neural processing of spatial information
The discovery of differences in hippocampal size
between food-storing and non-storing birds has
influenced research on the neural mechanisms of
spatial information processing. This work has
prompted researchers studying spatial learning in
mammalian systems to look for neural specializa-
tions that might correlate with specializations of
spatial cognition (Galea and McEwen 1999; Jacobs
et al. 1990; Jacobs and Schenk 2003; Pawluski and
Galea 2006). This vein of research has added an

ecological and evolutionary element to research on
the neurobiology of the hippocampus (Sherry 2006;
Sherry et al. 1992).
This research has also cast chickadees in a new
light, as a model species for examining the
operation of the hippocampus and the neural
mechanisms of memory formation. Because their
food storing behavior requires the processing of a
good deal of spatial information, chickadees may
provide useful insights into the neurobiology of
spatial behavior, much as London taxi drivers have
provided unexpected insights into the relation
between the human hippocampus and spatial
ability (Maguire et al. 2003).
One line of research has extended comparative
analysis of the hippocampus by examining the
ontogeny of hippocampal enlargement in food-
storers. In juvenile mountain chickadees and marsh
tits food-storing activity and spatial experience are
necessary for hippocampal growth and the
maintenance of increased hippocampal volume
(Clayton 2001; Patel et al. 1997). Other work has
compared levels of neurochemicals in the brains of
food-storers and non-storers. One such study
compared the distribution of two neuropeptides,
substance P and neuropeptide Y, in black-capped
chickadees, non-storing blue and great tits, and
non-storing dark-eyed juncos (Gould et al. 2001).
Substance P and neuropeptide Y are known to
modulate memory formation in other species.
While no significant differences in neuropeptide Y
expression were found among the four species,
chickadees showed significant enlargement of a
region of intense substance P immunoreactivity in
the area parahippocampalis (APH). This result
suggests that substance P may play a role in spatial
information processing in APH. A study which
examined the distribution of two different
receptors for the excitatory neurotransmitter
glutamatethe NMDA and AMPA receptors
found significantly fewer NMDA receptors in food-
storing marsh tits than in non-storing blue tits
(Stewart et al. 1999). In mammals, the AMPA
receptor is involved in normal glutamate neuro-
transmission within the hippocampus. The NMDA
receptor is normally inactivated, unless the neuron
is experiencing frequent stimulation. When this
occurs and the neuron is depolarized, glutamate
N E U R O B I O L O G Y O F S PAT I A L B E H AV I O R 17
can activate the NMDA receptor as well. Activation
of NMDA receptors is one step in the LTP of
neurons, described earlier. Another approach has
been to examine the expression of immediate early
genes (IEGs) in the hippocampus during various
components of food-storing behavior. IEGs are
activated in many neurons in response to frequent
firing of action potentials and their expression in
neural tissue therefore indicates areas where strong
activation has occurred during the performance of
a particular behavior or cognitive process (Mello
et al. 2004). Smulders and DeVoogd (2000) found
that the IEG expression in the chickadee hippo-
campus during food-storing was related to the
accuracy of cache retrieval, suggesting that the
intensity of neuronal activity in the hippocampus
has later effects on the strength of memory for
cache locations
A series of recent studies by Shiflett, DeVoogd,
and their colleagues examined the effects of
disrupting hippocampal neurotransmission and
neural processing on the spatial behavior of
chickadees. In one study the hippocampus was
reversibly inactivated by the administration of
lidocaine (Shiflett et al. 2003) while in another the
effects of antagonizing NMDA and cannabinoid
receptors were examined (Shiflett et al. 2004). In
both studies the same general methods were
used. Chickadees were tested on spatial memory
encoding and retrieval in a task in which food was
hidden in blocks of wood on the walls of a large
indoor aviary. Birds were trained to learn the
location of a food reward hidden in one blockthe
target blocklocated in an array of blocks that
were empty. The accuracy of returning to the target
block following various delay intervals was tested.
In both studies birds were implanted with bilateral
cannulas, the tips of which were in contact with
the dorsal surface of the hippocampus. Lidocaine,
the NMDA receptor antagonist AP5, and the
cannabinoid receptor antagonist SR141716A were
administered directly to the hippocampus through
the cannulas.
Reversible inactivation of the hippocampus with
lidocaine showed that the hippocampus was neces-
sary for encoding the spatial location of the target
and for short-term memory of the target location
tested 15 min following the initial encoding. Once
18 B E H AV I O R A N D E V O L U T I O N
the target location was encoded, however, retrieval
of its location from memory after 3 hours no longer
required activation of the hippocampus. These
results support the idea that the hippocampus is
more important for the initial encoding of spatial
memories rather than for their retrieval, which is
consistent with findings for mammals. The results
obtained for the NMDA receptor antagonist
AP5 showed that in order for information to be
accessible after long delays, that is, transferred to
long-term memory, NMDA receptors have to be
functional during initial encoding of the target loca-
tion. NMDA receptor inactivation during the
15-min period following encoding had no effect on
transfer to long-term memory. Similarly, NMDA
receptor activation during encoding was not neces-
sary for short-term memory of the target location
assessed 15 min after encoding. This latter result
suggests that other receptors are involved in the
processing of spatial information that results in
short-term memory.
Cannabinoid receptor inactivation produced
intriguing results. If cannabinoid receptors were
functional during the encoding of a first target
location, then memory for a second target location,
learned on a subsequent day, was better on a probe
1 day following the learning of the second location.
That is, cannabinoid antagonism during the
encoding session for the first target location caused
errors in recalling the second target location. This
result suggests that cannabinoid receptor activation
may be important for learning of multiple spatial
locationsa core component of food-storing
behavior.
2.3.3 Neurogenesis in the hippocampus of
the adult black-capped chickadee
A number of studies have addressed the role of
adult neurogenesis in the processing of spatial infor-
mation in the hippocampus. The first work to exam-
ine neurogenesis in the black-capped chickadee was
that of Barnea and Nottebohm (1994) Extensive
research had previously described adult neurogen-
esis in the oscine song control system, much of this
work conducted by Nottebohm and his colleagues
(Nottebohm 2002), leading to a detailed picture of
the location and nature of neural progenitor cells,
the migratory patterns of new neurons from their
place of origin, and the morphological and electro-
physiological properties of new neurons. The song
control nucleus HVC, which is involved in the inte-
gration of auditory input and motor output related
to song learning, exhibits striking seasonal variation
in the recruitment of new neurons, with maximum
levels occurring in the fall (Nottebohm 2004;
Tramontin and Brenowitz 2000). Because fall is the
time of year when many songbirds modify their
learned songs, it has been proposed that new
neurons must be added to neuronal circuits for new
learning to occur.
To test the hypothesis that neurogenesis is correl-
ated with seasonal change in neural processing
Barnea and Nottebohm (1994) examined neurogen-
esis in another system, the hippocampus of the
black-capped chickadee. They proposed that if new
neurons are necessary for new memories to be
created then more neurons should be recruited into
the chickadee hippocampus in the fall when
thousands of caches are being created. Chickadees
were caught in the wild throughout the year, injected
with the cell birth marker tritiated thymidine, and
then released back into the wild to be recaptured
at various times from 6 weeks to 1 year later.
Examination of the hippocampus of birds caught
6 weeks postinjection showed greatest levels of
neuronal recruitment in birds administered tritiated
thymidine in October. Heightened neuronal recruit-
ment at the time of year when chickadees were cre-
ating most cache sites provided further support for
the idea that new neurons are incorporated into
existing neuronal circuitry at times of year when
there are elevated demands on spatial memory.
To further understand the role of neurogenesis in
spatial memory in the chickadees hippocampus, we
conducted a study of seasonal variation in the pro-
duction of new hippocampal neurons (Hoshooley
and Sherry 2004). It could be that more neurons are
recruited into the chickadee hippocampus in
October because a greater number of neurons are
generated at that time of year, anticipating height-
ened spatial processing demands. It could also be
that neurons are generated at a constant rate
throughout the year and usually perish soon after
production, but in October more are incorporated
into hippocampal circuits and survive. To test this

first hypothesis we examined hippocampal neuron
production in chickadees in fall, winter, and spring
by administering the cell birth marker bromod-
eoxyuridine (BrdU) and sacrificing birds 1 to
2 weeks later. This interval between birth marker
administration and sacrifice was chosen to allow
time for new neurons to express a mature neuronal
phenotype, assessed morphologically, while at the
same time minimizing the time for possible attri-
tion of new neurons. No significant fluctuations in
neuron production were detected over fall, winter,
and spring. This suggests that the enhanced recruit-
ment described by Barnea and Nottebohm (1994)
comes about through greater recruitment of
October-born hippocampal neurons rather than an
overall increase in the production of such cells.
New neurons may be necessary to encode new
spatial memories in the hippocampus because old
neurons undergo irreversible structural modifica-
tion during memory formation that is incompatible
with the encoding of new spatial memories (Barnea
and Nottebohm 1996; Nottebohm 2002; Nottebohm
2002). New structurally unmodified neurons may
be necessary for new information to be encoded. To
make room for new neurons in hippocampal cir-
cuitry, neurons encoding expendable information
may be excised in a process of neuronal replace-
ment. Some support for this hypothesis comes
from the studies described above (Barnea and
Nottebohm 1994; Hoshooley and Sherry 2004)
which both found that the total number of hippo-
campal neurons did not change seasonally, sug-
gesting increased attrition must at some point equal
increased fall recruitment. The idea of seasonal
neuronal replacement is also supported by findings
with songbirds showing that neuronal recruitment
to HVC increases following targeted cell death
(Scharff et al. 2000).
Other work examining neurogenesis in chicka-
dees has revealed that a birds social status plays a
modulatory role on cell production in the ventricular
zone directly beneath the hippocampus. Dominant
birds show greater numbers of newly divided cells
(Pravosudov and Omanska 2005). A factor which
has been found not to have an effect on hippocampal
neurogenesis is corticosterone. Administration of
corticosterone had no significant effect on neural
proliferation in the hippocampal ventricular zone at
N E U R O B I O L O G Y O F S PAT I A L B E H AV I O R 19
the doses examined by Pravosudov and Omanska
(2005; see also Chapter 3).
Because hippocampal neurogenesis varies
seasonally it is possible that annual changes in
photoperiod influence its timing and magnitude.
We examined hippocampal neuron recruitment in
three groups of birds held in various photoperiodic
conditions in an attempt to determine whether
decreasing daylength in the fall may serve as a cue
enhancing the recruitment of fall-born neurons
(Hoshooley et al. 2005). The groups were held on
either long-days (15L: 9D) in a photostimulated
state, on long-days (15L:9D) in a photorefractory
state (assessed by gonadal regression and onset of
molting), or on short days (8L:16D) in a photo-
refractory state. No significant differences in
hippocampal neuron recruitment were detected
among the groups, suggesting that photoperiod is
not a cue that acts directly on the survival of adult-
generated neurons in the chickadee hippocampus.
It is plausible, though not proven, that hippocam-
pal neurogenesis plays a role in spatial memory in
food-storing birds. There are indications that the
seasonal pattern found in black-capped chickadees
does not occur in non-food-storing species such as
house sparrows (Hoshooley and Sherry in press).
Future research determining the properties of new
neurons may tell us more about their function.
The receptor profile of these new cellswhether
they possess NMDA or cannabinoid receptors, for
examplemay provide important clues about their
function in the hippocampus. Determining whether
adult-generated neurons become interneurons with
projections entirely within the hippocampus, or
projection neurons exchanging information with
other brain areas, or both, would likewise provide
important clues about their function.
The discovery of neurogenesis in the adult brain
overturned long held ideas about brain structure
and neural plasticity. Much of the initial evidence
for the occurrence of adult neurogenesis came from
research on the song control nuclei of songbirds.
Neurogenesis in the hippocampus of food-storing
birds may lead, similarly, to a greater understand-
ing of how spatial cognition, and perhaps other
cognitive processes, are implemented in the con-
stantly changing network of neurons that make up
the hippocampus.
20 B E H AV I O R A N D E V O L U T I O N
2.4 Summary and conclusions
Chickadees and tits have made an unexpected con-
tribution to our understanding of spatial ability and
the hippocampus because of their specialized food-
storing behavior. The jury is still out on the ques-
tion of whether spatial ability or spatial cognition is
specialized in chickadees and tits. Some properties
of spatial ability and spatial memory in food-stor-
ing birds are very similar to those of other species.
Some quantitative differences in spatial ability have
been found in laboratory studies, however, and no
laboratory studies have successfully simulated the
storage and recovery of thousands of cached food
items as it occurs in the wild over a period of many
months. One pattern that does emerge is that food-
storing birds may tend to solve foraging tasks spa-
tially to a degree not found in other birds.
In contrast to the complex pattern of results in
comparative studies of behavior, comparative
neuroanatomical studies of the hippocampus of
food-storing chickadees and tits are somewhat
clearer. Food-storing birds have a larger hippo-
campus than do non-storing birds, whether the
comparison is made within the Parids or between
Parids and non-storing families. The fine-scale
neuroanatomical causes of this difference in size,
its functional implications, and the role of adult
neurogenesis remain the topics of current research.
Acknowledgements
Preparation of this manuscript was supported by a
Natural Sciences and Engineering Research Council
Discovery Grant to DFS and by a Canadian Institutes
of Health Research Doctoral Research Award to JSH.
We thank Erin Skinner for all of her help with prep-
aration of the manuscript and Scott MacDougall-
Shackleton, Vladimir Pravosudov, and Leslie
Phillmore for their comments and suggestions.
References
Balda, R. P., Kamil, A. C., and Bednekoff, P. A. (1997).
Predicting cognitive capacities from natural history.
Current Ornithology, 13, 333366.
Barnea, A. and Nottebohm, F. (1994). Seasonal recruitment
of hippocampal neurons in adult free-ranging
black-capped chickadees. Proceedings of the National
Academy of Sciences USA, 91, 1121711221.
Barnea, A. and Nottebohm, F. (1996). Recruitment and
replacement of hippocampal neurons in young and
adult chickadees: an addition to the theory of hip-
pocampal learning. Proceedings of the National Academy
of Sciences USA, 93, 714718.
Brodbeck, D. R. (1994). Memory for spatial and local cues:
a comparison of a storing and a nonstoring species.
Animal Learning and Behavior, 22, 119133.
Brodbeck, D. R., Burack, O. R., and Shettleworth, S. J.
(1992). One-trial associative memory in black-capped
chickadees. Journal of Experimental Psychology: Animal
Behavior Processes, 18, 1221.
Brodbeck, D. R. and Shettleworth, S. J. (1995). Matching
location and color of a compound stimulus: comparison
of a food-storing and nonstoring bird species. Journal of
Experimental Psychology: Animal Behavior Processes, 21,
6477.
Brodin, A. (1992). Cache dispersion affects retrieval time
in hoarding willow tits. Ornis Scandinavica, 23, 712.
Brodin, A. (1994). The role of naturally stored food sup-
plies in the winter diet of the boreal willow tit Parus
montanus. Ornis Svevica, 4, 3140.
Brodin, A. and Ekman, J. (1994). Benefits of food hoarding.
Nature, 372, 510.
Brodin, A. and Lundborg, K. (2003). Is hippocampus vol-
ume affected by specialization for food hoarding in
birds? Proceedings of the Royal Society London B, 270,
15551563.
Casini, G., Bingman, V. P., and Bagnoli, P. (1986).
Connections of the pigeon dorsomedial forebrain stud-
ied with WGA-HRP and 3H-proline. Journal of
Comparative Neurology, 245, 454470.
Clayton, N. S. (2001). Hippocampal growth and mainten-
ance depend on food-caching experience in juvenile
mountain chickadees (Poecile gambeli). Behavioural
Neuroscience, 115, 614625.
Colombo, M. and Broadbent, N. (2000). Is the avian
hippocampus a functional homologue of the mam-
malian hippocampus? Neuroscience and Biobehavioral
Reviews, 24, 465484.
Cowie, R. J., Krebs, J. R., and Sherry, D. F. (1981). Food
storing by marsh tits. Animal Behaviour, 29, 12521259.
Crystal, J. D. and Shettleworth, S. J. (1994). Spatial list
learning in black-capped chickadees. Animal Learning
and Behavior, 22, 7783.
Erichsen, J. T., Bingman, V. P., and Krebs, J. R. (1991). The
distribution of neuropeptides in the dorsomedial telen-
cephalon of the pigeon (Columba livia): a basis for
regional subdivisions. Journal of Comparative Neurology,
314, 478492.

Galea, L. A. M. and McEwen, B. S. (1999). Sex and
seasonal differences in the rate of cell proliferation in
the dentate gyrus of adult wild meadow voles.
Neuroscience, 89, 955964.
Garamszegi, L. Z. and Eens, M. (2004). The evolution of
hippocampus volume and brain size in relation to food
hoarding in birds. Ecology Letters, 7, 12161224.
Garamszegi, L. Z. and Lucas, J. R. (2005). Continental
variation in relative hippocampal volume in birds: the
phylogenetic extent of the effect and the potential role
of winter temperatures. Biology Letters, 1, 330333.
Gebauer, A., Jacob, J., Kaiser, M., and Eck, S. (2004).
Chemistry of the uropygial gland secretin of
Humes ground jay Pseudopodoces humilis and its taxo-
nomic implications. Journal fr Ornithologie, 145,
352355.
Gill, F. B., Slikas, B., and Sheldon, F. H. (2005). Phylogeny
of titmice (Paridae): II. Species relationships based on
sequences of the mitochondrial cytochrome-B gene.
Auk, 122, 121143.
Gould, K. L., Newman, S. W., Tricomi, E. M., and
DeVoogd, T. J. (2001). The distribution of substance P
and neuropeptide Y in four songbird species: A com-
parison of food-storing and non-storing birds. Brain
Research, 918, 8095.
Haftorn, S. (1956). Contribution to the food biology of tits
especially about storing of surplus food. Part IV. A com-
parative analysis of Parus atricapillus L., P. cristatus L.
and P. ater L. Det Kgl Norske Videnskabers Selskabs Skrifter,
154.
Hampton, R. R. and Sherry, D. F. (1992). Food storing by
Mexican chickadees and bridled titmice. Auk, 109,
665666.
Hampton, R. R., Sherry, D. F., Shettleworth, S. J., Khurgel,
M., and Ivy, G. (1995). Hippocampal volume and food-
storing behavior are related in parids. Brain Behavior and
Evolution, 45, 5461.
Hampton, R. R. and Shettleworth, S. J. (1996a).
Hippocampal lesions impair memory for location but
not color in passerine birds. Behavioral Neuroscience, 110,
831835.
Hampton, R. R. and Shettleworth, S. J. (1996b).
Hippocampus and memory in a food-storing and in a
nonstoring bird species. Behavioral Neuroscience, 110,
946964.
Hampton, R. R., Shettleworth, S. J., and Westwood, R. P.
(1998). Proactive interference, recency, and associative
strength: comparisons of black-capped chickadees and
dark-eyed juncos. Animal Learning and Behavior, 26,
475485.
Harrap, S. and Quinn, D. (1996). Tits, Nuthatches and
Treecreepers. Helm , London.
N E U R O B I O L O G Y O F S PAT I A L B E H AV I O R 21
Healy, S. D., Clayton, N. S., and Krebs, J. R. (1994).
Development of hippocampal specialisation in two
species of tit (Parus spp.). Behavioural Brain Research, 61,
2328.
Higuchi, H. (1977). Stored nuts Castanopsis cuspidata as a
food resource of nestling varied tits Parus varius. Tori,
26, 912.
Hinde, R. A. (1952). The behaviour of the great tit (Parus
major) and some other related species. Behaviour,
Supplement 2, 1201.
Hitchcock, C. L. and Sherry, D. F. (1990). Long-term mem-
ory for cache sites in the black-capped chickadee.
Animal Behaviour, 40, 701712.
Hoshooley, J. S., Phillmore, L. S., and MacDougall-
Shackleton, S. A. (2005). An examination of avian hip-
pocampal neurogenesis in relationship to photoperiod.
Neuroreport, 16, 987991.
Hoshooley, J. S. and Sherry, D. F. (2004). Neuron produc-
tion, neuron number, and structure size are seasonally
stable in the hippocampus of the food-storing black-
capped chickadee (Poecile atricapillus). Behavioral
Neuroscience, 118, 345355.
Hoshooley, J. S. and Sherry, D. F. (in press). Greater
hippocampal neuronal recruitment in food-storing than
in non-food-storing birds. Journal of Neurobiology.
Jacobs, L. F., Gaulin, S. J. C., Sherry, D. F., and Hoffman,
G. E. (1990). Evolution of spatial cognition: sex-specific
patterns of spatial behavior predict hippocampal size.
Proceedings of the National Academy of Sciences USA, 87,
63496352.
Jacobs, L. F. and Schenk, F. (2003). Unpacking the
cognitive map: The parallel map theory of hippocampal
function. Psychological Review, 110, 285315.
James, H. F., Ericson, P. G. P., Slikas, B., Lei, F.-M., Gill,
F. B., and Olson, S. L. (2003). Pseudopodoces humilis, a
misclassified terrestrial tit (Paridae) of the Tibetan
Plateau: evolutionary consequences of shifting adaptive
zones. Ibis, 145, 185202.
Klln, B. (1962). II. Embryogenesis of brain nuclei in the
chick telencephalon. Ergebnisse der Anatomie und
Entwicklungsgeschichte, 36, 6282.
Karten, H. J. and Hodos, W. (1967). A Stereotaxic Atlas
of the Brain of the Pigeon. Johns Hopkins Press,
Baltimore, MD.
Krayniak, P. F. and Siegel, A. (1978). Efferent connections
of the hippocampus and adjacent regions in the pigeon.
Brain Behavior and Evolution, 15, 372388.
Krebs, J. R., Erichsen, J. T., and Bingman, V. P. (1991). The
distribution of neurotransmitters and neurotransmitter-
related enzymes in the dorsomedial telencephalon of
the pigeon (Columba livia). Journal of Comparative
Neurology, 314, 467477.
22 B E H AV I O R A N D E V O L U T I O N
Krebs, J. R., Healy, S. D., and Shettleworth, S. J. (1990).
Spatial memory of Paridae: Comparison of a storing
and a non-storing species, the coal tit, Parus ater, and
the great tit, P. major. Animal Behaviour, 39, 11271137.
Krebs, J. R., Sherry, D. F., Healy, S. D., Perry, V. H., and
Vaccarino, A. L. (1989). Hippocampal specialization of
food-storing birds. Proceedings of the National Academy of
Sciences USA, 86, 13881392.
Krushinskaya, N. L. (1966). Some complex forms of feed-
ing behaviour of nut-cracker Nucifraga caryocatactes,
after removal of old cortex. Zhurnal Evoluzionni
Biochimii y Fisiloggia, II, 563568.
Kuhlenbeck, H. (1938). The ontogenetic development and
phylogenetic significance of the cortex telencephali in
the chick. Journal of Comparative Neurology, 69, 273301.
Lucas, J. R., Brodin, A. de Kort, S. R., and Clayton, N. S.
(2004). Does hippocampal size correlate with the degree
of caching specialization? Proceedings of the Royal Society
London B, 271, 24232429.
Ludescher, F.-B. (1980). Fressen und Verstecken von
Smereien be der Weidenmeise Parus montanus im
Jahresverlauf unter konstanten Ernhrungsbedingungen.
kologie der Vgel, 2, 135144.
Maguire, E. A., Spiers, H. J., Good, C. D., Hartley, T.,
Frackowiak, R. S. J., and Burgess, N. (2003). Navigation
expertise and the human hippocampus: A structural
brain imaging analysis. Hippocampus, 13, 250259.
Margrie, T. W., Rostas, J. A. P., and Sah, P. (1998). Long-
term potentiation of synaptic transmission in the avian
hippocampus. Journal of Neuroscience, 18, 12071216.
Mello, C. V., Velho, T. A., and Pinaud, R. (2004). Song-
induced gene expression: a window on song auditory
processing and perception. Annals of the New York
Academy of Sciences, 1016, 263281.
Nakamura, H. and Wako, Y. (1988). Food storing behav-
iour of willow tit Parus montanus. Journal of the
Yamashina Institute of Ornithology, 20, 120.
Nottebohm, F. (2002). Neuronal replacement in adult
brain. Brain Research Bulletin, 57, 737749.
Nottebohm, F. (2002). Why are some neurons replaced in
adult brain? Journal of Neuroscience, 22, 624628.
Nottebohm, F. (2004). The road we travelled. Discovery,
choreography, and significance of brain replaceable
neurons. Annals of the New York Academy of Sciences,
1016, 628658.
Patel, S. N., Clayton, N. S., and Krebs, J. R. (1997).
Hippocampal tissue transplants reverse lesion-induced
spatial memory deficits in zebra finches (Taeniopygia
guttata). Journal of Neuroscience, 17, 38613869.
Patel, S. N., Clayton, N. S., and Krebs, J. R. (1997). Spatial
learning induces neurogenesis in the avian brain.
Behavioural Brain Research, 89, 115128.
Pawluski, J. L. and Galea, L. A. M. (2006). Hippocampal
morphology is differentially affected by reproductive
experience in the mother. Journal of Neurobiology, 66,
7181.
Pravosudov, V. V. (1985). Search for and storage of food by
Parus cinctus Lapponicus and P. montanus borealis
(Paridae). Zoologichesky Zhurnal, 64, 10361043.
Pravosudov, V. V. (1986). Individual differences in for-
aging and storing behaviour in Siberian tit Parus cinctus
Bodd. and Willow tit Parus montanus Bald. Soviet Journal
of Ecology, 4, 6064.
Pravosudov, V. V. and Omanska, A. (2005). Dominance-
related changes in spatial memory are associated
with changes in hippocampal cell proliferation rates
in mountain chickadees. Journal of Neurobiology, 62,
3141.
Pravosudov, V. V. and Omanska, A. (2005). Prolonged
moderate elevation of corticosterone does not affect
hippocampal anatomy or cell proliferation rates in
mountain chickadees (Poecile gambeli). Journal of
Neurobiology, 62, 8291.
Richards, T. J. (1958). The concealment and recovery of
food by birds, with some relevant observations on
squirrels. British Birds, 51, 497508.
Scharff, C., Kirn, J. R., Grossman, M., Mackis, J. D., and
Nottebohm, F. (2000). Targeted neuronal death affects
neuronal replacement and vocal behavior in adult
songbirds. Neuron, 25, 481492.
Sherry, D. F. (1984). Food storage by black-capped
chickadees: memory for the location and contents of
caches. Animal Behaviour, 32, 451464.
Sherry, D. F. (1989). Food storing in the paridae. Wilson
Bulletin, 101, 289304.
Sherry, D. F. (2006). Neuroecology. Annual Review of
Psychology, 57, 167197.
Sherry, D. F., Jacobs, L. F., and Gaulin, S. J. C. (1992).
Spatial memory and adaptive specialization of the
hippocampus. Trends in Neurosciences, 15, 298303.
Sherry, D. F., Krebs, J. R., and Cowie, R. J. (1981). Memory
for the location of stored food in marsh tits. Animal
Behaviour, 29, 12601266.
Sherry, D. F. and Vaccarino, A. L. (1989). Hippocampus
and memory for food caches in black-capped chicka-
dees. Behavioral Neuroscience, 103, 308318.
Sherry, D. F., Vaccarino, A. L., Buckenham, K., and Herz,
R. S. (1989). The hippocampal complex of food-storing
birds. Brain Behavior and Evolution, 34, 308317.
Shettleworth, S. D. and Krebs, J. R. (1986). Stored and
encountered seeds: A comparison of two spatial
memory tasks in marsh tits and chickadees. Journal of
Experimental Psychology: Animal Behavior Processes, 12,
248257.

Shettleworth, S. J. and Krebs, J. R. (1982). How marsh tits
find their hoards: the roles of site preference and spatial
memory. Journal of Experimental Psychology: Animal
Behavior Processes, 8, 354375.
Shettleworth, S. J., Krebs, J. R., Healy, S. D., and Thomas,
C. M. (1990). Spatial memory of food-storing tits (Parus
ater and P. atricapillus): Comparison of storing and non-
storing tasks. Journal of Comparative Psychology, 104,
7181.
Shettleworth, S. J. and Westwood, R. P. (2002). Divided
attention, memory, and spatial discrimination in food-
storing and nonstoring birds, black-capped chickadees
(Poecile atricapilla) and dark-eyed juncos (Junco hye-
malis). Journal of Experimental Psychology: Animal
Behavior Processes, 28, 227241.
Shiflett, M. W., Smulders, T. V., Benedict, L., and
DeVoogd, T. J. (2003). Reversible inactivation of the hip-
pocampal formation in food-storing black-capped
chickadees (Poecile atricapillus). Hippocampus, 13,
437444.
Shiflett, M. W., Tomaszycki, M. L., Rankin, A. Z., and
DeVoogd, T. J. (2004). Long-term memory for spatial
locations in a food-storing bird (Poecile atricapilla)
requires activation of NMDA receptors in the hip-
pocampal formation during learning. Behavioral
Neuroscience, 118, 121130.
Siegel, J. J., Nitz, D., and Bingman, V. P. (2002).
Electophysiological profile of avian hippocampal unit
activity: A basis for regional subdivisions. Journal of
Comparative Neurology, 445, 256268.
Siegel, J. J., Nitz, D., and Bingman, V. P. (2005). Spatial-
specificity of single-units in the hippocampal formation
N E U R O B I O L O G Y O F S PAT I A L B E H AV I O R 23
of freely moving homing pigeons. Hippocampus, 15,
2640.
Smulders, T. V. and DeVoogd, T. J. (2000). Expression of
immediate early genes in the hippocampal formation of
the black-capped chickadee (Poecile atricapillus) during
a food-hoarding task. Behavioral Brain Research, 114,
3949.
Southern, J. B. (1946). Unusual feeding behaviour of tits.
British Birds, 39, 214.
Stevens, T. A. and Krebs, J. R. (1986). Retrieval of stored
seeds by marsh tits Parus palustris in the field. Ibis, 128,
513525.
Stewart, M. G., Cristol, D., Philips, R., Steele, R. J.,
Stamatakis, A., Harrison, E., and Clayton, N. (1999). A
quantitative autoradiographic comparison of binding
to glutamate receptor sub-types in hippocampus and
forebrain regions of a food-storing and non-food-stor-
ing bird. Behavioural Brain Research, 98, 8994.
Stokes, T. M., Leonard, C. M., and Nottebohm, F. (1974).
The telencephalon, diencephalon, and mesencephalon
of the canary Serinus canarius in stereotaxic coordinates.
Journal of Comparative Neurology, 156, 337374.
Szekely, A. D. (1999). The avian hippocampal formation:
subdivisions and connectivity. Behavioural Brain
Research, 98, 219225.
Tramontin, A. D. and Brenowitz, E. A. (2000). Seasonal
plasticity in the adult brain. Trends in Neurosciences, 23,
251258.
Watanabe, S. and Bischof, H. (2004). Effects of hippocam-
pal lesions on acquisition and retention of spatial learn-
ing in zebra finches. Behavioural Brain Research, 155,
147152.
This page intentionally left blank
 CHAPTER 3
The relationship between
environment, corticosterone, food
caching, spatial memory, and the
hippocampus in chickadees
Vladimir V. Pravosudov
3.1 Introduction
Many species in the family Paridae are well known
for their food-caching behavior (Haftorn 1956;
Pravosudov 1985; Brodin and Lundborg 2003; Lucas
et al. 2004). All North American Parids have been
reported to cache food whereas in Eurasia there are
a few species that do not cache (Brodin and
Lundborg 2003a; Lucas et al. 2004). Natural food
caching in free-ranging Parids has been studied most
intensively in Eurasian specieswillow, coal,
crested, marsh, and Siberian tits (Haftorn 1956;
Pravosudov 1985; Brodin 1994)whereas data on
natural food caching in North American Parids are
extremely scant (Odum 1942; Brodin 2005). Some
well-studied Eurasian Parids (willow and Siberian
tits) have been reported to make more than a 100 000
individual food caches each autumn (Haftorn 1956;
Pravosudov 1985; Brodin 1994) to be used through-
out the winter. Food caching thus appears to be an
important adaptation, promoting the birds survival
during the winter (e.g. Pravosudov and Lucas 2001),
and it is important to understand how these birds
retrieve their caches. It is known that food-caching
birds rely, at least in part, on spatial memory to find
their caches (review in Shettleworth 1995; Chapter 2)
and research on spatial memory and the hippocam-
pus, a part of the brain involved in spatial memory
processing (Sherry and Vaccarino 1989; Hampton
and Shettleworth 1996a, b), has focused on both
Eurasian and North American Parids (Shettleworth
1995; Chapter 2). Glucocorticoid hormones are also
known to affect spatial memory (Sapolsky 1996;
McEwen and Sapolsky 1995; McEwen 2000) and
thus the local environment might influence spatial
memory via changes in glucocorticoid hormones
levels (Pravosudov 2003). Here, I review studies
dealing with the relationship between environment,
food caching, spatial memory, corticosterone, and
the hippocampus in North American chickadees
while providing comparisons with similar studies
done using Eurasian Parids.
3.2 Inter- and intraspecific differences in
caching, spatial memory, and the
hippocampus
3.2.1 Interspecific differences
Almost all food-caching birds live in environments
with pronounced differences between seasons in
accessibility of food. As a result, the benefits of
strong spatial memory and food caching might
typically be higher during the winter when envir-
onmental conditions are most energetically
demanding. Also, some species experience more
severe environmental conditions than others.
Consequently, the advantages of food caching
should be much higher for species living in more
energetically demanding environments, resulting
in higher selection pressure for more caching and
more efficient cache recovery (Krebs et al. 1989,
25
26 B E H AV I O R A N D E V O L U T I O N
1996). It has been hypothesized that the increased
demands for the spatial memory needed to recover
thousands of previously made food caches has
resulted in enhanced spatial memory and enlarged
hippocampus in food-caching birdscoined the
adaptive specialization hypothesis (Krebs et al.
1989, 1996; Sherry et al. 1989; Chapter 2). This
hypothesis has been mainly tested using species
from two avian familiesthe Paridae and
Corvidaeas both of these families contain food-
caching and non-caching species (Sherry et al. 1989;
Krebs et al. 1989, 1996; Chapter 2). Here I will briefly
review the comparisons using Parids.
Healy and Krebs (1996) reported that food-
caching Eurasian Parids have relatively larger
hippocampal volume compared to non-caching
species. Brodin and Lundborg (2003a) analyzed a
large multispecies data set, including both Eurasian
and North American Parids (the latter of whom all
cache) as well as many other caching and non-
caching species, and found little evidence that the
degree of caching specialization is related to hip-
pocampal volume. Lucas et al. (2004) reanalyzed
Brodin and Lundborgs (2003a) data set, introducing
a new variablethe continent on which the birds
occurredand their analysis supported the adaptive
specialization hypothesis. The different conclusions
reflected an apparent difference in hippocampal and
brain volumes between Eurasian and North
American Parids; once these differences were statis-
tically controlled, the relative hippocampal volume
appeared to be larger in food-caching Parids (Lucas
et al. 2004, see also Chapter 2). Lucas et al. (2004)
suggested that compared to North American
species, relative hippocampus and overall brain size
is larger in Eurasian birds, possibly due to different
environmental conditions (Garamszegi and Lucas
2005; Chapter 2) but it remains possible, however,
that these continental differences could be due to
differences between laboratories in processing and
analyzing the brains (Pravosudov and de Kort 2006).
While differences in hippocampal volume may
indicate differences in the potential for spatial
memory performance, behavioral tests to confirm
that these differences occur have focused on only a
handful of species. In Europe, most comparisons
concerned food-caching marsh and coal tits and
non-caching blue tits (Shettleworth 1995) while in
North America all comparative studies focused on
food-caching black-capped chickadees and non-
caching dark-eyed juncos (Junco hyemalis;
Shettleworth 1995). The results of these compari-
sons were not consistent; in the majority of tests,
food-caching birds outperformed non-caching
species (Biegler et al. 2001; Shettleworth 1995), but
some comparisons yielded non-significant results
(see Shettleworth 1995 for review) and in one study
non-caching dark-eyed juncos outperformed food-
caching black-capped chickadees on one spatial
memory task (Hampton and Shettleworth 1996b).
Hampton et al. (1995) compared three North
American Paridsblack-capped chickadees,
Mexican chickadees, and bridled titmicewhich
appear to differ in their food-caching behavior. Of
these three species, black-capped chickadees have a
more northerly distribution and are well known
food-cachers (Brodin 2005). Mexican chickadees and
bridled titmice, on the other hand, occupy a more
southerly range and have not been observed to cache
food in natural conditions (Hampton et al. 1995). In
captivity, however, both Mexican chickadees and
bridled titmice cached food, indicating that caching
behavior is present in these two species (Hampton
and Sherry 1992; Hampton et al. 1995). Hampton
et al. (1995) hypothesized that the more southerly
Mexican chickadees and bridled titmice do not have
a strong dependence on cached food for their
survival because of their relatively mild, southern
environmental conditions and, as a result, they
should cache less food and have smaller hippocampi
than black-capped chickadees. Indeed, Hampton
et al. (1995) found that black-capped chickadees have
relatively larger hippocampi than both Mexican
chickadees and bridled titmice but the data on food
caching were ambiguous. In two captive experiments
there were no significant differences in caching rates
between black-capped and Mexican chickadees. In
one of the two experiments, there were also no
statistical differences between all three species in the
amount of food caching (Hampton et al. 1995).
3.2.2 Intraspecific differences
In all interspecific comparisons employed to
test the adaptive specialization hypothesis, the
main underlying assumption was that the biggest
 THE HIPPOCAMPUS IN CHICKADEES 27

difference between the species lies in their food-
caching behavior (Krebs et al. 1989; Sherry et al.
1989; Brodin and Lundborg 2003a; Lucas et al. 2004;
Chapter 2). However, it is possible that there are
other differences between species, unrelated to
caching behavior, that could have resulted in differ-
ential selection pressure on both spatial memory
and the hippocampus. Comparing different popu-
lations within the same species might provide an
opportunity to control for such differences.
Many food-caching Parids occupy extremely wide
ranges, extending from south to north (Harrap and
Quinn 1995) with greatly varying environmental
conditions, especially during the winter. The range of
black-capped chickadees, for example, extends from
New Mexico in the south to Alaska in the north
(Harrap and Quinn 1995). Compared to more
southerly populations, Alaskan black-capped chicka-
dees regularly experience longer winters with lower
ambient temperatures, deeper and longer lasting
snow cover, and, most importantly, much shorter
day-length available for foraging during winter
(Pravosudov and Clayton 2002). Obtaining enough
food to build energy reserves sufficient to survive
the night is crucial for survival in these small birds
(e.g. Pravosudov and Lucas 2001) and, in December,
Alaskan chickadees have only about 5 hours of
daylight to obtain enough energy reserves to survive
about 19 hours of night. In Colorado, on the other
hand, these birds have almost twice as much daylight
hours to complete the same foraging task while prob-
ably requiring less energy due to generally warmer
night-time temperatures (Pravosudov and Clayton
2002). In both environments, caches should provide a
more predictable food source than naturally available
food. Having sufficient food caches, and the capacity
to successfully find them when needed should thus
have much larger survival consequences for chicka-
dees in energetically demanding Alaskan conditions.
Such differences in the significance of cached food
between southern and northern populations are
likely to provide higher selection pressure in north-
ern populations for more intense food caching, better
spatial memory, and larger hippocampi.
When black-capped chickadees from Alaska and
Colorado were acclimatized for 45 days and then
tested in identical laboratory conditions, birds
from Alaska cached significantly more food and
performed significantly better on a spatial version of
a one-trial associative learning task (Fig. 3.1;

(a) (b)

Alaska Alaska
8
Mean number of sites inspected

Colorado
Colorado 6

6
Number of seeds

4
4

2
2

0 0
Consumed Cached 70 sites 15 sites Color

Figure 3.1 Mean number of seeds consumed (fully or partially) and cached during 20-min food-caching trials (a) and memory performance in a
one-trial associative learning task (b) by black-capped chickadees from Alaska (black bars) and Colorado (hatched bars) (redrawn from Pravosudov
and Clayton 2002). Memory performance was measured as the number of sites inspected ( number of looks) in order to find the site previously
containing food among either 70 or 15 available sites. Fewer looks indicate better memory performance. A color version of a one-trial associative
learning task was used to investigate possible motivational differences between the groups. If one group were less motivated to search for food, it
would show similar poor performance on both spatial and color versions of the task. If there were differences in spatial memory between the
groups, there would be differences in performance on spatial but not on color version of a one-trial associative learning task.
28 B E H AV I O R A N D E V O L U T I O N

Pravosudov and Clayton 2002). Interestingly, experience in the laboratory. A separate analysis of a
Alaskan chickadees were significantly smaller, with control group of birds, which did not participate in
smaller brains, than chickadees from Colorado the experiment while being maintained in the
(Fig. 3.2; Pravosudov and Clayton 2002). Compared laboratory for the same duration of time, revealed no
to Colorado chickadees, however, individuals from differences in the hippocampal volume or neuron
Alaska had significantly larger hippocampi with numbers between the individuals that cached food
more neurons in both absolute terms and relative to and the ones that did not cache food (Pravosudov
telencephalon volume (Fig. 3.2; Pravosudov and and Clayton 2002). At the same time, the differences
Clayton 2002). These results support the adaptive between Alaska and Colorado remained even in
specialization hypothesis; because Alaskan individuals that did not cache food during the
chickadees exist in a more energetically demanding experiment, thus ruling out a possibility that larger
environment, they cache more food, and have hippocampus with more neurons in Alaskan chicka-
better spatial memorywhich may be associated dees resulted from more caching during the experi-
with their larger hippocampi containing more ment. It remains possible, however, that differences
neuronscompared to conspecifics from Colorado between Alaska and Colorado chickadees in food
(Pravosudov and Clayton 2002). caching and cache retrieval experience prior to cap-
Based on the above data, however, it was not ture produced long-term changes in memory and
possible to unambiguously conclude whether the the hippocampus and thus further testing is neces-
differences in caching, spatial memory, and hip- sary to differentiate between a genetic versus envi-
pocampal volume were genetic or experience based. ronmental basis of population differences.
Birds from both Alaska and Colorado were main- Irrespective of the basis of these differences
tained and tested in identical laboratory environ- between Alaskan and Colorado black-capped
ments, suggesting that the differences found chickadees, more food caching, better spatial
between these groups were not related to the imme- memory, and an enlarged hippocampus with more
diate environment. Alaskan chickadees cached more neurons in Alaskan individuals appear to be
food and thus they had more food-caching highly adaptive to life in extremely energetically

20
Volume of the hippocampal formation (mm3)

18

16

14

12

10

8
180 200 220 240 260 280 300 320 340 360 380 400
Volume of the remainder of telencephalon (mm3)

Figure 3.2 The relationship between the hippocampal volume and the volume of the rest of the telencephalon in black-capped chickadees from
Alaska (open circles) and Colorado (filled circles) (redrawn from Pravosudov and Clayton 2002).

challenging environments. More research is needed
to ascertain whether these differences have a
genetic basis. Similar intraspecific studies may also
be possible with tufted titmice, Carolina chicka-
dees, Siberian and willow tits, or high-elevation
populations of mountain chickadees, which would
test the generality of environmental selection on
caching behavior across species.
3.3 Unpredictable food, corticosterone,
spatial memory, and the hippocampus
3.3.1 Seasonality in food caching and
spatial memory
Most food-caching Parids live in highly seasonal envi-
ronments; food is abundant during summer and early
autumn but during the winter it is often limited and
unpredictable (Pravosudov and Grubb 1997a). Food-
caching patterns mostly follow a seasonal cycle; birds
cache most when food is plentiful outside the breed-
ing seasonlate summer and early autumn and,
sometimes, in spring when there is abundance of
conifer seeds (Haftorn 1956; Pravosudov 1985; Brodin
1994). During these periods, birds can cache thou-
sands of food items (Haftorn 1956; Pravosudov 1985;
Brodin 1994). These food caches appear to be crucial
for winter survival and thus the ability to retrieve
them should be of paramount importance. Parids
continue to cache throughout the winter although
they cache a fairly small amount of food during that
time (Pravosudov 1985). It is not clear whether winter
caching involves storing newly found food or
recaching previously hidden food stores (Pravosudov
and Grubb 1997a), but winter short-term caching
might be important for the birds survival on a daily
basis (Pravosudov and Lucas 2001).
In seasonal environments, demands for spatial
memory do not appear to be equal throughout the
year. If a bird does not remember where it stored
food during summer and early autumn when nat-
ural food is abundant, it is unlikely to die of starva-
tion. During the winter, however, failure to recover
food caches is more likely to result in mortality and
thus demands for spatial memory should be higher
during the winter (Pravosudov and Clayton 2001).
Thus there might be seasonal variation in the birds
spatial memory abilities and also in mechanisms
THE HIPPOCAMPUS IN CHICKADEES 29
underlying spatial memory function. Because birds
that cache more food appear to have larger hippo-
campi, it is possible to predict that if there is
seasonal variation in spatial memory it may be
accompanied by variation in hippocampal volume
and/or neuron numbers.
Despite numerous suggestions that spatial mem-
ory might vary seasonally, there have been no stud-
ies documenting such variation. Whereas it may be
difficult to measure seasonal variation in spatial
memory, it is possible to test whether any of the
parameters associated with seasonal changes in the
environment, such as photoperiod or food supply,
have an effect on spatial memory.
3.3.2 Seasonal variation in hippocampus
volume, neuron number, and neurogenesis
rates
Smulders et al. (1995, 2000) reported that hippocam-
pal volume and neuron numbers change seasonally,
with the largest hippocampal volume and most
neurons occurring during October. Smulders et al.
(1995, 2000) hypothesized that hippocampal volume
should track seasonally changing demands for spa-
tial memory and that the maximum hippocampal
volume should be observed in the autumn when
food caching is most intense (Haftorn 1956;
Pravosudov 1985; Brodin 2005). Other food-caching
Parids, however, do not rely on food caches during
the period when caching rates are at maximum
because natural food is relatively abundant during
this period (Haftorn 1956; Pravosudov 1985). This
appears to be also true for North American Parids
(Brodin 2005). Successful retrieval of food caches
may be more crucial later during the winter when
failure to find caches might result in increased mor-
tality (Pravosudov and Lucas 2001).
Smulders and Dhondt (1997) hypothesized that
food-caching Parids might specifically need extra
memory during food caching in order to memorize
cache locations and to create optimal cache distri-
bution that minimize cache pilferage. Based on
these assumptions, they suggest hippocampal
volume might be largest in October, when food
caching was assumed to be most intense. Shiflett
et al. (2003) argued that the hippocampus is
involved specifically in memory encoding, which
30 B E H AV I O R A N D E V O L U T I O N
occurs during food caching and that the hippocam-
pus might not be involved in memory recall during
cache retrieval. Clayton (2001), on the other hand,
showed that young mountain chickadees that were
allowed to cache, but not to retrieve, seeds had
smaller relative hippocampal volume than chicka-
dees that both cached and retrieved seeds. This
result seems to suggest that retrieving caches might
provide a stronger impact on hippocampal struc-
ture than food caching alone.
Another important detail is that, so far, there is
little good data on seasonal variation in food-
caching rates in North American Parids
(Pravosudov 2006). A single study showed that
black-capped chickadees cached most food at the
end of September but no observations were avail-
able for August or early September (Brodin 2005).
Much more extensive data on several Eurasian
food-caching Parids show strong variation in food-
caching rates; often these Parids cached most in
September and cached as much food in August as in
October (Pravosudov 2006). In addition, some
Eurasian Parids might also cache food intensely
during spring (Pravosudov 2006). Although North
American Parids might have different seasonal
food-caching patterns it remains difficult to inter-
pret data on seasonal changes in hippocampal struc-
ture without knowing the precise patterns of
food-caching activity.
Studies on seasonal variation in hippocampal vol-
ume (Hoshooley and Sherry 2004) or total number of
neurons (Barnea and Nottebohm 1994; Hoshooley
and Sherry 2004), however, have also not found sup-
port for seasonal differences (see also Chapter 2).
Barnea and Nottebohm (1994) did report seasonal
variation in hippocampal neuron recruitment rates
in black-capped chickadees; more new neurons were
observed in the hippocampus of birds injected with
a cell division marker during October than at any
other time of year. Barnea and Nottebohm (1994)
concluded that neurogenesis supports memory
function because the highest neuron recruitment
rates coincided with the predicted highest food-
caching rates during October, but they did not pres-
ent data on the actual variation in caching rates of
birds during these time frames. Further, their results
do contain some ambiguity, as they measured the
number of neurons which survived at least 6 weeks
from October injections, rather than the number of
neurons actually produced in October. Such a result
can be achieved through increased neuron produc-
tion, increased survival of new neurons, or both
(Prickaerts et al. 2004; Chapter 2). Hoosholey and
Sherry (2004) found no significant seasonal variation
in neuron production rates in the hippocampus of
black-capped chickadees, suggesting that Barnea
and Nottebohms (1994) results might be explained
by higher survival rates of neurons that were born in
October. Higher survival rates of new neurons
coupled with stable total neuron numbers suggest
that neuron turn over rates could potentially be
lower during October. Neurons born in October may
not be immediately functional, as it takes some time
for the neurons to mature and to incorporate into the
existing neuronal circuits in the hippocampus. Thus,
these neurons may become functional only by the
end of OctoberNovember and, because they appear
to survive longer, these new neurons could remain
functional in December and later. This might shift
the significance of these neurons from October, one
of the months when food caching is often assumed
to be most intense, to NovemberDecember when
food caching might be reduced (Haftorn 1956;
Pravosudov 1985) and cache retrieval becomes cru-
cial for survival. Neurons born in December were
reported to have lower survival (Barnea and
Nottebohm 1994), but these neurons would most
likely become functional only in JanuaryFebruary.
Further research is necessary to understand
whether hippocampal structure and neurogenesis
consistently undergo seasonal changes specifically
associated with changes in food-caching activity. In
particular, it would be important to investigate
whether hippocampal structure and neurogenesis
vary in individual birds in relation to their specific
food-caching behavior. More data are also neces-
sary to document variation in seasonal changes in
food-caching behavior.
3.3.3 Photoperiod
Seasonality is associated with predictable changes
in photoperiod and thus it is possible that photo-
period could trigger seasonal changes, if any, in food
caching, spatial memory, and the hippocampus
(Chapter 4). Food caching is often most intensive

during autumn when day-length becomes shorter;
however, intensive caching has also been reported
during spring when day-length actually becomes
longer (Haftorn 1956; Pravosudov 1985, 2006). Most
laboratory manipulations of photoperiod have
demonstrated that black-capped chickadees and
marsh tits cache more food on short days (Krebs
et al. 1995; Shettleworth et al. 1995; Clayton and
Cristol 1996), suggesting that decreasing day-length
may be responsible for the autumnal peak in food
caching (but Karpouzos et al. (2005) reported no
effect of photoperiod on food caching in black-
capped chickadees). However, these results do not
explain spring bursts of food caching and thus it
remains possible that seasonal peaks in long-term
caching are not necessarily under photoperiodic
control (Pravosudov 2006).
It is also not clear whether spatial memory is
affected by photoperiod. Clayton and Cristol (1996)
reported that marsh tits switched from long to short
days showed better spatial memory performance
than their conspecifics maintained on long days. But
when birds maintained on short, winter-like days
were changed to long days and the birds maintained
on long days were switched to short days, there were
no differences between the groups in spatial memory
performance, even though the birds on short days
were caching more food. If photoperiod was
involved in spatial memory regulation, birds on short
days should have shown better memory perform-
ance, which did not happen during the latter test.
Experimental manipulation of photoperiod
also failed to induce significant changes in the
hippocampal volume in black-capped chickadees
(Krebs et al. 1995; MacDougall-Shackleton et al. 2003)
and baseline corticosterone levels were statistically
indistinguishable between mountain chickadees
maintained on short and long days (Pravosudov
et al. 2002a). Thus whereas photoperiod appears to
affect food-caching rates in captive birds, there
appears to be insufficient evidence that it has an
effect on spatial memory and the hippocampus.
3.3.4 Unpredictable food supply
Most food-caching Parids live in the temperate zone
and experience seasonal variation in food availabil-
ity and predictability (Pravosudov and Grubb
THE HIPPOCAMPUS IN CHICKADEES 31
1997a). Food is usually abundant in summer and
autumn but becomes much less abundant during the
winter. Winter is also the most energetically
demanding season because of short days and low air
temperature, and successful retrieval of food caches
becomes critically important during the winter
(Pravosudov and Lucas 2001). Thus food availability
and predictability might directly affect food caching
and cache retrieval (Pravosudov and Clayton 2001).
When food supply was made limited and unpre-
dictable in a laboratory for 60 days, mountain
chickadees demonstrated more efficient cache
recovery (by searching significantly fewer available
cache sites) and showed better spatial memory
performance compared to individuals maintained
on ad libitum food (Fig. 3.3; Pravosudov and
Clayton 2001). Thus, it appears that chickadees
might have better spatial memory, resulting in
more efficient cache retrieval, during the winter
when available food is rather scarce. To determine
whether better performance on memory tests by
food-deprived chickadees was associated with bet-
ter spatial memory and not with higher levels of
motivation to search for food, Pravosudov and
Clayton (2001) used an associative learning task in
which a site containing food was associated with a
specific color (local) cues. If non-deprived chicka-
dees were less motivated to search for food, they
would show similar performance on both spatial
and color-associative learning tasks. Pravosudov
and Clayton (2001) found that differences in mem-
ory performance between deprived and non-
deprived individuals were present only in the
spatial test whereas in the non-spatial, color test the
groups showed similar performance (Fig. 3.3). Such
results suggested that the differences between
food-deprived and non-deprived chickadees were
most likely due to differences in spatial memory
and not in motivation to search for food.
Hippocampal volume and the total number of
neurons, however, were statistically indistinguish-
able between mountain chickadees maintained on
limited and unpredictable food supply and those
on ad libitum food supply (Pravosudov et al. 2002),
which suggests that changes in spatial memory
triggered by changes in food supply were not sup-
ported by structural changes in the hippocampus.
Interestingly, baseline corticosterone levels were
32 B E H AV I O R A N D E V O L U T I O N

(a) (b)
Unpredictable food

Mean number of sites inspected

Ad libitum food
6
Corticosterone (ng/ml)

2 4

1 2

0 0
Unpredictable Ad libitum 144 sites 12 sites color
food food

Figure 3.3 Baseline corticosterone levels (a) and memory performance in a one-trial associative learning task (b) in mountain chickadees
maintained on limited and unpredictable food schedule (black bars) and on ad libitum food (hatched bars). ((a) is reprinted from General and
Comparative Endocrinology, 123, Pravosudov et al. Long-term unpredictable foraging conditions and physiological stress response in mountain
chickadees (Poecile gambeli), pp. 324331, Copyright (2001), with permission from Elsevier; b is redrawn from Pravosudov and Clayton 2001).
Memory performance was measured as the number of sites inspected in order to find a single site previously containing food among either 144
or 12 available sites. Fewer sites inspected indicate better memory performance. A color version of a one-trial associative learning task was used
to investigate possible motivational differences between the groups (see also legend Fig. 3.1).

significantly elevated in birds maintained on corticosterone has an effect on memory in birds

limited food (Fig. 3.3; Pravosudov et al. 2001). Thus (Loscertales et al. 1997; Sandi et al. 1995; Sandi and
relatively long-term (2 months) limited and unpre- Rose 1997). Saldanha et al. (2000) reported that
dictable food supply resulted in moderately but short-term, strong corticosterone elevation resulted
significantly elevated baseline corticosterone and in in improved spatial memory performance in moun-
enhanced spatial memory. Such results suggested tain chickadees. Chickadees in the Saldanha et al.
that elevated corticosterone might have been (2000) study received extremely high doses of
directly responsible for spatial memory improve- corticosterone which likely resulted in unnaturally
ments observed in mountain chickadees in the high corticosterone plasma levels (Pravosudov
absence of any changes in hippocampal volume or 2005); it thus remains unclear whether naturally
neuron numbers. occurring corticosterone elevations would provide
similar effects on memory.
Unlike short-term (hours or maybe days),
3.4 Corticosterone, food caching, spatial
chronic (weeks or months) corticosterone eleva-
memory, and the hippocampus
tions have been reported to result in memory
It is well known that corticosterone has an effect on impairments (Sapolsky 1996; McEwen and
memory function (Sapolsky 1996; McEwen and Sapolsky 1995; McEwen 2000). It appears, however,
Sapolsky 1995; McEwen 2000). It has generally been that baseline corticosterone levels may remain
assumed that short-term (hours, days) elevations elevated in wintering Parids over several months
in corticosterone enhance spatial memory whereas (Silverin 1998willow tits), which would fall
prolonged, chronic (weeks) elevations might have under the long-term category for these rather short-
extremely deleterious effects. Most of the research lived birds. Experimental manipulations of food
addressing the relationship between corticosterone supply designed to decrease food predictability
elevation and memory has been focused on and/or availability also triggered a prolonged
mammals (McEwen and Sapolsky 1995; McEwen elevation of baseline corticosterone in mountain
2000) but there are also studies suggesting that chickadees (Pravosudov et al. 2001) and in red

knots (Calidris canutus; Reneerkens et al. 2002). It is
important to note that such elevations were only
moderate and they exceeded the baseline levels
only two or three times compared to stress-induced
levels which might exceed baseline concentration
by more than 10 times (Silverin 1998; Wingfield
et al. 1997, 1998).
Thus it is not clear whether long-term but mod-
erate corticosterone elevations are necessarily asso-
ciated with the same negative effects on memory
and the brain as long-term, stress-induced-like high
elevations. It appears that prolonged, moderate
corticosterone elevations might occur when birds
face both the highest demands for feeding effi-
ciency in order to survive and when memory for
the location of food caches could also be most crit-
ical for survival (Pravosudov and Clayton 2001;
Pravosudov 2005). Foraging conditions that caused
long-term (2 months), moderate corticosterone
elevation in mountain chickadees also resulted in
enhanced spatial memory and more efficient cache
retrieval (Pravosudov and Clayton 2001), a result
potentially contradicting a conventional assump-
tion that any chronic elevation in glucocorticoids
might be deleterious for memory function
(Sapolsky 1996; McEwen and Sapolsky 1995;
McEwen 2000) and suggesting that elevated
corticosterone might have actually caused the
observed memory improvements.
When given corticosterone implants designed to
maintain moderate corticosterone elevations (about
1.5 times higher than baseline; resembling those
observed in natural conditions during winter
(Silverin 1998) and in birds maintained on unpre-
dictable food supply (Pravosudov et al. 2001)) for
several weeks, mountain chickadees demonstrated
better spatial memory performance compared
to placebo-implanted individuals (Fig. 3.4b,
Pravosudov 2003), supporting a link between
elevated corticosterone and spatial memory.
Furthermore, compared to placebo-implanted
birds, corticosterone-implanted chickadees fed
more intensively and cached significantly more
food (Fig. 3.4a, Pravosudov 2003). Thus, long-term,
moderately elevated corticosterone might facilitate
more foraging and food caching while enhancing
the spatial memory required for successful cache
retrieval. This entire suite of behaviors is likely to
THE HIPPOCAMPUS IN CHICKADEES 33
increase birds probability of survival when envi-
ronmental conditions are energetically demanding,
such as during the winter. These results suggest
that prolonged but moderately elevated cortico-
sterone levels may be highly adaptive by enhancing
memory rather than impairing it, as it has been
widely suggested (Sapolsky 1996; McEwen and
Sapolsky 1995; McEwen 2000).
Elevated corticosterone might have a positive
effect on memory through several possible mechan-
isms including elevated glucose levels, enhanced
protein synthesis in the brain, and increased
hippocampal neuron firing rates (see review in
Pravosudov 2005). Interestingly, hippocampal
neuron firing rates seem to have an inverted-U
relationship with corticosterone levels (Diamond
et al. 1992), which is in agreement with our results
suggesting that moderate corticosterone elevations
might enhance spatial memory.
The fact that birds do not always maintain mod-
erately elevated corticosterone levels despite its
apparent benefits suggests that even moderate cor-
ticosterone elevations carry costs (e.g. weakening
immune function, Wingfield et al. 1997, 1998). These
costs, however, do not seem to concern memory
function.
It has been suggested that chronically elevated
corticosterone might impair memory through
increased neuronal death but most experimental
studies used high doses of corticosterone resulting
in unnaturally high elevations (e.g. 10 baseline)
(Sapolsky 1996; McEwen and Sapolsky 1995;
McEwen 2000). Such elevations might not necessar-
ily occur under naturally stressful conditions and it
is important to understand the consequences of
naturally occurring corticosterone elevations.
Prolonged, moderately elevated corticosterone
levels associated with unpredictable food had no
detectable effects on hippocampal structure
(Pravosudov et al. 2002b). Analogously, there were
no significant differences between corticosterone-
and placebo-implanted mountain chickadees in
either hippocampal volume, total number of hip-
pocampal neurons, or cell proliferation rates in the
ventricular zone adjacent to the hippocampus and
to the mesopallium (Pravosudov and Omanska
2005a). Thus relatively long-term (49 days with cor-
ticosterone implants and 94 days on limited and
34 B E H AV I O R A N D E V O L U T I O N

(a) (b)

Corticosterone Corticosterone
15 Placebo
Placebo

Mean number of sites inspected

12
Number of nuts

10
8

5 4

0 0
Cached Consumed Location Color Location
(precolor) (postcolor)

Figure 3.4 Mean number of consumed (fully or partially) and cached pine nuts during food-caching trials (a) and memory performance in a
one-trial associative learning task (b) in mountain chickadees implanted with corticosterone (black bars) or placebo (hatched bars) (redrawn from
Pravosudov 2003). Memory performance was measured as the number of sites inspected in order to find the site previously containing food.
Fewer sites inspected indicate better memory performance. A color version of a one-trial associative learning task was used to investigate
possible motivational differences between corticosterone- and placebo-implanted chickadees.

unpredictable food supply) moderate corticosterone

elevation, similar to the elevation observed in
chickadees maintained on unpredictable food
schedule, had no detectable effect on hippocampal
structure and cell proliferation rates. It has also been
reported that prolonged stress and associated
prolonged corticosterone elevation result in reduced
neurogenesis rates (Gould and Tanapat 1999).
Neurogenesis consists of cell proliferation and
neuron survival (Prickaerts et al. 2004; Chapter 2)
and thus it remains possible that even moderately
elevated corticosterone levels might negatively
impact neuron survival rates.
Experimental results with mountain chickadees
thus suggest that relatively long-term, moderate
corticosterone elevations in response to challenging
environmental conditions might be adaptive, at
least in wintering food-caching birds. When for-
aging conditions deteriorate, corticosterone levels
might rise, facilitating more active foraging behav-
ior and more food caching while enhancing spatial
memory which is important for successful cache
retrieval. When environmental conditions improve,
corticosterone levels return to normal suggesting
that corticosterone elevation has some costs, which
might be outweighed by the benefits during ener-
getically demanding periods.
3.4.1 Corticosterone in Alaskan and Colorado
chickadees
Black-capped chickadees in Alaska regularly experi-
ence more energetically challenging environmen-
tal conditions than chickadees in Colorado
(Pravosudov and Clayton 2002). Such conditions
are likely to effect availability and predictability of
food supply during the winter, and limited food
supply is known to affect corticosterone levels
in mountain chickadees (Pravosudov 2003).
Moderately elevated corticosterone appears to pro-
vide benefits to wintering birds by mediating more
intense foraging and food caching and by enhan-
cing spatial memory, which plays an important
role in cache retrieval (Pravosudov 2003). Whereas
it appears that even moderately elevated cortico-
sterone levels might carry some costs (Wingfield
et al. 1997, 1998), for birds experiencing energet-
ically demanding environments every year the
benefits of elevated corticosterone might outweigh
possible costs and thus selection may favor
elevated corticosterone.
There were, however, no significant differences
in either baseline or stress-induced corticosterone
levels between Alaskan and Colorado chickadees,
which indicates that differences in memory found

between these two populations were not related to
changes in corticosterone levels (Pravosudov et al.
2004). The fact that Alaskan and Colorado chicka-
dees did not differ in their corticosterone levels in
identical laboratory conditions also suggests that
different environmental conditions did not cause
permanently elevated corticosterone levels in
Alaskan birds. Instead, it appears that baseline cor-
ticosterone levels might only respond to immediate
environmental conditions in both populations.
Compared to birds in Colorado, corticosterone
levels in Alaskan environments may be elevated in
black-capped chickadees as a result of differences
in immediate conditions between Alaska and
Colorado during the winter. Such elevation (if it
exists) may aid spatial memory benefits already
achieved through enlarged hippocampus
(Pravosudov and Clayton 2002). Whereas the vol-
ume of the hippocampus and its number of neu-
rons appear to be permanently larger in Alaskan
chickadees, providing them with permanent
advantages when it comes to spatial memory per-
formance, temporary corticosterone elevations dur-
ing the most difficult times may provide additional
memory benefits (Pravosudov 2004).
3.5 Dominance, corticosterone, spatial
memory, and the hippocampus
Most Parids live in hierarchically structured social
groups in which dominants enjoy priority of access
to all available resources (Ekman 1989; Ekman and
Lilliendahl 1993; Chapter 9). It has been suggested
that subordinates experience less predictable condi-
tions because of their low social status; even when
they find food they can be supplanted by domin-
ants at any time (Ekman and Lilliendahl 1993).
Because social classes differ in the predictability of
their environment they might invoke different tac-
tics for managing their available energy resources.
In particular, it has been suggested that birds in less
predictable environments should accumulate and
maintain more energy reserves as a buffer against
the higher probability of starvation in case an ade-
quate amount of food cannot be obtained at a cri-
tical time (Ekman and Lilliendahl 1993; Brodin et al.
2001; Chapter 17). Indeed, there is some experi-
mental evidence that subordinate birds maintain
THE HIPPOCAMPUS IN CHICKADEES 35
higher levels of fat reserves than dominants
(Ekman and Lilliendahl 1993willow tits; Chapter
9black-capped chickadees), but other studies
found either a reverse pattern (Koivula et al. 1995
willow tits; Verhulst and Hogstad 1996willow
tits; Pravosudov and Lucas 2000Carolina chick-
adees) or no differences between dominants and
subordinates (Pravosudov and Lucas 2000
Carolina chickadees).
In addition to storing energy reserves as body fat,
food-caching birds can also accumulate and main-
tain energy reserves as food caches. Birds usually
increase their caching rates when food becomes less
predictable (Pravosudov and Grubb 1997), thus the
idea that subordinates should maintain more
energy reserves to buffer unpredictable conditions
could be extended to food caching. Brodin et al.
(2001) used a dynamic modeling approach to inves-
tigate the effect of social status on food-caching rates
and their model confirmed this prediction and sug-
gested that subordinates should cache more food
than dominants. The model, however, relied heavily
on the untested assumption that dominants can
freely pilfer caches made by subordinates whereas
subordinates could never pilfer dominants caches,
and it is not clear how the models predictions
would have changed if this assumption were
changed. Empirical results were also not consistent;
some studies of willow tits found that subordinates
indeed cache more food than dominants (Lahti and
Rytkonen 1996; Brodin and Lundborg 2003b),
whereas other studies found either the reverse to be
true or no differences between low and high social
ranks (Pravosudov 1985Siberian and willow tits;
Hitchcock and Sherry 1995black-capped chicka-
dees; Lahti et al. 1998willow tits; Pravosudov and
Lucas 2000Carolina chickadees; Lundborg and
Brodin 2003willow tits).
Most of the studies investigating the effect of
dominance hierarchy on food-caching behavior
used behavioral and ecological approaches while
ignoring possible mechanisms of food-caching
regulation. For example, unpredictable food trig-
gers more intense food caching (Hurly 1992
marsh tits; Pravosudov and Grubb 1997btufted
titmice) and at the same time it also triggers
corticosterone elevation (Pravosudov et al. 2001
mountain chickadees). An implant study with
36 B E H AV I O R A N D E V O L U T I O N
mountain chickadees (Pravosudov 2004) showed
that elevated corticosterone facilitates more eating,
more intense food caching, and enhanced spatial
memory. Thus, corticosterone might be a mechanis-
tic link between unpredictable foraging conditions
and energy management tactics. If socially subor-
dinate individuals experience an unpredictable
environment their corticosterone levels might be
elevated, which would support the idea that subor-
dinates should cache more food and even have bet-
ter memory for food caches. Available data on the
relationship between dominance status and cortico-
sterone levels from observational unmanipulated
studies, however, do not show a consistent pattern
(see Pravosudov et al. 2004 for review). In some
studies corticosterone levels were higher in subor-
dinate individuals whereas in other studies there
were no differences in baseline corticosterone levels
between dominants and subordinates.
To test the hypothesis that dominance hierarchy
has an effect on food caching and spatial memory,
Pravosudov et al. (2004) compared experimentally
created pairs of dominant and subordinate moun-
tain chickadees. Previous laboratory studies investi-
gating the effect of social dominance on food
caching failed to find significant differences
between dominants and subordinates (Pravosudov
and Lucas 2000; Lundborg and Brodin 2003).
However, in all of these studies, dominants and sub-
ordinates were tested together in a fairly small room
in which subordinates could not escape the dom-
inants view. Thus it is likely that the immediate
presence of dominants might have influenced the
behavior of subordinates in these studies. In natural
conditions, subordinates can easily move out of the
dominants sight, and, in fact, most birds avoid
caching when in a presence of a group mate
(Woodrey 1991; Lahti et al. 1998). Pravosudov et al.
(2004) attempted to simulate a more natural envir-
onment by testing dominants and subordinates
separately in an adjacent room. In this experimental
design, subordinates were not affected by the pres-
ence of the dominants during the short duration of
the food-caching trials. Results of this study were
directly opposite to all predictions; subordinates
cached significantly less food than dominants and
they also performed significantly worse in a cache
recovery task (Fig. 3.5). Baseline corticosterone
levels measured after almost 2 months following
formation of dominance relationships were
statistically indistinguishable between dominants
and subordinates but maximum corticosterone
levels achieved during a standardized stress
response were actually higher in dominants
(Pravosudov et al. 2004). These results suggest that
whereas corticosterone might be involved in
mediating food-caching behavior and spatial
memory, changes in caching rates and memory can
occur without changes in baseline corticosterone
levels. The inferior spatial memory found in
subordinate chickadees was not related to any
changes in hippocampal volume or neuron
numbers (Pravosudov and Omanska 2005b).
Barnea and Nottebohm (1994) suggested that
spatial memory might be affected by changes in hip-
pocampal neuron recruitment rates without changes
in the total number of neurons. Interestingly, subor-
dinate mountain chickadees which showed inferior
spatial memory performance compared to their
dominant group mates also had significantly lower
cell proliferation rates in the ventricular zone
adjacent to both the hippocampus and to the
mesopallium (Fig. 3.6; Pravosudov and Omanska
2005b). Cell proliferation is a first step during the
process of neurogenesis; after new cells are born,
some of them will survive to become functional
neurons and it is likely that the number of functional
neurons is proportional to the number of new cells
(Prickaerts et al. 2004). Pravosudov and Omanska
(2005b) showed that differences in spatial memory
performance were associated with differences in hip-
pocampal cell proliferation rates, thus suggesting
that cell proliferation and neurogenesis might be
involved in spatial memory function (Fig. 3.6b).
These data, however, are correlational and they do
not establish a causal effect; it remains possible that
social dominance simultaneously affected both
memory and cell proliferation. In another study, hip-
pocampal cell proliferation rates did not correlate
with spatial memory performance (Pravosudov and
Omanska 2005a), suggesting that elevated cortico-
sterone might affect memory function without
changes in hippocampal cell proliferation rates.
Irrespective of whether hippocampal cell prolif-
eration is directly involved in spatial memory
function, the results of the mountain chickadees
 THE HIPPOCAMPUS IN CHICKADEES 37

(a) (b)
Dominants
12 Dominants Subordinates
8
Subordinates

Mean number of sites inspected

10
6
Number of nuts

6 4

4
2
2

0 0
Cache Eat All caches All caches First cache First two
Unlimited Limited caches
caching caching

Figure 3.5 Mean number of consumed (fully or partially) and cached pine nuts during food-caching trials (a) and memory performance (b) in a
cache-recovery task in dominant (black bars) and subordinate (hatched bars) mountain chickadees. (Reprinted from Hormones and Behavior,
44, Pravosudov et al. The relationship between dominance, corticosterone, memory, and food caching in mountain chickadees (Poecile gambeli),
pp. 93102, Copyright (2003), with permission from Elsevier.)

(a) (b)
14

12
Number of BrdU-labeled cells

*
Number of sites inspected

600
10

8
400
6
*
4
200
2

0 0
HP 0 100 200 300 400 500 600 700 800
M
Number of BrdU-labeled cells

Figure 3.6 Mean number of BrdU-labeled cells in the ventricular zone adjacent to either hippocampus or mesopallium (a) and the relationship
between the number of BrdU-labeled cells in the ventricular zone adjacent to the hippocampus rates and spatial memory performance (b) in dominant
(black bars and circles) and subordinate (hatched bars and open circles) mountain chickadees (redrawn from Pravosudov and Omanska 2005b).

study suggest additional costs of subordination dominants and subordinates did not differ signifi-
subordinate chickadees might cache less food and cantly in the total number of hippocampal neurons
might show inferior spatial memory performance (Pravosudov and Omanska 2005b). It is possible
as a result of their low social status. Stress of social that neuron turnover rates are higher in dominants
subordination is also a likely factor suppressing and that is why they do not have more neurons,
hippocampal cell proliferation rates, although despite the fact that more new cells are being born
38 B E H AV I O R A N D E V O L U T I O N
in the ventricular zone. Lower caching rates and
less efficient cache retrieval as a result of inferior
spatial memory could potentially contribute to
the higher mortality of subordinates commonly
reported in literature.
3.6 Conclusions
Research on spatial memory in Parids has shown
that environmental conditions might affect mem-
ory performance through several different ways:
1. Temporary, season-like changes in spatial mem-
ory associated with variation in food availability and
predictability were related to changes in baseline
corticosterone levels whereas hippocampal volume
and neuron numbers appeared to remain stable.
2. In birds permanently living in higher latitudes
with harsher conditions, on the other hand,
enhanced memory was related to larger hippocam-
pal volume and more neurons in the absence of any
variation in corticosterone levels.
3. Changes in spatial memory associated with
social dominance were unrelated to either cortico-
sterone levels or to the hippocampal volume or
neuron numbers, but they were associated with
variance in hippocampal cell proliferation rates.
It is likely that all three of these patterns could be
involved the in regulation of spatial memory, sep-
arately or jointly. Elevated corticosterone levels
could provide yet another enhancement to spatial
memory in chickadees occupying northern parts of
their range, with less predictable conditions, in
addition to enhancements achieved via an enlarged
hippocampus with more neurons. Changes in hip-
pocampal structure (volume and neuron numbers),
however, are not necessary to induce changes in
spatial memory in food-caching birds.
Acknowledgements
I would like to thank Nicky Clayton, Sasha
Kitaysky, Alicja Omanska, and Pierre Lavenex who
collaborated with me on my studies of memory,
hormones, and the hippocampus in chickadees. My
research has been supported by NIH. Comments
from Ken Otter, David Sherry, and Laurene
Ratcliffe greatly improved the manuscript.
References
Barnea, A. and Nottebohm, F. (1994). Seasonal recruitment
of hippocampal neurons in adult free-ranging black-
capped chickadees. Proceedings of the National Academy
of Sciences, 91, 1121711221.
Biegler, R., McGregor, A., Krebs, J. R., and Healy, S. D.
(2001). A larger hippocampus is associated with longer-
lasting spatial memory. Proceedings of the National
Academy of Sciences, 98, 69416944.
Breuner, C. W., Greenberg, A. L., and Wingfield, J. C.
(1998). Noninvasive corticosterone treatment rapidly
increases activity in Gambels white-crowned sparrows
(Zonotrichia leucophrys gambelii). General and Comparative
Endocrinology, 111, 386394.
Brodin, A. (1994). The role of naturally stored food sup-
plies in the winter diet of the boreal willow tit Parus
montanus. Ornis Svecica, 4, 3140.
Brodin, A. (2005). Hippocampal volume does not correlate
with food-hoarding rates in the black-capped chickadee
(Poecile atricapillus) and willow tits (Parus montanus).
Auk, 122, 819828.
Brodin, A. and Lundborg, K. (2003a). Is hippocampal vol-
ume affected by specialization for food hoarding in
birds? Proceedings of the Royal Society B, 270, 15551563.
Brodin, A. and Lundborg, K. (2003b). Rank-dependent
hoarding effort in willow tits (Parus montanus): a test of
theoretical predictions. Behavioral Ecology and
Sociobiology, 54, 587592.
Brodin, A., Lundborg, K., and Clark, C. W. (2001). The
effect of dominance on food hoarding: a game theoret-
ical model. American Naturalist, 157, 6675.
Clayton, N. S. (2001). Hippocampal growth and mainten-
ance depend on food-caching experience in juvenile
mountain chickadees (Poecile gambeli). Behavioral
Neuroscience, 115, 614625.
Clayton, N. S. and Cristol, D. A. (1996). Effects of photo-
period on memory and food storing in captive marsh
tits, Parus palustris. Animal Behaviour, 52, 715726.
Diamond, D. M., Bennett, M. C., Fleshner, M. and
Rose, G. M. (1992). Inverted-U relationship between the
level of peripheral corticosterone and the magnitude of
hippocampal primed burst potentiation. Hippocampus, 2,
421430.
Ekman, J. (1989). Ecology of non-breeding social systems
of Parus. Wilson Bulletin, 101, 263288.
Ekman, J. B. and Lilliendahl, K. (1993). Using priority to
food access: fattening strategies in dominance-structured
willow tit (Parus montanus) flocks. Behavioral Ecology, 4,
232238.
Garamszegi, L. Z. and Lucas, J. R. (2005). Continental
variation in relative hippocampal volume in birds: the

phylogenetic extent of the effect and the potential
role of winter temperatures. Biology Letters, 1, 330333.
Gould, E. and Tanapat, P. (1999). Stress and hippocampal
neurogenesis. Biological Psychiatry, 46, 14721479.
Haftorn, S. (1956). Contribution to the food biology of tits,
especially about storing of surplus food: Part IV. A
comparative analysis of Parus atricapillus L., P. cristatus,
L., and P. ater L. Det Kgl Norske Videnskabers Selskabs
Skrifter, 4, 154.
Hampton, R. R. and Sherry, D. F. (1992). Food storing by
Mexican chickadees and bridled titmice. Auk, 109,
665666.
Hampton, R. P., Sherry, D. F., Shettleworth, S. J., Khurgel,
M., and Ivy, G. (1995). Hippocampal volume and food-
storing behavior are related in Parids. Brain Behavior and
Evolution, 4, 5461.
Hampton, R. R. and Shettleworth, S. J. (1996a).
Hippocampal lesions impair memory for location but
not color in passerine birds. Behavioral Neuroscience, 110,
831835.
Hampton, R. R. and Shettleworth, S. J. (1996b).
Hippocampus and memory in a food-storing and in a
nonstoring bird species. Behavioral Neuroscience, 110,
946964.
Harrap, S. and Quinn, D. (1995). Chickadees, Tits,
Nuthatches and Treecreepers. Princeton University Press,
Princeton, NJ.
Healy, S. D. and Krebs, J. R. (1996). Food storing and the
hippocampus in Paridae. Brain Behavior and Evolution,
47, 195199.
Hitchcock, C. L. and Sherry, D. F. (1995). Cache pilfering
and its prevention in pairs of black-capped chickadees.
Journal of Avian Biology, 26, 187192.
Hoshooley, J. S. and Sherry, D. F. (2004). Neuron produc-
tion, neuron number, and structure size are seasonally
stable in the hippocampus of the food-storing black-
capped chickadee (Poecile atricapillus). Behavioral
Neuroscience 118, 345355.
Hurly, T. A. (1992). Energetic reserves of marsh tits (Parus
palustris): food and fat storage in response to variable
food supply. Behavioral Ecology, 3, 181188.
Karpouzos, H., Hernandez, A. M., MacDougall-
Shackleton, E. A., and MacDougall-Shackleton, S. A.
(2005). Effects of day-length and food availability on
food caching, mass and fat reserves in black-capped
chickadees (Poecile atricapillus). Physiology and Behavior,
84, 465469.
Koivula, K., Orell, M., Rytkonen, S., and Lahti, K. (1995).
Fatness, sex and dominance: seasonal and daily body
mass changes in willow tits. Journal of Avian Biology, 26,
209216.
Krebs, J. R., Clayton, N. S., Hampton, R. R., and
Shettleworth S. J. (1995). Effects of photoperiod on food
THE HIPPOCAMPUS IN CHICKADEES 39
storing and the hippocampus in birds. Neuro Report, 6,
17011704.
Krebs, J. R., Clayton, N. S., Healy, S. D., Cristol, D. A.,
Patel, S. N., and Jolliffe, A. R. (1996). The ecology of the
avian brain: food-storing memory and the hippocam-
pus. Ibis, 138, 3446.
Krebs, J. R., Sherry, D. F., Healy, S. D., Perry, V. H., and
Vaccarino, A. L. (1989). Hippocampal specialization of
food-storing birds. Proceedings of the National Academy of
Sciences, 86, 13881392.
Lahti, K. and Rytkonen, S. (1996). Presence of conspecifics,
time of day age affect willow tits hoarding. Animal
Behaviour, 52, 631636.
Lahti, K, Koivula, K., Rytkonen, S., Mustonen, T., Welling,
P., Pravosudov, V. V., and Orell, M. (1998). Social influ-
ences on food caching in willow tits: a field experiment.
Behavioral Ecology, 9, 122129.
Loscertales, M., Rose, S. P. R., and Sandi, C. (1997). The
corticosteroid synthesis inhibitors metyrapone and
aminoglutethimide impair long-term memory for a
passive avoidance task in day-old chicks. Brain Research,
769, 357361.
Lucas, J. R., Brodin, A., de Kort, S. R., and Clayton, N. S.
(2004). Does hippocampal size correlate with the degree
of caching specialization? Proceedings of the Royal Society
B, 271, 24232429.
Lundborg, K. and Brodin, A. (2003). The effect of dom-
inance rank on fat deposition and food hoarding in the
willow tit Parus montanusan experimental test. Ibis,
145, 7882.
MacDougall-Shackleton, S. A., Sherry, D. F., Clark, A. P.,
Pinkus, R., and Hernandez, A. M. (2003). Photoperiodic
regulation of food storing and the hippocampus vol-
ume in black-capped chickadees, Poecile atricapillus.
Animal Behaviour, 65, 805812.
McEwen, B. S. (2000). The neurobiology of stress: from
serendipity to clinical relevance. Brain Research, 886,
172189.
McEwen, B. S. and Sapolsky, R. M. (1995). Stress and cogni-
tive function. Current Opinions in Neurobiology, 5, 205216.
Odum, E. P. (1942). Annual cycle of the black-capped
chickadee 3. Auk, 59, 499531.
Pravosudov, V. V. (1985). Search for and storage of food by
Parus cinctus lapponicus and P. montanus borealis.
Zoologicheskiy Zhurnal, 64, 10361043 [in Russian].
Pravosudov, V. V. (2003). Long-term moderate elevation in
corticosterone facilitates avian food caching behavior
and enhances spatial memory. Proceedings of the Royal
Society B, 270, 25992604.
Pravosudov, V. V. (2005). Corticosterone and memory in
birds. In: Dawson, A. and Sharp, P. J. eds. Functional
Avian Endocrinology, pp. 257268. Narosa Publishing
House, New Delhi, India.
40 B E H AV I O R A N D E V O L U T I O N
Pravosudov, V. V. (2006). On seasonality in food caching
behavior in parids: do we know the whole story?
Animal Behaviour, 71, 14551460.
Pravosudov, V. V. and Clayton, N. S. (2001). Effects of
demanding foraging conditions on cache retrieval
accuracy in food caching mountain chickadees (Poecile
gambeli). Proceedings of the Royal Society B, 268, 363368.
Pravosudov, V. V. and Clayton, N. S. (2002). A test of the
adaptive specialization hypothesis: population differ-
ences in caching, memory and the hippocampus in
black-capped chickadees (Poecile atricapilla). Behavioral
Neuroscience, 116, 515522.
Pravosudov, V. V. and de Kort, S. R. (2006). Is the western
scrub-jay (Aphelocoma californica) really an underdog
among food-caching corvids when it comes to hip-
pocampal volume and food caching propensity? Brain,
Behavior and Evolution, 67, 19.
Pravosudov, V. V. and Grubb, T. C., Jr (1997a). Energy
management in passerine birds during the non-breed-
ing season: a review. Current Ornithology, 14, 189234.
Pravosudov, V. V. and Grubb, T. C., Jr (1997b).
Management of fat reserves and food caches in tufted
titmice (Parus bicolor) in relation to unpredictable food
supply. Behavioral Ecology, 8, 332339.
Pravosudov, V. V. and Lucas, J. R. (2000). The effect of
social dominance on fattening and food-caching behav-
ior in Carolina chickadees, Poecile carolinensis. Animal
Behaviour, 60, 483493.
Pravosudov, V. V. and Lucas, J. R. (2001). A dynamic
model of short-term energy management in small food-
caching and non-caching birds. Behavioral Ecology, 123,
324331.
Pravosudov, V. V. and Omanska, A. (2005a). Prolonged
moderate elevation of corticosterone does not affect
hippocampal anatomy or cell proliferation rates in
mountain chickadees (Poecile gambeli). Journal of
Neurobiology, 62, 8291.
Pravosudov, V. V. and Omanska, A. (2005b). Dominance-
related changes in spatial memory are associated
with changes in hippocampal cell proliferation rates
in mountain chickadees. Journal of Neurobiology, 62,
3141.
Pravosudov, V. V., Kitaysky, A. S., Saldanha, C., Wingfield,
J. C., and Clayton, N. C. (2002a). The effect of photo-
period on adrenocortical stress response in mountain
chickadees (Poecile gambeli). General and Comparative
Endocrinology, 126, 242248.
Pravosudov, V. V., Kitaysky, A. S., Wingfield, J. C., and
Clayton, N. S. (2004). No latitudinal differences in
adrenocortical stress response in wintering black-
capped chickadees (Poecile atricapilla). Comparative
Biochemistry and Physiology A, 137, 95103.
Pravosudov, V. V., Kitaysky, A. S., Wingfield, J. C., and
Clayton, N. S. (2001). Long-term unpredictable foraging
conditions and physiological stress response in moun-
tain chickadees (Poecile gambeli). General and Comparative
Endocrinology, 123, 324331.
Pravosudov, V. V., Lavenex, P., and Clayton, N. S. (2002b).
Changes in spatial memory mediated by experimental
variation in food supply. Journal of Neurobiology, 51,
142148.
Pravosudov, V. V., Mendoza, S. P., and Clayton, N. S.
(2003). The relationship between dominance, cortico-
sterone, memory and food caching in mountain chicka-
dees (Poecile gambeli). Hormones and Behavior, 44, 93102.
Prickaerts, J., Koopmans, G., Blockland, A., and Scheepens,
A. (2004). Learning and adult neurogenesis: survival
with or without proliferation? Neurobiology of Learning
and Memory, 81, 111.
Reneerkens, J., Piersma, T., and Ramenofsky, M. (2002).
An experimental test of the relationship between tem-
poral variability of feeding opportunities and baseline
levels of corticosterone in a shorebird. Journal of
Experimental Zoology, 293, 8188.
Saldanha, C. J., Schlinger, B. A., and Clayton, N. C. (2000).
Rapid effects of corticosterone on cache recovery in
mountain chickadees (Parus gambeli). Hormones and
Behavior, 37, 109115.
Sandi, C., and Rose, S. P. R. (1997). Training-dependent
biphasic effects of corticosterone in memory formation for
a passive avoidance task in chicks. Psychopharmacology,
133, 152160.
Sandi, C., Rose, S. P. R., Mileusnic, R., and Lancashire, C.
(1995). Corticosterone facilitates long-term memory
formation via enhanced glycoprotein synthesis.
Neuroscience, 4, 10871093.
Sapolsky, R. M. (1996). Why stress is bad for your brain.
Science, 273, 749750.
Sherry, D. F. and Vaccarino, A. L. (1989). Hippocampus
and memory for food caches in black-capped chicka-
dees. Behavioral Neuroscience, 103, 308318.
Sherry, D. F., Vaccarino, A. L., Buckenham, K., and Herz,
R. S. (1989). The hippocampal complex of food-storing
birds. Brain Behavior and Evolution, 34, 308317.
Shettleworth, S. J. (1995). Memory in food-storing birds:
from the field to the Skinner box. In: Alleva, E., Fasolo,
A., Lipp, H. P., Nadel, L., and Ricceri, L., eds. Behavioral
Brain Research in Naturalistic and Semi-naturalistic
Settings, pp. 158179. Kluwer, the Hague, the
Netherlands.
Shettleworth, S. J., Hampton, R. R., and Westwood, R. P.
(1995). Effects of season and photoperiod on food-
storing by black-capped chickadees, Parus atricapillus.
Animal Behaviour, 49, 989998.

Shiflett, M. W., Smulders, T. V., Benedict, L., and DeVoogd,
T. J. (2003). Reversible inactivation of the hippocampal
formation in food-storing black-capped chickadees
(Poecile atricapillus). Hippocampus, 13, 437444.
Shiflett, M. W., Tomaszycki, M. L., Rankin, A. Z., and
DeVoogd, T. J. (2004). Long-term memory for spatial loca-
tions in a food-storing bird (Poecile atricapilla) requires
activation of NMDA receptors in the hippocampal forma-
tion during learning. Behavioral Neuroscience, 118, 121130.
Silverin, B. (1998). Stress responses in birds. Poultry and
Avian Biology Review, 9, 153168.
Smulders, T. V. and Dhondt, A. (1997). How much memory
do tits need? Trends in Ecology and Evolution, 12, 417418.
Smulders, T. V., Sasson, A. D., and DeVoogd, T. J. (1995).
Seasonal variation in hippocampal volume in a food-
storing bird, the black-capped chickadee. Journal of
Neurobiology, 27, 1525.
Smulders, T. V., Shiflett, M. W., Sperling, A. J., and
DeVoogd, T. J. (2000). Seasonal changes in neuron
THE HIPPOCAMPUS IN CHICKADEES 41
numbers in the hippocampal formation of a food-
hoarding bird: the black-capped chickadee. Journal of
Neurobiology, 44, 414422.
Verhulst, S. and Hogstad, O. (1996). Social dominance and
energy reserves in flocks of willow tits. Journal of Avian
Biology, 27, 203208.
Wingfield, J. C., Breuner, C., and Jacobs, J. (1997).
Corticosterone and behavioral responses to unpre-
dictable events. In: Harvey, S. and Etches, R. J., eds.
Perspectives in Avian Endocrinology, pp. 267278. Journal
of Endocrinology Ltd., Bristol, UK.
Wingfield, J. C., Maney, D. L., Breuner, C. W., Jacobs, J. D.,
Lynn, S., Ramenofsky, M., and Richardson, R. D. (1998).
Ecological bases of hormone-behavior interactions: the
emergency life history stage. American Zoologist, 38,
191206.
Woodrey, M. S. (1991). Caching behavior in free-ranging
white-breasted nuthatches: the effect of social dom-
inance. Ornis Scandinavica, 22, 160166.
This page intentionally left blank
 CHAPTER 4
Photoperiodism and the annual
cycle of black-capped chickadees
Leslie S. Phillmore and Scott A. MacDougall-Shackleton
4.1 Introduction
4.1.1 Seasonality
Virtually all parts of the planet exhibit seasonal
changes in climate. Some times of the year are more
favorable to survival of young than others, and
organisms have thus been selected to produce young
during those seasons when the offspring are most
likely to survive. Baker (1938) noted that the envir-
onmental factors that actually influence offspring
survival may differ from the environmental factors
that animals actually use to time reproduction. He
identified ultimate factors as those that influence
offspring survival; for seasonally breeding birds this
is typically food supply. In contrast, proximate envir-
onmental cues are what animals actually respond to
in order to time seasonal changes in reproductive
physiology and behavior. In some cases, such as
food availability, ultimate and proximate factors
may be one and the same. However, animals often
time reproduction in response to proximate cues that
are very different from the ultimate factors that actu-
ally determine reproductive success. In seasonally
breeding birds the primary proximate cue typically
used to time breeding and migration is the annual
change in photoperiod (Dawson et al. 2001).
Although a variety of environmental cues may be
used to fine tune the timing of reproductive effort
(Chapter 5), photoperiod seems to be the primary,
initial predictive cue used by seasonally breeding
birds. Other cues tend to modify the main physio-
logical response driven by photoperiod.
Reproduction has been the most extensively stud-
ied seasonally changing behavior in birds; however,
many other aspects of behavior and physiology also
change seasonally. These include geographic move-
ments such as the vernal and autumnal migrations,
and dispersal from natal territories. In addition,
some birds change habitat-use seasonally and may
also alternate between exclusive and non-exclusive
use of territories. Many aspects of energy balance
change seasonally including diet, food-storing, and
fat deposition. Feather molt is timed to occur when
the costs to reproduction and flight are minimized.
Social behavior, such as aggression and vocaliza-
tions, may vary over the annual cycle. In many cases
we know much less about the proximate environ-
mental factors that drive seasonal changes in behav-
ior other than reproduction.
Black-capped chickadees (along with many other
Parids) represent ideal species for the study of
seasonal changes in physiology, neurobiology, and
behavior. This species is resident year-round in an
extremely seasonal environment. Despite this, we
know relatively little about which proximate envir-
onmental cues black-capped chickadees use to
time neural and physiological changes, and the
subsequent changes in behavior. More information
is available through detailed and extensive studies
of photoperiodism in European species of titmice,
such as great tits (Silverin 1994). However, for
the Paridae as a whole we know relatively little
about photoperiodismespecially in comparison
to species such as white-crowned sparrows
(Zonotrichia leucophrys) and European starlings
(Sturnus vulgaris; see Dawson et al. 2001 for review).
In this chapter we will review photoperiodism and
seasonality in Parids focusing on recent studies of
43
44 B E H AV I O R A N D E V O L U T I O N
black-capped chickadees. These studies include the
effects of photoperiod on reproduction, on singing
and the neural system controlling song, and on
food-storing and the hippocampus. We first begin
with a general review of photoperiodism.
4.1.2 Photoperiodism and seasonal
reproduction
Since the pioneering studies by Rowan (1925), we
have known that the seasonal change in day length
has profound effects on avian physiology and
behavior. Extensive study of species such as
European starlings and white-crowned sparrows
have yielded a detailed model of how the annual
photocycle drives seasonal changes in reproduction
of seasonally breeding songbirds in particular
(Nicholls et al. 1988; Dawson et al. 2001; Dawson
2002), that we briefly review here.
In winter and early spring when day length
is short, birds are in a photosensitive physiological
state: gonad size is small, reproductive hormone
levels are low, and birds are not in breeding
condition. However, birds are ready to respond
to increases in day length that occur during spring.
Once length of day exceeds a critical threshold,
birds become photostimulated: gonadotropic
hormones (luteinizing hormone and follicle stimu-
lating hormone) are released and stimulate
recrudescence of the gonads and subsequent
release of sex steroid hormones and reproductive
behavior ensues (Dawson et al. 2001). Prolonged
exposure to long days induces photorefractoriness
such that birds are no longer stimulated by the
previously stimulatory long days: gonads regress
and the feathers molt (Nicholls et al. 1988). In some
species, photorefractoriness occurs quite early
in the summer and may even precede the summer
solstice. In songbirds, this state of photorefractori-
ness is typically absolute and at this time exposure
to very long days (even 24 h light) is ineffective
in inducing reproductive competence (Hamner
1968; Nicholls et al. 1988). Usually, exposure to
short-days is required to break photorefractoriness
and reinstate photosensitivity (Nicholls et al. 1988).
Thus, the annual cycle of reproduction in songbirds
is driven by a changing sensitivity to long-days
as birds alternate through the physiological
conditions of photosensitivity, photostimulation,
and photorefractoriness.
Variation between species in reproductive sched-
ule is due, in part, to variation between species in
photoperiodic responses. For example, the length
of day required to induce photostimulation and
the duration of long-day exposure required to
induce photorefractoriness are two variables that
could give rise to a variety of breeding schedules
(Hahn et al. 1997). Another form of interspecies
variation is in the nature of photorefractoriness.
Photorefractoriness in many songbirds is absolute;
Japanese quail (coturnix japonica), however, instead
become relatively photorefractory (Robinson and
Follett 1982). Normally, these quail do not undergo
gonadal regression until day length declines, and
they can be restimulated by returning them to very
long days at any time; no prolonged exposure to
short days is required to dissipate relative refrac-
toriness (Nicholls et al. 1988).
In addition to the distinction between absolute
and relative refractoriness, recent studies of
Cardueline finches suggest that bird species may
vary in whether gonads spontaneously regress
when held on constant long days and whether
birds are completely insensitive to very long days
(24 h light) when photorefractory (MacDougall-
Shackleton et al. 2005). Crossbills (Loxia species), for
example, may never become absolutely photo-
refractory. These opportunistically breeding song-
birds can breed at almost any time of year, but
exhibit an autumnal decrease in breeding that may
be due to a form of relative photorefractoriness
(Hahn 1995). Crossbills do not appear to regress
gonads when held on long days for many months
(Hahn 1995) and are responsive to very long
days even when the gonads are regressed in
autumn (MacDougall-Shackleton et al. 2005). There
is likely greater variation among species in photo-
periodism than previously supposed. Thus, for any
given species, experimental studies are required
before seasonal variation in behavior can be attrib-
uted to the standard photoperiodism model.
4.1.3 Seasonal neural plasticity
In addition to seasonal changes in peripheral physi-
ology and behavior, birds also exhibit remarkable

seasonal brain plasticity (Tramontin and Brenowitz
2000). There is good evidence that the entire brain
may exhibit seasonal morphological changes
(Smulders 2002). Most research on birds, however,
has focused on seasonal plasticity in three neural
systems: the gonadotropin-releasing hormone
(GnRH) system, the song-control system, and the
hippocampus.
GnRH is a hypothalamic neuropeptide that stimu-
lates release of gonadotropins from the pituitary
and thereby regulates the entire reproductive axis.
In a large number of seasonally breeding songbirds,
GnRH is dramatically down-regulated when birds
are photorefractory (Ball and Hahn 1997). Although
this down-regulation in and of itself does not cause
photorefractoriness (Dawson et al. 2001), it may
preclude physiological responses to stimulatory
environmental cues. In species that do not become
absolutely photorefractory GnRH plasticity is
absent or much reduced (Ball and Hahn 1997).
Research on GnRH in Parids is minimal (see Silverin
1994) and whether or not chickadees exhibit
seasonal fluctuations in GnRH remains unknown.
Songbirds possess a circuit of specialized brain
regions that control the learning and production of
song, called the song-control system. Regions
within this network, such as HVC, exhibit the most
extreme seasonal plasticity documented among
vertebrates (Tramontin and Brenowitz 2000). In
HVC, this extreme plasticity involves the incorp-
oration of tens of thousands of new neurons on an
annual basis and the volume of this region may
almost double in many species (Tramontin and
Brenowitz 2000). Seasonal changes in HVC typic-
ally track changes in reproduction; HVC tends to
be largest in the spring when birds are singing
most. However, the vernal increase in HVC size is
rapid and may precede reproduction (Caro et al.
2005). Seasonal plasticity of the song-control system
appears primarily to be regulated by seasonal
changes in gonadal steroid hormones (Brenowitz
2004); however, gonad-independent effects have
been reported as well (Ball et al. 2004). Other
hormones or singing behavior itself may also
contribute to seasonal plasticity of the song system
(reviewed in Ball et al. 2004).
Though less studied than the song system, sea-
sonal changes have also been reported for the avian
P H OTO P E R I O D I S M A N D T H E A N N UA L C Y C L E 45
hippocampus, including changes in volume
(Smulders et al. 1995; Clayton et al. 1997) and in
neuron survival and incorporation of new neurons
(Barnea and Nottebohm 1994). Most of the work on
seasonal plasticity of the hippocampus has been
conducted on black-capped chickadees, and we
review this field further below.
4.2 Annual cycle of black-capped
chickadees
4.2.1 Overview
Across most of their range, black-capped chicka-
dees are year-round residents; that is, once adults,
individuals live in the same small geographic area
throughout the year (Smith 1991). Because of this,
much is known about this species annual cycle of
behavior (Odum 1941a, 1941b, 1942; Smith 1991)
including alternation between winter flocking and
breeding territoriality, changing prevalence of
different vocalization types (Ficken et al. 1978), and
changes in diet and food storing (Odum 1942;
Shettleworth et al. 1995). Based on field observa-
tions in southern Ontario (populations near
Kingston, Toronto, and London, Ontario, Canada)
we have compiled a diagram illustrating the modal
annual cycle of reproduction, singing, molt, and
food storing of black-capped chickadees (Fig. 4.1).
Note that parameters associated with breeding
are asymmetric with respect to the annual
photocyclea hallmark of species that become
absolutely photorefractory (Dawson et al. 2001).
In fall and winter, chickadees live in flocks of
about six to eight birds, but flocks can range from
two to 12 birds (Smith 1991). Flocks, usually, are
made up of approximately equal numbers of males
and females. A flock defends a large territory (aver-
ages about 816 hectares, from several years, popu-
lations, and sources; see Smith 1991) over which it
ranges. There is a dominance hierarchy within the
flock, with a top, or alpha male; all other males rank
in order under this male (see Chapter 9). This dom-
inance is established usually through interactions
at feeding sites. Females also form a dominance
hierarchy under an alpha female. In early spring
flocks break up and males establish and defend ter-
ritories (e.g. flock break-up by mid-April, Fort and
Otter 2004). Breeding territories are formed within
46 B E H AV I O R A N D E V O L U T I O N

Food storing ? ?

Feather molt

Gonad size
?

Eggs in nest

Dawn singing

16
14
Hous daylight 12
10
8
Month
J F M A M J J A S O N D

Figure 4.1 Annual cycle of black-capped chickadees. Hours of daylight are indicated for southern Ontario. Dark portions of horizontal
bars indicate the annual changes in dawn singing, egg-laying, gonad size, feather molt, and food storing. Data for eggs in nest,
gonad size, and feather molt are based on unpublished data collected by the authors in southern Ontario (near the cities of London,
Toronto, and Kingston) over several years. Data for dawn singing rates indicate population levels of dawn song, not individual behavior;
data on this are presented in Phillmore et al. (2006). The bar for food storing is hatched because it is based on more anecdotal reports and
observations. There is often large variation between individuals in the timing of any single variable (see text for more details). Question
marks indicate a lack of data.

the flocks home range, although these individual
territories are much smaller than the flock range
(averages about 1.5 to 5 hectares, from several
years, populations, and sources; see Smith 1991).
Pairs are usually established by rank in the flock,
with the alpha male and female forming a pair, and
the rest of the flock pairing off in order of rank. Pair
formation occurs in fall or winter with flock forma-
tion and then again in spring (Smith 1991).
Once pairs are established nest building begins,
and eggs are laid (early May), incubated, and
hatched. Once young are fledged (about 16 days
after hatch, early to mid-June, Smith 1991) they
remain with parents in a family flock until they are
old enough to disperse (about 2 to 4 weeks after
fledging, late June, early July; Fort and Otter 2004;
Smith 1991). Young rarely stay in the same immedi-
ate geographical area in which they are born. By the
end of summer and early fall, flocks are once again
beginning to form and larger flock territories and
dominance hierarchies re-established.
Although the annual cycle described above is
clearly seasonal in nature, the proximate environ-
mental cues, such as photoperiod, that drive this
cycle remain relatively unstudied. Below, we
review the evidence for the role of photoperiod in
driving changes in: (i) reproduction, (ii) singing
and the song-control centers of the brain, and (iii)
food-storing and the hippocampus.
4.3 Photoperiodism and reproduction
in black-capped chickadees
4.3.1 Comparison with other species
There are few data regarding reproductive physi-
ology and photoperiodism in black-capped chicka-
dees; however, more extensive research has been
conducted on European species of titmice. This
research, using both natural changes in photoperiod
with wild-caught birds and manipulated
photoperiods with captive birds, shows there are
indeed seasonal and photoperiod-driven fluctuations

in gonad size, circulating gonadotropic hormones,
and reproductive behaviors. For example, great tits
have seasonal fluctuations in gonad size (Silverin
1978), circulating levels of luteinizing hormone
(Silverin 1991), and follicle stimulating hormone
(Silverin et al. 1997).
Although the onset of photostimulation varies
among and within different Parus species depend-
ing on latitude (Silverin et al. 1993), extended
exposure to long days in captivity does eventually
lead to gonadal regression (Silverin et al. 1993).
Also, extensive study of great tits (Silverin 1994)
shows that these birds likely exhibit absolute
photorefractoriness in late summer. At this time
great tits spontaneously regress their gonads and
are unresponsive to very long days (although
exposure to 24 h light has not been tested). On the
whole, the data support the idea that great tits
exhibit absolute photorefractoriness similar to that
observed in other species. However, the nature of
photorefractoriness (i.e. absolute versus relative) in
other species of titmice remains unclear and may
vary among species. For example, captive marsh
tits held on long days do not appear to initiate
feather molt until they are transferred to short days
(Clayton and Cristol 1996). This suggests that
marsh tits may not become photorefractory while
held on constant long days, although molt and
gonads were not measured systematically. On the
whole, work remains to be done to determine the
nature and extent of interspecific variation in
photoperiodic responses and photorefractoriness
among species of titmice and chickadees.
4.3.2 Photoperiodism in black-capped
chickadees
While the annual cycle of black-capped chickadee
behaviors, including singing, food storing, and flock
or territory formation, are well known, the informa-
tion about photoperiodism, or physiological
response to changing day length, is limited.
Although some assumptions could be made from
studies of European species of tits (see previous sec-
tion), few direct studies of photoperiodism in black-
capped chickadees have been undertaken. Some
data regarding photoperiodism of black-capped
chickadees can be gleaned from studies of seasonal
P H OTO P E R I O D I S M A N D T H E A N N UA L C Y C L E 47
changes in brain and behavior of this species. First,
chickadees captured in spring then transferred to
long days eventually initiate feather molt, whereas
birds captured at the same time and kept on short
days long term do not (Shettleworth et al. 1995).
Chickadees captured in winter then transferred to
long days also eventually initiate molt (Shettleworth
et al. 1995). These results suggest that in late winter
and spring black-capped chickadees are photosensi-
tive and transfer to long days at this time results in
photostimulation and eventual photorefractoriness
and feather molt. More recent data indicate that
exposure of chickadees captured in winter to
constant long days leads to rapid growth of the
gonads, and continued exposure to constant long
days leads to eventual complete gonadal regression
(MacDougall-Shackleton et al. 2003b). As well,
chickadees held long term on constant short days do
exhibit some modest gonadal development, at least
in females (MacDougall-Shackleton et al. 2003b).
These studies suggest that black-capped chickadees
exhibit photoperiodism similar to other seasonally
breeding songbirds: with long days inducing both
initial photostimulation and eventual photorefrac-
toriness and molt, and long-term exposure to short
days leading to some recrudescence of gonads
(Dawson et al. 2001).
In a recent laboratory study, Phillmore et al.
(2005) tested directly whether black-capped chicka-
dees were absolutely or relatively photorefractory.
Photosensitive chickadees on a short-day photo-
period (8 h light per day) were exposed to a long-
day photoperiod (15 h light per day). They were
held on this long-day photoperiod until they
became photorefractory (as indicated by regression
of gonads and onset of moult). Birds were then
either switched to constant light (24 h light) or
maintained on the original long-day photoperiod.
If chickadees responded to the constant-light
challenge by regrowing their gonads and becoming
photostimulated, it would indicate that chickadees
were relatively photorefractory and did not require
exposure to short day photoperiods in order to
return to breeding condition (Hamner 1968).
However, in this experiment chickadees exposed to
constant light did not have larger gonads than birds
maintained on the same long-day photoperiod
(15 h light). These birds also continued to molt
48 B E H AV I O R A N D E V O L U T I O N
feathers. Therefore, evidence from Phillmore et al.
(2005) and other studies support the suggestion
that black-capped chickadees are, in fact, absolutely
photorefractory, similar to other Parids and season-
ally breeding songbirds such as European starlings.
4.4 Seasonal changes in song and
the song-control system
Chickadees produce a wide range of vocalizations
that are used in different contexts (Ficken et al.
1978). The chickadee song, called the fee-bee, is a
two-tone whistled vocalization. It is a learned
vocalization; young birds must hear adults sing fee-
bees during development in order to accurately
sing it as adults (Shackleton and Ratcliffe 1993;
Chapter 12). The fee-bee is sung primarily by males
(but females may sometimes also fee-bee, Smith
1991) and is produced most frequently during
either the dawn chorus (Horn et al. 1992; Gammon
2004) or during aggressive territorial interactions
(Shackleton and Ratcliffe 1994; Chapter 14).
The fee-bee song is most frequently heard in
spring, when birds are in breeding condition
(Ficken et al. 1978; Phillmore et al. 2006). Dawn
singing may begin in January or February, and
continue to July, but is most pronounced in the
weeks prior to hatch of the young. Other seasonally
produced vocalizations include those associated
with breeding and reproductive behavior, such as
the faint fee-bee (males and females) and variable see
(females), both heard when birds were in close
proximity to the nest (Ficken et al. 1978). By con-
trast, the chick-a-dee call, also a learned vocalization
(Hughes et al. 1998), is probably not seasonal as it is
heard year round. However, it is more prevalent in
the non-breeding season (Ficken et al. 1978). This
call is used in many contexts, for example as a mild
alarm call and to maintain flock or pair contact
(Ficken et al.1978; Chapter 13).
Brain regions such as HVC that are involved in
song learning and song production undergo large
seasonal changes in many species (Tramontin and
Brenowitz 2000). The evidence that this occurs in
black-capped chickadees is mixed. Chickadees held
in captivity on short days for many weeks, then
photostimulated with long-day photoperiods exhib-
ited an increase in gonad size and an increase in the
size of song-control regions compared to birds kept
on short days (MacDougall-Shackleton et al. 2003a).
Chickadees held in captivity on long days for many
weeks become photorefractory and fail to show
gonadal responses to changes in photoperiod
(reviewed above). These birds also fail to show any
changes in the size of song-control regions includ-
ing HVC (Phillmore et al. 2005). These data suggest
the size of song-control regions is influenced by
photoperiod-driven changes in gonadal hormones.
In contrast to laboratory studies, studies of wild-
caught black-capped chickadees do not show
seasonal changes in HVC size. Smulders and
colleagues measured the size of song-control
regions in brains of black-capped chickadees
collected from the wild at different times of year.
These birds had been the subject of previous stud-
ies of hippocampal seasonal plasticity (Smulders
et al. 1995, see below) but failed to exhibit seasonal
changes in the size of song-control brain regions
(Smulders et al. 2006). More recently, we have
similarly examined the brains of black-capped
chickadees collected from the wild at four times of
year: July, October, January, and April. Though the
largest HVC sizes were found in April and July,
there was no statistically significant effect of time of
year on HVC volume (Phillmore et al. 2006).
How can we reconcile the laboratory versus field
studies? One explanation is that black-capped
chickadees do not exhibit large seasonal changes in
HVC size because they produce learned vocaliza-
tions (e.g. the chick-a-dee and gargle calls) all year
round, and thus need to maintain HVC size
throughout breeding and non-breeding seasons.
However, this would not explain the effect of
photostimulation on HVC in captive birds. A second
explanation is that a number of factors not present
in the laboratory and beyond photoperiod influence
HVC size when birds are in the wild. There is large
interindividual variation in the timing of gonadal
recrudescence and regression in the field (Fig. 4.2),
and this may reflect large individual variation in
hormone profiles as well. Supporting this second
explanation, in the study by Phillmore et al. (2006),
HVC was larger in breeding birds than in non-
breeding birds as assessed by gonad size. Thus
interindividual variation in the timing of breeding
may mask seasonal changes in HVC.

8
7 2003
Testis length (mm) 5
0
Jan Mar
Figure 4.2 Annual change in testis size in free-living black-capped chickadees. Data indicate the length of the left testis (measured via
laparotomy) of chickadees captured near London, Ontario, Canada in 2002 and 2003. Note the large variation in gonadal recrudescence in April
and May and in gonadal regression in July.
Other factors such as dominance rank, age, and
amount of singing could also influence circulating
hormones and HVC size. European starlings have
repeatedly been shown to exhibit seasonally plastic
song-control regions in laboratory studies, but
seasonal changes were not apparent in wild-caught
birds (Ball et al. 2004). A similar dichotomy between
field and laboratory studies has also been demon-
strated in wild canaries (Leitner et al. 2001). These
results support the explanation that the lack of
seasonal changes in HVC of free-living birds may
result from individual variation in the timing and
magnitude of these seasonal changes, rather than
the absence of seasonal plasticity per se. Because
many factors such as age, dominance and singing
can be quantified in black-capped chickadees they
represent an excellent species in which to address
this hypothesis.
4.5 Seasonal changes in food storing
and the hippocampus
4.5.1 Food storing
The most extensively studied seasonal behaviors
are those associated with reproduction. However,
P H OTO P E R I O D I S M A N D T H E A N N UA L C Y C L E 49
2002
May Jul Sep Nov
Date
many species of Parids also exhibit seasonal
changes in food-storing (Odum 1942; Haftorn 1956;
Ludescher 1980; Pravosudov 1985; Chapters 2
and 3). In fact, food storing is likely an adaptive
response to seasonal changes in food supply. In
spring and summer, chickadees are primarily
insectivores when that food source is abundant;
birds are not observed to store food at this time. In
autumn and winter birds store more often (Haftorn
1956; Nakamura and Wako 1988; Brodin 1994).
Black-capped chickadees are also frequently
observed caching in autumn and winter (Odum
1942). A recent study of free-living black-capped
chickadees reports high storing rates throughout
the autumn, with highest rates in September and
declining thereafter (Brodin 2005).
Because photoperiod is the principal cue regulat-
ing seasonal changes in reproductive behavior, it is
a tenable hypothesis that it may influence seasonal
changes in food storing as well. For example, the
autumnal increase in food storing could be driven
by short-day photoperiods. Several studies have
addressed this hypothesis in black-capped chicka-
dees. Shettleworth et al. (1995) found that birds
captured in November stored more in captivity
than birds captured in March. Birds at both times of
50 B E H AV I O R A N D E V O L U T I O N
year were then held under different photoperiods,
and birds tended to store more when on short days
than on long days. In particular, birds captured
in March then switched to long days, then switched
back to short days, greatly increased storing as
day-length decreased (Shettleworth et al. 1995).
MacDougall-Shackleton et al. (2003b) conducted a
study to determine whether the autumnal increase
in food storing resulted from decreasing day-length
or the onset of photorefractoriness that occurs in
late summer. They held birds in one of three condi-
tions: long-term long days (photorefractory), long-
term short days (photosensitive), or switched from
long-term short days to long days (photostimu-
lated). Birds on short days stored more than those
on long days, and the photostimulated birds
reduced storing when they were switched from
short to long days (MacDougall-Shackleton et al.
2003b). Thus, regardless of whether birds were
photorefractory or photostimulated, long days led
to a reduction in food storing.
Both captive studies and field observations sug-
gest that food storing is facilitated by experiencing
short-day photoperiods. The effects of photoperiod
on reproduction are direct; that is, the effects of
long days are not an effect of birds having more
time to forage and greater energy intake (Dawson
1986). The stimulatory effects of short days on food
storing, however, could be mediated either directly
or by the fact that birds on short days have less time
to forage and are thus food restricted. Food restric-
tion and food unpredictability do increase food
storing in Parids (Hurly 1992; Pravosudov and
Grubb 1997). A recent study attempted to deter-
mine whether short days per se or shortened time
available to forage was responsible for increased
food storing in fall and winter in black-capped
chickadees. Karpouzos et al. (2005) held birds on
long days, short days, or long days with only short
duration of food availability. For this latter group,
food was removed from the cages of birds held on
a long-day photoperiod at the same time as the
lights went out for the short-day group. There was
no significant variation among groups in food stor-
ing; all groups stored relatively little. However, fat
and mass profiles were identical for the two groups
of birds with short duration of food availability and
both differed from that of birds with long day
photoperiod and food availability (Karpouzos et al.
2005). Thus, energy balance seems to be mediated
by duration of food availability rather than photo-
period per se. Future work is needed to determine
whether this is also true for food-storing behavior.
4.5.2 Hippocampus
The hippocampus is a region of the brain that is
important for spatial memory in most vertebrates
and is required for accurate retrieval of food from
caches in black-capped chickadees (Sherry and
Vaccarino 1989). Indeed, there is much evidence
indicating that the hippocampus is adaptively
specialized in response to spatial memory demands
in food-storing birds such as black-capped chicka-
dees (Chapter 2). Because food storing is seasonal,
several researchers have examined the question of
whether the chickadee hippocampus shows
seasonal plasticity similar to that observed in the
song-control regions of many songbirds. Here we
briefly review the evidence that the hippocampus is
seasonally plastic and the potential role of photo-
period in such plasticity.
The evidence for seasonal changes in the size of
the hippocampus is mixed. Smulders et al. (1995,
2000) found an effect of season on hippocampus
size and the number of cells in the hippocampus in
black-capped chickadees caught from the wild at
different times of the year. However, no other study
has replicated this finding. Three further studies
that captured free-living chickadees at different
times of the year did not find an overall change in
hippocampus size (Barnea and Nottebohm 1994;
Hoshooley and Sherry 2004; Hoshooley et al. 2007).
Each of these studies was carried out on different
birds and a meta-analysis has yet to be conducted.
Laboratory studies also do not show an effect of
photoperiod on hippocampus size. Photoperiod
manipulations that successfully affect food-storing
behavior do not affect hippocampus size (Krebs
et al. 1995; MacDougall-Shackleton et al. 2003b;
Hoshooley et al. 2005). If hippocampus size does
change seasonally this effect is not as readily
observable as changes in the song-control system.
Several studies have now examined seasonal plas-
ticity of the black-capped chickadee hippocampus
using cell-birth markers to examine the incorporation

of new neurons. In free-living chickadees the recruit-
ment of new neurons to hippocampus appears to be
maximal during autumn, based on counts of new
neurons that had survived several weeks (Barnea
and Nottebohm 1994). More recently, a study has
found that incorporation of young cells (6 days old)
into hippocampus was greatest in January
(Hoshooley et al. 2007), a trend that was observed in
a prior study (but was not statistically significant,
Hoshooley and Sherry 2004, Chapter 2). Even in the
absence of seasonal changes in overall size, then, the
hippocampus may exhibit seasonal plasticity.
An open question in regards to seasonal plasti-
city of the hippocampus is what causes the
observed changes. Photoperiod might play a role,
by modulating circulating hormones that could
affect hippocampal tissue. Indeed, the songbird
hippocampus is rich in receptors for sex steroids
such as testosterone and estradiol (e.g. Saldanha
et al. 1998) and the photoperiodically modulated
hormone melatonin (Bentley et al. 1999). In addition,
food storing itself may modulate plasticity of the
hippocampus. Developmentally, the amount of
food storing affects the size of the hippocampus
(Clayton and Krebs 1994) and this may occur
seasonally as well. Finally, dominance status of
birds may influence hormone levels, food storing,
and plasticity in the hippocampus (Pravosudov
and Omanska 2005; Chapter 3). Thus, the
conditions under which seasonal plasticity of the
hippocampus is observed, and the factors that
cause it, remain largely to be explored.
4.6 Future directions
Recent studies have revealed that black-capped
chickadees exhibit photoperiodic responses and
photorefractoriness similar to many other songbird
species. However, seasonal changes in the brain
have produced mixed results, especially when
comparing birds caught from the wild with birds
held in captivity. Reconciling the differences among
these studies will likely require more detailed con-
sideration of variation among populations and
variation among individuals.
Dominance status is a pervasive factor affecting a
chickadees behavior and physiology (Chapter 9).
However, dominance status is rarely considered in
P H OTO P E R I O D I S M A N D T H E A N N UA L C Y C L E 51
studies of photoperiodism and seasonality. Recent
data indicate that dominance status influences
neural plasticity in addition to influencing food
storing (Chapter 3; Pravosudov and Omanska
2005) and singing (Christie et al. 2004; Chapter 14).
Another factor that may influence seasonal changes
in brain and behavior is age, but this is not typically
controlled for in studies of seasonality beyond
distinguishing hatch-year from older birds.
Because black-capped chickadees are year-round
residents of the same small geographic location,
typically for their entire postdispersal life, they
provide a tremendous opportunity to examine how
factors such as age and dominance rank interact
with environmental cues, such as photoperiod, to
drive seasonal changes in brain and behavior.
Given the current mixed results in regards to neural
plasticity in this species (possibly due to individual
variation), at the very least dominance rank of indi-
viduals needs to be considered more fully in future
studies. In addition, much of the work on seasonal
changes in reproductive physiology in chickadees
is based on gonadal data. Further analyses of
hormones, as has been carried out in Eurasian
Parids (e.g. Silverin 1991, 1994), are required.
Another tremendous opportunity provided by
black-capped chickadees is their extremely large
geographic range. Comparisons among popula-
tions living at different latitudes have already
yielded important results regarding the adaptive
specialization of spatial memory and the
hippocampus (Pravosudov and Clayton 2002;
Chapter 3). This approach could be expanded to
compare populations that experience more or less
annual variance in the duration of daylight, and
how they respond to this seasonal change in
photoperiod. This comparative approach should
also be expanded to include other Parids that
experience the same or different photoperiods as
black-capped chickadees. Black-capped chickadees
will likely continue to be an important species in
the study of photoperiod and seasonality from an
integrative ecological approach.
Acknowledgments
Our research has been funded by NSERC Canada
and a Premiers Research Excellence Award from
52 B E H AV I O R A N D E V O L U T I O N
the Province of Ontario. David Sherry and Jennifer
Hoshooley have provided invaluable input to our
research and our preparation of this chapter.
References
Baker, J. (1938). The Evolution of Breeding Seasons.
Clarendon Press, Oxford, United Kingdom.
Ball, G. F. and Hahn T. P. (1997). GnRH neuronal systems
in birds and their relation to the control of seasonal
reproduction. In: Parhar, I. S., Sakuma, Y., eds. GnRH
Neurons: Gene to Behavior, pp. 325342. Brain Shuppan,
Tokyo.
Ball, G. F., Auger, C. J., Bernard, D. J., Charlier, T. D.,
Sartor, J. J., Riters, L. V., and Balthazart, J. (2004).
Seasonal plasticity in the song-control system: multiple
brain sites of steroid hormone action and the impor-
tance of variation in song behaviour. Annals of the New
York Academy of Sciences, 1016, 586610.
Barnea, A. and Nottebohm, F. (1994). Seasonal recruitment
of hippocampal neurons in adult free-ranging black-
capped chicakdees. Proceedings of the National Academy
of Sciences USA, 91, 1121711221.
Bentley, G. E., Vant Hof, T. J., and Ball, G. F. (1999).
Seasonal plasticity in the songbird telencephalon: a role
for melatonin. Proceedings of the National Academy of
Sciences USA, 96, 46744679.
Brenowitz, E. A. (2004). Plasticity of the adult avian song
control system. Annals of the New York Academy of
Sciences, 1016, 560585.
Brodin, A. (1994). The role of naturally stored food
supplies in the winter diet of the boreal willow tit Parus
montanus. Ornis Svecica, 4, 3140.
Brodin, A. (2005). Hippocampal volume does not correlate
with food-hoarding rates in the black-capped chickadee
(Poecile atricapillus) and willow tit (Parus montanus).
Auk, 122, 819828.
Caro, S. P., Lambrechts, M. M., and Balthazart, J. (2005).
Early seasonal development of brain song control
nuclei in male blue tits. Neuroscience Letters, 386,
139144.
Christie P. J., Mennill, D. J., and Ratcliffe, L. M. (2004).
Pitch shifts and song structure indicate male quality in
the dawn chorus of black-capped chickadees. Behavioral
Ecology and Sociobiology, 55, 341348.
Clayton, N. S. and Cristol, D. A. (1996). Effects of
photoperiod on memory and food storing in captive
marsh tits, Parus palustris. Animal Behaviour, 52, 715726.
Clayton, N. S. and Krebs, J. R. (1994). Hippocampal
growth and attrition in birds affected by experience.
Proceedings of the National Academy of Science USA, 91,
74107414.
Clayton, N. S., Reboreda, J. C., and Kacelnik, A. (1997).
Seasonal changes of hippocampus volume in parasitic
cowbirds. Behavioural Processes, 41, 237243.
Dawson, A. (1986). The effect of restricting the daily
period of food availability on testicular growth of star-
lings Sturnus vulgaris. Ibis, 128, 572575.
Dawson, A. (2002). Photoperiodic control of the annual
cycle in birds and comparison with mammals. Ardea,
90, 355367.
Dawson, A., King, V. M., Bentley, G. E., and Ball, G. F.
(2001). Photoperiodic control of seasonality in birds.
Journal of Biological Rhythms, 16, 365380.
Ficken, M. S., Ficken, S. R., and Witken, S. R. (1978). Vocal
repertoire of the black-capped chickadee. Auk, 95,
3448.
Fort, K. A. and Otter, K. A. (2004). Effects of habitat
disturbance on reproduction in black-capped chicka-
dees (Poecile atricapillus) in northern British Colombia.
Auk, 121, 10701080.
Gammon, D. E. (2004). Black-capped chickadee dawn
chorus and subsequent sexual activity. Wilson Bulletin,
116, 252256.
Haftorn, S. (1956). Contribution to the food biology of tits
especially about storing of surplus food. Part IV: a
comparative analysis of Parus atricapillus L., P. cristatus
and P. ater. Det kgl Norske Videnskabrs selskabs Skrifter,
4, 154.
Hahn, T. P. (1995). Integration of photoperiodic and food
cues to time changes in reproductive physiology by an
opportunistic breeder, the red crossbill, Loxia curvirostra
(Aves, Carduelinae). Journal of Experimental Zoology, 272,
213226.
Hahn, T. P., Boswell, T., Wingfield, J. C., and Ball, G. F.
(1997). Temporal flexibility in avian reproduction:
patterns and mechanisms. Current Ornithology, 14, 3980.
Hamner, W. M. (1968). The photorefractory period of the
house finch. Ecology, 49, 211227.
Horn, A. G., Leonard, M. L., Ratcliffe, L., Shackleton, S. A.,
and Weisman, R. G. (1992). Frequency variation in
songs of black-capped chickadees (Parus atricapillus).
Auk, 109, 847852.
Hoshooley, J. S. and Sherry, D. F. (2004). Neuron produc-
tion, neuron number, and structure size are seasonally
stable in the hippocampus of the food-storing black-
capped chickadee (Poecile atricapillus). Behavioral
Neuroscience, 118, 345355.
Hoshooley, J. S., Phillmore, L. S., and MacDougall-
Shackleton, S. A. (2005). An examination of avian
hippocampal neurogenesis in relation to photoperiod.
Neuroreport, 16, 987991.
Hoshooley, J. S., Phillmore, L. S., Sherry, D. F., and
MacDougall-Shackleton, S. A. (2007). Annual cycle of
the black-capped chickadee: seasonality of food-storing

and the hippocampus. Brain, Behavior and Evolution,
in press.
Hughes, M., Nowicki, S., and Lohr, B. (1998). Call learning
in black-capped chickadees (Parus atricapillus): the role
of experience in the development of chick-a-dee calls.
Ethology, 104, 232249.
Hurly, T. A. (1992). Energetic reserves of marsh tits (Parus
palustris): food and fat storage in response to variable
food supply. Behavioral Ecology, 3, 181188.
Karpouzos, H., Hernandez, A. M., MacDougall-
Shackleton, E. A., and MacDougall-Shackleton, S. A.
(2005). Effects of day-length and food availability on
food caching, mass and fat reserves in black-capped
chickadees (Poecile atricapillus). Physiology and Behavior,
84, 465469.
Krebs, J. R., Clayton, N. S., Hampton, R. R., and
Shettleworth, S. J. (1995). Effects of photoperiod on food
storing and hippocampus in birds. NeuroReport, 6,
17011704.
Leitner, S., Voigt, C., Garcia-Segura, L. M., Vant Hof, T.,
and Gahr, M. (2001). Seasonal activation and inactiva-
tion of song motor memories in wild canaries is not
reflected in neuroanatomical changes of forebrain song
areas. Hormones and Behavior, 40, 160168.
Ludescher, F.-B. (1980). Fressen und Verstecken
von Smereieien bei der Weidenmeise Parus
montanus im Jahresverlauf unter koknstanten
Ernhrungsbedingungen. Okol Vogel, 2, 135144.
MacDougall-Shackleton, S. A., Hernandez, A. M., Valyear,
K. F., and Clark, A. P. (2003a). Photostimulation induces
rapid growth of song-control brain regions in male and
female chickadees (Poecile atricapilla). Neuroscience
Letters, 340, 165168.
MacDougall-Shackleton, S. A., Pereyra, M. E., and Hahn,
T. P. (2005). GnRH, photorefractoriness and breeding
schedules of cardueline finches. In: Dawson, A., and
Sharp, P. J., eds. Functional Avian Endocrinology, pp.
97110. Narosa Publishing House, New Delhi, India.
MacDougall-Shackleton, S. A., Sherry, D. F., Clark, A. P.,
Pinkus, R., and Hernandez, A. M. (2003b).
Photoperiodic regulation of food-storing and hip-
pocampus volume in black-capped chickadees (Poecilie
atricapilla). Animal Behaviour, 65, 805812.
Nakamura, H. and Wako, Y. (1988). Food storing behavior
of willow tit Parus montanus. Journal of Yamashina
Institute of Ornithology, 20, 2136.
Nicholls, T. H., Goldsmith, A. R., and Dawson, A. (1988).
Photorefractoriness in birds and comparison with
mammals. Physiological Review, 68, 133176.
Odum, E. P. (1941a). Annual cycle of the black-capped
chickadee1. Auk, 58, 314333.
Odum, E. P. (1941b). Annual cycle of the black-capped
chickadee2. Auk, 58, 518534.
P H OTO P E R I O D I S M A N D T H E A N N UA L C Y C L E 53
Odum, E. P. (1942). Annual cycle of the black-capped
chickadee3. Auk, 59, 499531.
Phillmore, L. S., Hoshooley, J. S., Hahn, T. P., and
MacDougall-Shackleton, S. A. (2005). A test of absolute
photorefractoriness and photo-induced neural plasti-
city of song-control regions in black-capped chickadees
(Poecile atricapillus). Canadian Journal of Zoology, 83,
747753.
Phillmore, L. S., Hoshooley, J. S., Sherry, D. F., and
MacDougall-Shackleton, S. A. (2006). Annual cycle of
the black-capped chickadee: seasonality of singing rates
and vocal-control brain regions. Journal of Neurobiology,
66, 10021010.
Pravosudov, V. V. (1985). Search for and storage of food by
Parus cinctus lapponicus and P. montanus borealis
(Paridae). Zoologichesky Zhurnal, 64, 10361043.
Pravosudov, V. V., and Clayton, N. S. (2002). A test of the
adaptive specialization hypothesis: population differ-
ences in caching, memory, and the hippocampus in
black-capped chickadees (Poecile atricapilla). Behavioral
Neuroscience, 116, 515522.
Pravosudov, V. V., and Grubb Jr, T. C. (1997). Management
of fat reserves and food caches in tufted titmice (Parus
bicolor) in relation to unpredictable food supply.
Behavioral Ecology, 8, 332339.
Pravosudov, V. V., and Omanska, A. (2005). Dominance-
related changes in spatial memory are associated with
changes in hippocampal cell proliferation rates in
mountain chickadees. Journal of Neurobiology, 62, 3141.
Robinson, J. E. and Follett, B. K. (1982). Photoperiodism in
Japanese quail: the termination of seasonal breeding by
photorefractoriness. Proceedings of the Royal Society of
London B, 215, 95116.
Rowan, W. (1925). Relation of light to bird migration and
developmental changes. Nature, 115, 494495.
Saldanha, C. J., Popper, P., Micevych, P. E., and Schlinger,
B. A. (1998). The passerine hippocampus is a site of high
aromatase: inter- and intra-species comparisons.
Hormones and Behavior, 34, 8597.
Shackleton, S. A. and Ratcliffe, L. M. (1993). Development
of song in hand-reared black-capped chickadees. Wilson
Bulletin, 105, 637644.
Shackleton, S. A. and Ratcliffe, L. M. (1994). Matched
counter-singing signals escalation of aggression in
black-capped chickadees (Parus atricapillus). Ethology,
97, 310316.
Sherry, D. F. and Vaccarino, A. L. (1989). Hippocampus
and memory for food caches in black-capped chicka-
dees. Behavioral Neuroscience, 103, 308318.
Shettleworth S. J., Hampton, R. R., and Westwood, R. P.
(1995). Effects of season and photoperiod on food
storing by black-capped chickadees, Parus atricapillus.
Animal Behaviour, 49, 989998.
54 B E H AV I O R A N D E V O L U T I O N
Silverin, B. (1978). Circannual rhythms in gonads and
endocrine organs of the great tit Parus major in south-
west Sweden. Ornis Scandinavia, 9, 207213.
Silverin, B. (1991). Annual changes in plasma levels of LH,
and prolactin in free-living female great tits (Parus
major). General and Comparative Endocrinology, 83,
425431.
Silverin, B. (1994). Photoperiodism in male great tits
(Parus major). Ethology, Ecology, and Evolution, 6,
131157.
Silverin, B., Kikuchi, M., and Ishii, S. (1997). Seasonal
changes in follicle-stimulating hormone in free-living
great tits. General and Comparative Endocrinology, 108,
366373.
Silverin, B., Massa, R., and Stokkan, K. A. (1993).
Photoperiodic adaptation to breeding at different lati-
tudes in great tits. General and Comparative
Endocrinology, 90, 1422.
Smith, S. (1991). The Black-capped Chickadee: Behavioral
Ecology and Natural History. Cornell University Press,
Ithaca.
Smulders, T. V. (2002). Natural breeding conditions and
artificial increases in testosterone have opposite effects
on the brains of adult male songbirds. Hormones and
Behavior, 41, 156169.
Smulders, T. V., Lisi, M. D., Tricomi, E., Otter, K. A.,
Chruszcz, B., Ratcliffe, L. M., and DeVoogd, T. J. (2006).
Failure to detect seasonal changes in the song system
nuclei of the black-capped chickadee (Poecile atricapil-
lus). Journal of Neurobiology (66, 9911001).
Smulders, T. V., Sasson, A. D., and DeVoogd, T. J. (1995).
Seasonal variation in hippocampal volume in a food
storing bird, the black-capped chickadee. Journal of
Neurobiology, 27, 1525.
Smulders, T. V., Shifflet, A. J., Sperling, A. J., and
DeVoogd, T. J. (2000). Seasonal changes in the
hippocampal formation of a food hoarding bird: the
black-capped chickadee. Journal of Neurobiology, 44,
414422.
Tramontin, A. D. and Brenowitz, E. A. (2000). Seasonal
plasticity in the adult brain. Trends in Neuroscience, 23,
251258.
 CHAPTER 5
Fine-scale variation in the timing
of reproduction in titmice and
chickadees
Scott M. Ramsay and Ken A. Otter
5.1 Introduction
Variation among female songbirds in the timing of
clutch initiation has been studied, nearly continu-
ously, for at least the last 60 years. Rather than a
focus on control of broad timing patterns across sea-
sons (Chapter 4), this research has concerned itself
with fine-scale adjustment of reproductive timing
for strategic breeding purposes. It has benefited
from long-term data sets that have accumulated in a
number of studies including, but not limited to, the
great and blue tits breeding at Wytham in Oxford,
UK (Lack 1966, and review in McCleery and Perrins
1988), great tits at a number of sites in the
Netherlands (Kluijver 1951, and reviewed in van
Noordwijk and van Balen 1988), and more recent
studies of blue tits nesting in the Mediterranean
forests of southern France and Corsica. Studies of
reproductive timing in North American Parids are
limited, but in recent years we have begun studying
reproductive timing in black-capped chickadees.
Our goal is to summarize the knowledge gained on
reproductive timing in Eurasian species, compare it
to the fledgling research on this topic in North
America, and, finally, suggest both directions and
species where comparable work could be initiated
on this continent.
Historically, there have been three distinct phases
of research on reproductive timing, each with a
slightly different focus. In the earliest phase,
research focused on describing the degree of vari-
ation in timing among females and some of the
effects of this variation (Section 5.2). In the second
phase, the focus shifted to determining the mech-
anisms responsible for this variation; much of this
work continues today (Section 5.3). The third phase
has shifted back to effects of variation in reproduc-
tive timing, particularly in the face of current and
anticipated changes in climate (Sections 5.4 and
5.5). In this most recent phase, researchers have
attempted to link female capacity for adjusting
clutch initiation to regular climatic cycles, such as
the North Atlantic Oscillation, and anthropogenic
changes in climate, as well as the changing selec-
tion regimes imposed by these climatic effects. In
all of this research, little effort has been directed
toward studying the onset of fertility in males;
however, the same questions posed about female
timing apply to males, and males face the same
problems as females with regard to climate vari-
ation (Section 5.6).
Parids offer ideal subjects for the study of repro-
ductive timing. First and foremost, clutch sizes are
larger and more variable than in most other species
of songbirds; one of the key effects of variation in
timing is a seasonal decline in clutch size, thus, the
effects of variable timing can be more finely dis-
sected. Second, most populations of tits are resi-
dent, with only occasional irruptive movements.
This behavior permits researchers to study the rela-
tionship between winter ecology and the timing of
breeding, both as a cause of variability leading up
to the breeding season and as an outcome of early
or late breeding. Third, most tits will readily visit
feeding stations throughout the year, permitting
researchers to experimentally manipulate food
55
56 B E H AV I O R A N D E V O L U T I O N
availability. Finally, many of the well-studied popu-
lations nest in boxes, giving researchers a greater
ability to monitor, and potentially manipulate,
nesting phenology and clutch sizes than would be
possible in populations nesting in natural cavities
(see also Chapter 18).
This final point may explain the greater volume
of research on reproductive timing in Eurasian ver-
sus North American species. While great and blue
tits readily take to nest boxes, the most commonly
studied North American Parid, the black-capped
chickadee, prefers natural cavities (Smith 1991).
This can make studies of chronology more difficult
despite the availability of long-term data sets.
Research on reproductive timing in North America
has instead focused on other box-using species,
such as tree swallows Tachycineta bicolor and eastern
bluebirds (Sialia sialis; reviewed in Dunn 2004).
Several North American Parids are more apt than
black-capped chickadees to use nest boxes, such as
Carolina and mountain chickadees. Increased focus
on these species may provide a better understand-
ing of reproductive timing; however, work similar
to that conducted on Eurasian Parids is possible
with black-capped chickadees, as our own studies
are beginning to reveal.
5.2 The history of research on
reproductive timing: Lack 1966
Work by David Lack and his colleagues revealed
that blue and great tits can vary in nest initiation by
as much as 5 weeks between years (Lack 1966),
with the two species varying in parallel. This work
is summarized in Lacks (1966) Populations Studies
of Birds, to which all references in this section refer.
In both Dutch great and blue tits, the annual mean
onset of laying varies with daily temperatures
through March and April: warmer springs lead
to earlier clutch initiation. Lack observed that
temperature could control annual variation in
clutch initiation directly or indirectly through some
third factor correlated with temperature. Sudden
cold snaps delayed the onset of clutch initiation
among females that had not already begun laying;
however, Lack also noted that laying dates were
often consistent among a number of woods in
both England and the Netherlands, and what
inconsistencies did occur (in both species) could
not be attributed to temperature.
An obvious correlate of temperature is food
availability. Great tits provision their nestlings with
the larvae of insects that feed on oak leaves. Insect
eggs hatch around the time of bud-burst, which
occurs later in cold springs, and the date by which
half of all winter moths pupated was tightly
matched to the mean hatch date of tits. Lack noted
that clutch initiation dates within a population can
vary by as much as 2 or 3 weeks in any given year.
As a result, some individuals will necessarily be
early or late in relation to caterpillar peaks. This
imperfect correspondence led Lack to wonder why
natural selection had not eliminated late laying,
since early-laying birds produce more surviving
young. Lack assumed that some other factor must
affect timing, and surmised this may be the time
required for a female to gather sufficient food to
produce a clutch.
Typical great tit females lay nearly their body
weight in eggs over 9 to 10 days. Lack used high
courtship feeding rates by males and age-based dif-
ferences between females in clutch initiation as evi-
dence that, both, females must be energy limited
during egg-laying and yearlings are more heavily
affected by food limitation than older females. Blue
tits lay a few days earlier than great tits in the same
wood. Since nestlings of both species have similar
food requirements, Lack concluded that the differ-
ence in clutch initiation must be due to the food
requirements of the adult females. In support of
this, Lack noted that great tits breeding in gardens
with winter feeders laid earlier than those breeding
in woods. Although offspring production was
timed to coincide with caterpillar production, Lack
concluded that selection would constrain females
to laying only when their condition reached the
level necessary for egg productionit was a coinci-
dence that these factors (food for eggs and food for
nestlings) have been temporally correlation in
the past.
Lack was aware that female great and blue tits
that laid later produced smaller clutches. He
suggested that although the laying date might be
constrained by the availability of food for egg
production, the decline of clutch size might very
well be related to the amount of food available for

nestlings when they reach their peak demand 10
days after hatching. Lack reasoned that this was the
only possible resolution to the apparent paradox
that by delaying laying females would have greater
amounts of food available to them for egg produc-
tion. Research in the intervening 40 years since has
focused on elucidating the causes and costs of vari-
ation in reproductive timing. In the sections that
follow we examine the work that has been con-
ducted on reproductive timing over the last four
decades.
5.3 Causes of fine-scale variation in
timing among individuals
Numerous factors have been identified as affecting
the onset of laying among individual females as
well as between populations. Among these are
intrinsic characteristics of the female, such as her
age, condition, and genotype, and extrinsic factors
such as photoperiod, weather, and food or energy
limitation. At the population level there may be
adaptations to local habitat characteristics. In the
sections below we review the evidence relating to
each of these factors.
5.3.1 Intrinsic factors
5.3.1.1 Female age/genetics
Across species, younger females typically lay later
than older females, and this pattern has been seen
in great tits (McCleery and Perrins 1988; Nager and
van Noordwijk 1995) as well as other tit species
(reviewed in Smith 1991). In spite of this effect of
age, numerous studies have also revealed effects of
genetics and female quality on clutch initiation
dates.
Both great tits (van Noordwijk et al. 1981; van der
Jeugd and McCleery 2002) and marsh tits (Smith
1993) show high individual repeatability of laying
date between years; females that lay relatively early
or late do so consistently across years. In addition,
the repeatability of laying dates among females was
independent of whether they were with the same or
different partners between years, whereas males
showed no repeatability with different partners (van
Noordwijk et al. 1981; Smith 1993); this suggests that
consistency between years is a female trait.
TIMING OF REPRODUCTION 57
Motherdaughter comparisons in a Dutch popu-
lation of great tits revealed that the heritability of
laying date is nearly the same as the repeatability
for individual females, suggesting that the repeat-
ability itself is genetic (van Noordwijk et al. 1981).
This finding differs from an English population, in
which heritability was non-zero for both females
and males. Further, this heritability varied spatially,
suggesting male characteristics and nest sites, in
addition to maternal characteristics, can affect
laying date in some populations (van der Jeugd and
McCleery 2002).
5.3.2 Extrinsic factors
5.3.2.1 Photoperiod
Increasing day-length in spring is well established
as the primary cue that stimulates the production of
hormones triggering the seasonal development of
the gonads in both males and females (reviewed in
Wingfield et al. 1992; Chapter 4). As noted above,
however, the exact timing of layingalthough con-
sistent within femalescan vary considerably
within and between populations and between
years. It is best to think of females responding to a
hierarchy of cues that finely tune the onset of repro-
duction. Increasing day-length is the first of these
cues and prevents individuals from nesting during
inappropriate seasons. Photoperiod changes on a
consistent annual cycle, and is the same for all
females breeding at the same latitude. Therefore, if
we are interested in understanding variation
between females, both within and between years,
we must consider other cues lower in the hierarchy
that vary spatially and temporally.
In spite of the limitations of photoperiod to
explain fine-scale variation within and between
females at a single location, evidence from island
and mainland populations of French blue tits
reveals that females in different populations may
have genetically different sensitivities to changing
photoperiod (Lambrechts et al. 1997). Under experi-
mental breeding conditions females began laying
when the photoperiod was similar to their home
environment, and not the local environment; how-
ever, females from both populations could be
induced to lay early by stimulating them with long
photoperiods in December (Lambrechts and Perret
58 B E H AV I O R A N D E V O L U T I O N
2000). The evidence from these experiments
suggests that variation in photoresponsiveness
between birds in evergreen vs. deciduous oak
forests at the same latitude results from a balance of
selection and migration (Lambrechts et al. 1997; see
also below).
5.3.2.2 Temperature
As Lack (1966) suggested, temperature may affect
clutch initiation either as a direct cue to begin lay-
ing, or as an indirect cue through its effects on both
food availability and the energy requirements of
the female; we discuss food and energy limitation
in the next section.
Exceptionally cold weather prior to clutch initi-
ation delayed breeding in a Finnish population of
Siberian tits (Eeva et al. 2000). Mean laying date of
great tits at the same site, likewise, correlated with
mean monthly temperatures in April. Variation in
timing was attributed to the direct effects of tem-
perature in both species. Similarly, temperatures
from mid-March to mid-April, but not the later
caterpillar peak, were correlated with the onset of
laying in a Swiss population of great tits, suggest-
ing that females are responsive to temperature
independent of its effects on later food availability
(Nager and van Noordwijk 1995). In the same
study, temperature during egg formation (~4 days
prior to laying) had a secondary influence on clutch
initiation over and above the effects of temperature
in the month before. Black-capped chickadees
began laying as much as 2 weeks earlier than usual
when conditions in April were warmer and drier
than normal (Odum 1941). Clutch completion dates
varied by nearly 2 weeks among years in our
population of black-capped chickadees in British
Columbia (Fig. 5.1) and were significantly earlier in
the years with warmer temperatures in April.
Similar patterns have also been seen in Ontario
populations (S. M. Ramsay and K. A. Otter,
unpublished data).
Once laying has begun, females of most species
typically continue until their clutches are complete;
this pattern has been observed in great tits (Nager
and van Noordwijk 1995) and black-capped chicka-
dees (Kluyver 1961). In these populations, females
that have not begun laying will delay clutch initi-
ation until the cold weather passes, usually with a
4-day delay corresponding to the time required for
egg formation (Smith 1991). Laying interruptions
that persist for the duration of cold weather have
been observed in great tits (Lessells et al. 2002).
They have also been observed in blue tits following
cold winters (Dhondt et al. 1983). Similar effects
have been observed in our northern British
Columbia study site with black-capped chickadees,
where episodic snowfalls and subzero tempera-
tures can persist through the regular egg laying
period of early to mid-May (K. A. Otter, K. T. Fort
and H. van Oort, unpublished data).
5.3.2.3 Food/energy limitation
A model of reproductive output suggested that
females must attain some threshold of condition
before they can begin laying (Rowe et al. 1994); the
later they achieve this threshold the smaller their
optimal clutch size. There is ample empirical
evidence from a number of studies to suggest that
females are energy limited prior to clutch initiation.
For example, laying interruptions in great tits were
more likely to coincide with the steepest clutch
size/initiation relationships, reflecting years when
females were in poor condition (Dhondt et al. 1983).
Most small passerines are income breedersthey
35
30
Date (1 May = 1)
25
20
15
10
2002 2003 2004
Year
Figure 5.1 Variation in clutch completion dates over 3 years in a
population of black-capped chickadees from British Columbia,
Canada. Sample sizes were as follows: 2002, n 34; 2003, n 36;
2004, n 14. The mean and variance of clutch completion dates
varied significantly among years (p 0.001).

rely on constant energy intake in order to form
eggsas opposed to capital breeders that rely on
stored reserves for egg formation. Parids are typical
in this respect and evidence from both natural and
experimental studies reveals the link between food
and the timing of laying.
In great tits, natural food abundance affected lay-
ing date and clutch size both within and between
years (Nager and van Noordwijk 1995; Seki and
Takano 1998). In one case, food supplementation
advanced laying date by approximately 5.5 days
(Nager et al. 1997). In blue tits, the effects of food
supplementation varied between individuals, with
low-quality females experiencing the greatest
benefit (up to 9 days advance in laying date) while
high-quality females showed little or no change
(Svensson and Nilsson 1995). In none of these
studies did food supplementation affect clutch size.
This change in laying date with no co-ordinated
change in clutch size supports the idea that females
must reach some condition threshold before laying,
but contradicts the idea that there is an optimal
clutch size associated with specific laying dates
(Rowe et al. 1994).
Two different studies of food supplementation
suggest that it is energy and not specific nutrients
that limit egg formation. Female great tits advanced
their laying dates independent of the protein con-
tent of the food supplement (Nager et al. 1997).
Similarly, female blue tits did not differ in the onset
of laying when receiving a high protein versus a
high fat supplement (Ramsay and Houston 1997).
Thus, females seem to be capable of synthesizing
the various nutrients they need for egg formation,
as long as they have an ample supply of food.
Energy limitation and parasite loads, independ-
ent of food supplementation, may also affect female
timing. Great and blue tits began laying earlier in
boxes that were naturally warmer; however, the
effects of box temperatures are not as strong as
would be predicted based on the energy limitation
hypothesis (Dhondt and Eyckerman 1979). Female
great tits nesting in experimentally cooled boxes
had reduced egg volumes, but temperature manip-
ulation had no effect on the onset of laying (Nager
and van Noordwijk 1992). Female blue tits in
heated boxes experienced fewer interruptions of
laying than controls (Yomtov and Wright 1993).
TIMING OF REPRODUCTION 59
In support of the energy limitation hypothesis, the
resting metabolic rate of great tits was highest in
the egg-laying phase of reproduction and correl-
ated significantly with egg mass (Nilsson and
Rberg 2001). Thus it appears that females are
energy limited, but only weakly in ways related to
thermoregulation.
Infection with blood parasites can have an inter-
mediate effect on timing of egg laying; unpara-
sitized female great tits laid earlier than parasitized
females (Allander and Bennett 1995). This appeared
to be the result of: (i) nutrient depletion to females
through competition with the parasites; and (ii) a
loss of tissue oxygenation capacity through red
blood cells being occupied by parasites. The
connection between blood parasites and laying
dates deserves further investigation in light of
evidence that a major cost of egg production in
zebra finches (Taeniopygia guttata) and Eurasian
starlings (Sturnus vulgaris) is prolonged anemia
(Williams 2005).
5.3.3 Population adaptations to local habitat
Evidence of adaptive variation of laying dates in
response to local forest phenology comes from a
long-term study of tits breeding in deciduous and
evergreen oak forests of the southern mainland in
France and on the island of Corsica. This work is
reviewed in detail in Chapter 17, but we highlight
the main habitat difference here. Breeding is earlier
in the mainland compared to the island popula-
tions of both blue and coal tits (Blondel 1985). In
both species this delay in breeding on the island is
accompanied by reduced clutch size and fledging
success, and a lack of second broods (Blondel 1985).
The differences of laying date between mainland
and island blue tits was related to phenology of
deciduous (mainland) vs. evergreen (island) oak
forests (Blondel et al. 1993). The birds in mainland
evergreen forests breed too early in relation to local
bud burst, but are well-timed for the neighboring
deciduous forest. A captive-rearing experiment
revealed that there is a genetic basis for the local
laying dates (Blondel et al. 1990).
One hypothesis explaining locally adapted lay-
ing dates is that females respond to cues in the buds
on local trees. However, three independent captive
60 B E H AV I O R A N D E V O L U T I O N

experiments and one natural experiment in blue 5.4.1 Offspring production and recruitment
and great tits failed to show any effect of bud phen-
5.4.1.1 Clutch size
ology on laying dates (Visser et al. 2002). Thus,
Numerous studies have repeated Lacks observa-
aside from photoresponsiveness, the cues that time
tion of a decline of clutch size with laying date:
reproduction in local habitats remain elusive. One
black-capped chickadees (Kluyver 1961; S. M.
possibility is that females are responsive to other
Ramsay unpublished data); marsh tits (Smith 1993);
aspects of tree phenology. Black-capped chickadees
blue tits (Nilsson and Svensson 1993). The box-
breeding in eastern Canada have been observed
nesting habits of Eurasian tits have allowed
feeding on the catkins of birch and aspen trees lead-
researchers to manipulate nesting conditions, such
ing up to laying (S. M. Ramsay personal observa-
as inducing females to delay laying; these experi-
tion). It would be productive to investigate the
ments have resulted in reduced clutch sizes in
possibility that nutrients or other compounds asso-
manipulated females (great tits, Verhulst and
ciated with the catkins trigger reproduction.
Tinbergen 1991, Barba et al. 1995; blue tits, Sanz
Oak and juniper titmice in the US southwest may
1999). The effects of delayed laying were popula-
provide useful insights into the effects of vegetation
tion-specific in one study of great tits, with the
differences, comparable to the blue tits of France.
quality of individual territories and vegetation-
Formerly classified as a single species (the plain
related food availability between the populations
titmouse), the oak titmouse inhabits warm, dry,
likely causing the difference (Verhulst and
evergreen oak forests in California while the
Tinbergen 1991).
juniper titmouse inhabits juniper or pion-juniper
One potential criticism of experimental delays
forests in the Sierra Nevada and Rocky Mountains.
lies in the typical protocol for these studies; delays
Differences in breeding chronology of these sister
are usually induced by removing first clutches once
species may result from differences in prey abun-
laying is complete. As a result, the experimentally
dance across the divergent habitats that they
delayed females have laid many more eggs than
occupy (see Harrap and Quinn 1995). Although
their unmanipulated counterparts. In the light of
they are reported to readily use nest boxes, little
evidence that females given supplemental food will
work has been done on these species; however, one
advance their laying dates without changing their
study of oak titmice revealed that box-nesting
clutch sizes, it would be reasonable to assume that
females laid earlier, had larger clutches, and had
the declines of clutch size seen in manipulated
higher fledging success than females in natural
females may have more to do with female condi-
cavities (Purcell et al. 1997). Clearly, these species
tion rather than timing per se. One solution to this
offer ample opportunity for further study.
problem is to manipulate food supply in one year
and examine the effects of altered timing in the sub-
5.4 Effects of fine-scale variation sequent year (Gienapp and Visser 2006; see below).
in timing
As Lack (1966) was aware, varying nest initiation 5.4.1.2 Synchronization with offspring food supply
dates can affect a number of individual fitness Lack (1966) suggested that the synchronization of
components. At the most basic level, clutch size offspring demand with food availability is a key
declines with laying date. The effects extend to component of selection on laying date. One bit of
hatching and fledging success, the condition of evidence used in Lacks argument was the observa-
offspringespecially as a function of the synchron- tion that clutch sizes decline with laying date
ization of offspring need with the abundance of despite the fact that food abundance for females
foodrecruitment of offspring into the breeding increases as the laying season progresses.
population, the survivorship of adults, and their English great tits varied clutch size and the onset
ability to invest in future bouts of reproduction. In of incubation in response to temperature (Creswell
this section we examine the evidence for each of and McCleery 2003); this maintained synchrony
these effects. between laying date and food availability for

offspring by increasing the time between clutch ini-
tiation and hatch dates without altering the
difference between hatch date and the date of half-
fall of winter moth larvae. Likewise, laying dates in
Dutch great tits have correlated with winter moth
half-fall dates for nearly 40 years (van Noordwijk
et al. 1995). Swiss great tits were most successful
when their broods were synchronized with the
local caterpillar peak (Nager and van Noordwijk
1995). Selection should favor early laying, as these
females could strategically delay hatching if neces-
sary by adjusting both clutch size or the onset of
incubation. Late-laying females, by comparison,
would have little capacity for adjusting hatching
date (van Noordwijk et al. 1995).
Timing of laying to synchronize offspring
demand with caterpillar production does not
appear to be a constraint in high-latitude popula-
tions. Great and Siberian tits breeding in northern
Finland experienced peaks of arthropod abundance
after young had fledged (Eeva et al. 2000). Although
food may be limited during the critical period of
nestling demand, the delayed food production may
still be useful for parents with dependent fledglings
(Eeva et al. 2000). This delay in caterpillar produc-
tion may also affect the over-winter survival of
adults who begin molting during the nestling
phase (see below).
5.4.1.3 Hatching/fledging success
In addition to the effects of clutch initiation date on
clutch size, female timing has also been shown to
have effects that carry on into the nestling and fledg-
ling stages. Great tits with experimentally delayed
broods showed greater hatching asynchrony, lighter
nestlings 15 days posthatch, and lower fledging
success (Barba et al. 1995; Verhulst and Tinbergen
1991). Hatching asynchrony in late nesting attempts
was also seen in black-capped chickadees pairs
renesting after their first nests were depredated
(Smith 1991). This hatch asynchrony appears to be
due to the females initiating incubation prior to
completing the clutch (Fig. 5.2; K. A. Otter, personal
observation). Such clutches are often smaller than
the population average, and the nestlings can hatch
over a period of 3 to 4 days. Pressure to hasten hatch
date in relation to seasonal food availability may be
the cause of this premature incubation.
TIMING OF REPRODUCTION 61
Figure 5.2 An example of asynchronous hatching in a brood of
black-capped chickadees. Photo credit K. A. Otter.
Experiments to alter the timing of egg-laying in
blue tits have yielded some surprising results. In
addition to the expected reductions of fledging suc-
cess in experimentally delayed broods (Sanz 1999),
females induced to lay early with supplemental
food also had reduced fledging success (Nilsson
1994). Experimentally delayed broods did not suf-
fer a reduction in fledging success as a proportion
of eggs laid; however, the fledglings were lighter
than controls, but not naturally late broods (Sanz
1999). These results suggest that clutch initiation,
incubation, and hatch timing are all under stabiliz-
ing selection.
5.4.1.4 Recruitment
The effects of variation in female timing on
offspring extend beyond the period of parental
effort, through to over-winter survival and recruit-
ment of offspring. Blue and great tits produced in
broods with early or intermediate hatch dates
experienced greater survival to winter (Norris 1993;
Barba et al. 1995; Svensson 1997; Verboven and
Visser 1998). This pattern persisted in cross-
fostering experiments suggesting that the effects on
survival were due to the female that laid the clutch
rather than the parents that raised the brood
(Norris 1993). This study also showed that early-
hatching broods were more synchronized with
available food.
Naturally low recruitment into natal populations
in black-capped chickadees makes them poor
62 B E H AV I O R A N D E V O L U T I O N
models to test whether future survival is affected
by hatch date. Other North American Parids which
exhibit higher philopatry may be more suited to
such studies. Regardless, there is cause to suggest
that early nesting may enhance survival in black-
capped chickadees indirectly, through the influence
of early settlement on dominance rank. Survival is
correlated with rank in black-capped chickadees
(Smith 1991), and there is evidence that early settle-
ment into flocks in the fall may increase the likeli-
hood of individuals dominating other same-aged
juveniles. In aviary trials, relative dominance
between two individuals was influenced by the
order they were placed in the aviary; first birds
were more likely to dominate later individuals in
both females (Ramsay and Ratcliffe 2004) and
males (K. A. Otter, unpublished data). If this pat-
tern occurs in wild flocks, there may be an advan-
tage to early dispersal, which would favor earlier
hatching and fledging dates. Early dispersal in
crested tits facilitates settlement in preferred habitat
(Lens and Dhondt 1994).
5.4.2 Future effects on adult fitness
components
5.4.2.1 Survivorship
Variation in clutch initiation dates has been linked
to over-winter survival of adults in a number of
studies. Female great tits with later laying dates
suffered higher mortality leading up to the subse-
quent breeding season (McCleery and Perrins 1988;
Verhulst and Tinbergen 1991). Reduced survival
was also evident in adult blue tits that raised
either experimentally advanced (Nilsson 1994) or
experimentally delayed broods (Nilsson and
Svensson 1996). The delayed blue tits expended
more energy, deposited more fat during cold
weather, lost more mass overnight when tempera-
tures were low (Nilsson and Svensson 1996) and
delayed females showed indications of lower
condition following fledging of their nests (Sanz
1999). Another study of blue tits revealed that
females with higher provisioning effort had lower
survival during the following winter (Thomas et al.
2001). Several of these studies have suggested that
delayed molts associated with late nesting may
influence later survival.
Populations nesting at high latitudes may face
a different set of tradeoffs between molt and
provisioning dependent offspring. In northern
populations of great and Siberian tits, molt over-
laps with the nestling phase (Dhondt 1981; Eeva
et al. 2000), possibly in response to time limitation
imposed by the short breeding season. Overall,
parental effort may be lower in these populations;
adult Siberian tits began caching food items for
autumn and winter while they were still feeding
fledglings (Eeva et al. 2000).
5.4.2.2 Future breeding costs
The effects of varying clutch initiation can extend to
future reproductive bouts, both in the current sea-
son and in future years. In blue tits (Nilsson 2000),
great tits (Verboven and Verhulst 1996), and black-
capped chickadees (Odum 1941) early breeding
dates are associated with an increased ability of
females to raise replacement clutches following
brood failure, or second clutches following the
successful first broods. Similarly, female great tits
with experimentally delayed broods were less
likely to renest following nest failure (Barba et al.
1995). The ability to attempt second broods may
have more to do with time constraints than with a
females ability to invest. A multipopulation study
across a latitudinal gradient would be necessary to
test this idea: if multiple brooding is time-limited
within a season, females breeding at higher
latitudes should be less likely to produce second
clutches than more southerly females of similar
condition.
Between years, females may also be affected by
the costs of delayed breeding. As noted above, lay-
ing dates are repeatable within females; however,
great tit females compensated for mistimed breed-
ing in one year by delaying or advancing laying in
the next year (Nager and van Noordwijk 1995;
Gienapp and Visser 2006), but the effects of
experimental mismatches were population specific
(Gienapp and Visser 2006). Experimentally manipu-
lated female blue tits laid later in the following
season both when their nests were delayed (Nilsson
and Svensson 1996), and when supplemental food
was used to reduce the asynchrony between
natural food abundance and nestling demand
(Grieco et al. 2002). One interpretation of this result

is that females may learn local food phenology (i.e.
if a territory is consistently early or late in relation
to other nearby territories) and the manipulated
females may thus have used a strategy that all
females employ once they have settled on a lifetime
breeding territory (Grieco et al. 2002). Females may
also use social strategies to compensate for delayed
nesting as evidenced by higher rates of divorce and
subsequent improvement among late-breeding
blue tits (Dhondt and Adriaensen 1994).
5.5 Consequences of long-term climatic
variation on reproductive timing
A number of recent studies have focused on the
effects of climatic variation on clutch initiation.
These studies have focused on two different aspects
of climatic variation, natural cyclic variation and
directional change due to anthropogenic effects.
The first of these effects is not exclusive of the
second (Fig. 5.3) and, indeed, the coincidence of
the two necessitates long-term studies to elucidate
the changes associated with each.
5.5.1 Cyclical climatic variation
The North Atlantic Oscillation (NAO), like the El
Nio Southern Oscillation, is an example of a tele-
connection pattern, a situation where temperature
and air pressure gradients affect climate over
Average spring temperature
Time (years)
Figure 5.3 Hypothetical change of average spring temperatures over several decades. A steady, long-term increase in average temperatures
occurs over a background of cyclical variation. This type of pattern is what we expect to see when we combine the effects of decadal cycles such
as the North Atlantic Oscillation with persistent global warming.
TIMING OF REPRODUCTION 63
great distances. The NAO is related to sea surface
temperatures between the Azores and Iceland.
Depending on the phase of the oscillation, which
varies on an approximately 8-year cycle, the NAO
affects the temperature and precipitation experi-
enced in North America and Europe, especially in
winter (Stenseth et al. 2003). Not surprisingly, the
NAO has been predicted to have significant effects
on the ecology of north temperate species (Stenseth
et al. 2003). Female great and blue tits from a
number of populations across Europe time their
clutch-initiation in relation to winter NAO index
(Sanz 2002). Although the slope of the relationship
differs between populations, females typically start
laying earlier following warmer, moister winters.
The NAO does not appear to affect clutch size,
which suggests that this climate pattern causes
changes in food phenology in concert with its
effects on egg production.
The relationship of breeding to NAO values for
North American species is starting to emerge
(reviewed in Dunn 1994). Preliminary analysis of
black-capped chickadees nesting in eastern
Ontario, Canada, reveals a somewhat similar pat-
tern to the European data: clutch initiation dates
over 7 years, from 1994 to 2001, showed a strong
relationship with May NAO values (Fig. 5.4;
r2 0.8431, p 0.0035). Unlike the European
results, clutch size was related to winter NAO
values (negative contributions of October,
64 B E H AV I O R A N D E V O L U T I O N
18
15
Mean first egg (1 May = 1)
12
0 Oscillation (NAO) index values and average clutch initiation
2 1 0 1
May NAO Index
December, and March NAO values, and positive
contributions of January and February NAO values
over nine breeding seasons; stepwise multiple
regression, whole model r2 0.9957, p 0.0010).
We treat these results with some caution as our data
span just a single NAO cycle; however, we consider
them ample evidence to justify further study.
5.5.2 Directional climatic variation
Over the last three decades, English great tits have
advanced their laying dates in association with
warming spring temperatures (McCleery and
Perrins 1998); the laying date in this population cor-
relates with the sum of daily maximum tempera-
tures over March and April which has increased
over the same period. Two decades of breeding
data from 24 populations of great and blue
tits revealed complex responses to climate
change (Visser et al. 2003). Overall, both species
have shown earlier laying, although there are
some exceptions where no change or delays have
occurred. The strength of the breeding advance
varies among populations regardless of their prox-
imity to one another. The warmer temperatures and
earlier laying have also led to an increase in the
frequency of second broods.
In one Dutch population of great tits, clutch initi-
ation has not changed over a 23-year period despite
Figure 5.4 The relationship between May North Atlantic
2 dates from 1994 to 2001 for a population of black-capped
chickadees breeding in eastern Ontario, Canada.
warmer spring temperatures, but the phenology of
caterpillars has advanced leading to mistiming
between offspring demand and food availability
(Visser et al. 1998). These results reveal the conflicting
selection pressures that females face when they begin
nesting. On the one hand, food and energy require-
ments restrict when females may begin laying, yet the
availability of caterpillars will determine the success
of rearing offspring (Visser et al. 2004). This difference
is predicted to lead to effects for both individuals and
whole populations. For individuals, selection may
favor advanced clutch initiation, reduced clutch sizes,
advanced onset of incubation, or some combination
of the three (Visser et al. 2004). At the population level,
the enhanced success of early broods should lead to
the evolution of earlier laying dates as long as there is
sufficient heritable variation among females to
respond (Visser et al. 2004). The evidence from French
blue and coal tits suggests that, at least in the past,
populations have had the capacity to evolve repro-
ductive responses to local forest phenology (Blondel
1985; see above). Finally, selection may favor reduced
phenotypic plasticity in females in response to the
mistiming (Visser et al. 2004). Continued long-term
studies will be required to reveal which of these
responses occurs.
Alternately, female may simply be limited in
their ability to adjust clutch initiation, resulting
from constraints imposed by the mechanisms

that control timing. The control of timing is
hierarchicalcontrolled at a coarse level by
photoperiod, and fine-tuned by temperature and
food availability as noted above. However, if
temperature cues are advanced, their effect may be
restricted by stabilizing selection acting on
photosensitivity, the primary cue stimulating
reproductionalthough French blue tits offer
evidence of the ability of nearby populations to
evolve different responses to photoperiod
(Lambrechts et al. 1997). Adjustment on a fine scale
through the effects of temperature on prey
development may allow females only limited
opportunities to better time clutches. Black-capped
chickadees in our northern BC population
faced a spring where high April temperatures
advanced tree phenology by 3 weeks in 2004.
Chickadees advanced laying by nearly a week
compared to prior years, but this still may have
been insufficient to compensate for the unusually
early springmore than 51% of monitored pairs
abandoned nesting attempts in this year (see
Chapter 17).
5.6 Reproductive timing in males
Research in a variety of species has focused on the
relationship between female reproductive syn-
chrony and extrapair mating. Because of its poten-
tial to enhance the reproductive success of males
beyond the number of eggs laid by their social
partners, variation in the timing of female fertility
may be an important determinant of the timing of
male fertility; however, the evidence for any rela-
tionship between reproductive synchrony and
extrapair mating in tits is mixed. There was no rela-
tionship between synchrony index and extrapair
paternity in blue tits (Kempenaers 1997; Krokene
and Lifjeld 2000; Charmantier and Blondel 2003) or
black-capped chickadees (Mennill et al. 2004). By
contrast, in great tits the difference in laying dates
between females was positively related to the
number of EPY in a nest (i.e. females that laid early
compared to the mates of their extrapair partners
had fewer EPY than later-laying females; Strohbach
et al. 1998).
A few studies have looked at the effects of
ecological factors on the timing of male fertility in
TIMING OF REPRODUCTION 65
Parids. An early study of great and blue tits
revealed that the timing of seasonal gonad devel-
opment is related to annual variation of spring
temperatures (Marshall 1949). This result was
further supported by an experiment that showed
temperature moderating the rate of testis
development in willow tits and circulating levels of
luteinizing hormone in great tits over and above
the effects of photoperiod manipulation (Silverin
and Viebke 1994). The timing of birch bud burst
had a significant effect on circulating levels of
luteinizing hormone but not testosterone or
gonadal development in captive Swedish great tits
(Visser et al. 2002). In a study of male Corsican
blue tits, singing activity, circulating levels of
testosterone, and testis development showed the
same patterns of local habitat adaptation to
deciduous-oak versus evergreen-oak phenology as
egg-laying in females from the same populations
(Caro et al. 2005); the population breeding in the
deciduous habitat was advanced by approximately
4 weeks compared to the evergreen population due
to the rate, but not the onset, of testis development.
A pilot study on black-capped chickadees in
eastern Canada revealed a rapid increase of cloacal
sperm count in males over the week leading up to
the laying of the first eggs in the population
(Fig. 5.5). More studies are needed to fully
understand the timing of sperm release in natural
populations.
5.6.1 Questions/predictions
What factors beyond photoperiod and weather
control the onset of male fertility? Evidence from
tropical antbirds revealed that the presence of food
is an important fine-tuning stimulus for gonad
development (Hau et al. 2000); perhaps the most
interesting finding from this study was that the
visual presentation of food was sufficient to trigger
testis development.
How is the timing of male fertility in male Parids
related to the timing of egg-laying? Selection
should favor males initiating sperm production
well in advance of female fertility; males that are
late in relation to females will face a number of
potential costs including the production of infertile
eggs and the loss of paternity to neighboring males.
66 B E H AV I O R A N D E V O L U T I O N
15
Ln (Sperm count + 1)
10
21/04/2001
Figure 5.5 Sperm counts in male black-capped chickadees over a 1-week period leading up to clutch initiation by females. Filled symbols
represent the first or only samples from individuals, while open symbols represent second samples. Squares represent males that were
subsequently resampled.
For males to successfully predict the onset of
female fertility, the cues used to time sperm pro-
duction should be correlated with those that time
egg production. With climate change, males may
potentially become mistimed, although the magni-
tude of any decoupling of the cues for the onset of
fertility between males and females is likely to be
less than the mistiming of egg-laying and offspring
demand; the difference between clutch initiation
and peak offspring demand for food is approxi-
mately 40 days, while the difference between sperm
mobilization and egg laying may be as little as
1 week.
Is sperm count related to synchrony among
females? If females are synchronous, then males
may be able to delay sperm release till just before
the onset of female fertility. Conversely, if females
are asynchronous then males should begin sperm
production very early, both to capitalize on possible
EPP benefits, and to avoid lost paternity if their
own partners are early. The ability of males to
respond to female synchrony will depend on the
effects of both genetics and condition on the onset
of male fertility.
23/04/2001 25/04/2001 27/04/2001 29/04/2001
Sample date
5.7 Conclusions
Evidence from a variety of populations of tits
reveals that clutch initiation is determined by a
hierarchy of cues. Photoperiod regulates timing at
the coarsest level, while temperature and food
availability fine tune the onset of egg-laying within
a year. There is ample evidence that females face
costs in a number of fitness components if their
reproduction is not optimally timed. In spite of all
this evidence, some questions remain concerning
the inter-relationships of timing, temperature, and
female quality. In addition, a question that puzzled
Lack (1966)why selection has not weeded out
females that breed lateremains unanswered
today. The current emphasis on the relationship of
female timing to climate change may reveal the
scope of populations to respond to selection for
earlier laying and changing sensitivity to the
relevant cues. Depending on the degree of climate
change over the coming decade, we may be witness
to a natural experiment that has the potential to
lead to widespread population declines (Visser et al.
2003). There is also a shortage of field studies on the

timing of male fertility, both in terms of the degree
of variation among males within populations and
the cost of any variation for individuals.
What has been a productive field of research for
most of the last century promises to continue to be
so, but the contribution of North American species
to our understanding of these issues is still in its
infancy compared to Eurasian tits. Even here, most
of our understanding of factors affecting timing
and breeding comes from blue and great tits, pri-
marily due to the long-term studies of box-nesting
populations. Although the best-studied North
American Parid is the black-capped chickadee, this
species is among the least likely to utilize nest
boxes. While natural-cavity nesting does not
preclude studies on timing, it makes them
more challenging. Capitalizing on Parids that are
predominantly secondary cavity nesters, such as
the mountain chickadee (see Chapter 8), may be
more productive in yielding the long-term data
needed to address these issues.
Acknowledgments
SMR has benefited from many conversations over
the last several years at conferences and invited
lectures that have helped to inspire his thinking on
this topic. H. van Oort, K. Fort, and L. M. Ratcliffe
shared unpublished data from collaborations on
our two study sites. N. Barker helped with
collecting and organizing the reference material
for this chapter. Both SMR and KAO receive
their primary research support from the Natural
Sciences and Engineering Research Council of
Canada.
References
Allander, K. and Bennett, G. F. (1995). Retardation of
breeding onset in great tits (Parus major) by blood para-
sites. Functional Ecology, 9, 677682.
Barba, E., Gil-Delgado, J. A., and Monros, J. S. (1995). The
costs of being late: consequences of delaying great tit
Parus major first clutches. Journal of Animal Ecology, 64,
642651.
Blondel, J. (1985). Breeding strategies of the blue tit and
coal tit (Parus) in mainland and island Mediterranean
habitats: a comparison. Journal of Animal Ecology, 54,
531556.
TIMING OF REPRODUCTION 67
Blondel, J., Dias, P. C., Maistre, M., and Perret, P. (1993).
Habitat heterogeneity and life-history variation of
Mediterranean blue tits (Parus caeruleus). Auk, 110,
511520.
Blondel, J., Perret, P., and Maistre, M. (1990). On the
genetical basis of the laying-date in an island popula-
tion of blue tits. Journal of Evolutionary Biology, 3,
469475.
Caro, S. P., Balthazart, J., Thomas, D. W., Lacroix, A.,
Chastel, O., and Lambrechts, M. M. (2005). Endocrine
correlates of the breeding asynchrony between two
Corsican populations of blue tits (Parus caeruleus).
General and Comparative Endocrinology, 140, 5260.
Charmantier, A. and Blondel, J. (2003). A contrast in
extra-pair paternity levels on mainland and island
populations of Mediterranean blue tits. Ethology, 109,
351363.
Creswell, W. and McCleery, R. (2003). How great tits
maintain synchronization of their hatch date with food
supply in response to long-term variability in tempera-
ture. Journal of Animal Ecology, 72, 356366.
Dhondt, A. A. (1981). Postnuptial moult of the Great tit in
southern Sweden. Ornis Scandinavica, 12, 127133.
Dhondt, A. A. and Adriaensen, F. (1994). Causes and
effects of divorce in blue tit Parus caeruleus. Journal of
Animal Ecology, 63, 979987.
Dhondt, A. A. and Eyckerman, R. (1979). Temperature and
date of laying by tits Parus spp. Ibis 121, 329331.
Dhondt, A. A., Eyckerman, R., and Hubl, J. (1983).
Laying interruptions in tits Parus spp. Ibis, 125, 370376.
Dunn, P. (2004). Breeding dates and reproductive per-
formance. Advances in Ecological Research, 35, 6987.
Eeva, T., Veistola, S., and Lehikoinen, E. (2000). Timing of
breeding in subarctic passerines in relation to food
availability. Canadian Journal of Zoology, 78, 6778.
Gienapp, P. and Visser, M. E. (2006). Possible fitness con-
sequences of experimentally advanced laying dates in
Great Tits: differences between populations in different
habitats. Functional Ecology, 20, 180185.
Grieco, F., van Noordwijk, A. J., and Visser, M. E. (2002).
Evidence for the effect of learning in timing of repro-
duction in blue tits. Science, 296, 136138.
Harrap, S. and Quinn, D. (1995). Chickadees, Tits,
Nuthatches and Treecreepers. Princeton University Press,
Princeton, New Jersey, 464 pp.
Hau, M., Wikelski, M., and Wingfield, J. C. (2000). Visual
and nutritional food cues fine-tune timing of reproduc-
tion in a neotropical rainforest bird. Journal of
Experimental Zoology, 286, 494504.
Kempenaers, B. (1997). Does reproductive synchrony limit
male opportunities or enhance female choice for extra-
pair paternity? Behaviour, 134, 551562.
68 B E H AV I O R A N D E V O L U T I O N
Kluijver, H. N. (1951). The population ecology of the great
tit, Parus m. major. Ardea, 39, 1135.
Kluyver, H. N. (1961). Food consumption in relation to
habitat in breeding chickadees. Auk, 78, 532550.
Krokene, C. and Lifjeld, J. T. (2000). Variation in the fre-
quency of extra-pair paternity in birds: a comparison of
an island and a mainland population of blue tits.
Behaviour, 137, 13171330.
Lack, D. (1966). Population Studies of Birds. Oxford
University Press, Oxford, 341 pp.
Lambrechts, M. M. and Perret, P. (2000). A long photo-
period overrides non-photoperiodic factors in blue tits
timing of reproduction. Proceedings of the Royal Society of
London B, 267, 585588.
Lambrechts, M. M., Blondel, J., Maistre, M., and Perret, P.
(1997). A single response mechanism is responsible for
evolutionary adaptive variation in a birds laying date.
Proceedings of the National Academy of Science USA, 94,
51535155.
Lens, L. and Dhondt, A. A. (1994). Effects of habitat frag-
mentation on the timing of Crested Tit Parus cristatus
natal dispersal. Ibis, 136, 147152.
Lessells, C. M., Dingemanse, N. J., and Both, C. (2002).
Weights, egg component weights, and laying gaps in
great tits in relation to ambient temperature. Auk, 119,
10911103.
Marshall, A. J. (1949). Weather factors and spermatogen-
esis in birds. Proceedings of the Zoological Society of
London, 119, 711716.
McCleery, R. H. and Perrins, C. M. (1988). Lifetime repro-
ductive success of the great tit, Parus major. In: Clutton-
Brock, T. H., ed. Reproductive Success: Studies of
Individual Variation in Contrasting Breeding Systems, pp.
136153. University of Chicago Press, Chicago.
McCleery, R. H. and Perrins, C. M. (1998). . . . temperature
and egg-laying trends. Nature, 391, 3031.
Mennill, D. J., Ramsay, S. M., Boag, P. T., and Ratcliffe,
L. M. (2004). Patterns of extrapair mating in relation to
male dominance status and female nest placement in
black-capped chickadees. Behavioral Ecology, 15,
757765.
Nager, R. G. and van Noordwijk, A. J. (1992). Energetic
limitation in the egg-laying period of great tits.
Proceedings of the Royal Society of London B, 249, 259263.
Nager, R. G. and van Noordwijk, A. J. (1995). Proximate
and ultimate aspects of phenotypic plasticity in timing
of great tit breeding in a heterogeneous habitat.
American Naturalist, 146, 454474.
Nager, R. G., Ruegger, C., and van Noordwijk, A. J. (1997).
Nutrient or energy limitation on egg formation: a feed-
ing experiment in great tits. Journal of Animal Ecology,
66, 495507.
Nilsson, J.- . (1994). Energetic bottle-necks during breed-
ing and the reproductive cost of being too early. Journal
of Animal Ecology, 63, 200208.
Nilsson, J.- . (2000). Time-dependent reproductive deci-
sions in the blue tit. Oikos, 88, 351361.
Nilsson, J.- . and Rberg, L. (2001). The resting metabolic
cost of egg laying and nestling feeding in great tits.
Oecologia, 128, 187192.
Nilsson, J.- . and Svensson, E. (1993). Energy constraints
and ultimate decisions during egg-laying in the blue tit.
Ecology, 74, 244251.
Nilsson, J.- . and Svensson, E. (1996). The cost of repro-
duction: a new link between current reproductive effort
and future reproductive success. Proceedings of the Royal
Society of London B, 263, 711714.
Norris, K. (1993). Seasonal variation in the reproductive
success of blue tits: an experimental study. Journal of
Animal Ecology, 62, 287294.
Odum, E. P. (1941). A comparison of two chickadee sea-
sons. Auk, 13, 154159.
Purcell, K. L., Verner, J., and Oring L. W. (1997). A com-
parison of the breeding ecology of birds nesting in
boxes and tree cavities. Auk, 114, 646656.
Ramsay, S. L. and Houston, D. C. (1997). Nutritional con-
straints on egg production in the blue tit: a supplemen-
tary feeding study. Journal of Animal Ecology, 66,
649657.
Ramsay, S. M. and Ratcliffe, L. M. (2003). Determinants of
social rank in female black-capped chickadees (Poecile
atricapilla). Canadian Journal of Zoology, 81, 117121.
Rowe, L., Ludwig, D., and Schluter D. (1994). Time, con-
dition, and the seasonal decline of avian clutch size.
American Naturalist, 143, 698722.
Sanz, J. J. (1999). Seasonal variation in reproductive suc-
cess and post-nuptial moult of blue tits in southern
Europe: an experimental study. Oecologia, 121, 377382.
Sanz, J. J. (2002). Climate change and breeding parameters
of great and blue tits throughout the western Palearctic.
Global Change Biology, 8, 409422.
Seki, S.-I. and Takano, H. (1998). Caterpillar abundance in
the territory affects the breeding performance of great
tit Parus major major. Oecologia, 114, 514521.
Silverin, B. and Viebke, P. A. (1994). Low temperatures
affect the photoperiodically induced LH and testicular
cycles differently in closely related species of tits (Parus
spp.). Hormones and Behavior, 28, 199206.
Smith, H. G. (1993). Seasonal decline in clutch size of the
marsh tit (Parus palustris) in relation to date specific sur-
vival of offspring. Auk, 110, 889899.
Smith, S. M. (1991). The Black-Capped Chickadee: Behavioral
Ecology and Natural History. Cornell University Press,
Ithaca, NY.

Stenseth, N. C., Ottersen, G., Hurrell, J. W., Mysterud,
A., Lima, M., Chan, K.-S., Yoccoz, N. G., and
dlandsvik, B. (2003). Studying climate effects on
ecology through the use of climate indices: the North
Atlantic Oscillation, El Nio Southern Oscillation and
beyond. Proceedings of the Royal Society of London B, 270,
20872096.
Strohbach, S., Curio, E., Bathen, A., Epplen, J. T., and
Lubjuhn, T. (1998). Extrapair paternity in the great tit
(Parus major): a test of the good genes hypothesis.
Behavioral Ecology, 9, 388396.
Svensson, E. (1997). Natural selection on avian breeding
time: causality, fecundity-dependent, and fecundity-
independent selection. Evolution, 51, 12761283.
Svensson, E. and Nilsson, J.-. (1995). Food supply, terri-
tory quality, and reproductive timing in the blue tit
(Parus caeruleus). Ecology, 76, 18041812.
Thomas, D. W., Blondel, J., Perret, P., Lambrechts, M. M.,
and Speakman, J. R. (2001). Energetic and fitness costs
of mismatching resource supply and demand in sea-
sonally breeding birds. Science, 291, 25982600.
van der Jeugd, H. P. and McCleery R. (2002). Effects of
spatial autocorrelation, natal philopatry and pheno-
typic plasticity on the heritability of laying date. Journal
of Evolutionary Biology, 15, 380387.
van Noordwijk, A. J. and van Balen, J. H. (1988). The great
tit, Parus major. In: Clutton-Brock, T. H., ed. Reproductive
Success: Studies of Individual Variation in Contrasting
Breeding Systems, pp. 119135. University of Chicago
Press, Chicago.
van Noordwijk, A. J., McCleery, R. H., and Perrins, C. M.
(1995). Selection for the timing of great tit breeding in
relation to caterpillar growth and temperature. Journal
of Animal Ecology, 64, 451458.
van Noordwijk, A. J., van Balen, J. H., and Scharloo, W.
(1981). Genetic variation in the timing of reproduction
in the great tit. Oecologia 49, 158166.
Verboven, N. and Verhulst, S. (1996). Seasonal variation in
the incidence of double broods: the date hypothesis fits
TIMING OF REPRODUCTION 69
better than the quality hypothesis. Journal of Animal
Ecology, 65, 264273.
Verboven, N. and Visser, M. E. (1998). Seasonal variation
in local recruitment of great tits: the importance of
being early. Oikos, 81, 511524.
Verhulst, S. and Tinbergen, J. M. (1991). Experimental evi-
dence for a causal relationship between timing and suc-
cess of reproduction in the great tit Parus m. major.
Journal of Animal Ecology, 60, 269282.
Verhulst, S., van Balen, J. H., and Tinbergen, J. M. (1995).
Seasonal decline in reproductive success of the great tit:
variation in time or quality? Ecology, 76, 23922403.
Visser, M. E., Adriaensen, F., van Balen, J. H., Blondel, J.,
Dhondt, A. A., van Dongen, S., du Feu, C., Ivankina, E.
V., Kerimov, A. B., de Laet, J., Matthysen, E., McCleery,
R., Orell. M., and Thomson, D. L. (2003). Variable
responses to large-scale climate change in European
Parus populations. Proceedings of the Royal Society of
London B, 270, 367372.
Visser, M. E., Both, C., and Lambrechts, M. M. (2004).
Global climate change leads to mistimed avian repro-
duction. Advances in Ecological Research, 35, 89110.
Visser, M. E., Silverin, B., Lambrechts, M. M., and
Tinbergen, J. M. (2002). No evidence for tree phenology
as a cue for the timing of reproduction in tits Parus spp.
Avian Science, 2, 7786.
Visser, M. E., van Noordwijk, A. J., Tinbergen, J. M., and
Lessells, C. M. (1998). Warmer springs lead to mis-timed
reproduction in great tits (Parus major). Proceedings of the
Royal Society of London B, 265, 18671870.
Williams, T. D. (2005). Mechanisms underlying the costs
of egg production. BioScience, 55, 3948.
Wingfield, J. C., Hahn, T. P., Levin, R., and Honey, P.
(1992). Environmental predictability and control of
gonadal cycles in birds. Journal of Experimental Zoology,
261, 214231.
Yomtov, Y. and Wright, J. (1993). Effect of heating nest
boxes on egg-laying in the blue tit (Parus caeruleus). Auk,
110, 9599.
This page intentionally left blank
 SYNOPSIS I
Proximate mechanisms in behavior
and evolution
David F. Sherry, Vladimir V. Pravosudov,
Scott A. MacDougall-Shackleton, Jennifer S. Hoshooley,
and Leslie S. Phillmore
Chickadees and tits have long been known as
highly tractable subjects for research in behavior
and ecology. Studies of Eurasian tits and North
American chickadees have made substantial
contributions to our understanding of breeding
phenology (Chapter 4; Chapter 5), food-storing
(Chapter 2; Chapter 3), social behavior (Chapter 9),
communication (Section III), foraging, and other
topics. More recently, research on the Paridae has
begun to address questions about the proximate
neural and neuroendocrine causes of behavior.
There are many reasons for the intense focus on
these small, familiar birds. Most Parids are rela-
tively tame, year-round residents that live in small
home ranges and are easily attracted to feeders.
Some, such as great and blue tits, readily breed in
artificial nest boxes (though the most intensely
studied North American Parid, the black-capped
chickadee tends not to). These traits make it
possible, at least in principle, to obtain complete
observations on development, social organization,
communication, and reproduction in individually-
marked birds over their entire lifetime. In both
North America and Eurasia there are enough
species to permit comparative analyses, and some
species, such as the black-capped chickadee, have
distributions large enough to permit comparisons
between populations living in very different
environmental conditions (Chapters 3 and 5).
Most chickadees and tits thrive in captivity. Early
in the 1700s Baron von Pernau kept marsh tits in
his room to observe their food-storing behavior
(Stresemann 1947). The ease of holding birds in
captivity has made possible a great deal of research
on behavior, cognition, and neurobiology in species
for which there is extensive information on behav-
ior in the wild (Chapters 2, 3, and 4). The integra-
tion of field and laboratory work has, for example,
led to advances in research on control of the annual
cycle. Although temperature, food supply, and
other factors exert important effects on the timing
of reproduction, photoperiod is the stimulus that
initiates the sequence of events leading to gonadal
recrudescence, mating, egg laying, and parental
care. These behavioral and physiological changes
are not, strictly, controlled by day-length but
instead, as Phillmore and MacDougall-Shackleton
describe, by an annual cycle in sensitivity to day-
length. Successive stages of photorefractoriness
and photosensitivity prepare birds to respond to
increasing day-length in spring and initiate
breeding. These responses include change in size of
the song control nuclei HVC and RA, and the
recruitment of new neurons into these structures.
Some recent research also shows an annual pattern
in the recruitment of new neurons into the
hippocampus and change in the overall size of this
structure, but data from different studies have not
been consistent. There are different opinions about
the function of such patterns (Chapter 3) and
seasonal change in the hippocampus continues to
be a topic of active investigation.
Remarkably, for both the song control nuclei
and the hippocampus, laboratory and field studies
71
72 B E H AV I O R A N D E V O L U T I O N
present rather different pictures. Change in the
size of song control nuclei can be produced in the
laboratory by manipulating photoperiod but is not
found in samples of birds taken from the wild at
different times of year. In contrast, change in the
size of the hippocampus has been found in samples
of birds collected in the field but does not occur
when photoperiod is manipulated in the laboratory.
There are a number of possible explanations for
these seemingly contradictory outcomes, discussed
by Phillmore and MacDougall-Shackleton in
Chapter 4. These results illustrate, however, one of
the significant challenges for research on chicka-
dees and tits, and other passerines, as well. In
many field studies, samples are collected from
wild populations at different times in order to
understand changes occurring over time within
individuals. The conclusion that change in a
temporal series of samples represents change
within a typical individual is, however, an infer-
ence. When annual change is observed in samples
collected in the wild, as is the case for hippocampal
size, the observed change may occur not because of
annual change within individuals but because of
demographic changes in the population from
which the samples are drawn (Chapter 3). In the
laboratory, control over diet, housing, temperature,
and the timing of experimental manipulations may
make it possible to detect annual change within
individuals, for example in the song control nuclei,
that is masked in samples collected from the wild
because individuals undergo annual change out of
phase with each other or exhibit other individual
differences (Chapter 4).
The many influences on behavior and physiology
in the wild may lead to a more complex determin-
ation of events such as the timing of laying than
might be suspected from laboratory studies. As
Ramsay and Otter (Chapter 5) describe, there is
considerable variation among females in the timing
of laying, which probably reflects variation in the
ability to obtain the resources for egg production,
heritable and perhaps adaptive variation in
response to environmental cues, and exposure to
varying environmental conditions. Although a
great deal is known about factors that influence
the timing of laying in females, there has been
much less work, as Ramsay and Otter describe
(Chapter 5), on fertility in males, who are exposed
to the same environmental cues as females but face
the problem not of timing hatch to the peak in
insect food for the young but timing sperm produc-
tion to the peak in female fertility.
As a buffer against environmental variation in
food availability, many chickadees and tits, though
not all, have available to them the tactic of food
storing. A food-storing chickadee can create many
thousands of food caches over the fall and winter
and these caches make an important contribution to
over-winter survival. Caches are widely scattered
over the birds home range and chickadees and tits
have been shown to retrieve stored food by remem-
bering where they put it. Remembering large num-
bers of scattered spatial locations for up to several
weeks is a striking cognitive achievement and a
great deal of recent research, described by Sherry
and Hoshooley (Chapter 2), has investigated
exactly how chickadees and tits manage this feat.
Controlled studies tend to show that chickadees
and tits are sometimes not much better than other
birds at laboratory spatial memory tasks. What
chickadees and tits do possess is a predisposition to
solve problems spatially, rather than by using non-
spatial cues such as color or form. Food-storing
birds, including Parids, also have a hippocampus
that is dramatically larger relative to the size of the
rest of the brain than the hippocampus of non-
storing birds such as thrushes, sparrows, and wood
warblers. The hippocampus is a forebrain structure
found in both birds and mammals and is known to
play a role in a variety of cognitive functions,
including spatial memory (Chapter 2). The
enlarged hippocampus of food-storing birds may
thus provide new information on the evolution of
the brain and the neural basis of spatial cognition.
Despite a great deal having been learned about
the behavior and brain of food-storing Parids,
much basic information remains tantalizingly out
of view. As Pravosudov (Chapter 3) points out,
there is little solid evidence on the exact annual
pattern of food storing in chickadees. There is
conflicting evidence about how long chickadees
leave their caches in place before retrieving them,
and, as noted above, about seasonal changes in the
brain of food-storing chickadees. There is current
debate over whether differences in the size of the

hippocampus that occur between food-storing and
non-storing families of birds (Krebs et al. 1989;
Sherry et al. 1989) occur within families like the
Paridae that contain both storing and non-storing
species (Brodin and Lundborg 2003; Garamszegi
and Eens 2004; Lucas et al. 2004; Garamszegi and
Lucas 2005). There is also controversy over whether
recently reported differences between North
American and European Parids in the relative size
of the brain and hippocampus (Lucas et al. 2004;
Garamszegi and Lucas 2005) are simply the result
of procedural differences between laboratories
(Pravosudov and de Kort 2006) or the consequence
of differences in life history traits (Garamszegi and
Lucas 2005). Research on food storing would bene-
fit enormously from an omniscient glimpse of just
one annual cycle of the caching activity of the mem-
bers of a single, winter flock of chickadees and the
fate of the food they stored. Better make that ten
annual cycles, to deal with year-to-year variation in
seed and insect abundance, flock demographics,
weather, habitat change, and other factors that
influence food storing behavior. Short of such
omniscience, however, a clearer partial picture of
food caching in the wild would still be invaluable.
As with the discovery of large capacity long-
lasting spatial memory in food-storers, research on
the Parids continues to uncover new and unex-
pected properties of proximate mechanisms of
behavior. Research described by Pravosudov
(Chapter 3) on the influence on memory of
corticosteronean adrenal steroid that plays an
important role in energy metabolism, stress and
immune functionis a good example. Unlike
previous results, which tend to show a positive
effect on memory of acute corticosterone elevation
and a negative effect of chronic elevation, mountain
chickadees show a positive effect on spatial
memory of prolonged, moderate corticosterone
elevation.
The future of research on proximate mechanisms
of behavior will surely lie in controlled laboratory
studies of the neural and neuroendocrine causes of
TIMING OF REPRODUCTION 73
behavior. Along with the control and repeatability
of laboratory research, however, comes the risk of
losing touch with the natural history of behavior
that both inspires new questions about proximate
mechanisms (Sherry 2005) and grounds studies of
causation with reliable information about how
chickadees behave in the wild. Field studies remain
the indispensable source of new questions about
the Paridae and the raison dtre for bringing to
bear the powerful techniques of laboratory
research.
References
Brodin, A. and Lundborg, K. (2003). Is hippocampus
volume affected by specialization for food hoarding in
birds? Proceedings of the Royal Society London B, 270,
15551563.
Garamszegi, L. Z. and Eens, M. (2004). The evolution of
hippocampus volume and brain size in relation to food
hoarding in birds. Ecology Letters, 7, 12161224.
Garamszegi, L. Z. and Lucas, J. R. (2005). Continental
variation in relative hippocampal volume in birds: the
phylogenetic extent of the effect and the potential role
of winter temperatures. Biology Letters, 1, 330333.
Krebs, J. R., Sherry, D. F., Healy, S. D., Perry, V. H., and
Vaccarino, A. L. (1989). Hippocampal specialization of
food-storing birds. Proceedings of the National Academy of
Sciences USA, 86, 13881392.
Lucas, J. R., Brodin, A. de Kort, S. R., and Clayton, N. S.
(2004). Does hippocampal size correlate with the degree
of caching specialization? Proceedings of the Royal Society
London B, 271, 24232429.
Pravosudov, V. V. and de Kort, S. R. (2006). Is the western
scrub-jay (Aphelocoma californica) really an underdog
among food-caching corvids when it comes to
hippocampal volume and food caching propensity?
Brain Behavior and Evolution, 67, 19.
Sherry, D. F. (2005). Do ideas about function help in the
study of causation? Animal Biology, 55, 441456.
Sherry, D. F., Vaccarino, A. L., Buckenham, K., and Herz,
R. S. (1989). The hippocampal complex of food-storing
birds. Brain Behavior and Evolution, 34, 308317.
Stresemann, E. (1947). Baron von Pernau, pioneer student
of bird behavior. Auk, 64, 3552.
This page intentionally left blank
 SECTION II
Reproductive ecology, evolution,
and behavior
Reproductive studies on Eurasian Parids have
traditionally focused on topics that arise from the
ability to induce large numbers of individuals to
nest in easily accessible boxes, such as optimum
clutch sizes, reproductive success, and reproductive
timing in relation to abiotic factors (see Chapter 5).
Fewer long-term research programs have been
initiated on chickadees and titmice, possibly due to
the greater difficulty in establishing box-nesting
populations with the same high-density breeding
potential exhibited by great and blue tits. While
long-term studies on natural-cavity-nesting Parids
are increasing, research on North American Parids
has tended to focus on the topics of intra and inter-
specific interactions and their influence on repro-
ductive ecology, evolution, and behavior. Whereas
the previous section of this book focused on the
extrinsic and intrinsic factors that affect behaviors,
including reproduction, it is the influence of social
interactions between and within species that form
the basis for grouping chapters in this section.
Typically, North American Parids have more
parapatric distributions than Eurasian Parids.
In these isolated circumstances, intraspecific
interactions may influence reproduction to a great
extent, as is evident by the work presented
by Ratcliffe, Mennill, and Schubert on social
dominance and reproductive potential in black-
capped chickadees (Chapter 9). Ratcliffe et al. use a
10-year data set of black-capped chickadees to
determine the influence of relative position in the
dominance hierarchy within wintering flocks on
the lifetime reproductive potential of individual
birds. Where sympatric populations are found,
interspecific interactions and hybridization poten-
tial add to the complexity of studying Parid repro-
ductive ecology (Chapter 7). Curry, Rossano, and
Reudink assess hybridization in the black-capped/
Carolina chickadee hybrid zone using genetic
markers and behavioral isolating mechanisms,
often finding little congruence between these two
means of characterizing species.
In contrast to interspecific overlap, isolation of
populations and speciation is an exciting avenue of
research on North American species, and has
potential among the groups of sister species that
have recently undergone taxonomic splits (see
Preface). Burg (Chapter 6) assesses the biogeog-
raphy of chestnut-backed chickadees using
microsatellite analysis, providing alternative scen-
arios for the glacial refugia and dispersal patterns
that could explain the present distribution of dis-
tinct, genetic populations. This chapter also consid-
ers the potential for hybridization within the
brown-capped chickadees to contribute to differen-
tiation among disjunct populations within the
chestnut-backed chickadees of northwestern
Canada and Alaska.
75
76 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

Even where hybridization may be limited, inter-
specific interactions of chickadees extends beyond
the Parid family, as these cavity-nesting species are
part of a larger guild of birds and mammals that are
primary or secondary cavity users (Nest Webs).
Martin and Norris (Chapter 8) examine the
influence of prey availability and interspecific inter-
actions on the population dynamics of mountain
chickadees in central British Columbia, especially in
light of an unprecedented epidemic of mountain
pine beetle in the region. Being primarily a second-
ary-cavity user rather than an excavating species,
the interaction between prey cycles and population
levels of other facilitating species, such as wood-
peckers, in these Nest Webs creates an intricate pic-
ture of interdependence in these communities.
 CHAPTER 6
Phylogeography of chestnut-backed
chickadees in western North America
Theresa M. Burg
6.1 Introduction
North American chickadees and titmice are
believed to be descendents of Eurasian lineages
that crossed the Bering land bridge in the late
Pliocene 3.5 to 4 million years ago (Gill et al. 2005;
see also Chapters 1 and 2). The North American
chickadees are divided into two groups based on
phenotypic differences (references in Gill et al.
1989). The black-capped group contains four
species: black-capped, Carolina, Mexican, and
mountain chickadees. As their name suggests, these
have a black-cap and morphologically they are
most similar to the Eurasian species in the Poecile
clade, particularly the willow tit. The brown-
capped group contains three species: boreal, chest-
nut-backed chickadees, and the Siberian tit. In
North America, Siberian tits are only found in the
northwestern Arctic and are considered by some to
be a distinct subspecies (gray-headed chickadee,
Sibley 2000). Birds of the brown-capped group have
brownish head feathers and a rusty colored back.
Several studies attempted to determine the phylo-
genetic relationship of Parids (Gill et al. 1989, 1993,
2005). Gill et al. (1989) using allozymes tentatively
concluded that the brown-capped and black-
capped groups were more similar to each other
than to any of the Eurasian lineages, and chestnut-
backed and boreal chickadees were closely related
as were Mexican and mountain chickadees. A
chromosomal rearrangement found in both Mexican
and mountain chickadees adds support to the
allozyme data (unpublished data cited in Gill et al.
1989). The two subsequent phylogenies employed
mitochondrial DNA (mtDNA) (Gill et al. 1993,
2005phylogeny reprinted earlier in this book, see
Fig. 2.1). The mtDNA restriction data placed the
Mexican chickadee within the brown-capped group
while phylogenies using mtDNA sequence data
showed the three brown-capped species as a mono-
phyletic clade nested within the black-capped
clade. Based on standard mtDNA divergence rates
of 2%/MY (million years), it appears that speci-
ation in the North American chickadees occurred
during the late Pliocene or early Pleistocene
(Gill et al. 1993, 2005). While any such dates are
approximate, and debated, the timing corresponds
with Pleistocene divergence of other avian taxa,
especially boreal species (e.g. Johnson and Cicero
2004; Weir and Schluter 2004; Lovette 2005).
The Pleistocene glaciations were influential in
shaping the population structure of many species,
particularly those now inhabiting temperate and
polar regions. Most of Canada and parts of the
northern United States were covered under thick
sheets of ice (Pielou 1991). Three main ice sheets
were present during the Pleistocene: Cordilleran
(west of Rocky Mountains), Innuitian (Arctic) and
Laurentide (east of Rocky Mountains: Pielou 1991;
Dyke et al. 2002). The glaciers expanded and
contracted during the alternating cold glacial and
warm interglacial periods creating a dynamic
environment for species living at the edges of the
glaciers. Populations became fragmented and
subsequently accrued genetic differences. As the
glaciers retreated, some of these allopatric popula-
tions merged, while others remained separated.
This chapter focuses on factors influencing the
contemporary patterns of population structure in
77
78 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

chestnut-backed chickadees including historical

range expansion, geographic distribution and dis-
cuss potential barriers to dispersal. I then compare
the patterns found in this western North American
species to other North American and Eurasian
Parids.

cAK
6.2 Chestnut-backed chickadees
6.2.1 Origin AA
Grinnell (1904) hypothesized that the chestnut-
backed chickadee diverged from the boreal chicka- QCI NBC
dee in the arid interior of Alaska from a
pre-hudsonicus ancestor. Chestnut-backed chicka-
dees colonized the more humid, coastal regions of
SEBC
Alaska and British Columbia expanding south VI
along the coast to California. Boreal chickadees are
found throughout most of Canada, but are rarely
found along the Pacific Coast. The coastal moun- MtR
tain ranges in British Columbia and Alaska form OR
the western and eastern range limits of the boreal
and coastal chestnut-backed chickadees, respect-
ively. In south-eastern British Columbia, the range
of the interior chestnut-backed chickadee (Fig. 6.1)
overlaps with that of the boreal chickadee. Genetic
studies by Gill et al. (1993, 2005) and Weir and
Schluter (2004) support the hypothesis that chest-
nut-backed and boreal chickadees are sister species
having diverged in the early Pleistocene
(~1.8 MYA). Given the contemporary distribution
of these two species, it is possible that chestnut-
backed chickadees originated in the north and
spread southward (Grinnell 1904). Figure 6.1 Distribution of chestnut-backed chickadees in western
North America. Species range is indicated by dashed lines. Sampling
sites include coastal, mainland Alaska (cAK, n 44), Alexander
6.2.2 Biogeography Archipelago (AA, n 9), Queen Charlotte Islands (QCI, n 43),
northern British Columbia (NBC, n 38), Vancouver Island (VI,
The chestnut-backed chickadee is a year-round resi- n 40), North Cascades Park (NCP, n 21), Mount Rainier (MtR,
dent of mature coniferous forests on the west coast n 16), Oregon (OR, n 8) and south-eastern British Columbia
(SEBC, n 30). The star represents 1904 Coeur dAlene, ID
of North America. Chestnut-backed chickadees are population (Grinnell 1904). Solid lines separate genetically distinct
the only Parid found on the larger coastal islands populations as determined by differences in allele frequency
off the British Columbia coast. On the mainland, distributions (see Table 6.1).
their distribution overlaps with black-capped and
mountain chickadees; however, it appears that they
do not directly compete for resources due to niche black-capped chickadee forages in deciduous trees
partitioning (Smith 1967; Sturman 1968; Brennan (Campbell et al. 1997). In California, where the
et al. 1999, 2000). The chestnut-backed chickadee chestnut-backed chickadee recently expanded its
forages in the canopy of conifers while the range into that of the mountain chickadee, the

chestnut-backed chickadees nest in denser forests
and forage on Douglas fir (Pseudotsuga menziesii)
and black oak (Quercus kelloggii) while mountain
chickadees nest in more open sites and forage on
Ponderosa (Pinus ponderosa) and sugar pine (P. lam-
bertiana) and white fir (Abies concolor) (Brennan et al.
1999, 2000). Chestnut-backed chickadees are found
in cedarhemlock forests in the Pacific Northwest
and nest in cavities of old trees, with breeding pairs
defending relatively large territories (Carey et al.
1991). However, during the winter months chest-
nut-backed chickadees can be seen in mixed species
flocks with red-breasted nuthatches (Sitta canaden-
sis), bushtits (Psaltriparus minimus), kinglets
(Regulus spp.), brown creepers (Certhia americana),
and other species of chickadee, such as boreal,
black-capped, or mountain, depending on the
region (Campbell et al. 1997).
Three subspecies of chestnut-backed chickadee
occur in western North America: P. r. rufescens
(Alaska to central California), P. r. neglectus (Point
Arena to San Francisco Bay, California) and P. r. bar-
lowi (San Francisco to Monterey, California)
(Dahlsten et al. 2002). The distribution of this
species follows closely that of the mesic temperate
forests (cedarhemlock), inhabiting a narrow band,
less than 200 km wide, along the Pacific Coast from
California north to Alaska, with a disjunct popula-
tion in the western Rocky Mountains of the Pacific
Northwest (Fig. 6.1). Both coastal and interior
populations appear to have experienced range
expansions in the last 100 years (Grinnell 1904;
Dahlsten et al. 2002). In the last 55 years, the coastal
population has undergone a rapid range expansion
into the Sierra Nevada Mountains of central
California (Brennan and Morrison 1991). A narrow,
inland strip of forest, more than 500 km, was
colonized in less than 50 years, demonstrating the
ability of chestnut-backed chickadees to rapidly
colonize new habitat (Fig. 6.1). It is hypothesized
that the expansion corresponded to forest regener-
ation following widespread logging. The forests
now contain a large amount of Douglas fir, a key
component of the chestnut-backed chickadee
habitat, and the current distribution of the
chestnut-backed chickadee in the Sierra Nevada
Mountains corresponds almost exactly to that of the
Douglas fir (Brennan and Morrison 1991). A second
PHYLOGEOGRAPHY 79
range expansion may have occurred in the interior,
mainly in Idaho and south-eastern BC. Descriptions
of the interior populations are limited; Grinnell
(1904) found two sites near Coeur dAlene, ID
(Fig. 6.1), however, the current distribution is
much larger (approx. 200 km2: Grinnell 1904;
Dahlsten et al. 2002). Other surveys in the early
1900s reported an abundance of chestnut-backed
chickadees west of the Cascades, but very few
sightings east of the Cascades (Bowles 1909; Brooks
and Swarth 1925).
The limited amount of information available
regarding individual movements of chestnut-
backed chickadees suggests that short distance
dispersal does occur. Banding data show that of the
97 recoveries made from 1929 to 2003, all but five
birds were recovered at the location where they
were banded (Bird Banding Lab). The five birds
that were recovered away from their original
banding site had moved 12 to 56 km. All of these
movements took place between the breeding and
non-breeding seasons or during the fall, when
limited movement is known to occur, however no
evidence of dispersal during the breeding season
has been found (Campbell et al. 1997).
6.3 Patterns of contemporary
population structure
6.3.1 Chestnut-backed chickadee
Microsatellite analyses revealed the presence of
four genetically distinct populations of chestnut-
backed chickadees in western North America:
Queen Charlotte Islands, south-eastern British
Columbia, mainland Alaska, and a large coastal
group (Box 6.1; Fig. 6.1). The levels of genetic
differentiation among the four groups are low, but
significant (Table 6.1). Individuals from each of
the four groups showed higher affinity to other
individuals in the same group than to individuals
from other groups (Fig. 6.2). The Queen Charlotte
Island and central Alaska populations are distinct,
and they appear as each others closest genetic
neighbors in factorial correspondence analysis
(FCA, Fig. 6.2) and analyses of allele frequency
distribution (Burg et al. 2006). The Oregon popula-
tion shows significant differences from Alaska,
80 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
Box 6.1 Samples and genotyping
The sampling area covers the majority of the
contemporary range of chestnut-backed
chickadee P. rufescens, including the disjunct
population in the western Rocky Mountains. A
total of 249 samples were collected from nine
populations in Alaska, British Columbia,
Washington, and Oregon (Fig. 6.1). The
populations sampled in Washington and
Oregon are from areas believed to have been
unglaciated during the Pleistocene. Blood
samples were collected from 223 individuals
during the summer of 2002 and 2003. Birds were
caught using mist nets, and blood was taken from
the brachial vein, dried on filter paper and stored
in individual plastic bags. Twenty six samples
(Alaska, n 6; Alexander Archipelago, n 9;
Oregon, n 1; and Queen Charlotte Islands,
n 10) were obtained from the University of
Alaska Museum.
DNA was extracted using standard proteinase
K/phenol chloroform extraction followed by
ethanol precipitation (Sambrook et al. 1989).
Seven microsatellite primer pairs isolated from
other passerine species were used for genotyping
(for details on primers and PCR amplification see
Burg et al. 2006). Alleles were scored using
GeneImagIR (Scanalytics) and sizing was
confirmed by visual inspection.
Statistical analyses
Tests for departures from HardyWeinberg
equilibrium (HWE) and for linkage disequilibrium
were examined using exact tests (Guo and
Thompson 1992) as implemented in GENEPOP
v3.3 (Raymond and Rousset 1995b) and
sequential Bonferroni corrections for multiple tests
were applied (Rice 1989). As estimates of allelic
diversity can be biased due to unequal samples
sizes, allelic richness was estimated using FSTAT
v2.9.3.2 (Goudet et al. 2001).
Of the standard statistical methods for testing
population differentiation, allelic goodness of fit
tests are the most powerful for detecting
population structure when sample sizes are
unequal (Goudet, 1996). TFPGA v1.3 was used to
test for differences in allele frequencies among
populations (1000 dememorization steps,
20 batches, and 20 000 permutations/batch,
Miller 1997). TFPGA uses a Markov chain Monte
Carlo (McMC) approximation of Fishers exact
test (Raymond and Rousset 1995a) and
significance values are combined across all loci
(Fisher 1954).
Relative measures of differentiation can be
difficult to compare directly (Hedrick 1999). The
genotype likelihood ratio distance (DLR, Paetkau
et al. 1997) is well suited to studying fine-scale
population structure and has lower variance than
other distance measures (Paetkau et al. 1997). DLR
is the likelihood of a genotype from one
population being identical to a genotype in
another population. When DLR 1, the genotypes
of individuals from the two populations being
compared are one order of magnitude more likely
to occur in the individuals own population than
in the other population (Paetkau et al. 1997). DLR
was calculated in Doh (http://biodb.biology.
ualberta.ca/jbrzusto).
A factorial correspondence analysis (FCA) was
performed to aid in visualization of the patterns
of genetic structure using GENETIX 4.02
(Belkhir et al. 2000). FCA uses individual
genotypic data to quantify the amount of
inertia among populations. The global
inertia is proportionally weighted relative to
sample size and the total number of alleles
present in each sample. The centre of gravity
or combined distribution of all individuals in each
population was plotted in three-dimensional
space.
Tests for isolation by distance allow us to
evaluate the relative historical roles of gene flow
and drift on population structure by comparing
expected pairwise genetic and geographic
distances with those expected under a stepping-
stone model of population structure (Hutchison
and Templeton 1999). They also allow us to
determine if gene flow is affected by geographic
distance. IBD tests were performed in TFPGA v1.3
(Miller 1997) and significance was determined
using 999 permutations. Geographic distances to
the south-eastern British Columbia population
were calculated as the shortest distance through
mesic forest habitat.
 PHYLOGEOGRAPHY 81

Table 6.1 Exact tests for population differentiation (below diagonal) and DLR (above diagonal) for nine chestnut-backed chickadee
populations; significant pairwise tests are indicated in bold; refer to Fig. 6.1 for abbreviations of sampling sites

cAK AA NBC QCI VI NCP MtR OR SEBC

cAK 1.64 0.74 0.82 2.01 2.69 0.70 1.21 1.21

AA 0.002 0.49 1.63 1.41 1.30 0.90 0.97 1.32
NBC 0.003 0.266 1.47 0.75 0.76 0.05 0.90 0.54
QCI 0.001 0.003 0.001 2.22 2.67 1.58 1.46 1.48
VI 0.001 0.055 0.008 0.001 0.55 0.99 1.16 1.40
NCP 0.001 0.013 0.014 0.001 0.155 0.38 2.69 1.94
MtR 0.001 0.157 0.470 0.001 0.014 0.405 0.96 0.62
OR 0.002 0.025 0.192 0.003 0.004 0.006 0.059 1.11
SEBC 0.001 0.003 0.001 0.001 0.001 0.001 0.001 0.025

OR

QCI
AA VI
Axis 2

SEBC NCP

MtR

AK

is 3
NBC

Ax
Axis 1

Figure 6.2 Factorial correspondence analysis (FCA) of chestnut-backed chickadee populations in western North America. Each point represents
the centre of the distribution of genotypes from all the individuals in the population. Refer to Fig. 6.1 for abbreviations.

Queen Charlotte Islands, and North Cascades
Park populations, but not the population in south-
eastern British Columbia. The allelic variation is
similar throughout the range, but the number
of private alleles (i.e. alleles found only in one
population) is not (Fig. 6.3). The proportion of
private alleles is not significantly heterogeneous
(Gcorr 13.2, P 0.11); however, the proportion
of private alleles is significantly correlated with
latitude (P 0.05).
6.3.1.1 Interior and coastal populations
The interior population in south-eastern British
Columbia and Idaho is most likely of relatively
recent, postglacial origin as surveys in the
early 20th century did not detect extensive
chestnut-backed chickadee populations east of the
Cascades (Grinnell 1904; Bowles 1909; Brooks and
Swarth 1925). Chestnut-backed chickadees are
easily detected during auditory surveys; therefore
it seems unlikely that all three surveys would have
failed to find chickadees if they were indeed pre-
sent. The 300 km of arid land presently separating
the coastal and interior populations appears to be
limiting dispersal between these two groups.
Similar patterns (i.e. coastal and interior popula-
tions) are found in other mesic temperate forest
species with similar ecological requirements and
distributions as the chestnut-backed chickadee,
including plants, salamanders, frogs, and voles
(reviewed in Brunsfeld et al. 2001). Genetic data
show that some of these populations are the result
82 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
cAK*
AA
QCI NBC*
SEBC
VI
NCP*
OR
MtR
Figure 6.3 Geographic distribution of private alleles in
chestnut-backed chickadees. The percentage of private (black) and
shared (white) alleles are shown for each population. Populations
with higher than average (cAK, NBC) and lower than average (NCP)
number of private alleles are indicated (*). Refer to Fig. 6.1 for
abbreviations.
of ancient vicariance events (large genetic diver-
gence between interior and coastal lineages), while
others result from postglacial, inland dispersal
from the coast (little or no genetic differences
between lineages). Genetic data and historical
records suggest that the interior chestnut-backed
chickadee population is the result of inland disper-
sal from the coast (Burg et al. 2006). If the interior
population was due to ancient vicariance, a large
number of unique alleles should have arisen
through mutation and the FCA (Fig. 6.2) would
not position the interior group amongst the coastal
populations. The south-eastern British Columbia
population shows some affinity to the Oregon
population (Fig. 6.2). This grouping may be an
artifact of the small number of samples from Oregon
or it could reflect genetic similarity between these
two populations. If it is the latter, then the interior
population may have been founded by birds from
Oregon via dispersal around the southern edge of
the Columbia Basin. Further genetic analysis,
including additional samples from Oregon and
samples from California, are required to determine
the colonization route and the source of the interior
population.
6.3.1.2 Central, coastal Alaska
The pattern of genetic differentiation at the north-
ern end of the range is interesting. Chestnut-backed
chickadees are found as far north as the Kenai
Peninsula (Fig. 6.1); however, the population in
central, coastal Alaska is genetically isolated. A
closer examination of the forests surrounding
Haines, AK (near cAK, Fig. 6.1) shows that there is
a 100-km break in the coastal forests near the
Alaska/British Columbia/Yukon border. The gap is
caused by the encroaching glaciers between the
Pacific Ocean and the St Elias and Chugach
Mountain ranges. The glaciers create a disruption
in the distributions of western hemlock (Tsuga het-
erophylla) and Alaska/yellow cedar (Chamaecyparis
nootkatensis), the only two components of the mesic
temperate forest found north of Haines, AK (Little
1971). Other coniferous species associated with
mesic forests, such as western red cedar (Thuja pli-
cata), extend into south-eastern Alaska reaching as
far north as Haines; however, Douglas fir and
mountain hemlock (Tsuga mertensiana) are absent
north of the Queen Charlotte Islands (Little 1971).
The peripheral location of the Alaskan population
may partially explain why it is genetically isolated
from other populations of chestnut-backed chicka-
dees. A second possibility is prolonged isolation in
a glacial refugium. This is supported by the large
number of private alleles present in the central
Alaska population. Limited postglacial dispersal
between central Alaska and other coastal popula-
tions would have restricted the distribution of these
alleles and resulted in genetic differentiation along
the coast (Figs 6.1 and 6.3).
6.3.1.3 Queen Charlotte Islands
Glaciation on the Queen Charlotte Islands, a large
archipelago in northern British Columbia (Fig. 6.1),
ended earlier than on the adjacent mainland (Pielou
1991; Mann and Hamilton 1995). Paleoecological
evidence suggests that areas of Hecate Strait, which
separates these islands from the mainland, were
exposed during parts of the Pleistocene (Lacourse

et al. 2003). In addition, at the end of the Wisconsin
glaciation ~10 kya, while most of British Columbia
was under thick sheets of ice, the Queen Charlotte
Islands were ice free and available for colonization.
During this time, parts of coastal mainland British
Columbia were also ice free and sea levels were
relatively low. Patterns of genetic structure in other
Parid species indicate limited dispersal across large
expanses of water (Gill et al. 1993; Kvist et al. 2005).
The reduced sea levels would have effectively
decreased the width of Hecate Strait, thereby
reducing the distance required for chickadees to
traverse over water from the mainland. As the sea
level rose, it effectively isolated chestnut-backed
chickadees on the Queen Charlotte Islands.
Several other resident passerine species on the
Queen Charlotte Islands also show evidence of
genetic isolation including Stellers jay (Cyanocitta
stelleri), pine grosbeak (Pinicola enucleator), and
hairy woodpecker (Picoides villosus) (Burg et al.
2005; K. Winker, personal communication). These
species appear to have diverged from mainland
populations during the Pleistocene glaciations
and limited postglacial dispersal has occurred.
Although it is possible that chestnut-backed chicka-
dees survived in the Hecate refugium on the east
coast of the Queen Charlotte Islands, it is also pos-
sible that they colonized this archipelago after the
glaciers melted on the islands.
6.3.1.4 Private alleles
Private alleles are present in each of the nine popu-
lations and the proportion of private alleles
decreases from north to south (r2 45.61, P 0.05).
Private alleles are often present in populations
though the ability to detect and accurately identify
them is dependent on sample sizes. When high lev-
els of genetic variation are present and only a small
number of samples are analyzed, some alleles may
be incorrectly classified as private alleles. With
the exception of two populations (Alexander
Archipelago and Oregon), sample sizes of chestnut-
backed chickadees were adequate to obtain realistic
allele profiles (plotting the number of alleles
detected against number of samples showed that
the number of alleles present reached an asymp-
tote). Therefore, the relatively large number of pri-
vate alleles in the northern British Columbia and
PHYLOGEOGRAPHY 83
central Alaska sites is unlikely to be the result of a
sampling artifact. Three alternative possibilities
exist to explain the pattern of private alleles,
particularly in the northern part of the range:
multiple refugia, unsampled source population,
and introgression (introduction of genes from one
population into a second).
Populations that are isolated for prolonged
periods of time may contain different alleles due to
mutation and genetic drift. Such isolation could
have occurred in populations originating from mul-
tiple refugia (Fig. 6.4a, b, and e). If the populations
containing a large number of private alleles (i.e.
northern British Columbia and Alaska) did indeed
arise from distinct, northern refugial populations,
either directly or indirectly, then these populations
may also show higher levels of genetic divergence
from other populations. There is some speculation
regarding the existence of coastal and/or northern
refugia near these locations (e.g. Byun et al. 1997;
Soltis et al. 1997; Ritland et al. 2000; Ritland et al.
2001). Ritland et al. (2001) found a divergent lineage
of yellow cedar, an important component of the
cedarhemlock ecosystem, in northern British
Columbia and postulated that it may have origi-
nated in a northern refugium. It is plausible that if
such a refugium was present, that chestnut-backed
chickadees may have been present. Environmental
conditions in such a refugium would be similar to
those present in the northern part of the chickadees
range.
The large number of private alleles may be the
result of insufficient samples, not in terms of the
number of individuals sampled but the number of
populations sampled. No populations in southern
Oregon or California were sampled. Given the
genetic homogeneity of the southern coastal popu-
lations, samples from Washington and northern
Oregon are likely representative of populations fur-
ther south. However, the tendency of peripheral
isolation in the chestnut-backed chickadee suggests
that the California P. r. rufescens populations might
also have private alleles.
Lastly, the large number of northern private
alleles could be the result of hybridization between
chestnut-backed and boreal chickadees (Fig. 6.4d).
Hybridization is known to occur in other
passerines in the same area as the chestnut-backed
84 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

(a) (b) (c)

R1 R1

R2 R2
R1

(d) Boreal (e)

chickadee
R3

R2

R1
R1

Figure 6.4 Alternate scenarios for the origin of private alleles and pattern of colonization in chestnut-backed chickadees. Hypothetical
distributions (white ovals) following dispersal (arrows) from glacial refugium (grey areas) are shown. (a) Colonization from multiple refugia with
admixture; (b) colonization from multiple refugia with no admixture; (c) multiple colonizations from a single refugium; (d) single colonization from
a refugium and hybridization with boreal chickadees; (e) multiple glacial refugia with colonization from only one refugium.

chickadee, namely hermit and Townsends warblers
(Rohwer et al. 2001). Many of the hybrids of these
two warbler species are phenotypically indistin-
guishable from pure Townsends warblers. In
fact, most of the Townsends warbler populations
in British Columbia and Alaska, where no hermit
warblers are found, have hermit warbler mtDNA.
Rohwer et al. (2001) hypothesized that the distribu-
tion of Townsends and hermit warblers 8000 years
ago was quite different from today. Almost imme-
diately following the retreat of the ice sheets, the
hermit warblers expanded northward along the
coast and to the west of the Coast and Cascade
Mountains, a pattern identical to the coastal distri-
bution of chestnut-backed chickadees described by
Grinnell (1904). Townsends warblers were present
in the Rocky Mountains from Idaho to Colorado.
As the boreal forests invaded the deglaciated
regions of central British Columbia (Pielou 1991),
the Townsends warbler population expanded
northwards and came into contact with hermit
warblers near the Skeena River Valley along the
northern British Columbia coast (Rohwer et al.
2001). Like chestnut-backed chickadees, both of
these warbler species depend on Douglas fir. In
addition, it is believed that like the boreal and
chestnut-backed chickadees, the Townsends
and hermit warblers were isolated in interior and
coastal refugia, respectively (Grinnell 1904; Rohwer
et al. 2001). Therefore like the two warbler species,
it is possible that boreal chickadees were present in
the northern part of the contemporary chestnut-
backed chickadee range and as chestnut-backed
chickadees expanded northward, they hybridized
with boreal chickadees and eventually displaced
the boreal chickadee from the coast. The two
chestnut-backed chickadee populations with the
highest number of private alleles are in areas where

the ranges of chestnut-backed and boreal chicka-
dees come into contact. While the hypothesized
hybridization could be confirmed by genetic
analysis with a non-recombining genetic marker,
such as mtDNA, hybridization in Paridae is not
uncommon (black-capped and Carolina chicka-
dees, Chapter 7; gray-headed chickadee and willow
tit, Gill et al. 2005; Curry 2005).
6.3.1.5 Recolonization patterns
Sixteen thousand years ago most of the chestnut-
backed chickadee current range was heavily
glaciated. One of the largest refugia was found on
the now submerged continental shelf in Hecate
Strait off the east coast of the Queen Charlotte
Islands. Paleoecological data show that vegetation
was present in the Hecate refugium (Lacourse et al.
2003). At the end of the Wisconsin glaciation, ice
sheets retreated asynchronously along the Pacific
Coast. The Queen Charlotte Islands were ice free
16 kya, while the mainland coast was not ice free
until 13 kya (Mann and Hamilton 1995). In south-
ern British Columbia, glaciers were present only at
higher elevations 10 kya (Mann and Hamilton 1995;
Clague and James 2002).
Trees colonized the deglaciated landscape in
stages. The main tree species found in chestnut-
backed chickadee habitat are late successional
species and were one of the last to colonize the north.
Based on paleoecological data, fir, hemlock, and
cedar advanced northwards arriving at different
times along that coast. Douglas fir arrived first;
favoring the warmer, drier conditions present dur-
ing the hypsithermal (106 kya in south-western
British Columbia and either 52 kya or 96 kya in
Alaska; Mann and Hamilton 1995). Hemlock colo-
nized deglaciated areas during the cooler and wetter
conditions that followed the hypsithermal. Western
cedar was not present until 6 to 4 kya (Mann and
Hamilton 1995). Long distance dispersal increased
the rate of reforestation. The presence of coastal or
northern refugia would have further increased the
colonization rate of these arboreal species. The limited
genetic data available for these species support the
presence of multiple refugia along the coast of
British Columbia and Alaska (Ritland et al. 2001).
Once suitable habitat was available, recoloniza-
tion could occur through gradual range expansion,
PHYLOGEOGRAPHY 85
leap-frog, or long distance dispersal. A recent study
by Pruett and Winker (2005) provides an excellent
example of linear recolonization from a southern
refugium. The Pacific coast of northern British
Columbia and Alaska were sequentially colonized
by song sparrows (Melospiza melodia) with popula-
tions experiencing gradual loss of genetic diversity
as colonization progressed northwards.
The contemporary population structure in the
chestnut-backed chickadee (Figs 6.1 and 6.2) sug-
gests that recolonization was likely complex. When
inferring colonization patterns, relative genetic dis-
tances, distribution of alleles, and contemporary
population structure are important. Small genetic
distances result from individual dispersal or popu-
lation expansion. Similarly, the absence of private
alleles generally indicates dispersal while a large
number of private alleles can indicate prolonged
isolation. Dispersal, even as few as one or two
migrants per generation, results in genetically
homogeneous populations (Wang 2004). The pres-
ence of four genetically distinct groups of chestnut-
backed chickadees suggests little or no dispersal
among these groups and that recolonization was
not simply a linear progression along the coast as
seen in song sparrows (Pruett and Winker 2005).
Several recolonization scenarios are possible: colon-
ization from a single southern refugium, coloniza-
tion from a single northern refugium, and/or
colonization from multiple refugia (Fig. 6.4).
The extensive glaciation in the north and large
ice-free areas in the south would make postglacial
colonization from a single southern refugium the
most plausible scenario. Many of the alleles in the
southern populations are present in the north, as
would be predicted based on a northern expansion
from Washington or Oregon. The main problem
with this scenario is the large number of private
alleles in the two northern populations (Fig. 6.3). It
is unlikely that two of the populations furthest
from a putative southern refugium would contain
alleles that are absent in the founding populations
unless colonization followed a leap-frog pattern
(Fig. 6.4c) and source populations for both Alaska
and northern British Columbia populations were
not sampled (e.g. southern Oregon or California).
Colonization from a single northern refugium is
also possible. This would explain the significant
86 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
decrease in the number of private alleles with
decreasing latitude (P 0.05); however, this scen-
ario requires that the northern refugium supported
large populations as the high levels of genetic
variation would require a relatively large
population size. Given the high population differ-
entiation present in the north and absence of popu-
lation structure in southern coastal populations, it
seems unlikely that all of the populations could
have descended from individuals originating in the
north.
The final colonization scenario, colonization
from multiple refugia in the north and south
(Fig. 6.4e), is the most complex of the three scen-
arios. In this scenario the population in the southern
refugium (e.g. Washington) expanded northwards
following the advancing forests while dispersal
from one or more northern refugia was limited.
This scenario would explain both the large number
of private alleles and the pattern of population
genetic structure. Limited emigration from north-
ern refugia means that any alleles present in these
areas would remain there, thus explaining the
higher number of private alleles in the north. The
absence of genetic differentiation in the southern
coastal populations is the result of dispersal from a
southern refugium. According to the pioneer model
of colonization, populations established ahead of
the leading front, either by long distance dispersal
or existing refugia, create high density barriers
restricting migration into previously colonized
areas. The resulting genetic pattern is a mosaic of
isolated populations embedded within a larger
group of homogeneous populations (Hewitt 1996;
Ibrahim et al. 1996).
6.3.2 Comparison to other Parids
6.3.2.1 North American chickadees
Limited genetic studies have been conducted on
North American chickadees (Gill et al. 1993, 2005;
Burg et al. 2006). The most extensive study by Gill
et al. (1993) examined not only the relationship
between the different Parid species, but also levels
of genetic differentiation within populations using
mtDNA restriction fragment length polymorphism
(RFLP). Most of the North American chickadee
species were included, though for several of the
species (chestnut-backed, Mexican, and mountain
chickadees) only two populations were sampled.
With the exception of the chestnut-backed chicka-
dee, all of the species studied by Gill et al. (1993)
showed phylogeographic structure (Fig. 6.5). Black-
capped chickadee populations in Newfoundland
contained a different set of haplotypes from those
in mainland North America. Similarly, boreal
chickadees in Nova Scotia and Newfoundland
were genetically distinct from those in other parts
of Canada and the northern United States. The only
other continuous population to show phylogeo-
graphic structure is the Carolina chickadees, which
exhibit an eastwest division with secondary
contact near the Tombigbee River (Gill et al. 1999).
In the south-western United States and Mexico,
disjunct populations of the Mexican chickadee in
Arizona and Michoacan are genetically distinct
(Gill et al. 1993).
6.3.2.2 Eurasian Parids
Extensive population genetic studies of five
Palaerctic Parids (Siberian tits, willow tits, great
tits, blue tits, and azure tits) have been conducted
with no fewer than 16 published studies in the last
15 years. Different phylogeographic patterns are
found in each of these species (Fig. 6.6). The
Siberian tit showed no evidence of genetic structure
(Uimaniemi et al. 2003). In contrast, four divergent
lineages were found in the Eurasian willow tit. Six
of the nine subspecies from the large, continuous
northern portion of the range (Salzburger et al.
2002a) formed a single clade while three remaining
subspecies (P. m. weigoldicus, P. m. affinis, P. m.
songarus) each formed a distinct clade. A similar
pattern was found using the more variable mtDNA
control region, though samples of P. m. weigoldicus
were not included (Kvist et al. 2001). Four great tit
lineages were found across the Eurasian continent:
bokharensis, cinereus, major and minor, with the major
and minor groups containing multiple subspecies
(Kvist et al. 2003). The fourth Eurasian species
studied, the blue tit, exhibited intermediate levels
of population structure with multiple, highly
divergent clades: northern Europe, southern
Europe (Spain, France and Italy), Africa, and the
Canary Islands (Salzburger et al. 2002b; Kvist et al.
2004). Additional population structure exists within
 PHYLOGEOGRAPHY 87

Boreal
Black-capped
Carolina
Chestnut-backed
Mexican
Mountain

Figure 6.5 Map showing geographic distribution of genetically distinct chickadee populations in North America (Gill et al. 1993; Burg et al.
2006). Each symbol represents a sampling location and genetically distinct populations are indicated by shading. The Carolina chickadee
population near the Tombigbee River (white and black stripes) contains haplotypes from eastern and western lineages.

the Canary Islands with many islands containing
closely related, but distinct, lineages (Kvist et al.
2005). The phylogeographic study of the fifth
Eurasian species, the azure tit, was limited with one
to three samples from six sites (Salzburger et al.
2002b). Two haplotypes were present, one exclu-
sively in central and eastern Asia and the second at
two sites near the extreme eastern and western
ends of the range. While no clear phylogeographic
structure was detected, the small number of sam-
ples precludes any definite conclusions. The study
by Salzburger et al. (2002b) shows azure and blue
tits are paraphyletic with Eurasian and African blue
tits forming two different clades.
Many of the Eurasian species survived the last
glaciation in one or more refugia. The proposed
pattern of colonization ranges from simple to
complex. The simplest pattern is found in the
Siberian tit. It is hypothesized that this species
survived in a single eastern refugium (Uimaniemi
et al. 2003). For the blue tit, a minimum of four
refugia were present: Balkans, Iberian Peninsula,
Africa, and Canary Islands (Salzburger et al. 2002b;
Kvist et al. 2004). As populations expanded, birds
colonized the deglaciated landscape. A wide area of
secondary contact between birds from the two
Eurasian refugia is present in southern Europe,
though it would appear that most of Europe was
founded by individuals from the Balkan refugium.
This is apparent not only in the geographic
distribution of haplotypes from the Balkan clade,
but also in the resulting phylogeny. The star-burst
pattern of the mtDNA haplotypes indicates
that a population expansion accompanied the
88 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
Figure 6.6 Genetic structure of Eurasian tit species (see text for references). Each genetic lineage is indicated (white, light grey, dark grey or
black). Blue tits on the Canary Islands (light grey circle) contain at least six closely related lineages.
colonization from the eastern refugium (Kvist et al.
2004). The Balkan clade contained individuals from
all of the sampled Eurasian populations. No evi-
dence of a recent expansion was found in the
Iberian or Canary clades. Instead the pattern of
a large number of divergent haplotypes with no
one predominant haplotype, suggests that these
populations are much older. The Iberian clade con-
tains individuals mostly from Spain and France (i.e.
Corsica) and some from Italy, suggesting limited
postglacial dispersal. Similarly, fixed genetic differ-
ences are found between different islands in the
Canary Island population. Phylogeographic recon-
structions for both the willow and great tits suggest
the presence of four Pleistocene refugia. For both of
these species, it is hypothesized that three of
the groups survived in refugium at or near their
present day location. The same Balkan refugium
suggested for the blue tits could have been used by
the major group of great tits (Kvist et al. 2003,
2004). However, the fourth group of willow tits,
containing six subspecies, may have persisted in a
Azure
Blue
Great
Siberian
Willow
refugium in south-east Asia (Kvist et al. 2001;
Salzburger et al. 2002a). Genetic diversity in willow
tits decreases from east to west, suggesting that
postglacial colonization proceeded in a westward
direction (Kvist et al. 2001).
Population structure of Eurasian species is similar
in many ways to that of chestnut-backed chickadees.
There is evidence of limited dispersal within contin-
uous populations (great tit, blue tit, and willow tit),
genetic isolation of island populations (blue tit and
willow tit), and restricted gene flow between central
and peripheral populations (blue tit). It would
appear that many of the factors influencing disper-
sal, and therefore population structure, in North
American and Eurasian Parids are similar.
6.4 Factors influencing population
genetics of Parids
In the following section, I discuss several recurring
themes that are present in the patterns of popula-
tion structure for both North American and
 PHYLOGEOGRAPHY 89

Eurasian Parids (Table 6.2), namely the role of refu-
gia, disjunct populations, and peripheral isolation
within continuous habitat.
6.4.1 Postglacial colonization and glacial
refugia
The Pleistocene glaciations played a critical role in
shaping contemporary populations in both the
Nearctic and Palaearctic. Genetic studies have
shown that the late Plioceneearly Pleistocene was
important for Parid speciation and the late
Pleistocene was responsible for creating many of
the contemporary population genetic patterns.
Even in unglaciated areas, environmental changes
that accompanied the glaciations altered the distri-
bution of many species. For many of the Parid
species, changes in forest distribution would have
altered their distribution. In Eurasia, as many as
seven refugia have been proposed: the Iberian
Peninsula, Balkans, Africa, Canary Islands, and at
least three in Asia. Suture zones or areas of second-
ary contact are present in several Eurasian popula-
tions which were previously isolated in different
refugia. In North America, it is reasonable, given
the mtDNA data, that multiple refugia were also
present; however, the location of most of these
refugia is unknown. Gill et al. (1993) suggested that
for boreal and black-capped chickadees one such
refugium may have existed in Newfoundland. It is
also probable that the distinct lineages of Carolina,
mountain, and Mexican chickadees are the result of
isolation in different refugia during the Pleistocene.
For the chestnut-backed chickadee, microsatellite
data do not conclusively support or refute the exist-
ence of multiple Pleistocene refugia. Until the
source of the private alleles is determined, it is rea-
sonable to speculate that multiple refugia were
present; one large refugium in the south and at least
one in the north.

Table 6.2 Summary of patterns of colonization and population genetic structure in contemporary Parid populations

Multiple refugia Pattern of genetic isolation

Disjunct Islands Within continuous habitat

Overall Peripheral

North America chickadees

Black-capped Y n/a Y (NF) Y Y
Boreal Y n/a Y (NF1) Y Y
Carolina Y n/a n/a Y N
Chestnut-backed2 ? Y Y (QCI) Y Y
Mexican Y Y n/a n/a n/a
Mountain Y n/a n/a Y Y3
Eurasian tits
Blue Y n/a Y (Canary Is., British Isles) Y Y
Great Y N N Y N
Siberian N n/a n/a N N
Willow Y Y Y (Japan4) Y N

For each of the categories the presence (Y) or absence (N) of population genetic structure is given. The three main categories of population structure
are isolation due to: disjunct populations, island populations, and peripheral populations within continuous habitat. The presence of genetic structure
(overall) and isolation of peripheral populations (peripheral) within continuous habitat are listed separately. For some species, the category did not
exist or no data was available (n/a). Azure tits are not included due to insufficient data.
1
Newfoundland and Nova Scotia share haplotypes.
2
Microsatellite data only.
3
Only two sampling sites, both peripheral.
4
One common haplotype found in all Japanese sites, haplotype restricted to Japan.
90 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
6.4.2 Disjunct populations
Genetic isolation between physically separated
populations can arise through limited dispersal
across large areas of unsuitable habitat. In the case
of Parids, unsuitable habitat may consist of changes
in forest composition, gaps in forest, large geo-
graphic distances, or water barriers.
6.4.2.1 Mainland populations
Studies of both chickadees and tits have shown that
disjunct mainland populations are genetically iso-
lated. Both the coastal and interior populations of
chestnut-backed chickadees and southern US and
Mexican populations of Mexican chickadees are
separated by relatively arid habitat. In Eurasia,
each of the four willow tit lineages occupies a dif-
ferent ecological niche (Salzburger et al. 2002a). The
result is that dispersal between physically isolated
populations is limited among each of these three
species. In the willow tit and chestnut-backed
chickadees, population subdivisions are present
within continuous habitat, indicating limited dis-
persal (Chapter 15). The habitat for the Mexican
chickadee is highly fragmented and insufficient
data are available to know if dispersal is limited
within continuous forest fragments.
6.4.2.2 Island populations
Gill et al. (1993) suggested limited dispersal across
water in both black-capped and boreal chickadee
populations. While the chestnut-backed chickadee
population on Vancouver Island (~30 km from the
mainland with numerous intervening islands) is
not genetically differentiated from the mainland
population, the Queen Charlotte Island population
(~80 km from the mainland with few islands that
could connect the mainland to the archipelago)
is genetically distinct. The pattern is repeated
in black-capped chickadees (Newfoundland is
genetically distinct from the mainland) and Canary
Island blue tits (~110 km from African coast and
substantial interisland distances) (Gill et al. 1993;
Kvist et al. 2005). For all three North American
species (black-capped, boreal, and chestnut-backed
chickadees) the lower sea levels during glacial
periods would have effectively decreased the
distance between islands (i.e. Newfoundland and
the Queen Charlotte Islands) and the adjacent
mainland, thereby facilitating dispersal. Strong
trade winds are thought to have aided in the
colonization of the Canary Islands by blue tits
(Kvist et al. 2001). It is not clear what is limiting
dispersal as it is evident by the presence of Parids
on these islands that they are capable of dispersing
across water barriers. Yet on some islands, species
found on the nearby mainland are absent. For
example, on Vancouver Island and the nearby
San Juan Islands, no black-capped or mountain
chickadees are present despite suitable available
habitat (Sturman 1968). Both of these species
are present on the British Columbia mainland
(Campbell et al. 1997).
6.4.3 Limited dispersal within continuous
habitat and peripheral populations
Several Parid species exhibit genetic structure
within a physically continuous habitat; however,
the isolation of peripheral populations is more
prevalent in North American species, particularly
those with northern distributions (e.g. black-
capped, boreal, and chestnut-backed chickadees).
Populations at the edge of a species distribution
may be genetically distinct due to restricted disper-
sal from the core to the periphery of a species range
(Wisely et al. 2004). This asymmetrical dispersal is
due to peripheral populations containing subopti-
mal habitat that further restricts dispersal into the
area, and limits both population size and density. In
the case of the chestnut-backed chickadee, dispersal
in general may be more restricted due to its linear
distribution (Slatkin 1993). Populations with linear
distributions are more likely to have restricted dis-
persal than widespread ones for some of the same
reasons that dispersal is more limited at the edge of
the species range (i.e. a limited number of direc-
tions in which dispersal can occur).
6.5 Conclusions and perspectives
The population structure of chestnut-backed
chickadees, and that of other Parids, appears to be
complex and influenced by a variety of factors,
most notably postglacial colonization and
distribution. Many of the factors limiting dispersal

in chestnut-backed chickadees seem to be
common in other Parids. These include isolation of
peripheral populations, and limited dispersal over
large water barriers or other areas of unsuitable
habitat. Within the northern portion of the
chestnut-backed chickadee range, a large number
of private alleles are present in two of the popula-
tions. Further genetic analyses are required to
determine the origin of these alleles. The simplest
and most probable explanation is that they resulted
from prolonged isolation in multiple refugia and
they are not present in other populations due to
limited emigration.
Acknowledgements
Tim Boucher, Roger Bull, Robert Dickerman, Chris
Gibb, Sandeep Girn, Andrew Johnson, James Maley,
Alison Ronson, and members of the Laskeek Bay
Conservation Society assisted with sample collec-
tion and the University of Alaska Museum provided
additional samples. Parks Canada and the US
National Parks permitted sample collection within
the parks. I would like to thank Vicki Friesen, Tony
Gaston, Kevin Winker, and Maia Bailey for helpful
discussions. Funding was provided by Canadian
Wildlife Service and Natural Sciences and
Engineering Research Council of Canada.
References
Belkhir, K., Borsa, P., Chikhi, L., Raufaste, N., Bonhomme,
F. (2000). GENETIX 4.02, logiciel sous WindowsTM pour la
gntique des populations. Laboratoire Gnome et
Populations, CNRS UPR 9060, Universit Montpellier
II, Montpellier.
Bowles, J. H. (1909). Notes on Parus rufescens in western
Washington. Condor, 11, 5557.
Brennan, L. A. and Morrison, M. L. (1991). Long-term
trends of chickadee populations in western North
America. Condor, 93, 130137.
Brennan, L. A., Morrison, M. L., and Dahlsten, D. L.
(1999). Influence of vegetation on occupation of nest
boxes by chestnut-backed and mountain chickadees.
Northwestern Naturalist, 80, 9098.
Brennan, L. A., Morrison, M. L., and Dahlsten, D. L.
(2000). Comparative foraging dynamics of chestnut-
backed and mountain chickadees in the western Sierra
Nevada. Northwestern Naturalist, 81, 129147.
PHYLOGEOGRAPHY 91
Brooks, A. and Swarth, H. S. (1925). A distributional list of
the birds of British Columbia. Pacific Coast Avifauna, 17,
1158.
Brunsfeld, S. J., Sullivan, J., Soltis, D. E., and Soltis, P. S.
(2001). Comparative phylogeography of northwestern
North America: a synthesis. In: Silverton, J. and
Antonovics, J., eds. Integrating Ecological and
Evolutionary Processes in a Spatial Context, pp. 319339.
Blackwell Science, Oxford.
Burg, T. M., Gaston, A. J., Winker, K., and Friesen, V. L.
(2005). Rapid divergence and post-glacial colonization
in western North American Stellers jays (Cyanocitta
stelleri). Molecular Ecology, 14, 37453755.
Burg, T. M., Gaston, A. J., Winker, K., and Friesen, V. L.
(2006). Effects of Pleistocene glaciations on population
structure of North American chestnut-backed chick-
adees. Molecular Ecology. 15, 24092419.
Byun, S. A., Koop, B. F., and Reimchen, T. E. (1997). North
American black bear mtDNA phylogeography: implica-
tions for morphology and the Haida Gwaii glacial
refugium controversy. Evolution, 51, 16471653.
Campbell, W., Dawe, N. K., McTaggart-Cowan, I., et al.
(1997). Birds of British Columbia, Vol. 3, Passerines-
Flycatchers through Vireos. UBC Press, Vancouver, BC.
Carey, A. B., Mae Hardt, M., Horton, S. P., and Biswell,
B. L. (1991). Spring bird communities in the Oregon
Coast Range. In: Ruggiero, L. F., Aubry, K. B., Carey,
A. B., and Huff, M. H., eds. Wildlife and Vegetation of
Unmanaged Douglas-fir Forests. General Technical Report
PNW-GTR-285, pp. 123142. US Department of
Agriculture, Forest Service, Portland, OR.
Clague, J. J. and James, T. S. (2002). History and isostatic
effects of the last ice sheet in southern British Columbia.
Quaternary Science Reviews, 21, 7187.
Curry, R. L. (2005). Hybridization in chickadees: much to
learn from familiar birds. Auk, 122, 747758.
Dahlsten, D. L., Brennan, L. A., McCallum, D. A., and
Gaunt, S. L (2002). Chestnut-backed chickadee (Poecile
rufescens). In: Poole, A. and Gill, F., eds. The Birds of
North America. The Birds of North America # 689, Inc.,
Philadelphia, PA.
Dyke, A. S., Andrews, J. T., Clark, P. U., et al. (2002). The
Laurentide and Innuitian ice sheets during the last
glacial maximum. Quaternary Science Reviews, 21, 931.
Fisher, R. (1954). Statistical Methods for Research Workers.
Oliver and Boyd, Edinburgh.
Gill, F. B., Funk, D. H., and Silverin, B. (1989). Protein rela-
tionships among titmice (Parus). Wilson Bulletin, 101,
182197.
Gill, F. B., Mostrom, A. M., and Mack, A. L. (1993).
Speciation in North American chickadees: I. Patterns of
mtDNA genetic divergence. Evolution, 47, 195212.
92 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
Gill, F. B., Slikas, B., and Agro, D. (1999). Speciation in
North American chickadees: II. Geography of mtDNA
haplotypes in Poecile carolinensis. Auk, 116, 274277.
Gill, F. B., Slikas, B., and Sheldon, F. H. (2005). Phylogeny
of titmice (Paridae): II. Species relationships based on
sequences of the mitochondrial cytochrome b gene.
Auk, 122, 121143.
Goudet, J. (2001). FSTAT, a program to estimate and test
gene diversities and fixation indices (version 2.9.3).
Available from http://www.unil.ch/izea/softwares/
fstat.html. Updated from Goudet (1995).
Goudet, J., Raymond, M., de Meeus, T., and Rousset, F.
(1996). Testing differentiation in diploid populations.
Genetics, 144, 19331940.
Grinnell, J. (1904). The origin and distribution of the chest-
nut-backed chickadee. Auk, 21, 364382.
Guo, S. W. and Thompson, E. A. (1992). Performing the
exact test of HardyWeinberg proportion for multiple
alleles. Biometrics, 48, 361372.
Hedrick, P. (1999). Perspective: Highly variable loci and
their interpretation in evolution and conservation.
Evolution, 53, 313318.
Hewitt, G. M. (1996). Some genetic consequences of ice
ages, and their role in divergence and speciation.
Biological Journal of the Linnean Society, 58, 247276.
Hutchison, D. and Templeton, A. (1999). Correlation of
pairwise genetic and geographic distance measures:
inferring the relative influences of gene flow and drift
on the distribution of genetic variability. Evolution, 53,
18981914.
Ibrahim, K. M., Nichols, R. A., and Hewitt, G. M. (1996).
Spatial patterns of genetic variation generated by dif-
ferent forms of dispersal during range expansion.
Heredity, 77, 282291.
Johnson, N. K. and Cicero, C. (2004). New mitochondrial
DNA data affirm the importance of Pleistocene speci-
ation in North American birds. Evolution, 58, 11221130.
Kvist, L., Broggi, J., Illera, J. C., and Koivula, K. (2005).
Colonisation and diversification of the blue tits (Parus
caeruleus teneriffae-group) in the Canary Islands.
Molecular Phylogenetics and Evolution, 34, 501511.
Kvist, L., Martens, J., Ahola, A., and Orell, M. (2001).
Phylogeography of a Paelaearctic sedentary passerine,
the willow tit (Parus montanus). Journal of Evolutionary
Biology, 14, 930941.
Kvist, L., Martens, J., Higuchi, H., Nazarenko, A. A.,
Valchuk, O. P., and Orell, M. (2003). Evolution
and genetic structure of the great tit (Parus major)
complex. Proceedings of the Royal Society, Series B, 270,
14471454.
Kvist, L., Viiri, K., Dias, P. C., Rytkonen, S., and Orell, M.
(2004). Glacial history and colonization of Europe by
the blue tit Parus caeruleus. Journal of Avian Biology, 35,
352359.
Lacourse, T., Mathewes, R. W., and Fedje, D. W. (2003).
Paleoecology of late-glacial terrestrial deposits
with in situ conifers from the submerged continental
shelf of western Canada. Quaternary Research, 60,
180188.
Little, E. L. (1971). Atlas of United States Trees. United States
Department of Agriculture Misc. Publication 1146.
Lovette, I. J. (2005). Glacial cycles and the tempo of avian
speciation. Trends in Ecology and Evolution, 20, 5759.
Mann, D. H. and Hamilton, T. D. (1995). Late Pleistocene
and Holocene paleoenvironments of the North Pacific
coast. Quaternary Science Review, 14, 449471.
Miller, M. (1997). Tools for Population Genetic Analysis
(TFPGA), version 1.3. Northern Arizona University,
Flagstaff, AZ.
Paetkau, D., Waits, L., Clarkson, P., Craighead, L., and
Strobeck, C. (1997). An empirical evaluation of genetic
distance statistics using microsatellite data from bear
(Ursidae) populations. Genetics, 147, 19431957.
Pielou, E. C. (1991). After the Ice Age: the Return of Life to
Glaciated North America. University of Chicago Press,
Chicago.
Pruett, C. L. and Winker, K. (2005). Northwestern song
sparrow populations show genetic effects of sequential
colonization. Molecular Ecology, 14, 14211434.
Raymond, M. and Rousset, F. (1995a). An exact test for
population differentiation. Evolution, 49, 12801283.
Raymond, M. and Rousset, F. (1995b). GENEPOP (Version
1.2): Population genetics software for exact tests and
ecumenicism. Journal of Heredity, 86, 248249.
Rice, W. R. (1989). Analyzing tables of statistical tests.
Evolution, 43, 223225.
Ritland, C., Pape, T., and Ritland, K. (2001). Genetic struc-
ture of yellow cedar (Chamaecyparis nootkatensis).
Canadian Journal of Botany, 79, 822828.
Ritland, K., Dupuis, L. A., Bunnel, F. L., Hung, W. L. Y.,
and Carlson, J. E. (2000). Phylogeography of the tailed
frog (Ascaphus truei) in British Columbia. Canadian
Journal of Zoology, 78, 17491758.
Rohwer, S., Bermingham, E., and Wood, C. (2001).
Plumage and mitochondrial DNA haplotype variation
across a moving hybrid zone. Evolution, 55, 405422.
Salzburger, W., Martens, J., Nazarenko, A. A., Sun, Y.-H.,
Dallinger, R., and Sturmbauer, C. (2002a).
Phylogeography of the Eurasian willow tit (Parus
montanus) based on DNA sequences of the mitochon-
drial cytochrome b gene. Molecular Phylogenetics and
Evolution, 24, 2634.
Salzburger, W., Martens, J., and Sturmbauer, C. (2002b).
Paraphyly of the blue tit (Parus caeruleus) suggested

from cytochrome b sequences. Molecular Phylogenetics
and Evolution, 24, 1925.
Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989).
Molecular CloningA Laboratory Manual. Cold Spring
Harbor Laboratory Press.
Sibley, D. A. (2000). The Sibley Guide to Birds. Alfred A.
Knopf, Inc., New York.
Slatkin, M. (1993). Isolation by distance in equilibrium
and non-equilibrium populations. Evolution, 47,
264279.
Smith, S. (1967). An ecological study of winter flocks of
black-capped and chestnut-backed chickadees. Wilson
Bulletin, 79, 200207.
Soltis, D. E., Gitzendanner, M. A., Strenge, D. D., and
Soltis, P. S. (1997). Chloroplast DNA intraspecific phylo-
geography of plants from the Pacific Northwest of
North America. Plant Systematics and Evolution, 206,
353373.
PHYLOGEOGRAPHY 93
Sturman, W. A. (1968). Description and analysis of breed-
ing habitats of the chickadees, Parus atricapillus and P.
rufescens. Ecology, 49, 418431.
Uimaniemi, L., Orell, M., Kvist, L., Jokimki, J., and
Lumme, J. (2003). Genetic variation of the Siberian tit
Parus cinctus populations at the regional level: a mito-
chondrial sequence analysis. Ecography, 26, 98106.
Wang, J. (2004). Application of the one-migrant-per-gen-
eration rule to conservation and management.
Conservation Biology, 18, 332343.
Weir, J. T. and Schluter, D. (2004). Ice sheets promote spe-
ciation in boreal birds. Proceedings of the Royal Society,
Biological Sciences, 271, 18811887.
Wisely, S. M., Buskirk, S. W., Russell, G. A., Aubry, K. B.,
and Zielinski, W. J. (2004). Genetic diversity and struc-
ture of the fisher (Martes pennanti) in a peninsular and
peripheral metapopulations. Journal of Mammalogy, 85,
640648.
This page intentionally left blank
 CHAPTER 7
Behavioral aspects of chickadee
hybridization
Robert L. Curry, Lindsay M. Rossano, and
Matthew W. Reudink
7.1 Introduction
Within the Paridae, hybridization is known to occur
regularly in a few pairs of sibling species and
sporadically between other taxa of varying degrees
of evolutionary proximity (Harrap and Quinn 1995;
Curry 2005). Interbreeding of black-capped chicka-
dees and Carolina chickadees represents a unique
situation in the family in that although these
congeners are not each others closest relatives (Gill
et al. 2005), they nonetheless hybridize regularly:
observations consistent with interbreeding have
been reported from numerous locations along their
predominantly eastwest line of parapatric contact
stretching from central New Jersey to south-eastern
Kansas, with a dip southward in the Appalachian
Mountains to western North Carolina (reviewed by
Bronson et al. 2005; Curry 2005). Hybridization
between black-capped and Carolina chickadees has
been investigated most recently in Ohio, where
both observational and experimental evidence have
documented reduced reproductive success associ-
ated with interbreeding (Bronson et al. 2003a, 2005),
and in Pennsylvania (Reudink et al. 2006).
Production of hybrids can result from either
reproduction by mixed pairs or extrapair copula-
tion involving heterospecific individuals. On a
proximate level, heterospecific mating is likely to
be facilitated by sexual imprinting: if individuals
are exposed during development to adults or nest-
mates of another species, they may develop prefer-
ences for mates of that species (Grant and Grant
1997; Irwin and Price 1999; ten Cate and Vos 1999).
Additionally, exposure to heterospecifics in a zone
of contact may cause abnormal development of
courtship displays such that individuals conse-
quently produce mixed signals, or only those char-
acteristic of another species. Even if normal mate
preferences determine mating, hybridization can
result if individuals produce displays that incor-
rectly signal their own identity.
In many songbirds, females base species recogni-
tion and mate choice in large part on songs and calls
(Nowicki and Searcy 2005). Unlike morphology,
vocal traits may be vulnerable to misimprinting
because development of songs and calls frequently
involves learning, including exposure to sounds
during an early critical period. To understand mech-
anisms of hybridization in any songbird system, it is
therefore worthwhile to examine the extent to
which males within contact zones produce vocaliza-
tions that reflect their own genetic identity, and the
ways in which females respond to these signals.
In this chapter, we summarize information from
our studies of the hybrid zone between black-
capped and Carolina chickadees in south-eastern
Pennsylvania. Our focus is on patterns of vocal vari-
ation in relation to among- and within-population
genetic variation. Primary questions we address
include: (1) What song and call types are produced
within this hybrid zone? (2) Are the vocalization
types congruent with one another within individu-
als? (3) What insights might we derive from these
patterns regarding mechanisms of hybridization in
chickadees? We then review available information,
and opportunities for further research, concerning
patterns and mechanisms of hybridization among
Parids of both North America and Eurasia.
95
96 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
7.2 Background and methods
Black-capped and Carolina chickadees are morph-
ologically and ecologically similar. Black-capped
chickadees, which inhabit much of Canada and the
northern tier of the USA, have been studied exten-
sively in Massachusetts, Ontario, and elsewhere
(Smith 1993; see also this volume, Chapters 9, 12,
and 14). Carolina chickadees, which are resident
throughout the south-eastern USA, have been stud-
ied less overall (Mostrom et al. 2002) but have been
the subjects of recent research, particularly on
vocalizations (e.g. Chapter 13).
A prominent feature of chickadee behavior is the
production of whistled song by males, mainly just
prior to and during the breeding season (Hailman
and Ficken 1996; Chapter 14). Development of the
whistled fee-bee of the black-capped chickadee,
despite a high degree of stereotypy across its
extensive geographic range (Kroodsma et al. 1999),
appears to involve learning (Kroodsma et al. 1995;
Baker et al. 2003). Pitch characteristics appear rele-
vant for species identification (Weisman and
Ratcliffe 1989; Chapter 10). Song repertoires in
Carolina chickadees are broader, with most males
producing two general song types: a four-note
song involving alternating high and low notes (see-
bee-see-bay) and an song incorporating one or more
high notes followed by variable numbers of lower
notes (e.g. see-see-bay-bay-bay; Smith 1972; see also
Fig. 4C in Ward and Ward 1974). Geographic
variation in Carolina chickadee song is more pro-
nounced (Ward 1966; Mostrom et al. 2002).
Both species also produce a wide variety of calls
(Hailman and Ficken 1996). The chick-a-dee call, used
throughout the year in pair and flock interactions
and during predator mobbing, has been studied in
depth (Chapter 13). Another complex vocalization,
the gargle call, has been examined in black-capped
chickadees (Chapter 11) and has been described in
Carolina chickadees (Mostrom et al. 2002), but
detailed interspecific comparisons of the call, which
is used in aggressive interactions, are lacking.
Unusual vocal patterns, including bilingual
singing, have been documented frequently among
chickadees within or close to the presumed contact
zone (e.g. Johnston 1971; Robbins et al. 1986). In
Missouri populations shown to include hybrid indi-
viduals based on genetic analysis (Braun and
Robbins 1986; Sawaya 1990), songs are intermediate
in pitch and duration of individual notes, even
among songs that can be grossly categorized based
on number of notes as black-capped-like or
Carolina-like (Robbins et al. 1986). In some parts of
the contact zone, an association between individual
genetic identity and song parameters may exist
(Sawaya 1990; Sattler 1996). No previous study has
examined quantitative aspects of calls in detail for
any local segment of the chickadee contact zone, nor
have genotypes, songs, and calls of individuals been
investigated concurrently. Here, we focus our atten-
tion on songs and on the D note of the chick-a-dee call,
which appears to function in flock discrimination
and species identity (Mammen and Nowicki 1981;
Charrier and Sturdy 2005; Chapters 10 and 13).
7.2.1 Study sites
We have studied chickadees principally at three
sites in south-eastern Pennsylvania (Fig. 7.1). The
southernmost, Great Marsh (GM), covers approxi-
mately 200 ha; research here, initiated in 1998,
involves resident Carolina chickadees. Nolde
Forest (NF), about 24 km north-west, is a state park
of 269 ha where research, initiated in 1998, focuses
on a population comprising predominantly hybrid
individuals (Reudink et al. 2006; see below). The
third site (HM), about 35 km north of NF, includes
~120 ha within Hawk Mountain Sanctuary, where
we began studying chickadees in 2001, as well as 10
nearby woodlots (123 ha, totaling ~80 ha) from
which we obtained data in a companion study. As
recently as 1988, all individuals studied at HM were
black-capped chickadees, but beginning in 2002 we
detected evidence of hybrid individuals in this
population (Reudink et al. 2007). We also used some
additional recordings from areas in Pennsylvania
south and east of GM (Carolina chickadees) and
from Nova Scotia, Vermont, and Massachusetts
(black-capped chickadees).
7.2.2 Field methods
We studied mainly resident chickadees using artifi-
cial snags (based on Grubb and Bronson 1995) for
nesting. We monitored up to 53 snags at GM, 152 at
NF, and 212 at HM. Total samples of nests reaching
at least the stage of egg-laying were 151 at GM
(930 per season, 19982005); 270 at NF (655, in
19982005); and 54 at HM (120, in 20002005).
 B E H AV I O R A L A S P E C T S O F H Y B R I D I Z AT I O N 97

Carbon Monroe
Schuylkill

Hawk Mountain Northampton

(HM)
Lehigh New
Jersey
Berks
Nolde Forest Bucks
Lebanon
(NF)
Montgomery

Lancaster Great Marsh

(GM) Phila.
Delaware
Chester
York N
Delaware 0 20 40 Kilometers
Maryland

Figure 7.1 Locations of primary study sites (names of Pennsylvania counties shown). Great Marsh (GM) is inhabited by Carolina chickadees.
Nolde Forest (NF) is inhabited by hybrid chickadees. The Hawk Mountain (HM) site, inhabited mainly by black-capped chickadees, comprises
property at Hawk Mountain Sanctuary and nearby woodlots. The contact zone is believed to run approximately from south-west (northern York
Co.) to north-east (southern Northampton Co.).

We used mist nets to capture adults at winter
feeding stations or at nests. Each received a Fish
and Wildlife Service (FWS) aluminum band and
two or three plastic colored bands. We banded
nestlings with FWS bands at 9 to 12 days after
hatching; the few that remained to breed locally
later received colored bands.
7.2.3 Genetic methods
We collected blood samples (1040 l from the
brachial vein) from nestlings and adults at each nest,
from which we extracted DNA using commercially
available kits. Characterization of mitochondrial
DNA (mtDNA) haplotypes involved polymerase
chain reactionrestriction fragment length poly-
morphism (PCRRFLP) analysis: amplified cyto-
chrome b mtDNA was cut by the enzymes EcoR V
(black-capped haplotype) or Xmn I (Carolina
haplotype), based on Kvist et al. (1996). We investi-
gated genetic identity of individuals, as well as
parentage patterns, using six microsatellite loci
developed in prior studies of black-capped chicka-
dee and blue tit; see Reudink et al. (2006) for details.
7.2.4 Hybrid index scores
Our analyses relied on the assumption that the two
reference populations (HM and GM) included pre-
dominantly black-capped and Carolina chickadees
respectively, and that genetic information from
these populations could be used to characterize
individuals at NF. This assumption has received
support from analyses using the program STRUC-
TURE (v. 2.1; Pritchard et al. 2000), which employs
Bayesian methods to estimate the number of distinct
populations and microsatellite allele frequencies
among residents in each population (Reudink et al.
2007). However, this method did not allow us to
characterize the genetic identities of individuals; to
98 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
produce a rule based on microsatellite genotypes
that we could use to characterize individual breed-
ers, we performed an iterative maximum-likelihood
assignment test based on genotypes from the two
reference populations, after omitting a few HM
birds carrying Carolina mtDNA. The analysis
yielded assignment probabilities, where px and py
are the likelihoods of an individual belonging to
population x or y respectively, and resulting hybrid
index scores (IH) for breeders at all three sites, on a
scale from 0 (Carolina) to 1 (black-capped) as
follows (after Hansen et al. 2000):
IH1ln(px)/[ln(px)ln(py)]
For additional details, see Reudink et al. (2006).
7.2.5 Song and call recordings
During the breeding seasons of 2000 and 2001, LMR
recorded songs from 28 breeding males at NF
(Rossano 2003). For comparison, we used songs of
four individuals from predominantly or exclusively
black-capped populations (HM, Nova Scotia, and
Vermont) and from five birds from Carolina popu-
lations (GM and Montgomery Co., PA).
LMR recorded calls between October 2000 and
October 2001 at NF from the same 28 males whose
songs were sampled either near winter feeders or
within each males breeding season territory but
away from the nest. For comparison, we used
recorded chick-a-dee calls from eight individuals
from reference populations of black-capped and
Carolina chickadees.
Observations of vocalizations at the three
primary sites continued in 20022005. In each year,
we categorized the song type of each breeding male
Table 7.1 Song parameters in hybrid zone (NF study site) in relation to corresponding songs from sites outside of the hybrid zone;
repeated-measures least-square means SEM shown for each parameter
Population and song type 1st note frequency
(kHz)
Black-capped (n 69) 3.8 0.1
NF, 2-note song (n 99) 3.9 0.1
NF, 4-note song (n 99) 6.8 0.1
Carolina (n 64) 6.7 0.1
a,b,c
Means sharing letter different at P 0.05, repeated-measures ANOVA and Tukeys HSD post-hoc contrast.
at NF, based on repeated observations during the
laying and incubation periods at active nests.
7.2.6 Sound analysis
We performed acoustic analyses using Canary 1.2
(Cornell Laboratory of Ornithology). We noted the
total number of notes (treating the bee of typical
black-capped chickadee song as one note) but
quantified only the first two notes to permit com-
parisons among all songs (Table 7.1). For chick-a-dee
calls, we focused on the middle D note in calls with
an odd number of D notes, or the first D of the mid-
dle two notes in calls with an even number of D
notes. We used a spectrum of a 2.0 msec section at
the midpoint of the note (44.1 kHz sample rate;
1024 FFT size) to measure frequency range for
sound components within 30 dB of the loudest part
of the note (based on Nowicki 1989).
7.3 Results
7.3.1 Genetic composition of study
populations
Analysis of mtDNA supported the assumption that
the three primary sites spanned the contact zone. At
GM, all breeders in all years had Carolina mtDNA
(n 84 individuals, including 40 females and 44
males). At NF, the majority of breeders exhibited
Carolina haplotypes: of 83 male breeders analyzed
from 19982005, only three (3.6%, associated with
four nests in 19982000) had black-capped mtDNA
and among 67 females sampled, only two (3.0%,
both breeding in 2000) had black-capped mtDNA.
At HM, all chickadees breeding before 2002 (three
females, three males) had black-capped haplotypes.
1st note duration Interval between 2nd note 2nd note
(msec) 1st and 2nd notes frequency (kHz) duration (msec)
(msec)
367.2 23.3 124.7 16.5a 3.3 0.1 386.4 37.1
330.6 6.4 101.4 4.5a 3.3 0.1 364.6 10.8
213.7 12.9b 117.8 15.5c 4.2 0.1 256.3 18.2
263.1 15.4b 145.2 18.6c 4.3 0.1 253.2 21.8

Of the HM males breeding in 20022005, 16 (94%)
had black-capped mtDNA and 1 (6%) had Carolina
mtDNA, whereas among females, 16 (72%) had
black-capped mtDNA and six (27%) had Carolina
mtDNA (2 3.3, df 1, p 0.068).
Analysis of microsatellite genotypes from birds
breeding in 19982003 further showed that the three
sites differed with respect to the genetic identity of
their resident chickadeesand that the NF popula-
tion included predominantly hybrids. Hybrid index
scores ranged from 0.36 to 0.46 (x 0.41 0.03 SE,
n 45) at GM (more Carolina-like) and from 0.53 to
0.69 (x 0.60 0.04 SE, n 24) at HM (more black-
capped-like; Fig. 7.2). Resident chickadees at NF
had scores ranging from 0.40 to 0.58 (x 0.48 0.03
SE, n 145), with 63.9% having intermediate scores
falling between the upper and lower ranges of the
GM and HM populations respectively (Fig. 7.2).
Approximately 27.8% of NF individuals fell within
the GM score range whereas 8.3% fell within the
HM score range.
7.3.2 Song patterns beyond and within
hybrid zone
Song patterns were consistent with the assumption
that sites other than NF were outside of, or at the
extreme edge of, the hybrid zone. Among songs
sampled in 20002001 from GM and other Carolina
localities, all songs analyzed matched the typical
see-bee-see-bay Carolina chickadee song type (n 51
0.20
Proportion of each population
0.15
0.10
0.05
0.00
0.35
Figure 7.2 Hybrid index scores (IH ), based on microsatellite genotypes, of resident chickadees from three primary study sites in south-eastern
Pennsylvania. Values range from low for Carolina chickadees to high for black-capped chickadees. Vertical axis shows relative proportions among
individuals from each site; gray bars, GM (n 45); white bars, NF (n 145); black bars, HM (n 24).
B E H AV I O R A L A S P E C T S O F H Y B R I D I Z AT I O N 99
songs), except we recorded one bird in southern
Montgomery Co., Pennsylvania, that gave only
three-note songs (see-bay-see; n 13) representing
the Song Variant category of Smith (1972). All songs
in 20002001 (n 69) from areas occupied predom-
inantly or exclusively by black-capped chickadees,
including HM, represented the characteristic black-
capped fee-bee. Despite genetic evidence of intro-
gression at HM, this pattern had not changed as of
2005: we have yet to hear any HM male include
Carolina song, or even variant black-capped song
(see below), in his repertoire.
At the NF hybrid zone site, 80% of the songs
(n 813) produced by the 28 resident males in
20002001 matched the typical black-capped fee-bee.
Other songs observed, in declining order of occur-
rence, included: four-note typical Carolina song
(see-bee-see-bay; 9%); variant black-capped type
(e.g. fee-bee-bee; 5%); variant Carolina type (e.g. see-
bay-see-bay-see; 3%); and mixed song, combining
typical elements of both songs (2%) (Fig. 7.3 and
Rossano 2003).
Although songs at NF sounded superficially like
the typical songs of one of the parental species,
values of several variables differed between the
songs from NF relative to the corresponding
parental areas (Table 7.1). In particular, two-note
songs at NF differed from typical black-capped
fee-bee songs in having a shorter pause between the
notes. Four-note songs at NF differed from those of
typical Carolina chickadees in having shorter first
0.40 0.45 0.50 0.55 0.60 0.65 0.70
Hybrid Index scores
100 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

(a) 8

kHz 0

(b) 8

kHz 0

(c) 8

kHz 0
0 0.5 1.0 1.5
Seconds

Figure 7.3 Variant and mixed songs from the hybrid zone study site at Nolde Forest. (a) Example with quantitative characteristics of typical
black-capped fee-bee-ee but with repetition of bee-ee note. (b) Example with quantitative characteristics of typical Carolina chickadee see-bee
see-bay but with extra terminal see note. (c) Example of mixed song, with quantitative characteristics of typical Carolina chickadee see-bee-see
bay followed by bee-ee note of typical black-capped chickadee song.

notes and a shorter interval between the first and
second notes.
Of the 28 different NF males recorded in
20002001, 19 (68%) produced only typical black-
capped fee-bee songs and one gave normal black-
capped song and a black-capped variant. Six (21%)
of the males were bilingual, producing both two-
note black-capped song and four-note Carolina
song types. Two other bilingual birds (7%)
produced typical songs of both species as well as
mixed songs that included notes characteristic of
both species (Fig. 7.3).
Based on the number of notes sung (pending
detailed acoustic analysis), we detected a trend
toward increasing representation of bilingual
singing over time. When our observations began at
NF in 19971998, we detected no males that
produced Carolina-type songs. Birds including
aberrant or Carolina song types in their repertoires
appeared in 1999. Of the males examined in
20002001, 71% gave only black-capped songs
while 29% were bilingual (see above). Among
males breeding at NF in 2005 (n 45), the propor-
tion of males singing only two-note black-capped
song had declined to 47% (2 4.40, df 1,
p 0.036), while 53% of males gave both song
types (n 23 males) or only songs involving a mix
of note types from both species (n 1).
Song patterns at NF contrast with vocal behavior
in nearby Carolina chickadee populations in two

ways. First, we have yet to detect any NF males that
give only Carolina songs; vocally, the population
included black-capped males and bilingual or
mixed-song males, but no males with a pure
Carolina repertoire. Second, those males that are
bilingual produce only the four-note see-bee-see-bay
Carolina song type; we have not heard any male at
NF give any version of Song Variant (e.g. see-see-bay
bay-bay) that Carolina chickadees in south-eastern
Pennsylvania routinely include in their repertoire
(Smith 1972; R. Curry, unpublished data), whereas
all breeding males at GM have done so in every
year (19982005).
7.3.3 Chick-a-dee calls beyond and
within hybrid zone
Analysis of dee notes of black-capped and Carolina
chickadees (Fig. 7.4) revealed clear differentiation
(a) 8
kHz 0
(b) 8
kHz 0
(c) 8
2 Figure 7.4 Chick-a-dee calls from hybrid
kHz 0
0 0.5 1.0
Seconds
B E H AV I O R A L A S P E C T S O F H Y B R I D I Z AT I O N 101
between the parental species in all parameters
measured (Table 7.2; repeated measures ANOVA
and Tukeys HSD post-hoc contrasts, P 0.05)
except minimum frequency. Discriminant function
analysis (DFA) indicated that the variables most
informative for distinguishing between the two sets
of calls were duration, peak amplitude frequency,
and maximum frequency of the dee note. DFA cat-
egorized 46 (92%) of 50 calls recorded at black-
capped sites as black-capped (i.e. having a
probability of being black-capped 0.8). The four
calls categorized as Carolina were produced by a
single male at HM; this bird had black-capped
mtDNA but could have been a hybrid. Of the calls
recorded from Carolina chickadee localities
(n 81), 80 (99%) were categorized as Carolina.
The one other call was intermediate (probability of
being Carolina 0.74), produced by a bird that also
gave 14 other calls classified as Carolina.
zone study site (NF) categorized by
discriminant function analysis as: (a) black-
1.5 capped; (b) Carolina-like (0.5 probability of
being Carolina 0.8); and (c) Carolina.
102 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
Table 7.2 Quantitative characteristics of D notes of chick-a-dee calls at localities beyond and within the chickadee contact zone
Population dee duration (msec)
Black-cappeda (n 50 calls) 152 21
Nolde Forest (n 453) 114 13
Carolinab (n 81) 105 12
a
Includes samples from Hawk Mountain supplemented with recordings from Nova Scotia, Vermont, Massachusetts, and New York.
b
Includes samples from Great Marsh supplemented with recordings from Montgomery and Delaware Cos., Pennsylvania; Maryland; and North
Carolina.
We used the same DFA formula to categorize
calls (n 453), based on dee notes, from the 28
males at NF whose song were also recorded (see
above). Most calls (87%) at NF were Carolina (prob-
ability 0.8); 8% were Carolina-like (0.5 probabil-
ity 0.8); 3% were black-capped-like (0.5
probability 0.8); and 2% were black-capped.
All males at NF gave individual calls that varied
in their quantitative characteristics and thus fell
into different categories. Of the 28 males, 17 (61%)
produced exclusively calls categorized as Carolina
or Carolina-like. Three other males gave calls that
were mostly Carolina/Carolina-like (70% of indi-
viduals calls) with the remaining calls being black-
capped-like. The six other birds (21%) gave calls
spanning all types of calls, including at least a few
calls categorized as black-capped.
7.3.4 Lack of congruence between
songs and calls
Using the quantitative categorization of chick-a-dee
calls from DFA, there was no association between
an individuals song and call categories among 27
males at NF. Of the 20 males that produced only
black-capped chickadee song, 14 (70%) gave
Carolina-type calls and six (30%) gave variable
calls; among the eight males that sang both song
types or mixed songs, seven (88%) gave Carolina-
type calls and one (12%) gave variable calls
(2 4.40, df 1, P 0.31).
Similarly, we detected no significant differences
in dee note components between NF males that fell
into the two categories of singer. Therefore, there
was an overall pattern at NF of males producing
relatively normal black-capped songswith or
Peak amplitude Maximum frequency (kHz) Interval between
frequency (kHz) dee notes (msec)
3.9 0.5 5.0 0.8 62 16
4.2 0.3 5.8 0.6 49 12
4.1 0.4 5.8 0.6 48 15
without also singing Carolina-type songs in the
case of bilingual malesbut with all males giving
at least some chick-a-dee calls that were Carolina-
like, and with some doing so exclusively.
7.3.5 Relationships between behavior
and genetics
Vocal patterns in the contact zone at NF were not
correlated with genetic variation among individ-
uals. Among 23 males whose songs we categorized
and whose microsatellite genotypes we evaluated
(all of which had Carolina mtDNA), those giving
only black-capped songs had average hybrid index
scores (x 0.47 0.036 SD, n 16) that were simi-
lar to those of all other bilingual and mixed-song
males (n 7; x 0.48 0.037 SD; t 0.50,
df 20, P 0.63). Birds categorized as giving
Carolina-like calls also had hybrid index scores that
were no different (x 0.48 0.031 SD, n 17) from
scores for males categorized as producing inter-
mediate calls (x 0.46 0.031 SD, n 7; t 1.72,
df 22, P 0.10).
While vocal patterns at NF were not associated
with genetic variation, aspects of the mating
system varied in relation to male genotypes
(Reudink et al. 2006). Females at NF that engaged in
extrapair mating were socially paired with males
having higher hybrid index scores (i.e. more black-
capped-like) than the social mates of females
that did not produce any extrapair offspring.
Furthermore, extrapair sires had hybrid index
scores that were lower (more Carolina-like) than
those of corresponding social males. Because there
was no relationship between hybrid index scores
and vocalizations among NF males, it is unlikely

that this pattern of extrapair mating was influenced
by male vocal behavior, but we have not tested
these relationships directly.
7.4 Discussion
7.4.1 Hybridization in south-eastern
Pennsylvania
Our results indicate that extensive hybridization
occurs within the region sampled. The genetic data
reveal an overall difference between the GM and
HM populations, and intermediacy of chickadees at
NF; the results also provide evidence that the
contact zone is shifting northward (see also
Reudink et al. 2007). At NF, black-capped genes
appear to be decreasing in the population, while at
HM, birds with Carolina-like genotypes are increas-
ing. Because all individuals at GM already
had Carolina genotypes at the start of our study,
changes were not apparent there during our study,
but the absence as of 1998 of black-capped songs,
reported in the vicinity of GM in the 1960s (Ward
and Ward 1974), suggests that the southern edge of
the hybrid zone has shifted north as well. The
persistence at NF of some black-capped chickadee
genetic influence contemporaneous with appear-
ance of birds at HM carrying Carolina genes
indicates that the hybrid contact in south-eastern
Pennsylvania is at least 50 km wide.
The patterns in Pennsylvania are broadly consist-
ent with evidence from other portions of the chicka-
dee contact zone with respect to hybrid zone
structure and northward movement. Genetic data
suggest a somewhat narrower zone (30 km wide)
in Missouri and in the mountains of the Virginias
(with some evidence of introgression over longer
distances in these regions) and in north-central
Ohio (Sawaya 1990; Sattler and Braun 2000;
Bronson et al. 2005). The hybrid zone in Ohio is
believed to have moved ~100 km northward over
approximately 70 years (Bronson et al. 2005).
Our finding that a large percentage of resident
chickadees within the contact zone may be hybrids
also is consistent with other studies. In Missouri and
in the Virginias, the proportion of hybrids among
samples of 100 or fewer specimens was 44 to 58%
(Sawaya 1990; Sattler and Braun 2000). Determining
B E H AV I O R A L A S P E C T S O F H Y B R I D I Z AT I O N 103
whether genetic and behavioral variability at NF is
similar to that in other areas will require further
molecular work in Pennsylvania and additional
field study at the local level elsewhere.
7.4.2 Song patterns in the Pennsylvania
contact zone
A striking finding in our study was the retention of
black-capped chickadee songs at NF, where essen-
tially all resident adults are now hybrids (and
where some may be genetically pure Carolina
chickadees). Even those males with the ability to
sing at least one Carolina song type continue to
produce black-capped songs as well.
That existence of bilingual chickadees may
indicate interbreeding has been long assumed, with
some even suggesting that bilingual males in zones
of overlap might gain a functional advantage by
being able to deter rivals of both parental species
(Robbins et al. 1986). However, retention of black-
capped song long after hybridization has occurred
at a given site has not been appreciated previously.
This finding has implications for the accuracy of
distributional surveys, such as the breeding bird
atlas program, where judgments about residency
are often based primarily on songs heard. The
tendency for hybrid males to produce relatively
normal black-capped song underscores the likely
existence of developmental mechanisms that result
in song stereotypy across most of the black-capped
chickadees range, but the nature of those mech-
anisms remains unknown (Kroodsma et al. 1999).
A distinct but related aspect of vocal patterns in
the hybrid zone concerns production of aberrant
song types. Song variants are particularly rare in
most black-capped chickadee populations; excep-
tions may be restricted to isolated populations at the
geographic range limits (see Chapter 14). Defining
aberrant song in Carolina chickadees is more chal-
lenging, because of greater inherent variability
among and within populations in this species.
Regardless, the tendency for chickadees in contact
zone populations to produce songs not characteristic
of parental populations has been noted frequently.
Aberrant songs fall into two main categories: (1)
songs with the number of notes and pattern typical
of parental forms, but with different quantitative
104 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
characteristics; and (2) songs that combine notes of
the typical songs of both parental species. We
observed both of these song categories at NF,
although many malesincluding some bilingual
malesnever produced markedly aberrant songs.
However, our finding that some seemingly nor-
mal songs had some intermediate quantitative
characteristics matches results from Missouri
(Robbins et al. 1986) more so than those from the
Virginias, where the pattern was bimodal (Sattler
1996). Our study adds detail to understanding of
song patterns the hybrid zone by showing that
males producing relatively normal black-capped
songswith or without Carolina song as wellcan
have Carolina mtDNA, along with microsatellite
genotypes consistent with hybrid status.
The vocal and genetic patterns we detected
suggest that many chickadees in the contact zone,
but perhaps not all, are capable of learning
heterospecific songs. This finding is consistent with
previous findings that individuals of these species
can, when reared together, learn notes of the other
(Kroodsma et al. 1995). However, the specific mech-
anisms that cause some chickadees to become
bilingual while others continue to sing only black-
capped song remain to be determined.
7.4.3 Chick-a-dee calls across the hybrid zone
That the D notes of the black-capped chickadees
chick-a-dee call are longer in duration and lower in
pitch than those of the corresponding Carolina chicka-
dee call has been known for a long time (see Chapter
13). It is therefore surprising that this vocalization has
not previously received particular attention in relation
to the hybrid zone between the species, apart from an
unpublished thesis (Crock 1975). As Crock observed
using a broad geographic approach, we found that
parameters of D notes from the hybrid zone were
quantitatively intermediate on average. Our observa-
tion that individual chickadees in the hybrid zone
produce highly variable D notes is novel.
Two aspects of our results suggest that genetic and
environmental influences on development of calls
operate differently than those affecting song learning.
First, a disparity exists at NF between the average D
notes characteristics (mainly Carolina-like) at the
population level and the persistence of black-capped
song. Second, we observed mismatches at the level
of individual males that produced quantitatively
variable or intermediate calls, independent of the
song types that the same birds sang.
Several explanations for conflicting patterns are
possible. One is that songs are learned whereas call
development is subject to stronger genetic influence,
such that birds with hybrid genotypes produce
acoustically intermediate call notes. Alternatively,
development of both vocalizations may involve
learning (Chapters 10, 11, and 13), but with different
influences such as the age at which learning occurs
or the social context. Because song is primarily pro-
duced by males, chickadees could be learning the
song of their father or those of neighbor males. In
contrast, calls are produced by both sexes and
develop early in life; accordingly, chickadees could
learn their calls not only from their father but from
their mother, as might happen when she is brooding.
7.4.4 Potentially confounding variables in
analysis of vocal patterns
Our understanding of the vocal behavior of
hybridizing chickadees is limited in some respects,
because in our observational study we cannot
control for several potentially confounding vari-
ables. With respect to songs, an important factor is
our ability to thoroughly characterize the full reper-
toire of a large sample of breeding male chickadees
at each site. In general, male chickadees display
their full repertoire most reliably during dawn
chorus song bouts that they deliver close to active
nests, during the phase of the breeding season
when females have begun laying eggs or are within
a few days of beginning to do so (see Chapter 14).
However, male chickadees at NF do not seem to
participate consistently in the dawn chorus, even
during the critical period of the breeding season;
characterizing song repertoires therefore has had to
depend additionally on observations throughout
the day, when each male sings intermittently
throughout its territory. While we continue to
investigate this impression, we can be confident
about characterizing males as bilingual once we
observe production of both black-capped and
Carolina song; we can, however, be less certain
that males that we classify as producing only

black-capped song are not in fact bilingual.
Similarly, our ability to determine precisely which
males produce aberrant or mixed songs is likely
dependent on the sample size of songs of each bird.
The number of songs recorded at high sound qual-
ity also influences our ability to characterize fully
the relatively subtle variation in quantitative song
parameters, above and beyond the major categories
based on note number, duration, and pitch.
However, because we can easily identify nearly all
notes as either black-capped-like or Carolina-like,
we believe that our conclusions about general
patterns of vocal variationincluding especially
the persistence of black-capped song types, and the
absence to date of the Song Variant version of the
Carolina song, in the hybrid zoneare robust.
Assessing vocal variation with respect to other
chickadee calls is even more challenging because of
the inherent complexity of chickadee vocal reper-
toires. Even when focusing only on the chick-a-dee
call, many sources of variation come into play. Our
population-level averages for the D notes, especially
given relatively small sample sizes, could incorp-
orate biases caused by inadvertently sampling
different proportions of males and females, birds of
different flocks, calls produced in different contexts,
or notes taken from calls that vary in overall syn-
taxall factors that may influence note structure
(see Chapter 13). The same considerations apply to
our characterization of calls at the level of individual
birds, along with an even greater challenge regard-
ing adequate sampling. Nevertheless, we are confi-
dent of the overall conclusion that mismatches exist
at NF between black-capped/bilingual singing and
Carolina-like calls. Recent observations offer further
support: in 200506, many large chickadees with
black-capped plumage wintered at NF as part of a
major regional irruption. We easily distinguished
these individuals, based on calls, from the local
(hybrid) residents; mtDNA data have invariably
confirmed that the irruption birds had black-capped
chickadee haplotypes.
7.4.5 Completing the behavioral picture
of chickadee hybridization
The finding that black-capped chickadee song
persists in a hybridizing population, coupled with
B E H AV I O R A L A S P E C T S O F H Y B R I D I Z AT I O N 105
documented patterns of extrapair paternity
(Reudink et al. 2006), suggests that chickadees in
the hybrid zone probably do not base mating deci-
sions on song categories. Pairing in chickadees
generally occurs within winter flocks, long before
males sing actively at the start of the nesting season
(see Chapter 9). It is therefore unlikely that a
females choice of a social mate would be based on
the males song repertoire.
However, extrapair mating decisions could be
influenced by the singing behavior of males in the
hybrid zone, as in allopatric populations of black-
capped chickadees (Chapter 14). We are currently
investigating whether differences exist in the
tendency to engage in extrapair mating between
females socially paired with bilingual males versus
males that sing only black-capped song. Regardless
of whether such a pattern exists, it is unlikely to be
correlated with the previously observed tendency
(Reudink et al. 2006) for females paired with black-
capped-like males to engage in extrapair mating,
and to do so with Carolina-like extrapair mates,
because there does not appear to be an association
between genetic identity and song types in the NF
population. Still, it will be interesting to assess
whether females could use song as a honest signal
of male quality within the hybrid zone, as might be
true if the vocal performance of hybrid males were
impaired by developmental stress (Nowicki and
Searcy 2005).
7.5 Hybridization throughout the
Paridae
7.5.1 Other examples in North America
While the extended contact zone between black-
capped and Carolina chickadees has been studied
most intensively, three other examples of inter-
breeding among North American Paridsall
involving sibling species pairsalso have been
examined in some detail. Mountain and black-
capped chickadees hybridize at least occasionally
in western North America, where their geographic
ranges overlap broadly (McCallum 1998).
However, these species remain ecologically sep-
arated by differences in habitat use (Hill and Lein
1989 Chapter 8); the circumstances leading to
106 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
hybridization remain to be worked out. Tufted and
black-crested titmice hybridize in a narrow zone in
Texas and were formerly considered conspecific,
but the combination of geographic stability of the
contact zone, genetic distinctiveness, and vocal dif-
ferences have supported their treatment as separate
species (Banks et al. 2002). Similarly, oak and
juniper titmice in the western United States were
formerly considered conspecific (plain titmouse)
until recent work revealed a low incidence of
hybridization in a small area of secondary contact
in north-eastern California (Cicero 1996, 2004).
Whether songs and calls, which differ between
these titmice (Cicero 2000), serve as barriers to
hybridization is a subject of current study.
Opportunities exist for research on potential
hybridization (or the avoidance of interbreeding) in
several other pairs of New World Parids that are at
least partly sympatric. No studies have explored in
detail breeding relationships between any species
pairs within the clade of brown-capped chickadees
(see Gill et al. 2005). Hybridization in the past
between chestnut-backed and boreal chickadees
represents one possible explanation for phylogeo-
graphic patterns (Chapter 6), but barriers to inter-
breeding between these sibling species have not
been investigated. The lack a whistled song in the
brown-capped species suggests that song recogni-
tion cannot serve as a primary isolating mechanism.
Boreal chickadees also are not known to hybridize
with Siberian tits where these species co-occur in
Alaska (Ficken et al. 1996), but knowledge of the
latter species in North America is limited (Hailman
and Haftorn 1995). Similarly, no study has investi-
gated reasons why black-capped chickadees appar-
ently never interbreed with boreal chickadees,
though the species have broadly overlapping
geographic ranges and habitat preferences that are
shared at least in part. A parallel situation exists
between mountain and chestnut-backed chickadees;
again, no hybridization has been observed
(McCallum 1998) but further study is merited.
Sympatric overlap occurs between juniper and
bridled titmice in Arizona, at the southern extreme
of the formers range, but no hybridization has been
reported (Nocedal and Ficken 1998).
Other combinations of sympatric Parids in North
America involve titmouse/chickadee pairs, such as
bridled titmouse with Mexican chickadee; oak or
juniper titmice with black-capped chickadees; or
tufted titmouse with Carolina or black-capped
chickadees. Hybridization appears to be exceed-
ingly rare in these cases, despite large areas of geo-
graphic overlap; the only known example involved
a black-capped chickadee tufted titmouse cross
(Cockrum 1952). The rarity of such matings is
unsurprising given that titmice typically are at least
50% larger than sympatric chickadees, except in the
case of bridled titmouse and Mexican chickadee,
which differ little in size but greatly in appearance.
7.5.2 Hybridization among Eurasian
Parids
Observations of mixed breeding pairs, or of pheno-
typically intermediate individuals, have provided
evidence for hybridization among numerous
European and Asian Parids. Rare hybridization,
implied by anecdotal reports of mixed pairs or
intermediate specimens, has involved willow
marsh tit; willow coal tit; willow crested tit;
coal crested tit; blue great tit; marsh great tit;
great coal tit; and willow varied tit (reviewed
by Harrap and Quinn 1995; Curry 2005 McCarthy
2006). Interbreeding occurs more frequently between
Siberian and willow tits in Finnish Lapland where
the former species is rare and the latter is more
common (Jrvinen 1997), an example illustrating a
general principle that large differences in relative
abundance facilitate hybridization in passerines
(Randler 2002). Blue, azure, and yellow-bellied tits
exhibit a complex pattern: hybridization between
the former two species has occurred following
irruptive movements or range expansion of azure
tit into the blue tits range, whereas azure and yel-
low-bellied tits, which some consider conspecific,
appear to maintain a more stable contact zone; the
case is complicated by evidence suggesting that
azure tits are evolutionarily nested within the blue
tit clade (Salzburger et al. 2002). In a different case
involving sibling species, a stable contact zone
appears to exist between coal tits and black-crested
tits in Nepal (Lhrl 1994; but see Harrap and Quinn
1995:302). Until recently, the great tit was con-
sidered a ring species exhibiting terminal contact in
Siberia, in addition to hybridization with the

Turkestan tit in Central Asia. However, comprehen-
sive analysis of genetic, morphological, and vocal
patterns support separation into three species
great tit (including the Turkestan tit), Japanese tit,
and cinereus titwith five different contact zones
(Pckert et al. 2005).
Analysis of hybridization has progressed to
analysis of potential isolating mechanisms in stud-
ies of several Eurasian Parids, with a major focus
on songs (reviewed by Martens 1996). In south-
western Germany, blue tits do not respond territor-
ially to normal songs of azure tits, but they
sometimes react to artificially constructed combin-
ations of azure tit notes; natural similarity in song
appears sufficient to permit heterospecific pairing,
but no introgression, where both species occur at
low density (Martens and Schottler 1991).
Breakdown of species recognition based on song
also has been suggested to account for hybridiza-
tion between great and Japanese tits in Siberia
(Pckert et al. 2005). Intraspecific vocal variation
within willow tits is particularly complex (Martens
1996). Two song types, alpine and lowland,
have been identified based on note structure; in
Central Europe, populations whose males sing only
one version are parapatrically separated. However,
throughout much of the northern and eastern range
of the species, males of the Siberian song
category are bilingual with respect to the two
song types, as they are in some local European
populations where interbreeding occurs between
song types. Full understanding of this system
awaits research focused on the responses of
both males (as rivals) and females (as mates) to
individual males as a function of their song type(s).
In contrast, there is less differentiation in song than
in morphology in coal and black-crested tits
(Martens 1996).
Mechanisms that facilitate heterospecific pairing
can be explored by cross-fostering, an approach
that has been pursued recently using blue and great
tits. Cross-fostered blue and great tit males both
react territorially to heterospecific intruders
(Hansen and Slagsvold 2003). Blue tits reared by
great tits have normal pairing success but occasion-
ally pair with great tits; in contrast, great tits raised
by blue tits suffer low pairing success, and the few
that pair do so with blue tits (Slagsvold et al. 2002).
B E H AV I O R A L A S P E C T S O F H Y B R I D I Z AT I O N 107
Cross fostering tends to reduce dominance status
(Hansen and Slagsvold 2004), which could indir-
ectly affect the tendency to be chosen as a mate;
females that pair with cross-fostered males do not,
however, engage in elevated rates of extrapair
paternity (Johannessen et al. 2005).
Though blue and great tits seldom hybridize in
nature, the cross-fostering work is relevant to the
study of Parid hybridization in two ways. First, the
experiments explore one possible mechanism for
the initial stage of interbreeding, that is interspe-
cific egg-dumping or brood takeover, followed by
sexual misimprinting and heterospecific mate
choice (Slagsvold and Hansen 2001). Second,
results demonstrate that exposure to both adults
and nestmates of another species during an indi-
viduals development can have diverse and long-
lasting effects on its subsequent behavior and
success. The work suggests that far-reaching
imprinting effectson vocalizations, dominance,
mate preferences, and moreshould be expected
as well during naturally occurring hybridization.
7.6 Future directions
The largest gap in understanding of the behavioral
ecology of hybridization in chickadees concerns
dominance interactions and their relationships with
both social pairing and extrapair mating. To date, no
thorough field study of dominance relationships
has been completed within any part of the contact
zone. Bronson et al. (2003b) found a tendency for
Carolina-like males in aviaries to dominate black-
capped males, and for females of both species to
associate with the dominant Carolina males.
However, proximate mechanisms involved in nei-
ther establishment of dominance nor mate choice by
females were examined as part of the study.
Furthermore, because the work was carried out
using captive birds, its relevance for understanding
patterns and mechanisms in the field is not yet
known (Curry 2005).
The preceding discussion underscores a paucity
of available information about relationships
between vocal patterns, dominance relationships,
and mating systems in Parid hybrid zones. Because
chickadees give calls at all times of the year,
those vocalizations potentially play a greater
108 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
role in establishing or maintaining dominance
relationships than do the songs that chickadees
give only in the spring, after pairs have already
become established. However, several other
factors besides vocal behavior could be important
determinants of dominance, and thus of any
mating patterns dependent on dominance; these
include, but are not limited to, age and plumage
brightness (Chapter 9).
An important question is whether song invari-
ably trumps other cues as the predominant etho-
logical isolating mechanism in the Paridae, as has
been accepted by European investigators (Martens
1996). That two distantly related North American
chickadees with different songs can continue to
hybridize challenges this viewunless the ability
to learn the others song, perhaps because both
retain ancestral song characteristics, facilitates
interbreeding through sexual misimprinting. The
importance of vocalizations relative to other influ-
ences, including calls and social dominance, on
mating decisions in hybridizing Parids can only be
assessed through further research that addresses
these relationships directly, as we are attempting to
do in our ongoing studies of chickadees.
Acknowledgments
We thank The Nature Conservancy, Pennsylvania
Bureau of State Parks, and Hawk Mountain
Sanctuary for permission to work on their proper-
ties. We are indebted to S. L. Guers for field work
that yielded many HM blood samples and to
S. G. Mech for critical help with molecular data
analyses; S. P. Mullen and K. L. Cornell also
contributed significantly through their M.S. thesis
projects. For additional assistance, we thank:
N. A. Lucchi, A. Nicodemus, L. Massarelli,
A. Ruscica, S. Slattery, S. Van Pelt, C. Yuan, M. N.
Weber, K. Whittemore, C. Zecchine, and R. Zitnay.
Villanova University provided primary funding;
MWR also received student research grants from the
American Ornithologists Union, the Frank
M. Chapman Memorial Fund, Sigma Xi, and the
Animal Behavior Society. We thank Theresa Burg,
Tom Grubb, and Ken Otter for comments on the
manuscript. Hawk Mountain Sanctuary contribu-
tion to conservation science number 137.
References
Baker, M. C., Baker, M. S. A., and Gammon, D. E. (2003).
Vocal ontogeny of nestling and fledgling black-capped
chickadees Poecile atricapilla in natural populations.
Bioacoustics, 13, 265296.
Banks, R. C., Cicero, C., Dunn, J. L., Kratter, A. W.,
Rasmussen, P. C., Remsen, J. V., Jr, Rising, J. D., and
Stotz, D. F. (2002). Forty-third supplement to the
American Ornithologists Union Check-list of North
American Birds. Auk, 119, 897906.
Braun, M. J. and Robbins, M. B. (1986). Extensive protein
similarity of the hybridizing chickadees Parus atricapil-
lus and P. carolinensis. Auk, 103, 667675.
Bronson, C. L., Grubb, T. C., Jr, and Braun, M. J. (2003a). A
test of the endogenous and exogenous selection
hypothesis for the maintenance of a narrow avian
hybrid zone. Evolution, 57, 630637.
Bronson, C. L., Grubb, T. C., Jr, Sattler, G. D., and Braun, M. J.
(2003b). Mate preference: a possible causal mechanism for
a moving hybrid zone. Animal Behaviour, 65, 489500.
Bronson, C. L., Grubb, T. C., Jr, Sattler, G. D., and Braun,
M. J. (2005). Reproductive success across the black-
capped (Poecile atricapillus) and Carolina chickadee
(P. carolinensis) hybrid zone in Ohio: implications for
characterization of hybrid zones based on genetic
indices. Auk, 122, 759772.
Charrier, I. and Sturdy, C. B. (2005). Call-based species
recognition in black-capped chickadees. Behavioral
Processes, 70, 271281.
Cicero, C. (1996). Sibling species of titmice in the Parus
inornatus complex. University of California Publications in
Zoology, 128, 1217.
Cicero, C. (2000). Oak titmouse (Baeolophus inornatus) and
juniper titmouse (Baeolophus ridgwayi). In: Poole, A. and
Gill, F., eds. The Birds of North America, No. 485, pp.
128. The Birds of North America, Inc., Philadelphia.
Cicero, C. (2004). Barriers to sympatry between avian
sibling species (Paridae: Baeolophus) in local secondary
contact. Evolution, 58, 15731587.
Cockrum, E. L. (1952). A check-list and bibliography of
hybrid birds in North America north of Mexico. Wilson
Bulletin, 64, 140159.
Crock, M. A. (1975). Competition and Chickadee Vocalizations:
Displacement and Convergence. M.S. thesis, University of
Pittsburgh.
Curry, R. L. (2005). Hybridization in chickadees: much to
learn from familiar birds. Auk, 122, 747758.
Ficken, M. S., McLaren, M. A., and Hailman, J. P. (1996).
Boreal Chickadee. In: Poole, A. and Gill, F. B., eds. The
Birds of North America, No. 254, pp. 123. The Academy
of Natural Sciences, Philadelphia.

Gill, F. B., Slikas, B., and Sheldon, F. H. (2005). Phylogeny
of titmice (Paridae): II. Species relationships based on
sequences of the mitochondrial cytochrome b gene. Auk,
122, 121143.
Grant, P. R. and Grant, B. R. (1997). Hybridization, sexual
imprinting, and mate choice. American Naturalist, 149,
128.
Grubb, T. C., Jr, and Bronson, C. L. (1995). Artificial snags
as nesting sites for chickadees. Condor, 97, 10671070.
Hailman, J. P. and Ficken, M. S. (1996). Comparative
analysis of vocal repertoires, with reference to chicka-
dees. In: Kroodsma, D. E. and Miller, E. H., eds. Ecology
and Evolution of Acoustic Communication in Birds, pp.
136159. Comstock/Cornell University Press, Ithaca,
New York, USA.
Hailman, J. P. and Haftorn, S. (1995). Siberian tit. In: Poole,
A. and Gill, F., eds. The Birds of North America, No. 196,
pp. 124. The Academy of Natural Sciences,
Philadelphia.
Hansen, B. T. and Slagsvold, T. (2003). Rival imprinting:
interspecifically cross-fostered tits defend their territor-
ies against heterospecific intruders. Animal Behaviour,
65, 11171123.
Hansen, B. T. and Slagsvold, T. (2004). Early learning
affects social dominance: interspecifically cross-fostered
tits become subdominant. Behavioral Ecology, 15,
262268.
Hansen, M. M., Ruzzante, D. E., Nielsen, E. E., and
Mensberg, K.-L. E. (2000). Microsatellite and mitochon-
drial DNA polymorphism reveals life-history depend-
ent interbreeding between hatchery and wild brown
trout (Salmo trutta L.). Molecular Ecology, 9, 583594.
Harrap, S. and Quinn, D. (1995). Chickadees, Tits,
Nuthatches and Treecreepers. Princeton University Press,
Princeton, New Jersey.
Hill, B. G. and Lein, M. R. (1989). Territory overlap and
habitat use of sympatric chickadees. Auk, 106, 259268.
Irwin, D. E. and Price, T. (1999). Sexual imprinting, learn-
ing and speciation. Heredity, 82, 347352.
Jrvinen, A. (1997). Interspecific hybridization between the
Siberian tit Parus cinctus and the willow tit Parus montanus
produces fertile offspring. Ornis Fennica, 74, 149152.
Johannessen, L. E., Slagsvold, T., Hansen, B. T., and
Lifjeld, J. T. (2005). Manipulation of male quality in wild
tits: effects on paternity loss. Behavioral Ecology, 16,
747754.
Johnston, D. W. (1971). Ecological aspects of hybridizing
chickadees (Parus) in Virginia. American Midland
Naturalist, 85, 124134.
Kroodsma, D. E., Albano, D. J., Houlihan, P. W., and Wells,
J. A. (1995). Song development by black-capped
chickadees (Parus atricapillus) and Carolina chickadees
(P. carolinensis). Auk, 112, 2943.
B E H AV I O R A L A S P E C T S O F H Y B R I D I Z AT I O N 109
Kroodsma, D. E., Byers, B. E., Halkin, S. L., Hill, C.,
Minis, D., Bolsinger, J. R., Dawson, J.-A., Donelan, E.,
Farrington, J., Gill, F. B., Houlihan, P., Innes, D., Keller,
G., Macaulay, L., Marantz, C. A., Ortiz, J., Stoddard, P.
K., and Wilda, K. (1999). Geographic variation in black-
capped chickadee songs and singing behavior. Auk, 116,
387402.
Kvist, L., Ruokonen, M., Orell, M., and Lumme, J. (1996).
Evolutionary patterns and phylogeny of tits and chicka-
dees (genus Parus) based on the sequence of the
mitochondrial cytochrome b gene. Ornis Fennica, 73,
145156.
Lhrl, H. (1994). Contribution to the still unsettled ques-
tion complex of hybridization between coal tit and
black-crested tit (Parus ater, P. melanolophus) (Aves:
Passeriformes: Paridae). Zoologische Abhandlungen
(Dresden), 48, 149157.
Mammen, D. L. and Nowicki, S. (1981). Individual differ-
ences and within-flock convergence in chickadee calls.
Behavioral Ecology and Sociobiology, 9, 179186.
Martens, J. (1996). Vocalizations and speciation of palearc-
tic birds. In: Kroodsma, D. E. and Miller, E. H., eds.
Ecology and Evolution of Acoustic Communication in Birds,
pp. 221240. Comstock/Cornell University Press,
Ithaca, New York, USA.
Martens, J. and Schottler, B. (1991). Acoustic barriers
between azure tit Parus cyanus and blue tit Parus
caeruleus? Journal fr Ornithologie, 132, 6180.
McCarthy, E. M. (2006). Handbook of avian hybrids of the
world. Oxford University Press, Oxford.
McCallum (1998). Mountain chickadee. In: Poole, A. and
Gill, F. B., eds. Birds of North America, No. 254, pp. 128.
Academy of Natural Sciences, Philadelphia.
Mostrom, A. M., Curry, R. L., and Lohr, B. (2002). Carolina
chickadee. In: Poole, A. and Gill, F., eds. The Birds of
North America, No. 636, pp. 128. The Birds of North
America, Inc., Philadelphia.
Nocedal, J. and Ficken, M. (1998). Bridled titmouse. In: Poole,
A. and Gill, F., eds. The Birds of North America, No. 375, pp.
120. The Birds of North America, Inc., Philadelphia.
Nowicki, S. (1989). Vocal plasticity in captive black-
capped chickadees: the acoustic basis and rate of call
convergence. Animal Behaviour, 37, 6473.
Nowicki, S. and Searcy, W. A. (2005). Song and mate
choice in birds: how the development of behavior helps
us understand function. Auk, 122, 114.
Pckert, M., Martens, J., Eck, S., Nazarenko, A. A.,
Valchuk, O. P., Petri, B., and Veith, M. (2005). The great
tit (Parus major)a misclassified ring species. Biological
Journal of the Linnean Society, 86, 153174.
Pritchard, J. K., Stephens, M., and Donnelly, P. (2000).
Inference of population structure using multilocus
genotype data. Genetics, 155, 945959.
110 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
Randler, C. (2002). Avian hybridization, mixed pairing
and female choice. Animal Behaviour, 63, 103119.
Reudink, M. W., Mech, S. G., and Curry, R. L. (2006).
Extra-pair paternity and mate choice in a chickadee
hybrid zone. Behavioral Ecology, 17, 5662.
Reudink, M. W., Mech, S. G., Mullen, S. P. and Curry, R. L.
(2007). Structure and dynamics of the hybrid zone
between Black-capped and Carolina chickadees in
southeastern Pennsylvania. Auk, 124, in press.
Robbins, M. B., Braun, M. J., and Tobey, E. A. (1986).
Morphological and vocal variation across a contact
zone between the chickadees Parus atricapillus and P.
carolinensis. Auk, 103, 655666.
Rossano, L. M. (2003). Vocal Patterns of Black-Capped and
Carolina Chickadees Hybridization in Southeastern
Pennsylvania. M.S. thesis, Department of Biology,
Villanova University.
Salzburger, W., Martens, J., and Sturmbauer, C. (2002).
Paraphyly of the blue tit (Parus caeruleus) suggested
from cytochrome b sequences. Molecular Phylogenetics
and Evolution, 24, 1925.
Sattler, E. D. (1996). The Dynamics of Vocal, Morphological
and Molecular Interaction Between Hybridizing Black-
Capped and Carolina Chickadees (Parus atricapillus, Parus
carolinensis). Ph.D. dissertation, Department of Zoology,
University of Maryland.
Sattler, G. D. and Braun, M. J. (2000). Morphometric
variation as an indicator of genetic interactions
between black-capped and Carolina chickadees at a
contact zone in the Appalachian Mountains. Auk, 117,
427444.
Sawaya, P. L. (1990). A Detailed Analysis of the Genetic
Interaction at a Hybrid Zone Between the Chickadees Parus
atricapillus and P. carolinensis as Revealed by Nuclear and
Mitochondrial DNA Restriction Fragment Length Variation.
Ph.D. dissertation, Department of Biological Sciences,
University of Cincinnati.
Slagsvold, T. and Hansen, B. T. (2001). Sexual imprinting
and the origin of obligate brood parasitism in birds.
American Naturalist, 158, 534367.
Slagsvold, T., Hansen, B. T., Johannessen, L. E., and
Lifjeld, J. T. (2002). Mate choice and imprinting in birds
studied by cross-fostering in the wild. Proceedings of the
Royal Society B, 269, 14491455.
Smith, S. M. (1993). Black-capped chickadee. In: Poole, A.,
Stettenheim, P., and Gill, F., eds. The Birds of North
America, No. 39, pp. 118. The Academy of Natural
Sciences, Philadelphia.
Smith, S. T. (1972). Communication and other social
behavior in Parus carolinensis. Publications of the Nuttall
Ornithological Club, 11, 1125.
ten Cate, C. and Vos, D. R. (1999). Sexual imprinting and
evolutionary processes in birds: a reassessment.
Advances in the Study of Behavior, 28, 131.
Ward, R. (1966). Regional variation in the song of the
Carolina chickadee. Living Bird, 5, 127150.
Ward, R. and Ward, D. A. (1974). Songs in contiguous
populations of black-capped and Carolina chickadees
in Pennsylvania. Wilson Bulletin, 86, 344356.
Weisman, R. and Ratcliffe, L. (1989). Absolute and relative
pitch processing in black-capped chickadees, Parus atri-
capillus. Animal Behaviour, 38, 685692.
 CHAPTER 8
Life in the small-bodied cavity-nester
guild: Demography of sympatric
mountain and black-capped
chickadees within nest web
communities under changing
habitat conditions
Kathy Martin and Andrea R. Norris
8.1 Introduction
8.1.1 Parids as members of the nest web
Parids live in cavity-nesting vertebrate communi-
ties that are structured by hierarchical guilds called
nest webs, whereby some species depend on others
to produce cavities (a critical resource) for breeding
or roosting, and interspecific and intraspecific
interactions are centered around nest-site availabil-
ity (Martin and Eadie 1999). Eurasian and North
American Parids contain both excavating and non-
excavating species, with some exhibiting consider-
able intraspecific variation in mode of cavity
acquisition (Monkkonen and Orell 1997). There are
reproductive costs and benefits associated with
nesting in newly excavated cavities: an energy
expenditure such as excavation at the beginning of
the breeding season may limit nest initiation date
and clutch size, however high competition for
previously excavated cavities may be avoided by
excavation, and parasite loads are typically lower
in newly excavated cavities (Moller 1993;
Monkkonen and Orell 1997; Wiebe et al. 2006).
These trade-offs may be weighted differently in
closely-related, competing species that occur
sympatrically, leading to niche partitioning of
excavators and non-excavators.
In a cluster analysis of nest-tree size and cavity
characteristics for a cavity-nester community of
over 40 species of vertebrates in interior British
Columbia, mountain chickadees, black-capped
chickadees, downy woodpeckers (Picoides pubes-
cens), and red-breasted nuthatches (Sitta canadensis)
formed one of five clusters, namely the smallest-
bodied cavity-nesters (Martin et al. 2004). This
group used the smallest diameter of trees, with the
most advanced decay and the smallest cavity
entrance holes for nesting (Martin et al. 2004). With
overlap in both foraging habits and nest-site
selection among the small-bodied cavity-nesters,
there is considerable scope for facilitation, competi-
tion, and consequent niche partitioning patterns of
resources. These strong inter- and intraspecific
ecological dependencies may vary with habitat
features such as forest type, stage, and condition,
and temporal variation in resource availability.
The purpose of this chapter is to discuss the role
and ecology of two chickadee species as members
of the small-bodied cavity-nester guild and their
general relationships in the nest web community.
We examine the ecological and environmental
factors that might explain demographic changes by
asking the general question of how changes in
community dynamics and habitat characteristics
111
112 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
influence population density and nest-site selection
of the Parids. Within the nest web community,
positive interspecific interactions may result from
diverse species assemblages, where cavity excava-
tors may enhance or facilitate the breeding condi-
tions for secondary cavity-nesters. In interior
British Columbia, population densities of chicka-
dees and other small cavity-nesters (competitors,
facilitators) and predators varied annually across a
range of habitat stands, but most showed substan-
tial increases in breeding density over the past
decade. Since these population increases were
correlated with changes in habitat condition, we
address how habitat use and nest-site selection
change with density. We approached this problem
at the level of the individual (nest-site selection)
and at the stand level (chickadee population
growth rates) in relation to nesting densities of
other members in the cavity-nester community and
changing habitat characteristics.
8.1.1.1 Mountain chickadees
Mountain chickadees are small-bodied, secondary-
cavity-nesting birds, common in montane forests in
western North America (McCallum et al. 1999).
Typically, they use coniferous trees for foraging and
aspen trees for nesting (Hill and Lein 1989; Aitken
et al. 2002). In a long-term study on mountain
chickadee populations in Northern California, nest
box occupancy was highest in open pine stands
(Dahlsten et al. 1992). In the Cariboo-Chilcotin
region of central British Columbia, mountain
chickadees are abundant, year-round residents
that typically occupy stands of mixed coniferous-
deciduous forest, especially where Douglas-fir
(Pseudotsuga menziesii), lodgepole pine (Pinus
contortus), and quaking aspen (Populus tremuloides)
are present (K. Martin, unpublished data). They are
the most abundant breeding Parid, with detections
ranging from 0.05 to 0.24 birds/ha over a 10-year
period and a doubling in detection rates in the
past 3 years (Figure 8.1a). The increased rate of
detections was accompanied by a tripling in the
number of nests located since 2001 (Figure 8.1b).
Since mountain chickadees are abundant, have
strongly increased in density, yet rarely excavate,
they are strong consumers of small cavities
and must compete with other small-bodied
cavity-nesters to obtain suitable holes in dead or
decaying aspen trees (Aitken et al. 2002).
8.1.1.2 Black-capped chickadees
Black-capped chickadees, about the same size and
mass as mountain chickadees (~1011 g mass), are
excavating Parids that inhabit a range of deciduous
and mixed forest habitats across North America
(Smith 1993). In central BC, black-capped chickadee
detections and nesting densities also increased
across the study but they always remained at about
one-third or lower abundance than mountain
chickadees (Figure 8.1). We found between four
and ten nests annually (Figure 8.1b). Black-capped
chickadees completely excavated about 77% of the
26 cavities located and another 15% of nests were in
natural holes (branch limb holes) with occasional
use of a cavity excavated by a downy woodpecker
or sapsucker (Table 8.1). Here, as in other regions,
black-capped chickadees did not reuse any existing
chickadee-excavated cavities (Smith 1993; Aitken
et al. 2002). Since black-capped chickadee densities
are low in the area and their cavities tend not to be
reused, their excavation activities are not expected
to influence mountain chickadee populations.
However, as black-capped chickadees tend to be
dominant when the two species coexist, we
expected their presence would alter settlement
patterns in mountain chickadees (Minock 1972; Hill
and Lein 1988, 1989).
8.1.1.3 Possible competitors of chickadees
The red-breasted nuthatch, with similar size and
weight to the chickadees (~1011 g mass), is a good
excavator, similar to black-capped chickadees, and
has preferences for coniferous habitat similar to
mountain chickadees (Ghalambor and Martin
1999). Unlike black-capped chickadees, however,
red-breasted nuthatches use old cavities approxi-
mately 51% of the time (9 years; n 173 nests
where cavity freshness was known; K. Martin,
unpublished data), directly competing with moun-
tain chickadees for cavity resources. The red-
breasted nuthatch distribution extends across the
boreal forest of Canada and south to the south-west
and Appalachian Mountains, with a preference for
fir and spruce forests (Ghalambor and Martin
1999). In our study, nuthatch detection rates
 S M A L L - B O D I E D C AV I T Y- N E S T E R G U I L D S 113

Parids
Mountain chickadee
(a) Black-capped chickadee
0.45 Competitors/Predators
Red-breasted nuthatch
0.4 Red squirrel
Average individuals per ha

0.35 Facilitators
Downy woodpecker
0.3 Red-naped sapsucker
0.25

0.2
0.15
0.1
0.05
0
1995 1996 1997 1998 1999 2000 2001 2002 2003 2004

(b)
60
Black-capped chickadee
Downy woodpecker
50
Red-naped sapsucker
Red-breasted nuthatch
40 Mountain chickadee
Number of nests

30

20

10

0
1995 1996 1997 1998 1999 2000 2001 2002 2003 2004

Figure 8.1 (a) Relative densities of chickadees, other small cavity-nesters, and red squirrels in Interior British Columbia across 26 forested sites
as measured by point count detections. (b) Numbers of nests of small cavity-nesting birds found on the same sites. Field data collected from May
through July. Fixed 50 m radius point counts completed from 05000930 hours for 6 min using observation and playback methods to measure
detections. We located nests by systematic nest searches across sites and recorded nest and tree characteristics, and, when possible, determined
which species made the cavity. Because cavity-nesters reused cavities and nest-trees in multiple years (Aitken et al. 2002), we checked existing
cavities and searched for new cavities (trees marked with numbered tags to facilitate relocation). Occupied cavities (contained at least one
offspring) were located by visual inspection of cavities or by looking or listening for excavation, behavior of adult birds, nestling begging, or
other activities.

doubled, similar to mountain chickadees, and (Figure 8.1). Nuthatches and both chickadee species
nesting densities increased from fewer than 10 coexisted on all study sitesdetected via point-
nests annually early in the study to 40 in 2004 count observationsand all three species nested on
 114
R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
Table 8.1 The small cavity-nester sub-nest web: nest flow for small cavity-nesters and the species that excavated their cavity

Nesting species Excavator species Knot-hole Total nests

Mountain Black- Red- Downy Red- Hairy American Northern Pileated

chickadee capped breasted woodpecker naped woodpecker three-toed flicker woodpecker
chickadee nuthatch sapsucker woodpecker

Mountain chickadee 0.01 0.01 0.23 0.17 0.40 0.04 0.02 0.02 0 0.11 163
Black-capped chickadee 0 0.77 0 0.04 0.04 0 0 0 0 0.15 26
Red-breasted nuthatch 0 0 0.77 0.08 0.05 0 0.04 0.01 0 0.05 167
Downy woodpecker 0 0 0 1.00 0 0 0 0 0 0 39
Red-naped sapsucker 0 0 0 0 0.99 0 0 0 0 0 270
Red squirrel 0 0 0.03 0 0.40 0.20 0.02 0.20 0.03 0.12 60
Total cavities 2 22 169 82 376 21 13 289 6 52 562

88% of our sites (although not always in the
same year; K. Martin, unpublished data). Since
nuthatches are common in the area and excavate
new cavities regularly, we expected nuthatch
population increases to facilitate nesting densities
and population growth rates of mountain chicka-
dees in years following nuthatch increases, but to
negatively impact nesting densities where they
overlap spatially and temporally, due to competi-
tion for foraging and cavity resources.
8.1.2 Facilitators of small-bodied
cavity-nesters
Several other species are important cavity excava-
tors that facilitate breeding in mountain chickadees.
Downy woodpeckers, a member of the small-
bodied cavity-nesting guild, are exclusively
excavators (Jackson and Ouellet 2002). Downy
woodpeckers were always at low density with
abundance varying from being basically absent at
the beginning of our study and increasing to about
0.04 detections/ha in the last 2 years (Figure 8.1a).
We found only three nests in the first 4 years, but in
the latter years we monitored three to nine nests
annually (Figure 8.1b). Red-naped sapsuckers,
(Sphyrapicus ruber) a member of the medium-sized
cavity-nester guild, are important cavity producers
for mountain chickadees (Hill and Lein 1988;
Martin et al. 2004). Sapsucker numbers varied
dramatically over the study, and their numbers
may relate negatively to densities of European star-
lings (Sturnus vulgaris) that also varied annually
(Koenig 2003; Martin et al. 2003). If cavities last for
multiple seasons, an increase in sapsuckers or
downy woodpeckers may increase nest site avail-
ability for mountain chickadees for several subse-
quent years. Thus, we expect that the densities of
downy woodpeckers and sapsuckers in the previ-
ous year will influence population growth rates
and nesting densities of mountain chickadees.
8.1.3 Predators of small-bodied cavity-nesters
Cavity-nesting mammals such as red squirrel
(Tamiasciurus hudsonicus), northern flying squirrel
(Glaucomys sabrinus), and bushy-tailed woodrat
(Neotoma cinerea) are predators of Parid nests and
S M A L L - B O D I E D C AV I T Y- N E S T E R G U I L D S 115
are also consumers of small and medium-sized
cavities. Density and activity of red squirrels, in
particular, may strongly depress Parid demog-
raphy because they are abundant and can alter
resource availability (use suitable cavities) and
quality (enlarge small cavities), and prey on Parid
nests (Mahon and Martin 2006). Red squirrel detec-
tions varied strongly over the study from about
0.32 detections/ha early in the study, to half that
level from 1999 to 2001, followed by increases to
comparable detections of mountain chickadees and
nuthatches from 2002 to 2004 (Figure 8.1a).
However, red squirrels are generalist predators and
able to switch from bird eggs and adults to conifer
cones and fungi, thus an increase in squirrel
abundance does not always influence Parid
demography (Mahon and Martin 2006).
8.1.4 Interspecific interactions among
small-bodied cavity-nesters
Competition between mountain and black-capped
chickadees may occur because of genetic, behav-
ioral, and habitat similarities. Phylogenetic analysis
of North American chickadees using mitochondrial
DNA placed mountain chickadees closest to black-
capped chickadees in divergence distance indicat-
ing that among the Parids, these two species are the
most genetically similar (Gill et al. 1993, 2005; see
phylogeny in Chapter 2, Figure 2.1). Occasional
hybridization between the two species has been
reported in sympatric populations in Colorado and
New Mexico (Howe 1985; Martin and Martin 1996).
Both species have complex social organizations
within populations, with established dominants
and subordinates, usually males over females and
older over younger individuals (Minock 1972;
Desrochers 1989; Smith 1993; McCallum et al. 1999).
We suggest that similarities between these two
Parids contribute to a significant niche overlap
where ranges are sympatric.
Black-capped chickadees are the only Parid to
broadly overlap in range with the mountain
chickadee in western North America. In sympatric
populations in Alberta, there was segregation in
both nesting and foraging habitats, with mountain
chickadees foraging less often on branches and
more on trunks and twigs than black-capped
116 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
chickadees (Hill and Lein 1988). Mountain chicka-
dees occupied only one of 14 nest cavities
excavated by black-capped chickadees in Alberta
(Hill and Lein 1988) and we found segregation of
nest use in our study (Table 8.1). Segregation of
sympatric mountain and black-capped chickadees
may occur as a result of interspecific behavioral
dominance. In a behavioral study of sympatric
populations in Utah, black-capped chickadees were
frequently dominant over mountain chickadees
(Minock 1972). During playback experiments in our
study, black-capped chickadees exhibited higher
aggression towards simulations of mountain
chickadee intruders in defending nesting cavities
than mountain chickadees exhibited towards
simulated black-capped chickadee intruders (A.R.
Norris, unpublished data). Thus, while mountain
chickadees are the most abundant Parid, black-
capped chickadees are the more dominant species.
The mountain/black-capped chickadee relation-
ship is analogous to two European Parids: the blue
tit and the great tit. The blue tit is smaller than the
great tit, and therefore can utilize a wider range of
cavity sizes, however the great tit is generally dom-
inant to the blue tit and excludes it from nesting
habitat (Dhondt 1977). Where ranges overlapped,
great tits excluded blue tits from optimal territories
during the winter months by competitive dom-
inance but, during the breeding season, great tit
clutch size was negatively correlated with blue
tit density, indicating that blue tits could limit great
tit reproductive success if they could secure a terri-
tory. A possible explanation for why blue tits were
able to establish territories in the presence of great
tits was that a greater number of cavities were
available to blue tits due to their smaller body size;
these smaller cavities were not suitable for great tits
(Dhondt 1977; Dhondt and Eyckerman 1980).
Similarly, mountain chickadees, like blue tits, may
be subordinate to black-capped chickadees, and
excluded from black-capped chickadee habitat;
however, mountain chickadees appear better able
to capitalize on available resources because they
use a broad range of cavities excavated by other
species, whereas black-capped chickadees rarely
use cavities excavated by other species (Hill and
Lein 1988; Aitken et al. 2002; Table 8.1). In terms of
foraging habitat, competition with the broadleaf
habitat specialist black-capped chickadee may
drive mountain chickadees into habitats containing
a higher coniferous component. In addition to
providing rich food sources, including bark beetles
and budworm, coniferous habitats may contain
more nest sites for the mountain chickadee because
these habitats support a rich assemblage of
excavating species, including woodpeckers and
nuthatches. Although the red-breasted nuthatch
may be a significant competitor to the mountain
chickadee in these habitats, they are less ecologic-
ally similar than the black-capped chickadee (e.g.
nuthatches are typically bark gleaners whereas
chickadees are typically foliage gleaners) so
coexistence in mixed coniferous forest areas might
be easier. In terms of foraging habitat and nest-site
selection, we expect the most extensive overlap
between red-breasted nuthatch and mountain
chickadee populations; we examine here whether
this relationship is primarily one of facilitation
(through creation of cavities) or competition. When
food availability is high and nest-site competition is
low, we expect nuthatches to have a facilitating
effect on mountain chickadees, but when food is
limited we expect nuthatches to exclude mountain
chickadees. We expect downy woodpeckers and
red-naped sapsuckers to be primarily facilitators in
their relationship with mountain chickadees,
depending on the extent of simultaneous overlap of
resource use.
8.2 Study area and habitat change
Our study area, in the Cariboo-Chilcotin region of
central interior British Columbia, Canada (51 52N,
122 21W), is comprised of mixed coniferous
and deciduous forest embedded in a matrix of
grassland and shallow ponds within the warm and
dry Interior Douglas-fir Biogeoclimatic Zone
(Meidinger and Pojar 1991). Predominant tree
species are trembling aspen, Douglas fir
(Pseudotsuga menziesii), lodgepole pine (Pinus con-
torta), and white and hybrid spruce (Picea glauca x
engelmannii). Our sampling sites (7 to 32 ha in size)
varied in character from continuous forest to two
sites that were a series of forest islands (0.2 to
5 ha) within the grassland matrix. Most sites were
mature forest (80200 years old), nine of which
 S M A L L - B O D I E D C AV I T Y- N E S T E R G U I L D S 117

were cut selectively for pine and/or spruce in (Otvos 1979). Small cavity-nester species may
19972002. Additional study area details are given be able to capitalize on enhanced food supply
in Aitken et al. (2002) and Martin et al. (2003). differently.
Recently, the interior forests of British Columbia
have undergone significant changes in condition
8.3 Data analysis
due to outbreaks of mountain pine beetle
(Dendroctonus ponderosae). The Ministry of Forests The same sites were surveyed for cavity-nester
estimated over a 42-fold increase in area affected by detections and nests to obtain accurate estimates of
mountain pine beetle in BC from 1999 to 2004 breeding and nesting densities per site. We counted
(164 567 ha to 7 million ha; BC MoF 2004). Our every individual bird or squirrel detected during a
vegetation surveys also revealed significant point count period as an independent data point.
increases in bark beetle attack on conifers, espe- Data from all point count stations surveyed were
cially lodgepole pine (Figure 8.2). The main factors averaged across each site and year. We also counted
contributing to the outbreak are assumed to be individual nesting attempts as independent data
increased availability of mature pine and drought and calculated the mean number of nests per
conditions causing increased susceptibility of trees hectare surveyed. We compared mean nest
to attack, and a series of mild winters resulting in cavity measurements pre- (19952000) and post-
low over-winter larval mortality (Carroll et al. 2004; (20012004) beetle outbreak years using a series of
Taylor and Carroll 2004). Bark beetle larvae and independent samples t-tests. Homoscedasticity
other forest insects associated with bark beetles was tested using Levenes test for homogeneity
presumably provide substantial increases in food of variance and where tests failed to meet the
availability for insectivorous, small cavity-nesters assumptions, we assumed unequal variances. We

1.00

0.90 1995
1996
Proportion ofconifer trees surveyed

0.80 1997 0.80

Proportion of lodgepole pine
trees with boring insects

1998 0.70
0.70 0.60
1999
0.60 2000 0.50
2001 0.40
0.50 2002 0.30
2003 0.20
0.40 2004 0.10

0.30 0.00
1995 1996 1997 1998 1999 2000 2001 2002 2003 2004

0.20

0.10

0.00
1 2 3 4 5 6 7 8

Decay class

Figure 8.2 Changes in the health of conifers on our sites across time as measured by decay class, and the proportion of lodgepole pine
recorded as having at least one beetle attack during the study. We used a tree decay classification system that ranged from 18, with
1 indicating a live and healthy tree, 2 indicating a live tree with visible signs of decay, and 38 indicating dead trees with advancing stages
of decay as per icons (Thomas et al. 1979).
118 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
performed all analyses using SAS (SAS Institute
Inc. 1998) and SPSS for Windows standard version
11.5.0 (SPSS Inc. 2002). All statistical tests were
two-tailed and significance levels of 0.05
were used. Continuous variables were tested for
normality using a one-sample Kolmogorov
Smirnov test at the 95% confidence level, and
residuals of all response variables were plotted
and visually examined for all regression analyses
(Zar 1999).
8.3.1 Population growth models
We calculated mountain chickadee population
growth rates (r) by taking the natural log of the
average number of individuals per study site at
time (year), t1 divided by the average number of
detections per site at time t (adding a correction
factor of 0.5 to each population count because
census data typically contain zeroes, and the
addition of a small constant to every estimate of
population density is needed to avoid division
by zeroes in calculating growth rates-Framstad
et al. 1997). We used the natural log of the growth
rate estimates to account for any spatial variance
and spatio-temporal covariances in the density
estimates, which reduces the risk of overesti-
mating growth rates (spatial variance) and the
masking of positive spatio-temporal covariance
in population distributions (Steen and Haydon
2000).
[rt ln (Nt1 0.5 / Nt 0.5)]
Estimates of population growth with respect to
mountain chickadee abundance, allow us to exam-
ine the effects of the other explanatory variables on
density dependence. We used Akaikes Information
Criterion (AIC) as the basis for model selection
techniques (Burnham and Anderson 2002).
8.3.2 Excavation history, nest tree, and cavity
characteristics
In terms of the flow of nest-cavity resources among
the small cavity-nesters, mountain chickadees
depended primarily on cavities excavated by red-
naped sapsucker (40% of 163 cavities where cavity
origin was determined), red-breasted nuthatch
(23%), downy woodpecker (17%), and natural holes
(11%; Table 8.1). Despite the presence of both
chickadee species nesting on 21 of the 26 sites
between 1995 and 2004, only two of 163 nesting
attempts by mountain chickadees were in holes
excavated by black-capped chickadees, a lower or
equivalent frequency to their use of much larger
holes excavated by hairy woodpecker (Picoides
villosus), three-toed woodpecker (Picoides dorsalis),
and northern flicker (Colaptes auratus). Thus despite
similar size, ecology, and coexistence on the same
sites, mountain and black-capped chickadees
exhibited strong segregation in nesting habitats in
these mixed forests. Mountain chickadees may be
unwilling to use cavities used by black-capped
chickadees because black-capped chickadees
excavate cavities in very decayed trees that are not
useable (tree down, cavity collapsed, or entrance
grown in) in a subsequent year, especially if they
have access to small holes in more sturdy trees. In
2004, 84.7% of 137 red-naped sapsucker cavities
and 64.1% of 103 nuthatch cavities were useable
compared to 56.7% of 30 black-capped chickadee
cavities (K. Martin, unpublished data). Thus
the non-use of black-capped chickadee cavities by
mountain chickadees may be due to a combination
of low density and lower reusability of black-
capped chickadee cavities compared to the abun-
dant sapsucker and nuthatch cavities.
Both black-capped chickadees and red-breasted
nuthatches excavated the majority of their cavities
(both 77%) and each used 4 to 5% of sapsucker-
excavated cavities (Table 8.1). Fifteen percent of
black-capped chickadee nests, but only 5% of
nuthatch cavities, were in natural holes (Table 8.1).
The small-bodied cavity-nesting guild followed
the same pattern as the overall cavity-nester
community in terms of selecting unhealthy aspen
for nesting trees (Martin et al. 2004). About 96% of
nest trees chosen by small cavity-nesters were aspen
(Table 8.2). With strong increases in mountain
chickadees and nuthatches, we expected to find
changes in nest tree and cavity characteristics later
in the study. In the last 4 years of the study, moun-
tain chickadees used nesting trees with significantly
larger diameter at breast height (DBH), and cavities
over 1 m higher in the tree, with shallower horizon-
tal depth and smaller entrance areas than in the first
Table 8.2 Species and decay class of nest trees used by small-bodied cavity-nesters in interior British Columbia, (a) before beetle (19952000) and (b) after beetle (20012004)

Cavity-nesting species Trembling aspen Douglas-fir Lodgepole pine Hybrid spruce All tree species

DBHa DECAYb nc DBH DECAY n DBH DECAY n DBH DECAY n DBH DECAY n
meanSD median meanSD median meanSD median meanSD median meanSD median
(range) (range) (range) (range) (range)

(a)
Mountain chickadee 23.5 5.8 3 (16) 100 44.8 4.5 (45) 2 19.9 1 1 23.7 6.1 103
Black-capped chickadee 21.3 8.5 3 (17) 24 21.3 8.5 24
Red-breasted nuthatchd 22.9 6.5 3 (110) 76 89.2 40.9 4 (35) 3 19.3 2.7 2 27.2 2.5 2 25.4 15.4 83
Downy woodpecker 23.8 4.4 3 (25) 17 23.8 4.4 17
(b)
Mountain chickadee 26.1 8.0 3 (110) 231 51.3 17.6 4 (34) 4 26.5 8.8 3 (110) 235
Black-capped chickadee 18.7 6.8 3 (25) 29 18.7 6.8 3 (25) 29

S M A L L - B O D I E D C AV I T Y- N E S T E R G U I L D S
Red-breasted nuthatchd 24.8 19.9 3 (15) 157 55.3 9.6 4 (35) 4 30.0 9.9 3 (34) 7 35.3 9.0 4 (34) 3 26.3 20.0 173
Downy woodpecker 25.8 6.1 3 (24) 25 25.8 6.1 3 (24) 25

Updated and reorganized from Martin et al. 2004.

a
DBH: Diameter at breast height (cm).
b
Decay classa total of two nests were in fallen aspen trees (decay class 10)
c
n: Number of occupied nests.
d
Two red-breasted nuthatch nests were in Cottonwood trees.

119
120 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

6 years of the study (Tables 8.2 and 8.3). Cavity 8.3.3 Site level changes in mountain
height on the tree also increased by about 1 m after chickadee populations using population
the beetle outbreak for both red-breasted nuthatch growth models
and downy woodpecker (P 0.05, Table 8.3). In con-
8.3.3.1 Population size
trast to all other small-bodied cavity-nesters, black-
Over our decade-long study, we observed strong
capped chickadees used cavities significantly lower
increases in mountain chickadee numbers, with
on the trees (Table 8.3). Thus, mountain chickadees
similar increases in their small-bodied competitors
showed the largest change in nest-site characteris-
and red squirrels (potential predators) and also a
tics, correlated with increases in population density
strong reduction in conifer health, especially lodge-
and bark beetle prevalence. The significance of the
pole pine (Figure 8.2). Population growth models
large increase in cavity height is not immediately
were used to determine the critical drivers in chicka-
apparent. None of the changes in nest-cavity use
dee demography; because the relative abundance
were related to tree growth because most nest trees
of chickadees, competing, and facilitating species,
used by mountain chickadees were mature and
and red squirrels occur at similar spatial scales,
dead or dying with no significant tree growth dur-
changes in relative abundance for all species can be
ing the study (K. Martin, unpublished data).
detected from standardized point counts. Growth
Mountain chickadees did not abandon lower nest
rate was used instead of population size so that
sites, but rather there was an increase in the range of
we could examine effects of other explanatory
nest site heights and other characteristics compared
variables on density dependence. Using model
to earlier in the study.

Table 8.3 Cavity nest-site characteristics for small-bodied cavity nesting birds in interior British Columbia, (a) before beetle (19952000) and
(b) after beetle (20012004)

Cavity-nesting species Height above Vertical Horizontal Entrance Number of

ground (m) depth (cm) depth (cm) area (cm2) cavities in tree

mean SE n mean SE n mean SE n mean SE n mean SE n

(a)
Mountain chickadee 4.4 0.2 103 14.2 1.2 57 9.9 0.5 57 13.5 0.9 57 2.3 0.2 101
Black-capped chickadee 4.6 0.6 24 15.6 1.7 7 6.6 0.8 9 14.6 2.1 9 1.3 0.2 24
Red-breasted nuthatch 4.9 0.3 83 10.8 0.8 22 7.4 0.5 30 9.3 0.8 30 1.9 0.2 82
Downy woodpecker 5.2 0.5 17 17.1 1.9 7 9.1 0.5 7 9.4 1.0 7 2.5 0.5 17
(b)
Mountain chickadee 5.5 0.2 235 12.7 0.4 112 8.7 0.3 118 11.3 0.6 124 2.2 0.1 235
Black-capped chickadee 3.2 0.4 29 14.1 0.9 20 7.1 0.4 20 12.0 1.0 20 1.2 0.1 29
Red-breasted nuthatch 5.8 0.3 174 11.6 0.4 70 7.5 0.3 76 9.9 0.7 78 1.8 0.1 173
Downy woodpecker 7.0 0.6 25 14.9 1.6 7 10.1 1.8 8 9.1 0.9 8 2.7 0.4 25

Updated and reorganized from Martin et al. 2004.

We established vegetation plots and measured trees and cavities in 11.2 m radius plots centered at nest-tree and point count stations 100 m apart
along transect lines throughout each site. Since most sites covered an area that included one or several small cavity-nester territories, habitat
characteristics averaged over all plots on a site represent availability of nesting resources (sampling effort ~1 plot/ha). After nest cavities were
vacated, we recorded for all trees 12.5 cm DBH (British Columbia Ministry of Forests inventory standard) tree species, size (DBH), decay class, and
the number of cavities (used or unused) present. Tree condition was assessed using British Columbia Ministry of Forests guidelines (Finck et al. 1989)
and included the presence of fungal conks, bark beetle sign, and broken top. Vertical cavity depth was measured from the bottom of the cavity
entrance to the bottom of the cavity. Internal cavity diameter was measured from the inner edge of the lower lip of the entrance to the back wall
of the cavity. Entrance hole area (cm2) was calculated using hole height and width and the formula for the area of an ellipse. Cavity volume (cm3)
was calculated using vertical and horizontal depth and the formula for the volume of a cylinder.
 S M A L L - B O D I E D C AV I T Y- N E S T E R G U I L D S 121

Table 8.4 General linear models predicting mountain chickadee population growth rate in central British Columbia from 1995 to 2004

Model e2 K n AICC AICC AIC wt

M Bi Bc Rb D Rn Sq St E M*Sq 109.2 12 182 192.6 0.0 0.52

M Bi Bc Rb D Rn Sq St E M*Bi 108.9 12 182 192.0 0.6 0.39
M Bi Bc Rb D Rn Sq St E M*Bc 105.8 12 182 185.7 6.9 0.02
M Bi Bc Rb D Rn Sq St E 104.6 11 182 185.6 7.0 0.02
M Bi Bc Rb D Rn Sq St E M*Rb 105.7 12 182 185.6 7.0 0.02
M Bi Bc Rb D Rn Sq St E M*Bi M*Bc
M*Rb M*D M*Rn M*Sq M*St M*E 114.0 19 182 185.3 7.3 0.01
M Bi Bc Rb D Rn Sq St E M*Rn 105.4 12 182 184.9 7.7 0.01
M Bi Bc Rb D Rn Sq St E M*St 105.0 12 182 184.1 8.5 0.01
M Bi Bc Rb D Rn Sq St E M*D 104.8 12 182 183.8 8.8 0.01
M Bi Bc Rb D Rn Sq St E M*E 104.7 12 182 183.6 9.0 0.01

Variables examined were mountain chickadee (M), mountain pine beetle (Bi), black-capped chickadee (Bc), red-breasted nuthatch (Rb),
downy woodpecker (D), red-naped sapsucker (Rn), red squirrel (Sq) abundance, stem density (St), and percentage edge (E). For each model,
the log-likelihood ratio (e2), the number of parameters (K), the number of observations (n), the second-order Akaikes Information Criterion
(AICC), the relative quasi-likelihood Akaike Information Criterion (AICC), and its weight (AIC wt) are given.

selection techniques, the top two models had about
the same level of support, and all models predicting
site-level mountain chickadee population growth
rate included nine variables (detections of
mountain chickadees, black-capped chickadees,
red-breasted nuthatches, downy woodpeckers,
red-naped sapsuckers, red squirrels, amount of
beetle attack, stem density, and edge) and two
included interaction terms, the strongest being an
interaction term of mountain chickadees with
squirrel abundance (Table 8.4; Figure 8.3).
Averaging across all models in Table 8.4, parameter
estimates indicated the most important factors
predicting mountain chickadee growth rates were
mountain chickadee, red squirrel, and mountain
pine beetle abundance and stem density in the
previous year (Table 8.5). The negative density
dependent effects on mountain chickadee
population growth were ameliorated with high
beetle abundance (Figure 8.3a). There was also a
negative density dependent response to squirrel
abundance, but the strength of these effects varied
with chickadee abundance. When abundance of
mountain chickadees was low (below 0.15 individ-
uals/ha), the model predicted higher chickadee
growth rates with high squirrel abundance,
whereas at higher mountain chickadee densities,
high squirrel abundance more strongly limited
population growth rate, as predicted (Figure 8.3b).
Thus, mountain chickadee population growth rates
were enhanced by an abundance of forest insects
and reduced by high squirrel abundancea high
abundance of squirrels, however, does not
necessarily mean high depredation of chickadees,
as squirrels are generalist foragers and can switch
to plant foods when these are abundant (Mahon
and Martin 2006).
8.3.3.2 Nest density
Overall nesting densities of mountain chickadees
were positively correlated with: relative abundance
of mountain chickadees (point count detections
for that site and year); proportion of bark-
beetle-attacked lodgepole pine; red-breasted
nuthatch nest density (both same year and 1-year
lag); and relative abundance of downy woodpeck-
ers (1-year lag). Detections of red-naped sapsuckers
(1-year lag), red-breasted nuthatches, and stem
density were negatively correlated with mountain
chickadee nesting density (Figure 8.4, Table 8.6).
The positive effect of red-breasted nuthatch nest
density and the negative effect of nuthatch detec-
tions is puzzling since nuthatch nest density and
abundance were positively correlated. We suspect
that both nuthatch nest density and abundance
significantly interacted with food abundance, but
122 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

further analyses are needed to determine the was greater when beetle-attacked pine was higher
strength of these interactions. Nonetheless, the (Figure 8.5a) and the negative effect of red-breasted
positive effect of red-breasted nuthatch nest density nuthatch abundance (see Figure 8.4f) was alleviated

(a) 0.4
Low Beetle
High Beetle
Predicted mountain chickadee
population growth rate 0.2

0.2

0.4

0.6
0 0.2 0.4 0.6
Mountain chickadee population density (Nt)

(b) 0.4
Low Squirrel
High Squirrel
Predicted mountain chickadee

0.2
population growth rate

0.2

0.4

0.6
0 0.2 0.4 0.6
Mountain chickadee population density (Nt)

Figure 8.3 Population growth rate of mountain chickadees at time, t1, with mountain chickadee abundance at time t, predicted from the
model, y 0.30 (1.12)*M (0.21)*Bi (0.14)*Bc (0.12)*Rb (0.06)*Rn (0.26)*Sq (0.0003)*St(0.11)*E(2.44)*M*Bi
(2.98)*M*Bc (0.84)*M*Rb (0.35)*M*D (0.73)*M*Rn (1.58)*M*Sq (0.0004)*M*St (0.19)*M*E. Significant
interactions were between mountain chickadee abundance and (a) beetle abundance, represented from the 25% quartile (low beetle) and 75%
quartile (high beetle); (b) squirrel abundance, represented from the 25% quartile (low squirrel) and 75% quartile (high squirrel). Variables
included in the candidate models as main effects were average number of mountain chickadee (M), black-capped chickadee (Bc), red-breasted
nuthatch (Rb), downy woodpecker (D), red-naped sapsucker (Rn), and red squirrel detections (Sq), at time (t), proportion of lodgepole pine trees
with mountain pine beetle attack (Bi), stem density (St, the average number of trees/ha), and percent edge (E, the percent of vegetation plots
within 50 m of an edge). Models chosen for analysis included all main effects and all two-way interactions of mountain chickadee abundance
with the remaining eight predictor variables. We chose only interaction terms containing mountain chickadee abundance for analyses because we
were interested in the effects of other variables on density dependence. We excluded population growth estimates from the year immediately
after a site was harvested (stem density) to reduce possible influence of disturbance from cutting activities during late winter and early spring
when mountain chickadees establish territories.
 S M A L L - B O D I E D C AV I T Y- N E S T E R G U I L D S 123

Table 8.5 Model average parameter estimates for the explanatory variables of mountain chickadee population
growth rate

Parameter Parameter estimate Standard error Upper 95% Lower 95% t-value

St 0.0003 0.0001 0.0002 0.0005 4.5

Intercept 0.28 0.09 0.45 0.10 3.1
M*Bi 2.36 0.84 4.00 0.72 2.8
M 1.08 0.40 0.29 1.87 2.7
M*Sq 1.47 0.57 0.36 2.58 2.6
E 0.10 0.05 0.01 0.19 2.2
Sq 0.24 0.16 0.54 0.07 1.5
M*Bc 3.84 2.86 1.76 9.45 1.3
Rb 0.15 0.12 0.40 0.09 1.2
M*E 0.39 0.35 0.30 1.08 1.1
M*St 0.00 0.00 0.00 0.00 1.1
M*Rb 1.07 1.01 0.91 3.05 1.1
M*Rn 1.00 0.97 0.90 2.90 1.0
D 0.20 0.22 0.63 0.22 0.9
M*C 0.36 0.42 0.47 1.18 0.8
Bi 0.21 0.25 0.70 0.28 0.8
C 0.02 0.03 0.07 0.04 0.6
Bc 0.16 0.27 0.68 0.36 0.6
Rn 0.03 0.12 0.20 0.27 0.3
M*D 0.44 1.61 3.59 2.71 0.3

Mountain chickadee (M), mountain pine beetle (Bi), black-capped chickadee (Bc), red-breasted nuthatch (Rb),
downy woodpecker (D), red-naped sapsucker (Rn), red squirrel (Sq), abundance and stem density (St), and
percentage edge (E) and all two-way interaction terms. Parameters have a significant effect (P 0.05) on
mountain chickadee growth rates where t-values than absolute value of 1.98 (indicated in bold).

under high beetle attack, and slightly reversed
under low beetle attack (Figure 8.5b).
Nest density was significantly greater in years of
high beetle and budworm abundance (mean
nests/ha 0.11 0.01 SE, n 170 nests) than in
years of low beetle and budworm abundance
(mean 0.03 0.01 SE, n 73; t 4.3; p 0.01).
In years of high forest insects, mountain chickadee
fecundity (mean 5.5 1.5 SE eggs or chicks,
n 117 clutches) showed a non-significant
tendency to increase compared to low insect years
(mean 4.9 1.6 SE, n 16; t 1.53, p 0.13).
Red-breasted nuthatch fecundity (mean 5.7 1.4
SE eggs or chicks, n 79 nests) increased
significantly compared to low insect years
(mean 4.3 1.4 SE eggs or chicks, n 18; t 3.7,
p 0.01). Excavators may be more constrained
than non-excavators in increasing their clutch size
because of a trade-off in resource allocation
between excavation and egg formation
(Monkkonen and Orell 1997; Wiebe et al. 2006). In
our system, this pattern appeared to hold for
Parids as mountain chickadees, dependent on
other excavators, had larger clutches than the
excavating black-capped chickadees. This pattern
did not, however, hold for other small-bodied
cavity nesters, as we observed larger increases
in clutch size in the excavating nuthatches than in
mountain chickadees. A study on crested tits
in Belgium found that excavating males fledged
nestlings earlier than non-excavating males and
the probability of excavating increased with
male condition and nest initiation date (Lens et al.
1994). Black-capped chickadees may not have
responded to the recent resource pulse because
their tendency to excavate energetically precludes
124 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

(a)
0.6

Mountain chickadee nest density/ha

0.5

0.4

0.3

0.2

0.1

0
0 0.1 0.2 0.3 0.4 0.5 0.6
Mountain chickadee individuals/ha

(b)
0.6
Mountain chickadee nest density/ha

0.5

0.4

0.3

0.2

0.1

0
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7
Lodgepole pine with mountain pine beetle (stems/ha)

(c)
0.6
Mountain chickadee nest density/ha

0.5

0.4

0.3

0.2

0.1

0
0 0.1 0.2 0.3 0.4 0.5
Red-naped sapsucker detections from previous year (individuals/ha)

Figure 8.4 Continues

 S M A L L - B O D I E D C AV I T Y- N E S T E R G U I L D S 125

(d)
0.6

Mountain chickadee nest density/ha

0.5

0.4

0.3

0.2

0.1

0
0 0.1 0.2 0.3 0.4 0.5 0.6
Red-breasted nuthatch nest density (previous year)

(e)
0.6
Mountain chickadee nest density/ha

0.5

0.4

0.3

0.2

0.1

0
0 0.1 0.2 0.3 0.4 0.5 0.6
Red-breasted nuthatch nest density (same year)

(f)
0.6
Mountain chickadee nest density/ha

0.5

0.4

0.3

0.2

0.1

0
0 0.1 0.2 0.3 0.4 0.5 0.6
Red-breasted nuthatch individuals/ha

Figure 8.4 Continues

126 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

(g)
0.6

Mountain chickadee nest density/ha

0.5

0.4

0.3

0.2

0.1

0
0.00 0.10 0.20 0.30 0.40 0.50 0.60 0.70 0.80 0.90
Stem density (number of trees/ha)

(h)
0.6
Mountain chickadee nest density/ha

0.5

0.4

0.3

0.2

0.1

0
0 0.05 0.1 0.15 0.2 0.25 0.3 0.35
Downy woodpecker density from previous year (individuals / ha)

Figure 8.4 Parameters at the site level with the strongest influences on mountain chickadee nesting densities: (a) relative abundance of
mountain chickadee detections in point counts, (b) density of beetle-infected pine on the stands, (c) relative abundance of red-naped sapsuckers
from the previous year, (d) red-breasted nuthatch nesting densities in the previous year, (e) red-breasted nuthatch nesting densities in the same
year, (f) relative abundance of red-breasted nuthatches (same year), (g) stem density, and (h) relative abundance of downy woodpeckers in the
previous year. Four candidate general linear models were used to examine factors influencing mountain chickadee nest density: (1) Competitor
and predator model which included black-capped chickadee, red-breasted nuthatch and downy woodpecker abundance and nest densities and
red squirrel abundance at time, t; (2) Facilitator model which included red-breasted nuthatch, downy woodpecker, and red-naped sapsucker
abundance and nest densities from the previous year; (3) Habitat model that included mountain pine beetle abundance, stem density, and
proportion of edge habitat, and; (4) The main effects model which included all of the above explanatory variables. Since the strongest model
predicting mountain chickadee nest density was the main effects model (AIC wt 0.999; K 18; n 168), parameter estimation was
calculated from the main effects model and model averaging was not necessary.

them from increasing their clutch size. Presumably, the cost of excavation for any cavity-nesting species
the benefits of excavation are still higher for (Wiebe et al. 2006).
them than those accrued from larger clutches. Changes in forest habitat condition affect the
However, there are essentially no empirical data on reproductive behavior of many forest songbirds
 S M A L L - B O D I E D C AV I T Y- N E S T E R G U I L D S 127

Table 8.6 Parameter estimates from the full mixed-effects model predicting mountain chickadee nest density per ha among
26 forest sites from 1995 to 2003

Parameter Parameter estimate Standard error Upper 95% Lower 95% t-value

M 0.27 0.06 0.38 0.15 4.43

Bi 0.16 0.06 0.27 0.04 2.63
Rn Lag 0.16 0.06 0.03 0.28 2.50
Rb Nest Lag 0.26 0.10 0.46 0.05 2.48
Rb Nest 0.22 0.09 0.40 0.04 2.35
Rb 0.15 0.07 0.01 0.29 2.17
St 0.08 0.04 0.01 0.16 2.14
D Lag 0.28 0.14 0.56 0.00 1.98
Rb Lag 0.12 0.07 0.02 0.27 1.68
Sq 0.07 0.04 0.15 0.01 1.61
Rn Nest Lag 0.10 0.10 0.29 0.09 1.05
E 0.03 0.03 0.08 0.03 0.95
D Nest 0.24 0.26 0.74 0.26 0.95
Intercept 0.03 0.04 0.10 0.05 0.66
D 0.05 0.12 0.28 0.18 0.41
Bc Nest 0.08 0.22 0.35 0.51 0.37
Bc 0.03 0.14 0.31 0.24 0.25
D Nest Lag 0.04 0.30 0.54 0.62 0.13

Fixed explanatory variables include: detection of mountain chickadee (M), red-breasted nuthatch (Rb), black-capped chickadee
(Bc), downy woodpecker (D), red squirrel (Sq), and mountain pine beetle (Bi) abundance and percent of edge (E) and stem
density (St) for each site. Time lags of 1 year were examined for red-naped sapsucker (Rn), downy woodpecker (D), and red-
breasted nuthatch (Rb) relative abundance (Species Lag: detections of individuals from the previous year) and nests (Nest Lag:
nesting densities from the previous year). Site was included as a random variable. Parameters have a significant effect (P 0.05)
on mountain chickadee growth rates where t-values than absolute value of 1.98 (indicated in bold).

when the changes affect resource availability (Fort
and Otter 2004). In our study, the number of nest
trees and cavity density did not vary with habitat
change, but rather extrinsic factors related to
food supply, predation pressure and inter- and
intraspecific competition among three species
occupying similar niches. During the breeding
season, successful reproduction is determined by
food abundance and nest-site availability. Some
small-bodied cavity-nesting birds may be able to
assess food availability prior to insect emergence
(Crawford et al. 1990). Mountain chickadees showed
the strongest ability to adapt to local differences in
habitat conditions, and nuthatches also showed
strong positive responses. Since black-capped
chickadees are behaviorally dominant to mountain
chickadees and able to excavate cavities, it is
puzzling that they did not capitalize on the resource
pulse arising from the enhanced habitat conditions
for insectivores.
Although we examined changes in local habitat
characteristics and conditions to explain our
observed changes in demography and population
growth of mountain chickadees, these are simple
correlations that may not be causally linked. In
2005, S. Coe (Univ. of California, personal commu-
nication) observed dramatic changes in annual
fecundity of mountain chickadees in Sierra Nevada
similar to those observed in our study (A. R. Norris
and K. Martin, unpublished data). Thus it is
possible that some of the temporal changes we
observed in chickadee demography are driven by
larger scale-environmental or ecological influences
(see Chapter 5).
128 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

(a)
0.6
low bi (<15%)
high bi (>15%)

Mountain chickadee nest density/ha

0.5 Linear (low bi (<15%))
Linear (high bi (>15%))

0.4

0.3

0.2

0.1

0
0 0.1 0.2 0.3 0.4 0.5 0.6
Red-breasted nuthatch nest density
(b)
0.6
Mountain chickadee nest density/ha

0.5

0.4

0.3

0.2

0.1

0
0 0.1 0.2 0.3 0.4 0.5 0.6
Red-breasted nuthatch detections/ha

Figure 8.5 Correlations of mountain chickadee nest densities at low (15%) and high (15%) levels of boring insect abundance in pine trees
at the site level with (a) red-breasted nuthatch nest density, and (b) relative abundance of red-breasted nuthatch detections in point counts.
Straight lines were fit to raw data for each correlation at the two levels of boring insect abundance to demonstrate potential interacting effects
between boring insect abundance and nuthatches on mountain chickadee nest density.

Burnham, K. P. and Anderson, D. R. (1998). Model Selection

References
Aitken, K. E. H. and Martin, K. (2004). Nest site availabil-
ity and selection in aspen-conifer groves in a grassland
landscape. Canadian Journal of Forest Research, 34,
20992109.
Aitken, K. E. H., Wiebe, K. L., and Martin, K. (2002). Nest-
site reuse patterns for a cavity-nesting bird community
in interior British Columbia. Auk, 119, 391402.
and Inference: a Practical Information-Theoretic Approach.
Springer-Verlag, New York, USA.
Carroll, A. J., Taylor, S. W., and Regniere, J. (2004). Effects
of climate change on range expansion by the mountain
pine beetle in British Columbia. In: Shore, T. L., Brooks,
J. E., and Stone, J. E., eds. Mountain Pine Beetle
Symposium: Challenges and Solutions, Kelowna, BC, Oct.
3031, 2003, pp. 223232. Natural Resources Canada,

Canadian Forest Service, Pacific Forestry Centre,
Victoria, British Columbia, Information Report
BC-X-399.
Crawford, H. S., Jennings, D. T., and Stone, T. L. (1990).
Red-breasted nuthatches detect early increases in
spruce budworm populations. Northern Journal of
Applied Forestry, 7, 8183.
Dahlsten, D. L., Copper, W. A., Rowney, D. L., and
Kleintjes, P. K. (1992). Population dynamics of the
mountain chickadee in northern California. In:
McCullough, D. R. and Barrett, R. H., eds. Wildlife 2001:
Populations, pp. 502510. Elsevier, London.
Desrochers, A. (1989). Sex, dominance and microhabitat
use in wintering black-capped chickadees: a field
experiment. Ecology, 70, 636645.
Dhondt, A. A. (1977). Interspecific competition between
great and blue tit. Nature, 268, 521523.
Dhondt, A. A. and Eyckerman, R. (1980). Competition
between the great tit and the blue tit outside the breed-
ing season in field experiments. Ecology, 61, 12911296.
Finck, D. M., Humphreys, P., and Hawkins, G. V. (1989).
Field Guide to Pests of Managed Forests in British Columbia,
Joint Publication No. 16. Canadian Forest Service/British
Columbia Ministry of Forests, Victoria, BC, Canada.
Fort, K. and Otter, K. A. (2004). Effects of habitat disturb-
ance on reproduction in black-capped Chickadees
(Poecile atricapillus) in Northern British Columbia. Auk,
12, 10701080.
Framstad, E., Stenseth, N. C., Bjornstad, O. N., and Falck,
W. (1997). Limit cycles in Norwegian lemmings: tension
between phase-dependent and density dependence.
Proceedings of the Royal Society London Series B, 246,
3138.
Ghalambor, C. K. and Martin, T. E. (1999). Red-breasted
nuthatch (Sitta canadensis). In: Poole, A. and Gill, F., eds.
The Birds of North America, no. 459. Academy of Natural
Sciences, Philadelphia, and American Ornithologists
Union, Washington, D.C.
Gill, F. B., Mostrom, A., and Mack, A. L. (1993). Speciation
in North American chickadees: Patterns of mtDNA
genetic divergence. Evolution, 47, 195212.
Gill, F. B., Slikas, B., and Sheldon, F. H. (2005). Phylogeny
of titmice (Paridae): II. Species relationships based on
sequences of the mitochondrial cytochrome-B gene.
Auk, 122, 121143.
Hill, B. G. and Lein, M. R. (1988). Ecological relations of
sympatric black-capped and mountain chickadees in
southwestern Alberta. Condor, 90, 875884.
Hill, B. G. and Lein, M. R. (1989). Territory overlap and
habitat use of sympatric chickadees. Auk, 106, 259268.
Howe, W. H. (1985). Hybridization in Black-capped (Parus
atricapillus) and Mountain (P. gambeli) Chickadees in the
S M A L L - B O D I E D C AV I T Y- N E S T E R G U I L D S 129
Middle Rio Grande Valley of New Mexico. M.Sc. thesis,
Univ. of New Mexico, Albuquerque.
Jackson, J. A. and Ouellet, H. R. (2002). Downy wood-
pecker (Picoides pubescens). In: Poole, A. and Gill, F., eds.
The Birds of North America, no. 613. Academy of Natural
Sciences, Philadelphia, and American Ornithologists
Union, Washington, D. C.
Koenig, W. D. (2003). European starlings and their effect
on native cavity-nesting birds. Conservation Biology, 17,
11341140.
Lens, L., Wauters, L. A., and Dhondt, A. A. (1994). Nest-
building by crested tit (Parus cristatus) males: an ana-
lysis of costs and benefits. Behavioural Ecology and
Sociobiology, 35, 431436.
Mahon, C. L. and Martin, K. (2006). Nest survival of
chickadees in managed forests: habitat, predator, and
year effects. Journal of Wildlife Management. 70, in press.
Martin, K. and Eadie, J. 1999. Nest webs: a community-
wide approach to the management and conservation of
cavity-nesting forest birds. Forest Ecology and
Management, 115, 243257.
Martin, K., Aitken, K., and Wiebe, K. L. (2004). Nest sites
and nest webs for cavity-nesting communities in inter-
ior British Columbia, Canada: Nest characteristics and
niche partitioning. Condor, 106, 519.
Martin, K., Mossop, M. D., and Aitken, K. E. H. (2003). Nest
Webs: The Structure and Function of Cavity-Nesting and
Songbird Communities in Interior British Columbia Forests,
111 pp. Environment Canada/Canadian Wildlife Service
Technical Report No. 403, CW695/403E.
Martin, S. G. and Martin, K. A. (1996). Hybridization
between a mountain chickadee and black-capped
chickadee in Colorado. Colo. Field Ornithol. J., 30,
6065.
McCallum, D. A., Grundel, R., and Dahlsten, D. L. (1999).
Mountain Chickadee (Poecile gambeli). In: Poole, A. and
Gill, F., eds. The Birds of North America, no. 453.
Academy of Natural Sciences, Philadelphia, and
American Ornithologists Union, Washington, D.C.
Meidenger, D. and Pojar, J. (1991). Ecosystems of British
Columbia. British Columbia Ministry of Forests Special
Report Series, no. 6. Victoria, British Columbia.
Minock, M. E. (1972). Interspecific aggression between
black-capped and mountain chickadees at winter feed-
ing stations. Condor, 74, 454461.
Monkkonen, M. and Orell, M. (1997). Clutch size and cav-
ity excavation in Parids (Paridae): The limited breeding
opportunities hypothesis tested. American Naturalist,
149, 11641174.
Otvos, I. S. (1979). The effects of insectivorous bird activ-
ities in forest ecosystems: An evaluation. In: Dickson,
J. G., Connor, R. N., Fleet, R. R., Kroll, J. C., and Jackson,
130 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
J. A., eds. The Role of Insectivorous Birds in Forest
Ecosystems. Academic Press, New York.
SAS Statistical Institute (1998). SAS/STAT Users Guide,
version 8. SAS Institute, Cary, NC.
Smith, S. M. (1993). Black-capped chickadee (Parus atri-
capillus). In: Poole, A. and Gill, F., eds. The Birds of North
America, no. 39. Academy of Natural Sciences,
Philadelphia, and American Ornithologists Union,
Washington, D. C.
SPSS Inc. (2002). SPSS, version 11.5.0. SPSS Inc., Chicago.
Steen, H. and Haydon, D. (2000). Can population growth
rates vary with the spatial scale at which they are meas-
ured? Journal of Animal Ecology, 69, 659671.
Taylor, S. W. and Carroll, A. L. (2004). Disturbance, forest
age, and mountain pine beetle outbreak dynamics in
BC: A historical perspective. In: Shore, T. L., Brooks, J.
E., and Stone, J. E., eds. Mountain Pine Beetle Symposium:
Challenges and Solutions, October 3031, 2003, Kelowna,
BC, pp. 4151. Natural Resources Canada, Canadian
Forest Service, Pacific Forestry Centre, Victoria, British
Columbia, Information Report BC-X-399.
Thomas, J. W., Anderson, R. G., Maser, C., and Bull, E. L.
(1979). Snags. In: Thomas, J. W., ed. Wildlife Habitats in
Managed ForestsThe Blue Mountains of Oregon and
Washington. U S Department of Agriculture, Forest
Service Agriculture Handbook, no. 553.
Wiebe, K. L., Koenig, W. D., and Martin, K. (2006).
Evolution of clutch size in cavity-excavating birds: the
nest site limitation hypothesis revisited. American
Naturalist, 167, 343353.
Zar, J. H. (1999). Biostatistical Analysis. 4th edn. Prentice-
Hall, Inc., Upper Saddle River, NJ.
 CHAPTER 9
Social dominance and fitness in
black-capped chickadees
Laurene Ratcliffe, Daniel J. Mennill, and
Kristin A. Schubert
9.1 Introduction
Dominance hierarchies mediate social interactions
in many group-living animals (Piper 1997;
Dugatkin and Earley 2004). Such hierarchies often
emerge rapidly as the result of dyadic interactions
between individuals over access to resources
(Drews 1993; Beacham 2003). An individuals rela-
tive social rank may be influenced by characteris-
tics such as personality (Dall et al. 2004), intrinsic
resource-holding potential and experience (Hansen
and Slagsvold 2004), as well as extrinsic, context-
dependent features of competition such as group
make-up (Wiley et al. 1999) and the value of
resources (Dale and Slagsvold 1995). Although
social rank, by definition, must always be a relative
trait (Drews 1993), dominance hierarchies predom-
inate in animal groups with stable membership;
thus rank relationships are typically long-lasting
(Wiley et al. 1999; Forkman and Haskell 2004). If
acquiring and maintaining high status is costly
(Hogstad 1987a; Hay et al. 2004), dominant birds
should derive sufficient benefits from improved
foraging, mating, or protection from predators to
offset these costs (Ellis 1995).
Studies of the family Paridae (tits, titmice, and
chickadees) have contributed important informa-
tion to our understanding of passerine life histories
(McCleery and Perrins 1988; Dhondt 1989; Blondel
et al. 1990; Smith 1991). Many Parids spend the non-
breeding portion of their annual cycle in flocks with
linear dominance hierarchies and depend on food
storage for winter survival (Ekman 1989; Lundborg
and Brodin 2003). Flock size, range, sex ratio,
coherence, and stability of hierarchies vary within
and between species (Hogstad 1989; Matthysen
1990; Smith 1991; Verbeek et al. 1999; Hay et al.
2004). Despite this variation there is abundant
evidence that social rank within flocks influences
individual success, as a result of differential access
to food (Glase 1973; Hogstad 1987b; Desrochers
1989; Ficken et al. 1990; Smith 1991) and breeding
partners (Smith 1988; Otter and Ratcliffe 1996;
Mennill et al. 2004), as well as rank-related variation
in predator avoidance (Zanette and Ratcliffe 1994;
Koivula et al. 1996).
Black-capped chickadees are undoubtedly the
best-studied of the North American Parids, yet data
on long-term reproductive output are scarce (Smith
1991). Only one study (Schubert et al. in press) has
evaluated the relationship between social rank and
lifetime fitness. Chickadees are an ideal species for
such a study (apart, perhaps, from the disinclin-
ation of black-capped chickadees to use nest boxes).
They are broadly distributed across a range of
temperate North American habitats. Like most
other Parids, including the willow tit (Lahti et al.
1996), black-capped chickadees winter in dom-
inance-structured flocks of three to 12 birds, in
which males dominate females and mature birds
dominate yearlings (Glase 1973). Flocks typically
consist of two or more adult birds and one or more
yearlings recruited from outside of the local popu-
lation. Birds often breed with a member of their
winter flock, and therefore chickadee flocks are
sometimes described as a hierarchy of pairs
131
132 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
(Smith 1991). Once recruited, chickadees are highly
philopatric, so the effects of winter social rank on
breeding success and status in succeeding winter-
ing flocks can be measured.
In this chapter we examine naturally- and sexu-
ally-selected consequences of social rank in a popu-
lation of black-capped chickadees studied for over a
decade in eastern Ontario, Canada. We begin by
reviewing what is known about the characteristics
that distinguish individuals attaining high social
rank from subordinates. We describe aspects of
status signaling, such as song and plumage features,
as well as rank-related differences in survival and
annual reproductive success. Using our extensive
observations of interactions among color-banded
individuals, we describe the process by which dom-
inance hierarchies are maintained. We then review
the effects of individual variation in rank acquisition
on lifetime reproductive success (LRS). To date most
studies of avian life histories, including the excellent
work on great tits (McCleery and Perrins 1988) and
blue tits (Dhondt 1989), have investigated pheno-
typic correlates of fitness, but few have examined
how the dynamics of social rank acquisition influ-
ence LRS. Analysis of LRS permits us to compare
how the overall genetic contribution of individuals
is affected by both lifespan and reproductive strat-
egies. Breeding lifespan has been identified as the
most important predictor of LRS in mammals and
birds (e.g. Clutton-Brock 1988; Newton 1989); never-
theless the interaction between social rank and LRS
may also be significant and warrants investigation
(Verhulst and Salomons 2004).
9.2 General methods
We have monitored black-capped chickadees at
Queens University Biological Station (QUBS),
Chaffeys Lock, Ontario, Canada (44 34N, 76
19W) since 1987. The life history data reported
here were collected from 1992 (initiation of breed-
ing studies) through 2002. Data on winter dom-
inance and flock memberships (but not flock
formation) were collected from 1994 though 2002.
During this period the 2-km2 study site supported
an average of 17.2 2.1 winter flocks and 60 8.2
breeding pairs per year. Mean flock size was
5.5 0.1 birds (N 155 flocks), smaller than
Smiths (1991) reported average of eight birds
in western Massachusetts. Flock sex ratios were
only slightly male-biased, averaging 1.2 0.1
males per female. Birds bred overwhelmingly
in natural cavities (80% of nests; Mennill and
Ratcliffe 2004a) rather than nestboxes. Field proto-
cols as described below were similar across
years (see Schubert et al. in press for full details of
methods and data analysis).
9.2.1 Winter field methods
From January to March, birds were captured in
baited Potter traps (average 146.8 12.5
birds/winter) and individually marked with
aluminum Canadian Wildlife Service bands and
one to three colored plastic bands. Standard
morphological measures (mass, tarsus, wing,
rectrix length, fat score) and 10 to 80 l of blood
were collected from each bird for sexing and pater-
nity analysis. Birds were aged as second year (SY)
or after-second year (ASY) using standard proto-
cols and banding records (Mennill et al. 2004). Flock
memberships were obtained by tracking flock
movements across the site and scoring arrival times
at feeders. Dominance relations among flock mem-
bers were already well-established by the start of
our observations each January.
We assessed dominance hierarchies within flocks
by tabulating over 20 000 pairwise interactions
(average of 2439 712 per year) between banded
birds at feeding platforms which accommodated
only one feeding individual at a time (Fig. 9.1). We
inferred that an individual was dominant over
an opponent when they: (i) supplanted or chased
an opponent, (ii) resisted a supplanting attack by an
opponent, (iii) elicited a submissive posture in an
opponent, or (iv) fed while an opponent waited to
approach the feeder (Ficken et al. 1990; Otter et al.
1998). These four types of interaction did not occur
in equal proportion; the last two types of interac-
tion occurred very frequently, supplants and chases
occurred less often, and resisting a supplanting
attack occurred very rarely. Hierarchies within
flocks were ordered using MatMan software
(Noldus Information Technologysee review by
deVries 1998). Dominant (high-ranking) males were
categorized as the male that held the top position in

(a)
(b)
(c)
Figure 9.1 Photographs of dyadic dominance interactions in a
wintering flock of black-capped chickadees. (a) A dominant
individual (left) flies in to supplant a subordinate individual.
(b) A dominant individual feeds while a subordinate
individual waits to approach the feeder. (c) A dominant
individual (left) elicits a submissive posture in his opponent
(turning his head away from the dominant). Photographs by
D. J. Mennill.
SOCIAL DOMINANCE AND FITNESS 133
flocks with two or three males, and the top two
positions in flocks with four or five males; subordin-
ate (low-ranking) males held the bottom position or
bottom two positions, respectively. In flocks with
three or five birds, the middle bird was classified as
mid-ranking. Most comparisons used these
nominal categories, so sample sizes were based on
numbers of flocks. In some cases, to allow compari-
sons across flocks, a continuous rank score for each
bird (number of interactions won divided by total
interactions) was also calculated (Mennill et al.
2004). Because dominance interactions occur at a
lower rate and intensity between females than
males, and their functional significance is still
incompletely understood (Ramsay and Ratcliffe
2003; L. Ratcliffe, unpublished data), we have lim-
ited most analyses presented here to male rankings.
9.2.2 Spring field methods
Pairs were monitored from flock break-up (typically
late March to early April) to determine territory
boundaries and locate nest cavities. Breeding data
were collected from a total of 536 pairings involving
294 males and 282 females. At approximately day 6
post-hatch, we collected 10 to 50 l blood from the
tarsal vein of nestlings for paternity analysis
(Mennill et al. 2004). Fledglings typically dispersed
outside the boundaries of our study area, precluding
accurate measures of recruitment. Thus we meas-
ured male realized reproductive success (RRS) as the
total number of within- and extrapair nestlings sam-
pled at day 6; female success equaled the number of
offspring in the nest, since egg dumping was
extremely rare (Otter et al. 1998; Mennill et al. 2004).
9.3 Correlates of social rank
Table 9.1 summarizes our current knowledge about
the morphological, behavioral, and reproductive
characteristics associated with social rank in back-
capped chickadees. Here we review some of these
features originally described by Smith (1991), and
describe new ones which have emerged from our
recent work. These findings provide good evidence
of important variation in features that signal male
quality and individuality. Undoubtedly future
work will reveal additional examples.
134 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

Table 9.1 Correlates of social rank in black-capped chickadees

Feature Pattern Reference

Age Adults dominate juveniles Smith 1991, Otter et al. 1999, Schubert 2003
No age effect in females Ramsay and Ratcliffe 2003
Sex Males dominate females Smith 1991
Seniority Residents dominate intruders:
Males Smith 1991
Females Otter and Ratcliffe 1996, Ramsay and Ratcliffe
2003, S Ramsay and L Ratcliffe, unpublished
Early dispersing fledglings dominate later dispersers Smith 1991
No effect of fledgling seniority Leonard et al. 1991
Body condition Dominant males and females leaner Schubert et al. 2006, S Ramsay and L Ratcliffe,
unpublished
Foraging Dominants access more profitable, safer feeding sites Desrochers 1989, Ficken et al. 1990
Predator responses Dominants show less risky behavior (calls and movement) Zanette and Ratcliffe 1994
Plumage Dominant males have darker melanin (cap, mantle, bib), brighter Mennill et al. 2003a, Doucet et al. 2005,
white, and faster tail feather growth Woodcock et al. 2005
Song structure Dominants better at transposing songs across species frequency Christie et al. 2004
range
Singing behavior Dawn chorus of dominants begins earlier in morning, lasts Otter et al. 1997
longer, higher song rate
Response to interactive Subordinates respond more agitatedly to playback, closer Mennill and Ratcliffe 2004b
intruder approach to speaker than dominants
Response to simulated Dominants more likely to approach simulated winner Mennill and Ratcliffe 2004c
vocal duels
Territory Dominants out-compete subordinates for access Desrochers et al. 1988
Dominants have larger territories Smith 1991, Mennill et al. 2004
Mate attraction Dominant widowers attract new female sooner Otter and Ratcliffe 1996, Smith 1991
Dominant males more attractive to nave females Bronson et al. 2003, Woodcock et al. 2005
Divorce Females desert mates for higher ranked males Ramsay et al. 2000
Extrapair paternity Extrapair males higher-ranked than social males Smith 1988, Otter et al. 1994, 1998; Mennill
et al. 2003b, 2004
Clutch size Mates of dominant males more likely to lay eggs, have larger Otter et al. 1999, Doucet et al. 2005
clutches and higher % hatch
Nest success Mates of dominant males incubate longer than mates of Otter et al. 1999
subordinates, feed nestlings less often, have higher nest
survival and fledging success

flock-mates (1.6 0.1 years) (P 0.0001) (Schubert

9.3.1 Age
Smith (1991) observed that male social rank correl-
ates with age class (ASY birds typically dominate SY
birds), whereas a females rank may better reflect that
of her mate than her own age. Like Smith (1991), we
have found that young (SY) males can, in some
circumstances, dominate older birds (ASY; see
below), but overall high-ranked males were signifi-
cantly older (3.4 0.1 years) than their subordinate
et al. 2006). Similarly, Otter et al. (1999) found that
among 27 pairs of chickadees where intrasexual
ranks and ages of both members were known, male
age and rank were strongly correlated, but female
rank was more strongly correlated with her mates
age and rank than her own age. In aviary-staged
dominance contests between females, age by itself
was also a poor predictor of winning (Ramsay and
Ratcliffe 2003).

9.3.2 Sex
Males are dominant over females (Smith 1991).
Although Smith (1991) reported that females may
sometimes be dominant over males, we found this
rarely occurred. Looking at a subset of our data,
including 22 flocks from 2000 and 2001 where there
was a clear hierarchy among both the males and
females, we found that in 21 of 22 flocks the lowest-
ranking male was dominant to the highest-ranking
female. Our data therefore match those of Glase
(1973) who found that males are quite consistently
dominant over females. Interestingly, most cases
where we observed females dominating males
occurred between birds who ended up as breeding
partners, where the male waited for his partner to
finish feeding before approaching the feeder (inter-
action type iv, above).
9.3.3 Seniority
Prior residency is an important correlate of social
dominance in tits during interactions at territory
boundaries and during flock formation. However
detailed studies of residency effects, especially in
females, are rare. In captive great tits, residents
dominate intruders, but adultspresumably more
experienceddominate juveniles when circum-
stances are unfamiliar to both (Sandall and Smith
1991). Smith (1991) found that chickadees removed
from winter flocks for up to 4 days generally
regained their former status. Our work shows that
at the onset of the breeding season, females
removed for up to 96 hours from their high-ranked
mates easily evicted replacement mates (Otter and
Ratcliffe 1996; S. Ramsay and L. Ratcliffe, unpub-
lished data). In aviary contests, female owners
out-ranked intruders (Ramsay and Ratcliffe
2003), as found in willow tits (Koivula et al. 1993).
Thus although rank differences are more challeng-
ing to measure among females than males, females
exhibit clear rank-related aggression outside the
context of the pair bond.
Work with captive tits shows early experience
may affect offspring dominance status (Hansen and
Slagsvold 2004). Smith (1991) reported very low
levels of aggression within chickadee families, with
no clear pattern of dominance hierarchies among
SOCIAL DOMINANCE AND FITNESS 135
fledglings. However she also suggested that earli-
est-dispersing juveniles were probably the most
successful at joining flocks by pairing with
widowed adults, with a correlated rise in status.
Glase (1973) showed that juveniles with greater
skull pneumatization (a reliable age indicator) in
early fall were more likely to dominate later-arriv-
ing birds. In marsh tits, larger and more aggressive
fledglings dispersed earlier than smaller fledglings
regardless of sex (Nilsson and Smith 1985, 1988). In
contrast, our studies of fledgling aggression and
dispersal in eight chickadee family groups over the
22-day fledgling period showed aggressors were no
larger than their victims, nor did they disperse
earlier (although sample sizes were smaller than
those in the marsh tit study; Leonard et al. 1991). We
have not documented flock formation in our popu-
lation, and thus the ontogeny of first-year rank
remains an important area for future research.
9.3.4 Size and condition
Because dominance is associated with preferential
access to food and decreased risk of predation, it
seems reasonable to predict that high-ranking birds
carry fewer reserves than subordinates in winter
when foraging conditions are challenging
(Cresswell 2003; see also Chapter 3). Modeling the
relation between dominance and mass (or condi-
tion) has turned out to be more complex than ori-
ginally thought because of the need to consider
variation in predation risk and environmental
conditions (Lundborg and Brodin 2003; Ekman
2004), including flock stability (Lange and Leimar
2004). Neither Glase (1973) nor Smith (1991) found
any compelling evidence that body size relates to
dominance effects in chickadees (but see Hogstad
1987b); condition was not measured. However,
in paired comparisons of the highest- and
lowest-ranking males in flocks, Schubert et al.
(2006) found dominant males had longer wings and
tarsi, lower fat scores, and were in leaner condition
than subordinates. Importantly, when age-matched
flock-mates were compared, the differences in wing
and tarsus disappeared but low-ranked birds were
still heavier and had greater fat scores. Thus high-
ranked males are leaner but not larger when age is
taken into account. Similarly, in 15 field trials where
136 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

females mated to dominant males were removed (a)

50
for 86 to 94 hours prior to onset of egg-laying, the WHITE
12 females that were able to oust their replacements 40
within a short time of being released and were, on

Reflectance
average, leaner than replacements ( S. Ramsay and 30
L. Ratcliffe, unpublished data, but note sample size
20 GREY
was insufficient to control for age effects). Overall,
our results agree with most other studies of Parids 10
showing dominance is not related to body size per BLACK
se (Hay et al. 2004; but see Braillet et al. 2002 for 0
300 400 500 600 700
population differences), whereas dominants tend to
Wavelength
carry lesser weight reserves than subordinates
(b) 0.6
(Pravosudov and Grubb 1997).

0.4
9.3.5 Plumage

Visual signaling in chickadees has attracted little
attention compared to the better-characterized
great and blue tits (Lemel and Wallin 1993; Lange
and Leimar 2003; Alonso-Alvarez et al. 2004). The
achromatic (black, white, grey) plumage of black-
capped chickadees looks monomorphic to the
human eye, as is described for many Parids. Smith
(1991) surmised from her observations of domin-
ance interactions that chickadees must be able to
recognize the sex and relative social rank of others
both quickly and accurately from considerable
distances. We confirmed her prescient suggestion
that there are substantial sex and rank differences
in chickadee plumage features across the visual
spectrum which are not detected by the human eye
(Fig. 9.2a). Reflectance spectrometry of six body
regions of chickadees captured in late winter flocks
has revealed that not only are males brighter white
than females, they also have larger black bibs and
greater plumage contrast between adjacent white
and black body regions. In addition, plumage
variation is related to differences in social rank.
High-ranked males have darker black caps, and
differences in the color of their black bibs and grey
mantles relative to their subordinates, independent
of age (Fig. 9.2b). Measurements of growth bars in
naturally-molted feather show dominant males
also grow their tail feathers significantly faster than
subordinates (Mennill et al. 2003a). This last finding
contrasts with that of Hay et al. (2004) who found
that dominant coal tits grew induced tail feathers
more slowly than subordinates. The different
Canonical variate
0.2
0
0.2
0.4
0.6
High-ranking Low-ranking
males males
Figure 9.2 (a) Average plumage reflectance spectra of the white
cheek patch, the gray mantle, and black cap in black-capped
chickadees (based on spectrophotometric measurements of 40 males)
(from Doucet et al. 2005). (b) Association between male rank and
achromatic plumage color. High-ranking males had high canonical
variate scores, indicating darker black caps, grey mantles with
proportionately greater reflectance at intermediate wavelengths, and
black bibs with proportionately less reflectance at intermediate
wavelengths (from Mennill et al. 2003a).
results may reflect effects of manipulating feather
regrowth in the latter study. A subsequent study on
our QUBS population has shown that the
UV-chroma of these melanin-based features
successfully predicts male realized reproductive
success (within and extrapair offspring) (Table 9.2;
Doucet et al. 2005). These data suggest that achro-
matic plumage provides reliable cues about sex and
quality. Female chickadees exposed to unfamiliar
males in aviary choice tests can identify dominant
individuals rapidly without observing them

Table 9.2 Significant plumage predictors of male reproductive success from multiple regression models constructed
using a backward stepwise procedure
Apparent reproductive success
No significant predictors
Proportion of within-pair young
Whole model
White brightness
Melanin UV chroma
Overall realized reproductive success
Melanin UV chroma
a
Standardized partial regression coefficients.
Each model was constructed using four color variables (brightness of white patches, UV chroma of white patches,
brightness of melanin-colored black patches, ultraviolet chroma of black patches), dominance rank, and body condition
as potential predictor variables. Dependent variables (measures of male reproductive success) are shown in italic. Full
details of analysis are presented in Doucet et al. 2005. Only plumage color variables were significant predictors of two
measures of reproductive success.
interact, consistent with this hypothesis (Woodcock
et al. 2005). Additional studies are needed to deter-
mine how individual and rank-based differences in
plumage mediate competitive interactions in flock
hierarchies. Achromatic plumage color may well
provide badges of quality in aggressive, intrasex-
ual encounters in chickadees, as does UV color in
blue tits (Alonso-Alvarez et al. 2004).
9.3.6 Vocalizations
The two-note fee-bee song of chickadees functions in
long-distance territorial communication, providing
both male and female audiences with a rich array of
cues correlated with the quality of the singer (see
Chapter 14). Males can frequency-match rivals by
transposing their single song type up and down a
continuous frequency range. Such pitch shifts
introduce fine structural changes in relative note
frequency, amplitude, and duration. While the
tendency to shift songs is not related to social rank,
dominant males are superior singers, that is they
maintain relative note stereotypy in shifted songs
significantly better than low-ranking males
(Christie et al. 2004). Dominants also begin the
dawn chorus earlier, sing for longer, and sing at
higher rates (Otter et al. 1997). In mock counter-
singing duels (playback from two loudspeakers at
SOCIAL DOMINANCE AND FITNESS 137
R2 a df P
0.65 2, 9 0.008
0.38 1.01 1, 10 0.002
0.27 0.65 1, 10 0.03
0.20 1, 38 0.01
the territory edge), dominant territory holders are
more likely to approach the simulated winner
(more threatening rival) than are subordinate terri-
tory holders (Mennill and Ratcliffe 2004c). When
territory holders are themselves challenged with
aggressive interactions via playback, dominants do
not engage with the intruder as intensely as
subordinates (Mennill and Ratcliffe 2004b).
Engaging in intense song contests may be particu-
larly costly for dominants, since they are unlikely to
be cuckolded unless they lose in countersinging
interactions with territorial intruders (Mennill et al.
2002). In a similar vein, dominants in winter flocks
are risk averse, that is when exposed to predator
models they take longer to call and break the freeze
than subordinates (Zanette and Ratcliffe 1994).
9.4 Hierarchy formation and
maintenance
Although the correlates of social rank have been
well established through ongoing research, the
process of hierarchy formation and the mechanics
of hierarchy maintenance have received little atten-
tion. Several hypotheses have been proposed to
explain how dominance hierarchies are formed and
maintained (reviewed in Forkman and Haskell
2004). The first fight hypothesis maintains that
138 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
dominance relationships arise from an initial
encounter between two individuals. The continu-
ous assessment hypothesis maintains that multiple,
ongoing interactions and challenges are responsible
for developing and maintaining dominance
hierarchies. As an extension of the continuous
assessment hypothesis, the suppression hypothesis
maintains that dominant individuals condition
their subordinates to lose through ongoing attacks.
Under the first fight hypothesis, the cost of an indi-
vidual fight is expected to be high, and aggression
is not necessarily expected to be greater between
pairs of animals who hold adjacent rank positions
versus pairs with non-adjacent rank positions.
Under the continuous assessment hypothesis, the
cost of an individual fight is expected to be low and
aggression between pairs of animals should occur
more frequently when they hold adjacent rank
positions (i.e. when they have similar fighting
abilities). Under the suppression hypothesis, the
cost of an individual fight is expected to be low, and
dominant animals should instigate aggressive
encounters with their subordinates whereas
the reverse should occur rarely (Forkman and
Haskell 2004).
To better understand chickadee dominance hier-
archy formation and maintenance, we tested the
predictions of these three hypotheses using a
dataset of 6234 dominance interactions between 278
birds from 48 flocks, collected in January to March
of 2000 and 2001 in our eastern Ontario study
population. Dominance interactions may be
divided into interflock and intraflock interactions,
and we focus on 3114 intraflock interactions to
investigate the three hypotheses for the formation
and maintenance of dominance hierarchies. Of
these interactions, we observed 129 interactions
that involved especially aggressive supplanting
attacks. These highly aggressive interactions are
particularly helpful for evaluating the predictions
for these three hypotheses.
Is the cost of intraflock chickadee aggression high
or low? Our observations suggest that the cost of
aggressive encounters between flock-mates during
the non-breeding season is low. For the 129 aggres-
sive supplants that we observed, none appeared to
lead to an injury in the dominant or subordinate
bird. The primary cost associated with these
aggressive interactions appeared to be a temporary
delay in access to food resources; in most observed
cases the supplanted individual returned to the
feeder shortly after the aggressive supplant. This
low cost of aggression stands in contrast to the
outcome of fights we have observed at other times
of the year. In mid and late April, when flock
hierarchies have dissolved and birds have begun
defending territories, we have observed many
aggressive encounters which have escalated to
extended physical contact, sometimes resulting in
lost feathers and, in a few cases, prolonged head
injuries (noticeable as persistent swollen skin
around the eyes). During the breeding season, we
have observed such high-cost aggressive encoun-
ters occur between two males and, less frequently,
between two females. From the onset of our studies
at QUBS (K. A. Otter, personal communication) we
have also observed a frequent form of aggression
during the early breeding season in the form of
triangle fights, which occur as a low-ranking
male persistently supplants and chases a high-
ranking female in the presence of her high-ranking
partner, who only occasionally steps in to harshly
supplant the low-ranking male. These triangle
fights rarely involve extreme aggression, but never-
theless appear to come at a high cost to the female,
who can spend up to an hour practicing evasive
maneuvers. Relative to these forms of aggression
during the breeding season, aggression between
flock-mates during the non-breeding period
appears to come at a low cost.
Does aggression between pairs of individuals
occur more frequently between individuals occu-
pying adjacent rank positions? To answer this
question, we focused on aggressive malemale
interactions that occurred in flocks with three, four,
or five males (in flocks with two males, all
malemale interactions necessarily occur between
birds with adjacent rank position). The highly
aggressive interactions we observed did not occur
between males with adjacent rank positions more
often than expected by chance. In flocks with three
males, 69% of highly aggressive interactions
occurred between males with adjacent rank pos-
itions (binomial test against expected proportion of
66%: P 0.68, N 13); in flocks with four males,
46% of highly aggressive interactions occurred

between males with adjacent rank positions (bino-
mial test against expected proportion of 50%:
P 0.42, N 26); and in flocks with five males,
60% of highly aggressive interactions occurred
between males with adjacent rank positions (bino-
mial test against expected proportion of 40%:
P 0.91, N 5). Therefore, our results do not
support the second prediction of the continuous
assessment hypothesis.
Do dominant birds instigate aggressive encoun-
ters? Of the 129 highly aggressive supplanting
attacks that we observed in 2000 and 2001, we
found that the overwhelming majority involved a
dominant individual attacking a subordinate indi-
vidual. For 58 aggressive supplants between males,
57 involved the dominant bird supplanting his
subordinate flock-mate; for 11 aggressive supplants
between females, 10 involved the dominant female
supplanting her subordinate flock-mate; for 60
aggressive supplants between a male and a female,
58 involved the dominant bird supplanting their
subordinate flock-mate. (Of the latter 58 supplants,
19 were cases where a male supplanted his own
breeding partner.)
Taken together, these data provide support for
the suppression hypothesis: the cost of an individ-
ual dominance fight appears to be low, and domin-
ant individuals instigate aggressive encounters
with their subordinates. In contrast to the predic-
tion of the continuous assessment hypothesis,
aggression does not occur between individuals
holding adjacent rank positions more often than
would be expected by chance. Further research is
required to evaluate the cost of fights during initial
encounters when birds first form flocks in the fall,
so that we may better understand the importance of
first fights in establishing position in chickadee
dominance hierarchies.
9.4.1 Consistency in dominance
relationships between sites
Some bird species exhibit dominance relationships
which are site-specific or context-specific, including
Carolina chickadees (Smith 1991) and mountain
chickadees (Dixon 1965; interactions between non-
flock-mates were site-specific). Many European
Parids show site-specific dominance relationships;
SOCIAL DOMINANCE AND FITNESS 139
in both great tits and blue tits, dominance relation-
ships depend on the proximity to the previous
years breeding territories (Colquhoun 1942; De
Laet 1984). In contrast, winter dominance relation-
ships within black-capped chickadee flocks are not
site-specific. This has been reported qualitatively
by Hartzler (1970) for a Minnesota population,
Smith (1976) for a Massachusetts population, and
Desrochers and Hannon (1989) for an Alberta
population. Using dominance data from our east-
ern Ontario population, we attempted to quantify
the consistency of chickadee dominance inter-
actions across sites. Of 2257 dyadic, malemale
dominance interactions we observed in 2000 and
2001, we found 27 dyads where the same two males
interacted at two different feeder sites. The
minimum distance between neighboring feeder
sites at our Ontario study site is 175 m, and in all 27
cases, the two winter feeders were in positions that
fell within two different birds breeding territories
in both the preceding and subsequent breeding
seasons. Of the 27 dyads, there were 22 where the
dominance relationship was consistent across the
two sites (binomial test: P 0.0005). Our results
therefore agree with previous qualitative assess-
ments in other populationsblack-capped chicka-
dee dominance relationships are not site-specific.
9.5 Variation in rank acquisition
Analysis of rank histories of known males from our
long-term data set provides a revealing picture of
the factors associated with change in status
(Schubert et al. 2006; K. A. Schubert, C. Kraus, D. J.
Mennill et al. unpublished data). As in willow tits
(Lahti et al. 1996), rank is a dynamic trait. The
majority of mid- and low-status birds increased in
rank over consecutive years; birds reaching high
rank seldom regressed (Table 9.3; Schubert et al. in
press). Most birds advancing from low to high rank
immediately dominated yearlings (22/29 cases),
and some younger or older adult flock-mates
(7 cases) (Schubert et al. 2006). Not surprisingly,
males reaching high rank lived longer, on average
(3.4 0.1 years, N 98) than males who never
moved beyond subordinate status (1.6 0.1 years,
N 99, P 0.0001) (Schubert et al. in press).
Similarly, low-ranked adult males were more
140 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
Table 9.3 Changes in male rank between two consecutive years
Original year Subsequent year
Low Middle
Low (n 58) 20 (34.5%) 8 (13.8%)
Middle (n 17) 2 (11.8%) 3 (17.6%)
High (n 76) 5 (6.6%) 4 (5.3%)
The majority of low- and middle-ranked males increased in rank
between years. Few high-ranked males decreased in rank (from
Schubert et al. in press).
likely to increase in rank than low-ranked juveniles
(K. A. Schubert, C. Kraus, D. J. Mennill et al.,
unpublished data). Rank advancement was not
simply a function of survival, however. Of 65
males that eventually attained high rank, 30%
achieved dominance in their first year, 35% by the
age of 2, and 35% required 3 or more years
(Schubert et al. 2006). How first-year males achieve
dominance is a fascinating question, and may be
related to reduced population density in late sum-
mer or early autumn (see below). Again, because
we have not studied the process of flock formation,
our winter rank data do not provide many clues.
Smith (1991) reported that first-year birds infre-
quently achieved high ranks by replacing dead
birds. This may explain how some juvenile mem-
bers in our population attained high rank, since
flocks form in October but we assessed dominance
in February.
While rank attainment in first-year birds remains
a mystery, our data show convincingly that changes
in status of adult birds are associated with changes
in group composition. Rank increases were often a
function of shifting flock membership while former
superiors were still alive (16 out of 29 cases) rather
than replacement of dead superiors (6 cases) or
dominance reversal over a former superior (2
cases); the other 5/29 birds stayed in the same flock
but became the second high-ranked male by dom-
inating new juveniles (Schubert et al. in press).
Changes in flock membership were rare, in that
surviving flock-matesboth male and female
frequently reassociated between years (Schubert
et al. 2006). However, males that remained at low
rank tended to reflock with a greater proportion
of surviving former flock-mates (64%) than males
rising from low to high rank (39%) (Schubert et al.
2006). These results show male chickadees advance
in rank predominantly by changing social group
High rather than out-living their superior flock-mates.
Thus, changes in local population density probably
30 (51.7%)
have a major influence on whether low-ranking
12 (70.6%)
birds can occupy a new home range and attract
67 (88.2%)
juveniles as flock-mates. For example, several cases
of low-ranking males rising in status by forming
new flocks occurred as density declined sharply
from 1997 through 1998 and then increased (K. A.
Schubert, C. Kraus, D. J. Mennill et al. unpublished
data; S. Ramsay, personal communication).
9.6 Rank, survival, and lifetime
reproductive success
Previous shorter-term studies from our group and
others (Table 9.1) have documented fitness benefits
accrued by high-ranking chickadees in the form of
greater over-winter survival (Desrochers et al. 1988;
Smith 1991), better or larger territories (Desrochers
et al. 1988; Mennill et al. 2004), enhanced success in
social and extrapair mate choice (Smith 1988; Otter
et al. 1994, 1998; Otter and Ratcliffe 1996; Ramsay
et al. 2000; Bronson et al. 2003; Mennill et al. 2003b,
2004; Woodcock et al. 2005), and greater clutch size,
hatching, and fledging success (Otter et al. 1999). A
primary goal of our long-term analyses was to
partition the effects of rank from those of age, and
to determine how year effects may influence this
relationship.
9.6.1 Survival
Schubert (2003) found that adult chickadees at
QUBS survived about two winters on average, with
25% of males and 20% of females surviving to a
third winter, in general agreement with Smiths
(1991) value for average lifespan of 2.5 years. In
these analyses, where missing adults were assumed
to have died if they were not resighted on the study
site, males survived better than females (Cox
regression: Wald 2 4.17, N 436 females, 427
males, P 0.04). This finding is in agreement with
other studies of Parid survival (Desrochers et al.
1988; Lens and Dhondt 1993). Interestingly, there
was no difference in mean life expectancy of males

that attained high rank in their first year compared
to those starting at low rank, nor was there a signifi-
cant difference in survival to second year for males
that achieved high versus low rank as yearlings.
The latter result contrasts with Koivula et al. (1996)
who found social rank predicted survival of
juvenile but not adult willow tits.
To examine the effects of age and sex on male and
female annual survivorship, Schubert (2003) first
used nested, generalized linear models (GLZ) to
analyze January recapture data from 1994 to 2002.
Analyses were performed in MlWiN using a
binomial error structure (Goldstein 1995), again
assuming that birds that disappeared had died. Our
models revealed no significant effects of age (as
measured in years), but significant effects of age
class (ASY versus SY), and sex, as well as high
annual variability. Models of male survivorship
which added variables of rank class (e.g. high, mid,
low) or rank score (interactions won divided by all
interactions) showed rank to be a marginally better
predictor of male survival than age (P 0.08). To
better untangle the effects of age and rank (here
categorized as high or low only), which are tightly
correlated, a more targeted analysis applied
multistrata, capturemarkrecapture models to
resighting data from 1997 to 2002 (K. A. Schubert,
C. Kraus, D. J. Mennill et al. unpublished data).
Population annual survival varied considerably
over the 6 years (3673%), with high-ranked males
surviving somewhat better than low-ranked males
(annual survival probabilities 0.56 0.09 for high-
ranked males vs. 0.50 0.08 for low-ranked males).
Moreover, none of the well-supported models
0.35
Proportion of observations
0.30
0.25
0.20
0.15
0.10
0.05
0.00
0 1 2 3 4 5 6 7 8 9
Number of genetic offspring
SOCIAL DOMINANCE AND FITNESS 141
contained an age effect ( K. A. Schubert, C. Kraus,
D. J. Mennill et al. unpublished data). Taken
together, these analyses reveal that rank, independ-
ent of age, has an influence on annual survival in
male chickadees, even in the face of environmental
and other variation captured by modeling year
effects.
9.6.2 Reproductive success
High-ranking males are more attractive social part-
ners to female flock-mates (Schubert 2003), consis-
tent with results from our short-term studies and
experiments on femalefemale competition
(Table 9.1). Analysis of 328 pairings from 1994 to
2002 showed that over 70% of high-ranked males
but fewer than 40% of low-ranked males paired
with adult females. An overwhelming majority
(91%) of high-ranked males paired with female
flock-mates, whereas only 72% of low-ranked
males did (P 0.01); male age was not associated
with likelihood of pairing within flock (P 0.6;
Schubert 2003). Among pairs of known rank where
both survived to breed again, high-ranking males
retained social mates somewhat more often (50/58,
or 86%) than mid- (3/6, or 50%) or low-ranking
males (7/11, or 64%) (K. A. Schubert, unpublished
data). Thus high-ranked males benefit from
enhanced mate fidelity during the breeding season
(Otter et al. 1998; Mennill et al. 2004).
Figure 9.3 shows annual RRS of males and
females in the QUBS population. Average clutch
size was 6.8 0.1 eggs (N 185 clutches), with
92% overall hatching success. Of 240 nests with
Males
Females
Figure 9.3 Annual realized reproductive success (RRS)
of male and female chickadees. Genetic paternity was
determined at ca. 6 days after hatching (N 126
10 11 12 observations for males and 123 for females; from
Schubert 2003).
 142
R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
Table 9.4 Summary of nested models of the influence of male age, female age, and male rank on annual reproductive success

Nesting Clutch size Hatching RRS Fledging

(i 264, j 159) (i 128, j 93) (i 154, j 106) (i 80, j 64) (i 170, j 108)

Coefficient Wald stat Coefficient Wald stat Coefficient Wald stat Coefficient Wald stat Coefficient Wald stat
(SE) (P-value) (SE) (P-value) (SE) (P-value) (SE) (P-value) (SE) (P-value)

Intercept 0.59 0.48 0.40 0.61 1.24

(0.24) (0.18) (0.17) (0.23) (1.16)
Male age 1.16 6.62 0.29 1.96 0.42 4.62 0.35 1.84 0.46 0.96
(0.45) (0.01) (0.21) (0.16) (0.20) (0.03) (0.26) (0.17) (0.47) (0.33)
Female age NA NA 0.27 2.20 0.05 0.07 0.17 0.57 0.02 0.00.
(0.18) (0.14) (0.17) (0.79) (0.23) (0.45) (0.42) (0.97)
Male rank (H) 2.12 9.94 0.18 0.76 0.13 0.40 0.47 3.17 0.06 0.02
(0.67) (0.01) (0.21) (0.38) (0.20) (0.53) (0.27) (0.08) (0.46) (0.90)
Male rank (M) 0.63 1.34 0.04 0.02 0.21 0.60 0.12 0.14 1.07 3.07
(0.54) (0.25) (0.28) (0.89) (0.27) (0.44) (0.33) (0.71) (0.61) (0.08)

Model coefficients are given with standard errors. Wald statistics are accompanied by significance values at 1 d.f. Sample sizes i and j denote the number of observations and number of individual
male birds, respectively. Clutch size, hatching, and RRS (number of genetic offspring at day six post-hatch) are standardized within year as (x xmean)/SD; models of nesting and fledging success
use binomial response data. The full fledging model included additional year effects not presented here. Male age and female age represent the effects of adult vs. juvenile age category on breeding
success. Male rank variables represent contrasts of high- and mid-ranked males against low-ranked males (modified from Schubert 2003).

known outcomes, 56% fledged at least one
offspring. Successful pairs fledged an average of
6.3 0.1 young; 29.8 % of broods contained extra-
pair young (N 131), with an average of 11%
extrapair young per brood (N 73), remarkably
consistent with our initial estimates of EPY based
on a much smaller sample of nests (Otter et al.
1994). Annual reproductive success was lower in
males than females: only 87% of males, but 93% of
females, paired and attempted to breed (P 0.03).
The standardized variance in annual RRS was
larger in males (0.16) than females (0.07), consistent
with moderate levels of extrapair paternity.
Table 9.4 summarizes the results of nested GLZ
analyses of the effects of male and female age and
male rank on annual reproductive success
(Schubert 2003). Both male age and rank influenced
whether a male paired with a female and attempted
any nesting (P 0.02). However, compared to age,
male rank may be a stronger predictor of male RRS
(P 0.08). Surprisingly rank was not associated
with clutch size, hatching, or fledging success in
this model, in contrast to the results of Otter et al.
(1999), which was based on 2 years breeding data,
including a year of severe nest predation. Thus the
benefits of rank probably vary from year to year
(see Chapter 17 for evidence of annual variation in
effects of habitat quality).
Lifetime reproductive success of both males and
females was highly variable and heavily influenced
30
25
Number of genetic offspring
20
15
10
5 and lifetime reproductive success (LRS). LRS
0 genetic offspring attributed to 51 male and 56
1 2 3 4
Years
SOCIAL DOMINANCE AND FITNESS 143
by lifespan (Ps 0.0001) (Fig. 9.4). To test the effect
of male rank over time on LRS, we calculated the
sum of all ranks held by a male, where 1 low,
2 mid, and 3 high rank in each year. Average
lifetime rank (the sum of ranks held divided by
lifespan) significantly predicted whether a male
attempted to reproduce (P 0.01). However rank
sum/lifespan did not predict LRS among the subset
of males that succeeded in reproducing (P 0.2). In
other words, males that lived longer and reached
higher rank sooner had greater fitness, but this was
a function of whether birds reproduced at all, rather
than fine-scale differences between individuals.
9.7 Future research
Male black-capped chickadees at QUBS vary in
their ability to dominate competitors, and high
social rank enhances both annual survival and
reproduction, leading in turn to increased LRS.
Although our study was not initiated in 1992 with
a long-term design, and the data set is admittedly
limited, the results suggest several profitable
avenues for further research. One obvious question
concerns the source(s) of individual variability in
signaling behavior associated with rank, including
the role of experience in modulating individuals
responses to competitors and potential mates.
Careful measurement of ontogenetic changes in
plumage, vocalizations, and dominance behavior,
Figure 9.4 The relationship between lifespan
Females
estimates are based on the total number of
Males
5 6 female chickadees and do not include birds
that never bred (from Schubert 2003).
144 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
coupled with their associated effects on male and
female receivers, are required.
A second, related question concerns the factors
that contribute to individual variation in first-year
rank. Our analyses point to male rank history as a
key predictor of fitness, thus it would be useful to
identify the individual attributes and ecological cir-
cumstances that combine to permit some males to
achieve high rank in their first year. For example,
short-term aviary experiments using juveniles
captured in late summer could measure behavioral
predictors of dominance (e.g. Verbeek et al. 1999).
Temporary removal of dominant adults from natural
flocks might also provide useful opportunities to
observe flock fission and reassembly, as suggested
by Smith (1991). Ideally, such experiments should
be combined with detailed information on both
temporal and geographic variation in population
density, to determine whether our findings extend to
other parts of the species range. Ironically, this
critically important flock formation period remains
the least-studied part of the chickadee annual cycle.
Acknowledgements
We thank Queens University Biology Station and
adjoining landowners for access to study sites and
logistical help and the many field assistants who have
helped us over the years. Additional, crucial long-term
data were kindly provided by K. Otter and S. Ramsay.
Funding was provided by grants from NSERC, OGS,
Queens University, the American Museum of Natural
History, American Ornithologists Union, Animal
Behavior Society, Association of Field Ornithologists,
John K. Cooper Foundation, Sigma Xi, Society of
Canadian Ornithologists, and by donations from E.
and I. Ramsay and PPG Canada.
References
Alonso-Alvarez, C., Doutrelant, C., and Sorci, G. (2004).
Ultraviolet reflectance affects malemale interactions in
the blue tit (Parus caeruleus ultramarines). Behavioral
Ecology, 15, 805809.
Beacham, J. L. (2003). Models of dominance hierarchy for-
mation: effects of prior experience and intrinsic traits.
Behaviour, 140, 12751303.
Blondel, J., Gosler, A., Lebreton, J.-D., and McCleery, R.,
eds. (1990). Population Biology of Passerine Birds, an
Integrated Approach. NATO ASI Series, vol. G-24.
Springer-Verlag, Heidelberg.
Braillet, C., Charmantier, A., Archaux, F., Dos Santos, A.,
Perret, P., and Lambrechts, M. M. (2002). Two blue tit
Parus caeruleus populations from Corsica differ in social
dominance. Journal of Avian Biology, 33, 446450.
Bronson, C. L., Grubb, T. C. Jr, Sattler, G. D., and Braun,
M. J. (2003). Mate preference: a possible causal mech-
anism for a moving hybrid zone. Animal Behaviour, 65,
489500.
Christie, P. J., Mennill, D. J., and Ratcliffe, L. M. (2004).
Pitch shifts and song structure indicate male quality in
the dawn chorus of black-capped chickadees. Behavioral
Ecology and Sociobiology, 55, 341348.
Clutton-Brock, T. H. ed. (1988). Reproductive Success.
University of Chicago Press, Chicago.
Colquhoun, M. K. (1942). Notes on the social behaviour of
blue tits. British Birds, 35, 234240.
Cresswell, W. (2003). Testing the mass-dependent preda-
tion hypothesis: in European blackbirds poor foragers
have higher overwinter body reserves. Animal
Behaviour, 65, 10351044.
Dale, S. and Slagsvold, T. (1995). Female contests for nest
sites and mates in the pied flycatcher Ficedula hypoleuca.
Ethology, 99, 209222.
Dall, S. R. X., Houston, A. I., and McNamara, J. M. (2004).
The behavioural ecology of personality: consistent indi-
vidual differences from an adaptive perspective.
Ecology Letters, 7, 734739.
De Laet, J. (1984). Site-related dominance in the Great Tit
Parus major. Ornis Scandinavica, 15, 7378.
Desrochers, A. (1989). Sex, dominance and microhabitat
use in wintering black-capped chickadees: a field
experiment. Ecology, 70, 636645.
Desrochers, A. and Hannon, S. J. (1989). Site-related
dominance and spacing among winter flocks of black-
capped chickadees. Condor, 91, 317323.
Desrochers, A., Hannon, S. J., and Nordin, K. E. (1988).
Winter survival and territory acquisition in a northern
population of black-capped chickadees. Auk, 105,
727736.
deVries, H. (1998). Finding a dominance order most con-
sistent with a linear hierarchy: a new procedure and
review. Animal Behaviour, 55, 827843.
Dhondt, A. A. (1989). Blue tit. In: Newton, I., ed. Lifetime
Reproduction in Birds. Academic Press, London.
Dixon, K. L. (1965). Dominance-subordination relation-
ships in mountain chickadees. Condor, 67, 291299.
Doucet, S. M., Mennill, D. J., Montgomerie, R., Boag, P. T.,
and Ratcliffe, L. M. (2005). Achromatic plumage
reflectance predicts reproductive success in male black-
capped chickadees. Behavioral Ecology, 16, 218222.

Drews, C. (1993). The concept and definition of domi-
nance in animal behaviour. Behaviour, 125, 283313.
Dugatkin, L. A. and Earley, R. L. (2004). Individual recog-
nition, dominance hierarchies and winner and loser
effects. Proceedings of the Royal Society of London B, 271,
15371540.
Ekman, J. (1989). Ecology of non-breeding social systems
among the Paridae. Wilson Bulletin, 101, 263288.
Ekman, J. (2004). Mass-dependence in the predation risk of
unequal competitors; some models. Oikos, 105, 109116.
Ellis, L. (1995). Dominance and reproductive success
among non-human animals: a cross-species compari-
son. Ethology and Sociobiology, 16, 257333 .
Ficken, M. S., Weise, C. M., and Popp, J. W. (1990).
Dominance rank and resource access in winter flocks of
black-capped chickadees. Wilson Bulletin, 102, 623633.
Forkman, B. and Haskell, M. J. (2004). The maintenance of
stable dominance hierarchies and the pattern of aggres-
sion: support for the suppression hypothesis. Ethology,
110, 737744.
Glase, J. C. (1973). Ecology of social organization in the
black-capped chickadee. Living Bird, 12, 235267.
Goldstein, H. (1995). Multilevel Statistical Models, 2nd edn.
Arnold, London.
Hansen, B. T. and Slagsvold, T. (2004). Early learning affects
social dominance: interspecifically cross-fostered tits
become subdominant. Behavioral Ecology, 15, 262268.
Hartzler, J. E. (1970). Winter dominance relationships
in black-capped chickadees. Wilson Bulletin, 82,
427434.
Hay, J. M., Evans, P. R., Ward, R. M., and Hamer, K. C.
(2004). Poor nutritional condition as a consequence of
high dominance status in the coal tit Parus ater. Ibis, 146,
103107.
Hogstad, O. (1987a). It is expensive to be dominant. Auk,
104, 333336.
Hogstad, O. (1987b). Social rank in winter flocks of willow
tits Parus montanus. Ibis, 129, 19.
Hogstad, O. (1989). Social organization and dominance
behavior in some Parus species. Wilson Bulletin, 101,
254262.
Koivula, K., Kimmo, L., Orell, M., and Rytkonen, S. (1993).
Prior residency as a key determinant of social dom-
inance in the willow tit (Parus montanus). Behavioral
Ecology and Sociobiology, 33, 283287.
Koivula, K., Orell, M., and Rytkonen, S. (1996). Winter
survival and breeding success of dominant and subor-
dinate willow tits Parus montanus. Ibis, 138, 624629.
Lahti, K., Koivula, K., Orell, M., and Rytkonen, S. (1996).
Social dominance in free-living willow tits Parus
montanus: determinants and some implications of hier-
archy. Ibis, 138, 539544.
SOCIAL DOMINANCE AND FITNESS 145
Lange, H. and Leimar, O. (2003). The function of threat
display in wintering great tits. Animal Behaviour, 65,
573584.
Lange, H. and Leimar, O. (2004). Social stability and daily
body mass gain in great tits. Behavioral Ecology, 15,
549554.
Lemel, J. and Wallin, K. (1993). Status signaling, motiv-
ational condition and dominance: an experimental
study in the great tit, Parus major. Animal Behaviour, 45,
549558.
Lens, L. and Dhondt, A. A. (1993). Individual variation in
mate care by alpha males in crested tit winter flocks.
Behavioral Ecology and Sociobiology, 33, 7985.
Leonard, M. L., Horn, A. G., and Ratcliffe, L. M. (1991).
Parental aggression in black-capped chickadees.
Behavioral Ecology, 2, 228233.
Lundborg, K. and Brodin, A. (2003). The effect of dom-
inance rank on fat deposition and food hoarding in the
willow tit Parus montanusan experimental test. Ibis,
145, 7882.
Matthysen, E. (1990). Nonbreeding social organization in
Parus. In: Power, D. M., ed. Current Ornithology, vol. 7,
pp. 209249. Plenum Press, New York.
McCleery, R. H. and Perrins, C. M. (1988). Lifetime repro-
ductive success of the great tit. Parus major. In: Clutton-
Brock, T. H., ed. Reproductive Success. University of
Chicago Press, Chicago.
Mennill, D. J. and Ratcliffe, L. M. (2004a). Nest cavity
orientation in black-capped chickadees Poecile atricapil-
lus: do the acoustic properties of cavities influence
sound reception in the nest and extra-pair matings?
Journal of Avian Biology, 35, 477482.
Mennill, D. J. and Ratcliffe, L. M. (2004b). Overlapping
and matching in the song contests of black-capped
chickadees. Animal Behaviour, 67, 441450.
Mennill, D. J. and Ratcliffe, L. M. (2004c). Do male black-
capped chickadees eavesdrop on song contests? A
multi-speaker playback experiment. Behaviour, 141,
125139.
Mennill, D. J., Boag, P. T., and Ratcliffe, L. M. (2003b).
The reproductive choices of eavesdropping female
black-capped chickadees, Poecile atricapillus.
Naturwissenschaften, 90, 577582.
Mennill, D. J., Doucet, S. M., Montgomerie, R., and
Ratcliffe, L. M. (2003a). Achromatic color variation in
black-capped chickadees, Poecile atricapilla: black and
white signals of sex and rank. Behavioral Ecology and
Sociobiology, 53, 350357.
Mennill, D. J., Ramsay, S. M., Boag, P. T., and Ratcliffe,
L. M. (2004). Patterns of extra-pair mating in relation to
male dominance status and female nest placement in
black-capped chickadees. Behavioral Ecology, 15, 757765.
146 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
Mennill, D. J., Ratcliffe, L. M., and Boag, P. T. (2002).
Female eavesdropping on male song contests in song-
birds. Science, 296, 873.
Newton, I. ed. (1989). Lifetime Reproduction in Birds.
Academic Press, London.
Nilsson, J.-A. and Smith, H. G. (1985). Early fledgling
mortality and the timing of juvenile dispersal in the
marsh tit Parus palustris. Ornis Scandinavica, 16, 293298.
Nilsson, J.-A. and Smith, H. G. (1988). Effects of dispersal
date on winter flock establishment and social dom-
inance in marsh tits Parus palustris. Journal of Animal
Ecology, 57, 917928.
Otter, K. and Ratcliffe, L. (1996). Female-initiated divorce
in a monogamous songbird: abandoning mates for
males of higher quality. Proceedings of the Royal Society
London B, 263, 351354.
Otter, K., Chruszcz, B., and Ratcliffe, L. (1997). Honest
advertisement and song output during the dawn
chorus of black-capped chickadees. Behavioral Ecology,
8, 167173.
Otter, K., Ramsay, S. M., and Ratcliffe, L. (1999). Enhanced
reproductive success of female black-capped chicka-
dees mated to high-ranking males. Auk, 116, 345354.
Otter, K., Ratcliffe, L., and Boag, P. T. (1994). Extra-pair
paternity in the black-capped chickadee. Condor, 96,
218222.
Otter, K., Ratcliffe, L., Michaud, D., and Boag, P. T. (1998).
Do female black-capped chickadees prefer high-rank-
ing males as extra-pair partners? Behavioral Ecology and
Sociobiology, 43, 2536.
Piper, W. H. (1997). Social dominance in birds: early find-
ings and new horizons. In: Nolan, V. Jr, Ketterson, E.,
and Thompson, C. F., eds. Current Ornithology, Vol. 14,
pp. 125187. Plenum, New York.
Pravosudov, V. V. and Grubb, T. C. (1997). Energy man-
agement in passerine birds during the non-breeding
season. In: Nolan, V. Jr, Ketterson, E., and Thompson,
C. F., eds. Current Ornithology. Vol. 14, pp. 189234.
Plenum, New York.
Ramsay, S. M. and Ratcliffe, L. M. (2003). Determinants
of social rank in female black-capped chickadees (Poecile
atricapilla). Canadian Journal of Zoology, 81, 117121.
Ramsay, S. M., Otter, K. A., Mennill, D. J., Ratcliffe, L. M.,
and Boag, P. T. (2000). Divorce and extrapair mating in
female black-capped chickadees (Parus atricapillus):
separate strategies with a common target. Behavioral
Ecology and Sociobiology, 49, 1823.
Sandall, M. and Smith, H. G. (1991). Dominance, prior
occupancy, and winter residency in the great tit
(Parus major). Behavioral Ecology and Sociobiology, 29,
147152.
Schubert, K. A. (2003). Lifespan, Social Rank and Lifetime
Reproductive Success in Black-Capped Chickadees. MSc
thesis, Queens University, Kingston, Canada.
Schubert, K. A., Mennill, D. J., Ramsay, S. M., Otter, K. A.,
Boag, P. T., and Ratcliffe. L. M. (2006). Variation in social
rank acquisition influences lifetime reproductive suc-
cess in black-capped chickadees. Biological Journal of the
Linnaean Society, 89, in press.
Smith, S. M. (1976). Ecological aspects of dominance
hierarchies in black-capped chickadees. The Auk, 93,
95107.
Smith, S. M. (1988). Extra-pair copulations in black-
capped chickadees: the role of the female. Behaviour,
107, 1523.
Smith, S. M. (1991). The Black-capped Chickadee. Behavioral
Ecology and Natural History. Cornell University Press,
Ithaca, NY.
Verbeek, M. E. M., De Goede, P., Drent, P. J., and
Wiepkema, P. R. (1999). Individual behavioural charac-
teristics and dominance in aviary groups of great tits.
Behaviour, 136, 2348.
Verhulst, S. and Salomons, H. M. (2004). Why fight?
Socially dominant jackdaws, Corvus monedula, have low
fitness. Animal Behaviour, 68, 777783.
Wiley, R. H., Steadman, L., Chadwick, L., and Wollerman,
L. (1999). Social inertia in white-throated sparrows
results from recognition of opponents. Animal
Behaviour, 57, 453463.
Woodcock, E. A., Rathburn, M. K., and Ratcliffe L. M.
(2005). Achromatic plumage reflectance, social
dominance and female mate preference in black-
capped chickadees (Poecile atricapillus). Ethology, 111,
891900.
Zanette, L. and Ratcliffe, L. M. (1994). Social rank
influences conspicuous behaviour of black-capped
chickadees (Parus atricapillus). Animal Behaviour, 48,
119127
 SYNOPSIS II
Parid reproductive behavior
Daniel J. Mennill, Theresa M. Burg, Robert L. Curry, Kathy
Martin, Andrea R. Norris, Laurene Ratcliffe, Matthew W.
Reudink, Lindsay M. Rossano, and Kristin A. Schubert
North American Parids are excellent organisms for
research on the evolution of avian reproductive
behavior, and how these are influenced by intra-
and interspecific interactions. As cavity-nesting
birds, they exhibit high reproductive success and
populations of most Parid species exist in high
numbers throughout their range. As social birds,
their reproductive behavior is shaped by group
dynamics, including flock hierarchy and territorial
behavior. Being non-migratory, their behavior can
be studied throughout the year, and their breeding
activities can be easily related to their non-breeding
activities. This section of the book covers a diversity
of topics within the general field of Parid reproduc-
tive behavior, using ongoing research on several
species of North American chickadees. The various
chapters discuss: phylogenetic structure within
populations, hybridization between closely related
species, nesting ecology, and the influence of social
dominance on reproductive biology.
Chapter 6 examines the phylogenetic structure of
chestnut-backed chickadee populations in western
North America and compares the resulting patterns
to those found in other North American and
Eurasian Parids. Chestnut-backed chickadees are
associated with cedarhemlock ecosystems, and
their movement into an area is dependent on the
availability of suitable habitat. Much of the chest-
nut-backed chickadees current range was glaciated
during the Pleistocene and was recolonized follow-
ing the retreat of the Cordilleran ice sheet. Four
genetically distinct groups are recognized: Queen
Charlotte Islands; southeastern British Columbia;
mainland Alaska; and a large coastal group. Several
scenarios may explain the current distribution
patterns found in chestnut-backed chickadees:
multiple colonizations from a single refugium,
colonization from multiple refugia, or a single
colonization from a single refugium and possible
introgression. Northern populations possess a large
number of alleles that are absent in other popula-
tions, indicative of prolonged isolation. Whether
this isolation is the result of historical isolation in
different glacial refugia or different founding popu-
lations is not known. The second pattern that
emerged from studying the phylogenetic structure
of chestnut-backed chickadees is that disjunct and
peripheral populations are genetically isolated
from the central core population. A similar pattern
is found in other Eurasian and North American
Parid species. Dispersal across large expanses of
unsuitable habitat and between the periphery and
core portions of the species range appear to be
limited, resulting in population substructuring.
Future phylogenetic research may determine the
origin of the private alleles in the northern popula-
tions of chestnut-backed chickadees. Is the large
number of unique alleles the result of hybridization
with another species, such as the boreal chickadee?
Hybridization between two brown-capped chicka-
dee species has not been reported; however,
hybridization between several other Parid species
is common (Curry 2005; Chapter 7). Do other
populations of chestnut-backed chickadees in the
interior Pacific North-west show the same pattern
of differentiation as the south-eastern British
Columbia population? Similarly, are we able to
determine the source population of the recent
147
148 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R
expansion into central California? On a larger scale,
further studies need to be conducted examining
population structure in other chickadee species,
expanding on the previous work by Gill et al. (1993,
2005). Are the patterns of peripheral isolation and
isolation of disjunct or island populations found in
chestnut-backed chickadeesas well as prelimi-
nary studies of other North American chickadees
present when more extensive sampling is
conducted? By addressing these questions, we can
further increase our understanding of movements
and speciation in Parids.
Chapter 7 continues on this theme by examining
the behavioral aspects of hybridization along the
extended contact zone between black-capped
chickadees and Carolina chickadees in south-east-
ern Pennsylvania. Intensive field research in this
contact zone since 1998 has focused on three large
study sites, with a specific focus on variation in
vocalizations among color-banded individuals,
while concurrently investigating genetic variation
among and within the populations. The most strik-
ing finding concerns discrepancies between the
songs, calls, and genotypes of chickadees at a geo-
graphically intermediate site. Within this popula-
tion, which mainly comprises hybrid individuals,
up to half of all males are bilingual, singing the
typical songs of both black-capped and Carolina
chickadees. The rest of the males sing only black-
capped songs, although the proportion of the popu-
lation falling into this category has gradually
declined over time. This pattern of song variation
probably represents cultural persistence of learned
behavior. Virtually all males in the population have
Carolina mitochondrial DNA, and no overall dif-
ference in nuclear genotype, assessed using
microsatellite DNA, is apparent between the two
types of males based on songs. On the other hand,
characteristics of the dee note of the chick-a-dee call
of the same birds are intermediate between those of
black-capped and Carolina chickadees; call charac-
teristics show no apparent correlation with either
song category or genetic background.
Numerous unresolved questions about behav-
ioral mechanisms associated with Parid hybridiza-
tion remain, both in the black-capped/Carolina
chickadee contact zone and for other members of
the family more broadly. Most investigators have
assumed or concluded that vocalizations play key
roles in species recognition within the Parids.
However, it seems clear that song development,
and possibly song recognition, in most (if not all)
Parids involves strong learning components (see
also Section III). Accordingly, the vocal behavior of
an individual male may inaccurately reflect its
genotype, but whether hybridization results from
female mate choice contingent on song features
remains incompletely tested. A second, and pos-
sibly independent, aspect of Parid behavior that
could exert a strong influence on pairing patterns is
social dominance. Extensive results from black-
capped chickadees have revealed that dominance
rank strongly influences both pairing success and
mating fidelity (Ramsay et al. 2000; Mennill et al.
2004; Chapter 9). Research on captive birds from
the hybrid zone has further suggested that mate
choice may depend mainly on relative dominance,
more so than vocal or physical phenotype (Bronson
et al. 2003). Nevertheless, work on black-capped
chickadees has also shown that both singing behav-
ior (e.g. Otter et al. 1997; Mennill et al. 2002 ) and
plumage coloration (Doucet et al. 2005) relate to
patterns of extrapair paternity and reproductive
success. Studies using both observational and
experimental approaches to thoroughly evaluate
the relative strengths of social dominance, song,
and plumage features within Parid hybrid zones
are needed to produce clearer resolution of the
behavioral mechanisms underlying hybridization
in the family. Further research on vocal develop-
ment, through experimental studies of captive
birds subjected to various acoustic and social stim-
uli, represents an additional area with great prom-
ise for advancing our understanding of the role of
vocal behavior in Parid hybridization.
Interspecific interactions can also influence
reproductive ecology in manners other than
hybridization, and these are not limited to include
only other Parids. Chapter 8 examines the nesting
biology of black-capped and mountain chickadees
and their ecological relationships within cavity-
nesting vertebrate communities. Parids live in com-
munities structured by hierarchical guilds termed
nest webs whereby some species depend on others
to produce cavities for breeding or roosting, and
interspecific and intraspecific interactions are

centered around nest site availability (Martin and
Eadie 1999). Despite similar size, ecology, and
coexistence on the same sites, mountain and black-
capped chickadees exhibit strong segregation in
nesting habitats in the mixed forests of central
British Columbia. From 1995 to 2004, mountain
chickadee numbers showed a strong increase, with
similar increases in their small bodied competitors
(red-breasted nuthatches) and potential predators
(red squirrels), and also a strong reduction in the
health of conifer trees, especially lodgepole pine.
Overall nesting densities of mountain chickadees
were positively correlated with the proportion of
lodgepole pine trees that had been attacked by bark
beetles, nesting densities of red-breasted nuthatch
and downy woodpeckers, and negatively corre-
lated with density of red-naped sapsuckers, red-
breasted nuthatches, and tree density. Nest density
of mountain chickadees was significantly greater in
years of high beetle and western spruce budworm
abundance. Population growth rates demonstrated
strong negative density-dependent responses to
chickadee density the previous year, but were
enhanced by an abundance of forest insects and
density of trees, and reduced by high abundance of
red squirrels. Thus mountain chickadees show
strong functional and numerical responses to
pulses in resource availability despite strong
increases in their competitors and predators.
While mountain chickadees showed the
strongest ability to adapt to local differences in
habitat conditions, black-capped chickadees
declined in density in 2003 and 2004. Since black-
capped chickadees are behaviorally dominant to
mountain chickadees and able to excavate their
own cavities, it is puzzling why they were not able
to capitalize on the resource pulse in the enhanced
habitat conditions. It is interesting that black-
capped chickadees, reasonably strong excavators,
could not respond to the increase in forest insects to
the same extent as mountain chickadees; perhaps
an ecologically-equivalent situation to subordinate
blue tits depressing reproductive success of the
dominant great blue tits in sympatric populations.
Martin and Norris assumed that the functional and
numerical responses observed were driven by local
pulses in resource availability or mild winter
conditions. However, it is possible that some of the
SOCIAL DOMINANCE AND FITNESS 149
temporal changes observed in chickadee abun-
dance were driven by larger-scale environmental or
ecological influences, as the dramatic changes in
annual fecundity of mountain chickadees they
observed in 2005 were similar to those observed in
the Sierra Nevada. Future research exploring
regional- or continental-scale patterns of Parid
breeding biology will help elucidate these critical
influences on demography.
Within-species, reproductive potential may be
influenced by social interactions, especially by the
dominance hierarchies established in wintering
chickadee flocks. The naturally- and sexually-
selected fitness consequences of social dominance,
the mechanics of dominance interactions, and the
relationship between dominance and lifetime
reproductive success in black-capped chickadees
are explored in Chapter 9. Data from over 10 years
of research on the dominance relationships and
breeding behavior of black-capped chickadees at
Queens University Biological Station in eastern
Ontario show that social dominance rank plays an
important role in structuring several aspects of an
individuals life history, from winter flock behavior
to territorial behavior and reproductive activities.
Dominant and subordinate birds show distinct
phenotypic characteristics (e.g. enhanced plumage
contrast, higher song output for high-ranking
males) and life history characteristics (e.g. higher
nesting success, larger clutch sizes for high-ranking
males). Longitudinal and cross-sectional analyses
of survival and reproduction show that social rank
is a better predictor than age of individual survival
from one winter to the next. In common with other
avian life history studies, lifespan was the best
predictor of average lifetime reproductive success.
However, male rank history also influenced life-
time realized reproductive success: individuals that
attained higher rank earlier had more offspring.
Dominance relationships mediate social inter-
actions in many Parids, and future studies should
explore how widespread are these patterns among
the Paridae. Future research exploring the early
ontogeny of social rank, as well as attributes associ-
ated with high and low rank such as plumage color
and singing behavior, is needed. The process of
flock formation in the autumn requires more
careful behavioral study, as this period of the
150 R E P R O D U C T I V E E C O L O G Y, E V O L U T I O N, A N D B E H AV I O R

annual cycle of black-capped chickadees has been Martin, K. and Eadie, J. (1999). Nest webs: a community-
neglected in the eastern Ontario studies. wide approach to the management and conservation of
cavity-nesting forest birds. Forest Ecology and
Management, 115, 243257.
References Mennill, D. J., Ramsay, S. M., Boag, P. T., and Ratcliffe,
L. M. (2004). Patterns of extrapair mating in relation to
Bronson, C. L., Grubb, T. C., Jr, Sattler, G. D., and Braun,
male dominance status and female nest placement in
M. J. (2003). Mate preference: a possible causal mech-
black-capped chickadees. Behavioral Ecology, 15,
anism for a moving hybrid zone. Animal Behaviour, 65,
757765.
489500.
Mennill D. J., Ratcliffe, L. M., and Boag, P. T. (2002).
Curry, R. L. (2005). Hybridization in chickadees: much to
Female eavesdropping on male song contests in song-
learn from familiar birds. Auk, 122, 747758.
birds. Science, 296, 873883.
Doucet, S. M., Mennill, D. J., Montgomerie, R., Boag, P. T.,
Otter, K., Chruszcz, B., and Ratcliffe, L. (1997). Honest
and Ratcliffe, L. M. (2005). Achromatic plumage
advertisement and singing during the dawn chorus of
reflectance predicts reproductive success in male black-
black-capped chickadees, Parus atricapillus. Behavioral
capped chickadees. Behavioral Ecology, 16, 218222.
Ecology, 8, 167173.
Gill, F. B., Mostrom, A. M., and Mack, A. L. (1993).
Ramsay, S. M., Otter, K., Mennill, D. J., Ratcliffe, L. M., and
Speciation in North American chickadees: I. Patterns of
Boag, P. T. (2000). Divorce and extra-pair mating in
mtDNA genetic divergence. Evolution, 47, 195212.
female black-capped chickadees (Parus atricapillus): sep-
Gill, F. B., Slikas, B., and Sheldon, F. H. (2005). Phylogeny
arate strategies with a common target. Behavioral
of titmice (Paridae): II. Species relationships based on
Ecology and Sociobiology, 49, 1823.
sequences of the mitochondrial cytochrome b gene.
Auk, 122, 121143.
 SECTION III
Vocal communication
Parids are among the best-studied avian family,
globally, with respect to vocal communication.
Although not necessarily elaborate songsters,
Parids have extremely diversified vocalizations
which have formed rich fodder for entire research
careers. North American chickadees and titmice
(and their Eurasian Poecile counterparts) also have
vocal attributes that make this family unusual, as
they do not follow the commonly held definition
that distinguishes songs (structurally complex,
learned vocalizations given primarily by males
during the breeding season for mate attraction and
territory defense) from calls (structurally simple,
innate vocalizations given by both sexes year-
round, in contexts other than mate attraction and
territory defense). Poecile chickadeesand
Baeolophus titmice, although less well studiedblur
these distinctions in the production of three classes
of vocalizationswhistled songs (often colloqui-
ally referred to as fee-bees after the song of the well-
studied black-capped chickadee), gargles, and
chick-a-dees.
There is evidence for learning and regional vari-
ation in all three of these vocalizations. Further, the
whistled songs of chickadees are typically less com-
plex than the structural components of the chick-a-
dee and gargle complexes. Chick-a-dees have a
syntactical structure that has resulted in direct com-
parisons to human language. Yet despite this, whis-
tled songs follow the behavioral patterns (restricted
use, primarily by males, in context of territorial
defense) typically associated with song. The intrica-
cies of these three vocalizations justify individual
chapters on each.
The section begins with a look at the production
and perception of fee-bees and chick-a-dees in both
field and laboratory studies of chickadees (Chapter
10). Sturdy, Bloomfield, Charrier, and Lee review
studies that use operant techniques to tease apart
the mechanisms by which note structure and
sequence are classified. Lucas and Freeberg
(Chapter 13) build on this by addressing the
potential for information encoding in the chick-a-dee
complex in Carolina and other species, and the
potential of this call to convey complex and
multifacetted aspects of information transfer. The
emphasis in this chapter is on the use of field
experimentation to determine the context and
message of calls, which complements the work
on classification and perception outlined by
Sturdy et al.
Baker and Gammon (Chapter 11) take a relatively
unprecedented look at dialectal variation, signal
convergence with populations, and signal match-
ing in a vocalization technically classified as a
call, the gargle complex of black-capped chicka-
dees. While the complexity of this vocalization is
one of the primary features blurring the distinction
between calls and songs, the matching and inter-
active playback studies may indicate subtle differ-
ences between how birds communicate with gargles
and with whistled songs.
151
152 V O C A L C O M M U N I C AT I O N
In Chapter 12, Gammon assesses the potential for
postdispersal environments to influence song struc-
ture in the fee-bee of black-capped chickadees. This
call is remarkably stereotyped throughout much of
the extensive distribution of this species across
North America, yet extreme cases of song variation
in isolated populations may give insight into the
nature of dialectal variation that arises through
social isolation.
Finally, Mennill and Otter (Chapter 14) investi-
gate the potential for an apparently simple song
the fee-bee of the black-capped chickadeeto con-
vey complex information. Through the use of fre-
quency shifting, chickadees appear to perform
similar aspects of signal matching and interactive
communication with their single song type typ-
ically associated with use of repertoires in other
species. Further, this chapter addresses the ability
to signal dominance status and condition, as well as
the ability of receivers to gather this information
about potential mates and rivals, in the context of
communication networks.
 CHAPTER 10

Chickadee vocal production and

perception: An integrative approach
to understanding acoustic
communication
Christopher B. Sturdy, Laurie L. Bloomfield,
Isabelle Charrier, and Tiffany T.-Y. Lee

10.1 Introduction song is produced mainly by males and the peak of

The three key elements in the scientific study of ani-
mal communication are the sender and the receiver,
and the interaction between these two elements.
Senders produce a signal that is perceived by the
receiver and, operationally, communication occurs
when the signal leads to an observable change in
the behavior of the receiver (Maynard Smith and
Harper 2003). Just as production and perception are
integral to communication in general, so too must
both sides of the equation be considered when
studying acoustic communication in any particular
species or in any animal group. Here we take this
integrative approach and equally consider both
production and perception, in an attempt to under-
stand acoustic communication in one of the most
well-recognized and well-studied groups of North
American songbirds, the chickadees.
10.2 Song production and perception
10.2.1 Song production
In the prototypic species of the genus Poecile, the
black-capped chickadee, the species song is termed
fee-bee (Fig. 10.1a; see Box 10.1 for notes on the
discovery of the black-capped chickadees song).
Since song in this species has been investigated
most heavily, it will be used as a model here. Fee-bee
production occurs in the spring and early summer.
The song of black-capped chickadees has been the
subject of intensive field studies over the past
decade (see Chapters 13 and 14), focusing primarily
on the functional aspects of singing behavior. Our
focus here will be on vocal production and
structure.
Black-capped chickadees sing their two-note
song at several distinct pitches (Fig. 10.1a). Initially
quantified in detail by Ratcliffe and Weisman (1985)
and Weisman et al. (1990), work over the last decade
has shown that there is a frequency range over
which the species songs are produced, spanning
approximately 1 kHz from lowest to highest songs,
and individual males can sing at a variety of
discrete pitches within this range (see Chapter 14
for further details on possible functions for pitch
shifting). However, at all of these various pitches,
the song remains a relatively high-frequency
vocalization that approximates a pure tone.
Average songs have a starting frequency of about
4000 Hz. The first note ( fee) then falls by about 200
Hz from the start to the end. There is another fre-
quency drop between the end of the fee and the start
of the second note (bee) equal to about a 400 Hz
drop. These regularities in pitch structure led
Weisman and colleagues (1990) to conduct a bio-
acoustic analysis, of a small sample and then an

153
154 V O C A L C O M M U N I C AT I O N

(a)
6
Frequency (kHz)

0
0 0.5 1.0 1.5 2.0 2.5
Time (sec)
(b)
6

Glissando Relative pitch ratio

~ 1.12
Frequency (kHz)

4 Fee
start Fee
end
Bee Bee
start end

2
Figure 10.1 (a) Two representative fee-
bee songs. Spectrogram settings: Hanning
window, 1024 points. (b) A fee-bee song
indicating the location of specified
0 measurements. Time (sec) is on the x axis
0 0.2 0.4 0.6 0.8 1.0 1.2 and frequency (kHz) is on the y axis in both
Time (sec) spectrograms.

exhaustive sample of songs, to determine first the
acoustic properties of the song and second, which if
any of these properties could be used in species and
individual identification.
One of the key findings from the initial bioa-
coustic analysis of black-capped chickadee fee-bee
song was males produced their songs with remark-
able regularity from one rendition to the next,
regardless of the initial starting frequency. Another
remarkable finding from these early studies of
chickadee song is that it maintains a constant and
equivalent relative pitch ratio between the two
notes. This relative pitch ratio was calculated by
dividing the end frequency of the fee note by the
starting frequency of the bee note: this ratio was
approximately 1.13 for all songs among all males.
Even more remarkable was the fact that this relative
pitch ratio was maintained when birds produced
shifted song. That is, when birds change the overall
starting frequency of the song, the frequency ratio
between the two notes remained constant. In other
words, male chickadees adjust the relative pitch
between notes when they frequency shift, so as to
maintain a constant tune. This implies that birds
were maintaining precise control over their vocal
production as well as monitoring their vocal
production in order to maintain this relative
pitch ratio.
In the follow-up, Weisman et al. (1990) recorded
songs from 156 males singing on their territories,

Box 10.1 What is the song of the black-capped chickadee?
Chickadee song, or more specifically what is
considered chickadee song, has been a matter of
debate (Ficken 1981). Although chickadees
produced several vocalizations, the particular
vocalization that functioned as song per se,
was contested. Two main contenders were
identified: the fee-bee and the acoustically
complex gargle call (Chapter 11). In fact, early
reports termed what is now considered to be
chickadee song (fee-bee) their call (Dwight 1897).
This is in large part due to the fact that
chickadees do not conform to commonly held
truism for songbird vocal production, this being
that songs are thought to be a complex
vocalization, produced mainly by males, are
and measured a greater number of acoustic features
than simply the constant frequency of the fee and
bee, along with temporal measures. Several impor-
tant findings regarding song production arose from
Weisman et al.s more extensive study. Absolute
pitch was found to be relatively consistent within
birds but variable among birds. Thus, as a species
marker, absolute pitch would provide a coarse
assessment of species identity, but it could be used
for individual recognition. It was when attention
was turned to relative pitch cues, however, that
things got particularly interesting.
Relative pitch production can be further subdiv-
ided into at least two other categories, relative
pitch contour and relative pitch ratio, both of which
were examined by Weisman et al. (1990). Relative
pitch contour refers to the ordinal pitch relation-
ships between adjacent notes, or features of notes. In
black-capped chickadee song, these relationships
were constant in almost every song sampled, with
the starting pitch of the fee greater than the end of
the fee, and the end of the fee greater than the pitch
of the bee note. A constant pitch ratio, on the other
hand, requires there to not only be the ordinal rela-
tionships described for pitch contour, but it requires
the additional feature of maintaining the same pitch
ratio between acoustic features, both between the fee
start and fee end, and between the end of the fee and
VOCAL PRODUCTION AND PERCEPTION 155
produced mainly during the breeding season, and
are acquired through imitative learning. Calls, by
contrast, are thought to be less complex,
produced by both sexes throughout the year in
contexts outside mate attraction and territory
defense, and are largely innate (Catchpole and
Slater 1995). These facts made the identification
of the chickadee song somewhat contentious. An
additional factor, that likely enhanced the
confusion around the issue, was not all chickadee
species produce a whistled, tonal vocalization. In
the end, the whistled song was accepted as the
species-typical vocalization that served the typical
functions of songmate attraction and territorial
defense.
the start of the bee note. Importantly, and strikingly,
these relationships could be perfectly accounted for
with a linear regression, so that, for instance, as the
pitch of fee start increased, so did the pitch of fee end.
A similar pattern also emerged for the ratio of fee
end to bee, and these relative pitch findings were
consistent regardless of the starting pitch of the
song. Moreover, variation in the relative pitch cues
observed within birds was tiny compared to those
among birds and even smaller than the within-bird
variation seen for absolute pitch cues. Put another
way, birds could potentially use relative pitch cues,
present in either normal or shifted songs, for species
and individual identification.
As intriguing as these findings were, they were
only one side of the coin, that of song production.
Whether the birds used any or all of the features for
species or individual recognition was unclear.
Perceptual experiments were required to systemat-
ically determine the role of each of these features
identified in the production analyses. We will there-
fore turn to song perception momentarily.
10.2.2 Song perception
Once potentially relevant, or at least invariant, song
features were identified, the next critical step was to
determine whether and how any or all of these
156 V O C A L C O M M U N I C AT I O N
features were related to song perception in black-
capped chickadees. This required perceptual
experiments in which natural and manipulated
versions of the songs, or, in some cases, synthetic
representations of the songs, were presented to
birds and their responses compared. To this end,
two main classes of experiments were conducted,
playback experiments and laboratory-based operant
conditioning experiments, with each approach
having its own advantages and limitations.
10.2.2.1 Playback experiments of song perception
Laboratory playback procedures were carried out
by Ratcliffe and Weisman (Ratcliffe and Weisman
1986, 1988; Weisman and Ratcliffe 1989) as first
steps towards determining which, if any, features
identified in the initial bioacoustic analyses were
used for species recognition in chickadees. Initially,
Ratcliffe and Weisman (1986, 1988) focused on
whether chickadees attend to the pitch contour and
number of notes present in their songs. This was
accomplished in a similar manner in each experi-
ment; individual male chickadees were isolated
from other birds for a period of time, followed by
presentations of various versions of altered song
(e.g. only the fee, bee-fee, bee-bee, fee-bee-bee, etc.).
These experiments returned several interesting
results. Ratcliffe and Weisman (1986) found that
birds discriminated between fee and bee notes and
also responded less to songs that were either artifi-
cially lengthened or shortened. Ratcliffe and
Weisman (1988) extended these results by showing
that birds responded more slowly to songs that con-
tained an extra note at the beginning, such as fee-fee-
bee, but not when an extra note was added to the
end, such as fee-bee-bee. These latter results implied
that birds were in fact sensitive not only to the
duration of their songs, but also to the temporal
locations of the two different notes in their songs.
Taken together, it became clear that chickadees
perceived rather strict rules in their seemingly
simple songs, with pitch contour playing an impor-
tant role.
While these experiments dealt with issues of note
type and number discrimination, along with pitch
contour perception, they did not deal specifically
with the role of absolute or relative pitch cues
in black-capped chickadee song. Two separate
laboratory playback experiments were devised; one
each to test birds reactions to songs altered either
in absolute or relative pitch. To alter the absolute
pitch, normal base songs were linearly shifted in
pitch so that they ranged from below to above the
absolute range of what is typical for black-capped
song production. In order to test for only absolute
pitch perception, the relative pitch ratio between
the end of the fee and start of the bee note was
maintained. To alter the relative pitch, base songs
were manipulated to produce several renditions
that started with the original fee start frequency, but
that contained various pitch ratios between the fee
end and bee start. Thus, in the second set of songs,
the absolute starting pitch remained consistent
while the relative pitch ratio between the fee and bee
notes varied.
When chickadees were presented with songs out-
side of the species-typical range of absolute pitch,
either higher or lower, birds in general responded
less to these than to normal songs. In particular,
birds were less likely to respond with social
vocalizations when song was played outside the
typical absolute frequency range.
Relative pitch-altered songs also lead to a differ-
ential response when presented to male chickadees,
but not in the same manner as those altered in
absolute pitch. When the relative pitch cues were
altered outside the species-typical range, birds
again responded less to altered songs than to
normal songs, but whereas birds responded with
less social vocalizations when presented with
absolute pitch-altered songs, birds responded less
aggressively when presented with relative pitch-
altered songs. Therefore, not only were black-
capped chickadees processing both absolute and
relative pitch information in their songs, but they
were doing so in a way that led to different classes
of behavioral responses depending on the type and
magnitude of frequency deviations.
Based on the results of previous bioacoustic
analyses and playback studies on pitch ratio
perception (discussed above), Shackleton et al.
(1992) investigated a more subtle pitch change in
the chickadee song, the small but reliable pitch
change of about 200 Hz over their approximately
400 ms duration of the fee note, the glissando
(Fig. 10.1). Testing whether the glissando was either

perceptible or meaningful to the birds in species
recognition poses a slight methodological chal-
lenge. This must be done by creating or finding a fee
note with little or no pitch change over the course
of the note. This problem was overcome through
the use of synthetic songs of three varieties. Normal
songs had a typical pitch change from the start to
the end of the fee (i.e. a glissando) and from the end
of the fee to the start of the bee. The alternative
songs were of two types: one started and ended
on the same pitch as normal fee notes started, with
no pitch change across the note (i.e. no glissando)
while the other type started on the pitch of the end
of normal fee notes, also with no pitch change
across the note. The result was not only a compari-
son of the effect of pitch changes in the fee note, but
was also a test of the consequence of the manipula-
tions. The pitch ratio between the two notes was
also tested, with the first alternative song having
a larger than normal ratio and the second having a
normal ratio.
Altering the pitch ratio of the fee note had a
significant effect on the birds behavior. Birds were
significantly less likely to approach the speaker or
to emit vocalizations upon hearing either of the two
altered versions of song. Therefore, even subtle
deviations in the relative pitch structure of chicka-
dee song had serious implications for behavioral
responses. The question that then arose from this
work was what role in particular did this small but
reliable pitch drop in the fee note play in species
recognition? One possibility was that this was used
as a cue for distance estimation, as the higher
frequencies at the start of the fee note would be
expected to degrade more rapidly over distance
than the lower pitched remainder of the note. Thus,
the pitch change would conceivably become muted
at longer distances, an idea that was tested directly
by Fotheringham and Ratcliffe (1995).
Fotheringham and Ratcliffe (1995) conducted a
two-part field study that included both a transmis-
sion/recording component and a playback compo-
nent. Black-capped chickadee songs were broadcast
in both open and forested environments and then
re-recorded at a number of distances. Various
acoustic measures were then taken to estimate the
effect that propagation over distance had on song
features. Specifically, they were investigating
VOCAL PRODUCTION AND PERCEPTION 157
whether the initial portion of the fee note would be
differentially degraded compared with the rest of
the fee note. If this were the case, the behavioral
responses observed by Shackleton et al. could be
accounted for by distance estimation. If not, the
conclusion was likely that birds used the pitch ratio
in the fee note as a species marker. Bioacoustic
analyses, combined with playback results indicat-
ing that chickadees did not respond differentially to
degraded and non-degraded songs when equalized
for playback amplitude, were unequivocal; the
glissando in the fee note appears to serve, as does
the pitch ratio between the fee end and bee start, as
a species marker in black-capped chickadee songs.
In addition to the pitch change in the fee note and
the pitch ratio between fee and bee notes being
species markers, more recent research has indicated
a number of other key findings with respect to
other aspects of signaling. First, not only are the
fine acoustic features in song relatively unaffected
by distance (Christie et al. 2004a), as was seen for
the glissando, but there are individually identifi-
able features within the song that remain even after
degradation over distance. Moreover, the ability of
a particular male to produce a reliable pitch ratio is
related to male quality, and can be used by females
to choose a high quality mate (Christie et al. 2004b).
10.2.2.2 Operant conditioning experiments of
song perception
While field studies are essential to understanding
the puzzle that is chickadee communication, they
can not ask or answer all research questions.
Furthermore, it is not always feasible or even
possible to test some hypotheses through the use of
field experimentation. For example examining
details of the fundamental perceptual grouping
mechanisms underlying song perception
and species-recognition, or the comparative percep-
tion of signals by birds raised under different
developmental conditions, are best conducted via
laboratory-based, operant conditioning techniques.
Results of playback studies indicated that
chickadees were attentive to both absolute and
relative pitch cues in their songs, but the types of
responses to these cues varied. To assess song
perception on a more detailed and controlled level,
Weary and Weisman (1991) conducted an operant
158 V O C A L C O M M U N I C AT I O N
discrimination experiment to determine the role
of relative pitch cues in the discrimination and
generalization of chickadee song.
In the first of two experiments, stimulus songs
were constructed from a sample of natural songs.
Positive, or food-rewarded songs, were those that
had a near-normal pitch ratio of 1.12. Negative, or
non-food-rewarded songs, were those with a larger
or smaller than normal pitch ratio. Once training
was complete and male chickadees showed signifi-
cant learning and steady-state discrimination
performance, they were tested with novel songs.
These songs were composed in the same manner as
training songs, with some having normal and
others having abnormal intervals. Surprisingly,
birds did not transfer their training neatly to those
novel songs with normal pitch ratios. Instead, there
appeared to be a strong absolute pitch component
to the discrimination, with birds allocating more
responses to test songs that had similar starting
pitches to rewarded training songs. The fact that
birds attended to absolute pitch in their songs was
not entirely surprising, as previous studies had
shown that it did indeed have a role in song
perception. What was surprising was that birds
attended to this cue even when they were explicitly
trained to attend to relative pitch. A follow-up
experiment was carried out that, instead of using
natural songs as discriminative stimuli, used
wholly synthetic songs. The results of this study
were more in line with expectationsbirds did in
fact attend to relative pitch cues, but there was still
a strong influence of absolute pitch in their results.
Because of the influence of absolute pitch cues in
the perception of relative pitch cues seen in Weary
and Weismans work with natural or synthetic
songs, Njegovan and Weisman (1997) adopted a
different approach to further understanding the
mechanisms of song perception. For their design,
Njegovan and Weisman used as their stimuli-of-
choice pure sine wave pairs that approximated the
acoustic parameters of normal songs. In common
with Weary and Weisman, Njegovan and Weisman
trained birds to discriminate between rewarded
tone pairs with a frequency ratio equal to that seen
in the wild (a ratio of 1.12) and non-rewarded tone
pairs with one of two ratios not seen in nature
(ratios of 1.00 and 1.24). Njegovan and Weisman
went further stillif birds were actually using the
pitch ratio as a mechanism of determining whether
a song is produced by a black-capped chickadee or
not, then it stands to reason that this task should be
accomplished quickly. One way that this could be
done is if birds treated pitch relations between
notes as perceptual categories. To determine
whether this was indeed the case, Njegovan and
Weisman used a pseudo category discrimination
where rewarded stimuli were selected at random
and had no common pitch relationships (i.e. the
rewarded stimuli were not united by a common
1.12 frequency ratio). In this way they could
determine whether birds were treating pitch ratios
as perceptual categories. If they were, the true
category discrimination would be performed much
more rapidly. If not, there would be no difference
between the two discriminations.
Njegovan and Weisman also tested black-capped
chickadees that had been hand-reared in the
absence of song stimuli on this discrimination.
Since at least the 1950s and the pioneering work of
Thorpe and Marler (e.g. Thorpe 1958; Marler, 1970),
it had been clear that young songbirds needed to
hear an adult conspecific if they were to develop
normal song. This has been shown in a variety of
species, including black-capped chickadees
(Shackleton and Ratcliffe 1993). One of the main
failures in hand-reared black-capped chickadee
song is the lack of normal relative pitch cues seen
reliably in the songs of normal, wild-caught birds.
The logic, therefore, for including hand-reared
birds in the frequency ratio discrimination was sim-
ple: birds that had not learned to produce or been
exposed to normal relative pitch cues in song may
be at a perceptual disadvantage when asked to per-
form a discrimination that is based on this feature.
The results of Njegovan and Weisman were clear
cut. Normal birds learned the true category dis-
crimination, that is the discrimination where all
normal tone pairs were rewarded, much more
quickly than the pseudo-category discrimination,
where rewarded tone pairs were selected at ran-
dom. The implication is that birds can use percep-
tual grouping mechanisms to quickly ascertain
whether a particular tone pair matches a particular
relative frequency ratio and then act accordingly. A
further implication, of course, is that they could use
 VOCAL PRODUCTION AND PERCEPTION 159

just such a mechanism in the wild to quickly and
efficiently determine whether a song is produced
by a black-capped chickadee or not.
The second main finding of Njegovan and
Weisman was also very clear. Birds that were hand-
reared in the laboratory, without exposure to nor-
mal song, did not perform nearly as well as
wild-caught birds on the true category discrimin-
ation. In fact, even when given significantly more
training than normal birds, hand-reared chickadees
could not even approximate performance by nor-
mal birds. This finding raised the possibility, which
has been confirmed in other species with other
acoustic discrimination tasks, that songbirds need
exposure to adults during development not only to
learn to produce species-typical song, but also to
perceive song accurately.
10.3 Call production and perception
10.3.1 Call production
Of all chickadee vocalizations, probably their most
well known is the species chick-a-dee call (Fig. 10.2).
This call, especially in black-capped chickadees, has
been exceedingly well studied in a formal sense

(a)
12

A A A A A B D D D D
Frequency (kHz)

0
0 1.0 2.0
Time (sec)

(b)
12
B B C C D D D D D D
Frequency (kHz)

0
0 1.0 2.0
Time (sec)

Figure 10.2 Two representative chick-a-dee calls with note types AAAAABDDDD (a) and BBCCDDDDDD (b). Spectrogram settings: Hanning
window, 512 points. Time (sec) is on the x axis and frequency (kHz) is on the y axis in both spectrograms.
160 V O C A L C O M M U N I C AT I O N
since about the early to mid 1970s. A description of
the call and its usage by Ficken et al. (1978) still
stands as a benchmark study. As they and others
have noted (e.g. Odum 1942; Saunders 1951), the
call is produced all year by both sexes and is com-
posed of four note types; A, B, C, and D. It is used
as a social signal to co-ordinate flock movements
and to indicate mild alarm. Recently it has been fur-
ther demonstrated that the note type composition,
specifically the number of D notes, of this call
varies depending on the degree of perceived threat
(Templeton et al. 2005).
During the winter months, chickadees form
flocks of between four and 12 birds that defend a
group foraging territory. One question that arose
from early observational work was by what mech-
anism did birds recognize the calls of their flock-
mates? Classic work by Mammen and Nowicki
(1981) investigated this issue by conducting an
acoustic analysis of the chick-a-dee call from free-
ranging flocks, and comparing these measures
among flocks. The results of this initial analysis
demonstrated that one of the mechanisms whereby
birds were able to recognize flock-mates was
through flock-specific convergence of their chick-a-
dee calls, specifically via a convergence of D note
acoustics. Mammen and Nowicki then captured
these wild flocks and formed ad hoc artificial flocks
in aviaries. After 1 month, call convergence was
observed on the same acoustic features posited to
control flock recognition from the field analyses.
These initial observational and experimental
studies of call convergence were completed by a
final study from Nowicki (1989), who examined in
detail both the nature and speed with which these
acoustic changes occurred in wholly artificial
flocks. This final study allowed for analysis of the
precise acoustic featuresnamely the first and sec-
ond frequency components in D notes, and, to a
lesser degree, the total frequency bandwidth of
D notesthat control flock identity. Moreover,
Nowicki showed that no one bird controlled the
convergence and that the pattern of convergence
observed was not determined by dominance rela-
tionships (i.e. the flock did not converge on the
acoustic structure of the dominant bird). Rather,
birds modify the acoustic properties of their
D notes to converge on a common mean and did so
within about 1 week. Taken together, these results
gave insight into the mechanisms of call production
and a possible acoustic basis of flock recognition.
Several studies of chick-a-dee call production con-
ducted by Jack Hailman and colleagues (e.g. 1985,
1986, 1987) have lead to an amazing understanding
of other aspects of this ubiquitous call, that is the
call variety, call syntax, and call note-type compos-
ition. One early finding was that the note types of
which the call is composed seem to form a graded
continuum, from A B C D, with As gradually
becoming Bs and so on. Hailman and others also
demonstrated that the call follows strict syntactical
rules, with A notes always preceding B notes,
always preceding C notes, always preceding
D notes. This set of syntactical rules, combined with
the fact that the variety of call types produced is
seemingly endless, makes the chickadee call system
one of the most complicated non-human animal
signaling systems ever described. In fact, Hailman
and others also proposed that the calls meaning
could vary with the note-type composition and the
context in which it is used.
Other more recent bioacoustic and playback
studies, many of which are discussed in Chapter 13,
tested these assumptions derived from research on
black-capped chickadees directly in Carolina
chickadees and have shown that Carolina chicka-
dees do respond differentially depending on
note-type composition of calls. These findings,
combined with those of Nowicki and Mammen dis-
cussed above, along with the more recent findings
of Templeton et al. (2005), clearly point to the fact
that this is a sophisticated call system that we are
still trying to fully understand. That said, in order
for any of the research on call note composition etc.
to be reliable, one must be able to confidently
assign the notes produced in this call into types or
classes. This problem of defining natural categories
has been around for as long as acoustic signals have
been studied scientifically, and has been the topic of
much debate (see Marler, 1982 and Hauser, 1996 for
extensive discussions of this problem). It is to this
area, with specific reference to the chick-a-dee call
that we now turn.
One of the first steps in analyzing any vocaliza-
tion is reducing the chaos that naturally occurs in
biological signals into workable units. This

reductionism requires sorting large numbers of
events into a few manageable types. For the black-
capped chickadee call this was relatively straight
forward. Ficken et al. (1978) labeled four obvious
notes types, based on their distinct acoustic
structures, A through D.
Nowicki and Nelson (1990) revisited the note-
type classification in the chickadee call by contrast-
ing several classification methods in an attempt
to determine the reliability, and to some degree
the validity, of this classification scheme.
Multidimensional scaling, k-means cluster analysis
and visual classification techniques lead to reliable
and converging classifications. Recent work from
our laboratory (Dawson et al. 2006) has found simi-
lar results using both artificial neural networks and
linear discriminant analyses. An open question that
numerous researchers, including Hailman and
Nowicki and Nelson, have pointed out is that such
human-based classifications need to be verified by
the animals that produce the vocalizations being
classified. Just such studies are described in the
following section on call perception.
Charrier et al. (2004) set out to conduct a similar
analysis of the chick-a-dee call of the black-capped
chickadee with three main goals. The first goal was
to provide a detailed acoustical account of the call
and its note types. The second goal was to deter-
mine which features, in which note types, had
potential individual markers. The third goal was to
determine the acoustic features that were respon-
sible for distinguishing among the various note
types.
When Charrier et al. (2004) analyzed the call
notes for individualized features, several of the
acoustic features had the potential to identify indi-
vidual birds. That is, the between-bird variability
on several features was larger than the within-bird
variability, making it theoretically possible for birds
to identify individuals on the basis of these acoustic
features. Of the four note types, C notes had the
greatest potential for individual identity; support
for the special status of C notes was observed by
Freeberg and Lucas (2002) who demonstrated
clearly that Carolina chickadees responded differ-
entially to calls with or without C notes.
Interestingly, when the features that could be
used for note-type identification were examined,
VOCAL PRODUCTION AND PERCEPTION 161
some clear winners emerged. Specifically, starting
frequency and the ascending frequency modulation
of notes was found to be the most distinctive
among all note types, and therefore likely to play an
important role in note-type discrimination and
classification. Just how much of a role would be
determined in an operant discrimination task, as
described in the following section.
10.3.2 Call perception
As well as a significant body of work on call
production, there is a growing understanding of
call perception, both from playback studies
and operant conditioning experiments. Playback
experiments have been aimed at a variety of issues,
including identification of species and flock
through the chickadee call. Operant conditioning
experiments have been aimed at related topics of
inquiry including species classification and dis-
crimination of different species chick-a-dee calls,
note-type categorization, and the mechanisms of
note-type discrimination. We will deal with
research from field playback designs first, followed
by research from operant conditioning designs.
10.3.2.1 Playback studies of call perception
Acoustic analyses of field and laboratory recordings
(Mammen and Nowicki 1981; Nowicki 1989, dis-
cussed above) discovered acoustic features that
could potentially identify flocks on the basis of their
chick-a-dee calls. In an experimental test of flock
identification, Nowicki (1983) examined whether
birds discriminate their own flocks calls from those
of others, and also whether they respond aggres-
sively to non-flock-mates calls. To investigate these
questions, Nowicki broadcast resident and foreign
flocks calls to resident chickadee flocks while they
were foraging. The results were unambiguous;
when chickadees heard playbacks of their own
flocks chick-a-dee calls, they continued to forage and
did not engage in any calling behavior above base-
line levels. Alternatively, playbacks of foreign calls
led to significant decreases in foraging behavior and
significant increases in chickadee calling. This study
provides the functional basis for call convergence
and clearly demonstrates that chickadees are not only
attending to the macroacoustical characteristics
162 V O C A L C O M M U N I C AT I O N
in their calls, but also the microacoustical
characteristics.
While the studies of Nowicki and Mammen
described above clearly showed how chickadees
react to a foreign flocks calls, an unresolved ques-
tion remained: what is a chick-a-dee call? Put
another way, what particular acoustic features are
chickadees attending to that allow them to identify
the call as species specific? As obvious as this ques-
tion seemingly is, it had not been tackled until
recently (Charrier and Sturdy 2005). In contrast to
the fee-bee song that was more easily paramatized
and the putative relevant features identified and
tested, the chick-a-dee call is highly complex with
multiple parameters that may function in or aid
species recognition. Based on a detailed bioacoustic
analysis already described (Charrier et al. 2004),
Charrier and Sturdy set out to test the limits of
species recognition via chick-a-dee calls using a field
playback design.
To accomplish this, several stimuli were con-
structed, including broadband noise signals, pitch
shifted calls, and calls in which the tempo had been
increased or decreased. Several signals were
responded to significantly less compared to normal
chickadee calls, including the negative control gray-
crowned rosy-finch (Leucosticte tephrocotis) calls, syn-
thetic stimuli, and manipulated natural calls, white
noise calls, calls that were delivered at a slower
tempo than normal, calls that were time reversed, as
well as those in which the typical syntax was
reversed. Moreover, in common with research con-
ducted on song, birds also responded less vigorously
to chick-a-dee calls that were shifted up and down in
frequency. Interestingly, the responsiveness to fre-
quency-shifted calls was not symmetrical, with those
shifted up by either 500 Hz or 1000 Hz or shifted
down by 500 Hz not treated differently than normal
calls, whereas or those shifted down by 1000 Hz
were treated as different from normal calls. Another
unexpected finding was that calls in which the
amplitude modulation was removed elicited less
response than normal calls, suggesting that in con-
trast to many other species tested, amplitude modu-
lation may play a role in species recognition in
black-capped chickadees. Taken together, the
acoustic properties that appear to control species
recognition in chickadee calls appear in many ways
to parallel those documented for species recognition
via song, with some important caveats that will be
the subject of future research.
10.3.2.2 Operant conditioning studies of call
perception
While research on call perception in the field has
dealt mainly with large-scale issues of flock and
species recognition, research in the laboratory has
the ability and control to study finer-scale issues of
the mechanisms of call perception (but see Clucas
et al. 2004 and Chapter 13 for a recent change in this
trend). In particular, one of the outstanding issues
in the area of chickadee call perception is the
classification of call notes into types. Typically, the
classification is done by humans and is based
either on visual sorting of sound spectrograms or
analyses of note features taken from sound
spectrogram measurements. However, whether the
birds that produce these calls perceive the same
note types as humans and statistical techniques
needs to be verified by testing the birds that
produce the vocalizations that are classified.
To begin to answer this question, Sturdy et al.
(2000) trained black-capped chickadees to discrimin-
ate among their call-note categories in an operant
discrimination task. The goals of this task were
twofold. The first goal was to determine whether
the birds perceived the note-type categories of
bioacousticians as such. The second related goal
was to determine the mechanism behind call-note
perception. Earlier work (Sturdy et al. 1999a), also
using operant conditioning techniques, found that
zebra finches (Taeniopygia guttata) perception of
their song notes agreed with human-based classifi-
cation methods of these notes (Sturdy et al. 1999b).
It also showed, through the use of transfer tests,
that zebra finches perceived their song notes as
natural, open-ended categories. This suggested that
songbirds use this fundamental perceptual mecha-
nism of treating similar but discriminable auditory
objects as classes, to perceive the building blocks of
their vocalizations.
Black-capped chickadees agree with human
classification and use open-ended categorization to
perceive their call-note types. Birds learned to
discriminate among the four call-note types, and
along the way, provided clues to support the

open-ended categorization hypothesis. First, birds
were slower to learn the within-category discrimin-
ation than the between-category discrimination.
This provides clear evidence that note types within
a class (defined by humans) were more similar than
those among classes. Second, birds showed strong
transfer of inhibition (i.e. generalization) from
unrewarded, between-category note types used in
discrimination training to novel notes from these
same note categories during reversal training; this
in spite of the fact that these note types were now
rewarded (i.e. the contingencies were reversed
relative to during discrimination training). Finally,
when birds were exposed to previously unre-
warded notes following a period of retraining with
rewarded notes from those same classes, they based
their responding on the contingencies most recently
in effect. This last evidence provided the strongest
test of transfer of training and, taken together, these
results suggested that birds did agree with human
sorters and used open-ended categorization as a
perceptual mechanism to perceive their note types.
Interestingly, an analysis of errors lent support
for an earlier observation of Hailman (Hailman
et al. 1985); he suggested that chickadee call-note
types formed a continuum from A D notes, with
each note type grading into the next. By inspect-
ing how birds responded to non-rewarded notes,
Sturdy et al. (2000) were able to show that in fact
birds were more likely to confuse adjacent note
types (e.g. A with B) than they were non-adjacent
note types (e.g. A with C). But how was this
accomplished? What features were birds using to
discriminate among their call-note types?
Bioacoustic analyses by Charrier et al. (2004) iden-
tified some acoustic features, namely that start fre-
quency and the initial ascending portion of notes,
that are more variable between note types than
within note types and are therefore likely to con-
tribute to note-type discrimination and classifica-
tion. To determine the extent to which these features
were in play, Charrier et al. (2005) trained birds to
discriminate adjacent note types (e.g. A+/B-, A-/B+;
see Fig. 10.2 for example note types) and then tested
them with novel, altered notes. Test stimuli
consisted of notes that were linearly shifted either
up or down in pitch by 0.5 SD steps, or cut notes,
with only the first or the second half presented. The
VOCAL PRODUCTION AND PERCEPTION 163
results of the test sessions were striking. Birds
altered their response based on the pitch of the note;
when A notes were reduced in pitch and therefore
made more B-note like, birds responded to them as
if they were B notes, and vice versa for B notes
shifted up in pitch to be made more A-note like. The
same was true for B versus C notes. Furthermore,
birds could generally maintain their discrimination
using only the ascending portion of the note
whereas the descending portion of the notes was
not sufficient to maintain discrimination perform-
ance. Whether, and to what extent, other acoustic
features in call notes control discrimination and
categorization remains to be determined. The
results from Charrier et al. (2005), however, showed
a role for frequency and initial frequency modu-
lation in note perception and provide another
example of how a solid understanding of a signal
can drive research into the perception of the same.
While laboratory studies are ideal for studying
fine-grained problems of vocal perception, more
holistic questions can also be dealt with quite effect-
ively. In a series of two operant conditioning
experiments, Bloomfield et al. (2003) and L. L.
Bloomfield and C. B. Sturdy (unpublished data),
extended the initial findings of Sturdy et al. (2000)
for open-ended classification of call-note types to
species classification of chick-a-dee calls. Specifically,
Bloomfield and colleagues trained chickadees
(black-capped only, 2003; black-capped and
mountain chickadees, unpublished data) to dis-
criminate and classify both their own and other
species chick-a-dee calls to determine: first, to what
degree birds could perform the task with their own
and other species calls; and second, whether birds
treated these higher-level species categories in an
open-ended way as they did for lower-level
note-type categories. Results of these studies
paralleled those of Sturdy et al. (2000), with clear
evidence through transfer and propagation tests
that chickadees classified species based on their
chick-a-dee call. Taken together, the results of both
the low-level note-type classification and the high-
level species classification tasks point to a general
perceptual mechanism driving discrimination and
classification, much in the same way as relative
pitch perception drove song perception as
described earlier in this chapter.
164 V O C A L C O M M U N I C AT I O N
10.4 Summary and future directions
Our understanding of vocal communication in the
North American chickadees has continued to grow
over the last 35 plus years, with more research
being added each year. This has greatly increased
our knowledge not only of how chickadees use
acoustic communication, but has also provided
more general insights into communication in song-
birds and in other animal group as well. One of the
reasons, we believe, for the success that this field
has seen is due in large part to the reliance on com-
plimentary and integrative studies of vocal produc-
tion and perception using a variety of techniques in
the field and in the laboratory. Much has been
learned about chickadee production and percep-
tion, and, importantly, the growth of this know-
ledge has occurred in tandem. That is, production
research has been followed with research aimed at
understanding the perception of features eluci-
dated in the studies on production.
This general approach has also been profitable in
the understanding of one of the chickadees
European relatives, the great tit. Weary and
McGregor and colleagues (Falls et al. 1982;
McGregor and Avery 1986; Weary et al. 1990; Weary
and Krebs 1992; Weary 1989, 1990, 1991), in a series
of studies of song production and perception, have
produced similar insights as those described above
for the vocalizations of the black-capped chickadee.
For example, in common with the results of
Charrier et al. (2005) for note-type perception in
black-capped chickadees, Weary (1990), also using
an operant conditioning task, found that great tits
relied mainly on note frequency, and far less on
other acoustic parameters, when classifying their
note types. Also in common with findings for the
individualization of black-capped chickadee fee-bee
song and chick-a-dee calls (Christie et al. 2004a;
Weisman et al. 1990; Charrier et al. 2004), great tits
produce individualized songs, accomplished in
part via the production of individual-specific song
types (Weary et al. 1990). In addition, great tit songs
contain cues to individual recognition, and great
tits can use the individual voice characteristics
contained in their songs to recognize individuals
(Weary and Krebs 1992). This suggests that great
tits can form an open-ended category for each
individual male into which novel songs can be
assigned, highly similar to that observed by
Phillmore et al. (2002) for black-capped chickadees.
Although the studies just described provide won-
derful complementary evidence to those conducted
on North American chickadees, there are many tit
species that remain to be explored and tested if we
are to come to a more extensive comparative under-
standing of Parid communication in general. This is
not only true of tits, but it is also relevant in North
America, where the majority of studies have
focused on chickadee species and largely ignored
titmice, leaving a further void in our understand-
ing. Further research into vocal production and
perception for chickadees, tits and titmice is sure to
add even more to our understanding of Parid
communication and perception.
Acknowledgements
CBS was supported by an NSERC Discovery Grant,
an Alberta Ingenuity New Faculty Grant, a Canada
Foundation for Innovation New Opportunities
Grant, and the University of Alberta through start-
up funding and CFI partner funding. LLB was sup-
ported by an NSERC PGS-B Scholarship, an Alberta
Ingenuity Fund Studentship, and a Walter Johns
Scholarship from the University of Alberta. IC was
supported by a Killam Postdoctoral Fellowship and
an Alberta Ingenuity Fund Fellowship. TTYL was
supported by a Province of Alberta Graduate
Scholarship.
The authors dedicate this chapter to Ron
Weisman: mentor, collaborator, and friend.
References
Bloomfield, L. L., Sturdy, C. B., Phillmore, L. S., and
Weisman, R. G. (2003). Open-ended categorization of
chick-a-dee calls by black-capped chickadees (Poecile atr-
icapilla). Journal of Comparative Psychology, 117, 290301.
Catchpole, C. K. and Slater, P. J. B. (1995). Bird Song:
Biological Themes and Variations. Cambridge University
Press, Cambridge, UK.
Charrier, I. and Sturdy, C. B. (2005). Call-based species-
recognition in Black-capped chickadees. Behavioral
Processes, 70, 271281.
Charrier, I., Bloomfield, L. L., and Sturdy, C. B. (2004).
Note types and coding in parid vocalizations. I: The

chick-a-dee call of the black-capped chickadee (Poecile
atricapillus). Canadian Journal of Zoology, 82, 769779.
Charrier, I., Lee, T.-Y., Bloomfield, L. L., and Sturdy, C. B.
(2005). Acoustic mechanisms of note-type perception in
Black-capped chickadees. Journal of Comparative
Psychology, 119, 371380.
Christie, P. J., Mennill, D. J., and Ratcliffe, L. M. (2004a).
Chickadee song structure is individually distinctive
over long broadcast distances. Behavior, 141, 101124.
Christie, P. J., Mennill, D. J., and Ratcliffe, L. M. (2004b).
Pitch shifts and song structure indicate male quality in
the dawn chorus of black-capped chickadees. Behavioral
Ecology and Sociobiology, 55, 341348.
Clucas, B. A., Freeberg, T. M., and Lucas, J. R. (2004).
Chick-a-dee call syntax, social context, and season affect
vocal responses of Carolina chickadees (Poecile
carolinensis). Behavioral Ecology and Sociobiology, 57,
187196.
Dawson, M. R. W., Charrier, I., and Sturdy, C. B. (2006).
Using an artificial neural network to classify note types
in the chick-a-dee call of the black-capped chickadee
(Poecile atricapillus). Journal of the Acoustical Society of
America, 119, 31613172.
Dwight, J. (1897). The whistled call of Parus atricapillus
common to both sexes. Auk, 14, 99.
Falls, J. B., Krebs, J. R., and McGregor, P. K. (1982). Song
matching in the great tit (Parus major): the effect of sim-
ilarity and familiarity. Animal Behaviour, 30, 9971009.
Ficken, M. S. (1981). What is the song of the black-capped
chickadee? Condor, 83, 384386.
Ficken, M. S., Ficken, R. W., and Witkin, S. R. (1978). Vocal
repertoire of the black-capped chickadee. Auk, 95,
3448.
Fotheringham, J. R. and Ratcliffe, L. (1995). Song degrad-
ation and estimation of acoustic distance in black-
capped chickadees (Parus atricapillus). Canadian Journal
of Zoology, 73, 858868.
Freeberg, T. M. and Lucas, J. R. (2002). Receivers respond
differently to chick-a-dee calls varying in note compos-
ition in Carolina chickadees (Poecile carolinensis). Animal
Behaviour, 63, 837845.
Hailman, J. P. and Ficken, M. S. (1986). Combinatorial ani-
mal communication with computable syntax: chick-a-dee
calling qualifies as language by structural linguists.
Animal Behaviour, 34, 18991901.
Hailman, J. P., Ficken, M. S., and Ficken, R. W. (1985). The
chick-a-dee calls of Parus atricapillus: A recombinant sys-
tem of animal communication compared with written
English. Semiotica, 56, 191224.
Hailman, J. P., Ficken, M. S., and Ficken, R. W. (1987).
Constraints on the structure of combinatorial chick-a-
dee calls. Ethology, 75, 6280.
VOCAL PRODUCTION AND PERCEPTION 165
Hauser, M. D. (1996). The Evolution of Communication. MIT
Press, MA.
Mammen, D. L. and Nowicki, S. (1981). Individual differ-
ences and within-flock convergence in chickadee calls.
Behavioral Ecology and Sociobiology, 9, 179186.
Marler, P. R. (1970). A comparative approach to vocal
learning: song development in white-crowned spar-
rows. Journal of Comparative Physiological Psychology
Monographs, 71, 125.
Marler, P. R. (1982). Avian and primate communication:
The problem of natural categories. Neuroscience and
Biobehavioral Reviews, 6, 8794.
Maynard-Smith, J. and Harper, D. (2003). Animal Signals.
Oxford University Press, NY.
McGregor, P. K. and Avery, M. I. (1986). The unsung songs
of great tits (Parus major): Learning neighbours songs
for discrimination. Behavioral Ecology and Sociobiology,
18, 311316.
Njegovan, M. and Weisman, R. G. (1997). Pitch discrim-
ination in field- and isolation-reared black-capped
chickadees (Parus atricapillus). Journal of Comparative
Psychology, 111, 294301.
Nowicki, S. (1983). Flock-specific recognition of chickadee
calls. Behavioural Ecology and Sociobiology, 12, 317320.
Nowicki, S. (1989). Vocal plasticity in captive black-
capped chickadees: the acoustic basis and rate of call
convergence. Animal Behaviour, 37, 6473.
Nowicki, S. and Nelson, D. A. (1990). Defining natural cat-
egories in acoustic signals: comparison of three meth-
ods applied to chick-a-dee call notes. Ethology, 86,
89101.
Odum, E. P. (1942). Annual cycle of the black-capped
chickadee-3. Auk, 59, 499531.
Phillmore, L. S., Sturdy, C. B., Turyk, M. R., and Weisman,
R. G. (2002). Discrimination of individual vocalizations
by black-capped chickadees (Poecile atricapilla). Animal
Learning and Behaviour, 30, 4352.
Ratcliffe, L. and Weisman, R. G. (1985). Frequency shift in
the fee-bee song of the black-capped chickadee. Condor,
87, 555556.
Ratcliffe, L. and Weisman, R.G. (1986). Song sequence
discrimination in the black-capped chickadee (Parus
atricapillus). Journal of Comparative Psychology, 100,
361367.
Ratcliffe, L. and Weisman, R. G. (1988). Representation of
conspecific song by chickadees: comparisons among
embedded fee-bees. Behavioural Processes, 17, 199203.
Saunders, A. A. (1951). A Guide to Bird Songs. Country Life
Press, NY.
Shackleton, S. A. and Ratcliffe, L. (1993). Development of
song in hand-reared black-capped chickadees. Wilson
Bulletin, 105, 637644.
166 V O C A L C O M M U N I C AT I O N
Shackleton, S. A., Ratcliffe, L., and Weary, D. M. (1992).
Relative frequency parameters and song recognition in
black-capped chickadees. Condor, 94, 782785.
Sturdy, C. B, Phillmore, L. S., Price, J. L., and Weisman,
R. G. (1999a). Song-note discrimination in zebra finches
(Taeniopygia guttata): Categories and pseudocategories.
Journal of Comparative Psychology, 113, 204212.
Sturdy, C. B., Phillmore, L. S., and Weisman, R. G. (1999b).
Note types, harmonic structure, and note order in the
songs of zebra finches (Taeniopygia guttata). Journal of
Comparative Psychology, 113, 194203.
Sturdy, C. B., Phillmore, L. S., and Weisman, R. G. (2000).
Call-note discriminations in black-capped chickadees
(Poecile atricapillus). Journal of Comparative Psychology,
114, 357364.
Templeton, C. N., Green, E., and Davis, K. (2005).
Allometry of alarm calls: black-capped chickadees
encode information about predator size. Science, 308,
19341937.
Thorpe, W. H. (1958). The learning of song patterns by
birds, with special reference to the song of the Chaffinch
Fringilla coelebs. Ibis, 100, 535570.
Weary, D. M. (1989). Categorical perception of bird
song: how do great tits (Parus major) perceive temporal
variation in their song? Journal of Comparative
Psychology, 103, 320325.
Weary, D. M. (1990). Categorization of song notes in great
tits: which acoustic features are used and why? Animal
Behaviour, 39, 450457.
Weary, D. M. (1991). How great tits use song-note and
whole-song features to categorize their songs. Auk, 108,
187190.
Weary, D. M. and Krebs, J. R. (1992). Great tits classify
songs by individual voice characteristics. Animal
Behaviour 43, 283287.
Weary, D. M. and Weisman, R. G. (1991). Operant dis-
crimination of frequency and frequency ratio in the
black-capped chickadee (Parus atricapillus). Journal of
Comparative Psychology, 108, 253259.
Weary, D. M., Norris, K. J., and Falls, J. B. (1990). Song fea-
tures birds use to identify individuals. Auk, 107, 623625.
Weisman, R., Ratcliffe, L., Johnsrude, I., and Hurly, T. A.
(1990). Absolute and relative pitch production in the
song of the black-capped chickadee. Condor, 92,
118124.
Weisman, R. G. and Ratcliffe, L. (1989). Absolute and
relative pitch processing in black-capped chickadees,
Parus atricapillus. Animal Behaviour, 38, 685692.
 CHAPTER 11
The gargle call of black-capped
chickadees: ontogeny, acoustic
structure, population patterns,
function, and processes leading
to sharing of call characteristics
Myron C. Baker and David E. Gammon
11.1 Introduction
In this chapter, we summarize investigations of a
common vocalization in the repertoire of the black-
capped chickadee. This vocalization, known as the
gargle call (Ficken et al. 1978; called the dominance
note by Odum 1942) has an ontogeny that is
dependent upon learning events occurring from
early life through adulthood. As is the case for the
territorial songs of a great many species of song-
birds (Marler 1997), social interactions most likely
play a significant role in gargle call ontogeny. Thus,
these calls evidently result from socially biased
individual learning (Galef 1996), which we will
simply term social learning in this chapter.
Although vocal plasticity tends to decrease during
ontogeny, the continuing effect of social learning is
that members of a local population often come to
share, in considerable detail, the acoustic character-
istics of their gargle signals. Such convergence of sig-
nal properties in populations results in geographic
or microgeographic variation, or dialects
(Mundinger 1982). Whereas such differences in
vocal patterns from one geographic locale to
another are relatively easy to describe, uncovering
the social and developmental processes that gener-
ate and maintain local convergence and geographic
differences is more difficult. An even more tren-
chant problem is to determine how the sharing of
vocal characters in a local population benefits indi-
viduals (i.e. is adaptive) in their social behavior.
Although potential explanations for the advantages
of sharing vocal signals within populations have
been treated for territorial songs in a general way
(Catchpole and Slater 1995), and considered in
depth for songs of particular species (e.g. Searcy
and Nowicki 1999), few studies have examined non-
song calls in this regard (but see Nowicki 1983).
The gargle call together with the chick-a-dee call
and the fee-bee song constitute the great majority of
loud chickadee vocal signals one normally encoun-
ters in the field, and they are referred to as the
major vocalizations of the species (Hailman 1989).
These and other vocalizations in the repertoires of
species in the family Paridae, including Poecile, have
previously been examined from a comparative
standpoint (Hailman 1989; Hailman and Ficken
1996), and similarities and homologies across
species have been well described. Hailman (1989),
in particular, provides a comprehensive treatment
of the form and structures of the vocal signal rep-
ertoires of a number of members of the Paridae.
In examining the gargle call, we give a brief
description of the call, provide information on the
ontogeny of the call as it occurs in natural popula-
tions, describe the fundamental features of the call,
the nature and extent of sharing of calls by birds in
a local area, and the similarities and changes in calls
167
168 V O C A L C O M M U N I C AT I O N
across years. Additionally, we report observational
and experimental evidence on the roles of the calls
in the social lives of the birds, and draw inferences
about the ways social behavior selects for vocal
convergence among birds in a local area, and the
possible functional significance of convergence.
11.2 The gargle
11.2.1 Brief description of the call
The gargle call (Fig. 11.1a) was named in early
descriptions of the vocal repertoire of the black-
capped chickadee because of its noisy complexity
(Ficken et al. 1978). Given primarily by males, a call
lasts about half a second and consists of several
distinct syllables. An individual may have a reper-
toire of three to 18 different gargle call types
(mean 78; Baker et al. 2000; Box 11.1).
11.2.2 Ontogeny of the call
Studies of color-banded birds revealed that gargle-
like syllables begin to emerge in fledglings around
30 to 35 days of age when the young are still in fam-
ily groups together with parents and siblings
(Baker et al. 2003). The precursor gargle calls are
produced in strings of somewhat amorphous
sounds of low amplitude, with the duration of such
strings lasting up to a minute or more. The common
context for these utterances is while the individual
is perched in one place, and apparently not inter-
acting with another bird. The acoustic structures
produced in these rambling strings of elements are
comparable to vocalizations often referred to as
sub-song in the song learning literature (Marler and
Peters 1982a). We referred previously to these
vocalizations as sub-song (Baker et al. 2003), and
here we denote the gargle-like components of sub-
song as sub-gargles to emphasize their uncrystal-
lized condition. In our first attempt to identify
sub-gargles as matching adult gargle syllables
characteristic of the local breeding area (Baker et al.
2003), we were able to find only one or two juvenile
sub-gargle syllables that were reasonably close
approximations to adult syllables.
Since that first attempt to monitor gargle devel-
opment in young chickadees, we have recorded a
representative set of juvenile sub-gargles at the age
of juvenile dispersal. In this follow-up study, the
juveniles were not color-banded. As studies of
banded birds have shown, family break-up and
dispersal occur suddenly in chickadees, literally
from one day to the next, with the abrupt dis-
appearance of young from a family group and a
corresponding influx of many immigrant juveniles
(Smith 1991). That an immigrant we recorded was a
juvenile and not an adult was evident by the nature
of the vocalization delivery. Juveniles gargle with
low amplitude, recombinant syntax, and lack
frequency control during production of notes, all of
which are rare in adult gargle episodes (Gammon
et al. 2005). For our recordings, a given site was
visited daily or every second day, allowing deter-
mination within one day of the date of natal
dispersal from a family group, as well as allowing
us to recognize the occurrence of juveniles not
found previously at that location. Our recordings
were therefore taken from juveniles in family
groups in the 2 days before juvenile dispersal (fam-
ily group dissolution), and from new juveniles the
first day they were observed at the site.
Examination of sub-gargles from a representative
fledgling still in the family group indicates that
these vocalizations are produced in a variety of
forms but lack the sharply articulated structure of
adult gargle syllables (Fig. 11.1b). Sub-gargles
produced at this predispersal stage of ontogeny not
only are poorly formed in comparison to adult
gargles, but they also lack stereotypy when repeti-
tion is attempted. Sub-gargle syllables are produced
in nearly continuous strings with little evidence
of partitioning into sets of syllables of typical gargle
call duration (Fig. 11.1b). In some recordings,
however, we found sub-gargles delivered in tem-
poral patterns typical of gargle calling in adults
(Fig. 11.1c) even though the constituent sounds
remain amorphous compared to adult gargle
syllables. During sub-song, elements of the vocal
repertoire other than sub-gargles often are included,
elements such as the A-notes of the chick-a-dee
call (Hailman et al. 1985), entire chick-a-dee calls, high
zee notes (Ficken and Witkin 1977), and fee-bee songs
(Ficken et al. 1978; Fig. 11.2ac).
For one set of juvenile sub-gargles, recorded from
four to six individuals while their family groups
 THE GARGLE CALL 169

(a)
10

(b)
10

6
Frequency (kHz)

10

(c)
10

10

1s

Figure 11.1 Gargle calls of black-capped chickadees. (a) Three gargle types from the repertoire of an adult male. We use spectral
derivative displays (upper three panels) to illustrate chickadee sounds described in this report. Spectral derivatives are changes in power across
time and frequency axes of a sound. Visually, these displays are similar to traditional sonograms (lower three panels are sonograms of the
same calls) but often show more detail. More importantly, spectral derivatives are the analysis framework from which are derived, by
automated techniques, a number of acoustic features that we use for quantitative characterization and similarity measurements of sounds
(Tchernichovski et al. 2000). (b) Representative sub-gargle vocalizations recorded from a fledgling while still in the family group prior to
dispersal. (c) Representative sub-gargles recorded in early July from a hatching year individual showing tendency toward temporal
partitioning into clusters of sub-gargle elements.
170 V O C A L C O M M U N I C AT I O N
Box 11.1 Repertoire sizes
Cumulative (saturation) plots of the number of
types of gargle calls versus the number of samples
recorded were used to establish both individual
repertoire sizes and population repertoires.
Individual repertoire size was estimated from
the plateau of the cumulative plot as in this
illustration. For estimates of individual repertoires,
we used birds for which at least 500 calls were
recorded. A population repertoire refers to all
the kinds of gargle calls found in a sample of
birds in a local area. Because of the large extent
of sharing of call types among birds in a local
area, we found that recordings of five to six birds
were usually sufficient to capture all the call types
of the population, as revealed by saturation plots
(examples in Baker et al. 2000). Across three
populations and eight seasons the number of
birds recorded each season in each population
averaged 9.1. One cannot be certain to have
uncovered the entire repertoire of call types
(whether of an individual or a population) despite
a substantial plateau in the cumulative plot.
Apparent saturation in such plots can provide
reasonable confidence in the estimate, but it
remains an estimate nevertheless.
In comparing the repertoire of an individual
across two time periods (e.g. year 1 vs. year 2,
were still together, we also obtained a complete set
of recordings of all adult gargle calls of the same
area. This recording site was one of three popula-
tions that we studied for eight successive seasons,
and we had obtained extensive samples of calls
there (see Box 11.1). Some fledgling syllables were
similar to those of adult birds in the area, but there
were no apparent matches of whole gargle calls. In
the days following family break up, gargle compo-
nents of immigrant young begin to emerge in a
more recognizable form. In one especially well-
recorded individual (Fig. 11.3a), we identified
approximately five different gargle types being
expressed as a repertoire, although the lack of
stereotypy makes the estimate uncertain. This
tendency toward the emergence of recognizable
gargle types suggests a later stage of ontogeny, but
etc.) samples in the second time period may
reveal new call types, or may show that call
types formerly present are not now found.
New call types could be ones that have been
developed during the interim or ones that
were previously in the repertoire but either
unexpressed or used so rarely that they did not
show up in the sample. Similarly, call types that
appear to have been dropped from a repertoire
may have simply been suppressed to a very
low level of use. These caveats apply to any
study of repertoire size.
10
Cumulative no. gargle types
8
6
4
2
0
0 200 400 600 800 1000
Number of calls recorded
it is also apparent that such juveniles have not yet
produced adult-quality gargles.
Our evidence from juvenile sub-gargles,
produced in the few days immediately pre- and
postdispersal, suggests juveniles have developed a
large variety of gargle-like sounds, can produce
them in a temporal pattern approximating that of
adult gargle calling, and express the primitive
gargle calls as a repertoire of call types.
Unfortunately, we lack recordings of known-age
juveniles from late July to early September, an
important period in development. During the
north temperate autumn, the juveniles become
established in a local area to which they may
have emigrated during dispersal. This is the time
when winter flocks are formed, and juveniles
become members of such flocks (Smith 1991). It is
 THE GARGLE CALL 171

(a) 10
Sub-gargle notes

6
High zees

1s

Chick-a-dee call

D-notes
Frequency (kHz)

Introductory notes

(b) 10
Sub-gargle notes B-notes

6 Fee-bee

1s

(c) 10
Sub-gargle & B-notes
6 Fee-bee

1s

Figure 11.2 Sub-song of juvenile black-capped chickadees including: (a) sounds representing sub-gargles, followed by high zee predator
alarm notes grading into a chick-a-dee call with poorly-formed introductory A-, B-, C-notes but well-developed D-notes; (b) sub-gargles followed
by renditions of B-notes and ending with fee-bee song; and (c) sub-gargle notes, B-notes, and fee-bee song.

instructive to compare the quality of juvenile

gargles recorded in mid-September with those
sub-gargles of mid-July (Fig. 11.3b). In those two
months the sub-gargle calls have developed into
well-articulated gargle calls with a high degree
of stereotypy. Measurements of the quality
(Wiener entropy: Tchernichovski et al. 2000) of
these signals show a marked improvement over
those calls recorded at dispersal age (M. C. Baker
and D. E. Gammon, unpublished data). Once the
over-wintering flocks have been formed, the gargle
call repertoires in a local population can be
examined.
11.3 Features of the call and population
patterns
We recorded gargle calls in our three study popula-
tions for eight successive years. All captured individ-
uals were banded. Our sample consists of 215
chickadees (some of these were recaptures, usually in
the season following first capture) from which we
recorded 123 707 gargle calls (average 575 per bird).
Capture, recording methods, spectrographic ana-
lyses, and syllable and gargle classification
procedures are detailed elsewhere (Baker et al. 2000).
Briefly, each captive chickadee was stimulated to
172 V O C A L C O M M U N I C AT I O N

(a) 10
1 2 3 first

10
4 5 3 second

2
Frequency (kHz)

0.5s

(b) 10
1 2 3 first

10
4 5 3 second

Figure 11.3 Juvenile gargle calls. (a) Repertoire of five different gargle calls uttered by an individual soon after natal dispersal (July) and
exhibiting lack of stereotypy (compare first and second attempts of the same gargle type; 26 other calls were uttered before the recurrence of
this similar call). (b) Repertoire of a different individual juvenile 2 months later (September), well after dispersal and establishment in a winter flock
(compare stereotypy of first and second utterances of the same gargle type; 48 other calls were uttered before the recurrence of this similar call).

vocalize its repertoire of gargle calls by viewing its
mirror image (Censky and Ficken 1982). This evokes
an aggressive response including postures and gargle
calls similar to the visual and vocal displays observed
when two birds, strangers to one another, interact in
close proximity. These recordings show that many of
the gargle types in the repertoires of two or more birds
from the same area are shared (Fig. 11.4a, see also
Baker et al. 2000). The similarity of shared gargle types
contrasts with the differences in gargle types within a
given birds repertoire (Fig. 11.4b).
Gargle calls constituting the repertoires of indi-
viduals in a local population are apparently
assembled from a common pool of syllables. The
size of the syllable pool for our three main study
populations is approximately 50 to 60 (Baker et al.
2000). Many of the syllables are rapid frequency
sweeps. Some syllables are buzzy, broadband
sounds, and these tend to be at the ends of calls.
Calls often decline in mean frequency over their
brief half-second duration. The rapid frequency
modulation of gargle syllables makes them propa-
gate poorly through the environment, and in their
use they are mostly near-distance signals. The
structural properties of gargle calls were described
in detail in previous studies (Ficken and Weise
1984; Hailman et al. 1987; Hailman and Griswold
1996; Baker et al. 2000).
 THE GARGLE CALL 173

(a) 10

2
10

(b) 10

6
Frequency (kHz)

10

(c) 10

2
10

0.5s

Figure 11.4 Gargle calls of adult black-capped chickadees showing: (a) the same gargle type produced by six different birds in the same
population; (b) a repertoire of six gargle types produced by one bird from the same population as individuals in (a) (this comparison indicates
that differences between gargle types within a birds repertoire are much larger that differences between birds within a gargle type); and (c)
three gargle calls vocalized by three different birds (upper row) in the 1996/97 season and the form of the same calls uttered by three other birds
from the same population in the 2003/04, the eighth successive year these calls were present in the population.

Because there is considerable sharing of gargle
syllables among gargle types within and between
birds in a local area, and whole gargle types often
are shared among birds, it is possible to examine
the individual or population from the standpoint of
the entire syllable repertoire as well as from the
standpoint of the gargle call repertoire (Baker et al.
2000). In one analysis covering two years, we
described three adjacent populations with a total of
56 different kinds of gargle syllables from which the
birds constructed an average of 7.6 gargle types as
their repertoires (Baker et al. 2000). Gargle call shar-
ing and syllable sharing are greater within a local
population than between adjacent populations,
174 V O C A L C O M M U N I C AT I O N
supporting the view that these birds exhibit local
dialects in this call (Ficken and Weise 1984;
Miyasato and Baker 1999a; Baker et al. 2000).
11.3.1 Persistence and change in gargle
calls over time
In one of our populations, 63% of the gargle types
found in the first year were present 8 years later. In the
intervening years, a low level of turnover in call types
occurred each season. Examples of gargle types first
recorded in 1996/97 and their representative form
in 2003/04 shows little change (Fig. 11.4c). From
trapping efforts in each population each season, we
know that no individual birds persisted for this time
period. An earlier analysis of gargle persistence also
showed long-term stability in the forms of this call
(Ficken and Popp 1995). Additional to the evidence of
stable calls across time, some gargle types are lost from
a population, and new gargles discovered in new
recruits. For the population mentioned above, for
example, we found five new gargle types in 2003/04
not present in 1996/97. A detailed accounting of the
time course of gargle call persistence and year-to-year
changes in population repertoires over eight seasons
is in preparation (Baker and Gammon, in press).
11.3.2 Year-to-year changes in
repertoires of individuals
In our study populations, during the eight seasons
of sampling, 32 birds with sufficient samples of
gargles (500 or more) were recorded in two succes-
sive seasons. Their average repertoire in the first
season was 8.7 gargle types, and a year later it was
7.6. To accomplish this net loss, an average bird
added 1.2 gargle types to its repertoire and dropped
2.4 gargle types. Given the changes in repertoires
over successive years, and our observations of
juvenile gargle development, we examined a larger
data set to find out if young birds and older birds
differed in repertoire size. Our field season for
capture and recording chickadees was from
September to February. Birds hatched the previous
breeding season (May) we refer to as young birds
(HY/SY; Pyle et al. 1987), whereas birds hatched in
some earlier season we refer to as old birds
(AHY/ASY; Pyle et al. 1987). Young chickadees had
significantly larger repertoires than old chickadees
(young: n 32, mean 9.22, SE 0.55; old:
n 65, mean 7.85, SE 0.37; P 0.03,
MannWhitney U-test; Siegel 1956). These findings
raise questions about the possible social influences
that may cause the observed patterns. We address
these questions by providing background on the
ways gargle calls are used and describe several
experiments and observations that provide insight.
11.4 Contexts of use of the call
The gargle call was referred to in earlier literature as
the fighting call (Dixon and Stefanski 1970) or the
supplanting call (Dixon et al. 1970). It tends to be
a close-range signal, and it is observed commonly
during interactions at food sources in natural
circumstances (Ficken et al. 1987). A similar call is
produced in similar situations by several other
species of chickadees and titmice (Smith 1972;
McLaren 1976; Hailman 1989; Haftorn 1993;
Hailman and Haftorn 1995; McCallum et al. 1999).
The call can be elicited by placing two males, unfa-
miliar with each other, together in a cage or aviary
or in closely adjacent cages. In these circumstances
the birds produce gargle calls as they interact in the
establishment of dominance, with the emerging
dominant bird giving the greatest number of gargles
(Baker et al. 1991). In the field, with color-banded
birds of known dominance relationships, higher-
ranking individuals give more gargles than lower
ranking ones (Popp et al. 1990).
When two birds interact at a food source in a
field setting, the individual that gives gargle calls
wins the contest (Ficken et al. 1987; Popp et al. 1990;
personal observations). A single gargle by a bird
arriving at a food supply often is sufficient to drive
away a bird already at the food, suggesting the call
signals status. Experimentation developed from
these observations showed that two males,
unfamiliar with each other, when placed together in
a neutral cage quickly established a dominance
relationship (Baker et al. 1991). One individual
usually produced a large number of gargle calls
while attacking and supplanting the other bird, and
the dominant individual was the one to attack first
and gargle. In later meetings of the two birds, the
mere utterance of gargles by the dominant was able

to cause the other bird to retreat. Subsequent
encounters staged days or weeks later indicated a
reduction in the frequency of gargle calling during
the encounters. Measurements of wing length, an
index of size, showed that dominants tended to be
slightly larger than their subordinate opponents.
These experiments confirmed that gargling was
an aggressive signal employed in fighting and in
the establishment of dominance relationships.
Smith (1972), in studies of the Carolina chickadee
rasp call (equivalent to the gargle call), pointed out
that confrontations between strangers often
occurred in the context of individuals from one
flock coming into contact with intruders of another
flock. In that context, two antagonists may not be
familiar with one another or at least have not had
recent fights. In field observations of black-capped
chickadees, we have witnessed adjacent territory
holders in gargling contests at territorial borders
during the breeding season (see also Ficken et al.
1987). In these situations, although obviously
agonistic, several meters usually separates the birds,
and gargling tends to be more prolonged than in
winter contests at food sources. Longer duels reveal
more of the gargle call repertoire of an individual.
Experimentation revealed that in an aviary a
repertoire of three gargle types was more aversive
than a single gargle type when both treatments were
paired with a video display of a chickadee (Baker
et al. 1996). Thus, the degree of threat or the intention
to escalate an encounter could be signaled by display
of a larger repertoire. In this experiment, the gargle
stimuli were recorded from the same population as
that of the subjects. In a different laboratory experi-
ment (Miyasato and Baker 1999b), gargle calls repre-
sentative of subjects own local population (familiar,
shared) were more aversive than calls representative
of a distant population (unfamiliar, not shared) and
unfamiliar calls were approached more readily.
These results suggest that it is adaptive to learn the
gargle calls of the local population.
Our further experiments and theoretical consid-
erations address the issues of how social inter-
actions might induce the repertoire changes we
documented in our comparisons of young and old
birds, and how the repertoire is used in ongoing
agonistic interactions. We used several experimen-
tal approaches to these questions.
THE GARGLE CALL 175
11.5 Interactive playback
experiment I
To see if repertoire alteration could be induced by an
aggressive encounter in the short term, we
conducted five trials of interactive playback using
SingIt software (Bradbury and Vehrencamp 1994).
We captured five birds from a single population and
recorded their repertoires by mirror-image stimula-
tion. We selected a gargle type from another bird that
differed distinctly from any of the gargle types in the
subjects repertoire. For a playback trial (2030 min),
we placed a small speaker near the mirror in the
recording chamber. We let the subject give five gar-
gles and then played three of the stimulus gargles in
succession of a temporal pattern typical of normal
gargle delivery. We continued this fivethree bout
structure about 24 times for four of the five subjects.
The fifth bird grew silent after the ninth bout.
During these tests, subjects switched call types fre-
quently, averaging four to five calls then switching
to a differing type in their repertoire. Compared to
our experiences recording birds with the mirror
alone when obtaining samples for repertoire estima-
tion, the playback routine appeared to cause more
frequent switching among call types.
During these playback tests, however, subjects
did not produce a gargle that matched or even
approximated the stimulus gargle. The only gargles
produced by a subject were the same as those found
by the mirror-only stimulation during initial
recording. This suggests that, in a single simulated
agonistic encounter, stimulation by a gargle type not
shared in an opponents repertoire did not reveal
hidden or unexpressed gargle types that were not
previously recorded, nor is the subject able to
assemble a new and matching gargle type in
response to the different gargle used as the stimulus.
Evidently, short-term gargling encounters may not
provide the social circumstances that cause a bird to
change its repertoire. Pursuing this issue further,
we conducted a laboratory aviary study.
11.6 Aviary experiments on
gargle changes
We designed an experiment to determine if chicka-
dees alter their gargle call repertoire when in the
176 V O C A L C O M M U N I C AT I O N
presence of birds from a different population for
several weeks. We simulated the immigration of
young males, hatched in the recent summer, into a
different population in autumn. In its new location,
a hatching year bird in the field would join a local
resident flock and encounter adult males with
gargle call repertoires differing from those of the
juveniles natal population. Our ontogeny studies
suggested that by this time of the autumn season
the hatching year juveniles would have dispersed
and be faced with social learning circumstances
that may cause them to conform to the gargle calls
of their current site.
Two aviary trials were conducted each autumn
for 3 years (20012003). Two experimental aviaries
were in separate rooms removed from auditory
contact with each other. Four of the six aviary
groups were established with a young male from
one population and two old males from another
population. Two aviary groups were established
with a young male from one population and one
old and one young male from another population.
We aged the birds according to the condition
(pneumatization) of the skull and characteristics of
the tail feathers (Pyle et al. 1987). Prior to placement
into the aviaries, each bird was tape-recorded to
obtain a full account of its gargle call repertoire.
During the time the birds were together in an
aviary, we made frequent observations to deter-
mine dominance relationships. Following an aviary
trial, we tape-recorded the birds using the mirror-
image procedure to obtain the postexperimental
repertoire of gargle calls.
To evaluate the extent to which gargle types were
shared among the birds in an aviary, we calculated
for each bird an index of sharing, defined as the
proportion of its gargle types shared (range 01)
with any other bird in its aviary (Hughes et al. 1998;
Baker et al. 2000). We calculated the index for each
bird before the start of the aviary trial and after
completion of the trial, for all 18 birds over the six
aviary trials. Further, we examined the average
sharing index for the group of three birds before
and after an aviary trial. We also determined if age
or dominance status was correlated with changes in
the sharing index of the subjects. Within the first
2 days following the introduction of the birds into
the aviary, we observed a clear linear dominance
hierarchy. In these early encounters gargling was
frequent but decreased as days passed, as expected
from our previous study (Baker et al. 1991). In
the first year, the subjects were together in
their aviaries from 28 September through 20
October (23 days); in the second year, from 12
October through 26 November (46 days); and in the
third year, from 18 October through 29 November
(43 days).
Average values of sharing increased from the
beginning to the end of each aviary trial. The
increased sharing was only marginal in one aviary
in 2001 (from 0.38 initially to 0.39 at the end) and
one aviary in 2002 (from 0.58 to 0.61), but in
the remaining four trials it was more substantial
(0.15 0.41; 0.16 0.25; 0.19 0.38; 0.23 0.44).
Including all six trials, the change in sharing was
significant (T 0, P 0.028, Wilcoxon matched-
pairs signed-test; Siegel 1956). We also examined
changes in the amount of repertoire sharing for
individuals and found no relationship with age
(U 36, P 0.76, MannWhitney U-test) or dom-
inance rank (Xr 2.48, P 0.38, Friedman
ANOVA; Siegel 1956).
Increased sharing occurred mostly because
individuals dropped unshared gargle types. Over
all aviary trials, 42 gargle types were dropped
from repertoires of the 18 subjects and only 18
gargle types added. Dropping gargles was more
common in young birds: 26 gargle types were
dropped by eight young birds (3.25/bird) whereas
only 16 gargle types were dropped by 10 old birds
(1.6/bird).
We conclude that birds in a prolonged social
group alter their gargle call repertoire in a way that
leads to increased sharing within the group. We
now ask how such a change in repertoire may
benefit the individuals involved. Within a popula-
tion, where individuals have repertoires with
substantial sharing of gargle types between them,
an individual possesses the plasticity of expression
to match the calls of an opponent during aggressive
interactions. In a number of songbird species,
matching songs or matching repertoires is a signal
of an increased level of aggression (Krebs et al. 1981;
Burt et al. 2001; Vehrencamp 2001; Otter et al. 2002;
Mennill and Ratcliffe 2004). To examine the possible
benefits in sharing gargle calls with an opponent,
we conducted an additional interactive playback
experiment.

11.7 Interactive playback experiment II
We tape-recorded subjects by the mirror-only
stimulation so that their complete repertoires were
known. We tested six birds in a setup like that used
in Interactive Playback Experiment I. The micro-
phone led to a sound spectrograph operating in real
time, which allowed experimenters to monitor the
vocal output of the subject. Another experimenter
operated a computer, with icons on the screen
representing the gargle types in the repertoire of the
subject (Bradbury and Vehrencamp 1994). The
gargle calls stored in computer memory, and that
were triggered as stimuli when an icon was clicked,
were recorded from a different bird in the popula-
tion but were classified as the same gargle types as
those of the subject. Thus, the experimenter could
play either a matching or a non-matching gargle in
response to the gargle of the subject, but the gargle
would always be within the subjects repertoire.
During a trial (30 min) we played matching or
non-matching gargles in response to the subjects
gargles. We alternated throughout a trial by match-
ing the subject five to ten times then used non-
matching replies five to ten times, then matching
again for five to ten times, and so on. Sometimes a
subject gargled a second time before we could iden-
tify the gargle type and respond with a stimulus
presentation. This occurred in 25 to 50% (range) of
the gargles delivered by subjects.
With this simulation, we addressed three ques-
tions: (i) When a subject hears a non-matching gargle
from the presumed opponent, does it switch to
match the stimulus, switch to a non-matching gargle,
or produce the same gargle type it gave prior to the
stimulus? (ii) When a subject hears a matching gargle
from the opponent, does it respond with the same
gargle it gave prior to stimulation, or does it switch to
a different gargle type? (iii) Is there a difference in
response latency by a subject when it hears a match-
ing versus non-matching gargle from the simulated
opponent? Our hypothesis was that if matching
indicates an escalation of fighting then playing non-
matching stimuli to the subject should cause it to
switch gargles and match the stimulus. Second, when
we played matching gargles to the subject it should
continue to match us and not switch gargle types.
Third, we predicted that if matching indicates esca-
lation, then the latency of response to our matching
THE GARGLE CALL 177
stimuli should be less than that given to non-match-
ing stimuli. In the latter case, we assumed that if
matching indicates escalation, then matching more
quickly would reinforce the signal valence. In gen-
eral, our assumption in all these predictions was that
the subject, in its familiar home cage, will perceive
the stimulus as a challenge/intrusion and will
respond by escalation of the encounter.
We examined the first 50 occasions when we
responded to a subjects gargle with a non-matching
gargle. We had complete samples for five birds, and
a sixth bird received only eight instances of non-
matching gargles before it quit vocalizing. The
subjects showed a tendency not to switch, but
instead to use the same call they used immediately
prior to playback stimulation. Of 258 non-matching
stimuli delivered to the six subjects, there were only
38 (15%) instances of switching to another gargle
type. Of these switches, 31 (82%) were to a non-
matching gargle type. Thus, our experiment did not
obtain evidence that subjects followed a matching
strategy, perhaps as an attempt to dominate an
opponent or signal an escalation of a contest.
We also examined the first 50 occasions of match-
ing presentations and found little evidence for
switching in five of the six subjects. These five
received 250 matching stimuli and there were only
11 (4%) cases of switching. The subject that received
nine matching stimuli, before it stopped respond-
ing, switched in six of the stimulus presentations.
We examined the latency of response to the
next gargle given by a subject when stimulated
with matching versus non-matching gargles. For
each of five subjects, we compared 50 values of
latency following matching gargles to 50 values of
latency following non-matching gargles. One bird
had only nine values for matching and eight for
non-matching gargles. Using the median response
times, following matching versus non-matching
gargle stimuli for each bird, we found no significant
difference for the two conditions (T 5, P 0.249,
Wilcoxon matched-pairs signed-ranks test).
11.8 Combined analysis of interactive
playback tests
We examined our data from the 11 interactive
playback trials to address the question of how inter-
178 V O C A L C O M M U N I C AT I O N
1.0
1.96*Std.Error
0.9
1.00*Std.Error
Mean
Diversity (H/Hmax)
0.8
0.7
0.6
0.5
Playback Mirror only
plus mirror
Figure 11.5 Diversity of gargle calls uttered by black-capped
chickadees stimulated by mirror image and gargle calls during
interactive playback, compared to stimulation by mirror image only
(no playback). Diversity was greater during interactive playback
(P 0.003).
active playback influenced a subject, regardless of
whether the opponents gargles were present or not
in the subjects own repertoire. In a natural popula-
tion, a bird is likely to encounter opponents who
share some of its gargle calls, and other opponents
that do not. We compared the way that a subject
distributed its gargle calls when stimulated by the
mirror-only treatment to the way it used its reper-
toire when stimulated by its mirror image and
gargle playback. We interpret this as a simulation of
a bird interacting with an opponent that does not
gargle, such as a subordinate male or female, versus
one that interacts vocally during the encounter.
We used the ShannonWiener species diversity
index to examine the relative abundance of gargle
calls found in each gargle type category. The diver-
sity index is:
H P logP
i i i
in which Pi refers to the proportion of gargles of
the ith gargle type. To take account of birds with
differing repertoire sizes we used H/Hmax for our
comparisons. Hmax is the maximum diversity pos-
sible for a subject with a given repertoire size. Two of
the subjects delivered fewer gargles than the other
nine during the trials, but we include their data
because they were qualitatively similar to the others.
In every subject, H/Hmax was greater during
interactive playback than during mirror-only
stimulation (Fig. 11.5), although for some birds the
differences were not large. The overall result, how-
ever, was statistically significant (T 0, P 0.003,
Wilcoxon matched-pairs signed-ranks test). The
results suggest that a subject uses more of its
repertoire, switching among gargle types frequently,
when its opponent is responding with gargle calls.
This pattern of use contrasts with the mirror-only
stimulation in which the subject tends to repeat a
gargle in longer strings of the same type before
switching to another type. High rates of switching
among territorial song types in other species of
birds, has been shown to signal a more aggressive
interaction (Kramer and Lemon 1983; Kramer et al.
1985).
A caveat is that our analysis of gargle switching
fails to consider a possible order effect. Mirror-only
recordings were performed first and were followed
some days later by the interactive playback tests. To
achieve the main purpose of the interactive tests,
we had to determine the repertoire of the subjects
prior to interactive testing and that precluded a
design in which some birds were first recorded then
tested and others were tested then recorded. We
believe, however, that the diversity result is prob-
ably not an effect of treatment order. In our aviary
experiments, for example, we recorded the subjects
by mirror-only before and after the time they were
together in the aviary. We randomly selected one
bird from each of the six experimental aviaries and
calculated its repertoire diversity from the before
and after recordings. In five of the six birds, the
diversity decreased from the first to the second
recording, and in one bird diversity increased.
These data therefore suggest that the increased
diversity expressed in the subjects in the playback
experiments did not result from an order effect.
11.9 Synthesis of theory and
empirical results
The pattern of use of gargle calls in year-round
agonistic encounters points to the probable function
of this vocal signal as aiding in the acquisition and

maintenance of resources (food, female mate, terri-
tory). From the accumulated knowledge of the
behavioral ecology of black-capped chickadees
(Smith 1991) we know that postdispersal hatching
year males in the autumn of the northern temperate
zone are joining, or attempting to join, flocks whose
members will be associated through the winter.
Gargle calling is a pronounced feature of young
males in the early autumn. Furthermore, the major
peak of pair formation is in this autumn period, and
this time of the annual cycle also sees decreasing
food supplies and increased competition. We
hypothesize that vocal convergence by young males,
still in the condition of vocal plasticity, on gargle call
features of older and dominant residents may
provide benefits to the young birds in: (i) gaining
access to flock membership; (ii) competing more
effectively for food; and (iii) increasing their mating
potential in the context of female choice. Attaining a
high ranking in the winter flock evidently is of
advantage to obtaining a breeding territory in the
home range of the winter flock, whereas lower-
ranked pairs may be excluded and frequently are
unable to obtain breeding territories (Smith 1991).
From a consideration of the social context in
which the gargle call is used, together with the
results of the population data, aviary experiments,
and the interactive playback trials, we suggest
a theoretical explanation of local population
conformity in gargle call structures and the
evolution of gargle call repertoires. We imagine an
immigrant chickadee arriving in a new population.
Upon gargle calling in aggressive encounters with
residents, its calls announce its status. If the immi-
grant is a young chickadee, our data on gargle
ontogeny suggest its calls will still be in a plastic
stage, and such calls will signal juvenile age and
subordinate status. Although immigration by
second-year or older birds is probably rare, if the
immigrant is an older bird from another area and
with well-formed gargle calls, its different call struc-
tures (Ficken and Weise 1984; Miyasato and Baker
1999a; Baker et al. 2000) will advertise its status of a
stranger. The resident therefore has information
about the asymmetrical nature of the agonistic
interaction. As observed in neighborstranger
interactions in territorial singing contests, noted in
many bird species, the resident will escalate the
THE GARGLE CALL 179
fight using a diverse array of call types (interactive
playback results), serving as a more aversive signal
(Baker et al. 1996), while the stranger retreats. The
residents status and access to resources (food,
territory, mate) is thus successfully maintained.
Such interactions place a pressure on the immigrant
individual to reduce the asymmetry in contests
with local dominants by altering its gargle signals to
conform to local patterns, which is accomplished
by the immigrant by adding or dropping gargle
types so that its repertoire more closely matches
those of residents (aviary experiments).
It is more likely that gargle types are dropped than
added (aviary experiments), and young birds may
achieve matching more easily than older birds
because of the larger repertoire size of young birds
(population data) and because of their inherent vocal
plasticity (ontogeny data). However, in considering
the potential for alterations of the repertoire in older
birds by adding new gargle types, we note that new
elements may be added to the territorial song
repertoires of older birds, as described in canaries
(Serinus canaria; Nottebohm et al. 1986), European
starlings (Sturnus vulgaris; Hausberger 1997), great
tits (McGregor and Krebs 1989), and northern
mockingbirds (Mimus polyglottos; Derrickson 1987).
Therefore, while we think it possible that entirely
new calls may be developed and added to the
repertoires of older birds, we cannot rule out that a
new call, apparently added to a repertoire, may be
the reinstatement of a call long unused. This general
model we have outlined here (see also Ficken et al.
1987) to explain local conformity of acoustic signals
has been applied to territorial songs (Payne et al.
1988; Craig and Jenkins 1982) and also in the context
of mate choice (Rothstein and Fleischer 1987),
although without the addition or deletion of reper-
toire components as the means by which conformity
is achieved.
Within a local population of chickadees, there is
substantial sharing of gargle calls and syllables
among birds (Baker et al. 2000). In the context of the
local population, however, individuals vary in
repertoire size (Baker et al. 2000) as well as in
dominance status. Asymmetries in dominance
status will be tested frequently during contests over
resources. Under such conditions we can imagine a
subordinate bird adding a gargle call, common in
180 V O C A L C O M M U N I C AT I O N
the area, to its repertoire, which sometimes leads to
its successful bluffing in contests. As modeled by
Andersson (1980), this would place a social evolu-
tionary pressure on dominants to develop new calls
to counteract the bluffing tactic. The process, analo-
gous to an arms race, could explain the evolution of
gargle call repertoires.
Our interactive playback tests did not reveal
clear and immediate adjustments by subjects either
through matching or avoiding matching during the
ongoing flow of the interaction. The negative
results could derive from an experimental problem,
such as not simulating closely a natural encounter.
In our tests, for example, the visual display seen in
the mirror by a subject would always be that of an
equal-ranked and equally aggressive bird, preclud-
ing a dominantsubordinate visual interaction.
Also, our results could be attributed to the short
duration of a trial in comparison to repeated
contests over resources in the field. However, we
did observe a consistent pattern of an increase in
the diversity of gargle calls that subjects gave
during playback, and this may be an important
finding in these tests. Hailman (1989:336) antici-
pated this in his review of vocalizations in
the ParidaeIt is possible that acoustical variety
represents information at a different level: instead
of each variant representing a different message,
it is the ensembles diversity per se that is
informative. We believe that additional playback
experiments with the gargle call would be of benefit
in addressing this issue.
From comparative reviews of the literature that
describes the different kinds of vocalizations of the
members of the Paridae (Hailman 1989; Hailman
and Ficken 1996), it appears to us that the informa-
tion being obtained by studies of black-capped
chickadees will be broadly applicable to many
other species of Paridae. This is especially true for
members of Poecile. We suggest that as comparable
studies are carried out in other species it will be
found that vocalizations with functional equiva-
lence to the gargle call will show similar patterns of
local similarity and between-population differ-
ences, and that the local convergence in the acoustic
features of the calls will be influenced strongly by
social learning throughout ontogeny.
We are only beginning to appreciate the social
learning circumstances that shape chickadee vocal
signals. It seems clear that plasticity in vocal signals
is greatest early in the lives of black-capped chicka-
dees when the major classes of signals are being
established (Baker et al. 2003). Evidently gargle call
development extends into the immediate postdis-
persal phase of life, and probably beyond. We point
to our aviary studies in this regard, and the field
evidence that suggests older birds may alter their
repertoires. Although they are preliminary, the
results are reminiscent of patterns seen in territorial
song of a number of other songbird species. In these
cases, the social influences of resident males on
younger birds during the time of territory
establishment causes the young male to drop
certain components of it song patterns and attain
better matching to residents. The process of gargle
call repertoire alteration is therefore not unlike
the selective attrition or action-based learning
observed in territorial song repertoires of a
number of songbirds (Marler and Peters 1982a;
Nelson 1992a, 1992b; Marler and Nelson 1993;
Marler 1997).
Acknowledgments
We thank the students, undergraduates and
graduates, who in various ways assisted this
research: Adriana Acosta, Merrill Baker,
Lindsay Barnhill, April Becker, Brad Bisbee, Alice
Campbell, Owen Davis, Rachel Dill, Nicole Ernst,
Trina Howard, Stephanie Kane, Mehmet Kpeli,
Rita Lerner, David Logue, Chandra Malpede, Lori
Miyasato, Katie Payne, Rebecca Promessi,
Samantha Sasman, Mala Sawhney, Paul Sweet,
Todd Tracy, Wallace Turner, and Meagan Tovado.
We also acknowledge gratefully the many research
contributions of Susan M. Smith and Millicent S.
Ficken, which have informed and stimulated our
investigations of the behavioral ecology of chick-
adees in general and the gargle call in particular.
During our investigations, DEG was supported by
a predoctoral fellowship from the National Science
Foundation. The research was supported by the
National Science Foundation (grants BNS-8706526,
IBN-0090400 to MCB).

References
Andersson, M. (1980). Why are there so many threat
displays? Journal of Theoretical Biology, 86, 773781.
Baker, M. C., Baker, M. S. A., and Gammon, D. E. (2003).
Vocal ontogeny of nestling and fledgling black-capped
chickadees Poecile atricapilla in natural populations.
Bioacoustics, 13, 265296.
Baker, M. C., Boylan, J. T., and Goulart, C. A. (1991). Effect
of gargle vocalizations on behavior of black-capped
chickadees. Condor, 93, 6270.
Baker, M. C. and Gammon, D. E. (in press). Persistence
and change of vocal signals in natural populations of
chickadees: annual sampling of gargle calls over eight
seasons. Behaviour.
Baker, M. C., Howard, T. M., and Sweet, P. W. (2000).
Microgeographic variation and sharing of the gargle
vocalization and its component syllables in black-
capped chickadees (Aves, Paridae, Poecile atricapillus)
populations. Ethology, 106, 819838.
Baker, M. C., Tracy, T. T., and Miyasato, L. E. (1996).
Gargle vocalizations of black-capped chickadees: test
of repertoire and video stimuli. Animal Behaviour, 52,
11711175.
Bradbury, J. W. and Vehrencamp, S. L. (1994). SingIt!: a
program for interactive playback on the Macintosh.
Bioacoustics, 5, 308310.
Burt, J. M., Campbell, S. E., and Beecher, M. D. (2001).
Song type matching as threat: a test using interactive
playback. Animal Behaviour, 62, 11631170.
Catchpole, C. K. and Slater, P. J. B. (1995). Bird Song:
Biological Themes and Variations. Cambridge University
Press, Cambridge, UK.
Censky, E. J. and Ficken, M. S. (1982). Responses of black-
capped chickadees to mirrors. Wilson Bulletin, 94,
590594.
Craig, J. L. and Jenkins, P. F. (1982). The evolution of com-
plexity in broadcast song of passerines. Journal of
Theoretical Biology, 95, 415422.
Derrickson, K. C. (1987). Yearly and situational changes in
the estimate of repertoire size in northern mockingbird
(Mimus polyglottos). Auk, 104, 198207.
Dixon, K. L. and Stefanski, R. A. (1970). An appraisal of
the song of the black-capped chickadee. Wilson Bulletin,
82, 5362.
Dixon, K. L., Stefanski, R. A., and Folks, F. N. (1970).
Acoustic signals in the mating of mountain and black-
capped chickadees. Auk, 87, 322328.
Ficken, M. S. and Popp, J. W. (1995). Long-term persist-
ence of a culturally transmitted vocalization of the
black-capped chickadee. Animal Behaviour, 50, 683693.
THE GARGLE CALL 181
Ficken, M. S. and Weise, C. M. (1984). A complex call of
the black-capped chickadee (Parus atricapillus). I
Microgeographic variation. Auk, 101, 349360.
Ficken, M. S. and Witkin, S. R. (1977). Responses of black-
capped chickadee flocks to predators. Auk, 94, 156157.
Ficken, M. S., Ficken, R. W., and Witkin, S. R. (1978).
Vocal repertoire of the black-capped chickadee. Auk,
95, 3448.
Ficken, M. S., Weise, C. M., and Reinartz, J. A. (1987). A
complex vocalization of the black-capped chickadee. II
Repertoire, dominance and dialects. Condor, 89, 500509.
Galef, B. G., Jr. (1996). The adaptive value of social learn-
ing: a reply to Laland. Animal Behaviour, 52, 641644.
Gammon, D. E., Baker, M. C., and Tipton, J. R. (2005).
Cultural divergence within novel song of the black-
capped chickadee (Poecile atricapillus). Auk, 122, 853871.
Haftorn, S. (1993). Ontogeny of the vocal repertoire in the
willow tit Parus montanus. Ornis Scandinavica, 24,
267289.
Hailman, J. P. (1989). The organization of major vocaliza-
tions in the Paridae. Wilson Bulletin, 101, 305343.
Hailman, J. P. and Ficken, M. S. (1996). Comparative
analysis of vocal repertoires with reference to chicka-
dees. In: D. E. Kroodsma and E. H. Miller, eds. Ecology
and Evolution of Acoustic Comminication in Birds, pp.
97117. Cornell University Press, Ithaca, NY.
Hailman, J. P. and Griswold, C. K. (1996). Syntax of black-
capped chickadee (Parus atricapillus) gargles sorts many
types into few groups: implications for geographic
variation, dialect drift, and vocal learning. Bird Behavior,
11, 3957.
Hailman, J. P. and Haftorn, S. (1995). Siberian tit. In: Poole,
A. and Gill, F., eds. The Birds of North America, No. 196,
pp. 123. Academy of Natural Sciences, Philadelphia,
and American Ornithologists Union, Washington, DC.
Hailman, J. P., Ficken, M. S., and Ficken, R. W. (1985). The
chick-a-dee calls of Parus atricapillus: A recombinant
system of animal communication compared with
written English. Semiotica, 56, 191224.
Hailman, J. P., Ficken, M. S., and Ficken, R. W. (1987).
Constraints on the structure of combinatorial chick-
a-dee calls. Ethology, 75, 6280.
Hausberger, M. (1997). Social influences on song acquisi-
tion and sharing in the European starling (Sturnus
vulgaris). In: Snowdon, C. T. and Hausberger, M., eds.
Social Influences on Vocal Development, pp. 128156.
Cambridge University Press, New York.
Hughes, M., Nowicki, S., Searcy, W. A., and Peters, S.
(1998). Song-type sharing in song sparrows: implica-
tions for repertoire function and song learning.
Behavioral Ecology and Sociobiology, 42, 437446.
182 V O C A L C O M M U N I C AT I O N
Kramer, H. G. and Lemon, R. E. (1983). Dynamics of terri-
torial singing between neighbouring song sparrows
(Melospiza melodia). Behaviour, 85, 198223.
Kramer, H. G., Lemon, R. E., and Morris, M. J. (1985). Song
switching and agonistic stimulation in the song
sparrow (Melospiza melodia): Five tests. Animal
Behaviour, 33, 135149.
Krebs, J. R., Ashcroft, R., and Van Orsdal, K. (1981). Song
matching in the great tit Parus major L. Animal Behaviour,
29, 918923.
Marler, P. (1997). Three models of song learning: evidence
from behavior. Journal of Neurobiology, 33, 501516.
Marler, P. and Nelson, D. A. (1993). Action-based learning:
a new form of developmental plasticity in bird song.
Netherlands Journal of Zoology, 43, 91103.
Marler, P. and Peters, S. (1982a). Subsong and plastic
song: their role in the vocal learning process. In.
Kroodsma, D. E. and Miller, E. H., eds. Acoustic
communication in birds, vol. 2, pp. 2550. Academic Press,
New York.
Marler, P. and Peters, S. (1982b). Developmental overpro-
duction and selective attrition: new processes in the
epigenesis of birdsong. Developmental Psychobiology, 15,
369378.
McCallum, D. A., Grundel, R., and Dahlsten, D. L. (1999).
Mountain chickadee. In: Poole, A. and Gill, F., eds. The
Birds of North America, No. 453, pp. 127. Academy of
Natural Sciences, Philadelphia, and American
Ornithologists Union, Washington, DC.
McGregor, P. K. and Krebs, J. R. (1989). Song learning in
adult great tits (Parus major): effects of neighbours.
Behaviour, 108, 139159.
McLaren, M. A. (1976). Vocalizations of the Boreal chicka-
dee. Auk, 93, 451463.
Mennill, D. J. and Ratcliffe, L. M. (2004). Overlapping and
matching in the song contests of black-capped chicka-
dees. Animal Behaviour, 67, 441450.
Miyasato, L. E. and Baker, M. C. (1999a). Black-capped
chickadee call dialects along a continuous habitat corri-
dor. Animal Behaviour, 57, 13111318.
Miyasato, L. E. and Baker, M. C. (1999b). Discrimination
of gargle calls by black-capped chickadees (Poecile atri-
capillus). Bird Behavior, 13, 914.
Mundinger, P. C. (1982). Microgeographic and macrogeo-
graphic variation in acquired vocalizations of birds. In:
Kroodsma, D. E. and Miller, E. H., eds. Acoustic
Communication in Birds, vol. 2, pp. 147208. Academic
Press, New York.
Nelson, D. A. (1992a). Song overproduction and selective
attrition lead to song sharing in the field sparrow
(Spizella pusilla). Behavioral Ecology and Sociobiology, 30,
415424.
Nelson, D. A. (1992b). Song overproduction, song
matching and selective attrition during development.
In: McGregor, P. K., ed. Playback and Studies of
Animal Communication, pp. 121133. Plenum Press,
New York.
Nelson, D. A. and Marler, P. (1994). Selection-based learn-
ing in bird song development. Proceedings of the National
Academy of Science USA, 91, 1049810501.
Nottebohm, F., Nottebohm, T. M., and Crane, L. (1986).
Developmental and seasonal changes in canary song
and their relation to changes in the anatomy of song
control nuclei. Behavioral and Neural Biology, 46,
445471.
Nowicki, S. (1983). Flock-specific recognition of chickadee
calls. Behavioral Ecology and Sociobiology, 12, 317320.
Odum, E. P. (1942). Annual cycle of the black-capped
chickadee3. Auk, 59, 499531.
Otter, K., Njegovan, M., and Fotheringham, J. (2002).
Importance of frequency and temporal song matching
in black-capped chickadees: evidence from interactive
playback. Ethology, 108, 181191.
Payne, R. B., Payne, L. L. and Doehlert, S. M. (1988).
Biological and cultural success of song memes in indigo
buntings. Ecology, 69, 104117.
Popp, J. W., Ficken, M. S., and Weise, C. M. (1990). How
are agonistic encounters among black-capped chicka-
dees resolved? Animal Behaviour, 39, 980986.
Pyle, P., Howell, S. N. G., Yunick, R. P., and DeSante, D. F.
(1987). Identification Guide to North American Passerines.
Slate Creek Press, Bolinas, CA.
Rothstein, S. I. and Fleischer, R. C. (1987). Vocal dialects
and their possible relation to honest status signalling in
the brown-headed cowbird. Condor, 89, 123.
Searcy, W. A. and Nowicki, S. (1999). Functions of song
variation in song sparrows. In: Hauser, M. D. and
Konishi, M., eds. The Design of Animal Communication,
pp. 577595. MIT Press, Cambridge, MA.
Siegel, S. (1956). Nonparametric Statistics. McGraw-Hill,
New York.
Smith, S. M. (1991). The Black-Capped Chickadee: Behavioral
Ecology and Natural History. Cornell University Press,
Ithaca, NY.
Smith, S. T. (1972). Communication and other social
behavior in Parus carolinensis. Publication of the Nuttall
Ornithological Club, 11, Cambridge, MA.
Tchernichovski, O., Nottebohm, F., Ho, E., Pesaran, B., and
Mitra, P. P. (2000). A procedure for an automated meas-
urement of song similarity. Animal Behaviour, 59,
11671176.
Vehrencamp, S. L. (2001). Is song-type matching a con-
ventional signal of aggressive intentions? Proceedings of
the Royal Society of London, B, 268, 16371642.
 CHAPTER 12
How postdispersal social
environment may influence
acoustic variation in birdsong
David E. Gammon
12.1 Introduction
Learned vocalizations vary across space and time
in nearly all songbird species examined (Kroodsma
and Baylis 1982) including North American and
Eurasian Parids (Hailman 1989). To understand the
process behind this nearly universal pattern, we
must understand how social and ecological factors
affect song learning. Specifically we must under-
stand the mechanisms by which cultural innova-
tions arise in birdsong, because these innovations
must play a role in the generation of acoustic
variation across space and time.
The fee-bee song of the black-capped chickadee is
often cited as an exception to the general pattern of
acoustic variation across space and time (Kroodsma
et al. 1999; Chapter 14). Individuals across most of
this species North American geographic range
possess a single song type that does not vary in its
acoustic structure. For some chickadee populations,
however, such as those in Fort Collins, Colorado,
cultural innovations in the fee-bee song have
become established (Gammon and Baker 2004). By
examining the social and ecological circumstances
within which such cultural innovations become
established, we may gain insight into the evolution
of within and between-individual diversity in
birdsong.
There is an enormous diversity of song-learning
programs among songbirds. Species vary in the
timing and accuracy of learning, in the number and
identity of tutors, in the number of song types
learned, and in the species-specific constraints
within which song is acceptable as a learning
model (Brenowitz and Beecher 2005). At one
extreme, Puget Sound white-crowned sparrows
(Zonotrichia leucophrys pugetensis) learn only one or
two song types early in life by precisely imitating
adult conspecific males in their natal area, and they
never learn new syllables, phrases, or song types
following natal dispersal (Nelson 2000). At the
other extreme, European starlings (Sturnus vulgaris)
continue to learn syllables, phrases, and song types
throughout life by imitating both conspecifics and
the sounds of other species (Mountjoy and Lemon
1995). Despite this diversity of song-learning
programs, there are a few general patterns among
songbirds. For example the same neural circuits
control song in every songbird species examined
(Brenowitz 1997). Furthermore, the vocal output of
a developing bird for a given song type nearly
always varies early in the learning process, but
becomes more stereotyped over developmental
time (e.g. Marler and Peters 1982; Tchernichovski
et al. 2001). Novel song material produced early in
development could represent inaccurate imitation,
improvisation on an existing song type, an inven-
tion, or a developmental mutation. Some of this
novel material may persist into adulthood as a
cultural innovation and be responsible for acoustic
variation across space and time in songbirds.
The amount of acoustic variation in the songs of
a developing bird is affected by its environment
before and after natal dispersal. For example if
fledglings do not receive sufficient exposure to
appropriate conspecific song (e.g. Marler and
183
184 V O C A L C O M M U N I C AT I O N
Tamura 1964) or if they are malnourished (e.g.
Nowicki et al. 2002), they may learn song inaccur-
ately. This could result in novel song types or
novel song type variants. In many songbird species
the environment continues to exert an effect on the
vocal output of juveniles following natal dispersal.
Immediately after dispersal in many songbird
species, juvenile song is still plastic with regard to
both the number of song types and the acoustic
structure of each song type (e.g. Kroodsma 1974;
Nelson 2000; Baker et al. 2003). Dispersing juveniles
might possess song types not shared with their
adult neighbors, or they may possess a song
type shared with neighbors but containing a unique
acoustic structure such as a novel syllable. Because
sharing song with neighbors is often adaptive
(Beecher et al. 1997; McGregor et al. 1992; Molles
and Vehrencamp 2001), juveniles of many species
selectively retain only the song material that best
matches their neighbors. As such, novel acoustic
variation seldom becomes established into a popu-
lation (McGregor and Krebs 1989; Nelson and
Marler 1994; Nordby et al. 2001).
In this chapter I pose the question, In what
social and ecological circumstances should
Natal
dispersal Bird A
Bird B
within a song type
Acoustic variation
VA
of a bird
Vpop
VB
Developmental time
Figure 12.1 In the visual model of song learning for a given song
type, acoustic variation always exists in the vocal output of juveniles
during early developmental stages, but this variation decreases over
time. Further, individual birds may vary slightly in the final production
of an individual song type (referred to as the range of variation
within each individualVA or VB). This will result in a range of
variation among individuals in the population for this song type (VP).
For birds singing multiple song types (i.e. most songbirds, Krebs and
Kroodsma 1980), one funnel would be needed to represent each
song type of an individual.
juveniles retain novel acoustic material as adults?
I first present a visual model of song learning
(Fig. 12.1). I then hypothesize how the environment
following natal dispersal affects variation in the
vocal output of a juvenile songbird, and I test this
hypothesis using data from the fee-bee song of the
black-capped chickadee. I end by taking a broad
look at cultural evolution and the origin and
maintenance of song variation.
12.2 Description of model and
hypothesis
The model asserts that for each song type learned,
the vocal output of juveniles in early developmen-
tal stages is variable but becomes more stereotyped
over developmental time. This assumption has
empirical support (Haftorn 1993; Kroodsma et al.
1995; lveczky et al. 2005), and it is represented in
Fig. 12.1 as a funnel that begins wide and then
narrows over time. When young birds precisely
and accurately model their song(s) after the song(s)
of neighbors following natal dispersalas has been
shown for numerous songbirds in the field and
laboratory (e.g. Nelson and Marler 1994; Nordby
et al. 2001)acoustic conformity throughout the
population will result in little acoustic variation
within or between birds for each song type
(Fig. 12.2a). Acoustic variation for a given song type
could originate between birds (individuals use
different variants for that song type, Fig. 12.2b),
within birds (a single individual uses multiple
variants for that song type, Fig. 12.2c), or both
between and within birds (Fig. 12.2d). As
mentioned in the introduction to this chapter, song
sharing between adult neighbors is adaptive
for many songbird species. Therefore, failure of a
juvenile to conform the acoustic structure of its
song types to the song types of its neighbors could
result in decreased fitness for the developing bird.
I hypothesize that the tendency of an individual
to retain song material that conforms in its acoustic
structure to the local pattern varies as a function
of both the size and degree of isolation of that
individuals adult population. In one scenario a
juvenile settles into a large, contiguous population
(Fig. 12.2a); in the other a juvenile settles into
a small, isolated population (Fig. 12.2bd).
 A C O U S T I C VA R I AT I O N I N B I R D S O N G 185

(a) No variation within or between birds (c) Variation within but not between birds
Bird A Bird A
Bird B Bird B V
A
VA
Vpop Vpop
Acoustic variation within a

VB
song type of a bird

VB

(b) Variation between but not within birds (d) Variation within and between birds
Bird A Bird A
Bird B Bird B VA
VA
Vpop Vpop
VB
VB

Developmental time

Figure 12.2 Juveniles that disperse into large contiguous populations encounter many singing neighbors. With this large number of tutors,
these juveniles develop song that conforms acoustically to the local pattern (a). This leads to small V values for each individual (narrow at the
right end of the individuals funnel), and low acoustic variation between individuals using that song type (VA, VB and VP very similar). Alternately,
juveniles that disperse into small, isolated populations may encounter fewer tutors. This can lead to high regional variation in song types among
individuals (large VP), but this regional variation may arise by three different scenarios in individual learning (bd). In the first scenario (b), each
individual becomes highly stereotyped for the version of the song type it crystallizes upon (low within-individual variation), but individuals
crystallize upon different variants for that song type (high between-individual variation, little overlap between VA and VB). In the second scenario
(c) individuals continue to produce multiple song type variants (high within-individual variation, large values for VA and/or VB), but all individuals
use the same multiple song type variants (low between-individual variation). In the third scenario (d) variation both within and between
individuals is large.

Individuals in large, contiguous populations
should be more likely to learn precisely and accur-
ately than individuals in small isolated popula-
tions because they encounter numerous singing
neighbors and thus have greater social pressure to
conform, although this assumption may be true
only in species with highly stereotyped vocaliza-
tions such as the black-capped chickadee. Based on
my hypothesis, I predict that in large, contiguous
populations, an adult will sing with little acoustic
variation in successive renditions for a given song
type (i.e. low variation within birds) and that
shared song types will possess a similar acoustic
structure for each adult (i.e. low variation between
birds, Fig. 12.2a). Conversely, in small isolated
populations, developing birds will encounter few
adult tutors and will be more likely to develop
variation for a given song type. Three possibilities
exist for how this variation might develop: first,
juveniles might introduce novel song type variants
or settle on extreme variants of that song type
seldom used by its neighbors (leads to variation
between, but not necessarily within individuals,
Fig. 12.2b); second, juveniles might continue to sing
multiple song type variants as adults (variation
within, but not necessarily between individuals,
Fig. 12.2c); finally, both variation within and
between individuals might develop (Fig. 12.2d).
Later in this chapter, I test each of these three
possibilities by separately quantifying variation
within and variation between individuals for
chickadees in small, isolated populations.
12.3 Description of study system
I first explain what is known about song learning in
black-capped chickadees and then describe my
study system. Laboratory audio-tutoring experi-
ments demonstrate that chickadees exposed to
appropriate conspecific song are more likely to
develop whistled song than chickadees without
such exposure (Shackleton and Ratcliffe 1993;
186 V O C A L C O M M U N I C AT I O N
Kroodsma et al. 1995; K. A. Otter unpublished
data). Chickadees in all previous audio-tutoring
experiments failed to imitate song precisely and
accurately, suggesting that social and ecological
influences missing in the laboratory likely play an
important role in normal song development. In the
field, juvenile chickadees first attempt to sing 2 to
3 weeks prior to natal dispersal, and their first
attempts at song are imprecise and inaccurate
(Baker et al. 2003). At the time of natal dispersal,
their vocal output for a given song type is still vari-
able (Gammon et al. 2005), but by the following
spring song becomes especially stereotyped for
each song type both within and between individ-
uals (Kroodsma et al. 1999). It is unknown whether
chickadees can learn novel fee-bee song types later
in life, although older birds have been shown to
acquire new gargle types (Chapter 11).
I used song recordings from black-capped
chickadees in and around Fort Collins, Colorado to
test the model and hypothesis presented in this
chapter. These chickadees sing a repertoire of three
discrete song types (Fig. 12.3) that differ acoustic-
ally from the typical fee-bee vocalization that char-
acterizes song of most populations of black-capped
chickadees in their North American range
(Kroodsma et al. 1999; Gammon and Baker 2004).
Two of the local song types, chick-a-fee-bee and fa-fee-
bee, contain novel introductory syllables, whereas
the third song type, low fee-bee, does not. The
introductory notes of chick-a-fee-bee superficially
6kHz
Chick-a-fee-bee
2kHz
1s
Figure 12.3 Spectrograms and oscillograms of the three black-capped chickadee song types found in Fort Collins, Colorado: chick-a-fee-bee,
fa-fee-bee, and low fee-bee. Chick-a-fee-bee and fa-fee-bee possess novel introductory syllables, and chick-a-fee-bee also possesses a novel
amplitude break in the fee syllable.
appear similar to the introductory notes of the
chick-a-dee call, although this similarity may not
represent homology. The chick-a-fee-bee also
normally contains an amplitude break in the fee
syllable not found in the typical fee-bee. The low fee-
bee (called fee-bee-3 in Gammon and Baker 2004)
differs from the typical fee-bee in that it consistently
uses low frequencies for the fee and bee notes rather
than transposing them across a large range of
frequencies.
The three song types of the Fort Collins area vary
within and between study sites separated by just a
few kilometers, and there is greater acoustic diver-
gence between birds in the songs of adult birds
located in discontinuous, low-abundance habitat
islands north of Fort Collins (hereafter referred to
as Islands North) versus continuous high-abun-
dance habitat located along the Poudre River that
runs through Fort Collins (Gammon et al. 2005).
This divergence usually consists of variation in the
number or type of syllables and in the
presence/absence of an amplitude break in the fee
syllable. These acoustic differences are similar to
the acoustic differences distinguishing the song
type variants of a juvenile at the time of its natal
dispersal (Gammon et al. 2005). For example an
adult at one study site sang fa-fee-bee whereas
an adult at a different study site sang fa-fa-fee-bee,
and this difference parallels the vocal output of an
individual juvenile at a third study site, which sang
both fa-fee-bee and fa-fa-fee-bee, even though all of its
Fa-fee-bee Low fee-bee
1s 1s

adult neighbors sang nothing but fa-fee-bee
(Gammon et al. 2005). This and similar findings
demonstrate that acoustic variation present at
the time of natal dispersal could account for
geographic variation in adult song.
Previous work using this study system
(Gammon and Baker 2004; Gammon et al. 2005)
sampled only a single representative of each song
type per bird, thus ignoring variation within the
song types of individuals. This type of variation
could contribute to population patterns and be
functionally important (Stoddard et al. 1988;
Nowicki et al. 1999), but it is rarely examined.
Furthermore, previous work sampled only one
point in time, thus ignoring how acoustic variation
might change in response to variation in popula-
tion size and/or isolation over time.
A bottleneck in the Fort Collins chickadee popu-
lations in late 2003 provided an opportunity to
address both of these issues. Data from the
Christmas Bird Count in Fort Collins show that its
overall population decreased by approximately
75% between the 2003 and 2004 breeding seasons
(Fig. 12.4, National Audubon Society 2002). The
cause of this bottleneck is unknown, but it resulted
in a more patchy distribution of chickadees
throughout Fort Collins. During the breeding sea-
son of 2003, populations were distributed continu-
ously along the Poudre River in Fort Collins, but in
2.0
Population size
1.0
0.0
Dec. Dec. Dec. Dec.
1994 1997 2000 2003
Figure 12.4 Graph showing the relative size of the populations of
black-capped chickadees over a 10-year period in Fort Collins,
Colorado. Data were taken from the Christmas Bird Count, and the y
axis represents the average number of chickadees observed per hour
by each group involved in the Fort Collins count. As shown, there was
a 75% reduction in population size between the 2003 and 2004
breeding seasons.
A C O U S T I C VA R I AT I O N I N B I R D S O N G 187
2004 numerous gaps in distribution occurred along
the same riparian corridor. During a typical dawn
chorus in the breeding season of 2003, each singing
male had an average of seven audible singing
neighbors; during the breeding season of 2004 most
individual chickadees in this same habitat had few
or even no singing neighbors (unpublished data).
These changes in population size and distribution
offered a chance to test the above hypothesis to see
if there was greater acoustic variation within and
between 2004 birds compared to 2003 birds. Such a
test may provide insights into the mechanisms of
cultural evolution and specifically into the origin
and maintenance of acoustic variation in birdsong.
12.4 Acoustic variation before and
after the bottleneck
12.4.1 Sampling procedure
I recorded the songs of unbanded adult male
chickadees along a 6-km stretch of the Poudre River
in Fort Collins during the 2003 and 2004 breeding
seasons (see Box 12.1 for details of sampling
methodology). My goal was to record at least ten
high-quality renditions, of each of the three song
types depicted in Fig. 12.3, from each male, so that
I could examine acoustic variation both within and
between males.
I made spectrograms of all song recordings using
Syrinx software (John Burt; www.syrinxpc.com/
index.html), sampling at 22.05 kHz with 16-bit
accuracy and 1024-point transform size. This
allowed classification of all songs by song types
based upon which syllables appeared on the spec-
trogram. Recordings were used only if the quality
was sufficiently high to allow measurement of the
following variables for a given song: (i) number of
each syllable type ( fee, bee, and the introductory
syllables chick-a or fa), (ii) presence or absence of an
amplitude break in the whistled syllables fee and
bee, and (iii) any distinguishing order of syllables.
After these measurements were made, I randomly
chose ten representative renditions of each song type
for each bird recorded. If there were not ten rendi-
tions available, I excluded that song type for that
bird. This meant that some birds contributed all
three song types to my sample (i.e. 30 high quality
188 V O C A L C O M M U N I C AT I O N
Box 12.1 Sampling method
Most birds were recorded during the dawn
chorus, but several were recorded later in the day
or in response to playback of synthetic songs
modeled after the three Fort Collins song types.
There were no differences between 2003 and
2004 in the relative frequencies with which each
sampling method was used. Recordings were
made on multiple days and by multiple recordists,
but recordings of a given male were always made
on the same day, and recordings made on
songs, 10 from each song type) whereas others con-
tributed only one or two song types. This problem
was unavoidable, however, given that ~20% of birds
lack one of the song types (Gammon and Baker 2004)
and given the difficulties of obtaining large samples
of high-quality recordings.
12.4.2 Analysis of data
Acoustic variation for a given song type can exist
within birds (an individual uses multiple variants
for that song type) and between birds (different
individuals use different variants for that song
type). For example a bird might sing both fa-fee-bee
and fa-fa-fee-bee (variation within that bird), and a
second bird might consistently sing fa-fee without
the bee (no variation within the second bird, but
variation between the two birds). To quantify
this variation, I computed a within-bird and
between-bird diversity measure for each bird
using information gathered from the acoustic
measurements made on its 10, 20, or 30 representa-
tive songs.
For the within-bird measure, I adapted the
ShannonWiener species diversity index for each
song type of a given bird. I considered each song
type variant as a different species and computed
a single diversity value for each group of ten songs
using the formula:
S exp( pi*ln(pi)) song types and then average across that birds song
in which pi refers to the proportion of the ten songs
that existed as the ith song type variant. For a bird
different days were always made at least 300 m
from each other. The latter precaution makes it
highly unlikely that the same bird was recorded
twice during the same season, given that territory
boundaries are stable throughout the breeding
season (Smith 1991). Birds were recorded using a
MiniDisc recorder (either Sony MZ-N1 or Sony
MZ-R700) attached to a Sennheiser microphone
(ME62) mounted in a parabola (either 60 or
45 cm).
that contributed multiple song types to my sample,
I computed one diversity value for each of its song
types and then averaged these values across song
type to get a single within-bird diversity value
for each bird (range {110}).
To obtain between-bird diversity values, I
examined the amount of acoustic overlap between
birds for a given song type in a given year. As an
example of how this was done, suppose that a
population contained three individuals that con-
tributed fa-fee-bees. Bird 1 contributed three typical
fa-fee-bee and seven fa-fa-fee-bee, bird 2 contributed
seven typical fa-fee-bee, one fa-fa-fee-bee and two
fa-fee, and bird 3 contributed 10 typical fa-fee-bee. I
would compare each birds set of 10 songs to
another birds set to yield overlap values. In com-
paring birds 1 and 2, these overlap with three fa-fee-
bees and a single fa-fa-fee-bee, so the overlap value
between birds 1 and 2 would be (3 1)/10 40%.
Birds 1 and 3 overlapped with three fa-fee-bees, due
to bird 1 having numerous other variants of this
song type; therefore, their overlap would be
3/10 30%. Using this same principal, the overlap
between birds 2 and 3 is seven fa-fee-bees, so
7/10 70%. I would then average values to get
a single overlap value per bird for that song
type (35% for bird 1, 55% for bird 2 and 50% for
bird 3). If a bird contributed multiple song types, I
would compute an overlap value for each of its
types to get a single overlap value for that bird.
Finally I took the inverse of this overlap value to
yield a single between-bird diversity value
 A C O U S T I C VA R I AT I O N I N B I R D S O N G 189

(range {1}) for each bird. Birds with high
acoustic overlap would receive low diversity
values, whereas birds that frequently sang novel
song type variants not shared with other birds that
year, would receive high diversity values.
After computing a within-bird and between-
bird diversity value for each bird included in my
sample, I compared the diversity values for 2003 to
those of 2004 birds using a MannWhitney U-test
adjusted for ties. Because I sampled birds in
roughly the same locations each year and because
all birds were unbanded, it is possible that I
sampled some of the same birds in both years.
However, given an estimated 2003 population of
70 to 110 male chickadees in my study site (unpub-
lished data), and given that after the bottleneck
about 40% of the birds in my study population
were SY birds (M. C. Baker, unpublished data), it is
unlikely that I sampled many birds twice. If this
problem existed, however, it would have decreased
the likelihood of detecting differences when
comparing 2003 versus 2004.
12.4.3 Effect of the bottleneck
Sample sizes were N 12 birds for 2003 and
N 12 birds for 2004. For the 2003 data, three birds
contributed three song types, five birds contributed
two song types, and four birds contributed one
song type. For the 2004 data, five birds contributed
three song types, five birds contributed two song
types, and two birds contributed one song type.
These numbers do not represent repertoire sizes,
only the number of song types for a given bird for
which I was able to obtain at least 10 high-quality
songs of that song type.
In 2003, I found very little acoustic variation
within birds. Ten of the 12 birds sampled in 2003
had a within-bird diversity of 1.00, indicating
that the ten representative songs for each of their
song types were the same with regard to the
acoustic measures I took (number and type of
syllables, presence/absence of amplitude breaks in
the whistled syllables, and syllable recombination).
Likewise, there was very little acoustic variation
between birds in 2003. The median measure of
between-bird diversity in 2003 was 1.02, which
indicates high overlap between birds in the song
type variants used. Both of these results contrast
greatly with 2004 data in which only five of the
12 birds sampled had a within-bird diversity
measure of 1.00, and the median measure was 1.20
(significantly different than 2003, U 116,
P 0.026, MannWhitney U-test, Fig. 12.5a).
Furthermore, the median measure of between-
bird diversity for 2004 was 1.45 (significantly
different than 2003, U 78, P 0.001,
MannWhitney U-test, Fig. 12.5b). Spectrograms

(a) (b)
2.5 2.5
Variation between birds
Variation within birds

2.0 2.0

1.5 1.5 1.45

1.38
1.20
1.0 1.00 1.0 1.02

2003 2004 Islands North 2003 2004

Fort Collins Fort Collins

Figure 12.5 Boxplots comparing the amount of acoustic variation found within (a) and between (b) adult Fort Collins chickadees in 2003
(N 12 birds) vs. 2004 (N 12 birds), and also acoustic variation within adult chickadees located in isolated habitat patches north of Fort
Collins (N 21 birds). Medians (horizontal line within the box, labeled), quartiles (top and bottom of box), 0.05 and 0.95 quantiles (tips of
vertical whiskers) and extreme data points (asterisks) are shown for each treatment. Acoustic variation was always higher in the songs of birds
that came from small isolated populations. See text for details on how the measurements were made.
190 V O C A L C O M M U N I C AT I O N

illustrating these comparisons are in Fig. 12.6ad.
To conclude this section, acoustic variation in Fort
Collins songs increased both within and between
birds following the population bottleneck.
12.5 Comparison of acoustic variation in
Fort Collins 2004 and Islands North
Recall that suitable chickadee habitat immediately
north of Fort Collins is found only in isolated habi-
tat patches. Even when regional populations are
large, Islands North populations contain a median
of only two adult males during the breeding season
and a maximum of four (Gammon et al. 2005).
Because black-capped chickadees are a resident
species, I can assume that an adult male in an
Islands North population must have experienced a
limited social environment during the later stages
of his song development with few or no adult male
tutors. If the greater amount of acoustic variation
within 2004 birds resulted from the fact that many
of these birds completed their song development
with few or no adult song tutors, then similar
amounts of acoustic variation should exist within
Islands North birds.
To test this I recorded unbanded Islands North
males during the 2003 and 2004 breeding seasons
using recording and sampling methods identical to
those described above for Fort Collins males. When
a habitat patch was sampled in both 2003 and 2004,
I included songs from only one seasonwhichever
season yielded a larger sample. This ensured that
each bird was represented only once. For each song
included in the sample, I made the same acoustic
measurements as described above. I then computed
a within-bird diversity measure for each bird as
described above. I did not compute a between-
bird diversity measure because the Islands North
area is many times larger than the Fort Collins area
so the comparison would not be valid. I compared
the within-bird diversity values between Fort
Collins 2004 birds and Islands North birds using a
MannWhitney U-test adjusted for ties.
I sampled a total of 21 Islands North birds. For
these data, 12 birds contributed three song types,
five birds contributed two song types, and four
birds contributed one song type. Seventeen birds
were sampled in 2003 from 10 habitat patches,
and the other four were sampled in 2004 from three
different habitat patches. I found within-bird

(a) FtC'03

(b) FtC'03

(c) FtC'04

(d) FtC'04

(e) IsN

(f) Juv

1s 1s 1s

Figure 12.6 Spectrograms illustrating the pattern shown in Fig. 12.5. The ticks on the y axis represent 2, 4, and 6 kHz as in Fig. 12.3. In 2003,
adult Fort Collins chickadees sang with little acoustic variation (e.g. Birds a and b), but after the population bottleneck resulted in smaller
discontinuous populations, adult Fort Collins chickadees in 2004 were more likely to introduce novel song type variants (e.g. Bird c consistently
left off the second half of the bee syllable in his fa-fee-bee) and were more likely to sing multiple song type variants (e.g. Bird d sang two
different versions of low fee-bee). Multiple song type variants were also used by adult chickadees in isolated habitat patches north of Fort Collins
(e.g. Bird es fa-fee-bee song type) and by juvenile chickadees singing near the time of natal dispersal (e.g. Bird fs chick-a-fee-bee song type).

diversity 1 for most (18/21) of the Islands North
birds. The median measure of within-bird diver-
sity in Islands North birds was 1.38, which was not
significantly different from the 1.20 value for Fort
Collins birds in 2004 following the bottleneck
(U 171, P 0.22, MannWhitney U-test, Fig.
12.5a, Fig. 12.6e). To summarize, acoustic variation
in chickadee song originated in response to both
population bottlenecks in regions of continuous
habitat as well as in small isolated populations.
12.6 Acoustic variation within
juveniles
According to the model of song learning, the vocal
output of juveniles should vary acoustically at the
time of natal dispersal, and juveniles should sing a
few novel song type variants at that time period. To
see if this was the case for black-capped chickadees
in Fort Collins, I sampled songs from four solitary
juvenile chickadees at three separate study sites
around the time of natal dispersal in late June and
early July 2003. Each juvenile was recorded the day I
first observed an individual in a study site, presum-
ably soon after or during its dispersal. I recognized
juveniles because they sing with lower amplitude
and more structural variability in their fee-bees, gar-
gles, and chick-a-dee calls. Further details on identifi-
cation and recording methods are provided in
Gammon et al. (2005). Each juvenile contributed
between four and 45 songs to my sample. All four
juveniles used several variants of each song type
(Fig. 12.6f), and at least one of these song type vari-
ants was not shared by the adults recorded at that
study site. I also sampled several novel song type
variants in each of two chickadee family groups a
day or two prior to their natal dispersal. Baker et al.
(2003) also found that juvenile song was highly
variable in black-capped chickadees, and similar
findings have been reported for other songbird
species (Marler and Peters 1982; Tchernichovski et al.
2001). Thus, dispersing juveniles probably have the
capacity to introduce cultural innovations into a
population if selective retention does not occur.
12.7 Ages of singing adults in 2004
If song development is age-limited in chickadees,
then the novel song type variants recorded in 2004
A C O U S T I C VA R I AT I O N I N B I R D S O N G 191
should have been more likely to come from birds
that hatched in 2003 (i.e. SY birds), whereas 2004
ASY (i.e. those hatched prior to 2003) birds should
have been less likely to introduce novel song type
variants because they became adults prior to the
bottleneck.
To test this, I collected recordings in and around
Fort Collins during the breeding season of 2004.
After recording each birds repertoire using the
same sampling procedure described above, I
captured the bird by luring it into a mist net with
playback, and classified the bird as a SY or ASY bird
through observation of its outer tail feathers (Pyle
1997). For each song included in the sample, I made
the same acoustic measurements as described
above. I then computed a within-bird diversity
measure for each bird as described above, and I also
computed a novelty score that measures the
proportion of the birds songs that were novel song
type variants in 2004. By novel, I mean that no
bird recorded at that study site in 2003 ever gave a
song that would be classified as the same song type
variant. Novelty scores were averaged across song
type to get a single novelty score for each bird
sampled. If a bird received a novelty score of 0.5,
then half of songs uttered by that bird were novel
song type variants in 2004.
Eight birds were sampled from five study sites
(Table 12.1). Five of these birds were aged as SY
birds, and the other three were aged as ASY birds.
Within-bird diversity values were high for all but
one of the birds (an ASY bird), and novelty scores
were high for about half of the birds (Table 12.1). All
five SY birds sang a novel song type variant
(i.e. novelty score 0), but only one of the three
ASY birds sang a novel song type variant. Given
the small sample size, the results are suggestive but
not conclusive.
12.8 Synthesis of empirical results
To summarize all of these studies, greater acoustic
variation existed for adult black-capped chickadees
in small, isolated populations (Islands North and
2004 Fort Collins) than in large contiguous popula-
tions (2003 Fort Collins). Prior to a population
bottleneck in late 2003, the songs of Fort Collins
chickadees were remarkably stereotyped, but
acoustic variation both within and between birds
192 V O C A L C O M M U N I C AT I O N

Table 12.1 Information about the songs of eight Fort Collins birds aged during the 2004 breeding season

Bird Site Song types Age Within-bird Novelty

diversity score

Wuss Dixon 3 ASY 1.00 0.00

Boss Cem 2 ASY 1.32 0.00
Buck Poudre 3 SY 1.41 0.03
Joey Zimdahl 3 SY 1.41 0.03
Jared Poudre 3 SY 1.59 0.30
Red Poudre 3 SY 1.32 0.33
Ventura Poudre 2 ASY 1.52 0.40
Anthony WSpCrk 3 SY 1.87 0.67

Birds with a high score for within-bird diversity used multiple variants of each song type, and birds with a
novelty score 0 used novel song type variants not found at that site in 2003.

increased substantially following the bottleneck.
Juvenile chickadees sang novel song type variants
at the time of natal dispersal, and SY birds recorded
at several Fort Collins study sites in Spring 2004
often used novel song type variants not previously
recorded from adults at that study site. Thus it
appears that Fig. 12.2d best represents what occurs
for developing juveniles that disperse into small
isolated populations.
12.8.1 Potential explanations
At least three explanations could account for these
data. The first is that these data represent simply a
sampling artifact and that the 12 chickadees
recorded in 2003 do not accurately represent the
overall population. Because I sampled unbanded
birds, it is also possible that the 2003 sample may
contain mostly ASY birds with fully crystallized
songs whereas the 2004 sample may have
contained mostly SY birds with songs retaining
some plasticity. Given that 35 to 45% of the Fort
Collins populations were SY birds before and after
the bottleneck (M. C. Baker, unpublished data),
however, this possibility seems unlikely.
Another potential explanation is that small,
isolated habitats are more likely to attract lower-
quality individuals and that these individuals may
have a more plastic song structure. Christie et al.
(2004) showed that male black-capped chickadees
of low quality possess a more variable frequency
interval between whistled notes than males of
higher quality. It is unlikely for my study that all
2004 Fort Collins individuals were of low quality,
however, because there was no suitable habitat
nearby other than Fort Collins for higher quality
individuals to disperse. Furthermore, a recent
study failed to show any link between the quality
of male black-capped chickadees and the quality of
the habitat into which they dispersed (van Oort and
Otter 2005).
A third explanation for these patterns is that the
postdispersal social environment had an effect on
the song development of young chickadees. This
explanation is consistent with data from this
chapter and with data from previous studies in
song learning (McGregor and Krebs 1989; Nelson
and Marler 1994; Nordby et al. 2001; Chapter 11).
Juveniles dispersing into large contiguous popula-
tions should discard novel song type variants so
that the acoustic structure of each song type
becomes stereotyped within and between adult
birds, whereas juveniles dispersing into small
isolated populations should be more likely as
adults to retain multiple song type variants, some
of which are novel to that population.
12.8.2 How postdispersal social environment
may affect song development
Although a relationship between postdispersal
social environment and song development appears
likely in black-capped chickadees, the mechanism
of such a relationship remains unclear. What

aspects of a birds social environment following
dispersal would affect the amount of acoustic
plasticity during its song development? According
to the model of song learning presented earlier
(Fig. 12.1), acoustic plasticity in a young birds song
type gradually decreases throughout development.
This reduction in plasticity may occur as a develop-
ing bird discards song type variants not shared
with its adult neighbors (McGregor and Krebs
1989). Song sharing among neighbors is often
adaptive (Beecher et al. 1997; Molles and
Vehrencamp 2001), which results in juveniles that
selectively retain song type variants that best match
their adult neighbors (Nelson and Marler 1994;
Nordby et al. 2001).
I hypothesize that a juveniles tendency to retain
shared song type variants is related to the amount
of social pressure to conform faced by that juvenile.
The magnitude of social pressure to conform likely
varies within and between songbird species. When
social pressure is high, an individual retains only
those song type variants that are shared with its
adult neighbors, but when social pressure is low, an
individual retains greater plasticity in the acoustic
structure of its song types. Brown and Laland
(2002) used a similar explanation to explain the
origin of cultural innovations in strategies used by
guppies to escape predators.
Social pressure within a population might mani-
fest itself to a developing bird in many ways, such
as the number of its adult neighbors, its spatial
proximity to these neighbors, and the number of
countersinging interactions involving the young
bird or overheard by the young bird. Any or all of
these factors might play a role. In the 2004 Fort
Collins and Islands North populations, chickadees
experienced fewer adult neighbors, greater spatial
isolation, and fewer countersinging interactions
(unpublished data), and this may explain why the
acoustic structure of their song types never became
fully stereotyped. If countersinging interactions
indeed have an effect on the level of song plasticity,
it would be interesting to compare in an adult the
amount of acoustic variation present during a
countersinging interaction involving that bird
versus the amount of variation present during its
broadcast singing (e.g. during the dawn chorus). It
would also be interesting to compare songs
A C O U S T I C VA R I AT I O N I N B I R D S O N G 193
recorded from young males before and after coun-
tersinging interactions to see if song plasticity
decreases. In their studies of song development in
zebra finches (Taeniopygia guttata), lveczky et al.
(2005) found that acoustic variation in juveniles had
a neurological basis. After they inactivated a partic-
ular group of neurons located in the basal ganglia
of the songbird brain, variation in the vocal output
of juveniles decreased. The neural circuits involved
in song learning are plastic to some degree
(Brenowitz and Beecher 2005) and may rewire
themselves in response to particular social inter-
actions. Perhaps countersinging interactions stimu-
late the inactivation of the neural circuits of the
basal ganglia in a developing bird, thus resulting in
decreased song plasticity, although this idea has not
been tested.
12.8.3 Future studies needed
Because human activities often fragment songbird
habitat, resulting in isolated habitat patches with
smaller population sizes (Vitousek 1994), there are
plenty of opportunities to test the effects of isola-
tion and population size on song learning in future
observational studies. It is also possible to manipu-
late a young birds social environment in field and
laboratory populations during the later stages of
song learning, and then monitor closely the sub-
jects song development as it proceeds. In a labora-
tory experiment with song sparrows (Melospiza
melodia), Nordby et al. (2000) placed young males in
contact with four adult sparrows for several
months following the age typical of natal dispersal
in sparrows. In accordance with the model, acoustic
variation within the young birds decreased until
their songs became stereotyped and matched the
songs of their adult tutors. This type of study could
be extended by varying the number of adult tutors
later in development, by measuring the counter-
singing interactions between birds, by considering
acoustic variation both within and between the
song types of birds and by tracking developmental
changes more closely (e.g. Tchernichovski et al.
2004). Perhaps in some cases a juvenile requires
only a single tutor song to learn accurately and pre-
cisely, and novel song will arise only in the absence
of any social tutors. This alone may account for
194 V O C A L C O M M U N I C AT I O N
some of the novel song found in Islands North and
2004 Fort Collins birds considering that some of
these birds possessed no singing neighbors during
the dawn chorus in which they were recorded.
12.9 On the origin and maintenance of
acoustic variation in birdsong
12.9.1 Acoustic variation across space and
time in Parids
Socially learned vocalizations vary across space
and time for most songbirds (Catchpole and Slater
1995) and for Parids in particular (Hailman 1989).
Although the songs of Parids usually vary geo-
graphically, within a local population conspecific
neighbors often share song types (e.g. blue tit,
Thielcke 1969; great tit, Gompertz 1961; McGregor
and Krebs 1989; willow tit, Haftorn 1993; and tufted
titmouse, Schroeder and Wiley 1983), thus showing
a tendency towards cultural conformity. Kroodsma
et al. (1999) found extensive cultural conformity in
the acoustic structure of the fee-bee song of the
black-capped chickadee throughout much of North
America, yet they also sampled populations con-
taining variant song. These populations existed in
geographically isolated regions such as the islands
off the coast of Massachusetts. The data from this
chapter suggest that novel song type variants such
as these are more likely to originate in small, iso-
lated populations. Perhaps the variant populations
of Kroodsma et al. (1999) began as small founder
populations, which facilitated the fee-bee song to
diverge from its typical acoustic form. I predict that
novel song type variants are also likely to be found
in other isolated populations of black-capped
chickadees across North America not yet examined
(e.g. isolated urban areas in the Great Plains).
12.9.2 Development of song in Parids
The development of song in Parids has been stud-
ied less frequently than variation in adult song.
Haftorn (1993) monitored vocal development in the
field for the willow tit. He found that acoustic vari-
ation decreased over developmental time for all
learned vocalizations, but he provided only limited
detail regarding the acoustic structure of the
resulting vocalizations. Investigators in the labora-
tory audio-tutored fledgling black-capped chicka-
dees (Shackleton and Ratcliffe 1993; Kroodsma et al.
1995; K. A. Otter unpublished data) and fledgling
Carolina chickadees (Kroodsma et al. 1995), and
then monitored subsequent vocal development. For
both species, high acoustic variation was found
within juvenile song during early developmental
stages, just as I found for juveniles in the field. This
variation decreased over developmental time until
the songs of males that were raised in the same
group converged in acoustic structure (Shackleton
and Ratcliffe 1993; Kroodsma et al. 1995).
Interestingly, some of the acoustic features distin-
guishing the songs of adult black-capped chicka-
dees in Fort Collins from typical fee-bee song
(e.g. introductory syllables, novel amplitude
breaks, and syllable recombination) also arose in
the songs of black-capped chickadees reared in the
laboratory with a limited social environment
(Shackleton and Ratcliffe 1993; Kroodsma et al.
1995; K. A. Otter unpublished data), suggesting
that similar developmental mechanisms may be
involved. Similar acoustic variants have also been
found in the songs of adult black-capped chicka-
dees in islands near Massachusetts (Kroodsma et al.
1999), Ontario (Christie et al. 2004), and several
other continental locations (unpublished data).
12.9.3 Does the possession of novel song
material affect reproductive fitness?
One remaining question is whether retaining novel
song type variants as an adult would affect the
reproductive fitness of a male. The fact that con-
formity in the fee-bee song is maintained within
large contiguous populations (Kroodsma et al. 1999;
data from 2003 Fort Collins chickadees) suggests
that conformity may be adaptive. Conformity in
song structure could be adaptive in at least two
ways: (i) conformity allows males to match the
songs of their opponents during countersinging,
thus signaling an increased likelihood of escalation,
and (ii) females could respond preferentially to
song that conforms to a local pattern (e.g. Searcy
et al. 2002). With regard to the first possibility,
male chickadees in Ontario responded differently
to playback of acoustically matching versus

non-matching song (Chapter 14), although Fort
Collins chickadees did not discriminate between
matching and non-matching playback in a similarly
designed study (unpublished data).
With regard to the second possibility, Ratcliffe
and Otter (1996) found that female black-capped
chickadees responded with fewer copulation solici-
tations to playback of novel song material such as
an irregular frequency interval between fee and bee.
In a similar study, Baker et al. (1987) found that
female great tits solicited fewer copulations in
response to unfamiliar versus familiar song types.
It would be interesting to know if female chicka-
dees in the Fort Collins area also discriminate
against novel song material. Perhaps females in
small isolated populations discriminate less than
females in large contiguous populations, particu-
larly if females must also learn songs in order to
discriminate among males. Females in isolated
populations may learn multiple song variants and
accept males that produce these, rather than typical
stereotyped song.
12.9.4 Implications for the origin and
maintenance of dialects and repertoires
The existence of dialects (e.g. Nelson et al. 2004) and
repertoires of song types (e.g. Krebs and Kroodsma
1980) are well documented for many songbird
species, but we have only a limited understanding
of what causes a new dialect or a new song type to
originate. The data from this chapter suggest that in
small, isolated populations the acoustic plasticity in
the vocal output of young birds fails to become
stereotyped acoustically as adults. Thus, popula-
tion bottlenecks and separation of populations into
isolated subpopulations could result in the intro-
duction of novel song material. Conversely, when
populations remain large and contiguous, novel
song material should be less likely to originate. The
introduction of novel song type variants could
result in acoustic divergence that eventually leads
to new dialects and song types. Through investi-
gating how the postdispersal social environment
affects song development, we can gain greater
insight into the mechanisms of acoustic divergence
and a greater understanding of cultural evolution
in general.
A C O U S T I C VA R I AT I O N I N B I R D S O N G 195
Acknowledgments
Thanks to Mike Baker for advice during my Ph.D.
studies at Colorado State University. David Logue,
Don Kroodsma, John Tipton, Ken Otter, Dan
Mennill, and Chris Sturdy provided ideas, criti-
cisms and fruitful discussion. Land access for
recording chickadees was provided by the Belinski,
Lesser, Martin, McGraw, McGrew, Turek, and
Zimdahl families, and by Phil Carpenter, Tinka
Greenwood, and Jan Kollar. Michelle Bartz, Alice
Campbell, Nicole Ernst, Jean Hans, Sarah Niemuth,
Derek Perry, Jessica Prada, Kerry Robison and sev-
eral students from the CSU Ornithology class
helped with audio recordings and other fieldwork.
I was supported during much of this research by a
graduate research fellowship from the National
Science Foundation.
References
Baker, M. C., Baker, M. S. A., and Gammon, D. E. (2003).
Vocal ontogeny of nestling and fledgling black-capped
chickadees (Poecile atricapilla) in natural populations.
Bioacoustics, 13, 265296.
Baker, M. C., McGregor, P. K., and Krebs, J. R. (1987).
Sexual response of female great tits to local and distant
songs. Ornis Scandinavica, 18, 186188.
Beecher, M. D., Nordby, J. C., Campbell, S. E., Burt, J. M.,
Hill, C. E., and OLoghlen, A. L. (1997). What is the
function of song learning in songbirds? In: Owings, D.
H., Beecher M. D., and Thompson, N. S., eds.
Perspectives in Ethology, Vol. 12, pp. 7797. Plenum
Press, New York, New York.
Brenowitz, E. A. (1997). Comparative approaches to the
avian song system. Journal of Neurobiology, 33, 517531.
Brenowitz, E. A. and Beecher, M. D. (2005). Song learning
in birds: diversity and plasticity, opportunities and
challenges. Trends in Neurosciences, 28, 127132.
Brown, C. and Laland, K. N. (2002). Social learning of a
novel avoidance task in the guppy: Conformity and
social release. Animal Behaviour, 64, 4147.
Catchpole, C. K. and Slater, P. J. B. (1995). Birdsong:
Biological Themes and Variations. Cambridge University
Press, Cambridge.
Christie, P. J., Mennill, D. J., and Ratcliffe, L. M. (2004).
Pitch shifts and song structure indicate male quality in
the dawn chorus of black-capped chickadees. Behavioral
Ecology and Sociobiology, 55, 341348.
Gammon D. E. and Baker, M. C. (2004). Song repertoire
evolution and acoustic divergence in a population
196 V O C A L C O M M U N I C AT I O N
of black-capped chickadees. Animal Behaviour, 68,
903913.
Gammon, D. E., Baker, M. C., and Tipton, J. R. (2005).
Cultural divergence within novel song in the
Black-capped chickadee (Poecile atricapillus). Auk, 122,
853871.
Gompertz, T. (1961). The vocabulary of the great tit. British
Birds, 54, 369418.
Haftorn, S. (1993). Ontogeny of the vocal repertoire in the
willow tit, Parus montanus. Ornis Scandinavica, 24,
267289.
Hailman, J. P. (1989). The organization of major vocaliza-
tions in the Paridae. Wilson Bulletin, 101, 305343.
Krebs, J. R. and Kroodsma, D. E. (1980). Repertoires and
geographical variation in bird song. In: Rosenblatt, J. S.,
Hinde, R. A., Beer, C., and Busnel, M. C., eds. Advances
in the Study of Behavior, Vol. 11, pp. 134177. Academic
Press, New York, New York.
Kroodsma, D. E. (1974). Song learning, dialects, and dis-
persal in the Bewicks Wren. Zeitschrift fr
Tierpsychologie, 35, 352380.
Kroodsma, D. E. and Baylis, J. R. (1982). Appendix: A
world survey of evidence for vocal learning in birds. In:
Kroodsma, D. E. and Miller, E. H., eds. Acoustic
Communication in Birds, Vol. 2, pp. 311337. Academic
Press, New York, New York.
Kroodsma, D. E., Albano, D. J., Houlihan, P. W., and Wells,
J. A. (1995). Song development by black-capped
chickadees (Parus atricapillus) and Carolina chickadees
(P. carolinensis). Auk, 112, 2943.
Kroodsma, D. E., Byers, B. E., Halkin, S. L., Hill, C., Minis,
D., Bolsinger, J. R., Dawson, J. A., Donelan, E.,
Farrington, J., Gill, F. B., Houlihan, P., Innes, D., Keller,
G., Macaulay, L., Marantz, C. A., Ortiz, J., Stoddard, P.
K., and Wilda, K. (1999). Geographic variation in black-
capped chickadee songs and singing behavior. Auk, 116,
387402.
Marler, P. and Peters, S. (1982). Subsong and plastic song:
Their role in the vocal learning process. In: Kroodsma,
D. E. and Miller, E. H., eds. Acoustic Communication in
Birds, Vol. 2, pp. 2550. Academic Press, New York,
New York.
Marler, P. and Tamura, M. (1964). Culturally transmitted
patterns of vocal behavior in sparrows. Science, 146,
14831486.
McGregor, P. K. and Krebs, J. R. (1989). Song learning in
adult great tits (Parus major): Effects of neighbours.
Behaviour, 108, 139159.
McGregor, P. K., Dabelsteen, T., Shepherd, M., and
Pedersen, S. B. (1992). The signal value of matched
singing in great tits: evidence from interactive playback
experiments. Animal Behaviour, 43, 987998.
Molles, L. E. and Vehrencamp, S. L. (2001). Songbird
cheaters pay a retaliation cost: evidence for auditory
conventional signals. Proceedings of the Royal Society of
London, Series B, 268, 20132019.
Mountjoy, D. J. and Lemon, R. E. (1995). Extended song
learning in wild European starlings. Animal Behaviour,
49, 357366.
National Audubon Society (2002). The Christmas Bird
Count Historical Results [Online]. Available http://
www.audubon.org/bird/cbc [accessed 3 June 2005].
Nelson, D. A. (2000). Song overproduction, selective attri-
tion and song dialects in the white-crowned sparrow.
Animal Behaviour, 60, 887898.
Nelson, D. A. and Marler, P. (1994). Selection-based learn-
ing in bird song development. Proceedings of the National
Academy of Sciences, USA, 91, 1049810501.
Nelson, D. A., Hallberg, K. I., and Soha, J. A. (2004).
Cultural evolution of Puget Sound white-crowed spar-
row song dialects. Ethology, 110, 879908.
Nordby, J. C., Campbell, S. E., and Beecher, M. D. (2001).
Late song learning in song sparrows. Animal Behaviour,
61, 835846.
Nordby, J. C., Campbell, S. E., Burt, J. M., and Beecher,
M. D. (2000). Social influences during song development
in the song sparrow: a laboratory experiment
simulating field conditions. Animal Behaviour, 59,
11871197.
Nowicki, S., Peters, S., Searcy, W. A., and Clayton, C.
(1999). The development of within-song type variation
in song sparrows. Animal Behaviour, 57, 12571264.
Nowicki, S., Searcy, W. A., and Peters, S. (2002). Brain
development, song learning and mate choice in birds: a
review and experimental test of the nutritional stress
hypothesis. Journal of Comparative Physiology A, 188,
10031014.
lveczky, B. P., Andalman, A. S., and Fee, M. S. (2005).
Vocal experimentation in the juvenile songbird requires
a basal ganglia circuit. PLoS Biology, 3, e153.
Pyle, P. (1997). Identification Guide to North American Birds.
Part I. Slate Creek Press, Bolinas, California.
Ratcliffe, L. and Otter, K. (1996). Sex differences in song
recognition. In: Kroodsma, D. E. and Miller, E. H.,
eds. Ecology and Evolution of Acoustic Communication in
Birds, pp. 339355. Cornell University Press, Ithaca,
New York.
Schroeder, D. J. and Wiley, R. H. (1983). Communication
with shared song themes in tufted titmice. Auk, 100,
414424.
Searcy, W. A., Nowicki, S., Hughes, M., and Peters, S.
(2002). Geographic song discrimination in relation to
dispersal distances in song sparrows. American
Naturalist, 159, 221230.

Shackleton, S. A. and Ratcliffe, L. (1993). Development of
song in hand-reared black-capped chickadees. Wilson
Bulletin, 105, 637644.
Smith, S. M. (1991). The Black-capped Chickadee: Behavioral
Ecology and Natural History. Cornell University Press,
Ithaca, New York.
Stoddard, P. K., Beecher, M. D., and Willis, M. S. (1988).
Response of territorial male song sparrows to song
types and variations. Behavioral Ecology and Sociobiology,
22, 125130.
Tchernichovski, O., Lints, T., Deregnaucourt, S., and
Mitra, P. P. (2004). Analysis of the entire song develop-
ment: methods and rationale. Annals of the New York
Academy of Science, 1016, 348363.
A C O U S T I C VA R I AT I O N I N B I R D S O N G 197
Tchernichovski, O., Mitra, P. P., Lints, T., and Nottebohm,
F. (2001). Dynamics of the vocal imitation process:
how a zebra finch learns its song. Science, 291,
25642569.
Thielcke, G. (1969). Geographic variation in bird vocaliza-
tions. In: Hinde, R. A., ed. Bird Vocalizations, pp.
311341. Cambridge University Press, Cambridge.
Van Oort, H. and Otter, K. A. (2005). Natal nutrition and
the habitat distributions of male and female black-
capped chickadees. Canadian Journal of Zoology, 83,
14951501.
Vitousek, P. M. (1994). Beyond global warmingecology
and global change. Ecology, 75, 18611876.
This page intentionally left blank
 CHAPTER 13
Information and the chick-a-dee
call: Communicating with a
complex vocal system
Jeffrey R. Lucas and Todd M. Freeberg
13.1 Introduction
The chick-a-dee call is one of the most commonly
used, and complex, vocal signals of chickadees
and is given by all members of the genus Poecile.
The complexity of the chick-a-dee call arises not
just from its structural characteristics, but also from
its potential functions in social organization.
Earlier work demonstrated that the call is unusual
because it has a computable syntax that can gener-
ate an open-ended number of unique call types
(e.g. Hailman et al. 1985, 1987; Hailman and Ficken
1986; Ficken et al. 1994). Hypothetically, this
means the call could convey an enormous amount
of information. However, despite two decades since
the generative properties of the call were described,
we know little about how much information is
actually conveyed by this call. In this sense,
Hailman et al. (1987, p. 63) were prescient in
suggesting that the information encoded in these
calls presents a difficult challenge in decoding.
Nevertheless, some progress has been made in
the study of this fascinating system, as we demon-
strate below.
The review is broken into three sections. First, we
describe some general characteristics of chickadee
vocal behavior and some of the major arguments
regarding definitions of communication and
information, as these ideas are important for
interpreting the notions of complexity in the
chick-a-dee call. Second, we review work of the
Hailmans and Fickens on the structural complexity
of chick-a-dee calls in black-capped and Mexican
chickadees. We also review some of our own stud-
ies on the chick-a-dee call of Carolina chickadees, as
well as studies from others on various chickadee
species, all of which are beginning to address
exactly what chickadees might be communicating
when the birds vary the structure of their calls.
Third, we draw some conclusions about chick-a-dee
call complexity and raise the need for comparative
research to elucidate chick-a-dee call evolution and
function.
Most of the work on North American Paridae
vocal behavior has concentrated on chickadee
species. One reason for this concentration is the
large repertoires of diverse vocalizations possessed
by these species (e.g. Hailman 1989; Hailman and
Ficken 1996). The different vocal signals used by
chickadees and related species are believed to
represent different communicative entitiesfor
example, an individual producing fee-bees is
presumably communicating something different
than if it were producing chick-a-dee calls. Even
within the chick-a-dee call itself, structurally differ-
ent chick-a-dee variants (e.g. calls differing in note
composition) likely hold different meanings to
receivers. This raises the question of what is being
communicated about the signaler or the signalers
immediate environmental context. Indeed what,
exactly, is communication?
Most definitions of communication (e.g.
Burghardt 1970, p. 16; Wilson 1975, p. 176; Hailman
1977, p. 52) focus on three parts of communica-
tiona feature (often a signal) of one individual
(the signaler) affects the behavior of another
199
200 V O C A L C O M M U N I C AT I O N
individual (the receiver). However, two major argu-
ments have arisen over the definition. The first
argument relates to whether the signaler primarily
benefits, or the signaler and receiver both benefit,
from the communicative interaction (e.g. Dawkins
and Krebs 1978; Owings and Morton 1998;
Bradbury and Vehrencamp 1998). One can argue
that the target of selection argument is tangential
to the question of how and whether communica-
tion occurs, although clearly it is important to
determining the types of communicative events
that occur (e.g. distinctions between signals and
cues as discussed in Maynard Smith and Harper
2003). The second argument revolves around
the usefulness of the notion of information or
information transfer.
A precise definition of information has proven
difficult to pin down, despite a general under-
standing of the concept. There are two major
viewsone is the view that if communication
involves one individual signaling about some-
thing to another individual, then that about
something is the information. The other view
defines information not in the terminology of
meaning, but mathematically as a measure of
ones freedom of choice when one selects a mes-
sage in the simplest cases, to be measured by the
logarithm of the number of available choices
(Shannon and Weaver 1949, p. 9). Smith (1977,
p. 193) bridges these two ideas nicely by defining
information as an abstract property of entities and
events that makes their characteristics predictable
to individuals with suitable sensory equipment for
receiving the information. Information thus enables
such individuals to make choices (see also
Halliday 1983). In the next section, we attempt to
place these ideas of information in the context of
the chick-a-dee call by discussing the seminal work
on black-capped chickadees by the Hailmans and
Fickens and our work on Carolina chickadees.
13.2 Information and the
chick-a-dee call
13.2.1 Basic note types of chick-a-dee calls
The first detailed investigation of the chick-a-dee
call from the mathematically-based information
perspective was carried out on black-capped
chickadees. Hailman et al. (1985) recorded roughly
3500 calls from at least 20 individuals. The call was
described as being composed of four note types
(see Fig. 13.1 for Carolina chickadee examples).
Two note typesA and Bare relatively pure
tones and span a considerable frequency range. A
notes tend to have a higher peak frequency, with a
short ascending arm followed by an abrupt and
long descending arm (in Carolina chickadees, the
ascending arm is typically much longer than the
descending arm in terms of frequency span). B
notes tend to be relatively lower in frequency and
shorter in duration, and both the ascending and
descending arms are relatively similar in the fre-
quencies they span.1 C notes are harsh sounding
notes with a fairly complex and noisy structure,
with a relatively lower pitch than A or B notes. D
notes have a longer duration that the other three
note types, and are relatively unmodulated in
terms of frequency, with a characteristic harmonic-
like structure when seen in sonagram form.
Hailman et al.s (1985) sample of nearly 3500 calls
resulted in 362 calls that were distinct in note
composition. This large number of unique calls
illustrates one component of chick-a-dee call
complexitythe number of distinct calls (in terms
of note composition) increases with sample size.
This is very different from, for example, the songs
of many songbird species, in which the sampling of
dozens or a few hundred songs will often com-
pletely capture the song repertoire of an individ-
ualthe chick-a-dee call possesses the language-like
feature of being open-ended.
13.2.2 Variability in note types
One aspect of the chick-a-dee complex that needs
more attention is how many notes any one species
actually uses in its callswe cant understand the
call complex completely without understanding its
1
Note that Bloomfield et al. (2003) redefined Carolina chicka-
dee A notes in a series as A, B1, and B2 notes. Given the prece-
dence in the literature, we will define their B1 and B2 notes as
A notes and suggest that only their B3 notes be called true B
notes. Of course, the only way to resolve this issue is to evalu-
ate whether the birds themselves distinguish these notes as
we have defined themsee also Chapter 10.
 THE CHICK-A-DEE CALL 201

kHz
10
A A A A A A A A A
8

(a) 6
4
2

0.2 0.4 0.6 0.8 1.0 1.2 1.4 s

kHz
10
A A A A C C C
8
6
(b)
4
2

0.2 0.4 0.6 0.8 1.0 1.2 1.4 s

kHz
10 A A C D D D
8
(c) 6
4
2

0.2 0.4 0.6 0.8 1.0 1.2 1.4 s

kHz
10 B D D D
8
(d) 6
4
2

0.2 0.4 0.6 0.8 1.0 1.2 1.4 s

kHz
10 A Dh D D D D
8
(e) 6
4
2

0.2 0.4 0.6 0.8 1.0 1.2 1.4 s

kHz
10 A A C D D D D D D D D
8
6
(f)
4
2

0.2 0.4 0.6 0.8 1.0 1.2 1.4 s

Figure 13.1 Sonagrams of Carolina chickadee calls that vary in syntax using A, B, C, and D note classifications. (a) String of A notes. (b) Four
A notes, three C notes. (c) Two A notes, one C note, three D notes. (d) One B note, three D notes. (e) One A note, one hybrid D note, four D
notes. (f) Two A notes, one C note, eight D notes. Sonagrams were generated using Avisoft SASLab Pro with an FFT length of 512, frame 75%,
and Blackman window.
202 V O C A L C O M M U N I C AT I O N
elements. Clearly, virtually all chickadees have
some variant of the A, B, C, D series of primary
note types (Hailman 1989). However, there are
some intriguing species differences. Mountain
chickadees (Bloomfield et al. 2004) and Mexican
chickadees (Ficken et al. 1994) have a common
hybrid note described by Ficken et al. (1994) as an A
running into a D note. We found these notes in
Carolina chickadees (e.g. Fig. 13.1e), but they were
rare enough that we concluded that they were
anomalies. Given that this note occurs in 94% of
mountain chickadee calls analyzed by Bloomfield
et al. (2004), our notion of anomalous notes needs
to be revisited. Interestingly, Mexican chickadees
(Ficken et al. 1994) have, for the most part, lost one
of the four primary notes from their repertoireB
notes are quite rare in their chick-a-dee calls. Also, in
mountain chickadees (Gaddis 1985) C notes and D
notes appear to be a single graded series (see also
Hailman et al. 1985). Thus, for most chickadee
species, it is arguably an open question as to how
many distinct note types occur in the call.
New or hybrid notes notwithstanding, it is clear
that in many species the A, C, and D notes have
several subtypes (Fig. 13.2). The A note in particu-
lar is quite varied. A spectral analysis by Nowicki
and Nelson (1990) showed that A and B notes in
black-capped chickadees grade into each other.
A note variants should therefore grade into each
other as well, but these variants are sufficiently dis-
tinct that Smith (1972) defined at least four different
A-like notes in Carolina chickadees (high see, high
tee, loud tee, lisping tee), and our own analyses of
Carolina chickadee calls (T. M. Freeberg and J. R.
Lucas, unpublished data) support this conclusion
(Fig. 13.2).
C notes also vary. Smith (1972) described at least
two, the chip and chick notes, that were elicited in
different situations: the chip is an aggressive call
usually given in a string without D notes, and the
chick note is a component of the more standard
chick-a-dee call given in a variety of circumstances.
Similarly, Haftorn (1993) suggested that willow tits
have two C-like notes, one used in mobbing calls
and the other in more standard chick-a-dee calls. We
have sonagrams of a third C-like note in Carolina
chickadees that Arch McCallum (personal commu-
nication) called a begging C, which appears
structurally similar to the soft dee described by
Smith (1972).
Smith (1972) defined four different D notes in
Carolina chickadees: dee, broken dee, harsh dee, and
soft dee. Ficken et al. (1994) indicated that D notes in
Mexican chickadees varied from banded (Smiths
dee note) to uniformly noisy (Smiths harsh dee).
Similarly, mobbing black-capped chickadees
employ a noisy variant of the D note (Ficken and
Popp 1996), and female black-capped chickadees
use a broken dee when they solicit food from their
mates (Ficken et al. 1978).
In some cases, there are species differences in the
structure of notes. Introductory notes of most
chickadees are pure tones (Carolina chickadees,
Smith 1972; black-capped chickadees, Ficken et al.
1978; mountain chickadees, Gaddis 1985; willow
tits, Haftorn 1993). However, the A note is a
frequency-modulated trill in Mexican chickadees
(Ficken 1990; Ficken et al. 1994). The D note of
Mexican chickadees is also noisier than its North
American counterparts (Ficken 1990), although as
noted above, noisy D notes are found in a number
of other species as well.
A critical question related to our perception of
note types is whether the birds themselves share
this perception. An acoustical analysis of black-
capped chickadee note types by Nowicki and
Nelson (1990) suggested that they should: A and B
notes are statistically distinguishable from one
another, although they tend to be a part of a graded
series, and C and D notes are quite distinct. Sturdy
et al. (2000) showed that black-capped chickadees
can learn to discriminate between note types more
rapidly than within variants of the same note type,
suggesting that the birds do indeed discriminate
among note types and generalize within note types.
Moreover, the birds behavior was consistent with
the suggestion of Nowicki and Nelson (1990) that
A and B notes are more similar to one another than
to the other note types. This is good news for the
field, although Sturdy et al.s (2000) important con-
tribution needs to be extended to other chickadee
species.
Arguably the most interesting aspect of the chick-
a-dee call complex is that it shares some similarities
to human language (Hailman et al. 1985, 1987;
Hailman and Ficken 1986). As we will discuss
 THE CHICK-A-DEE CALL 203

(a)
Tseet notes, 2 beggingC notes, A note
kHz
10 Tseet C C A
B B

0.2 0.4 s

(b)
Tseet, 3 A notes plus chip (C-variant) string
kHz
10
Ts eet A A A Chip
8
6
4
2

0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 s

(c)
2 A notes, Abrupt T note
kHz
10
A A AT
8
6
4
2

0.2 0.4 0.6 0.8 1.0s

(d)
Rapid D string
kHz
10
8
6
4
2

0.2 0.4 0.6 s

(e)
Harsh D string
kHz
10
8
6
4
2

0.2 0.4 0.6 0.8 1.0 1.2 1.4s

Figure 13.2 Sonagrams of Carolina chickadee calls illustrating note type diversity (partly based on Smith 1972). Sonagrams generated
as in Fig. 13.1.
204 V O C A L C O M M U N I C AT I O N
below, the call system has a rudimentary
syntaxnotes that occur in any given call follow
simple rules of note ordering. In addition to syntax,
the literature on chick-a-dee calls has addressed a
number of other non-syntactical components of
information. We will address these alternative
sources of information first, in part because they
may influence how we think about syntax, or at
least about constraints on syntax.
13.2.3 Signal redundancy
The first component of information we will address
is internal information, or the redundancy in a
signal. Redundancy results from multiple signals, or
multiple components of a signal, encoding similar
information. Theoretically, redundancy increases
the probability that receivers correctly perceive the
information embodied in the signal, although
redundancy also reduces the total amount of infor-
mation that can be encoded in the signal (Bradbury
and Vehrencamp 1998). A more practical aspect of
redundancy is that we can potentially over-interpret
experimental results if we ignore redundant cues.
Freeberg et al. (2003) showed that, in Carolina
chickadees, the spectral structure of the first A, C,
and D notes in a string of similar notes is signifi-
cantly correlated with the note composition in that
call. This suggests that a chickadee might be able to
predict the syntax of the rest of the call even if it
were able to hear only a fraction of that call,
although this statement must be tested. Nowicki
and Nelson (1990) offer a complementary view-
point: single A and B notes in a string of notes tend
to decline in frequency and amplitude (black-
capped chickadees: Hailman et al. 1985; Carolina
chickadees: Freeberg et al. 2003). Chickadees may
be able to use the change in frequency and ampli-
tude as an index of syntax, again without hearing
the entire call.
The statistical analysis of Freeberg et al. (2003)
suggested that we can expect note properties to
change if syntax changes. We need to be careful
about reading anything more complex into the call.
As such, conclusions about chick-a-dee calls could be
premature if spectral analyses fail to correct for syn-
tax (e.g. Nowicki 1989; Mammen and Nowicki
1981; Templeton et al. 2005).
13.2.4 Identity
One kind of information a signal can communicate
is identity. Identity can range from individual to
group to species, although we will limit our discus-
sion to the population level and below.
Signals communicating individual identity are
well established (Bradbury and Vehrencamp 1998),
at least in relatively stable social groups (Slater et al.
2000). In black-capped chickadees, Nowicki (1989)
suggested that the D note plays a special role in
encoding identity and Hailman et al. (1987) sug-
gested that this may be why chick-a-dee calls tend to
be more likely than chance to have at least one D
note in themthe trailing D essentially acts as an
identification flag. More recent work by Charrier
et al. (2004) and Bloomfield et al. (2004) has made
this viewpoint even more intricate. These studies
showed that both mountain chickadees and black-
capped chickadees (and, by extension, other
species) have individually specific introductory
notes in addition to individually specific D notes,
although both studies concluded that the D note
has the highest potential for identity coding.
The implication is that identity coding need not
reside only in the D note, but playback experiments
are needed to resolve this issue.
Mammen and Nowicki (1981) were the first
authors to suggest that flock-level call properties
develop in black-capped chickadees. This possibil-
ity was strengthened by a playback experiment
showing that birds played foreign calls were less
likely to visit a feeder than those played calls of
flock members (Nowicki 1983). Nowicki (1989)
then put five birds together in an aviary flock and
demonstrated convergence in one component of
the D note of the call. However, a potential con-
found of the Mammen and Nowicki (1981) study is
that syntax was not controlled for in the spectral
analysis; indeed, their data suggest that birds from
different flocks tended to have calls with different
syntax. Given that syntax itself affects note struc-
ture (Freeberg et al. 2003), Mammen and Nowickis
(1981) results may have had artifacts of flock-
specific differences in note composition. It is also
possible that the putative flock-level recognition
detected in these studies was actually due to
individual recognition. Nowicki (1989) found a

single trait converging in a single flock in the
laboratory; this is not, however, unequivocal
evidence for convergence among flock members
of a chick-a-dee call structure that marks flock
membership.
There is stronger evidence for population-level
variation in the structure of chick-a-dee calls. For
example, Baker and Logue (2003) were able to
identify the population of origin of 100% of black-
capped chickadees calls based on multitaper
spectral analysis (see Tchernichovski et al. 2000).
Spectrogram cross-correlation was nearly as effec-
tive. Similarly, Freeberg et al. (2003) demonstrated
population-level differences in Carolina chickadees
in both A and D notes. These results mirror the
demonstration of population-specific dialects in the
gargle call of black-capped chickadees (Ficken et al.
1985; Miyasato and Baker 1999).
13.2.5 Syntactical information
There are at least three ways that we can begin to
understand the meaning of the chick-a-dee call
from the perspective of syntactical information. The
first, pioneered by Hailman et al. (1985), is a struc-
tural analysis of syntax per se to determine the hypo-
thetical information that may reside in a signaling
system. The second is a natural-history approach,
documenting calls produced in natural settings and
what behavioral or other contextual correlates exist
(e.g. Smith 1972). The third is an experimental
analysis, using playbacks to test predicted informa-
tion content in the calls (e.g. Freeberg and Lucas
2002; Clucas et al. 2004; Templeton et al. 2005).
13.2.5.1 Syntax
Hailman et al. (1985) measured the amount of infor-
mation that might be conveyed by the chick-a-dee
call system of black-capped chickadees. From
Shannon and Weavers (1949) theory of communi-
cation, a communicative system with four distinct
units (note types) has a maximum uncertainty of
two bits of information (UM log2 N, where
N number of units). The maximum information
in a communicative system occurs when all of
the systems units are used with equal probability.
As is the case with letters in the English language
(e.g. relative use of e vs. x), however, note types nonetheless constrained by its note ordering rules.
THE CHICK-A-DEE CALL 205
in chick-a-dee calls are not used equallyD notes are
far more common. This means that the actual infor-
mation in terms of note use in chick-a-dee calls is
lower than the maximum possible information. The
uncertainty measured for actual use of the different
units of a communication system is referred to as
the zero-order uncertainty, and is calculated as:
U0 Pi (log2 Pi)
where Pi is the probability of each of the i units
occurring in the system. In the case of the chick-a-dee
call of black-capped chickadees, there is indeed a
drop-off from UM to U0. However, a much greater
drop-off in uncertainty occurs when one assesses
the transition probabilities between pairs of notes.
This measure of first-order uncertainty, U1, repre-
sents the uncertainty of a given unit to occur in a
sequence when a previous unit has already
occurred. It is calculated as:
U1 Pij (log2 Pj|i)
where Pij is the probability of the i and j note occur-
ring in the ijth sequence, and Pj|i is the conditional
probability of the j unit occurring given that the
i unit has occurred. For the chickadee call this
analysis would address the ability to predict that,
for example, a D note will follow if a C note occurs
in a call. Hailman et al. (1985) found that there is a
considerable drop-off in information at this level of
uncertaintyif a researcher (and, presumably, a
chickadee receiver) detects one note type in a call,
there is a good probability of predicting what the
next note type will be in the call.
The preceding discussion leads into one of the
other major structural features of the chick-a-dee call.
Notes and pairs of notes do not occur with equal
probability. Instead, the chick-a-dee call obeys rules
of note ordering, a simple form of syntax. In black-
capped chickadees, the two most common call
structures are [A][D] and [B][C][D], with brackets
indicating that the particular note type can occur
more than once. In other words, if the following
notes occurred in a nine-note call, BBCCCDDDD,
they would virtually always (e.g. over 99% of the
time) occur in the order [B][C][D]. Taken together,
the chick-a-dee call represents an interesting case of
an open-ended communicative system that is
206 V O C A L C O M M U N I C AT I O N
In addition to the constraints upon the call
imposed by the note ordering rules, other con-
straints appear to limit the diversity of potential call
structures (Hailman et al. 1987). For example, as the
number of A, B, and C notes increase in a call, the
number of D notes that might occur decreases.
Therefore, there seems to be a constraint on the
overall number of notes that can occur in an
average call. However, calls with extremely large
numbers of D notes are more common than
expected by chance, suggesting that the constraints
on introductory notes are relaxed when calls
contain many D notes (Hailman et al. 1987).
This mathematic approach to the question of
information in the chick-a-dee call was extended to
another species, Mexican chickadees (P. sclateri;
Ficken et al. 1994), and interesting comparative
results emerge. The Mexican chickadee chick-a-dee
call system is open-ended, the C note is more com-
mon than the D note, and the B note is extremely
rare. Notes follow the A-B-C-D note-ordering rule
shared by black-capped chickadees. The most com-
mon call structures were [A][D], [C], and [A], and
calls tended to be shorter in note number than
black-capped chickadee calls. Ficken et al. (1994,
p. 80) indicate that, relative to the chick-a-dee call of
black-capped chickadees, the rarity of B notes
and the shorter note length of calls means that
the Mexican chickadees utterances tend to be
syntactically simpler, although not necessarily
semantically simpler This quote nicely cap-
tures the two approaches to information discussed
earlier. For information as a mathematically-
defined measure, Mexican chickadee calls appear
to convey less information than black-capped
chickadee calls. Mountain chickadee calls also
appear to convey less information than black-
capped or Carolina chickadees because their calls
are substantially shorter (threefour notes/call vs.
sixeight notes/call, respectively; Bloomfield et al.
2004). For information as meaning, however, it is
an open question in these species as to which call
system conveys more information.
Hailman et al. (1987) published an additional
method of evaluating the syntactical properties of
black-capped chickadees calls. They compared
the cumulative number of calls containing at
least some number of A, B, C, and D notes
(a survivorship plot) with the expected cumula-
tive number of notes based on a semi-Markovian
model. A departure from the simple semi-
Markovian expectation implies some meaning in
the note composition of the call beyond a simple
repetition of notes. They found that A notes fit
expectations almost exactly. B notes did not: calls
with three or fewer notes fit expectations whereas
those with four or more B notes were too common.
As with A notes, the probability of repeating a
C note was constant, albeit somewhat less than
expected by chance. The survivorship curve for D
notes departed completely from semi-Markovian
expectations, with too many short-D calls, too few
intermediate-D calls, and too many long-D calls.
Hailman et al. (1987) suggested that this distribu-
tion represented a compound of two or more
separate processes, and potentially separate
syntactical functions.
We repeated Hailman et al.s (1987) analysis with
a preliminary data set of 2153 Carolina chickadee
calls recorded in non-manipulated field settings in
eastern Tennessee (nine sites) and central Indiana
(six sites). The uncertainty measures for Carolina
chickadees for this sample of the field recordings
showed a similar pattern to those reported for
black-capped chickadees (Hailman et al. 1985) and
Mexican chickadees (Ficken et al. 1994), with a
marked reduction between zero-order and first-
order uncertainty (UM 2, U0 1.49, U1 0.63). A
and D notes did not meet semi-Markovian expecta-
tions (Fig. 13.3). Long strings of A notes (six A
notes/calls) were more common than expected by
chance. The survivorship curve for D notes was
qualitatively similar to that of black-capped chicka-
dees: too many calls with a few notes, too few with
a large number of notes (1025), and too many with
a very large number of notes.
We asked whether our chick-a-dee calls met
expectations of Mandlebrots modification of Zipfs
Law (see Hailman et al. 1985). Stated simply, Zipfs
law argues that the frequency of utterances should
be reciprocally related to their frequency rankthe
tenth most common utterance (word in a human
language, call syntax in the chick-a-dee call) should
occur with 1/10th the frequency of the most
common utterance. Human language meets this
criterion, but black-capped chick-a-dee calls do not.
 THE CHICK-A-DEE CALL 207

A notes D notes
100.00 100.00
Cumulative percent of calls

10.00 10.00

1.00 1.00

0.10 0.10

0.01 0.01
0 5 10 15 0 10 20 30 40
No. A-notes/call No. D-notes/call

Figure 13.3 Survivorship plots of A notes and D notes of the Carolina chickadees. These are based on a sample of 2153 calls. The triangles
represent calls in the sample, the line is the predicted survivorship from a semi-Markovian model, based on the transitions between same-type
notes (e.g. in the left panel, the transition probability from A to another A note).

However, black-capped calls do fit a broader

form suggested by Mandelbrot (Hailman et al.
1985). Interestingly, our Carolina chickadees do not
fit Mandelbrots function (Fig. 13.4), at least based
Percent of use

on a least-squares best fit of the data. Nonetheless,
the general increase in cumulative call types with
an increase in the number of calls sampled
indicates that the call system is generative, or
open-ended.
As Hailman et al. (1987) showed in black-capped
chickadees, the probability that a call ends (instead
of continuing with a new note) increases with an
increase in the number of A and C notes
(Table 13.1). In Carolina chickadees, longer strings
of A notes (eightten) are more likely to transition
to C notes whereas shorter strings (onefive) are as
likely to transition to B or D notes. B notes almost
always transition into D notes or end the call.
We need to add a caveat that the differences
between black-capped and Carolina chickadees
could result from differences in the field recording
contexts. Assuming that this caveat does not
generate a bias in our data sets, the results suggest
that Carolina chickadees use long strings of intro-
ductory notes in different ways (with different
meanings?) than black-capped chickadees. It would
be instructive to perform this analysis on mountain
and Mexican chickadees, given the species
differences reported earlier. It would also be
1.0
0.1
1.0 10.0 100.0
Frequency rank
Figure 13.4 Percent use of chick-a-dee variants as a function the
frequency rank (1 most common). Triangles are data from our set
of 2153 calls of Carolina chickadees. Line represents the best fit line:
p i(rk)s, where p percent use, r rank, and i, k, and s are
fit constants (see Hailman et al. 1985).
instructive to see this analysis done on European
tits, particularly the marsh and willow tits, which
are closely related to the North American chicka-
dees (Gill et al. 2005).
13.2.5.2 Context
Studies of correlations between chick-a-dee variants
and behavior are critical because they give us some
insight into the potential for syntactically-mediated
information transfer. Results to date clearly
208 V O C A L C O M M U N I C AT I O N

Table 13.1 Transition probabilities for strings of A, B and C notes in chick-a-dee calls of Carolina chickadees; in each case, the number of
elements in a string of same-type notes is given, followed by the probability that the string ends in another note type or silence (A0, B0, or C0)

AA AB AC AD A0 BB BC BD B0 CC CD C0

1 0.11 0.32 0.36 0.21 1 0.06 0.82 0.12 1 0.81 0.19

2 0.20 0.20 0.29 0.31 2 0.5 0 0.5 2 0.77 0.23
3 0.10 0.22 0.29 0.39 3 0 0.5 0.5 3 0.48 0.52
4 0.08 0.26 0.08 0.58 4 0.33 0.67
5 0.06 0.14 0.28 0.52 5 0.63 0.37
6 0 0.11 0.05 0.84 6 0.36 0.64
7 0 0.11 0.35 0.54 7 0.43 0.57
8 0 0.14 0 0.86 8 0.50 0.50
9 0 0.17 0 0.83
10 0 0.20 0 0.80
11 0 0 1.0 0
1317 0 0 0 1.0

demonstrate that different chick-a-dee variants are
given under different conditions.
The first extensive, though qualitative, study of
this type was published by Smith (1972) on
Carolina chickadees. Smith suggested that different
note types had different meanings. For example,
chip (a C-variant) notes are aggressive calls whereas
chick notes (another C variant) are non-aggressive,
often heard around feeding stations. Haftorns
(1993) study of willow tits demonstrated similar
meaning in the C note, with one variant character-
istic of alarm calls and another typically embedded
in less aggressive calls.
Ficken et al. (1994) suggested that A notes are
given by Mexican chickadees moving in space,
whereas C notes are given in response to a
disturbing stimulus (e.g. when mobbing a screech
owl tape) or when birds change directions. D notes
tend to be given by perched birds. These trends for
A and D notes are similar to those reported by Smith
(1972) for Carolina chickadees. Gaddis (1985) found
that chick-a-dee variants were context specific in
mountain chickadees. For example B notes are
given when birds leave food; A notes are given
when birds fly up, and [A][D] strings are given in
flocks.
There are at least three studies of the syntactical
cues given in black-capped chickadee mobbing
calls. Hurd (1996) suggested that mobbing calls had
more introductory notes than non-mobbing calls
but the same number of C and D notes. Baker and
Becker (2002) showed a similar pattern, with more
B notes and fewer A notes given under more imme-
diate risk (1 m vs. 6 m from a stuffed prairie falcon),
but no difference in the number of C or D notes. In
contrast, Templeton et al. (2005) showed that the
number of D notes correlated strongly with the
intensity of risk represented by different species of
predators. It is not clear why these results are so dif-
ferent, although there were considerable method-
ological differences across the three studies.
In addition to syntactical cues, some cues may be
given by call rate itself, with higher rates indicating
more intense conditions. Black-capped chickadee
mobbing calls, for example, tend to be given at
higher rates under more immediate risk (Baker and
Becker 2002). Carolina chickadee chick-a-dee call
rates are higher when the birds are light-weight
and hungry than when they are heavy or sated
(Lucas et al. 1999)chick-a-dee calls may encode
information about signaler physiological condition.
We (K. Bledsoe and J. Lucas, unpublished data)
have limited data on two Carolina chickadees that
indicate just this: D note fundamental frequency
and duration correlated strongly with changes in
corticosterone levels. These results are consistent
with Owings and Mortons (1998) assessment/
management model of communication, although
clearly we need more extensive studies of this
aspect of the chick-a-dee complex.

13.2.5.3 Playback studies
We can use playback experiments to test implica-
tions about syntactical information derived from
field (or laboratory) observational studies. Here we
focus on recent field-based playback studies
(Sturdy et al. review laboratory-based studies of
perception in Chapter 10). Freeberg and Lucas
(2002) proposed that the C-note (chick variant) was
food related, based on preliminary field observa-
tions. They tested this by broadcasting either C-rich
or D-rich chick-a-dee calls at a temporary seed stand.
Consistent with the hypothesis, birds tended
to come to the stand and take seeds in response to
C-rich calls but never took a seed in response to
D-rich calls. Moreover, the rate of chick-a-dee calling
was significantly higher in playbacks with C-rich
calls than those with D-rich calls. There are at least
two alternative explanations for this result. One is
that the C note is indeed a food-associated note.
The second is that D-rich calls are aggressive calls
that elicit an aggressive reaction by receivers (and,
by comparison, C-rich calls are non-aggressive).
While we cannot distinguish these alternatives with
this experimental design, the results indicate that
chick-a-dee variants vary in their meaning to
receivers.
Templeton et al. (2005) tested the relative function
of black-capped chickadee mobbing calls. They
found that the number of D notes was negatively
correlated with predator wingspan and body
length (smaller, more dangerous, predators elicit
more D notes). Smaller predators elicited D notes
with a narrower band width and more narrowly
spaced overtones. Templeton et al. (2005) used play-
backs of the mobbing calls in the absence of preda-
tors as an important test of the proposed
information embodied in the calls. The birds gave
responses appropriate to the predator that was
being mobbed when the calls were first recorded,
suggesting the calls conveyed some quantitative
index of predation risk.
Finally, Clucas et al. (2004) monitored Carolina
chickadees responses to artificially constructed
calls that varied in both note composition
(AAAACCCC, AAAADDDD, and CCCCDDDD)
and note ordering (AAAACCCC vs. CACACACA,
CCCCDDDD vs. DCDCDCDC). The playback was
repeated in two seasons, spring and fall/winter, to
THE CHICK-A-DEE CALL 209
test for the potential role of seasonal context on
receivers responses to the calls. The experiment
tested whether chickadees respond to manipula-
tion of the two components of syntactical organiza-
tion, note composition and note order, but did not
test any specific hypotheses about the meaning of
chick-a-dee variants. The birds showed no differen-
tial response to calls with atypical note ordering
that varied in note composition (CACACACA vs.
DCDCDCDC). Birds did, however, distinguish
between calls that varied in note composition if the
note order followed the species-typical A-B-C-D
ordering. Season and social context also affected
the birds response to the playbacks. The number of
introductory notes in the responding birds chick-a-
dee calls was affected by note composition in the fall
but not in the spring: AAAACCCC playback calls
elicited A/B-rich responses, and D-rich playback
calls elicited C-rich responses. But this latter
response was evident only when white-breasted
nuthatches and tufted titmice (two dominant het-
erospecifics) were present. In the fall, the number of
D notes in the call was also positively correlated
with the number of birds responding, but this rela-
tionship was positive only when heterospecifics
were not present. Only the number of birds
responding affected the number of D notes in the
spring [note: Table 2 in Clucas et al. (2004) is correct,
but the discussion of this pattern in the text of that
paper and Figure 8 are not correct].
Our results suggest that both note ordering and
note composition affect the information content of
the chick-a-dee complex. In addition, context (season
and presence of dominant heterospecifics) matters,
as predicted by Hailman et al. 1985 (also see Leger
1993; Marler and Evans 1996).
13.3 Conclusions, concessions, and a
call for comparative work
The chick-a-dee call is complex both structurally and
functionally. The structure of chick-a-dee calls can
depend upon numerous characteristics of the
signaler or its contextenergetic state, flock/local
population, sex, feeding behavior, flight behavior,
and presence of avian predators. Thus, the chick-a-dee
call can potentially convey a great deal of
information about the different states, behavioral
210 V O C A L C O M M U N I C AT I O N
probabilities, events, etc. relevant to the signals
sender. Furthermore, chick-a-dee calls of black-
capped chickadees (Hailman et al.1985), Mexican
chickadees (Ficken et al. 1994), and Carolina chicka-
dees (Fig. 13.4) are generative and possess fairly high
levels of uncertainty. Thus, in terms of information
as a mathematical measure of binary choices, call
structural rules result in an information-rich signal-
ing system. In addition, the number of a particular
note type seems to influence acoustic characteristics
and numbers of other notes, which suggests an inter-
esting form of redundancy in these calls. This redun-
dancy may increase a signalers ability to transmit,
and a receivers ability to exploit, a message of a call,
while limiting the total number of different messages
a single call might convey. As we noted earlier, our
claim about chick-a-dee call complexity is by no
means novel to usHailman et al. (1985) first raised
it two decades ago in their work with black-capped
chickadees. In this final section of the chapter, we
draw some conclusions about this complexity and
why it might exist, point out some gaps in our
understanding of the call system, and suggest a need
to make broader comparative analyses of the call
system in other Paridae groups.
A possible driving force for such a complex call
system in chickadees might be their complex and
fairly atypical social structure (at least for temper-
ate zone birds). In late summer and early fall,
chickadee femalemale pairs join other pairs (and
often juveniles) to form a flock with a relatively
stable membership (Ekman 1989; Smith 1991).
Flocks remain together, generally defending their
territory from other flocks or individual intruders,
until the following early spring, when flocks break
up into breeding pairs. Thus, chickadee social
organization changes over the course of a year from
femalemale pairs in the breeding season to larger,
stable social units in the fall and winter. Could it be
that the demands of a complex social structure have
driven the evolution of a complex communicative
system (see Blumstein and Armitage 1997;
Wilkinson 2003)? It is too early to answer this
question definitively for chickadees (our first
concession). And although we still cannot unequivo-
cally state what structurally different calls mean to
the birds themselves (our second concession), some
interesting findings are emerging.
Playback studies in field settings are one of the
strongest ways of testing whether structural vari-
ation in chick-a-dee calls conveys information (oper-
ant conditioning experiments offer an important
complementary approach, see Chapter 10).
Unfortunately, playback studies are relatively rare
for this call system in the Paridae. Those that have
been conducted, however, indicate that chick-a-dee
calls that vary in their note composition and/or in
the structural characteristics of their notes can
influence receiver behavior dramatically. In
Carolina chickadees, receivers respond differently
in a feeding context to calls containing a large
number of C notes relative to calls containing no C
notes and a relatively large number of D notes
(Freeberg and Lucas 2002). In black-capped chicka-
dees, individuals respond differently to playbacks
of chick-a-dee calls of flockmates relative to
chick-a-dee calls of non-flockmates (Nowicki 1983),
and acoustic variation in D note structure is
thought to be the basis for this discrimination
(Mammen and Nowicki 1981; although see our
caveat about these studies described above).
Playbacks of calls recorded in a high threat con-
text of a northern pygmy owl, Glaucidium gnoma,
resulted in more receivers approaching the play-
back speaker and also producing more chick-a-dee
calls, relative to playbacks of calls recorded in a
low threat context of a great horned owl, Bubo
virginianus (Templeton et al. 2005). The results from
these three playback studies in two chickadee
species indicate that variation in chick-a-dee call
structure can potentially convey information about
a feeding context, identity, and degree of threat cor-
responding to predator size.
In terms of general structural characteristics of
the note types and note ordering in chick-a-dee
calls, all of the North American Paridae possess
a chick-a-dee-like call (Hailman 1989), although
work on Baeolophus (titmice) species is needed.
Ficken (2000) indicates that chick-a-dee call note
similarities extend beyond the chickadees and
titmice in North America (even if the chick-a-dee
call itself does not), to include some of the species
that occur in mixed-species flocks with those
Paridae species, including golden-crowned
kinglets, Regulus satrapa, and brown creepers,
Certhia americana.

Many of the European tit species possess a simi-
lar call system (Hailman 1989). Perhaps the most
thoroughly studied European chick-a-dee call
system is that of the willow tit. Haftorn (1993)
describes a long-term study of the major vocaliza-
tions of willow tits in central Norway, including the
si-t call of this species that appears homologous
with the chick-a-dee call. In adults, the call seems to
be a medium range signal for flock members
moving through their territory and often out of
visual contact. The call system thus has a general
function in social cohesion, similar to that of North
American Paridae. It often occurs with two distinct
note types, alarm (zi) notes and spitt notes, in ting together a terrific book and for putting in so
what are defined as mixed vocalizations, and its
structure appears to vary with context (e.g. mixed
calls containing alarm notes are produced more
often in contexts of tits mobbing perched predators
or in surprising or other potentially threatening
situationssee also Haftorn 2000). The pj call is
produced primarily in agonistic contexts such as
when two flocks interact, and is often combined
with the pure-tone introductory notes and/or the
D-like t notes of the si-t call into mixed 223242.
calls.
Hailman (1989, p. 305) argued that Parid vocal-
izations represent one of the most interesting and
theoretically important communication systems
known in the animal kingdom. We agree. We have
to conclude, though, that it is still largely an open
question as to how rich in information this system
may be. Studies aimed at documenting whether
different call structures are produced in different
contexts have been conducted in only a handful of
species. There is a more serious paucity of informa-
tion from playback studies to determine experi-
mentally what different call structures might mean
to the birds themselves. In short, comparative
studies are desperately neededstudies not just of
other members of the Paridae but also of the
penduline tits (Remizidae). We are not yet in a posi-
tion to answer fundamental questions about the
evolution of this call system. For example to what
extent do phylogeny and ecology impact the struc-
ture, and perhaps function, of this call system in
different groups of Paridae? Phylogenies are being
established and clarified, but we dont have
sufficient information about the chick-a-dee call
THE CHICK-A-DEE CALL 211
system to provide a firm answer. We do hope,
however, that our review has been of sufficient
interestand informationto generate more
observational and experimental work to help
elucidate the information-rich nature and evolution
of this call system.
Acknowledgements
We thank Chris Sturdy, Dave Gammon, Ben and
Kerry Fanson, Mark Nolen, Ken Henry, and
Christine Jonason for reading previous versions of
the manuscript. Special thanks to Ken Otter for put-
much effort to get this done.
References
Baker, M. C. and Becker, A. M. (2002). Mobbing calls of
black-capped chickadees: effects of urgency on call
production. Wilson Bulletin, 114, 510516.
Baker, M. C. and Logue, D. M. (2003). Population differ-
entiation in a complex bird sound: a comparison of
three bioacoustical analysis procedures. Ethology, 109,
Bloomfield, L. L., Charrier, I., and Sturdy, C. B. (2004).
Note types and coding in parid vocalizations. II: The
chick-a-dee call of the mountain chickadee (Poecile
gambeli). Canadian Journal of Zoology, 82, 780793.
Bloomfield, L. L., Sturdy, C. B., Phillmore, L. S., and
Weisman, R. G. (2003). Open-ended categorization of
chick-a-dee calls by black-capped chickadees (Poecile atr-
icapilla). Journal of Comparative Psychology, 117, 290301.
Blumstein, D. T. and Armitage, K. B. (1997). Does sociality
drive the evolution of communicative complexity? A
comparative test with ground-dwelling sciurid alarm
calls. American Naturalist, 150, 179200.
Bradbury, J. W. and Vehrencamp, S. L. (1998). Principles of
Animal Communication. Sinauer Associates, Sunderland,
Massachusetts.
Burghardt, G. M. (1970). Defining communication. In:
Johnston, J. W., Jr, Moulton, D. G., and Turk, A., eds.
Advances in Chemoreception, Vol. 1: Communication by
chemical signals, pp. 518. Appleton-Century-Crofts,
New York.
Charrier, I., Bloomfield, L. L., and Sturdy, C. B. (2004).
Note types and coding in parid vocalizations. I: The
chick-a-dee call of the black-capped chickadee (Poecile
atricapillus). Canadian Journal of Zoology, 82, 769779.
Clucas, B. A., Freeberg, T. M., and Lucas, J. R. (2004).
Chick-a-dee call syntax, social context, and season affect
212 V O C A L C O M M U N I C AT I O N
vocal responses of Carolina chickadees (Poecile caroli-
nensis). Behavioral Ecology and Sociobiology, 57, 187196.
Dawkins, R. and Krebs, J. R. (1978). Animal signals: infor-
mation or manipulation? In: Krebs, J. R. and Davies,
N. B., eds. Behavioural ecology: an Evolutionary Approach,
pp. 282309. Sinauer Associates, Sunderland,
Massachusetts.
Ekman, J. (1989). Ecology of non-breeding social systems
of Parus. Wilson Bulletin, 101, 263288.
Ficken, M. S. (1990). Vocal repertoire of the Mexican
chickadee. I. Calls. Journal of Field Ornithology, 61,
380387.
Ficken, M. S. (2000). Call similarities among mixed species
flock associates. Southwestern Naturalist, 45, 154158.
Ficken, M. S. and Popp, J. W. (1996). A comparative ana-
lysis of passerine mobbing calls. Auk, 113, 370380.
Ficken, M. S., Ficken, R. W., and Apel, K. M. (1985).
Dialects in a call associated with pair interactions in the
black-capped chickadee. Auk, 102, 145151.
Ficken, M. S., Ficken, R. W., and Witkin, S. R. (1978). Vocal
repertoire of the black-capped chickadee. Auk, 95,
3448.
Ficken, M. S., Hailman, E. D., and Hailman, J. P. (1994).
The chick-a-dee call system of the Mexican chickadee.
Condor, 96, 7082.
Freeberg, T. M. and Lucas, J. R. (2002). Receivers respond
differently to chick-a-dee calls varying in note compos-
ition in Carolina chickadees (Poecile carolinensis). Animal
Behaviour, 63, 837845.
Freeberg, T. M., Lucas, J. R., and Clucas, B. (2003).
Variation in chick-a-dee calls of a population of Carolina
chickadees, Poecile carolinensis: identity and redundancy
within note types. Journal of the Acoustical Society of
America, 113, 21272136.
Gaddis, P. K. (1985). Structure and variability in the vocal
repertoire of the mountain chickadee. Wilson Bulletin,
97, 3046.
Gill, F. B., Slikas, B., and Sheldon, F. H. (2005). Phylogeny
of titmice (Paridae): II. Species relationships based on
sequences of the mitochondrial cytochrome-B gene.
Auk, 122, 121143.
Haftorn, S. (1993). Ontogeny of the vocal repertoire in the
willow tit Parus montanus. Ornis Scandinavica, 24,
267289.
Haftorn, S. (2000). Contexts and possible functions of
alarm calling in the willow tit, Parus montanus; the prin-
ciple of better safe than sorry. Behaviour, 137, 437449. Nowicki, S. and Nelson, D. A. (1990). Defining natural
Hailman, J. P. (1977). Optical Signals: Animal
Communication and Light. Indiana University Press,
Bloomington, Indiana.
Hailman, J. P. (1989). The organization of the major vocal-
izations in the Paridae. Wilson Bulletin, 101, 305343.
Hailman, J. P. and Ficken, M. S. (1986). Combinatorial ani-
mal communication with computable syntax: chick-a-dee
calling qualifies as language by structural linguistics.
Animal Behaviour, 34, 18991901.
Hailman, J. P. and Ficken, M. S. (1996). Comparative
analysis of vocal repertoires, with reference to chicka-
dees. In: Kroodsma, D. E. and Miller, E. H., eds. Ecology
and Evolution of Acoustic Communication in Birds, pp.
136159. Comstock Publishing Associates of Cambridge
University Press, Ithaca, New York.
Hailman, J. P., Ficken, M. S., and Ficken, R. W. (1985). The
chick-a-dee calls of Parus atricapillus: a recombinant sys-
tem of animal communication compared with written
English. Semiotica, 56, 191224.
Hailman, J. P., Ficken, M. S., and Ficken, R. W. (1987).
Constraints on the structure of combinatorial chick-a-
dee calls. Ethology, 75, 6280.
Halliday, T. (1983). Information and communication. In:
Halliday, T. R. and Slater, P. J. B., eds. Animal Behaviour,
Vol. 2: Communication, pp. 4381. W. H. Freeman and
Company, New York.
Hurd, C. R. (1996). Interspecific attraction to the mobbing
calls of black-capped chickadees (Parus atricapillus).
Behavioral Ecology and Sociobiology, 38, 287292.
Leger, D. W. (1993). Contextual sources of information
and responses to animal communication signals.
Psychological Bulletin, 113, 295304.
Lucas, J. R., Schraeder, A., and Jackson, C. (1999). Carolina
chickadee (Aves, Paridae, Poecile carolinensis) vocaliza-
tion rates: effects of body mass and food availability
under aviary conditions. Ethology, 105, 503520.
Mammen, D. L. and Nowicki, S. (1981). Individual differ-
ences and within-flock convergence in chickadee calls.
Behavioral Ecology and Sociobiology, 9, 179186.
Marler, P. and Evans, C. (1996). Bird calls: just emotional
displays or something more? Ibis, 138, 2633.
Maynard Smith, J. and Harper, D. (2003). Animal Signals.
Oxford University Press, Oxford.
Miyasato, L. E. and Baker, M. C. (1999). Black-capped
chickadee call dialects along a continuous habitat corri-
dor. Animal Behaviour, 57, 13111318.
Nowicki, S. (1983). Flock-specific recognition of chick-a-dee
calls. Behavioral Ecology and Sociobiology, 12, 317320.
Nowicki, S. (1989). Vocal plasticity in captive black-
capped chickadees: the acoustic basis and rate of call
convergence. Animal Behaviour, 37, 6473.
categories in acoustic signals: comparison of three meth-
ods applied to chick-a-dee call notes. Ethology, 86, 89101.
Owings, D. H. and Morton, E. S. (1998). Animal Vocal
Communication: a New Approach. Cambridge University
Press, Cambridge.

Shannon, C. E. and Weaver, W. (1949). The Mathematical
Theory of Communication. University of Illinois Press,
Urbana, Illinois.
Slater, P. J. B., Lachlan, R. F., and Riebel, K. (2000). The
significance of learning in signal development: the
curious case of the chaffinch. In: Espmark, Y.,
Amundsen, T., and Rosenqvist, G., eds. Animal Signals:
Signalling and Signal Design in Animal Communication,
pp. 341352. Tapir Academic Press, Trondheim,
Norway.
Smith, S. M. (1991). The Black-Capped Chickadee: Behavioral
Ecology and Natural History. Cornell University Press,
Ithaca, New York.
Smith, S. T. (1972). Communication and other social
behavior in Parus carolinensis. Publications of the Nuttall
Ornithological Club, 11, 1125.
Smith, W. J. (1977). The Behavior of Communicating: an
Ethological Approach. Harvard University Press,
Cambridge, Massachusetts.
THE CHICK-A-DEE CALL 213
Sturdy, C. B., Phillmore, L. S., and Weisman, R. G. (2000).
Call-note discrimination in black-capped chickadees
(Poecile atricapillus). Journal of Comparative Psychology,
114, 357364.
Tchernichovski, O., Nottebohm, F., Ho, C. E., Pesaran, B.,
and Mitra, P. P. (2000). A procedure for an automated
measurement of song similarity. Animal Behaviour, 59,
11671176.
Templeton, C. N., Greene, E., and Davis, K. (2005).
Allometry of alarm calls: black-capped chickadees
encode information about predator size. Science, 308,
19341937.
Wilkinson, G. S. (2003). Social and vocal complexity in
bats. In: de Waal, F. B. M. and Tyack, P. L., eds. Animal
Social Complexity: Intelligence, Culture, and Individualized
Societies, pp. 322341. Harvard University Press,
Cambridge, Massachusetts.
Wilson, E. O. (1975). Sociobiology: the New Synthesis.
Belknap Press of Harvard University Press, Cambridge,
Massachusetts.
This page intentionally left blank
 CHAPTER 14
Status signaling and communication
networks in chickadees: Complex
communication with a simple song
Daniel J. Mennill and Ken A. Otter
14.1 Introduction
Black-capped chickadees produce an extensive var-
iety of calls, including the versatile gargle call
(Chapter 11) and the namesake chick-a-dee call
(Chapter 13). In contrast to these complex calls, the
song of black-capped chickadees demonstrates a
remarkable simplicity. Males sing a tonal, two-note
phrase: fee-bee1 (Fig. 14.1a). The fine structure of the
chickadee song is highly conserved across the
species range throughout North America, with
noteworthy exceptions described in a few isolated
populations (Hailman 1989; Kroodsma et al. 1999;
Gammon and Baker 2004; Chapter 12). Although
the black-capped chickadee song is simple, young
males inherit songs culturally, and nestlings raised
in absence of adult tutors do not develop normal
adult song (Kroodsma et al. 1995). In this chapter,
we explore the ways in which male black-capped
chickadees use this simple, learned song to achieve
remarkably complex forms of communication.
After a brief description of the ways in which male
chickadees vary their songs over time, we evaluate
1
Several mnemonics have been used to describe the chicka-
dees two-note song. Odum (1941) described the song as phoebe,
while Desfayes (1964) suggested dee-dh. Brewer (1961) and
then Ficken et al. (1978) opted for the more intuitive spelling of
fee-bee. Kroodsma et al. (1999) suggest the mnemonic hey sweetie,
which nicely describes the amplitude break in the second half of
the chickadee song but also suggests that male song is directed
at females, which we know to be only half of the singing males
audience. Among these options, we favor fee-bee, which is easily
extended to fee-bee-ee when the amplitude break in the second
syllable is of particular interest.
two singing contexts: diurnal countersinging inter-
actions and the dawn chorus. We then evaluate
chickadee singing behavior within the new
communication network model and highlight
recent research on chickadees which has generated
exciting insights into the ecology and evolution of
sexual signaling in songbirds.
14.2 The fee-bee song: Variation
on a two-note theme
In contrast to birds where each individual
possesses a repertoire of song types, male black-
capped chickadees typically have just one song
type. However, male chickadees vary their songs
by transposing the two-note fee-bee up and down a
frequency continuum (Fig. 14.1b; Horn et al. 1992).
Originally, black-capped chickadees were under-
stood to have two song variants: a normal song at
one frequency and a shifted song at another
(Ratcliffe and Weisman 1985; Hill and Lein 1987;
Chapter 10). Today we understand that male
black-capped chickadees sing across a continuous
frequency range of approximately 860 Hz (Horn
et al. 1992; Christie et al. 2004b). Among songbirds,
frequency transposition of an otherwise invariant
phrase is an uncommon strategy, although it does
occur in other species of birds, including the
male songs of stripe-breasted wrens Thryothorus
thoracicus (D. J. Mennill, personal observation) and
eastern whipbirds Phsophodes olivaceous (Mennill
and Rogers 2006). In other songbirds, including
215
216 V O C A L C O M M U N I C AT I O N

(a) fee bee-ee

Amplitude
5.0
Frequency (kHz)
4.5
4.0
3.5
3.0
2.5
0 0.2 0.4 0.6 0.8 1.0
Time (seconds)
(b)
3.7
Frequency (Hz)

3.5

3.3

3.1

2.9
0 100 200 300 400 500 600
3.7
Frequency (Hz)

3.5

3.3

3.1

2.9
0 100 200 300 400 500 600
Number of songs

Figure 14.1 (a) Waveform and sound spectrogram of a black-capped chickadee fee-bee song. The fee note is higher in frequency and contains
a subtle downslurred glissando. The bee note is relatively constant in pitch and contains a very short amplitude break which is audible at close
range, i.e. fee-bee-ee. (b) Frequencies of all songs sung at dawn by two males, arranged along the x-axis in the order they were sung. Males
transpose the fee-bee song across a frequency continuum, singing bouts of song at one frequency and then pitch shifting their song by
intervals 80 Hz. Part b redrawn with permission from The Auk.

European nightingales Luscinia megarhynchos,
Harris sparrows Zonotrichia querula, and Kentucky
warblers Opornis formosus, males emphasize certain
frequency components within their songs
(reviewed in Mennill and Ratcliffe 2004) even
though they do not transpose the entire phrase.
The songs of black-capped chickadees, despite
their simplicity and extreme similarity throughout
most of North America, nevertheless show
substantial variation in fine structure. This vari-
ation mayin conjunction with other vocal cues
(Chapters 10, 11, and 13) aid individual recognition.
Christie et al. (2004a) analyzed nine songs recorded
from each of 46 male black-capped chickadees from
eastern Ontario and measured five fine structural
features: (1) song length, (2) relative length of the fee
note, (3) relative loudness of the fee note, (4) the
frequency ratio of the beginning to the end of the fee
note (also known as the glissando frequency ratio),
and (5) the frequency interval between the fee and
the bee note. All five song features showed more
variation between males than within males.
 S TAT U S S I G N A L I N G A N D C O M M U N I C AT I O N N E T W O R K S
Multivariate analyses demonstrated that the
fine structure of chickadee songs is sufficiently
distinctive to allow individual identification
(Christie et al. 2004a). In a test of laboratory-reared
chickadees, Phillmore et al. (2002) confirmed that
chickadees can indeed discriminate between the
songs of at least eight different males. By using a
sound transmission experiment, Christie et al.
(2004a) demonstrated that these cues of individual
identity persist over long broadcast distances, and
Phillmore et al.s (2002) laboratory test demon-
strated that birds continue to distinguish between
different individuals songs when they are
degraded by distance.
In addition to providing information on singer
identity, the fine structure of black-capped chicka-
dee songs may convey cues of singer quality.
Males do not show rank-related differences in the
fine structural features of their songs (Christie et al.
2004a). However, high-ranking males maintain
more consistent frequency ratios between their fee
and bee notes when singing at low frequencies
(Christie et al. 2004b). Therefore, by listening to an
extended song bout which contains songs sung at
multiple frequencies, a listening chickadee may
be able to identify the singer and also extract cues
to the quality of the singer. In this regard, the abil-
ity to alter song frequency could allow chickadees
to signal individual condition, which is conveyed
via repertoire size in other species of Parids
(McGregor et al. 1981; Lambrechts and Dhondt
1988; Lambrechts 1992). The difference, however,
appears to be in how that information is encoded.
In black-capped chickadees it appears to be the use
of different frequencies and the control of fine
structure across those frequencies, rather than the
absolute number of song type variants, that indi-
cate male quality. Frequency shifting and the ability
to maintain consistent frequency ratios may be
analogous to the ability to regulate and control
strophe length in great tits (Lambrechts and
Dhondt 1988; Lambrechts 1992) or the incorpor-
ation of particular note types into songs (Forstmeier
et al. 2002). As we discuss below, frequency shifting
in chickadees also allows for other signaling
patterns typically associated with repertoires, but it
is important to first investigate the contexts in
which chickadees sing.
217
14.3 Context of singing in chickadees
Black-capped chickadees sing in two primary
contexts: males sing an extended bout of song in the
early morning dawn chorus and males sing during
diurnal song bouts, which are often manifest as
countersinging interactions between multiple
males. Although birds sing throughout the year
(Ficken et al. 1978), singing activity increases
dramatically in late winter when birds break out of
their winter flocks and begin defending territories
against their former flock-mates. In our eastern
Ontario population, where the first egg is typically
laid around April 30, diurnal countersinging inter-
actions are common as early as late February,
especially on sunny days. Pronounced dawn
choruses, on the other hand, do not begin until mid-
April. Both diurnal countersinging interactions and
dawn choruses persist into the breeding season, but
decrease substantially when parents begin offspring
care. Near identical patterns occur in our Northern
BC population, although egg-laying and the onset
of the other activities occur about a week later,
suggesting the influence of photoperiod and
weather on controlling these behaviors (see Chapter
4). Black-capped chickadee communication appears
to operate differently in these two contexts, so we
discuss each context separately. We first discuss
communication during diurnal countersinging
interactions, where the intricacies of chickadee
communication are better understood, and then
discuss communication during the dawn chorus.
14.3.1 Singing context 1: Diurnal
countersinging interactions
Before migratory birds return to North Americas
temperate forest, the quiet of a crisp, sunny spring
morning is often interrupted when a male black-
capped chickadee begins to sing from a high song
post. A moment later, a distant male may respond
with his own songs and the forest becomes the site
of a vocal duel. Intense dyadic countersinging inter-
actions are especially common during the period of
territory establishment and egg-laying (Dixon and
Stefanski 1970). Participants in these interactions are
typically neighboring territorial males (Shackleton
and Ratcliffe 1994), or else territorial males and
218 V O C A L C O M M U N I C AT I O N

interlopers in search of mating opportunities (Smith
1989; personal observations). Contestants typically
exchange songs from a substantial distance from
one another, although countersinging interactions
sometimes escalate to extremely aggressive physical
encounters (Dixon and Stefanski 1970); in the
weeks prior to female fertility, song contests may
escalate to the point where the two males, feet
locked, tumble to the ground in a burst of feathers,
usually with a crowd of observers close at hand.
During countersinging interactions, contestants
vary both the pitch of their songs and rhythm of
their singing relative to their opponent (Fig. 14.2).
Both the relative timing and relative frequency
of contestants songs are salient features of song
contests.
14.3.1.1 Variation in song frequency during
countersinging interactions
Several experimental studies have helped elucidate
the signal function of frequency variation during
diurnal countersinging interactions. Both loop
playback and interactive playback techniques have
been used to simulate the songs of a chickadee
intruding into a male subjects territory. Horn et al.
(1992) broadcast chickadee songs at low, moderate,
or high frequencies (3130, 3380, or 3630 Hz
measured at start of bee note) from a loudspeaker
positioned near the center of the territories of 24
male chickadees. Territorial males responded with
songs that fell within 120 Hz of the frequency of the
playback-simulated intruder (Horn et al. 1992).
Otter et al. (2002) expanded on this approach and

6.0
male 2
male 1 male 1 male 1
5.0

4.0

3.0

0 2 4 6 8 10
6.0
male 2 male 2 male 2
Frequency (kHz)

male 1 male 1
5.0

4.0

3.0

12 14 16 18 20 22
6.0
male 2 male 2 male 2
male 1 male 1 male 1
5.0

4.0

3.0

24 26 28 30 32 34
Time (seconds)

Figure 14.2 Sound spectrogram of a countersinging interaction between two neighboring territorial male black-capped chickadees. The
spectrogram is shown in three consecutive stretches, depicting 34 seconds of countersinging. The two opponents are not frequency matched;
male 1 sings at a frequency approximately 330 Hz lower than male 2. The two birds alternate songs until the final exchange (at second 32)
where male 2 overlaps the song of male 1.
 S TAT U S S I G N A L I N G A N D C O M M U N I C AT I O N N E T W O R K S
gave playback to 24 territorial males using three
different treatments: (1) loop playback of a 3200 Hz
song played every 5 seconds; (2) interactive
playback of a 3200 Hz song played immediately
after every song sung by the territorial male; and
(3) interactive playback of songs that matched the
frequency of the subjects songs (matching accur-
acy: 24 11 Hz) and immediately followed the
subjects songs. These treatments incited increas-
ingly close approaches from the territorial male,
indicating that chickadees perceive frequency
matching, in concert with one-to-one temporal
correspondence, as a threatening signal (Otter et al.
2002). Interestingly, males in treatment 2 often
shifted to frequency match the playbacks, thus
effectively becoming treatment 3 although not
through our intervention; these males showed
heightened levels of response compared to those
that did not frequency match the playback.
Mennill and Ratcliffe (2004c) employed a fully-
interactive approach to engage 81 territorial males
in countersinging interactions with a playback-
simulated intruder. In half of the trials, the simu-
lated intruder matched the frequency of the resident
male (matching accuracy: 7 15 Hz). In the other
half of the trials, the intruder sang at a frequency
346 16 Hz higher than the resident male. All
males who received interactive playback responded
very aggressively to playback, exhibiting closer
average approach distances than had been reported
in any previous study. However, birds who were
frequency matched during playback retreated away
from the loudspeaker and spent more time singing
from a greater distance from the simulated intruder,
indicative of an aversive response (Mennill and
Ratcliffe 2004c). Taken together, these three play-
back studies indicate that frequency variation has
important consequences during countersinging
interactions. Frequency matching during diurnal
countersinging interactions appears to be a directed
signal of aggression and functionally similar to
song-type matching in other birds.
Many birds who sing with a repertoire of discrete
song types communicate aggressive signals by
tactically choosing songs that match their opponents
song type (Vehrencamp 2001). Type matching, as
an aggressive countersinging strategy, has been
219
demonstrated in many birds, including great tits
(Krebs et al. 1981; McGregor et al. 1992). As with
type matching, our analyses of chickadee singing
strategies suggest that frequency matching is a
directed signal of aggression. Thus, the ability to
frequency shift songs compensates black-capped
chickadees for the lack of song-type variation found
in other Parids. Innovative, interactive playback
experiments with repertoire singing birds have
revealed a complex system of graded signals based
on the relative song choice of countersinging birds,
which have helped the understanding of the
evolutionary pressures responsible for the evolution
of repertoires (reviewed in Beecher and Brenowitz
2005). Further research on the subtleties of chickadee
countersinging behavior is needed to answer ques-
tions about the importance of frequency variation
during song contests. For example is high-frequency
singing more or less aggressive than low-frequency
singing, and are changes in song frequency signals of
aggression per se?
14.3.1.2 Variation in song timing during
countersinging interactions
Although frequency variation during diurnal coun-
tersinging interactions is well studied, variation in
song timing is more poorly explored. Detailed stud-
ies of the function of song overlapping require tight
regulation of the timing of signals broadcast during
playback, and only since the proliferation of inter-
active playback software have researchers rigor-
ously applied an experimental approach to field
studies of overlapping. The topic of overlapping of
song was originally studied in association with the
repetitive phrasing of great tit song strophes, which
can lengthen or shorten a song bout. Male great tits
increase variation in song timing (Dabelsteen et al.
1996) and stop songs short (Langemann et al. 2000)
when overlapped by playback. Blue tits show
higher song rates when overlapped (Poesel 2004).
Territorial males respond in like fashion in other,
non-Parid songbirds including nightingales,
European robins Erithacus rubecula (Todt 1981), and
blackbirds Turdus merula (Brindley 1991).
Mennill and Ratcliffe (2004c) used interactive
playback to simulate a singing chickadee who
either overlapped every song given by each
220 V O C A L C O M M U N I C AT I O N
playback subject or avoided overlapping by
singing 1.5 seconds after the playback subjects
song was complete. In response to an overlapping
opponent, territorial males sang significantly more
shortened songs, dropping the bee note from signifi-
cantly more songs when they were overlapped by
an opponent. Furthermore, overlapped males
sang with significantly more variation in the
silent interval between consecutive songs. These
responses of male black-capped chickadees to an
overlapping opponent mirror the responses of
other songbirds to overlapping opponents outlined
above. This cross-taxa similarity of response to
overlapping playback suggests that the very nature
of overlapping, as a signal that masks an oppon-
ents signal, is a more antagonistic countersinging
approach than non-overlapping. Both the increase
in shortened songs and the increase in variable
song timing exhibited by black-capped chickadees
may be strategies used by countersinging birds to
avoid having their songs masked by an opponent.
To further quantify the occurrence of frequency
matching and overlapping during chickadee coun-
tersinging interactions, we transcribed 68 naturally-
occurring song contests heard between March 21
and May 6, 2001 and 2002 (D. J. Mennill, unpub-
lished data). Using a different symbol for each
contestant, we noted the relative pitch and relative
timing of each song by the relative position of the
symbols on graph paper. (One challenge with
documenting song overlap during naturally-
occurring countersinging interactions is that the
observers perception of overlapping signals may
differ from the birds perceptions of those signals
owing to the slow speed of sound propagation
through air. During the transcriptions we describe
here, the observer was typically in relatively close
proximity to the countersinging males, such that
the perception of overlapping likely matched the
perception of overlapping by the counter-singing
chickadees.) From these transcriptions, we extracted
the following variables for each song contest: (1) the
number of song overlaps; (2) whether or not the con-
testants were frequency-matched with one another;
and (3) whether or not the countersinging contest
escalated (as indicated by the contestants approach-
ing each other and giving extended bouts of chick-
a-dee and gargle calls; sample sizes vary depending
on how reliably overlapping and frequency match-
ing could be determined in each contest). Song
contests that escalated tended to contain more song
overlaps (3.9 0.7 overlaps per contest; mean SE)
than song contests that did not escalate (3.0 0.7
overlaps per contest) but this difference was not
significant (Wilcoxon: Z 1.1, P 0.11, N 61).
Frequency matching, on the other hand, showed a
significant relationship with contest outcome:
25 of 32 contests (78%) that escalated contained
frequency matching between the contestants,
whereas only 20 of 36 contests (56%) that did not
escalate contained frequency matching (Fisher exact:
p 0.04; birds were considered to be frequency-
matched if the musically trained transcriber could
detect no difference in their song frequency). These
results mirror those of Shackleton and Ratcliffe
(1994) who found that frequency matching was asso-
ciated with contest escalation in 27 interactions
recorded in 1991. Therefore, observations of natural
contests support the idea that song overlapping and
frequency matching are directed signals of aggres-
sion, important during the diurnal countersinging
interactions of black-capped chickadees. These
results also suggest that song overlapping and
frequency matching serve distinct signal functions.
Mennill and Ratcliffes (2004c) interactive playback
experiment showed that overlapping primarily
influenced the birds singing rhythm and frequency
matching influenced the birds movement behavior.
Our observations of naturally occurring counter-
singing interactions support this idea; song contests
that involved frequency-matching usually resulted
in the opponents approaching one another, whereas
song contests that involved overlapping did not.
14.3.2 Singing context 2: The dawn chorus
In the early twilight before sunrise, when dark tree-
tops can just barely be distinguished from the dark
sky, male black-capped chickadees begin an
extended period of singing. The fee-bee of one male
penetrates the still dawn air, then two more males
join the chorus, and soon the entire neighborhood
comes alive with song. Each male may continue to
sing for as long as 70 min, singing an average of
282 36 songs (Horn et al. 1992; Christie et al.
2004b). Song output during the chorus varies with
 S TAT U S S I G N A L I N G A N D C O M M U N I C AT I O N N E T W O R K S
male dominance status. Males with high-ranking
dominance status begin singing earlier, they sing for
longer, and they sing at a higher rate than their low-
ranking counterparts (Otter et al. 1997). Therefore,
during the chorus, males broadcast cues to their
quality not only through the fine structure of their
songs (see above) but also through song output
(Otter et al. 1997). Male chorus output also reflects
male pairing status. Following experimental
removal of the female, male chorus length
dramatically increases (Otter and Ratcliffe 1993).
During the chorus, males pitch shift their song by an
interval of 80 Hz every 30.7 3.7 songs (Christie
et al. 2004b). The rate of pitch shifting varies dramat-
ically, both between males and between the choruses
from any particular male, where some chorus
performances featuring a pitch shift after nearly
every song while others contain no pitch shifts what-
soever. In general, however, male choruses consist of
bouts of songs at similar frequencies punctuated by
marked changes in frequency (Fig. 14.1b).
Egg-laying female black-capped chickadees sleep
inside their nest cavities, and males typically sing
much of the dawn chorus in close proximity to their
nest (Otter and Ratcliffe 1993; Gammon 2004;
Mennill and Ratcliffe 2004b). Males often pause or
stop singing upon the females emergence from the
nest cavity (Otter and Ratcliffe 1993; Gammon
2004). Upon the emergence of the female from the
nest cavity, males often switch from singing to
giving variable see and gargle calls (Gammon 2004;
personal observation). Both withinpair copulations
(Otter and Ratcliffe 1993; Gammon 2004) and extra-
pair copulations (Smith 1988; Mennill et al. 2004)
commonly follow the end of the dawn chorus.
Based on the observation that males tend to give
their dawn chorus in close proximity to the nest cav-
ity, several authors have suggested that the male
chorus is directed at the female (Otter and
Ratcliffe 1993; Gammon 2004). We encourage a
cautious approach to this interpretation for several
reasons. First, male dawn song is far louder than
necessary to communicate with a female inside the
nest cavity; indeed, males accomplish this task
with the remarkably quiet faint fee-bee vocalization
later in the breeding season (Smith 1991). Instead,
males sing songs at a high amplitude, such that a
human observer listening to the dawn chorus can
221
consistently hear more than one male and often as
many as four males (Hansen et al. 2005). Second,
males may benefit by remaining near their nest
cavity for reasons that are independent of commu-
nication with the female. Most notably, females
often solicit copulations, both withinpair and extra-
pair, upon exiting the nest cavity at dawn. Males
may find an advantage in remaining near the nest
cavity so that they can either copulate with their
partner or mate guard her when she emerges. This
idea could be tested by conducting a pair-wise
comparison of the position of males during the
dawn chorus when their partner is fertile and when
she is not, or by comparing the chorus locations of
high-ranking males (whose females seldom follow a
mixed reproductive strategy) versus low-ranking
males (whose females often follow a mixed
reproductive strategy). Third, males may sing the
dawn chorus near their nest cavity to mask their
partners ability to hear the dawn chorus perform-
ance of neighboring males. Analyses of recordings
made with microphones mounted inside nest boxes
suggest that this sort of masking comes into play in
the dawn chorus of great tits (see below; K. A. Otter,
T. M. Peake, A. M. R. Terry, and P. K. McGregor,
unpublished data).
The interactive nature of chickadees diurnal
countersinging contests is obvious, but the
processes that govern the timing and frequency of
chorusing male chickadees songs are very poorly
understood. Upon hearing the apparent cacophony
of a busy black-capped chickadee chorus, which
includes the dissonant harmonies of multiple song
frequencies and the irregular overlaps and alterna-
tions between many males songs, a human listener
may be inclined to believe that chorus singing is
non-interactive. To test whether the dawn chorus
was interactive, Shackleton and Ratcliffe (1994)
simultaneously recorded three males in neighboring
territories during two mornings of dawn chorus.
They found little evidence for correspondence in the
frequency of songs given by neighboring males.
However, analysis of larger groups of birds over a
much longer periods of time is required to rigor-
ously determine whether song frequency and
timing show any correspondence between neigh-
bors during the chorus. As Burt and Vehrencamp
(2005) have demonstrated using multichannel array
222 V O C A L C O M M U N I C AT I O N
recordings of banded wrens Thryothorus pleurostic-
tus, the dawn chorus can involve interactive behav-
ior with complex processes of tactical song choice.
14.4 Communication networks
Conventionally, animal communication has been
understood as a dyadic process of information
exchange involving one signaler and one receiver: a
songbird may defend his territory by signaling to a
male receiver and he may attract a breeding partner
by signaling to a female receiver (e.g. Kroodsma
and Byers 1999). The dyadic model of communica-
tion is useful for understanding pitch matching and
overlapping during dyadic countersinging contests
of black-capped chickadees (see above). However,
chickadees share two characteristics, in common
with many other songbirds, which are not easily
accounted for within the dyadic model. First, chicka-
dee songs are long-range signals that may convey
information across broad distances to multiple
receivers simultaneously. Second, each breeding
neighborhood of chickadees consists of multiple
males and females who may all benefit by assessing
the quality of their neighbors. A communication
network model, which accounts for multiple
signalers and multiple receivers exchanging infor-
mation simultaneously (McGregor 2005), may
therefore provide an enhanced understanding of
communication in black-capped chickadees in
particular, and in songbirds in general.
Within a communication network, individuals
may transmit information in novel ways that
occur outside of the traditional dyadic model.
Eavesdropping is a network-based receiver behav-
ior, whereby an individual gathers information
from a signaling interaction between conspecifics
without being directly involved in that interaction
(McGregor and Dabelsteen 1996; sensu social
eavesdropping Peake 2005). Eavesdropping on the
diurnal countersinging contests of male songbirds
may facilitate low-cost and direct comparisons of
the relative quality of countersinging contestants.
Female black-capped chickadees, who are genet-
ically promiscuous (Otter et al. 1998; Mennill et al.
2004) and are quick to divorce their partner if a
higher-status male becomes available (Otter and
Ratcliffe 1996; Ramsay et al. 2000), might eavesdrop
on malemale countersinging interactions to evalu-
ate the quality of potential partners. Male chicka-
dees might benefit from eavesdropping on the
countersinging interactions of other combatants;
this information could then be used to adjust his
own willingness to escalate in subsequent inter-
actions with one or the other of these rivals. We
tested these ideas using multispeaker playback and
interactive playback approaches.
14.4.1 Male eavesdropping in black-capped
chickadees
To test whether male black-capped chickadees
eavesdrop, Mennill and Ratcliffe (2004a) used a
multispeaker experiment to evaluate the responses
of territorial males to a countersinging contest
between two simulated intruders. Playback was
given through three loudspeakers arranged in an
equilateral triangle with 24 m between each loud-
speaker. Playback occurred in three stages
(Fig. 14.3a). In stage 1, the territorial male was
attracted to within 5 m of a loudspeaker broadcast-
ing chick-a-dee calls, thereby bringing the male to a
position equidistant from the remaining two loud-
speakers. In stage 2, fee-bee songs were broadcast
from the other two loudspeakers, simulating a
countersinging contest between two unknown
males. The two simulated males sang songs at the
same frequency, the same rate, and the same ampli-
tude; the only difference between the two loud-
speakers was that the songs of one male consistently
overlapped the other (after Naguib and Todt 1997).
During playback, an observer evaluated which
loudspeaker the subject approached first. In stage 3,
a postplayback assay, songs were broadcast from
the loudspeaker that the male did not first approach
in stage 2, to confirm that both loudspeakers were
positioned in such a way as to elicit a territorial
response from the subject.
The responses of territorial males to the
multispeaker playback demonstrated that male
black-capped chickadees do eavesdrop on the
countersinging interactions between others. High-
ranking males preferentially approached the
overlapping loudspeaker (Fig. 14.3b). Because there
were no absolute differences in information
broadcast by the two loudspeakers, only relative
 S TAT U S S I G N A L I N G A N D C O M M U N I C AT I O N N E T W O R K S 223

(a)
Stage 1: Chick-a-dee calls Stage 2: Simulate song Stage 3: Songs broadcast
attract resident male to first contest between speakers from the non-approached
speaker two and three speaker

1 1 1

2 3 2 3 2 3

(b) High-ranking Males Low-ranking Males

1.0 15/16

0.8
playback subjects
Proportion of

0.6 5/10

0.4 3/10
2/10
0.2
1/16
0/16
0.0
Approach Approach Remain Approach Approach Remain
overlapping overlapped at lure overlapping overlapped at lure
speaker speaker speaker speaker speaker speaker

Response to playback

Figure 14.3 (a) Schematic representation of a multispeaker playback experiment designed to test whether male black-capped chickadees
eavesdrop on the countersinging interactions of other males. Stage 2 simulated a countersinging interaction between two males where one bird
consistently overlapped the others songs. (b) High-ranking males preferentially approached the loudspeaker broadcasting overlapping songs,
demonstrating that males eavesdrop on malemale interactions. Reprinted with permission from Behaviour.

information in the form of song overlapping, the
high-ranking males responses indicate that males
extract relative information from rivals counter-
singing interactions. This result adds to a growing
body of research documenting male eavesdropping
in great tits and other species (see Peake 2005 for
review). In contrast to the strong directional
response exhibited by high-ranking male black-
capped chickadees, low-ranking males showed a
mixed response. Although low-ranking males
approached the overlapping loudspeaker most
often, they sometimes approached the overlapped
loudspeaker and, in three cases, approached
neither loudspeaker. These differential responses of
high and low-ranking males support the idea that
responses to conspecific rivals varies with the
quality of the territorial male: high-ranking males,
who are better able to dominate other birds during
physical encounters, preferentially approach a
loudspeaker broadcasting a more aggressive signal.
Future playback studies expanding on this
multispeaker experimental design may shed
insight into the signal function of pitch matching
and pitch shifting behavior, and may even help to
tease apart which signals are most salient to eaves-
droppers.
224 V O C A L C O M M U N I C AT I O N
14.4.2 Female eavesdropping in
black-capped chickadees
Using a modified version of Otter et al. (1999) inter-
active playback study, Mennill et al. (2002, 2003)
engaged male chickadees in countersinging con-
tests with a simulated intruder to test whether
female black-capped chickadees eavesdrop on
malemale song interactions. The experiment
involved playback to groups of four birds: two
pairs of breeding partners in neighboring territo-
ries, where the males had been flock-mates during
the previous winter, one high-ranking and one low-
ranking. Playback was conducted at the onset of
female fertility and occurred in four successive
stages (Fig. 14.4a). In stage 1, one male was
engaged in a 6-min countersinging contest with a
playback-simulated intruder. In stage 2, an hour
later, the other male was engaged in a 6-min coun-
tersinging contest with the same playback-simu-
lated intruder. We used the same catalogue of songs
to interact with both males, but with one male we
simulated an aggressive opponent (one who over-
lapped and pitch-matched all of the subjects songs)
and to the other male we simulated a submissive
countersinging opponent (one who avoided over-
lapping and sang at a frequency 300400 Hz higher
than the subject) (Fig. 14.4b). There were no
absolute differences in the song output of the play-
back between aggressive and submissive trials,
only relative differences between the pitch and tim-
ing of the songs of the resident male and the simu-
lated intruder. Stages 1 and 2 of playback were
repeated to each male on two subsequent days. In
the final two stages of the experiment, we assessed
females responses to playback. In stage 3, a behav-
ioral assay, we followed each pair for 30 min on the
day following playback in the early morning, a
time when chickadee extrapair copulations are
common (Smith 1988; Mennill et al. 2004). In stage
4, a genetic assay, we used microsatellite paternity
analyses to sample the broods of both females for
extrapair offspring.
The genetic assay (stage 4) confirmed that female
black-capped chickadees eavesdrop on malemale
vocal interactions. The proportion of nests contain-
ing extrapair young was significantly greater in the
broods of females paired to high-ranking males
who received aggressive playback, compared to
the broods of females paired to high-ranking
males who received submissive playback or to
males who received no playback (Fig. 14.4c,
Mennill et al. 2002). In other words, after hearing
their high-ranking partner lose a song contest to
an opponent, females paired to high-ranking males
changed from a monogamous mating strategy to a
promiscuous mating strategy. Surprisingly, the
behavioral assay (stage 3) yielded no evidence that
female black-capped chickadees eavesdrop on
malemale song contests; neither female behavior
nor male behavior showed any difference on the
morning following aggressive or submissive play-
back manipulations (Mennill et al. 2002, 2003).
Although no extraterritorial forays were observed
during the observation period, one extrapair copu-
lation was observed outside the observation period.
A female paired to a high-ranking male who had
received aggressive playback had an extrapair
copulation with a low-ranking male who had
received submissive playback (Mennill et al. 2004).
Genetic assignment of extrapair fathers demon-
strated two more cases where females paired to
aggressive-playback high-ranking males had extra-
pair copulations with submissive-playback low-
ranking males. No other study of the black-capped
chickadee mating system (Smith 1988; Otter et al.
1998; Mennill et al. 2004) has documented a female
seeking an extrapair copulation from a low-ranking
male from the same winter flock as her high-
ranking partner. The three cases that followed
Mennill et al.s playback experiment therefore
indicate that eavesdropping on malemale song
contests influences not only the females decision
about whether or not to follow a mixed reproduct-
ive strategy (Mennill et al. 2002) but also whom to
target as an extrapair sire (Mennill et al. 2003).
Females paired to high-ranking male chickadees
are typically genetically monogamous (Otter et al.
1998; Mennill et al. 2004), yet these females increased
the proportion of extrapair young in their broods
after hearing their partner lose an aggressive coun-
tersinging contest. In contrast, females paired to low-
ranking males continued to produce similar
proportions of extrapair young regardless of the
playback treatment given to their partner
(Fig. 14.4c). Why were aggressive playback sessions
 S TAT U S S I G N A L I N G A N D C O M M U N I C AT I O N N E T W O R K S 225

(a)
Stage 1: Playback to first male Stage 2: Playback to neighboring male

High-ranking males territory Low-ranking males territory High-ranking males territory Low-ranking males territory

Stage 3: Observe birds after playback Stage 4: Sample paternity of broods

High-ranking males territory Low-ranking males territory High-ranking males territory Low-ranking males territory

(b) Submissive playback Aggressive playback

4.5
Frequency (kHz)

4.0
3.5
3.0
2.5

0 1 2 3 4 0 1 2 3 4
Time (seconds)

(c) High-ranking Males Low-ranking Males

0.6
12/23
3/6
containing extra-male young

0.5
7/17 4/10
Proportion of nests

0.4

0.3

0.2
1/10 1/10
0.1

0.0
Aggressive Submissive No Submissive Aggressive No
Playback Playback Playback Playback Playback Playback
Playback treatment

Figure 14.4 (a) Schematic representation of an interactive playback experiment designed to test whether female black-capped chickadees
eavesdrop on malemale countersinging interactions. (b) During submissive playback interactions, interactive playback simulated an opponent
(black) who avoided overlapping the subject (white) and sang at a higher frequency than the subject. During aggressive playback interactions,
the playback-simulated intruder overlapped and pitch matched the subject. (c) High-ranking males who received aggressive playback
lost paternity significantly more often than high-ranking males who received submissive playback or no playback. Low-ranking
males lost paternity at equivalent levels regardless of the playback treatment they received. Parts b and c reprinted with permission from
Science.
226 V O C A L C O M M U N I C AT I O N
sufficient to increase the proportion of extrapair
young in the broods of high-ranking males whereas
submissive playback sessions did not reduce the
proportion of extrapair young in the broods of low-
ranking males? In complex systems, Gould (1998)
suggests that a great asymmetry exists between
the perception of constructive and destructive forces,
where the apparent severity of one negative event
outweighs the product of many positive events.
Such an asymmetry may influence the mate choice
decisions of eavesdropping female black-capped
chickadees. Females paired to high-ranking males
are accustomed to observing their partner dominate
contests over food resources throughout the winter
and dominate territorial countersinging interactions
during the breeding season. Therefore, the poor
vocal performance of high-ranking males during
aggressive playback trials was unusual and may
have been sufficiently extraordinary to call into
question previous female assessments. Females
paired to low-ranking males, in contrast, observe
their partner dominate some contests (e.g. with
interlopers of even lower quality) and be dominated
in other contests (e.g. with a higher-ranking neigh-
bor). Consequently, the strong performance of low-
ranking males during the playback manipulated
song contests may not have been outside the normal
experience of females paired to low-ranking males.
Otter et al. (1999) evaluated female eavesdrop-
ping in great tits using a similar interactive play-
back experiment. Two differences between the
great tit studies and those described above for
chickadees may be salient in comparing results. As
great tits do not have cohesive flock membership or
strict dominance hierarchies, males were randomly
assigned to receive aggressive or submissive play-
back during playback interactions. Further, because
great tits do not pitch shift and song type matching
does not appear to have an additive effect to over-
lapping alone (Dabelsteen et al. 1996), overlapping
versus non-overlapping was the primary difference
between aggressive and submissive treatments.
Like the results with chickadees, the evidence
from interactive playback sessions with great tits
suggests that breeding females eavesdrop on the
vocal interactions of males. Female great tits paired
to males who received aggressive playback readily
forayed into the territories of neighboring males
who had received submissive playback, presumably
to assess alternative mating opportunities (Otter
et al. 1999). Genetic analyses demonstrated that
these extraterritorial forays did not, however, trans-
late into extrapair fertilizations (Otter et al. 2001).
Otter et al.s (1999, 2001) experiments with great
tits and Mennill et al.s (2002, 2003) experiments
with black-capped chickadees demonstrate that
female Parids eavesdrop. Both experiments docu-
mented a change in female reproductive activities
following manipulation of male signals. However,
the reproductive activities of females changed in
different ways for these two species. Great tit
females readily forayed into neighboring territories
but did not change their genetic mating strategy,
whereas black-capped chickadee females did not
readily foray outside of their territory and yet they
changed their genetic mating strategy. These differ-
ences may be related to differences in the behav-
ioral ecology of chickadees and tits. Black-capped
chickadees spend the winter in small cohesive
flocks with stable flock membership where inter-
actions follow a strict linear dominance hierarchy
(Smith 1991). In contrast, great tit flocks are larger,
flock membership is transitory, and rank relation-
ships are more labile (Dent et al. 2002). For female
great tits, surrounded by breeding males whose
relative quality is less resolved, eavesdropping may
be a means of initial assessment of male quality,
which females follow up with forays into neigh-
bors territories. If detailed assessments fail to
confirm the information gained through eaves-
dropping, female great tits may forgo extrapair
copulations (Otter et al. 2001). Female black-capped
chickadees, however, are expected to be intimately
familiar with the relative status of all males singing
within earshot. Consequently, information gained
through eavesdropping may be especially import-
ant to female black-capped chickadees when that
information reveals quality differences that contrast
the females previous assessments. Having lost
confidence in her mates status after hearing him
dominated in a song contest with an aggressive
opponent, female chickadees may adopt the next
best strategy of seeking an extra-pair fertilization
from another nearby, high-ranking male (Mennill
et al. 2003). Despite their differences, these
two studies of Parid eavesdropping behavior
 S TAT U S S I G N A L I N G A N D C O M M U N I C AT I O N N E T W O R K S 227

demonstrate that female eavesdropping is an theory. Black-capped chickadees routinely con-

important means of female assessment of male
quality.
14.4.3 Nest cavities and male singing
behavior
Communication network theory suggests that
females should position themselves in order to
maximize assessment of the males around them
(Otter and Ratcliffe 2005). The nesting behavior of
black-capped chickadees provides support for this
struct their nests closer to the edges of their territor-
ies than would be expected by chance (Ramsay
et al. 1999). Nests typically fall within 20 m of
territory edges, despite the large size of chickadee
territories (Fig. 14.5; average territory diameter:
152 27 m; Mennill et al. 2004). Detailed investiga-
tion of food abundance and vegetation features
show no marked differences between nest sites at
territory edges versus comparison sites at territory
centers, suggesting that chickadees nest at territory
peripheries based on conspecific attraction

100m
High

High

Low Low
High

Low

High
High

Low Low

Low High
Low

High

Queens University Biological Station

on Lake Opinicon

Figure 14.5 Territory map of part of the breeding population of black-capped chickadees at Queens University Biological Station in 2000. Nest
cavities are shown as circles. Arrows indicate the orientation of the nest cavity entrance. Territories were assessed by spot mapping the birds
movement patterns (see Mennill et al. 2004). The rank of the territorial male is shown for each territory.
228 V O C A L C O M M U N I C AT I O N

(Ramsay et al. 1999). Female chickadees, who
remain inside of the nest cavity for much of the
dawn chorus, may be better able to hear the dawn
chorus performance of neighboring males by
nesting near territory boundaries. Given that black-
capped chickadee song transmits over a minimum
distance of 80 to 100 m (Christie et al. 2004a;
Fotheringham and Ratcliffe 1995), females maxi-
mize the number of males audible to them during
the chorus by nesting near territory edges. Analyses
of black-capped chickadee nest positions in 190
territories over 5 years showed that nest sites fell
within 100 m of more chorusing positions of neigh-
bors than did comparison sites at territory centers
(Mennill et al. 2004). Females may also nest at
territory edges to facilitate early morning extrapair
copulations with neighbors (Ramsay et al. 1999).
However, although extrapair copulations do often
occur shortly after female emergence from the nest
(Smith 1988), they do not usually occur in close
proximity to the nest (Mennill et al. 2004), suggest-
ing that the edge-nesting behavior of female
chickadees maximizes acoustic contact rather than
physical contact with neighbors.
Recordings made inside the nest boxes of great
tits provide further support for the idea that roost-
ing female Parids may monitor the dawn chorus
performance of neighboring males while they roost
inside the nest cavity. Microphones were placed
inside the nests of seven different females in a

(a) 25 m from source (b) 50 m from source

4.0 4.0
0 0
3.5 3.5

3.0 3.0

2.5 2.5

4.0 4.0
90 90
Frequency (kHz)

3.5 3.5

3.0 3.0

2.5 2.5

4.0 4.0
180 180
3.5 3.5

3.0 3.0

2.5 2.5
0 0.5 1.0 1.5 0 0.5 1.0 1.5
Time (seconds) Time (seconds)

Figure 14.6 Sound spectrograms of black-capped chickadee songs recorded by a microphone mounted inside an abandoned nest cavity. Songs
were broadcast through a loudspeaker positioned either 25 m from the nest cavity (a) or 50 m from the nest cavity (b). The nest was rotated so
that the entrance to the nest cavity was oriented facing the loudspeaker (0; top), at a right-angle to the loudspeaker (90; middle), or away from
the loudspeaker (180, bottom). The nest cavity demonstrated acoustically directional properties, such that a female chickadee roosting inside the
cavity will be better able to hear a male in front of her nest than a male singing behind her nest. Reprinted with permission from Journal of
Avian Biology.
 S TAT U S S I G N A L I N G A N D C O M M U N I C AT I O N N E T W O R K S
population of breeding great tits at Strdam
Biological Station near Hillerd, Denmark. For all
seven recordings, the dawn chorus of both the pair
male plus at least one neighboring male were
audible (K. A. Otter, T. M. Peake, A. M. R. Terry, and
P. K. McGregor, unpublished data). The recordings
further showed that songs from males singing more
than 75 m away from the roosting female were
clearly audible. Similarly, in black-capped chicka-
dees, recordings made with microphones placed
inside nest cavities could clearly detect males
singing more than 50 m away (Mennill and
Ratcliffe 2004b). Although cavity nesting may
impede the transmission of some signals, these
findings of the acoustics of Parid nest cavities
demonstrate that cavity nesting does not impair
female assessment of distant male dawn chorus
performances.
Black-capped chickadee nest cavities have
acoustically directional properties. Recordings
made with microphones placed inside a chickadee
nest demonstrate that a female is better able to hear
males singing in front of her nest cavity than males
singing behind her nest cavity (Fig. 14.6; Mennill
and Ratcliffe 2004b). Analyses of the orientation of
132 chickadee nests in eastern Ontario demon-
strated that chickadee nests have random compass
orientation and are not specifically directed at the
territories of high-ranking neighbors (e.g. Fig. 14.5).
However, the nest cavities of females who nested in
the soft wood substrate of birch, Betula papyrifera,
and aspen, Populus tremuloides, were oriented
towards their extrapair partners territory (n 17;
Mennill and Ratcliffe 2004b). Consequently, the
drive to monitor the singing behavior of neighbors
may influence not only nest cavity location
(Ramsay et al. 1999, Mennill et al. 2004) but also nest
entrance orientation (Mennill and Ratcliffe 2004b).
These intriguing results demonstrate how commu-
nication network thinking may provide new
insights into the breeding biology of songbirds.
14.5 Singing behavior in other
North American Parids
The male songs of North American Parids vary
substantially between each species. The other
North American Poecile chickadees demonstrate
229
two major themes of variation, both of which are
distinct from the pitch-shifting behavior of black-
capped chickadees. Mountain chickadees P. gambeli,
Carolina chickadees P. carolinensis, and Mexican
chickadees, P. sclateri, appear to have repertoires of
discrete song types. The songs of mountain chicka-
dees are superficially similar to black-capped
chickadees, but each male has a repertoire of four to
seven song types, each consisting of two to four
whistled notes (Wiebe and Lein 1999). Mountain
chickadees engage in countersinging interactions,
during which males use songs with lower fre-
quency terminal notes in the most aggressive
contests (Hill and Lein 1989). The songs of Carolina
chickadees vary substantially from black-capped
chickadee songs, although males of both species
can learn the other species song (Kroodsma et al.
1995). Studies of pure Carolina chickadees show
that their songs usually possess four whistled notes
(Hailman 1989), although the number can vary
from one to 12 (Ward 1966), and individuals have at
least two distinct song variants (Lohr et al. 1991),
which may be important during countersinging
interactions (D. J. Mennill, personal observation).
The songs of Mexican chickadees are poorly under-
stood. Two types of songs have been described for
Mexican chickadees (Ficken 1990), at least one of
which appears to occur as complex song types, but
countersinging behavior has not been described.
Thus, most North American chickadees possess
song repertoires akin to those of European
congeners, such as the marsh tit and willow tit.
Similarly, the songs of male North American titmice
(genus Baeolophus) also exhibit repertoires. Tufted
titmice sing with a repertoires of up to 14 song
types (Gaddis 1983) and during countersinging
interactions males type-match their opponents
(Duguay and Ritchison 1998). Oak titmice B.
inornatus have repertoires of up to 11 song types
(Dixon 1969) and certain song types are associated
with countersinging interactions between males
(Gaddis 1983). From a communication network
perspective, North American Parids with song
repertoires are expected to behave in a way similar
to Eurasian Parids with song repertoires. So far,
however, black-capped chickadees appear unique
in the use of frequency shifting to achieve functions
associated with multiple song types in other Parids.
230 V O C A L C O M M U N I C AT I O N
The remaining two North American Poecile chicka-
dees, chestnut-backed chickadees and boreal chicka-
dees, are (along with their Eurasian congener the
Siberian tit) anomalous songbirds: none exhibit a
long-range, male song. Male boreal chickadees pro-
duce a varied warbling song in aggressive
situations with other males (McLaren 1976) and
chestnut-backed chickadees give modified gargle
calls in aggressive situations (Dahlsten et al. 2002),
but neither of these vocalizations travel sufficient
distances to be used in long-range advertising.
Hailman et al. (1994) studied the dawn behavior of
Siberian tits, and found that these birds center their
activity around the nest, as do chorusing black-
capped chickadees, but use chick-a-dee and gargle
calls in place of song. Like black-capped chickadees,
male Siberian tits cease their vocalizations when the
female emerges from the nest cavity, but the lack of a
long-range signal coupled with the highly dispersed
spacing of this species would seemingly preclude
the ability of a communication network to form
around dawn calling activity. Similar patterns of
dawn activity using chick-a-dee calls have been noted
in the boreal chickadee (C. T. Naugler, personal
communication), but these are yet to be formally
studied. These species therefore represent an inter-
esting opportunity to test the importance of commu-
nication networks for songbirds. If other female
Parids use male chorus performance for assessing
male quality, do females in brown-headed chickadee
species suffer a loss of network-based assessment?
Alternately, do females use different mechanisms of
assessing the relative quality of their mates, such as
the extreme levels of copulation solicitation by
females seen in crested titmice (Lens et al. 1997)?
14.6 Summary and future studies
The two-note fee-bee song of black capped chickadees
ranks among the simplest learned songs of oscine
songbirds. Male chickadees vary the timing and pitch
of this vocalization during both extended dawn
chorus performances and interactive countersinging
exchanges with rivals. Since the publication of Susan
Smiths book on the behavioral ecology of black-
capped chickadees in 1991, our knowledge of chicka-
dee singing behavior has expanded dramatically and
the complex processes of communication between
breeding males and females have become a model
system in animal communication. Our research with
black-capped chickadees, taken together with
research on communication networks in other Parids,
demonstrates that male singing behavior is a net-
work-based process that can convey information
about male quality to rival males and choosy females
simultaneously.
Many aspects of chickadee communication
require further research. Within the context of the
dawn chorus, the interplay between broadcast
communication and directed communication is
poorly understood. Within the context of diurnal
countersinging interactions, overlapping is
relatively well understood, although future studies
should evaluate how often birds overlap during
natural contests and whether partial overlap is
functionally equivalent to complete overlap.
Communication through pitch variation, in
contrast, is poorly understood. During non-
matched countersinging, is singing at a lower
frequency a more or less aggressive communication
strategy? Is pitch shifting a signal per se? The con-
tinuity between the dawn chorus and diurnal
singing merits further investigation. Poesel et al.s
(2004) study of blue tits demonstrated that dawn
chorus performance predicted male performance
during malemale countersinging contests. Other
singing contexts in chickadees also merit more
careful study. During the late winter and early
spring it is not uncommon to hear a lone male belt
out a song bout that is unanswered by other males.
Are these solo bouts unchallenged contest proclam-
ations, or do these song bouts serve a separate
function? These and other questions will allow us
to better understand the dyadic and network-based
dynamics of communication and the complex ways
in which chickadees use their simple song.
Acknowledgements
Laurene Ratcliffe, Peter McGregor, Tom Peake, and
Andrew Terry cooperated in designing and inter-
preting many of the studies reported here. For
helpful discussions we thank Stphanie Doucet and
also Raleigh Robertson. We are deeply thankful to
the many agencies that funded our research on
black-capped chickadees, most notably NSERC,
 S TAT U S S I G N A L I N G A N D C O M M U N I C AT I O N N E T W O R K S
who has funded our ongoing chickadee research
programs since 1993.
References
Beecher, M. D. and Brenowitz, E. A. (2005). Functional
aspects of song learning in songbirds. Trends in Ecology
and Evolution, 20, 143149.
Brewer, R. (1961). Comparative notes on the life history of
the Carolina chickadee. Wilson Bulletin, 73, 348373.
Brindley, E. L. (1991). Response of European robins to
playback of song: neighbour recognition and overlap-
ping. Animal Behaviour, 41, 503512.
Burt, J. M. and Vehrencamp, S. L. (2005). The dawn chorus
as an interactive communication network. In:
McGregor, P. K., ed. Animal Communication Networks,
pp. 320343. Cambridge University Press, Cambridge.
Christie, P. J., Mennill, D. J., and Ratcliffe, L. M. (2004a).
Chickadee song structure is individually distinctive
over long broadcast distances. Behaviour, 141, 101124.
Christie, P. J., Mennill, D. J., and Ratcliffe, L. M. (2004b).
Pitch shifts and song structure indicate male quality in
the dawn chorus of black-capped chickadees.
Behavioural Ecology and Sociobiology, 55, 341348.
Dabelsteen, T., McGregor, P. K., Shepherd, M., Whittaker,
X., and Pedersen, S. B. (1996). Is the signal value of over-
lapping different from that of alternating during
matched singing in great tits? Journal of Avian Biology,
27, 189194.
Dahlsten, D. L., Brennan, L. A., McCallum, D. A., and
Gaunt, S. L. L. (2002). Chestnut-backed Chickadee (Poecile
rufescens). In: Poole A. and Gill, F., eds. The Birds of North
America. Academy of Natural Sciences, Philadelphia.
Dent, P. K., van Oers, K., and van Noordwijk, A. J. (2002).
Realized heritability of personalities in the great tit
(Parus major). Proceedings of the Royal Society of London
Series B, Biology, 270, 4551.
Desfayes, M. (1964). An observation on the song of the
black-capped chickadee. Wilson Bulletin, 66, 438439.
Dixon, K. L. (1969). Patterns of singing in a population of
the plain titmouse. Condor, 71, 94101.
Dixon, K. L. and Stefanski, R. A. (1970). An appraisal of
the song of the black-capped chickadee. Wilson Bulletin,
82, 5362.
Duguay, J. P. and Ritchison, G. (1998). A contextual ana-
lysis of singing behavior in male tufted titmice. Journal
of Field Ornithology, 69, 8494.
Ficken, M. S. (1990). Vocal repertoire of the Mexican
chickadee. II. Song and song-like vocalizations. Journal
of Field Ornithology, 61, 388395.
Ficken, M. S., Ficken, R. W., and Witkin, S. R. (1978). Vocal
repertoire of the black-capped chickadee. Auk, 95, 3448.
231
Forstmeier, W., Kempenaers, B., Meyer, A., and Leisler, B.
(2002). A novel song parameter correlates with extra-
pair paternity and reflects male longevity. Proceedings of
the Royal Society of London Series B, Biology, 269,
14791485.
Fotheringham, J. R. and Ratcliffe, L. (1995). Song degrad-
ation and estimation of acoustic distance in black-
capped chickadees (Parus atricapillus). Canadian Journal
of Zoology, 73, 858868.
Gaddis, P. K. (1983). Differential usage of song types by
plain, bridled and tufted titmice. Ornis Scandinavica, 14,
1623.
Gammon, D. E. (2004). Black-capped chickadee dawn
chorus and subsequent sexual activity. Wilson Bulletin,
116, 252256.
Gammon, D. E. and Baker, M. C. (2004). Song repertoire
evolution and acoustic divergence in a population of
black-capped chickadees, Poecile atricapillus. Animal
Behaviour, 68, 903913.
Gould, S. J. (1998). The great asymmetry. Science, 279,
812813.
Hailman, J. P. (1989). The organization of major vocaliza-
tions in the Paridae. Wilson Bulletin, 101, 305343.
Hailman, J. P., Haftorn, S., and Hailman, E. D. (1994). Male
siberian tit Parus cinctus dawn serenades: suggestion for
the origin of song. Fauna Norv Ser C Cinclus, 17, 1526.
Hansen, I. J. K., Otter, K. A., and van Oort, H. (2005).
Communication breakdown? Habitat influences on the
communication networks in black-capped chickadees.
Acta Ethol, 82, 111120.
Hill, B. G. and Lein, M. R. (1987). Function of frequency-
shifted songs of black-capped chickadees. Condor, 89,
914915.
Hill, B. G. and Lein, M. R. (1989). Natural and simulated
encounters between sympatric black-capped chicka-
dees and mountain chickadees. Auk, 106, 645652.
Horn, A. G., Leonard, M. L., Ratcliffe, L., Shackleton, S. A.,
and Weisman, R. G. (1992). Frequency variation in
songs of black-capped chickadees (Parus atricapillus).
Auk, 109, 847852.
Krebs, J. R., Ashcroft, R., and Van Orsdol (1981). Song
matching in the great tit Parus major. Animal Behavior,
29, 918923.
Kroodsma, D. E. and Byers, B. E. (1991). The function(s) of
bird song. American Zoologist, 31, 318328.
Kroodsma, D. E., Albano, D. J., Houlihan, P. W., and Wells,
J. A. (1995). Song development by black-capped
chickadees (Pars atricapillus) and Carolina chickadees
(P. carolinensis). Auk, 112, 2943.
Kroodsma, D. E., Byers, B. E., Halkin, S. L., et al. (1999).
Geographic variation in black-capped chickadee songs
and singing behavior. Auk, 116, 387402.
232 V O C A L C O M M U N I C AT I O N
Lambrecht, M. M. (1992). Male quality and playback in
the great tit. In: McGregor, P. K., ed. Playback and Studies
of Animal Communication, pp. 135152. Plenum Press,
New York.
Lambrechts, M. M. and Dhondt, A. A. (1988). Male quality
and territory quality in the great tit Parus major. Animal
Behaviour, 36, 595601.
Langemann, U., Tavares, J. P., Peake, T. M., and McGregor,
P. K. (2000). Response of great tits to escalating patterns
of playback. Behaviour, 137, 451471.
Lens, L., Van Dongen, S., Van den Broeck, M., Van
Broeckhovan, V., and Dhondt, A. A. (1997). Why female
crested tits copulate repeatedly with the same partner:
evidence for the mate assessment hypothesis. Behavioral
Ecology, 8, 8791.
Lohr, B., Nowicki, S., and Weisman, R. (1991). Pitch
production in Carolina chickadee songs. Condor, 93,
197199.
McGregor, P. K. (2005). Animal Communication Networks.
Cambridge University Press, Cambridge.
McGregor, P. K. and Dabelsteen, T. (1996).
Communication networks. In: Kroodsma, D. E. and
Miller, E. H., eds. Ecology and Evolution of Acoustic
Communication in Birds, pp 409425. Cornell University
Press, Ithaca.
McGregor, P. K., Dabelsteen, T., Shepherd, M., and
Pedersen, S. B. (1992). The signal value of matched
singing in great tits: evidence from interactive playback
experiments. Animal Behavior, 43, 987998.
McGregor, P. K., Krebs, J. R., and Perrins, C. H. (1981).
Song repertoires and lifetime reproductive success in
the great tit (Parus major). American Naturalist, 188,
149159.
McLaren, M. (1976). Vocalizations of the boreal chickadee.
Auk, 93, 451463.
Mennill, D. J. and Ratcliffe, L. M. (2004a). Do male black-
capped chickadees eavesdrop on song contests? A
multi-speaker playback experiment. Behaviour, 141,
125139.
Mennill, D. J. and Ratcliffe, L. M. (2004b). Nest cavity
orientation in black-capped chickadees Poecile atricapil-
lus: do the acoustic properties of cavities influence
sound reception in the nest and extra-pair matings?
Journal of Avian Biology, 35, 477482.
Mennill, D. J. and Ratcliffe, L. M. (2004c). Overlapping
and matching in the song contests of black-capped
chickadees. Animal Behaviour, 67, 441450.
Mennill, D. J. and Rogers, A. C. (2006). Whip it good!
Geographic consistency in male songs and variability
in female songs of the duetting Eastern Whipbird
(Psophodes olivaceus). Journal of Avian Biology, 37,
93100.
Mennill D. J., Boag, P. T., and Ratcliffe, L. M. (2003).
The reproductive choices of eavesdropping female black-
capped chickadees, Poecile atricapillus. Naturwissenschaften,
90, 577582.
Mennill, D. J., Ramsay, S. M., Boag, P. T., and Ratcliffe,
L. M. (2004). Patterns of extrapair mating in relation to
male dominance status and female nest placement in
black-capped chickadees. Behavioral Ecology, 15, 757765.
Mennill, D. J., Ratcliffe, L. M., and Boag, P. T. (2002).
Female eavesdropping on male song contests in song-
birds. Science, 296, 873883.
Naguib, M. and Todt, D. (1997). Effects of dyadic vocal
interactions on other conspecific receivers in nightin-
gales. Animal Behavior, 54, 15351543.
Odum, E. P. (1941). Annual cycle of the black-capped
chickadee. Auk, 58, 314333.
Otter, K. and Ratcliffe, L. (1993). Changes in the singing
behaviour of male black-capped chickadees (Parus atri-
capillus) following mate removal. Behavioural Ecology
and Sociobiology, 33, 409414.
Otter, K. and Ratcliffe, L. (1996). Female initiated divorce
in a monogamous songbird: abandoning mates for
males of higher quality. Proceedings of the Royal Society of
London Series B, Biology, 263, 351354.
Otter, K. and Ratcliffe, L. (2005). Enlightened decisions:
female assessment and communication networks. In:
McGregor, P. K., ed. Animal Communication Networks,
pp. 133151. Cambridge University Press, Cambridge.
Otter, K., Chruszcz, B., and Ratcliffe, L. (1997). Honest
advertisement and singing during the dawn chorus of
black-capped Chickadees, Parus atricapillus. Behavioral
Ecology, 8, 167173.
Otter, K., McGregor, P. K., Terry, A. M., Burford, F. R. L.,
Peake, T. M., and Dabelsteen, T. (1999). Do female great
tits (Parus major) assess males by eavesdropping? A field
study using interactive song playback. Proceedings of the
Royal Society of London Series B, Biology, 266, 13051310.
Otter, K., Ratcliffe, L., Michaud, D., and Boag, P. T. (1998).
Do female black-capped chickadees prefer high ranking
males as extra-pair partners? Behavioural Ecology and
Sociobiology, 43, 2536.
Otter, K., Stewart, I. K., McGregor, P. K., Terry, A. M. R.,
Dabelsteen, T., and Burke, T. (2001). Extra-pair paternity
in great tits in relation to manipulation of male signals.
Journal of Avian Biology, 32, 338344.
Otter, K. A., Ratcliffe, L., Njegovan, M., and
Fotheringham, J. (2002). The importance of frequency
and temporal matching in aggressive vocal signalling of
black-capped chickadees: evidence from interactive
playback. Ethology, 108, 181191.
Peake, T. M. (2005). Eavesdropping in communication
networks. In: McGregor, P. K., ed. Animal Communication
 S TAT U S S I G N A L I N G A N D C O M M U N I C AT I O N N E T W O R K S
Networks, pp. 1338. Cambridge University Press,
Cambridge.
Phillmore, L. S., Sturdy, C. B., Turyk, M. M., and Weisman,
R. G. (2002). Discrimination of individual vocalizations
by black-capped chickadees (Poecile atricapilla). Animal
Learning and Behavior, 30, 4352.
Poesel, A. (2004). Singing in territorial defence and mate
choice in the blue tit Parus caeruleus. Ph.D thesis,
University of Copenhagen, Denmark.
Ramsay, S. M., Otter, K., Mennill, D. J., and Ratcliffe, L.
(2000). Divorce and extrapair mating in female black-
capped chickadees (Poecile atricapillus): Separate strate-
gies with a common target. Behavioural Ecology and
Sociobiology, 49, 1823.
Ramsay, S. M., Otter, K., and Ratcliffe, L. M. (1999).
Nest site selection by female black-capped chicka-
dees: settlement based on social attraction. Auk, 116,
604617.
Ratcliffe, L. and Weisman, R. G. (1985). Frequency shift in
the fee-bee song of the black-capped chickadee. Condor,
87, 555556.
233
Shackleton, S. A. and Ratcliffe, L. (1994). Matched counter-
singing signals escalation of aggression in black-capped
chickadees (Parus atricapillus). Ethology, 97, 310316.
Smith, S. M. (1988). Extra-pair copulations in black-capped
chickadees: the role of the female. Behaviour, 107, 1523.
Smith, S. M. (1989). Black-capped chickadee summer
floaters. Wilson Bulletin, 101, 344349.
Smith, S. M. (1991). The Black-Capped Chickadee: Behavioral
Ecology and Natural History. Cornell University Press:
Ithaca.
Todt, D. (1981). On functions of vocal matching: effect of
counter-replies on song post choice and singing.
Zeitschrift fur Tierpsychologie, 57, 7393.
Vehrencamp, S. L. (2000). Is song-type matching a con-
ventional signal of aggressive intentions? Proceedings of
the Royal Society of London, Series B, 268, 16371642.
Ward, R. (1996). Regional variation in the song of the
Carolina chickadee. Living Bird, 5, 127150.
Wiebe, M. O. and Lein, M. R. (1999). Use of song types by
mountain chickadees (Poecile gambeli). Wilson Bulletin,
111, 368375.
This page intentionally left blank
 SYNOPSIS III
Complexities in vocal
communication
Todd M. Freeberg, Myron C. Baker, Laurie L. Bloomfield,
Isabelle Charrier, David E. Gammon, Jack P. Hailman,
Tiffany T.-Y. Lee, Jeffrey R. Lucas, Daniel J. Mennill,
and Christopher B. Sturdy
Overview
The vocal systems of Parids are among the
most complex communicative systems docu-
mented in the avian world. Part of this complexity
stems from the large number of acoustically
and functionally distinct vocal signals, each
of which has its own acoustic and functional
diversity (Ficken et al. 1978; Hailman and
Ficken 1996; Chapter 13). Because of the vocal
complexity of most, if not all Parids, this
group could be a model system for understanding
how social and physical environmental pressures
might drive variation in signaling systems. In
this synopsis, we briefly review some of the
major advances that have been made in
understanding the vocal systems of chickadees
and related species and then draw comparisons to
vocal systems in Parids outside North America.
Our primary focus, however, is to delineate
questions that need to be addressed if we hope to
answer perhaps the most fundamental question
about this vocal complexity; namely, why does it
exist in this group?
Vocal complexity of chickadees
and titmice
Beginning with the seminal work of Ficken et al.
(1978) on the vocalizations of black-capped
chickadees, we have made significant advances in
understanding vocal communication in a number
of chickadee species. Much of this work is
described in the chapters in this section of the book.
Research on fee-bee vocalizations shows the extent
of species-level information (Chapter 12), eluci-
dates the causes and functions of absolute and
relative pitch changes (Chapters 10 and 14), and
demonstrates significant geographic variation
(Chapter 12). We are starting to understand the
syntax of gargles and the nature and functions
of local sharing and social transmission of gargle
types (Chapter 11). We continue to decode the
information conveyed in chick-a-dee calls, from
messages and meanings of different note types to
different markers of identity that reside in acoustic
parametersindividual, population, and species
(Chapters 10 and 13).
As the chapters in this section attest, the vocal-
izations of chickadees and titmice offer an exciting
and rich comparative system with which to
address questions of mechanisms, development,
function, and phylogeny of vocal behavior
(e.g. Tinbergen 1963). Of these four why ques-
tions for behavior, we know much more about
the function question than the other three, so
clearly one of our general aims should be to gain
greater understanding of mechanistic, ontogen-
etic, and phylogenetic influences on Parid vocal
communication.
235
236 V O C A L C O M M U N I C AT I O N
The song versus call distinction and
social complexity
One intriguing feature of the vocal systems of North
American Parids is the seemingly reversed struc-
turefunction relationship of their songs and calls
(also intriguing is the fact that the major vocaliza-
tions of many European Parids do seem to fit into
the typical song/call distinctions). As described
recently by Marler (2004, p. 132): songs are usually
longer and more complex acoustically, involving a
variety of different notes and syllables, ordered in
statistically reliable sequences; calls are often short,
monosyllabic, with simple frequency patterning,
often delivered in what often appears to be a disor-
derly fashion. Functionally, whereas songs play a
somewhat restricted role, in territory establishment
and maintenance, and mate attraction, the functions
of calls include not only reproduction, but also
predator alarm, the announcement and exchange of
food, and the maintenance of social proximity and
group composition and integration.
Whereas the fee-bee song and chick-a-dee call obey
the functional criteria outlined in the quote above,
the structural characteristics of these two vocal
signals are quite reversed, with fee-bees being,
acoustically, relatively simple and chick-a-dee calls
variable and diverse (but its combinatorial nature is
by no means disorderly). The gargle is similarly
difficult to fit into this traditional songcall frame-
work, as it is structurally complex like the chick-a-dee
call (though more stereotyped and not as combina-
torial), but appears to be used in fewer social
contexts than the chick-a-dee call. The gargle shares a
functional characteristic with the chick-a-dee call that
makes them different from fee-beesgargles and
chick-a-dees are used year-round (feature of calls),
whereas fee-bees are used almost exclusively in pair-
ing and breeding (feature of songs). Furthermore,
songs in oscine passerines are usually characterized
as being learned, and calls as being unlearned (e.g.
Catchpole and Slater 1999). Research has found
evidence of vocal learning for all three vocal signals:
fee-bees (Shackleton and Ratcliffe 1993; Kroodsma
et al. 1995), gargles (Ficken and Popp 1995), and
chick-a-dees (Hughes et al. 1998).
Why do these species seem to defy the more
typical songcall structurefunction characteristics
followed by most passerines? We do not know, but
we suggest the following possibilities. First, gargle
and chick-a-dee calls can convey individual, popula-
tion, and species identity (e.g. Ficken and Popp
1995; Chapter 10), so perhaps this has taken
pressure off fee-bees to solely encode this informa-
tion, resulting in structurally simpler signals.
Alternatively, perhaps song is more complex
than we have realized. For example, complexity in
the fee-bee vocalization may occur in different
dimensions than is typical of other passerines (e.g.
frequency shiftingChapter 14). The complexity of
the fee-bee vocalization could also be augmented by
the addition of other vocal signals, particularly
gargles, to song displays. Another possibility is that
the complex social structure of many chickadee
species (Chapter 9) may have generated selection
pressure for greater complexity in their year-round
social signals (chick-a-dees and gargles) than would
otherwise be the case.
The complexity in the vocal repertoire of
chickadees and titmice seems to exist for the purpose
of conveying different kinds of information, and not
as a result of selection for diversity per se, as in the
case of sexual selection for larger song repertoires in
male northern mockingbirds, Mimus polyglottos
(Howard 1974). Might the vocal complexity be
driven by social complexity? Recent findings
indicate that chickadees in larger (and presumably
therefore more complex) social groups produce
chick-a-dee calls that contain greater information
than chickadees in smaller social groups (Freeberg
2006). Further support for this hypothesis is
the fact that other groups with complex social
structures, such as the Corvidae (jays, crows, and
magpies) and Psittaciforms (parrots), often seem to
show considerable complexity in their vocal
repertoires (e.g. Brown and Farabaugh 1997;
Bradbury 2003).
One major unanswered question circles back to
the title of this book and how little we actually
know about titmouse vocal behavior. Titmouse
vocal repertoires seem to be comparable to chicka-
dee vocal repertoires in terms of the diversity of
vocal types that occur and the functions they likely
serve (Gaddis 1979; Hailman 1989). However,
titmice have been severely understudied relative to
chickadees for virtually all aspects of their vocal
 S TAT U S S I G N A L I N G A N D C O M M U N I C AT I O N N E T W O R K S
behavior. Of the small number of studies on
titmouse vocal behavior, most have addressed the
song and what social contexts promote singing
behavior (Gaddis 1983; Johnson 1987; Schroeder
and Wiley 1983; Duguay and Ritchison 1998). Do
titmouse signals, like those of the chickadees that
have been studied, fall with difficulty into the
traditional songcall distinctions? Finally, vocal
behavior of the true tits (Paridae) has been studied
much more extensively than that of the penduline
tits (Remizidae). One of our major aims should
therefore be to increase our understanding of the
vocal systems of these under-studied groups, a
point to which we return later.
Methodological advances
We know much more about the vocal systems of
chickadees and titmice, and of songbirds in general,
than we do about their visual (or other) display
systems. The primary reason is that it has been far
easier to record, analyze, and manipulate sounds
produced by birds in the laboratory and field than
it has been to conduct studies of other signaling
systems, largely due to the availability of portable
recording and playback equipment (e.g. Baptista
and Gaunt 1994). Video and other methods of
visual analysis (e.g. measuring UV) are becoming
more accessible and providing some exciting
avenues of research (see Chapter 2) , but have yet
to catch up to the decades of research on vocal
behavior in tits. Playbacks of vocal signals have a
long history in studies of birds in field and
laboratory settings (McGregor 1992). Various
methodological advances are aiding our ability to
understand the behavior of receivers and signalers
with respect to vocal communication. For example,
the recent development of interactive playback
designs has revealed behavioral outcomes that
might not otherwise have been obtainable. These
developments include work on black-capped
chickadees and great tits (reviewed in Chapter 14).
Other methodological advances, such as multi-
channel real-time spectrogram capabilities and
multimicrophone recording arrays are allowing
for very detailed information about multiple
signalers interacting over time and space (Bower
and Clark 2005; Burt and Vehrencamp 2005). As
237
our thinking about communication extends from a
sender signal receiver framework to that of
senders and receivers interacting in complex
communication networks, our understanding of the
real-world causes and consequences of vocal signal-
ing in these species will continue to grow
(McGregor 2005).
Within chickadees, there has perhaps also been a
bias against investigations of visual signals by the
apparent lack of sexual dimorphism in coloration
patterns. However, increased understanding of UV
perception in birds and techniques for measuring
these cues has resulted in recent work showing
previously unsuspected variation in plumage
brightness in chickadees (Mennill et al. 2003). Not
only does variation in plumage brightness appear
to convey information about male rank and repro-
ductive success (Doucet et al. 2005), but females
appear to be able to assess male social standing on
these visual cues in the absence of witnessing
dominance interactions, and apparently in the
absence of other vocal signals (Woodcock et al.
2005). Clearly, visual signaling in chickadees is an
avenue for future research.
What is to be done?
We end this synopsis by raising some additional
questions we need to pursue in vocal communica-
tion in Parids. We also try to link our understand-
ing of North American Parids to some of the work
that has been conducted with species outside North
America.
Previous research in Parids has demonstrated a
severe geographic and taxonomic bias.
Phylogenetic relationships of Parids are being
clarified, but in terms of gaining understanding of
vocal system evolution, we have a long way to go
because vocal repertoires of so few of the species
have been adequately documented (see also
Hailman and Ficken 1996). We have minimal infor-
mation on dawn chorus behavior, on types of vocal-
izations and their contexts of use, and on the
relationship between vocal signaling and mating
behavior in most of the Paridaefor example,
much of the Voice descriptions for Paridae
species provided in Harrap and Quinn (1995) are
taken from field guides and not from primary
238 V O C A L C O M M U N I C AT I O N
science articles devoted to addressing vocalizations
for a given species. To cite a couple of examples, we
know almost nothing about the vocal behavior of
the penduline, black, and grey tits in Africa. The
one example documented thus far of commonly
occurring syntactic permutation in the chick-a-dee
call (thus perhaps approaching more closely the
human language notion of syntax) exists in the call
of the black-lored tit, Parus xanthogenys, of India
(Hailman 1994). However, very little is known
about the vocal behavior of the other Parus
genus members in India and east Asia (though
much more is known about the European member
of this genus, the great tit). In North America,
we know relatively little about the vocal behavior
of the brown-capped chickadee groupthe
Siberian tit and the chestnut-backed and boreal
chickadees.
From recent work with interactive playbacks, it is
clear that how a chickadees signals are perceived is
not just dependent upon what it signals but also
how and when it signals. This raises the need for us
to study countersinging and countercalling in these
species. How does assessment of senders occur in
species such as chestnut-backed chickadees that
seem to lack long-range signals, or in species that
rely more on the shorter-range gargles in their dawn
choruses? Recent work indicates that environmen-
tal noise impacts frequency characteristics of song
in great tits (Slabbekoorn and Peet 2003); do back-
ground noises also impact the shorter-range gargles
and chick-a-dee calls?
Within even the well-studied chickadee species,
numerous questions remain to be answered. For
example are pitch-shifted versions of fee-bees
perceived as being distinct from one another by
receivers? How are intermediate pitch shifts
perceived? In the chick-a-dee call, the C and D
notes seem to have been most studiedwhat
roles do the A and B notes play in communication?
In the gargle, do patterns of geographic variation
and local sharing occur in species other than
black-capped chickadees, and do these other
species follow the same rules for constructing
gargles?
Earlier we raised the difficulty of placing the fee-
bee, gargle, and chick-a-dee neatly into song or
call bins. An exciting prospect that stems from
these different vocal signals is to understand the
neural underpinnings of the behaviors. For
example, are the neural circuits for vocal develop-
ment and production the same for the three sig-
nals? Decades of work have clarified the neural
substrates for bird song (Nottebohm 1999), but
only recently have neural influences on calls in
songbirds been addressed (Vicario et al. 2002).
Neural regions underlying signals used seasonally
would likely themselves show seasonal changes
(for example brain regions underlying spatial
memory change seasonally with respect to the time
periods of reliance on cached food items in these
species; Chapters 2, 3, and 4). Very interestingly,
recent work with black-capped chickadees found
no seasonal changes in nuclei of the song system
despite seasonal changes in song structure
(Smulders et al. 2006). Seasonal influences in
song system nuclei have been documented in blue
tits (Caro et al. 2005), but the extent to which these
neural changes may differentially influence singing
and calling behavior is not known. Gene expression
patterns in the brain may help our understanding
of vocal variation in these species, particularly if
calls induce such patterns in different ways in
the brain relative to songs (e.g. Mello 2002).
Chickadees, tits, and titmice would thus seem to
offer a powerful experimental system with which
to address neurophysiological questions related to
vocal signaling, learning, and seasonal changes.
We have learned an enormous amount of infor-
mation about the vocal complexity of chickadees in
the past three decades. The richness and variation
in the vocal and social behavior of these species is
such that they likely represent an ideal system for
tackling important questions about ecological and
evolutionary influences on vocal communication.
Still, it is important to take a cautious view about
how much we really do understand about Parid
vocal complexitywe will likely need all the
conceptual and methodological advances at our
disposal to gain a firm hold of this daunting
system. We have learned enough at this point,
however, to feel confident in arguing that the
payoffs of continued efforts to integrate proximate
and ultimate approaches to understanding this
complex system of vocal behavior could be quite
large indeed.
 S TAT U S S I G N A L I N G A N D C O M M U N I C AT I O N N E T W O R K S
References
Baptista, L. F. and Gaunt, S. L. L. (1994). Advances in the
study of avian sound communication. Condor, 96,
817830.
Bower, J. L. and Clark, C. W. (2005). A field test of the
accuracy of a passive acoustic location system.
Bioacoustics, 15, 114.
Bradbury, J. W. (2003). Vocal communication in wild
parrots. In: de Waal, F. B. M. and Tyack, P. L., eds.
Animal Social Complexity: Intelligence, Culture, and
Individualized Societies, pp. 293316. Harvard University
Press, Cambridge, Massachusetts.
Brown, E. D. and Farabaugh, S. M. (1997). What birds with
complex social relationships can tell us about vocal learn-
ing: vocal sharing in avian groups. In: Snowdon, C. T. and
Hausberger, M., eds. Social Influences on Vocal Development,
pp. 98127. Cambridge University Press, Cambridge.
Burt, J. M. and Vehrencamp, S. L. (2005). Dawn chorus
as an interactive communication network. In: McGregor,
P. K., ed. Animal Communication Networks, pp. 320343.
Cambridge University Press, Cambridge.
Caro, S. P., Lambrechts, M. M., and Balthazart, J. (2005).
Early seasonal development of brain song control nuclei
in male blue tits. Neuroscience Letters, 386, 139144.
Catchpole, C. K. and Slater, P. J. B. (1999). Bird Song:
Biological Themes and Variations. Cambridge University
Press, Cambridge.
Doucet, S. M., Mennill, D. J., Montgomerie, R., Boag, P. T.,
and Ratcliffe, L. M. (2005). Achromatic plumage varia-
tion predicts the reproductive success of male black-
capped chickadees. Behavioral Ecology, 16, 218222.
Duguay, J. P. and Ritchison, G. (1998). A contextual ana-
lysis of singing behavior in male tufted titmice. Journal
of Field Ornithology, 69, 8594.
Ficken, M. S. and Popp, J. W. (1995). Long-term persist-
ence of a culturally-transmitted vocalization of the
black-capped chickadee. Animal Behaviour, 50, 683693.
Ficken, M. S., Ficken, R. W., and Witkin, S. R. (1978). Vocal
repertoire of the black-capped chickadee. Auk, 95,
3448.
Freeberg, T. M. (2006). Social complexity can drive vocal
complexity: Group size influences vocal information in
Carolina chickadees. Psychological Science. 17, 557561.
Gaddis, P. K. (1979). A Comparative Analysis of the Vocal
Communication Systems of the Carolina Chickadee and the
Tufted Titmouse. Ph.D. dissertation, University of Florida.
Gaddis, P. K. (1983). Differential usage of song types by
plain, bridled, and tufted titmice. Ornis Scandinavica, 14,
1623.
Hailman, J. P. (1989). The organization of the major vocal-
izations in the Paridae. Wilson Bulletin, 101, 305343.
239
Hailman, J. P. (1994). Constrained permutation in chick-
a-dee-like calls of a black-lored tit (Parus xanthogenys).
Bioacoustics, 6, 3350.
Hailman, J. P. and Ficken, M. S. (1996). Comparative ana-
lysis of vocal repertoires, with reference to chickadees.
In: Kroodsma, D. E., and Miller, E. H., eds. Ecology and
Evolution of Acoustic Communication in Birds, pp. 136159.
Cornell University Press, Ithaca, New York.
Harrap, S. and Quinn, D. (1995). Chickadees, Tits,
Nuthatches and Treecreepers. Princeton University Press,
Princeton, New Jersey.
Howard, R. D. (1974). The influence of sexual selection
and interspecific competition on mockingbird song
(Mimus polyglottos). Evolution, 28, 428438.
Hughes, M., Nowicki, S., and Lohr, B. (1998). Call learning
in black-capped chickadees (Parus atricapillus): the role
of experience in the development of chick-a-dee calls.
Ethology, 104, 232249.
Johnson, L. S. (1987). Pattern of song type use for territor-
ial defense in the plain titmouse Parus inornatus. Ornis
Scandinavica, 18, 2432.
Kroodsma, D. E., Albano, D. J., Houlihan, P. W., and Wells,
J. A. (1995). Song development by black-capped
chickadees (Parus atricapillus) and Carolina chickadees
(P. carolinensis). Auk, 112, 2943.
Marler, P. (2004). Bird calls: a cornucopia for communica-
tion. In: Marler, P. and Slabbekoorn, H., eds. Natures
Music: the Science of Birdsong, pp. 132177. Elsevier,
London and San Diego, California.
McGregor, P. K., ed. (1992). Playback and Studies of Animal
Communication. Plenum Press, New York.
McGregor, P. K., ed. (2005). Animal Communication
Networks. Cambridge University Press, Cambridge.
Mello, C. V. (2002). Mapping vocal communication
pathways in birds with inducible gene expression. Journal
of Comparative Physiology, A, 188, 943959.
Mennill, D. J., Doucet, S. M., Montgomerie, R., and
Ratcliffe, L. M. (2003). Achromatic colour variation in
black-capped chickadees, Poecile atricapilla, black and
white signals of sex and rank. Behavioral Ecology and
Sociobiology, 53, 350357.
Mennill, D. J., Ratcliffe, L. M., and Boag, P. T. (2002).
Female eavesdropping on male song contests in song-
birds. Science, 296, 873.
Nottebohm, F. (1999). The anatomy and timing of vocal
learning in birds. In: Hauser, M. D. and Konishi, M.,
eds. The Design of Animal Communication, pp. 63110.
MIT Press, Cambridge, Massachusetts.
Otter, K. A., McGregor, P. K., Terry, A. M. R., Burford, F. R.
L., Peake, T. M., and Dabelsteen, T. (1999). Do female
great tits (Parus major) assess males by eavesdropping?
A field study using interactive song playback.
240 V O C A L C O M M U N I C AT I O N
Proceedings of the Royal Society of London Series B:
Biological Sciences, 266, 13051309.
Schroeder, D. J. and Wiley, R. H. (1983). Communication
with shared song themes in tufted titmice. Animal
Behaviour, 31, 11281138.
Shackleton, S. A. and Ratcliffe, L. (1993). Development of
song in hand-reared black-capped chickadees. Wilson
Bulletin, 105, 637644.
Slabbekoorn, H. and Peet, M. (2003). Birds sing at a
higher pitch in urban noise. Nature, 424, 267.
Smulders, T. V., Lisi, M. D., Tricomi, E., Otter, K. A.,
Chruszcz, B., Ratcliffe, L. M., and DeVoogd, T. J.
(2006). Failure to detect seasonal changes in the song
system nuclei of the black-capped chickadee (Poecile
atricapillus). Journal of Neurology. 66, 9911001.
Tinbergen, N. (1963). On aims and methods of ethology.
Zeitschrift fr Tierpsychologie, 20, 410433.
Vicario, D. S., Raksin, J. N., Naqvi, N. H., Thande, N., and
Simpson, H. B. (2002). The relationship between
perception and production in songbird vocal imitation:
what learned calls can teach us. Journal of Comparative
Physiology, A, 188, 897908.
Woodcock, E. A., Rathburn, M. K., and Ratcliffe, L. M.
(2005). Achromatic plumage reflectance, social
dominance and female mate preference in black-capped
chickadees (Poecile atricapillus). Ethology, 111, 891900.
 SECTION IV
Landscape ecology, behavior, and
conservation issues
At first glance, it may seem counterintuitive to
think of Parids in the context of conservation. The
birds in this family, particularly the well-studied
species, are apparent paragons of adaptability to
human disturbance. However, it is the ability to
persist in human-altered landscapes that makes
this group useful for understanding the subtle
impacts of landscape-level changes on native
organisms. In particular, chickadees and titmice are
forest generalists that can be used to test some of
the theories associated with forest fragmentation,
especially in relation to impacts on movement,
breeding, and winter survival. The three chapters
in this section of the book address such topics of
habitat fragmentation and landscape ecology.
In Chapter 15, Desrochers and Blisle use meta-
analysis to study Parid habitat use at three spatial
scalesedge, patch, and the landscape. The focus
then shifts to how landscape features, particularly
the behavioral response of black-capped and boreal
chickadees to gaps and forest corridors, influence
interpatch dispersion and its potential for metapopu-
lation dynamics. Olson and Grubb (Chapter 16)
review the literature on the physiological response
to cold among overwintering resident Parids,
such as controlled hypothermia and shivering
thermogenesis. They then consider these evolved
responses in chickadees and tufted titmice in
isolated woodlots in agricultural landscapes,
where fragmentation and patch size greatly alter
the microclimate to which species are exposed. In
the final chapter of the section, Otter, van Oort, and
Fort (Chapter 17) address the potential for breeding
in altered habitats, such as those found in managed
habitat matrices that separate remnant, native
forest. Using studies on both Eurasian tits and
North American chickadees, Otter et al. parallel
studies investigating breeding in forests of
divergent habitat quality with proposed manage-
ment of matrix vegetation as alternative breeding
habitat for matrix-tolerating species.
The chapters in this section emphasize the advan-
tage that can be gained by using common, generalist
species to test theoretical assumptions in landscape
ecology and conservation. The ability to closely
monitor movement and breeding in Parids in a
variety of habitats allows researchers to assess even
subtle impacts of habitat disturbance on species
ecology. By understanding what impacts human-
altered landscapes have on resistant species such as
Parids, we gain better understanding of how these
same impacts may affect more sensitive species.
241
This page intentionally left blank
 CHAPTER 15
Edge, patch, and landscape effects on
Parid distribution and movements
Andr Desrochers and Marc Blisle
15.1 Introduction
The fact that birds, despite their great vagility, are
often absent from small or isolated patches of habi-
tat has puzzled ecologists for years, if not decades.
Answering the isolation question for forest birds
in general would be a daunting task, to say the
least. But we feel that Parids provide a good start-
ing point and a true model system. The basic
ecology of most species of Parids is covered in
detail by outstanding works such as Birds of North
America (Poole et al. 19922003), Birds of the Western
Palearctic (Cramp et al. 19781997), and will
undoubtedly be treated in detail in an upcoming
issue of the monumental series, Birds of the World
(del Hoyo et al. 1992present). Yet, there is very
little information on individual movements in
Parids, with the exception of natal dispersal dis-
tances, which were documented in both Europe
(Greenwood et al. 1979) and North America (Weise
and Meyer 1979) but have received less attention
since these initial studies. Further, studies of natal
dispersal have typically focused on their popula-
tion and genetic consequences (e.g. Postma and van
Noordwijk 2005), rather than the immediate
processes involved, such as what happens when
an individual encounters a barrier between two
habitat patches.
Landscape ecologists interested in birds gener-
ally focus on entire communities. As a result,
there is a sizeable body of literature on relation-
ships between Parids and edges, patches, and
landscapes. While that literature is mainly based
on species distribution data, it does provide
useful background information that may help us
understand challenges that Parids face when they
move through landscapes. A cursory look at
the Parid-versus-landscape literature shows that,
although very similar in appearance and life
history, Parids exhibit a great diversity of responses
to the challenges posed by habitat pattern and
isolation.
In this chapter, we ask the general questions, how
do Parids use landscapes and can we explain it by
the study of movements of individuals? We review
available evidence, observational and manipula-
tive, on space use at three scales: edge, patch, and
landscape. We link evidence on Parid distribution
with general insights on forest bird movements, in
an attempt to explain the former by the latter.
Throughout the chapter, we place the emphasis on
individuals, not populations (e.g. dispersal), which
receives more thorough treatment in Chapter 16.
15.2 Response to edges by Parids
Habitat edges are especially important in the study
of animal movements, because edges define land-
scape heterogeneity as well as movement opportun-
ities and challenges. Thus, it is along edges that
birds will often face movement options, such as
flying into the open versus remaining under forest
cover. The way edges refract or reflect bird
movements should tell us much about how birds
perceive their landscapes. Researchers have stud-
ied responses of birds to edges mostly by looking at
distribution patterns in relation to distances from
edges, but also through the detailed analysis of
passive or experimentally-induced movements
243
244 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
(reviewed by Desrochers et al. 1999 and Harris and
Reed 2002). Here we address these approaches, and
their relevance to the study of Parids, especially in
the case of non-breeding flocks, whose home range
sizes are relevant to what is commonly understood
as landscapes, that is areas spanning more than
just a few hectares.
There is a plethora of studies, spanning over
70 years (e.g. Leopold 1933), on the relative occur-
rence or abundance of birds near or far from habi-
tat boundaries (hereafter referred to as edges).
These studies have mostly focused on species
inhabiting forest habitats, and have been conducted
along strong gradients or hard edges created by
agriculture, forestry, or urban sprawl. Several
mechanisms, most often unrelated to movement
per se, have been proposed to explain why some
species are associated with, or avoid, habitat edges.
Some species may indeed be attracted to intrinsic
properties of habitat edges (e.g. shrubby vegetation
or the encounter of two complementary resources),
while the association (positive or negative) of other
species to edges may simply reflect processes unre-
lated to an edge effect per se, for example artefactual
(Imbeau et al. 2003), or reflecting constraints on
movements (Desrochers and Fortin 2000).
Parids often occur in open areas adjoining
forests, such as transmission-line corridors
(Anderson et al. 1977; Pearson 1993), agricultural
fields (Blisle and Desrochers 2002), and recent
clearcuts (A. Hadley, personal communication). Of
25 studies that we found reporting associations (or
the lack thereof) between edge proximity and the
occurrence or abundance of Parids, at least 22
focused on the breeding season (AprilJuly), a
period during which movements of individuals are
generally restricted to a few hectares. Studies of
edge versus distribution of breeding Parids are of
limited interest to the study of movements, because
associations between Parid territory locations and
edges may largely result from nesting (e.g. Doherty
and Grubb 2002a) rather than movement. The few
published studies of edge use by Parids outside the
breeding season provide more scope for insights on
movement behavior, given the large extent of
movements of flocks relative to breeding pairs
(e.g. reaching over 30 ha; Siffczyk et al. 2003). Those
studies provide at least four non-exclusive
explanations for edge use or avoidance by Parid
flocks: (1) higher food abundance near edges, (2)
avoidance of harsh microclimate, (3) avoidance of
predators, and (4) edges as movement corridors.
15.2.1 Food abundance
In a Pennsylvania, US, study on Parids versus
edges, Rodewald and Brittingham (2002) showed
that black-capped chickadees and tufted titmice
tended to have slower movement rates when they
were near forest edges (~4.7 m/min) than when
they were away from edges (~5.6 m/min). Based
on this evidence, they suggested that forest edges
functioned more as feeding habitats than move-
ment corridors. On the other side of the Atlantic,
Hansson (1983) found that tits (coal, crested, great,
and willow) occurred more frequently near clearcut
edges than away from them, and interpreted this as
resulting from higher arthropod abundance near
clearcut edges. In support of his hypothesis, he
explained that the association between tree-
gleaners and forest edges was more pronounced
than that for other types of foragers (e.g. grani-
vores), which he attributed to the rich supply of
insects in decaying trees along forest edges.
Thus far, Brotons and Herrando (2003) provide
the best evidence (i.e. with data on food abun-
dance), that winter flocks of coal tits indeed
concentrated their activities near forest edges,
apparently to take advantage of higher food supply.
However, Desrochers and Fortin (2000) found no
increase in foraging success of black-capped chicka-
dees near edges versus chickadees away from
edges. To our knowledge, these are the only studies
examining in detail the question of edges as food
sources for Parids, and it is therefore impossible to
draw general conclusions yet on this phenomenon.
15.2.2 Microclimate
In an early study in Pennsylvania, US, Yahner
(1987) found that black-capped chickadees avoided
the edges of clearcuts, and interpreted this as a pos-
sible avoidance of harsh microclimate. Yahner was
apparently unaware of the earlier work by Grubb
(1977) in New Jersey, in which Grubb showed that
black-capped chickadees and tufted titmice indeed

avoided windward edges of forest patches under
cold and windy weather. Twelve years later, Dolby
and Grubb (1999) replicated the latter study in
Ohio, and again they showed how Carolina
chickadees and tufted titmice avoided forest edges
on windward sides of forest patches when weather
was cold and windy (see also Chapter 16). Dolby
and Grubbs 1999 Ohio study area was highly
fragmented (10% forest cover), however, and
presumably provided no opportunity for its Parid
inhabitants to use forest edges as movement
conduits.
Parid flocks may not only avoid windward forest
edges, but they may also have the ability to
expect that forest edges, especially windward
ones, will provide poor foraging conditions.
Indeed, Brotons et al. (2001) showed that black-
capped chickadees hoard food towards the forest
interior when they have access to a feeder at ca.
30 m from an edge, but they do not exhibit such a
pattern when the feeder is deeper into a forest.
15.2.3 Predator avoidance
Parids foraging outside forest cover have been
shown experimentally to adjust their use of open
habitats with respect to predation risk. Individuals
do not venture out of cover in the presence of a
predator (Desrochers et al. 2002), and will leave the
forest only if in reduced body condition or if the
open offers improved foraging conditions com-
pared to the forest (Todd and Cowie 1990; Turcotte
90
% of movements parallel to edge
80
70
60
50
40
30
20
10
0 flocks tend to move along forest edges (Alberta, Canada).
0 50 100 150
Distance to nearest forest edge (m)
PA R I D D I S T R I B U T I O N A N D M O V E M E N T S 245
and Desrochers 2003). These conclusions fit well
with field observations. Rodrguez et al. (2001)
studied the effect of predation risk on the behavior
of coal, crested, and willow tits at the edge of
patches of mature boreal forest in Sweden. Birds
used the exposed side of the edge (matrix) mainly
during periods with low levels of predation
pressure by European pygmy owls (Glaucidium
passerinum). Although tits did not respond consist-
ently to predator pressure, they clearly avoided
habitats presenting high predation risk and, as a
result, were more or less confined to mature forest
stands. In particular, coal tits behaved more
conservatively (lower exposure) than the other,
larger, two species of tits (Rodrguez et al. 2001). A
similar pattern of predator avoidance was noted in
Spain, especially with blue tits, which foraged
deeper in the canopy when predator pressure was
greatest (Tellera et al. 2001).
15.2.4 Movement corridors
A concentration of Parid occurrences near forest
edges should be found if forest edges act as effect-
ive movement barriers for these birds, because
flocks would tend to move along edges in order to
reach distant habitat patches with the smallest
possible fitness cost. The first quantitative evidence
for edge use as movement conduits for flocks was
presented by Desrochers and Fortin (2000), who
found that black-capped chickadee flocks in
Alberta, Canada, often followed forest edges to
Figure 15.1 A corridor effect: Black-capped Chickadee
200 From Desrochers and Fortin (2000). Printed with
permission from Oikos.
246 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N

avoid flying through open areas, and thereby spent
more time along edges. In support of their interpret-
ation, they showed that chickadee flocks tended to
move parallel to forest edges when they were near
them (Fig. 15.1). Given the high latitude of their
study area (54N) and its similar forest cover type
(deciduous), it would be difficult to imagine that
microclimatic conditions at forest edges were
milder than in the earlier Eurasian studies of edges
versus microclimate (both located south of 45N).
The preceding studies on Parid flocks versus
edges provide first steps towards a better
understanding of the significance of edges,
especially in relation to movements. But they
provide a minimalist interpretation of habitat types
(and their roles for movements), by basically
reducing landscapes to binary objects (forest versus
non-forest). Of course, the reality is more
complicated. For example some habitats may be
used primarily for movement as opposed to
feeding or cover habitats. Additionally, the cost
of traveling through different types of forest may be
highly variable. In south-central Sweden, Rodrguez
et al. (2001) showed that the movements of three

Fort Montmorency
Roads
Rivers
Open
a
are

Mature
dy

Regeneration
stu

Meters
e of

0 50 100 200 300 400

Edg

Figure 15.2 Movements of four flocks of boreal chickadees, at Fort Montmorency (Quebec, Canada), each followed on a single occasion
(JanFeb 2004). Flocks are denoted by different symbols. Each symbol represents a period of 30 seconds. Positions obtained by GPS while
following the flock on showshoes. Note use of regeneration stands and movements at the edge of open areas. Data courtesy of A. Hadley.

species of tits (coal, crested, and willow) were less
frequent in young plantations relative to mature
forests, and therefore that a barrier effect was not
limited to truly open areas. By contrast, movements
of boreal chickadees at Fort Montmorency, Quebec,
Canada, were apparently not impaired by regener-
ating forest stands (27 m), but they did travel along
edges of open areas (Fig. 15.2). Boreal chickadees are
typically found in mature boreal forests (Ficken et al.
1996), but they also venture into earlier successional
stages occasionally (A. Hadley, personal communi-
cation; Fig. 15.2).
There are undoubtedly other studies document-
ing edge use by Parid flocks, but evidence
published so far is inadequate to provide general-
izations regarding edge use, and especially its
causes, by Parids. However, it seems likely that
microclimate (present and future), food abundance,
predator pressure, and barrier effects all affect the
use of forest edges by Parids. Of those four factors,
the barrier effect seems the most difficult to study,
because we normally do not have information on
where the birds are heading when they move, and
how strongly they are motivated to get to their
destination (Desrochers et al. 1999). To circumvent
this problem, we have devised techniques in recent
years where movements are induced experimen-
tally. Early experimentation involved attracting
birds (including black-capped chickadees) to a
speaker located in sites where the birds had to
choose between approaching via a short, but risky
open route (i.e. exposed to predators), or a long but
safer forested route (i.e. providing cover against
predators). This experiment established that black-
capped chickadees were prepared to travel twice as
far, using forest edges, to avoid open areas
(Desrochers and Hannon 1997). Further work
showed that even though black-capped chickadees
are willing to cross gaps, they will seldom venture
over 25 m from forest edges when a forested detour
is available (Blisle and Desrochers 2002).
Although Blisle and Desrochers (2002) did not
find seasonal effects on responses to forest edges, it
is likely that food, microclimate, predation, or
movement barriers will take precedence depending
on the locality and the season, and, as a result, a
single bird species may exhibit great variability in
its association with habitat edges. For example
PA R I D D I S T R I B U T I O N A N D M O V E M E N T S 247
McCollin (1998) argued that while some common
species of European tits (blue, coal, crested, marsh,
and willow) had consistent interior distribution
patterns in woodlands/forests across studies,
great tits were subject to conflicting interior and
edge classifications. Such variability would
explain why leading researchers such as Villard
(1998) started to question the validity of generaliza-
tions such as forest-interior species or edge
species.
15.3 Responses to patches
Finding a link between bird responses to forest
edges and their apparent sensitivity to patch size
(Ambuel and Temple 1983) would be rewarding,
given the allometric relation between the propor-
tion of edge a patch has, and its size. Patch use, like
edge use, has been investigated by ornithologists
for decades, particularly under the paradigm of
Island Biogeography. While Island Biogeography
and the study of patch use in general was mostly
concerned with species diversity (MacArthur and
Wilson 1967), these fields of investigation are
relevant for those of us interested in movements,
because they originate largely from the idea of
isolation. The association between occurrence or
abundance and patch size may simply reflect basic
area requirements by forest birds with all-purpose
territories, such as Parids (Galli et al. 1976). Given
their sometimes large breeding territories, and still
larger flock home ranges, one would expect that
Parids may often exhibit patch-area sensitivity. A
second potential explanation for the association
between occurrence or abundance and patch size
would be edge avoidance, which would lead to the
avoidance of very small patches.
To get a general idea of edge associations in the
Parids, we searched the published literature using
the Science Citation Index Expanded from January
1986 to June 2005 (ISI Web of Science) for studies
with edge, patch, landscape, or fragmenta-
tion and Parid generic names as keywords.
Additionally, one of us (AD) used a database on
studies of edge effects on entire avian communities
and searched it for studies that included Parids. Of
the 49 documented edge associations we found for
12 species of Parids (including observations for all
248 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
seasons), only 10 pointed to the avoidance of edges,
mostly due to predator avoidance (see above),
which suggests that edge avoidance would be a
relatively uncommon explanation for responses of
Parids to patch size.
Our compilation of published work points to a
great diversity of apparent responses to patch size
by Parids, both interspecifically and intraspecifi-
cally (Table 15.1). Nonetheless, it is interesting to
note that 55% of the 75 patch-area associations
documented in 24 studies were significantly (and
strictly) positive. This proportion may be some-
what inflated because of publication bias, but
since the large majority of studies cited in Table 15.1
involved several species of birds, without a focus
on Parids, we believe that this compilation pro-
vides an accurate picture, at least for the species
and regions concerned. Moreover, this proportion
did not depend on whether patch-area sensitivity
was assessed using a species incidence (53%) or its
abundance (50%). It is also noteworthy that none of
the 13 Parid species under consideration exhibited
apparent preference for smaller patch sizes.
However, all of the 10 species for which there was
more than one assessment of patch-area sensitivity,
exhibited somewhat conflicting results, being either
area-independent or area-sensitive, depending on
the study. Long-tailed and marsh tits stood out as
being the most reliably area-sensitive among the
studies concerned (9/11 and 5/7, respectively;
Table 15.1), but none of the authors concerned pro-
posed an explanation for these birds patch-area
sensitivity. Finally, it is interesting to note that there
were four times as many clear cases of area-sensi-
tivity versus insensitivity in winter (i.e. 12/15 ver-
sus 3/15), while cases of area-sensitivity versus
insensitivity were nearly equivalent in summer (i.e.
29/60 versus 28/60). It must, however, be stressed
that only four of the 24 studies reported winter
observations (Table 15.1). Finally, the figures we
report probably best reflect the response of Parids
versus patch size within agricultural landscapes,
where 76% of the 75 patch-area associations were
obtained.
How do we make sense of the variation in area-
sensitivity by Parids? Edge avoidance by Parids,
although uncommon, may partly explain it. For
example in Spain, wintering tits foraging in small
forest patches exhibited more antipredator behav-
ior (e.g. foraged deeper in the canopy) than tits for-
aging in unfragmented forest (Tellera et al. 2001).
Furthermore, under cold and windy winter condi-
tions, forest birds such as Parids may experience
negative microclimatic conditions over the entire
area of the smallest forest patches, especially decidu-
ous ones (Dolby and Grubb 1999), which would
explain the apparently greater area-sensitivity dur-
ing winter (see also Chapter 16). The intraspecific
diversity of responses to patch size may also result
from variation in the spatial arrangement of habitat
patches among studies. Indeed, a group of small
patches can accommodate some individuals if spa-
tially close enough to limit travel cost (Dunning
et al. 1992; Hinsley 2000; see below). Such an influ-
ence, though, like the ones pertaining to the range
of patch sizes and regional amount of habitat
involved, are difficult to assess because the relevant
information is hard, if not impossible, to obtain
from the published accounts.
As with the study of edge use, manipulative
experiments can help better quantify how Parids
and other birds respond to patch attributes such as
their size and isolation. In an intriguing study,
Grubb and Bronson (2001) showed that the site-
tenacity of black-capped chickadees relocated to
small forest patches previously cleared of con-
specifics was unaffected by patch size or isolation.
Their interpretation of those results was that dis-
persing chickadees are not unduly reluctant to
cross substantial gaps between habitat patches
(Grubb and Doherty 1999). However, as acknow-
ledged by Grubb and Bronson, the range of patch
sizes they used was small, which may limit the
scope of their conclusions to the most extreme cases
of forest fragmentation where birds may be con-
strained to manage with such conditions.
15.4 Beyond the patch: response to
landscapes
Forest patches offer a series of measures that can be
related to patterns of distribution of birds, but they
also provide a very incomplete picture of land-
scapes, especially in cases where patches have com-
plex shapes and connections between each other.
For example Whitcomb et al. (1981) reported that
Table 15.1 Distribution of Parids in relation to forest patch size

Species Season Location Matrix Variable Patch size Reference

Long-tailed tit Breeding England A A Bellamy et al. (2000) Ecography 23 130138

Long-tailed tit Breeding England A A Hinsley et al. (1995) J. Avian Biol. 26 94104
Long-tailed tit Breeding Japan A A Kurosawa and Askins (2003) Conserv. Biol. 17 695707
Long-tailed tit Breeding Spain A/N O Brotons et al. (2004) Landscape Ecol. 19 663675
Long-tailed tit Breeding Spain A O Daz et al. (1998) J. Appl. Ecol. 35 562574
Long-tailed tit Breeding Sweden A/F/N O 0 Enoksson et al. (1995) Landscape Ecol. 10 267275
Long-tailed tit Breeding The Netherlands A O 0 Opdam et al. (1985) Biol. Conserv. 34 333352
Long-tailed tit Breeding The Netherlands A O van Dorp and Opdam (1987) Landscape Ecol. 1 5973
Long-tailed tit Winter Spain A A/O Tellera and Santos (1995) Biol. Conserv. 71 6167
Long-tailed tit Winter Spain U O Fernndez-Juricic (2002) coscience 9 450458
Long-tailed tit Winter Spain A A/O Tellera et al. (2001) Oikos 95 253264
Tufted titmouse Breeding Connecticut F? A 0 Askins et al. (1987) Biol. Conserv. 39 129152
Tufted titmouse Breeding Massachussetts U A 0 Tilghman (1987) For. Ecol. Manage. 21 163175
Tufted titmouse Breeding N Carolina N A 0/ Sallabanks et al. (2000) Condor 102 748758
Tufted titmouse Breeding N Jersey, Maryland, A O Robbins et al. (1989) Wildl. Monogr. 103 134
N Carolina
Tufted titmouse Breeding South Carolina A/N O Kilgo et al. (1997) Wildl. Soc. Bull. 25 878885

PA R I D D I S T R I B U T I O N A N D M O V E M E N T S
Tufted titmouse Winter Massachussetts U A 0 Tilghman (1987) For. Ecol. Manage. 21 163175
Coal tit Breeding Japan A A 0 Kurosawa and Askins (2003) Conserv. Biol. 17 695707
Coal tit Breeding Spain A/N O Brotons et al. (2004) Landscape Ecol. 19 663675
Coal tit Breeding Spain A O Daz et al. (1998) J. Appl. Ecol. 35 562574
Coal tit Breeding Sweden A A 0 Berg (1997) Bird Stud. 44 355366
Coal tit Winter Spain A A/O Tellera and Santos (1995) Biol. Conserv. 71 6167
Coal tit Winter Spain U O Fernndez-Juricic (2002) coscience 9 450458
Blue tit Breeding England A A Bellamy et al. (2000) Ecography 23 130138
Blue tit Breeding England A A Hinsley et al. (1995) J. Avian Biol. 26 94104
Blue tit Breeding Spain A/N O 0 Brotons et al. (2004) Landscape Ecol. 19 663675
Blue tit Breeding Spain A O Daz et al. (1998) J. Appl. Ecol. 35 562574
Blue tit Breeding Sweden A/F/N O 0 Enoksson et al. (1995) Landscape Ecol. 10 267275
Blue tit Breeding Sweden A A Berg (1997) Bird Stud. 44 355366

249
 250
L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
Table 15.1 continued

Species Season Location Matrix Variable Patch size Reference

Blue tit Breeding The Netherlands A O 0 Opdam et al. (1985) Biol. Conserv. 34 333352
Blue tit Breeding The Netherlands A O 0 van Dorp and Opdam (1987) Landscape Ecol. 1 5973
Blue tit Winter Spain A A/O 0 Tellera and Santos (1995) Biol. Conserv. 71 6167
Blue tit Winter Spain U O Fernndez-Juricic (2002) coscience 9 450458
Blue tit Winter Spain A A/O 0 Tellera et al. (2001) Oikos 95 253264
Crested tit Breeding Spain A/N O Brotons et al. (2004) Landscape Ecol. 19 663675
Crested tit Breeding Sweden A A 0 Berg (1997) Bird Stud. 44 355366
Crested tit Winter Spain A A/O Tellera and Santos (1995) Biol. Conserv. 71 6167
Crested tit Winter Spain A A/O Tellera et al. (2001) Oikos 95 253264
Great tit Breeding England A A Bellamy et al. (2000) Ecography 23 130138
Great tit Breeding England A A Hinsley et al. (1995) J. Avian Biol. 26 94104
Great tit Breeding Japan A A 0 Kurosawa and Askins (2003) Conserv. Biol. 17 695707
Great tit Breeding Spain A/N O 0 Brotons et al. (2004) Landscape Ecol. 19 663675
Great tit Breeding Spain A O Daz et al. (1998) J. Appl. Ecol. 35 562574
Great tit Breeding Sweden A/F/N O 0 Enoksson et al. (1995) Landscape Ecol. 10 267275
Great tit Breeding Sweden A A - Berg (1997) Bird Stud. 44 355366
Great tit Breeding The Netherlands A O 0 van Dorp and Opdam (1987) Landscape Ecol. 1 5973
Great tit Winter Spain A A/O Tellera and Santos (1995) Biol. Conserv. 71 6167
Great tit Winter Spain U O Fernndez-Juricic (2002) coscience 9 450458
Great tit Winter Spain A A/O Tellera et al. (2001) Oikos 95 253264
Willow tit Breeding Japan A A 0 Kurosawa and Askins (2003) Conserv. Biol. 17 695707
Willow tit Breeding Sweden A O 0 Berg (1997) Bird Stud. 44 355366
Willow tit Breeding The Netherlands A O 0 Opdam et al. (1985) Biol. Conserv. 34 333352
Willow tit Breeding The Netherlands A O van Dorp and Opdam (1987) Landscape Ecol. 1 5973
Marsh tit Breeding England A A Hinsley et al. (1995) J. Avian Biol. 26 94104
Marsh tit Breeding England U A Taylor et al. (1987) Acta Oecol. 8 293299
Marsh tit Breeding Japan A A Kurosawa and Askins (2003) Conserv. Biol. 17 695707
Marsh tit Breeding Sweden A/F/N O 0 Enoksson et al. (1995) Landscape Ecol. 10 267275
Marsh tit Breeding Sweden A O 0 Berg (1997) Bird Stud. 44 355366
Marsh tit Breeding The Netherlands A O Opdam et al. (1985) Biol. Conserv. 34 333352
Marsh tit Breeding The Netherlands A O van Dorp and Opdam (1987) Landscape Ecol. 1 5973
Varied tit Breeding Japan A A 0 Kurosawa and Askins (2003) Conserv. Biol. 17 695707
Black-capped chickadee Breeding Connecticut F? A 0 Askins et al. (1987) Biol. Conserv. 39 129152
Black-capped chickadee Breeding Illinois A A 0/ Blake and Karr (1987) Ecology 68 6471
Black-capped chickadee Breeding Massachussetts U A Tilghman (1987) For. Ecol. Manage. 21 163175
Black-capped chickadee Breeding Michigan N A Crozier and Niemi (2003) Can. J. Zool. 81 441452
Black-capped chickadee Breeding N Jersey, Maryland, F/U/N O 0 Robbins et al. (1989) Wildl. Monogr. 103 134
N Carolina
Black-capped chickadee Breeding Ontario A O 0 Austen et al. (2001) Condor 103 701714
Black-capped chickadee Breeding Rhode Island N A 0 Golet et al. (2001) Wilson Bull. 113 217227
Black-capped chickadee Breeding Saskatchewan A A Hobson and Bayne (2000) Wilson Bull. 112 373387
Black-capped chickadee Winter Massachussetts U A Tilghman (1987) For. Ecol. Manage. 21 163175
Carolina chickadee Breeding N Carolina N A 0 Sallabanks et al. (2000) Condor 102 748758
Carolina chickadee Breeding N Jersey, Maryland, F/U/N O 0 Robbins et al. (1989) Wildl. Monogr. 103 134
N Carolina
Carolina chickadee Breeding South Carolina A/N O Kilgo et al. (1997) Wildl. Soc. Bull. 25 878885
Boreal chickadee Breeding Saskatchewan A A 0 Hobson and Bayne (2000) Wilson Bull. 112 373387

PA R I D D I S T R I B U T I O N A N D M O V E M E N T S
Chestnut-backed chickadee Breeding California F A Rosenberg and Raphael (1986) Wildlife 2000, 263272

Responses can be positive (), neutral (0), or negative () associations. A positive response means greater rate of occurrence (Variable O) or abundance (Variable A) in larger forest
patches. Sampled forest patches were surrounded by one of the following matrices: agricultural (A), forestry (F), natural (N), or urban (U). We searched the published, peer-reviewed literature
based on the Science Citation Index Expanded (January 1986 to May 2005; ISI Web of Science) for studies with edge, patch, landscape, or fragmentation, and Parid generic names as
keywords. Additionally, one of us (AD) used a database on landscape use studies on entire avian communities and searched it for studies that included Parids.

251
252 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
tufted titmice occurred in forest patches sometimes
smaller than their territory size. Those puzzling
occurrences were interpreted as involving non-ter-
ritorial birds, but they may also have been birds
whose territories were spread over a number of dis-
crete patches. In Finland, Siffczyk et al. (2003) found
that willow tit flocks responded to habitat loss by
enlarging their home range size.
Networks of forest patches may pose challenges
for wintering Parids whose flock territories may
encompass several forest patches. For example
crossing gaps between forest patches may incur
predation as well as physiological costs. By meas-
uring how far into the open black-capped chicka-
dees were willing to go to obtain a sunflower seed,
Turcotte and Desrochers (2003) concluded that
chickadees in highly deforested landscapes experi-
enced greater food stress than chickadees in well-
forested landscapes. They interpreted their results
as the outcome of greater loss of energy caused by
repeated flights across gaps in fragmented home
ranges, combined by risk-awareness in open areas.
Having to cross gaps may reduce fitness not only
for wintering Parids, but also through increased
cost (in energy and time) incurred during central-
place foraging, as shown by modeling on great tits
(Hinsley 2000).
Of course, the greatest movement challenge
faced by forest birds such as Parids may come at the
time of natal dispersal. It is easy to imagine that
juvenile Parids, which often disperse at distances of
several kilometers or more (e.g. Verhulst et al. 1997),
may experience major challenges posed by habitat
isolation. For example in Belgium, Lens and
Dhondt (1994) found that juvenile crested tits born
in forest fragments dispersed later than con-
specifics born in contiguous forests, and immigra-
tion into forest fragments was also delayed. Lens
and Dhondt interpreted this result as indicative of
lower habitat quality in fragments, possibly associ-
ated to a barrier effect preventing birds to dis-
perse early. In accord with the barrier effect,
Matthysen (2002) found in another Belgian study
that the likelihood that blue and great tits emigrate
out of their natal patch was independent of the dis-
tance separating their birth site from the forest
edge. Indeed, if edges were highly permeable, we
may have expected that individuals born close to
an edge to show a greater probability of emigration
than individuals born toward the interior of the
patch.
In the last 20 years, Geographic Information
Systems (GIS) have provided more sophisticated
tools for analyzing bird distributions over spatial
expanses beyond the patches or territories occupied
by individual birds. Do analyses of Parid distribu-
tion at the landscape scale (e.g. within a radius of
500 m) provide evidence for landscape-sensitiv-
ity? As for edge and patch size effects, the answer
has to be, sometimes (Table 15.2). The only pattern
common to all Parids is that they are not preferen-
tially associated to landscapes with small amounts
of habitat. Indeed, only three out of the 54 associ-
ations between occurrence and amount of forest
within a fixed radius documented in 28 studies
were negative. Moreover, clearly neutral and
clearly positive responses to amount of forest
composed 46% and 41% of cases, respectively.
Although the proportion of positive associations
did not depend on whether landscape-sensitivity
was quantified using a species occurrence (41%) or
its abundance (48%), it depended on matrix type.
Positive associations were twice as frequent in
landscapes strictly managed for agriculture (43%
of 23 cases) than for forestry (20% of 10 cases). Yet,
this difference may not only result from a matrix-
type effect, but also from a lower regional amount
of forest habitat within the agricultural landscapes
used in the studies we compiled. As for patch-area
associations (see above), though, published
accounts often lack the details that would allow us
to conduct a proper meta-analysis, and thereby
avoid confounding effects and reach clearer
conclusions.
In spite of this drawback, it is interesting to note
that 11 of the 14 species studied so far sometimes
exhibited positive associations with the amount of
forest habitat in the landscape. Of 12 species for
which we have occurrence or abundance data from
more than one study, however, only three had con-
sistent relationships between occurrence or abun-
dance and area of forest habitat within a fixed
radius (500 m; Table 15.2). These include long-
tailed (5/5), crested (3/4), and marsh tits (3/4)
which generally were more abundant in areas with
greater habitat. It is noteworthy that long-tailed
Table 15.2 Distribution of Parids in relation to landscape composition and configuration (amount of edges and patch isolation)

Species Season Location Matrix Variable % Forest Configuration Reference

Long-tailed tit Breeding England A O Hedgerows Hinsley et al. (1995) J. Avian Biol. 26 94104
Long-tailed tit Breeding Spain A/N O Brotons et al. (2004) Landscape Ecol. 19 663675
Long-tailed tit Breeding Sweden A/F/N O Isolation () Enoksson et al. (1995) Landscape Ecol. 10 267275
Long-tailed tit Breeding Sweden F O Isolation () Jansson and Angelstam (1999) Landscape Ecol. 14 283290
Long-tailed tit Breeding The Netherlands A O Isolation () Opdam et al. (1985) Biol. Conserv. 34 333352
Long-tailed tit Breeding The Netherlands A O Isolation () van Dorp and Opdam (1987) Landscape Ecol. 1 5973
Tufted titmouse Breeding Maryland A A 0 Isolation (0) Lynch and Whigham (1984) Biol. Conserv. 28 287324
New Jersey
Tufted titmouse Breeding Maryland, F/U/N O 0 Isolation (0) Robbins et al. (1989) Wildl. Monogr. 103 134
N. Carolina
Tufted titmouse Breeding Oklahoma A A Coppedge et al. (2002) Ecol. Appl. 11 4759
Tufted titmouse Breeding S. Carolina A/N A/O 0 Isolation (0/) Kilgo et al. (1997) Wildl. Soc. Bull. 25 878885
Coal tit Breeding Spain A/N O 0 Brotons et al. (2004) Landscape Ecol. 19 663675
Coal tit Breeding Sweden A A Berg (1997) Bird Stud. 44 355366
Coal tit Breeding Sweden U O Mrtberg (2001) Landscape Ecol. 16 193203

PA R I D D I S T R I B U T I O N A N D M O V E M E N T S
Blue tit Breeding England A A Hedgerows () Hinsley et al. (1995) J. Avian Biol. 26 94104
Blue tit Breeding Spain A/N O 0 Brotons et al. (2004) Landscape Ecol. 19 663675
Blue tit Breeding Sweden A A - Berg (1997) Bird Stud. 44 355366
Blue tit Breeding Sweden A/F/N O 0 Isolation (0) Enoksson et al. (1995) Landscape Ecol. 10 267275
Blue tit Breeding The Netherlands A O 0 Isolation (0) van Dorp and Opdam (1987) Landscape Ecol. 1 5973
Siberian tit Breeding Finland A/F/N A Brotons et al. (2003) Landscape Ecol. 18 377393
Crested tit Breeding Finland A/F/N A Brotons et al. (2003) Landscape Ecol. 18 377393
Crested tit Breeding Spain A/N O 0 Brotons et al. (2004) Landscape Ecol. 19 663675
Crested tit Breeding Sweden A A Berg (1997) Bird Stud. 44 355366
Crested tit Breeding Sweden U O Mrtberg (2001) Landscape Ecol. 16 193203
Great tit Breeding England A A Hedgerows () Hinsley et al. (1995) J. Avian Biol. 26 94104

253
 254
L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
Table 15.2 continued

Species Season Location Matrix Variable % Forest Configuration Reference

Great tit Breeding Spain A/N O 0 Brotons et al. (2004) Landscape Ecol. 19 663675
Great tit Breeding Sweden A A 0 Berg (1997) Bird Stud. 44 355366
Great tit Breeding Sweden F A/O 0 Edenius and Elmberg (1996) Landscape Ecol. 11 325338
Great tit Breeding Sweden A/F/N O 0 Isolation (0) Enoksson et al. (1995) Landscape Ecol. 10 267275
Great tit Breeding The Netherlands A O 0 Isolation (0) van Dorp and Opdam (1987) Landscape Ecol. 1 5973
Willow tit Breeding Sweden A O Berg (1997) Bird Stud. 44 355366
Willow tit Breeding Sweden F A/O 0 Edenius and Elmberg (1996) Landscape Ecol. 11 325338
Willow tit Breeding Sweden U O Mrtberg (2001) Landscape Ecol. 16 193203
Willow tit Breeding The Netherlands A O Isolation (0) Opdam et al. (1985) Biol. Conserv. 34 333352
Willow tit Breeding The Netherlands A O 0 Isolation (0) van Dorp and Opdam (1987) Landscape Ecol. 1 5973
Marsh tit Breeding Sweden A O - Berg (1997) Bird Stud. 44 355366
Marsh tit Breeding Sweden A/F/N O Isolation () Enoksson et al. (1995) Landscape Ecol. 10 267275
Marsh tit Breeding Sweden U O Mrtberg (2001) Landscape Ecol. 16 193203
Marsh tit Breeding The Netherlands A O Isolation () Opdam et al. (1985) Biol. Conserv. 34 333352
Marsh tit Breeding The Netherlands A O Isolation () van Dorp and Opdam (1987) Landscape Ecol. 1 5973
Black-capped chickadee Breeding Alberta F A Isolation () Schmiegelow et al. (1997) Ecology 78 19141932
Black-capped chickadee Breeding Saskatchewan A A 0 (3/4 years) Hobson and Bayne (2000) Wilson Bull. 112 373387
Black-capped chickadee Breeding Maine F A/O 0 Hagan et al. (1996) Conserv. Biol. 10 188202
Black-capped chickadee Breeding New Jersey, F/U/N O 0 Isolation (0) Robbins et al. (1989) Wildl. Monogr. 103 134
Maryland,
N. Carolina
Black-capped chickadee Breeding Ontario A O 0 Austen et al. (2001) Condor 103 701714
Black-capped chickadee Breeding S. Carolina F O 0 Mitchell et al. (2001) Ecol. Appl. 11 16921708
Black-capped chickadee Breeding Wisconsin N A Hedgerows () Hawrot and Niemi (1996) Auk 113 586598
Black-capped chickadee Winter Quebec A A /0/- Hedgerows (/0/) Turcotte and Desrochers (2005) Ecography 28 129140
Black-capped chickadee Year round Wisconsin A A - Howe (1984) Ecology 65 15851601
Carolina chickadee Breeding Maryland A A 0/ Isolation (0) Lynch and Whigham (1984) Biol. Conserv. 28 287324
Carolina chickadee Breeding N. Carolina, N A 0 Patch shape, Lichstein et al. (2002) Ecol. Appl. 12 836857
Tennessee isolation
Carolina chickadee Breeding New Jersey, F/U/N O 0 Isolation (0) Robbins et al. (1989) Wildl. Monogr. 103 134
Maryland,
N. Carolina
Carolina chickadee Breeding Oklahoma A A Coppedge et al. (2002) Ecol. Appl. 11 4759
Carolina chickadee Breeding S. Carolina F O 0 Mitchell et al. (2001) Ecol. Appl. 11 16921708
Mountain chickadee Breeding Wyoming F A 0/ Hedgerows (0/-) Keller (1992) Condor 94 5565
Boreal chickadee Breeding Saskatchewan A A 0 Hobson and Bayne (2000) Wilson Bull. 112 373387
Boreal chickadee Breeding Quebec F O 0 Patch shape (0) Drolet et al. (1999) Condor 101 699704
Chestnut-backed chickadee Breeding British Columbia N/W A Isolation (-) Martin et al. (1995) Oikos 72 115131
Chestnut-backed chickadee Breeding California F A 0 Rosenberg and Raphael (1986) Wildlife 2000: modeling
habitat relationships of terrestrial vertebrates 263272
Chestnut-backed chickadee Breeding Oregon F A Hedgerows (0) McGarigal and McComb (1995) Ecol. Monogr. 65 235260

Responses can be positive (), neutral (0) or negative (-). A positive response means greater rate of occurrence (Variable O) or abundance (Variable A) in larger forest patches. Sampled
forest patches were surrounded by an agricultural (A), forestry (F), natural (N) or urban (U) matrix. See caption of Table 15.1 for details on literature search.

PA R I D D I S T R I B U T I O N A N D M O V E M E N T S
255
256 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
and marsh tits have been shown to be generally
sensitive to patch size as well (see Table 15.2). The
influence of the overall isolation of habitat patches
or the amount of hedgerows on the distribution of
Parids are for now difficult to assess, especially
given the diversity of responses and the lack of
information on the level of intercorrelation among
the variables used to describe landscape structure.
Finally, all but two of the 28 compiled studies were
solely conducted during the breeding season.
Given that landscape-sensitivity was found to vary
for black-capped chickadees between the onset and
the middle of the winter in Quebec (Turcotte and
Desrochers 2005) and that Carolina chickadee win-
ter survival increased with woodlot area in Ohio
(Doherty and Grubb 2002b), there is certainly a
need to put more effort into characterizing the
effect of landscape structure on the distribution of
Parids at this crucial time of the year.
There are obvious limits to inferences on land-
scape responses based on species distributions
alone. With increasing amounts of data on move-
ment decisions as well as simulation tools, it has
become possible to ask how birds such as Parids
tend to respond to real-life, spatially explicit chal-
lenges. Recently, we were able to induce move-
ments by black-capped chickadees, under
controlled conditions, and parameterize their
movement decisions near gaps in the canopy
(Blisle and Desrochers 2002). We have evidence
suggesting that there is a threshold distance of ca.
25 m into open areas beyond which black-capped
chickadees seldom fly when a detour under forest
cover is available. When no such detour is avail-
able, we found that the likelihood that black-
capped chickadees move between two woodlots
decreases at an increasing rate with the size of gap
which must be crossed (Desrochers and Hannon
1997; St. Clair et al. 1998).
Simulating the experiments above using a spa-
tially explicit, individual-based approach and the
SELES language (Fall and Fall 2001), M. Blisle and
A. Fall were able to parameterize a cost function for
back-capped chickadees moving within agricul-
tural landscapes (unpublished data). This simula-
tion work suggests that the relative cost of moving
1 m in open habitat increases exponentially with
the distance to all forest edges (Fig. 15.3); what is
more, these results came from consideration of
spatial landscapes with a radius less than 0.5 km.
By calculating the cost of moving through each
pixel of a grid-based representation of a landscape
(e.g. a classified Landsat TM satellite image), it
becomes possible to find the least-cost path
between any two points, such as two forest patches.
This leads to many research opportunities as
least-cost paths can be used to weigh alternative
pathways, quantify patch isolation and assess
landscape functional connectivity at relatively
small scales (e.g. a few home ranges; Fig. 15.4).
Furthermore, least-cost paths could help us better
predict Parid distribution along forest edges and in
highly fragmented landscapes, as they could be
used to predict how an individual should respond
to predation risk as a function of its distance to
all forest edges. In addition, such paths could be
used to assess the movement cost of territories
composed of several small forest patches (i.e. the
cost of landscape supplementation sensu Dunning
et al. 1992).
While our previous experiments on responses to
forest edges provide useful parameters for simula-
tions, they still need to be confronted to empirical
data on large-scale movements. One way to study
movement at spatial scales relevant to dispersal is
to induce them by relocation experiments, thus
forcing birds to home by flying through selected
landscapes. Homing experiments have been
90
80
70
60
Relative cost
50
40
30
20
10
0
0 100 200 300 400 500
Distance to all forest edges (m)
Figure 15.3 Cost function for black-capped chickadees moving in
the open within agricultural landscapes. The cost of moving one
distance unit under forest cover was set to one (M. Blisle and
A. Fall unpublished data).

180
160
Mean least cost (x103)
140
120
100
80
60
40
20
0 translocation experiments (Blisle and St Clair 2001;
0 10 20 30 40 50 60 70 80 90 100
Forest cover (%)
Figure 15.4 Influence of landscape composition on the
functional connectivity of agricultural landscapes for black-capped
chickadees as assessed by the cost function shown in Fig. 15.3.
With the help of A. Fall and using the SELES language, we created
810 neutral landscapes composed of 100 100 square pixels
covering 625 m2. Landscapes were composed of forest and open
habitat only. Ninety landscapes were allocated to each of nine
forest cover categories with a contagion index of 0.95. We then
placed at random 100 cyber-chickadees on the south side and asked
them to choose at random a destination on the north side.
Cyber-chickadees were finally asked to find the least cost path
between their start and end points. As expected, the cost increased
as forest cover decreased. Yet, it is only when forest cover reached
30% that some landscapes showed a substantial increase in
cost. Interestingly, it is not only the mean cost of paths within a
given landscape that increased as forest cover decreased, but also
the absolute variation in mean cost among landscapes. Indeed, some
landscapes with only 5% or 20% forest cover presented the same
mean level of functional connectivity as landscapes with 30% or
70% forest cover, respectively.
conducted mostly for the study of navigation (Able
1995), and they have also historically been done
with wintering Parids (Odum 1941 and references
therein). The Parid homing work by Odum and
others showed that black-capped chickadees were
not site-tenacious during winter; however, they did
not offer insights on the responses of these birds to
gaps in the canopy. More recently, we investigated
homing by territorial, mated male black-capped
chickadees, specifically with the purpose of testing
for a barrier effect caused by forest fragmentation
within agricultural landscapes (Blisle et al. 2001).
Overall, we found that homing time (over 14 km)
increased with decreasing forest cover. The greatest
discrepancy in homing rate was observed after
30 h, when only 33% of the 18 individuals translo-
cated in landscapes with less than 50% forest cover
had returned compared to 87% of the 23 individ-
PA R I D D I S T R I B U T I O N A N D M O V E M E N T S 257
uals in landscapes with more than 50% forest cover.
The most parsimonious explanation for this
contrast is that habitat loss and fragmentation
impaired the movement of black-capped chicka-
dees. If so, low forest cover would affect the ability
of these birds to find and select resources of high
quality, including territories (Blisle et al. 2001).
Given that other forest bird species differ in their
response to landscape structure when subjected to
Gobeil and Villard 2002), the latter should be
replicated with other species of Parids in order to
assess the generality of our conclusions.
Some individuals may suffer more than others
from habitat fragmentation. For example floaters
have been recorded in wintering populations of
chickadees (Smith 1984) and tits (Ekman et al. 1981),
and shown to have daily fattening patterns sug-
gesting that they face lower food predictability than
residents (Broggi and Brotons 2001; see Chapters 16
and 17 for more on fat deposition versus habitat
quality). By definition, floaters will have much
larger home ranges than other individuals, and will
therefore need to cope with habitat barriers more
frequently. Like Rodrguez et al. (2001), we expect
that forest fragmentation will hurt floaters
more than flock residents (Smith 1984) and there-
fore may significantly alter social relationships.
Furthermore, fragmentation may affect mating
strategies among flock members, for example by
imposing greater movement costs that counter the
potential benefits of seeking copulations with
conspecific neighbors (K. Otter, personal commu-
nication). Finally, Pravosudova et al. (1999) provide
an excellent example of how forest fragmentation
may impact the genetic composition of tufted
titmouse flocks either through lower nesting suc-
cess or parentoffspring relations after fledging.
The consequences of landscape changes such as
fragmentation on animal social organization
remain virtually unknown and Parids offer excel-
lent opportunities for advances in this field.
15.5 Parids as leaders of other
forest birds
Field naturalists have often observed that non-
breeding Parids do not generally travel alone.
258 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
Instead, they are often accompanied by other forest
birds, resident or migrant. Thus, Parid movements
may have implications for the movements of other
species, especially in the postfledging (dispersal)
and migration periods. Ornithologists have often
wondered whether Parids lead other species in
their movements, possibly because other species
should benefit from their knowledge of local
dangers and opportunities. In Louisiana,
Maryland, and Maine, US, Morse (1970) had
evidence showing that black-capped chickadees,
Carolina chickadees, and tufted titmice generally
led other species in mixed flocks. In
Pennsylvania, US, Rodewald and Brittingham
(2002) also showed that black-capped chickadees
and tufted titmice led mixed-species flocks most of
the time (68%). Additionally, Dolby and Grubb
(2000) showed that white-breasted nuthatches (Sitta
carolinensis) were less reluctant to forage outside
forest cover in the presence of tufted titmice, even
after controlling for flock-size effects. Analogously,
Sieving et al. (2004) showed that the presence of
tufted titmice facilitated the movement of other
birds, mostly migrants, across gaps in the forest
canopy. However, J. Bourque and C. Aznar (unpub-
lished data), in a series of playback experiments
using chickadee mobbing calls, found that the
presence of black-capped chickadees did not influ-
ence gap-crossing behavior of other species. It is
difficult to tell at this time whether this pattern of
leaderfollower is general with mixed-species
flocks outside of North America, because of the
small number of published studies of this phenom-
enon to date. In Europe, it is also possible that
leaderfollower patterns occur among different
species of Parids, because non-breeding flocks
generally comprise several species of Parids
(e.g. Mnkknen et al. 1996).
15.6 Conclusions
Neither Eurasian nor North American Parids exhibit
consistent patterns in distribution and movement
in relation to edges, patches, and landscapes. Near
habitat edges, movements of Parids often result
from food distribution and microclimate, and an
avoidance of open areas and edges mediated by
predator avoidance. Avoiding open areas may
explain why Parids will often travel along forest
edges, around open areas, especially outside the
breeding season, when flock movements usually
cover much larger areas than breeding territories.
We thought that edge avoidance would be a candi-
date mechanism for the patch-area sensitivity
found in about half of Parid populations studied,
but it appeared irrelevant in the large majority of
cases. We propose the spatial arrangement of
patches as an alternative explanation for patch-area
sensitivity by Parids. In support of this, we showed
that larger-scale (landscape) studies yielded twice
as many cases of area-sensitivity (within a fixed
radius) by Parids in agricultural (highly frag-
mented) than in forestry (connected) landscapes.
Also, our simulation work clearly shows that
landscape pattern (with a fixed amount of habitat)
leads to substantial variation in functional
connectivity, especially at low amounts of habitat
cover, a situation typical of most distribution
studies on forest birds.
We found no evidence of contrast between
Eurasian and North American Parids, as far
as landscape distribution and movement are
concerned. In fact, intraspecific variation in the
movement ecology of Parids appears as important
as interspecific variation. The only patterns valid
among Parids were either trivial, that is lack of
specific associations to small habitat patches, or of
little-understood significance, that is the role
played by Parids as leaders for the movements of
other species outside the breeding season.
Although differences in methodology among
studies may explain part of the variability among
published results, it is likely that regional effects,
such as climate, predator pressure, and landscape
type, play a major role in shaping movement con-
straints and opportunities for Parids. Furthermore,
our own work and the literature we reviewed
here do not generally address differences in habitat
quality, which may prove to be key in understand-
ing Parid movements (see Chapter 16). In short, the
movement ecology of Parids is highly idiosyncratic.
Where do we go from here? As with the study of
larger problems of avian landscape ecology, the
time is ripe for behavioral experiments and meta-
analyses in search for more general patterns, taking
advantage of differences among populations

(Desrochers et al. 1999, Blisle 2005). Parids are
probably the best-suited avian family to make
progress in this field, given their wide distribution
and adaptability to experimental setups, as well as
the abundance of baseline data. Since there is as
much variability in landscape distribution within
as among Parid species, one focus should be on
intraspecific variation for widespread, and well-
studied species, such as black-capped chickadees
and blue tits. Additionally, dozens of essentially
unstudied species in mainland Asia and in Africa
would provide an excellent opportunity to test
some of the ideas presented in this chapter and
generalize to new systems. Further, Parids offer the
opportunity of studying how birds respond to
given landscape structures throughout their annual
cycle, and, hence, how landscape structure affects
trade-offs among conflicting demands. Published
work rarely provides details on landscape
structure, and those details may be difficult, or
impossible, to obtain. We may thus need to obtain
new distribution data in a variety of regional
landscapes in order to progress in the study of
Parids as models for the study of avian movement
ecology.
References
Able, K. P. (1995). Orientation and navigation: a perspec-
tive on fifty years of research. Condor, 97, 592604.
Ambuel, B. A. and Temple, S. A. (1983). Area-dependent
changes in the bird communities and vegetation of
southern Wisconsin forests. Ecology, 64, 10571068.
Anderson, S. H., Mann, K., and Shugart, H. H., Jr (1977).
The effect of transmission-line corridors on bird popu-
lations. American Midland Naturalist, 79, 216221.
Blisle, M. and Desrochers, A. (2002). Gap-crossing deci-
sions by forest birds: an empirical basis for parameter-
izing spatially-explicit, individual-based models.
Landscape Ecology, 17, 219231.
Blisle, M. and St Clair, C. C. (2001). Cumulative effects of
barriers on the movements of forest birds. Conservation
Ecology, 5, 9. [online] URL: http://www.consecol.org/
vo15/iss2/art9.
Blisle, M., Desrochers, A., and Fortin, M.-J. (2001).
Influence of forest cover on the movements of forest
birds: a homing experiment. Ecology, 82, 18931904.
Broggi, J. and Brotons, L. (2001). Coal tit fat-storing
patterns during the non-breeding season: the role of
residence status. Journal of Avian Biology, 32, 333337.
PA R I D D I S T R I B U T I O N A N D M O V E M E N T S 259
Brotons, L. and Herrando, S. (2003). Effect of increased
food abundance near forest edges on flocking patterns
of coal tit Parus ater winter groups in mountain conifer-
ous forests. Bird Study, 50, 106111.
Brotons, L., Desrochers, A., and Turcotte, Y. (2001). Food
hoarding behaviour of black-capped chickadees (Poecile
atricapillus) in relation to forest edges. Oikos, 95,
511519.
Cramp, S., Simmons, K. E. L., Perrins, C. M., and Brooks,
D. J., eds (19781997). Handbook of the Birds of the Western
Palearctic. Oxford University Press, Oxford, UK.
del Hoyo, J., Elliott, A., Sargatal, J., and Christie, D., eds
(1992-present). Handbook of the Birds of the World. Lynx
Edicions, Barcelona, Spain.
Desrochers, A. and Fortin, M.-J. (2000). Understanding
avian responses to forest boundaries: a case study with
chickadee winter flocks. Oikos, 91, 376384.
Desrochers, A. and Hannon, S. J. (1997). Gap crossing
decisions by forest songbirds during the post-fledging
period. Conservation Biology, 11, 12041210.
Desrochers, A., Blisle, M., and Bourque, J. (2002). Do
mobbing calls affect the perception of predation risk by
forest birds? Animal Behaviour, 64, 709714.
Desrochers, A., Hannon, S. J., Blisle, M., and St Clair,
C. C. (1999). Movement of songbirds in fragmented
forests: Can we scale up from behaviour to explain
occupancy patterns in the landscape? In: N. J. Adams
and R. H. Slotow, ed. Proceedings of the 22nd International
Ornithological Congress, Durban, pp. 24472464. BirdLife
South Africa, Johannesburg.
Doherty, P. F., Jr and Grubb, T. C., Jr (2002a). Nest usurp-
ation is an edge effect for Carolina chickadees Poecile
carolinensis. Journal of Avian Biology, 33, 7782.
Doherty, P. F., Jr and Grubb, T. C., Jr (2002b). Survivorship
of permanent-resident birds in a fragmented forested
landscape. Ecology, 83, 844857.
Dolby, A. S. and Grubb, T. C. (1999). Effects of winter
weather on horizontal vertical use of isolated forest
fragments by bark-foraging birds. Condor, 101, 408412.
Dolby, A. S. and Grubb, T. C. (2000). Social context affects
risk taking by a satellite species in a mixed-species for-
aging group. Behavioral Ecology, 11, 110114.
Dunning, J. B., Danielson, B. J., and Pulliam, H. R. (1992).
Ecological processes that affect populations in complex
landscapes. Oikos, 65, 169175.
Ekman, J., Cederholm, G., and Askenmo, C. (1981).
Spacing and survival in winter groups of willow tit
Parus montanus and crested tit P. cristatusa removal
study. Journal of Animal Ecology, 50, 19.
Fall, A. and Fall, J. (2001). A domain-specific language for
models of landscape dynamics. Ecological Modelling,
137, 121.
260 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
Ficken, M. S., McLaren, M. A., and Hailman, J. P. (1996).
Boreal chickadee. In: A. Poole and F. Gill, eds. The Birds
of North America, No. 254, pp. The Academy of Natural
Sciences, The American Ornithologists Union,
Philadelphia, PA, Washington, D.C.
Galli, A. E., Leck, C. F., and Forman, R. T. T. (1976). Avian
distribution patterns in forest islands of different sizes
in central New Jersey. Auk, 93, 356364.
Gobeil, J.-F. and Villard, M.-A. (2002). Permeability of
three boreal forest landscape types to bird movements
as determined from experimental translocations. Oikos,
98, 447458.
Greenwood, P. J., Harvey, P. H., and Perrins, C. M. (1979).
The role of dispersal in the great tit (Parus major): the
causes, consequences and heritability of natal dispersal.
Journal of Animal Ecology, 48, 123142.
Grubb, T. C., Jr (1977). Weather dependent foraging
behavior of some birds wintering in a deciduous wood-
land: horizontal adjustments. Condor, 79, 271274.
Grubb, T. C., Jr and Bronson, C. L. (2001). On cognitive
conservation biology: why chickadees leave a patch of
woodland. Journal of Avian Biology, 32, 372376.
Grubb, T. C., Jr and Doherty, P. F., Jr (1999). On home-
range gap-crossing. Auk, 116, 618628.
Hansson, J. (1983). Bird numbers across edges between
mature conifer forests and clearcuts in central Sweden.
Ornis Scandinavica, 14, 97103.
Harris, R. and Reed, J. M. (2002). Behavioral barriers to
non-migratory movements of birds. Annales Zoologici
Fennici, 39, 275290.
Hinsley, S. A. (2000). The costs of multiple patch use by
birds. Landscape Ecology, 15, 765775.
Imbeau, L., Drapeau, P., and Mnkknen, M. (2003). Are
forest birds categorised as edge species strictly asso-
ciated with edges? Ecography, 26, 514520.
Lens, L. and Dhondt, A. A. (1994). Effects of habitat frag-
mentation on the timing of crested tit Parus cristatus
natal dispersal. Ibis, 136, 147152.
Leopold, A. (1933). Game Management. Charles Scribners
Sons, New York, NY, USA.
MacArthur, R. and Wilson, E. O. (1967). The Theory of
Island Biogeography. Princeton University Press,
Princeton, NJ, USA.
Matthysen, E. (2002). Boundary effects on dispersal
between habitat patches by forest birds (Parus major,
P. caeruleus). Landscape Ecology, 17, 509515.
McCollin, D. (1998). Forest edges and habitat selection in
birds: a functional approach. Ecography, 21, 247260.
Mnkknen, M., Forsman, J. T., and Helle, P. (1996).
Mixed-species foraging aggregations and heterospecific
attraction in boreal bird communities. Oikos, 77,
127136.
Morse, D. H. (1970). Ecological aspects of some mixed-
species foraging flocks of birds. Ecological Monographs,
40, 119168.
Odum, E. P. (1941). Winter homing behavior of the
chickadee. Bird-Banding, 12, 113119.
Pearson, S. M. (1993). The spatial extent and relative
influence of landscape-level factors on wintering bird
populations. Landscape Ecology, 8, 318.
Poole, A., Stettenheim, P., and Gill, F., eds (19922003). The
Birds of North America. The Academy of Natural
Sciences, The American Ornithologists Union,
Philadelphia, PA, Washington, D.C.
Postma, E. and van Noordwijk, A. J. (2005). Gene flow
maintains a large genetic difference in clutch size at a
small spatial scale. Nature, 433, 6568.
Pravosudova, E. V., Grubb, T. C., Jr, Parker, P. G., and
Doherty, P. F., Jr (1999). Patch size and composition of
social groups in wintering tufted titmice (Baeolophus
bicolor). Auk, 116, 11521155.
Rodewald, P. G. and Brittingham, M. C. (2002). Habitat
use and behavior of mixed species landbird flocks
during fall migration. Wilson Bulletin, 114, 8798.
Rodrguez, A., Andrn, H., and Jansson, G. (2001).
Habitat-mediated predation risk and decision making
of small birds at forest edges. Oikos, 95, 383396.
Sieving, K. E., Contreras, T. A., and Maute, K. L. (2004).
Heterospecific facilitation of forest boundary crossing
by mobbing understory birds in North-central Florida.
Auk, 121, 738751.
Siffczyk, C., Brotons, L., Kangas, K., and Orell, M. (2003).
Home range size of willow tits: a response to winter
habitat loss. Oecologia, 136, 635642.
Smith, S. M. (1984). Flock switching in chickadees: why be
a winter floater? American Naturalist, 123, 8198.
St Clair, C. C., Blisle, M., Desrochers, A., and Hannon,
S. J. (1998). Winter responses of forest birds to habitat
corridors and gaps. Conservation Ecology, 2, 13. [online]
URL: http://www.consecol.org/vo12/iss2/art13.
Tellera, J. L., Virgs, E., Carbonell, R., Prez-Tris, J., and
Santos, T. (2001). Behavioural responses to changing
landscapes: flock structure and anti-predator strategies
of tits wintering in fragmented forests. Oikos, 95, 253264.
Todd, I. A. and Cowie, R. J. (1990). Measuring the risk of
predation in an energy currency: field experiments with
foraging blue tits, Parus caeruleus. Animal Behaviour, 40,
112117.
Turcotte, Y. and Desrochers, A. (2003). Landscape-
dependent response to predation risk by forest birds.
Oikos, 100, 614618.
Turcotte, Y. and Desrochers, A. (2005). Landscape-
dependent distribution of northern forest birds in
winter. Ecography, 28, 129140.

Verhulst, S., Perrins, C. M., and Riddington, R. (1997).
Natal dispersal of great tits in a patchy environment.
Ecology, 78, 864872.
Villard, M.-A. (1998). On forest-interior species, edge
avoidance, area-sensitivity, and dogmas in avian con-
servation. Auk, 115, 801805.
Weise, C. M. and Meyer, J. R. (1979). Juvenile dispersal
and development of site-fidelity in the black-capped
Chickadee. Auk, 96, 4055.
PA R I D D I S T R I B U T I O N A N D M O V E M E N T S 261
Whitcomb, R. F., Robbins, C. S., Lynch, J. F., Whitcomb,
B. L., Klimkiewicz, M. K., and Bystrak, D. (1981). Effects
of forest fragmentation on avifauna of the Eastern
deciduous forest. In: R. L. Burgess and D. M. Sharpe,
eds. Forest Island Dynamics in Man-dominated Landscapes,
pp. 125205. Springer-Verlag, New York, NY, USA.
Yahner, R. H. (1987). Use of even-aged stands by winter
and spring bird communities. Wilson Bulletin, 99,
218232.
This page intentionally left blank
 CHAPTER 16
Winter adaptations in chickadees
and titmice and the added effect
of habitat fragmentation
Jennifer R. Olson and Thomas C. Grubb, Jr
16.1 Introduction
Many North American Paridae have ranges that
expose them to temperate winter seasons.
Chickadees and titmice possess several physiologi-
cal and behavioral adaptations that allow them to
manage the reduced food supply and high ther-
moregulatory demands of this environment. Yet,
increased habitat fragmentation posed by agricul-
tural and urban expansion also presents a further
stress to these populations. Furthermore, the inter-
action between responses to winter and responses
to fragmentation is assumed to be a major factor
constraining populations that are presented with
both of these tasks. With this chapter, we review
research on physiological adaptations to reduced
temperatures, and then address how microclimate
change induced by habitat fragmentation can affect
the response potential of over-wintering birds.
16.2 Physiological adaptations to
winter conditions
Over-wintering in north-temperate regions can be
energetically challenging for small passerines that
must endure cold temperatures, reduced food
supply, and a shorter foraging time. For example
during harsh winters at the northern edge of their
range, black-capped chickadees are exposed to
normal low temperatures of 30C and as few as
5 hours of daylight (Sharbaugh 2001).
Relative to their body size, chickadees and
titmice possess a large surface area over which heat
can be lost. Most mature adults are in the 10 to 20 g
range and are therefore challenged by a high
surface-to-volume ratio. Such birds have an inter-
nal body temperature of approximately 40C, so
exposure to extreme winter environments (50C)
can result in a 90C temperature gradient in less
than 2 cm between ambient conditions and body
core (Sharbaugh 2001). In order to survive in condi-
tions of high thermoregulatory demand, chicka-
dees and titmice have developed several
physiological adaptations, including the use of noc-
turnal hypothermia and shivering thermogenesis.
16.2.1 Nocturnal hypothermia and
seasonal metabolic adjustments
Maintaining an appropriate body temperature
is metabolically demanding and birds can partially
overcome this challenge through the use of
nocturnal hypothermia. Nocturnal hypothermia
has been observed in several families of Order
Passeriformes, including Parids (Reinertsen 1996).
This moderate reduction in body temperature is not
as extreme as the torpor observed in hummingbirds
(Wolf and Hainsworth 1972) and poor-wills (Jaeger
1949). Several species of European (Grossman and
West 1977) and North American Parids exhibit
moderate nocturnal hypothermia in response to
low ambient temperatures (Chaplin 1976), and the
exact nocturnal energy savings to a hypothermic
bird depend on several factors, including ambient
temperature, body temperature, body mass, and
the duration of hypothermia.
263
264 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
In order to survive overnight in winter, birds
must achieve a thermal balance where the meta-
bolic heat production equals the heat lost. In low
ambient temperatures, such a balance is accom-
plished by either increasing consumption of energy
stores or decreasing the core body temperature.
Reinertsen and Haftorn (1983) suggested that a
change in posture or erection of the feathers is an
initial response to colder temperatures, followed by
a reduction in body temperature until a thermal
balance is achieved. It is at this body temperature
that the bird will remain throughout the night.
Entering a hypothermic state can result in
substantial energy savings throughout the night,
perhaps allowing for survival that otherwise would
not be possible. For example lowering the body
temperature from 39C to 33C in an ambient
temperature of 30C will result in a 10% reduction
in oxygen consumption. For an 11.5 g bird, this
yields an over-night energy savings of approxi-
mately 925 calories (Reinertsen and Haftorn 1983,
1986). Another study showed that reducing noctur-
nal body temperature by only 8C will provide a
chickadee with 72 additional minutes of fasting
endurance, an energy savings that could mean the
difference between over-night survival and death
(Sharbaugh 2001).
The proximate factor that induces a hypothermic
state is unknown, although the degree of hypother-
mia is correlated with body mass and fat reserves.
Reinertsen (1996) suggests that hormones or
plasma metabolites contribute to a sequence of
events transforming information on energy
reserves into the appropriate thermal response.
There is some lack of consistency in the results of
studies on Parid hypothermia, which might be
attributed to several factors, including different
techniques of body temperature measurement and
the period of time for which the birds were held
captive prior to testing. Grossman and West (1977)
observed an average decrease in body temperature
of only 3C (to 38.5C) for winter-acclimatized
black-capped chickadees in Fairbanks, Alaska
(65N) when the birds were measured at ambient
temperatures of 27C to 50C. However, birds
of the same species in New York have shown body
temperatures approximately 10C below normal
when exposed to ambient temperatures of 0C,
which resulted in a 32 to 45% lower oxygen
consumption than predicted for homeotherms of a
similar size (Chaplin 1976). Nocturnal body
temperatures of European great tits (Steen 1958)
and willow tits (Reinertsen and Haftorn 1983)
showed similar patterns to New York chickadees
and were 6 to 8C lower than their diurnal temp-
eratures. In addition, the stable hypothermic body
temperature of willow tits was strongly correlated
with ambient temperature.
North American and Eurasian Parids apparently
differ in their arousal from a hypothermic state.
Chaplin (1976) found that black-capped chickadees
captured in New York and kept at over-night ambi-
ent temperature of 0 to 5C were still hypothermic
in the early morning, but could regain normal body
temperatures with 1 to 2 minutes of intermittent
flying. This does not conform to the data from
European species that returned to normal body
temperatures in the morning even if kept in dark
chambers (Chaplin 1976).
Wind intensity can also affect a birds use of
hypothermia. Mayer et al. (1982) found that
Carolina chickadees would reduce their body
temperatures to 35C at 5C ambient temperatures
in the absence of wind. Body temperatures were
reduced further (to 30C) when birds were exposed
to 10C temperatures and a wind speed of
10 km/h, and this decrease in body temperature
corresponded to a 33% energy savings when
compared to the metabolic requirements for a bird
maintaining a 40C body temperature under those
same conditions.
Seasonal variation in hypothermic states is also
present in North American chickadee populations.
For black-capped chickadees collected in South
Dakota (42N), a larger percentage of winter than
summer birds became hypothermic in cold stress
tests (Cooper and Swanson 1994). Similar trends
were also evident in willow tits from Norway
(63N); birds acclimatized to winter conditions
showed a much larger decrease in body tempera-
ture than summer-acclimatized birds (Reinertsen
and Haftorn 1983) (Fig. 16.1). In contrast, measure-
ments from mountain chickadees and juniper
titmice captured in Utah (4152N) showed that
both species achieved considerable nocturnal
hypothermia throughout the year (Cooper and

40
38 (>12L)
Body temperature (C)
36
(10L, 14D)
34
(6L, 18D)
32
30 20
Figure 16.1 Relationship of body temperature to ambient temperate for willow tits during different seasons with different light:dark (L:D)
cycles: summer (crosses), late autumn or early spring (open circles), and midwinter (filled circles). Each point represents the minimum value
recorded on a single night. Curves were fitted by hand. (From: Reinertsen and Haftorn 1983.)
Gessaman 2005). Depth of hypothermia also did
not vary seasonally for either species (Fig. 16.2),
and the authors suggest that the regions high
climatic variability may be the source of this indif-
ference. Both species reduced their body tempera-
tures by 3 to 11C, which resulted in nocturnal
energy savings of up to 28% in titmice and up to
50% in chickadees. Similar results were seen in
Alaskan black-capped chickadees which also
utilize nocturnal hypothermia in both winter and
summer months (Sharbaugh 2001). This could be
due, in part, to the relatively cold and short
summers experienced at this latitudeconditions
favoring individuals that maintain their cold
acclimatization year-round.
Several studies also provide evidence that win-
ter-acclimatized birds are more cold tolerant than
summer birds. Standard metabolic rates of winter
chickadees were 18% greater than those of summer
birds, and winter birds also showed a significant
increase (36%) in maximal thermogenic capacity,
another likely adaptation to winter conditions
(Cooper and Swanson 1994). These differences in
W I N T E R A D A P TAT I O N S A N D H A B I TAT F R A G M E N TAT I O N 265
10 0 10 20
Ambient temperature (C)
physiology occurred despite the fact that there was
no seasonal variation in body mass or visible fat
(Cooper 2002). In contrast, the standard metabolic
rates of Alaskan black-capped chickadees did not
differ between seasons (Sharbaugh 2001).
16.2.2 Thermogenesis by shivering
In addition to lowering nocturnal body tempera-
tures, chickadees also respond to cold ambient
temperatures with shivering thermogenesis, facili-
tated primarily by the pectoral muscles. Shivering as
a means of heat production has been documented in
several avian species, including pigeons (Columba
livia, Hohtola 1982), house finches (Carpodacus mexi-
canus, Marsh et al. 1984), and Japanese quail (Coturnix
japonica, Hohtola and Stevens 1986), and the inverse
relationship between shivering magnitude and ambi-
ent temperatures is well established.
Chaplin (1976) observed an increase in both
frequency of shivering bursts and mean duration of
bursts at lower ambient temperatures in winter-
acclimatized black-capped chickadees. When these
266 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N

44 20 Y = 0.013T2a 0.863Ta+15.142
42
Body temperature (C)

Amplitude (mV/sec)
40 15
38

36 10
34

32 Mountain chickadees 5
30 Summer
Winter
28 0
14:00 18:00 22:00 02:00 06:00 10:00 14:00 0 10 20 30

44 Ta(C)

42 Figure 16.3 Shivering amplitude (mV/sec) of six black-capped

Body temperature (C)

chickadees exposed for at least 2 hours to ambient temperatures of

40
2C, 10C, 15C, 20C, and 27C. One data point represents the
38 mean amplitude of 10 shivering bursts. (From: Chaplin 1976.)

36
34
32
30
28
14:00 18:00 22:00 02:00 06:00 10:00 14:00
Time of day (hours)
Figure 16.2 Daily body temperatures of summer- and winter-
acclimatized mountain chickadees and juniper titmice. Each point
represents one individual. Lines represent a quadratic fit of the data.
(From: Cooper and Gessaman 2005.)
measurements were combined, there was a seven-
fold increase in total shivering time as temperature
decreased from 27C to 2C. Electromyographic
measurements of the pectoralis muscle also showed
an increase in shivering amplitude with decreasing
temperature, corresponding to a dramatic increase
in heat production (Fig. 16.3). The fact that during
their normal daily activities chickadees spend so
little of their time in continuous flight supports the
hypothesis that the pectoral muscles have a vital
role as organs of heat production. Cooper (2002)
found that pectoral muscle mass of wintering
mountain chickadees and juniper titmice was 33%
and 18% greater, respectively, than during the
summer. This seasonal variation could help to
satisfy the increased need for shivering thermogen-
Juniper titmice esis experienced by wintering birds.
Summer
Winter
16.3 Behavioral modifications and
ecological adaptations to winter
conditions
Permanent-resident woodland birds, such as
chickadees and titmice, possess several behavioral
modifications that may reduce energetic costs under
conditions of high thermoregulatory demand. This
can be accomplished through adjustments in their
foraging and roosting locations in order to minimize
exposure to harmful winds and temperatures.
However, as members of heterospecific flocks, these
birds must do so while minimizing interspecific
competition for food and roosting sites.
16.3.1 Over-wintering in heterospecific flocks
Most North American Parids over-winter as mem-
bers of mixed-species flocks. Within these flocks,
chickadees and titmice serve functionally as
nuclear species, facilitating the flocks formation
and movement. Additional, satellite species, such
as woodpeckers and nuthatches, maintain a
more passive role as flock followers (Morse 1970;
Austin and Smith 1972; Buskirk 1976; Hutto 1994;
 W I N T E R A D A P TAT I O N S A N D H A B I TAT F R A G M E N TAT I O N
Dolby and Grubb 1999b; Chapter 15). Removing
chickadees and titmice from small woodlots
resulted in satellite species occurring together less
often, further supporting the nuclear species role
in flock cohesion (Dolby and Grubb 1999b).
Although this multispecies social arrangement
can provide individuals with both antipredator
defense and increased foraging efficiency (Morse
1970; Berner and Grubb 1985), the resulting inter-
specific competition can also have a negative effect.
For example Carolina chickadees and tufted titmice
forage together during the non-breeding season,
with the titmice the more socially dominant
species. When titmice were removed from a wood-
lot, the more subordinate chickadees responded by
increasing feather growth rate (an index of an
energetically demanding process; Box 16.1) and
expanding their foraging niche (Cimprich and
Grubb 1994). This suggests the presence of inter-
specific competition between the species for local
food resources. This response has also been
observed in palearctic Parids. When varied tits
were removed from flocks containing the smaller
great tits, the great tits expanded their niche and
Box 16.1 Ptilochronology: feather time and avian biology
Ptilochronology is a term describing a relatively
new technique for indexing the nutritional
condition of birds (Grubb 1989, 2006). If you
pluck a feather and release the bird, then recatch
the same individual more than a month later and
pluck the newly grown replacement feather, the
replacement (or induced) feather can provide a
day-by-day record of the nutritional regime of the
bird during the previous weeks. Individual growth
bars (one dark band plus one light band) can be
counted to establish the number of days taken to
grow the feather. Matching induced feathers from
two birds from whom feathers had been pulled at
the same time, and then released in the same
habitat, could be used to determine the
relationships of species, sex, age, social dominance
status, kinship, and other factors to nutritional
condition. The wider the growth bar, the better the
nutritional condition.
267
foraged at greater heights (Jablonski and Lee 2002).
A similar change in foraging location was also
observed in socially subordinate coal tits when
dominant crested tits and willow tits were removed
from Swedish forests (Alatalo et al. 1985). Coal tits
shifted their foraging sites in trees to include the
inner regions previously occupied by the more
dominant species, suggesting the presence of either
interference or exploitation competition. In a subse-
quent study (Alatalo et al. 1987), the smaller species
were removed, causing the dominant species to
expand their foraging regions, suggesting that in
forest tits, competition for limited resources can
occur even without interference from dominants.
In Cimprich and Grubbs experiment, the
removal of titmice from a woodlot may have also
reduced competition for roosting sites, providing
the remaining chickadees with more protection
from harsh winter conditions. Although competi-
tion for roosting sites is common among great tits
and blue tits (Dhondt et al. 1991), the refusal of
chickadees to use artificial roost boxes in winter
suggests that roosting sites in this system may not
be a limiting resource.
The induced feather is retained until the next
molt. In most temperate- and boreal-zone birds,
tail feathers are replaced annually during the
so-called prebasic molt of late summer and
autumn. Thus, a bird plucked in late autumn will
grow the induced feather and will carry this record
of nutritional status to be collected any time during
the next 6 to 8 months.
The general technique for obtaining
ptilochronology feather measurements starts with
capturing a bird and plucking a feather, typically
the outermost right tail feather, or rectrix.
Removing a feather causes no visible trauma to a
bird, likely because a fully grown feather is held in
place in the follicle solely by non-living connective
tissue. After being so plucked, the bird is released,
recaptured after the 5 to 6-week growth period of
the induced feather, and the induced feather
pulled.
268 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
16.3.2 Foraging behavior and food caching
Inclement winter weather can have a deleterious
effect on the foraging of chickadees and titmice by
reducing the variety of locations a bird can exploit
while keeping thermal stress at a minimum. In a
study examining the effect of several climatic
factors on the foraging rates of black-capped
chickadees and tufted titmice in New Jersey, Grubb
(1975) found that temperature and wind speed
significantly affected the choice of substrate. In cold
and windy weather, birds adjusted their foraging
habits to minimize exposure to these elements. As
wind speed increased, both chickadees and titmice
reduced their foraging height and spent more time
foraging in shrub-type vegetation, both of which
would offer more protection from the wind.
In addition to altering their foraging location,
black-capped chickadees and tufted titmice reduced
foraging rates as ambient temperature decreased
and wind speed increased (Grubb 1978). For
example, in conditions of high wind (3.14.0 m/s),
tufted titmice spent 11.5% more time stationary and
traveled only 15.3% as rapidly as in low winds
(0.11.0 m/s). An increase in temperature from
10C to 20C quadrupled the foraging speed of
chickadees. The difference in foraging rate can be
partially explained by a change in foraging
substrate, and it may not be the weather conditions
themselves that dictate the speed at which an indi-
vidual feeds. In higher winds, both chickadees and
titmice spent more time foraging on the ground
where their movements were dominated by small,
short hops. The change in location was then more
directly responsible for modifying the foraging tech-
nique to a method that was not as rapid (Fig. 16.4).
For birds with access to supplementary food at
bird feeders, as temperatures decrease, time spent
participating in energetically demanding activities,
such as foraging and flight, decreases and more time
is spent at rest. During cold weather, black-capped
chickadees spent as much as 70% of the day at their
roosting site, and 10% of the time not spent at
the roost was spent resting (Kessel 1976). Foraging
ranges also decrease in size with temperature,
presumably to minimize time spent away from the
roost. Black-capped chickadee populations in Alaska
tend to become more concentrated at higher
elevations due to the presence of thermal inversions.
For example temperatures can be 25C warmer at
1000 m than in lowland areas (Hotly 1973).
Many Parids collect and store food for consump-
tion at a later time. Although time from caching to
food retrieval varies (see Chapter 2), birds do
accumulate caches during late autumn in prepar-
ation for the colder months when nutritional
resources are more difficult to find and foraging
time is limited due to shorter, colder days. Caching
of food resources has many benefits to birds that
over-winter in harsh climates. The presence of a
predictable food source decreases a wintering birds
risk of starvation while allowing it to maintain a
lower body mass, thereby reducing the risk of
predation. In addition, caching birds are able to
spend less time foraging, minimizing their exposure
to low temperatures and high winds (Pravosudov
and Grubb 1998). Further discussion of food caching
in Parids can be found in Chapters 2 and 3.
16.3.3 Cavity roosting
Chickadees and titmice utilize both natural and arti-
ficial cavities as nocturnal roost sites (Bent 1947).
The microclimate of a roosting cavity can minimize
thermoregulatory stress by providing shelter from
wind and precipitation, and by reducing radiative
heat loss. North American and Eurasian Parids
roost in a variety of locations, but most roosting
sites can be found in holes and recesses of dead or
rotting trees (Bent 1947; Pitts 1976; Perrins 1979).
Most roosts observed by Pitts (1976) had only a sin-
gle side opening, but others had multiple openings
and did not offer any better protection than dense
vegetation. Willow tits and Siberian tits will also
roost in holes in the snow (Smith 1991), and this
behavior has also been witnessed in black-capped
chickadees (C. C. St Clair, personal communication).
Communal roosting is not employed by chicka-
dees or titmice; however, several different chicka-
dees may use the same roost over several nights
(Pitts 1976). Occasionally, these roosts were also
occupied by other species, such as tufted titmice.
Small cavities provide a relatively stable microcli-
mate for over-night roosting, especially in metaboli-
cally challenging winter conditions. Mayer et al.
(1982) found that by roosting in a cavity, a birds net
radiant heat loss could be reduced 60 to 100%, and
convective heat loss was essentially zero due to the
 W I N T E R A D A P TAT I O N S A N D H A B I TAT F R A G M E N TAT I O N 269

30 Carolina 0.11.0 30 Tufted 0.11.0

(a) Conditions chickadee m/sec titmouse m/sec
sun shining or occluded 25 25
temperature 0.110.0C
20 20
1.12.0

Meters
m/sec
15 15 1.12.0
m/sec

10 10
2.13.0
m/sec 3 140 m/sec
05 05

10 20 30 40 50 60 10 20 30 40 50 60
Seconds Seconds

30 30
Carolina 10.1 To Tufted 10.1 To
(b) Conditions 20.0C
titmouse
chickadee 20.0C
sun shining or occluded 25 25
wind vel. 0.11.0 m/sec
20 20 9.9 To
0.0C
Meters

15 9.9 To 15
0.0C

10 10
19.9 To
10.0C
05 19.9 To 05
10.0C

10 20 30 40 50 60 10 20 30 40 50 60
Seconds Seconds

Figure 16.4 Wind-dependent (a) and temperature-dependent (b) foraging curves for black-capped chickadees and tufted titmice wintering in a
deciduous woodlot. Each sawtooth consists of a slope representing the average rate of individual movement, and a flat segment denoting the
time spent on an average stop. The diagonal common to all sawteeth indicates the average foraging speed over 1 min. (From: Grubb 1978.)

lack of any wind inside the roost site. In fact, wind
protection may be the primary benefit conveyed by
cavity roosts. Cooper (1999) showed that when air
temperatures inside a cavity were 4.3 to 5.6C
warmer than open sites for chickadees (1.76.3C
warmer for titmice), the standard operative tempera-
ture (Tes)which incorporates solar and thermal
radiation, ambient temperature, and windspeed with
a species resistance to heat losswas much higher:
4.5 to 14.8C warmer than open sites for chickadees
and 3.2 to 23.0C warmer for titmice. This dramatic
increase in Tes translates into significant over-night
energy savings. For example in Coopers study, the
wind reduction experienced by winter cavity roost-
ing led to nocturnal energy savings of 37.6% for
chickadees and 25.1% for titmice, which increased
fasting endurance by 7.3 and 5.7 hours, respectively.
Fasting endurance can become especially important
when foraging is hindered by inclement weather.
16.4 Responses to habitat fragmentation
The ranges of many North American Parids are at
least partially coincident with agricultural and
urban habitat modifications, which often results in
a fragmented or patchy distribution of the birds
(see also Chapter 15). Habitat fragmentation in
avian populations has received much attention,
especially in light of recent conservation concerns.
The negative effects of habitat fragmentation
on avian communities are well documented
and include reduced food supply, higher nest
predation, and greater risk from predators of
adults. In addition, smaller woodlots may contain
270 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
lower-quality individuals. These consequences are
of concern regarding persistence of chickadee and
titmice populations.
16.4.1 Species richness and density
Several studies have shown species richness and
within-species density to be strongly associated
with woodlot size; in general, woodlots with
greater area will harbor more species and more
individuals. In studies of permanent-resident birds
in northern Ohio, including Carolina chickadees
and tufted titmice, Doherty and Grubb (2000)
found that woodlot area was the most important
predictor of species presence and density. Smaller
woodlots tend to have lower food supplies, fewer
refuges from predation, and greater thermoregula-
tory costs due to less protection from harsh winter
temperature and wind, all of which presumably
contribute to the observed trends in avian presence.
Researchers (Telleria and Santos 1995) working in
winter landscapes have also detected highly signifi-
cant positive relationships between woodland
fragment size and both species richness and density
in Eurasian Parid species, including great tits,
crested tits, and coal tits, as well as several other
woodland passerines. However, blue tits failed to
show an increase in density with woodlot size.
16.4.2 Woodlot edge effect
Forest fragmentation also contributes to an increase
in edge habitat. Some avian species will nest along
woodland edges in addition to the interior, though
with different degrees of success. For example the
nests of Carolina chickadees (in addition to other
Poecile spp.) are often usurped by migratory house
wrens (Troglodytes aedon). Due presumably to
the house wrens preference for edge habitat,
chickadee nesting success is significantly greater in
woodland interiors (Doherty and Grubb 2002).
16.5 Effects of fragmentation on
wintering permanent resident birds
16.5.1 Survivorship
In addition to being associated with species pres-
ence and density, it stands to reason that woodlot
size also affects the annual survivorship of
permanent-resident birds. Combining previously
mentioned constraints of a fragmented landscape
(e.g. lower food supplies, higher predation rates,
etc.) with the increased thermoregulatory demands
of winter may reduce survivorship in such wood-
lots. Temperature may magnify any effects of
fragmentation alone because sufficient energy and
nutritional resources may become even more
difficult to find on cold, short winter days (Grubb
and Pravosudov 1994). Although studies have
shown temperature to be positively correlated with
great tit survivorship in Holland and Finland
(see citations in Doherty and Grubb 2000), its effect
on black-capped chickadee populations was min-
imal (Loery and Nichols 1985; Loery et al. 1987).
Doherty and Grubb (2002) were the first to
explore the relationship of survival in a fragmented
landscape to factors influencing winter severity,
including the presence or absence of supplemental
food. Their study was executed in a highly-
fragmented agricultural county of Ohio, with
approximately 10% forested area (Steiger et al. 1979)
and two riparian corridors. Carolina chickadee
numbers responded more strongly to woodlot size
and supplemental food than the other species
tested. Results showed that the annual probability
of survival was positively associated with woodlot
area in chickadees; however, a similar association
was not apparent in tufted titmice (Fig. 16.5).
In addition, the presence of supplemental food
also increased survivorship, most notably for the
chickadees, a result that is consistent with observa-
tions from gray jays (Perisoreus canadensis, Waite
1990) and European nuthatches (Sitta europaea,
Nilsson et al. 1993).
Due to their subordinate status within a het-
erospecific flock, chickadees are often forced to
forage in suboptimal areas (Pierce and Grubb 1981).
The possible foraging locations in a smaller wood-
land patch are, therefore, even further reduced,
putting an even greater strain on this species to
consume the necessary resources for over-night sur-
vival. Chickadees are also less likely than other flock
species to cross gaps between woodlots in search of
more optimal foraging conditions (Cimprich and
Grubb 1994; Chapter 15). Logically, increasing a
woodlots size or providing supplemental food
would help to counteract these disadvantages.
 W I N T E R A D A P TAT I O N S A N D H A B I TAT F R A G M E N TAT I O N 271

Annual probability of survival

1.0 1.0
Carolina chickadee Tufted titmouse
0.8 0.8
Food-supplemented
0.6 0.6
Food-supplemented
0.4 0.4
Unsupplemented
0.2 0.2 Unsupplemented
0.0 0.0
0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35
Woodlot area (ha)

Figure 16.5 Relationship between annual probability of survival, woodlot area, and the presence of supplemental food for Carolina chickadees
and tufted titmice. (From: Doherty and Grubb 2002.)

Woodlot size and supplemental food not only Snow cover can also impact the survivorship of
influence the annual survivorship of Carolina winter-resident birds. In fragmented woodlots,
chickadees in a fragmented landscape, but also the tufted titmice showed higher survivorship in years
nutritional condition of those that do survive with less snow cover (Doherty and Grubb 2000).
(Doherty and Grubb 2003). Food consumption has Similarly, when examining feathers for evidence of
a direct effect on the fitness of winter birds, and the nutritional condition, the researchers found that
health of individuals can be compromised without titmice had significantly wider growth bars in years
making them victims of over-night mortality. with less snow cover (Doherty and Grubb 2003).
Through the use of ptilochronology (Box 16.1), Relationships between snow cover and either
Doherty and Grubb (2003) were able to evaluate the survivorship or nutritional condition were not seen
nutritional condition of permanent-resident birds in any chickadees, woodpeckers, or nuthatches.
in winter and ascertain whether food availability Tufted titmice spend more time foraging on the
was having a direct effect on survivorship, as ground than the other three species (Rybcynski
opposed to other factors associated with a small 1977), so snow cover may not have had as strong an
woodlot size, such as increased predation (Nupe impact on birds that concentrate their foraging on
and Swihart 1998). Using the width of growth bars other substrates. Reduced snow cover due to the
on induced feathers as a surrogate for overall nutri- effects of global warming may be one mechanism
tional health, the researchers compared birds from promoting the northward range expansion of
both large and small woodlots, with and without tufted titmice (Harrap and Quinn 1996).
supplemental food.
Daily feather growth of Carolina chickadees was
16.5.2 Effects of wind and temperature
positively correlated with the woodlot area food
on isolated woodlots
interaction, such that birds from large, supplemented
woodlots had the widest growth bars. Similar results The effects of wind and temperature below the
were not observed in other species testedtufted thermoneutral zone become much more pro-
titmice, white-breasted nuthatches (Sitta carolinensis), nounced in isolated woodlots, reducing the
and downy woodpeckers (Picoides pubescens)all of suitability of such patches for permanent-resident
which maintain distinctly different foraging niches. birds. Edge effects become much more pronounced.
Previous studies on these species did record benefits In the most extreme conditions, such effects could
from food supplementation (Grubb 1989; Grubb and potentially penetrate deep enough into a woodlot
Cimprich 1990), however, that work was conducted to render it completely uninhabitable (Dolby and
in a landscape of more continuous woodland. The Grubb 1999a).
additional food in this study may not have been Dolby and Grubb (1999a) examined wind-chill
enough to counteract the harm from such a small effects specifically on small (mean area 5.3 ha)
woodlot. isolated wooded patches in rural Ohio, each
272 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N

containing one mixed-species flock. As observed in woodlots edge. The investigators found a signifi-
previous studies (Grubb 1975, 1978), both wind cant correlation between a wind/temperature
speed and temperature influenced the vertical interaction term and the distance of birds from the
foraging location of the birds within a woodlot. As woodlots edge. The relationship with wind speed
wind speed increased, both chickadees and titmice was most pronounced at the lowest temperatures
were found increasingly lower in the canopy. The observed (Fig. 16.6). A resident flock often adjusted
increased wind did not elicit the same response their location in the woodlot based not only on
from downy woodpeckers or white-breasted wind speed, but also on its direction. 62% of the
nuthatches. Chickadees and titmice tend to forage time, the researchers observed a majority of the
on smaller-diameter substrates and may not be able flock on the leeward side of the woodlot, presum-
to shelter themselves from the wind as easily as ably there to minimize exposure to the wind.
woodpeckers and nuthatches which are more likely These observations provide evidence for an add-
to respond by foraging on the leeward side of a tree itional challenge to the flock. If severe conditions
or by moving to substrates of larger diameter persist and the flock remains constricted to one sec-
(Grubb 1975, 1977). tion of a woodlot, the availability of food resources
In addition to adjustments in foraging height, may potentially become an exigent issue, further
birds observed in these small fragments also modi- reducing the suitable habitat. In addition, returning
fied their foraging location with respect to the to windward edges for the purpose of cache

(a) 15.0 to 6.5C (b) 6.0 to 2.0C

Distance from windward edge (m)

400 P = 0.008 400 P = 0.48

R2 = 0.52
300 300 R2 = 0.04

200 200

100 100

0 0
0 1 2 3 4 5 6 0 1 2 3 4 5 6

(c) 1.5 to 2.5C (d) 3.0 to 8.0C

Distance from windward edge (m)

400 P = 0.56 400 P = 0.61

R2 = 0.04 R2 = 0.03
300 300

200 200

100 100

0 0
0 1 2 3 4 5 6 0 1 2 3 4 5 6
Wind speed (m/sec) Wind speed (m/sec)

Figure 16.6 Linear regressions for the distance of Carolina chickadees and tufted titmice from the windward edges of woodlots against the
wind speed, blocked by temperature range (ad). (From: Dolby and Grubb 1999.)
 W I N T E R A D A P TAT I O N S A N D H A B I TAT F R A G M E N TAT I O N
retrieval may become difficult, if not averted
altogether. Other permanent resident species may
not be as distressed by low temperatures and high
winds as the smaller chickadees, but woodpeckers
and nuthatches were also present on the leeward
side of woodlots. One explanation for this behavior
is that they followed chickadees and titmice to that
location to maintain the antipredation and foraging
benefits of social flocking (Dolby and Grubb 1999a).
The available foraging substrate may also affect
flock distribution within a woodlot (Telleria and
Santos 1995). Patch edges that contain dense vegeta-
tion may provide the same wind protection as the
woodlots interior or the leeward side. Likewise, a
lack of appropriate foraging substrate on the leeward
side of the woodlot may reduce a species presence
even when conditions may warrant wind protection.
16.5.3 Woodlot connectivity and
interpatch movement
In a fragmented landscape, the degree of patch con-
nectivity can affect winter movement among
wooded habitat patches (see also Chapter 15). Also,
if adverse winter conditions result in individual
mortality and, in the most severe cases, local patch
extinctions, the reoccupation of a woodlot may be
directly related to its connectivity within the land-
scape. The presence of travel corridors, such as
fencerows, may help to facilitate interpatch move-
ments, especially during times of inopportune
weather conditions when protection from wind and
precipitation, as well as the usual protection from
aerial predators, would be more advantageous.
The impact of winter weather conditions on
movements among fragmented woodlands has
been demonstrated by Groom and Grubb (in press),
who simulated local patch extinctions by removing
Carolina chickadees from selected woodlots in an
agricultural landscape, and then monitoring
recolonization events. All 25 woodlots selected for
the study were eventually recolonized, and birds
moved sooner into those patches that contained
more wooded area and were connected via
fencerows to another woodlot. If, as previous stud-
ies have suggested (Grubb 1975, 1977, 1978; Dolby
and Grubb 1999a,1999b), abiotic factors, such as
wind, can reduce the amount of suitable habitat in
273
a woodland patch, occupants may be more likely
to disperse into and remain in larger patches.
During the winter, a larger patch will offer greater
protection from the wind effects experienced at a
woodlot edge. Mated pairs will also benefit by
remaining in a larger woodlot during the breeding
season. As discussed earlier, nesting in a larger
patch provides an opportunity for the pair to
maximize their distance from the woodlots
edge, minimizing the risk of nest usurpation by
house wrens.
In addition, Groom and Grubb (in press)
discovered that chickadees were more likely to
reoccupy a woodlot during periods of relatively
benign wind chill. During conditions of high
thermoregulatory demand, minimizing exposure to
deleterious abiotic factors, such as wind, is critical
to survival. Interpatch dispersal may, therefore, be
further regulated by the current microclimatic con-
ditions, in addition to degree of woodlot isolation.
Inclement weather may not only restrict the current
foraging habitat, but could also prevent individuals
from seeking more suitable habitat.
For small birds, the task of surviving temperate
winter seasons can be physiologically demanding,
and the additional stress created by a fragmented
habitat can further reduce a populations annual
survivorship and the nutritional condition of indi-
viduals. Many chickadees and titmice have large
ranges that expose them to a variety of habitats,
seasonal intensities, and microclimates. While
several studies have documented energy-saving
physiological adaptations and behavioral modifica-
tions to better manage increased thermoregulatory
demands, most studies have been limited to a
single species or to multiple species in the same
area. The intraspecific variation of these responses
across a broad geographical range has received less
attention. Comparisons of this sort, along with a
better understanding of the physiological chain of
events that induce these responses, will provide
insights into how a population may respond in
environments that differ in thermal and spatial
structure. The development and use of innovative
techniques, such as ptilochronology, and improve-
ments to current technology, such as radio tracking
and thermal sensors, will continue to provide
additional information as well.
274 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
Habitat fragmentation is likely to increase due to
agricultural and urban expansion. Global climate
change in also underway, though the magnitude and
consequences at the regional scale are still hotly
debated. In both matters, an effect on avian commu-
nities is likely to be observed. Combining a complete
knowledge of ecological and physiological con-
straints will facilitate more effective conservation
and management of over-wintering Parid species.
References
Alatalo, R. V., Gustafsson, L., and Linden, M. (1985).
Interspecific competition and niche shifts in tits and the
goldcrest: an experiment. Journal of Animal Ecology, 55,
977984.
Alatalo, R. V., Eriksson, D., and Gustafsson, L. (1987).
Exploitation competition influences the choice of for-
aging sites by tits: experimental evidence. Ecology, 68,
284290.
Austin, G. T. and Smith, E. L. (1972). Winter foraging
ecology of mixed insectivorous bird flocks in oak wood-
land in southern Arizona. Condor, 74, 1724.
Bent, A. C. (1947). Life histories of North American
jays, crows, and titmice. U.S. National Museum
Bulletin, 170.
Berner, T. O. and Grubb, T. C., Jr (1985). An experimental
analysis of mixed-species flocking in birds of deciduous
woodland. Ecology, 66, 12291236.
Buskirk, W. H. (1976). Social systems in a tropical forest
avifauna. American Naturalist, 110, 293310.
Chaplin, S. B. (1976). The physiology of hypothermia in
the black-capped chickadee, Parus atricapillus. Journal of
Comparative Physiology, 112, 335344.
Cimprich, D. A. and Grubb, T. C., Jr (1994). Consequences
for Carolina chickadees of foraging with tufted titmice
in winter. Ecology, 75, 16151625.
Cooper, S. J. (1999). The thermal and energetic significance
of cavity roosting in mountain chickadees and juniper
titmice. Condor, 101, 863866.
Cooper, S. J. (2002). Seasonal acclimatization in mountain
chickadees and juniper titmice. Physiological and
Biochemical Zoology, 74, 386395.
Cooper, S. J. and Gessaman, J. A. (2005). Nocturnal
hypothermia in seasonally acclimatized mountain
chickadees and juniper titmice. Condor, 107, 151155.
Cooper, S. J. and Swanson, D. L. (1994). Seasonal acclima-
tization of thermoregulation in the black-capped
chickadee. Condor, 96, 638646.
Dhondt, A. A., Kempenaers, B., and De Laet, J. (1991).
Protected winter roosting sites as a limiting resource
for blue tits. Acta XX Congressus Internationalis
Ornithologici.
Doherty, P. F. and Grubb, T. C., Jr (2000). Habitat and land-
scape correlates of presence, density, and species
richness of birds wintering in forest fragments in Ohio.
Wilson Bulletin, 112, 388394.
Doherty, P. F. and Grubb, T. C., Jr (2002). Survivorship of
permanent-resident birds in a fragmented forested
landscape. Ecology, 83, 844857.
Doherty, P. F. and Grubb, T. C., Jr (2003). Relationship of
nutritional condition of permanent-resident woodland
birds with woodlot area, supplemental food, and snow
cover. Auk, 120, 331336.
Dolby, A. S. and Grubb, T. C., Jr (1999a). Effects of winter
weather on horizontal and vertical use of isolated forest
fragments. Condor, 101, 408412.
Dolby, A. S. and Grubb, T. C., Jr (1999b). Functional roles
in mixed-species foraging flocks: a field manipulation.
Auk, 116, 557559.
Groom, J. D. and Grubb, T. C., Jr (in press). Patch coloniza-
tion dynamics by Carolina chickadees (Poecile carolinensis)
in a fragmented landscape: a manipulative study. Auk
Grossman, A. F. and West, G. C. (1977). Metabolic rate
and temperature regulation of winter acclimatized
black-capped chickadees Parus attricapillus of interior
Alaska. Ornis Scandinavica, 8, 127138.
Grubb, T. C., Jr (1975). Weather-dependent foraging
behavior of some birds wintering in a deciduous wood-
land. Condor, 77, 175182.
Grubb, T. C., Jr (1977). Weather-dependent foraging
behavior of some birds wintering in a deciduous wood-
land: horizontal adjustments. Condor, 79, 271274.
Grubb, T. C., Jr (1978). Weather-dependent foraging rates
of wintering woodland birds. Auk, 95, 370376.
Grubb, T. C., Jr (1989). Ptilochronology: Feather growth
bars as indicators of nutritional status. Auk, 106,
314320.
Grubb, T. C., Jr (2006). Ptilochronology: feather time and the
biology of birds. Oxford University Press.
Grubb, T. C., Jr and Cimprich, D. A. (1990).
Supplementary food improves the nutritional condition
of wintering woodland birds: Evidence from
ptilochronology. Ornis Scandinavica, 21, 277281.
Grubb, T. C., Jr and Pravosudov, V. V. (1994). Toward a
general-theory of energy management in wintering
birds. Journal of Avian Biology, 25, 255260.
Harrap, S. and Quinn, D. (1996). Chickadees, Tits,
Nuthatches and Treecreepers. Princeton University Press,
Princeton, New Jersey.
Hohtola, E. (1982). Thermal and electromyographic
correlates of shivering thermogenesis in the pigeon.
Comparative Biochemistry and Physiology, 73A, 159166.
 W I N T E R A D A P TAT I O N S A N D H A B I TAT F R A G M E N TAT I O N
Hohtola, E. and Stevens, E. D. (1986). The relationship of
muscle electrical activity, tremor, and heat production
to shivering thermogenesis in Japanese quail. Journal of
Experimental Biology, 125, 119135.
Hotly, J. G. (1973). Air quality in a subarctic community
Fairbanks, Alaska. Arctic, 26, 292302.
Hutto, R. L. (1994). The composition of mixed-species
flocks in a tropical deciduous forest in western Mexico.
Condor, 96, 105118.
Jablonski, P. G. and Lee, S. D. (2002). Foraging niche shifts
in mixed-species flocks of tits in Korea. Journal of Field
Ornithology, 73, 246252.
Jaeger, E. (1949). Further observations on the hibernation
of the poor-will. Condor, 50, 105109.
Kessel, B. (1976). Winter activity patterns of black-
capped chickadees in interior Alaska. Wilson Bulletin,
88, 3661.
Loery, G. and Nichols, J. D. (1985). Dynamics of a black-
capped chickadee population, 19581983. Ecology, 66,
11951203.
Loery, G., Pollock, K. H., and Nichols, J. D. (1987). Age-
specificity of black-capped chickadee survival rates.
Analysis of capture-recapture data. Ecology, 68,
10381044.
Marsh, R. L., Carey, C., and Dawson, W. R. (1984).
Substrate concentrations and turnover of plasma
glucose during cold exposure in seasonally acclima-
tized house finches, Carpodacus mexicanus. Journal of
Comparative Physiology B, 154, 469476.
Mayer, L., Lustick, S., and Battersby, B. (1982). The import-
ance of cavity roosting and hypothermia to the energy
balance of the winter acclimatized Carolina chickadee.
International Journal of Biometeorology, 26, 231238.
Morse, D. H. (1970). Feeding behavior and predator
avoidance in heterospecific groups. BioScience, 27,
332339.
Nilsson, J.-A., Kallander, H., and Owe, P. (1993). A
prudent hoarder: Effects of long-tern hoarding in the
European nuthatch, Sitta europaea. Behavioral Ecology, 4,
369373.
Nupe, T. E. and Swihart, R. K. (1998). Effects of forest
fragmentation on population attributes of white-footed
mice and eastern chipmunks. Journal of Mammology, 79,
12341243.
Perrins, C. M. (1979). British Tits. William Collins and Co.,
Glasgow.
Petit, D. R., Petit, L. J., and Petit, K. E. (1989). Winter
caching ecology of deciduous woodland birds and
275
adaptations fro protection of stored food. Condor, 91,
766776.
Pierce, V. and Grubb, T. C., Jr (1981). Laboratory studies of
foraging in four bird species of deciduous woodland.
Auk, 98, 307320.
Pitts, T. D. (1976). Fall and winter roosting habits of
Carolina chickadees. Wilson Bulletin, 88, 603610.
Pravosudov, V. V. and Grubb, T. C., Jr (1998). Management
of fat reserves in tufted titmice Baeolophus bicolor in
relation to risk of predation. Animal Behaviour, 56, 4954.
Reinertsen, R. E. (1996). Physiological and ecological
aspects of hypothermia. In: Carey, C., ed. Avian
Energetics and Nutritional Ecology, pp 125157. Chapman
and Hall, New York.
Reinertsen, R. E. and Haftorn, S. (1983). Nocturnal
hypothermia and metabolism in the willow tit Parus
montanus at 63N. Journal of Comparative Physiology,
151B, 109118.
Reinertsen, R. E. and Haftorn, S. (1986). Different meta-
bolic strategies of northern birds for nocturnal survival.
Journal of Comparative Physiology, 156, 655663.
Rybcynski, R. (1977). Dynamic Aspects of Bird Flocking: The
Influence of Weather and Patterns of Spatial Utilization.
Ph.D. dissertation, Cornell University, Ithaca, New York.
Sharbaugh, S. M. (2001). Seasonal acclimatization to
extreme climatic conditions by black-capped chickadees
(Poecile atricapilla) in interior Alaska (64N). Physiological
and Biochemical Zoology, 74, 568575.
Smith, S. M. (1991). The Black-capped Chickadee: Behavioral
Ecology and Natural History. Cornell University Press,
Ithaca, NY.
Steen, J. (1958). Climatic adaptation in some small north-
ern birds. Ecology, 39, 625629.
Steiger, J. R., Brug, W. H., Parkingson, R. J., and Lemaster,
D. D. (1979). Soil survey of Crawford County, OH. Soil
Conservation Service, U.S. Department of Agriculture.
Washington, D.C., US.
Telleria, J. L. and Santos, T. (1995). Effects of forest frag-
mentation on a guild of wintering passerines: the role of
habitat selection. Biological Conservation, 71, 6167.
Waite, T. A. (1990). Effects of caching supplemental food
in induced feather regeneration in wintering Gray Jays
Perisoreus canadensis: A ptilochronology study. Ornis
Scandinavica, 21, 122128.
Wolf, L. L. and Hainsworth, F. R. (1972). Environmental
influence on regulated body temperature in torpid
hummingbirds. Comparative Biochemistry and Physiology,
41, 167173.
This page intentionally left blank
 CHAPTER 17
Habitat quality and reproductive
behavior in chickadees and tits:
Potential for habitat matrix use
in forest generalists
Ken A. Otter, Harry van Oort, and Kevin T. Fort
17.1 Introduction
Habitat destruction and fragmentation is one of
the most serious threats to biodiversity loss in
conservation biology (Davies et al. 2001). Isolated
fragments may be too small to maintain viable
populations, leading to extirpation within rem-
nant patches of pristine habitat. If the remnant
patches are also sufficiently isolated from one
another, dispersal and recolonization may be
limited (Noss and Cooperrider 1994; Cooper and
Walters 2002). However, what distinguishes habi-
tat fragments from classic island biogeography
theory is that the intervening gaps are often vege-
tated, rather than open expanses of ocean. This
intervening habitat, referred to as the matrix
(Noss and Cooperrider 1994), differs in species
composition (Fig. 17.1a) or age and/or structure
of the vegetation (Fig. 17.1b) so as to be
sufficiently distinct from the remnant habitat
islands they surround. Matrix habitat is
considered less hospitable for remnant-dwelling
species, yet terrestrial matrices may not be quite
as impermeable as open oceans (Ricketts 2001).
The distinction is probably more akin to
extremely poor versus high-quality habitat, than
between inhospitable ocean versus habitable
islands.
If the matrix is sufficiently distinct from the
remnant habitat, as in the case of farmland or
clearcuts surrounding retained forest, the abrupt
transition can create edge effects into the remnant
patches (Laurance 2000; Davies et al. 2001). By
comparison, the maintenance of a matrix struc-
turally similar to the remnant (e.g. a managed
exotic forest surrounding native forests) can
reduce some of the microclimatic effects of abrupt
edges on remnant habitats (Noss and Cooperrider
1994; Davies et al. 2001) and can promote species
movement between habitat patches (Ricketts 2001;
Cooper and Walters 2002; Tabarelli and Gascon
2005; Castelln and Sieving 2006; Chapter 15).
Such studies have shown that managing matrix
vegetation may enhance dispersal between breed-
ing patches. However, suggestions have also been
made that the matrix, if well managed, could be
utilized for foraging and breeding by generalist
species typical of remnant habitat (Gascon et al.
1999; Davies et al. 2001; Tabarelli and Gascon 2005).
Noss and Cooperrider (1994) suggest that even if
such disturbed matrices serve as sinks, they may
temporarily maintain populations associated with
the core habitat area.
This chapter assesses the prospect of managed
matrix habitat to facilitate either supplementary or
alternative breeding areas. It is presupposed that the
species likely to utilize these buffers or matrix
patches are generalist in their habitat requirements,
and can compensate for the exotic and often
disturbed nature of these habitatsthat is they are
classified as matrix-tolerating species (Gascon et al.
1999). However, whether matrices function as sinks
277
278 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
(a)
Remnant Habitat Matrix
(b)
Matrix Remnant Habitat
or are able to sustain populations is largely
untested. Using data on habitat-generalist species in
the Paridae family, evidence would suggest that
even small changes in the habitat characteristics
can have profound effects on reproduction, condi-
tion, and behavior. If Parids serve as an indicator
of how slight habitat variation could affect less-
adaptable species, the potential of a matrix to
amplify the size of remnant patches (Tubelis
et al. 2004b) may be less than is currently
hypothesized.
17.2 Fragmentation, the matrix,
and halo effects
In fragmented landscapes, a matrix consisting of
mature vegetation (e.g. mature exotic forest or
Matrix
Remnant
Figure 17.1 Remnant habitats surrounded by a matrix
of contrasting vegetation. Matrix habitat that facilitates
movement between island remnant patches may consist
of vegetation that differs in species composition (e.g.
exotics) but is similar in density and size to the remnant
(a), or could be similar in vegetation composition to the
remnant but differ in age or successional stage (b).
young regenerating forest) may be incorporated
into territories of birds residing in the remnant
patches themselves (Gascon et al. 1999; Tubelis et al.
2004b). Despite the difference in vegetative
composition, such a matrix may provide a large-
pore filter for dispersal between remnant forest
patches (Gascon et al. 1999; Tabarelli and Gascon
2005; Castelln and Sieving 2006), and may even be
utilized for reproduction by species that can adapt
to the matrix (Gascon et al. 1999; Tubelis et al.
2004b). Further the ability to utilize the matrix may
reduce a species potential for extirpation within
patches immediately following fragmentation. This
conceptknown as a matrix-vulnerability index
is based on observations that forest species that
utilize the matrix following fragmentation are more
likely to persist in the remnant patches than those
 H A B I TAT Q UA L I T Y A N D R E P R O D U C T I V E B E H AV I O R
that do not venture into the matrix (Gascon et al.
1999). Tubelis et al. (2004b) found that species in
small remnants incorporate areas of the matrix into
their breeding territories. The utilization of the
matrix was greater when the matrix contained
more mature (although, in this case, exotic) vegeta-
tion, and thus structurally mimicked the remnant
patch. Such use of the matrix around remnant
patchesreferred to as the halo effectis argued
to effectively increase the functional size of the
remnant patch for habitat generalists (Fig. 17.2b).
The halo effect specifically describes the use of
matrix adjoining good quality remnant patches, but
this concept has been extended to suggest that
some species may settle solely in the matrix, such
that it becomes an alternative breeding habitat
(Gascon et al. 1999depicted in Fig. 17.2c). While
the ability to use matrix habitat (either to supple-
ment territories or as a substitute for breeding in
remnant patches) may allow species to persist
following disturbance, less is known about whether
such matrix use compensates for the loss of
(a) Exclusive use of remnant
Matrix
Remnant
100 m
(b) Halo effect (c) Alternative breeding habitat
279
remnant habitat among such matrix-tolerating
species.
Tubelis et al.s (2004b) results suggest that forest
generalists are more willing to utilize the matrix
when faced with small remnant patches. It is also
likely that creating a matrix with similar structural
composition (but exotic species composition) is
likely far better than abrupt transitions between rem-
nants and harvested areas. Similarly, several studies
have found that more vegetated matrices promote
dispersal between remnant patches (Ricketts 2001;
Cooper and Walters 2002; Tabarelli and Gascon
2005; Castelln and Sieving 2006; Chapter 15).
However, the utilization of matrix habitat as alterna-
tive breeding/foraging habitat, rather than simply
as a dispersal corridor, makes an implicit assump-
tion that the matrix is somewhat equivalent to the
remnant habitatuse of the matrix offsets the loss of
the remnant. While this could be true, one can not
assume that the willingness to use the matrix is
equivalent to the birds perceiving the matrix as com-
pensatory. The fact that birds in larger remnants are
Territory
Figure 17.2 Where remnant patches are
sufficiently large, matrix-tolerating species will likely
occupy territories solely contained within the
remnant (a). In the small remnant patches, territories
may be expanded to utilize the matrix, either for
foraging or breeding (b). As a result, the matrix may
extend the functional size of the remnant patch,
referred to as a halo effect (after Tubuelis et al.
2004b). The extension of this usage is when
matrix-tolerating species begin to utilize the matrix
as alternative breeding habitat (c).
280 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
less likely to utilize matrix habitat (Tubelis et al.
2004b) would indicate these may be perceived as
lower quality by the birds themselves. Even where
matrix is partially, or completely, used in breeding
territories, settlement in these patches may not
constitute successful breeding attempts. Viewing
these areas as potential sinks, but with prospects of
helping sustain overall populations in the short term
(Noss and Cooperrider 1994) may de-emphasize
retention of remnant breeding habitat. To evaluate
the potential of the matrix to supplement or act as
alternative to remnant habitat, detailed studies of
how breeding behavior and success are modified by
subtle differences in habitat quality are required.
Such information is available from long-term studies
on members of the Paridae family.
17.3 Habitat variation and
reproductive success in the Paridae
17.3.1 Matrix of similar age or structure
but dissimilar species composition
Species are typically more likely to be found in a
matrix that consists of vegetation with similar
canopy heights compared to the remnant patches,
despite the vegetation potentially being of different
species composition (Tubelis et al. 2004b; Gascon
et al. 1999). One can see why this may facilitate
movement of the animals among remnant patches,
as exposure while moving through such matrix may
be far lower than moving across large habitat open-
ings (Chapter 15). From a structural standpoint,
birds may also view these kinds of habitats as more
contiguous and less disruptive than those where the
matrix is an abrupt structural transition (such as for-
est bordered by grasslande.g. Tubelis et al. 2004a).
It is the secondary function of managing matrices for
supplemental breeding habitat, however, that is less
clearly understood. Research on great tits and blue
tits conducted over the past three decades may shed
light on the ability of birds to compensate for vari-
ation in species composition within their habitats.
17.3.1.1 Blue tits in evergreen versus
deciduous oak forests
For over 20 years, Jacques Blondel and colleagues
have been conducting detailed work on the
reproductive behavior of blue tits occupying Oak
forests in Mediterranean habitats of Southern
France and Corsica. Although the predominant tree
species are oak, forests are dominated by one of two
species: deciduous downy oak (Quercus pubescens)
versus sclerophyll (evergreen) holm oak (Q. ilex).
This apparently subtle difference has enormous
biological significance to the birds. Deciduous oak
drop their leaves annually, replenishing these with
new growth early each spring. The young leaves
have lower levels of tannins than mature leaves,
and are more palatable to folivorous caterpillars,
the primary prey of the birds (Blondel and Dias
1994). When available, these caterpillars are the
preferred prey for provisioning nestlings (Blondel
1985; Blondel et al. 1991; Tremblay et al. 2004), and
have the highest energetic yield for the young birds
in digestible proteins (Blondel et al. 1991).
Evergreen oak shed only a small portion of their
leaves annually, which are replaced later in the spring
compared with those of deciduous oaks. As a greater
portion of their leaves are mature and tannin rich,
evergreen oaks support a much smaller caterpillar
population (Blondel et al. 1991; Banbura et al. 1994). In
addition, the delayed development of the new leaves
each year results in differences in the peak timing of
caterpillar abundance. Development of the caterpil-
lar instars begins soon after bud-burst of the new
leaves, which in evergreen oaks occurs nearly
3 weeks later in the spring compared to deciduous
oaks; the result is that peak abundance of caterpillar
larvae to feed nestlings is delayed by the same period
(Blondel et al. 1993). The timing of reproduction in
passerines is closely associated with prey cycles
(Chapter 5), as there is highly stabilizing selection on
matching the timing between the peak feeding
demands of young with the peak of prey abundance.
Mismatching nest timing and prey peak has been
shown to reduce breeding success in great tits (Seki
and Takano 1998) and blue tits (Dias and Blondel
1996; Blondel et al. 1999; Lambrechts et al. 2004) and
growth rates in willow tits (Thessing 2000).
Can birds that breed in evergreen oak forests
compensate for these differences from deciduous
oak forests? Studies of populations in isolated
evergreen oak patches on the island of Corsica
suggest they can. Blondel et al. (1991) found the
seasonal timing of breeding in Corsica is delayed
 H A B I TAT Q UA L I T Y A N D R E P R O D U C T I V E B E H AV I O R
by approximately the same time interval as the
difference in caterpillar abundance, as compared to
deciduous oak habitat on the French mainland.
Subsequent studies have found similar timing
shifts in isolated patches of evergreen versus
deciduous oak forests that both occur on Corsica
(Blondel et al. 1999; Tremblay et al. 2004). Despite
the ability of the birds in these isolated forests to
alter timing to match the caterpillar peaks, the habi-
tats themselves are not equivalent. Birds in
Corsican evergreen oak forests have lower clutch
sizes than those anywhere else in Europe (Blondel
et al. 1993; Blondel et al. 1998; Lambrechts et al.
2004), possibly due to differences in the diet
composition fed to nestlings, which is lower in
caterpillars versus arthropods and other prey
(Blondel et al. 1991; Banbura et al. 1994). Birds
occupying these evergreen forests may also be in
poorer condition than those in deciduous forests.
Blue tit males in Corsican populations have lower
levels of aggressiveness than mainland counter-
parts (Perret and Blondel 1993), pairs occupying
evergreen forests are subordinate to those in decidu-
ous forests (Braillet et al. 2002), and adults are in
poorer physical condition (Lambrechts et al. 2004).
Despite indications that the birds view the habi-
tats differently in terms of quality, Corsican popu-
lations in isolated evergreen habitat appear to have
adapted to local conditions, likely facilitated by
genetic isolation (Blondel et al. 1999; Thomas et al.
2001; Tremblay et al. 2004). However, contiguous
populations of blue tits breeding in southern France
occupying either evergreen or deciduous habitats
show a different pattern in reproductive timing.
These two populations are not isolated from one
another and birds occupying the evergreen habitats
on the mainland appear to mismatch their repro-
ductive timing with the peak in caterpillar abun-
dance for these habitats (Blondel et al. 1999; Thomas
et al. 2001). These mainlandevergreen birds do not
differ in the timing of breeding from those in neigh-
boring deciduous forests, suggesting that the gene
flow occurs across habitats maintains traits adapted
for breeding in the richer, deciduous habitat
(Blondel et al. 1999). The result is extremely poor
reproductive behavior of birds in evergreen forests
on the mainland; their lack of compensation for the
difference in timing of prey availability would
281
appear to be maladaptive (Thomas et al. 2001). This
is more likely, however, to be a constraint of contin-
uous gene flow between these populations (Dhondt
et al. 1990; Blondel et al. 1999; Thomas et al. 2001)
resulting in a sourcesink scenario (Dias 1996).
In the mainland habitats, the richer territories of
the deciduous oak habitat would constitute habitat
sourcesthe higher fledgling quality in these areas
are likely to result in greater fledging success than in
evergreen habitats (Dias 1996). Thus, the extreme
mismatching of clutch initiation and prey abun-
dance in the mainland evergreen habitats is unlikely
to change as long as there is potential emigration of
birds from the deciduous forest, as reproductive
timing appears to be largely under genetic control
(Blondel et al. 1990). Without the genetic isolation of
the evergreen populations from source populations,
there will be no potential to adapt to the very differ-
ent circumstances in these areas. This could result in
sink populations that persist due to replenishment
from source populations (Dias 1996; although some
ambiguity still remains on long-term population
effects of habitat qualitysee Lambrechts et al. 2004).
Regardless, the inability to adapt to species-atypical
local conditions is not unheard ofrather this
phenomenon has also been reported in clutch size
differences between great tits breeding in woodland
and hedgerow settings (Dhondt et al. 1990).
The conclusion drawn is that structurally similar
habitats differing in vegetative species composition
may, nevertheless, differ markedly in habitat quality.
In all circumstances noted, these have the potential
to affect reproductive success. However, the extent
of this impact varies based on whether local adapta-
tion occurs. Adaptation to local environments
appears to require reproductive isolation from
populations in native habitat. Among neighboring
patches that differ in composition (such as would
occur among remnant patches embedded in a
matrix) there is increased potential for a mismatch
between genotype and the local environment for
birds settling in the matrix. This will occur if
remnant patches are higher in quality and function
as source populations. Emigration from these
patches, followed by settlement within the matrix, is
likely to result in settling birds retaining genes
adapted for breeding within the remnant. If optimal
behavior for breeding within the matrix (such as
282 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
shifting timing of reproduction) is required for suc-
cess, such local adaptations are unlikely to arise with
the influx of recruits from neighboring remnant
patches. The result could be a mismatch between
exhibited behavior and the optimal behavior for
breeding in the context of the matrix. If the matrix
also provides different or reduced prey availability
(as is the case for evergreen oak habitat) the com-
pounding effect of settlement in these habitats could
be very low productivity. However, populations in
the matrix may appear to be sustained if sufficient
emigration occurs from remnant patches. The latter,
however, requires that sufficient remnant habitat is
retained to serve as sources. Even halo territories
that incorporate mixed habitat could result in
reduced prey availability compared to pure remnant
habitat and reduce breeding potential. The ability of
few large remnant patches to sustain a large number
of sink populations (either birds breeding in the
matrix itself or in small remnant/matrix halos) will
be limited.
17.3.1.2 Comparison of blue tits to greats tits
and other study sites
The data from Mediterranean blue tits would appear
to have dire consequences for viewing non-native
matrix habitat for breeding or possibly even for-
aging, despite its probable utility as a corridor.
However, not all of the research on tit species shows
major effects of breeding in disturbed or altered
habitats. For example Nour et al. (1998) found no
impact on feeding rates, prey volume, nestling con-
dition, nor nestling survival in either great tits or
blue tits breeding within small or large habitat frag-
ments. Similarly, Verhulst and Tinbergen (2001)
failed to find a correlation between energetic work-
load and mismatching of reproduction with caterpil-
lar peak in their great tit population. Why are these
results contradictory? It may simply stem from how
much the habitat differed in composition. The habi-
tat patches studied by Nour et al. (1998) do not
appear to have differed in species; all appear to be in
deciduous oak woodland. Tremblay et al. (2003)
found that food supply in high-quality habitats may
exceed the requirements of breeding tits (i.e. there is
a saturation threshold beyond which breeding
success no longer increases linearly with food
supply). In these cases, population density is
presumably limited by other resources, such as
defense of nesting areas. It is, therefore, possible that
species may be less susceptible to small patch size in
highly productive habitats (Nour et al. 1998). The
same may not be true in low-quality habitat.
Tremblay et al. (2003) found that overall food avail-
ability, mistiming of clutches, and variation in clutch
size resulted in lower fledging success in low-quality
habitats than was the case in high-quality habitats.
Where the birds are able to adapt to low-quality
habitat through reproductive isolation, however,
Tremblay et al. (2004) found evidence that pairs can
adapt to both differences in prey availability and
clutch timing. In comparing two isolated Corsican
populations (one deciduous and one evergreen
habitat), birds in the deciduous habitat make more
frequent foraging visits to the nest and have
shorter foraging flights away from the nest
compared to those in evergreen habitats. However,
birds in evergreen habitat compensate for longer
foraging flights by bringing larger prey items. The
result is that the overall biomass of prey brought to
the nest was equivalent between the sites.
Conversely, in two neighboring plots that differed
in species composition (a deciduous oak versus a
mixed oak/pine forest in Germany), Stauss et al.
(2005) found that blue tits were less compensatory.
Birds in the deciduous forest also made shorter
foraging trips during nestling feeding, but in this
population the nestling growth rates and fledging
mass was much lower than in the mixed forest.
Thus, the ability to adjust provisioning behavior to
compensate for poorer breeding habitat may also
rely on reproductive isolation of the populations,
which allows for development of local adaptation.
In a practical sense, this would require manage-
ment of matrices so large that emigration from
remnant patches is unlikely.
17.3.2 Matrix: Habitat of similar species
but dissimilar age
Research on great tits has long suggested that mar-
ginal habitats surrounding woodlots are lower in
quality than the woodlots themselves (Dhondt et al.
1992; Riddington and Gosler 1995). However, less
work has focused on the effect of occupying
second-growth forest on European tits than has
 H A B I TAT Q UA L I T Y A N D R E P R O D U C T I V E B E H AV I O R
been conducted on comparing birds in evergreen
versus deciduous oak forests. Our work in northern
British Columbia (BC) on black-capped chickadees
addresses the former scenario.
Northern Canadas sub-boreal forest is a mixture
of deciduous and coniferous species. In north
central BC, the deciduous component of these
forests consists predominantly of two species
favored for nest excavation by chickadees
trembling aspen (Populus tremuloides) and paper
birch (Betula papyrifera). Coniferous components are
largely hybrid spruce (Picea glauca Picea engel-
mannii), lodgepole pine (Pinus contorta), Douglas-fir
(Pseudotsuga menziesii), and subalpine fir (Abies
lasiocarpa), the latter two being associated mostly
with the climax forests. Lodgepole pine and
Douglas-fir have been the focus of heavy logging in
the resource-based economy of northern BC, result-
ing in large tracts of the landscape being clear-cut
logged within the last half century.
Commercial forestry in the region creates a
mosaic of habitats of varying age. Young regenerat-
ing forests in the region are often dominated by
lodgepole pine and a deciduous component of
green alder (Alnus crispa) and numerous willow
species (Salix spp.) intermixed with the aspen and
birch. The large scale of the landscape and forestry
regulations in northern BC allow harvesting while
remnant forest patches still retain corridors of
continuous, mature vegetation, but movement
between patches is also facilitated by the matrix
of regenerating forests (see also Chapter 15).
However, commercial replanting focuses on conifer
rather than deciduous species, the latter of which
constitute the primary species used by cavity
excavating guilds in the region (Chapter 8). As
forests are also reharvested before reaching full
maturity (e.g. 50-year rotations), coupled with the
loss of mature and dead aspen/birch forests, a
greater proportion of the landbase could become
early seral forests.
Since 2000, we have studied two adjacent forest
patches near the University of Northern British
Columbia which differ in the degree of habitat
disturbance (Fig. 17.3). The main disturbed site is a
100-ha forest logged for agricultural pasture land
in the late 1960s. The land was allowed to begin
natural regeneration in the late 1970s, and was
283
acquired as a municipal park in the 1980s. In 1986,
portions of the park (approximately half the land
base) were cleared and replanted with various
conifer species to serve as an example of a model
forest. The park now consists of native habitat in
early seral forest, 30 years in age, which will here-
after be referred to as young forest. Several small
patches (the largest approximately 4 ha) of mature
forest are interspersed throughout the larger area
and surrounded by the younger forest. The canopy
varies between 5 and 15 m in height, with the major-
ity of the canopy not exceeding 10 m. Most aspen
and birch found in the forest is of a diameter and age
marginal for use by chickadees and few decayed
snags of these species occur.
By comparison, university-endowed lands adja-
cent to the park constitute mature, undisturbed
forest that has not undergone any large-scale logging
for over 80 years. The forest is composed of a mixed
mosaic of mature aspen and birch stands inter-
spersed with mature pine and Douglas-fir forest.
The canopy is relatively uniform at 25 to 30 m. In
addition to these two main patches, two smaller
patches (one young forest and one mature) are also
monitored. Our work compares the reproduction
and behavior of neighboring populations of birds
occupying habitat of similar species composition,
but largely divergent seral stage (mature versus
young forest). While not a perfect test of the halo
effect (as we focus primarily on birds nesting entirely
in one habitat or the other), the work that we
conduct may shed light on the potential for regener-
ating natural matrix to serve as alternative breeding
habitat. Between 2000 and 2004, the average number
of chickadee territories falling completely in either
young or mature forest was 15.2 and 17.4 respect-
ively (range of 12 to 19 pairs/year for young forest,
and 13 to 22 for mature). A low productivity year
during spring of 2004 (see below) resulted in low
breeding densities in 2005, with eight pairs in young
forest and 11 in mature.
17.3.2.1 Chickadees breeding in mature versus
young forestssettlement
The two habitats are adjacent, and thus birds occu-
pying the two sites are not genetically isolated.
Recruitment into local populations is extremely low
(5% of nestlings banded since 2000) due to the high
284 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N

Figure 17.3 Black-capped chickadee study site in northern British Columbia. The study compares chickadees breeding in adjacent patches of
mature sub-boreal mixed forest that has not undergone disturbance for more than 80 years, against younger forest (30 years) that has
undergone disturbance in the recent past. Vegetation differences between forest types mimic differences between a matrix and remnant patch
depicted in Fig. 17.1b.

dispersal propensity of juvenile chickadees (Weise
and Meyer 1979). Recruits that have been found are
not philopatric to natal habitat type; juveniles
fledged from one habitat type are found as com-
monly in non-natal versus natal habitat (K. A. Otter,
H. van Oort, and K. T. Fort, unpublished data).
Dispersal in this species occurs during the first fall
(Smith 1991), and each year a large number of
juvenile recruits from the surrounding forests
occupy both sites. In contrast to juvenile behavior,
settled birds are sedentary, often breeding in the
same territories their entire life (Smith 1991). Within
the study area, minor shifting of territories between
years does not include the movement of adults
from one habitat type to the other (K. A. Otter,
H. van Oort, and K. T. Fort, unpublished data); once
a bird has settled in either the young or mature
forest, movement to the other site for subsequent
breeding has not been witnessed.
Initial settlement does not appear to be biased
by condition of juveniles. Using ptilochronology
(see Box 16.1 in Chapter 16), van Oort and Otter
(2005) found a correlation between body condition
and growth bar size on tail feathers among first
wintering juveniles; this suggests that growth bar
size of tail featherswhich in this first wintering
cohort reflect growth during the nestling/fledgling
periodcould be used as an index of the relative
condition of settling juveniles. Despite this, there
was no difference in the growth bar size of males
occupying mature versus young forest sites. This
suggests that male settlement among habitats is not
influenced by condition. Females that settle in
mature habitat, however, had larger growth bars
than those that settled in young habitat, suggesting
females may pay more attention to habitat attrib-
utes during settlement (van Oort and Otter 2005).
Yet, unlike the results found by Braillet et al. (2002)
in blue tits between evergreen and deciduous
forests, there is no indication that males occupying
the mature forest site are inherently dominant to
birds in the young forest (Fort and Otter 2004a).
Thus, males at least do not appear to settle based on
a perception of differences in habitat quality.
Further, despite the populations being functionally
distinct following settlement, the interchange of
juvenile birds between sites and from surrounding
habitats prevents genetic isolation, and with it the
potential to adapt to local habitat variation.
17.3.2.2 Habitat quality and reproductive
success in chickadees
Despite little evidence of differential settlement
based on habitat type, the young and mature forest
 H A B I TAT Q UA L I T Y A N D R E P R O D U C T I V E B E H AV I O R
sites are not equivalent in quality. Birds occupying
the young forest have higher rates of nest abandon-
ment than those in the mature forest sites (Fort and
Otter 2004b). Like studies of blue tits, the severity of
this effect appears to vary between yearsin
productive years, the disparity between success-
fully nesting pairs is dampened, but in low
productivity years the disparity can be extreme. In
2000 and 2001, the pairs in the young forest were
only 64% as likely to fledge young as those nesting
in neighboring mature forest, and the effect appears
to be most pronounced among birds that are
subordinate in winter dominance hierarchies (Fort
and Otter 2004b). Both 20002001 had prolonged
periods of cold weather in the critical nesting
period (May and June), and may have been the
cause of dramatic differences in abandonment
across habitats (Fort and Otter 2004b). Conversely,
the springs of 2002 and 2003 were warmer with less
precipitation than the preceding 2 years, and the
disparity in nesting success between sites was
diminished (Fig. 17.4). In 2002, fledging success
was extremely high in both habitats; despite the
pattern of lower fledging in young forest continu-
ing, the effect was dampened by pairs in both habi-
tats being highly likely to fledge. The pattern across
habitats reverses slightly in 2003, the only year that
this occurred in the study. This, however, may have
been associated with high local predation on
nesting pairs, as the majority of nest abandonment
was confined to one area of the mature site where
a sharp-shinned hawk, Accipiter striatus, was
known to be nesting. Spring of 2004, however, was
unseasonably mild, with snowmelt and leaf-burst
3 weeks earlier than normal. The result was
unexpected61.9% (13/21) of pairs in the mature
forest sites fledged young, but only 31.3% (5/16
pairs) of birds in the younger forest fledged, the
lowest success rates in the 5 study years, with only
48.6% of birds across habitats breeding successfully
(Fig. 17.4). Following 2004s low productivity year,
the wintering population of chickadees was
reduced by nearly 50% in 2005approximately
70 to 75 birds in the study area during the winter
compared to normal years of between 120 and 130.
The result, in 2005, was the lowest density of breed-
ing pairs across sites (N 19) seen during all years
of the study (average number of breeding pairs in
285
20002004 was 32.6). The spring of 2005 was similar
in temperature and timing of leaf burst to those in
2002 and 2003, and low breeding densities seemed
to result in high fledging success (Fig. 17.4) in both
sites. Despite this, the tendency remained for the
mature forest to have higher success. Thus, the
effect that settling in either habitat has on breeding
success appears to be magnified in years of more
atypical weather.
Even in years where success rates are more
comparable between habitats, habitat influences
the condition of resident birds. The data suggests
that the birds perceive the habitats to differ in qual-
ity, and this may be attributable to differences
in relative food availability. Chickadees in the
younger forest carry higher winter fat loads than
those in the mature forest sites (van Oort and Otter
2005); higher fat deposition is typical of lower-
ranked birds in the Paridae (Ekman and Lilliendahl
1992) and is more common when birds perceive
that local food resources are uncertain (Gosler
1996).
If birds in the young forests are being subjected
to lower food reserves in the winter, then there is
the possibility that these birds are more likely to
enter the breeding season in poorer condition. Over
the past few years, we have used condition-
dependent behavioral traits of birds in either habi-
tat to determine whether there is evidence for a
difference in condition between sites (Godfrey
2003). The traits measured include the dawn
chorus, calling by females to solicit courtship feed-
ing, territorial behavior, parental provisions, and
condition of adults.
17.3.2.3 Habitat quality and condition-dependent
behaviors in chickadees
Dawn chorus: the extended period of dawn singing
in chickadees typically reflects male condition, as
there is a strong correlation between the relative
song output of males and their social rank (Otter
et al. 1997)dominant males start singing earlier,
sing for longer periods, and attain higher average
and maximum song rates than their subordinate
flock-mates. During the springs of 2000 to 2003, we
recorded the dawn choruses of dominant and
subordinate males in either habitat. In the mature
forest, van Oort et al. (2006) found that the relative
286 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N

Young forest Mature forest

1.00

0.90
Proportion of Nests that Fledged Young
0.80

0.70

0.60

0.50

0.40

0.30

0.20

0.10

0.00
2000 2001 2002 2003 2004 2005
Year

Figure 17.4 Variation in the proportion of successfully fledged nests between young and mature sites among black-capped chickadees
breeding in northern British Columbia. Although the pattern of lower fledging success in the young forest is relatively consistent, the
magnitude of the difference between habitats appears to vary across years. The disparity appears to be greatest in years associated
with atypical weather patterns (see text). High local predation on nesting adults by a sharp-shinned hawk may account for reversal pattern
in 2003.

song output during the dawn chorus matched clutches (Chapter 5). Tobias and Seddon (2002)
expectationsdominant males had higher song suggest that rates of solicitation calling among
output than subordinate males. However, this pat- female birds may reflect relative hunger level; this
tern was not found in the young forest sites. appeared testable in female chickadees, which
Overall, males in the young forest had lower song often produce several hundred calls during 20-min
output during the dawn chorus than males in the observation periods conducted during the egg-
mature forest, but the differences was driven by laying period (Otter, S. Atherton, and H. van Oort,
abnormally low song output among dominant unpublished data).
males in the young forest (van Oort et al. 2006). A Solicitation calling rates of female chickadees
direct comparison of the dominant males between drop dramatically if the pair is provisioned with
sites indicated that males in the young forest sang supplemental food (10 min of feeding on meal-
at lower rates than those in the mature forest. worms), declining by nearly 50% compared to
Food solicitation calling: during the energetically- prefeeding rates (Otter et al. in press). Control birds
demanding egg laying period, female chickadees did not differ in call rates before and after being
produce a vocalization that appears to be used in presented with a similar feeder, but not being
soliciting feedings from malesthe broken dee allowed to feed. This suggests that the call rates
(Ficken et al. 1978; Smith 1991). Such solicitation may reflect immediate hunger levels in female
calls appear in other Parids, and food provisioning chickadees. We then compared calling rates
to females by their mates during the egg-laying between birds occupying the two forest types.
period may influence the females ability to initiate Females in the young forest had significantly
 H A B I TAT Q UA L I T Y A N D R E P R O D U C T I V E B E H AV I O R
higher call rates than birds in the mature forest, but
this relationship was driven almost entirely by
subordinate birds. There was little difference in the
call rates of females mated to dominant males
across sites. Further, the difference between the
calling rates of dominant versus subordinate
females in the mature forest was less then between
females mated to subordinate males in the young
forest. This suggests that there may be differences
in the relative hunger level (and possibly food
availability) between the sites, and that it may be
disproportionately affecting the subordinate pairs
during courtship feeding.
Territoriality: Fort and Otter (2004a) used both
radiotelemetry and observations of intrusions
during daily surveys to show that intrusions into
neighboring territories were both more common,
and more tolerated by residents, in the young forest
sites than in the mature forest. All observations
suggested that these intrusions differ from those
associated with extrapair behavior in this species
(Smith 1988), which are surreptitious in nature and
often only involve the soliciting female. Rather,
intrusions commonly involved both male and
female together and pairs continued to use contact
calls as they foraged. Pairs were often discovered
by residents, and not only tolerated, but the
residents often joined the intruders and foraged in
flock-like formation. Such behaviors were not
witnessed in the mature forest.
These behaviors suggest that resources may
be limited in the younger forests, forcing some
pairs outside of their defended territories. Providing
that these interlopers do not appear to be attempt-
ing to usurp the territory (e.g. for nest site locations),
the low resources in the habitat may make defense
uneconomical and intruders are tolerated. The
elevated food solicitation call rates of birds in this
habitat during these same periods would further
support this interpretation. However, this behavior
may itself be risky for residents if there is the
prospect for intraspecific brood parasitism (see
below).
Parental feeding effort and adult condition: we
compared the feeding rates of males during
the incubation and nestling period over 2 years
to determine whether differences seen in the win-
ter and early breeding season persist through to
287
fledging (van Oort et al. in press). Feeding rates
were recorded by observations of color-banded
males provisioning young and show a trend that is
similar in pattern to that for female call rates noted
abovethere was no difference in the number of
feeding trips made by dominant versus subordin-
ate ranked males in the mature forest, but a large
disparity between dominant and subordinate pairs
in the young forests. Dominant males in the young
forest had much higher provisioning rates than
their subordinate counterparts, the latter of whom
had the lowest provisioning rates of all categories
of nests. It is worth noting that the analysis was
done using those subordinate pairs who had
successfully managed to breed in the young forest,
as many subordinate pairs did not succeed long
enough to produce nestlings in these years.
We caught males during the early nesting period
soon after feeding observations had ended,
measuring these males condition using morpho-
logical and haematocrit measures. The latter
compares the proportion of blood volume that is
red blood cells, and has been used as an index of
workload in different habitats in great tits (Ots et al.
1998). The haematocrit measures may also be
sensitive for assessing workload in chickadees, as
dominant males with their associated higher
metabolic costs consistently had higher haematocrit
levels than their subordinate counterparts (van
Oort et al. in press). In addition, blood haematocrits
were nearly 10% higher among males in the young
forest sites compared to the mature forest sites. The
increase in haematocrits was parallel across
ranksdominant males in both habitats had
higher haematocrit levels than their subordinate
neighbors, but both rank classes had higher haema-
tocrits in the young forests than their rank counter-
part in the mature forests (van Oort et al. in press).
This would appear to indicate that males, regard-
less of their social rank, may be induced to work
harder in the young forest, which makes the high
feeding rates of dominant males in these sites even
more costly.
Taken individually, there are potentially alterna-
tive interpretations that could be made to each of
the behavioral differences noted above. For example
high ranked males in the young forest may not sing
at dawn simply because there isnt much advantage
288 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
to itHansen et al. (2005) found that fewer males
are audible in these habitats during the dawn
chorus, so perhaps simply no one is listening.
However, females in this species appear to assess
males as extra-pair partners or divorce partners
during the dawn chorus (Chapter 14), so the reduc-
tion in singing by dominant males may be
ultimately disadvantageous. Alternatively, males
may have to balance energy reserves more in the
young forests, being unable to allocate large effort
in their own advertisement in order to ensure
adequate food supplies to their mates through
courtship feeding effort. The higher workloads
indicated by haematocrits during the nestling
feeding period would support this increased
energy requirement of birds in the young forests. In
poor habitats, dominant males may be forced to
allocate limited reserves to parental effort as
opposed to extra-pair advertisement. Such a trade-
off may explain the lower solicitation call rates of
females mated to dominant males in the young for-
est sites contrasting with low dawn song rates by
these dominant males. If dominant males in young
forests allocate more of the apparently limited
reserves offered in these sites to parental effort, it
may also explain the greater disparity between
fledging success and feeding rates of dominant and
subordinate pairs in this habitat compared to pairs
in mature forest. Thus, dominant males may adopt
a more paternal role to ensure within-pair repro-
ductive efforts rather than capitalizing on extra-
pair opportunities that are common in mature
forests (Otter et al. 1998; Mennill et al. 2004).
Possibly, the high nest abandonment rates of the
subordinate neighbors make allocating limited
resources to siring extra-pair young undesirable.
Comparisons are underway to determine whether
there are differing mating tactics with respect to
extra-pair behavior across the two habitat types.
If dominant males in young forests focus on
within-pair parental effort rather than extra-pair
matings, this effort may still be thwarted.
Chickadees are known to engage in intraspecific
brood parasitism, but do so at an extremely low
rate in mature woodlands (only two of over 110
Ontario nests tested had young unrelated to
both parentsOtter et al. 1998, Mennill et al. 2004).
The scenario in the Ontario population promoting
egg-dumping appeared to be a subordinate pair
whose own nesting attempt failed parasitized the
nest of their dominant flock-mates. In mature
forest, nest abandonment by subordinate pairs is
low and tends to occur during the latter parts of
incubation (K. A. Otter, K. T. Fort, and H. van Oort,
unpublished data); by comparison, many subordi-
nate pairs in the young forest sites abandon prior
to completion of a clutch (Fort and Otter 2004b).
Thus, the potential for intraspecific brood
parasitism is high. Although there is no difference
in clutch size between the two habitats (Fort and
Otter 2004b), it is still unknown whether egg
dumping in the young forest is high and what, if
any, impact this has on both reproductive success
and future survival condition of dominant males in
these habitats. Thus, even when birds successfully
fledge nestlings in the young forest, there are
numerous potential impacts to the condition and
behavior of these residents. Although these
impacts may have significant consequences to the
birds themselves, many of these will not be
detected by simply censuses for presence/absence
of breeding birds in the matrix.
17.4 Parids and insight into the use
of matrix in conservation planning
Parids are ideal in testing the potential of matrix
habitat to sustain or enhance breeding populations
of forest generalist birds. Most members of the
family are generalist enough to occupy a wide
variety of habitats, ranging from pristine wood-
lands to suburban yards. However, as indicated
above, all habitats are not perceived equally by
these highly matrix-tolerating bird species. If
success is merely equated with use of these habi-
tats, presence in the matrix could easily be miscon-
strued as sufficient compensation for a small
allocation of remnant habitat. However, as the
work on European tits indicates, minor differences
in the vegetative structure between habitats can
have enormous implications on prey availability.
The ability to adapt to these local differences
appears to rely on the genetic isolation of popula-
tions, which is antithetical to the objectives of using
a matrix to facilitate interpatch movement. Even
 H A B I TAT Q UA L I T Y A N D R E P R O D U C T I V E B E H AV I O R
when genetic differentiation occurs, it may simply
allow minor adjustments to living in a resource-
poor environment, but reproductive success and
individual condition may still be largely depressed.
Research on chickadees suggests that similar
habitat quality issues can arise with the use of a
matrix of similar vegetation, but much different
seral stage, from the remnant habitats.
This does not negate the importance of managing
matrix habitat. The matrix likely serves a very
important role in facilitating movement between
patches, and creating habitat with structural matur-
ity and/or similar species composition to the
remnant forests should promote this function. Our
research has also yet to directly test the halo effect
of the effects of breeding on the edge, and
whether birds in these circumstances perform and
behave similarly to birds breeding in either pure
habitat, or whether they are intermediate in nature.
However, caution needs to be emphasized so that
management planners dont simply perceive
matrix and remnant patches as interchangeable. It
is important to emphasize that the retention of a
species in a disturbed landscape does not necessar-
ily mean that the species is unaffected by disturb-
ance. Retention is merely the first step in
managementit should not be the final measure of
impact.
Acknowledgements
Z.McDonell, C. Holschuh, I.-J. Hansen, E. Brunsch,
S. Atherton, M. Kellner, K. Litwinow, and innumer-
able volunteers have contributed greatly to the
work at UNBC. We also greatly appreciated add-
itional comments on the manuscript provided by
Robert Curry and Marc Blisle. Our research is
supported primarily through the Natural Sciences
and Engineering Research Council of Canada.
References
Banbura, J., Blondel, J., de Wilde-Lambrechts, H., Galan,
M.-J. and Maistre, M. (1994). Nestling diet variation in
an insular Mediterranean population of blue tits Parus
caeruleus: effects of years, territories and individuals.
Oecologia, 100, 413420.
289
Blondel, J. (1985). Breeding strategies of the blue tit and coal
tit (Parus) in mainland and island Mediterranean habi-
tats: a comparison. Journal of Animal Ecology, 54, 531556.
Blondel, J. and Dias, P. C. (1994). Summergreenness, ever-
greenness and life history variation in Mediterranean
blue tits. In: Arianoutsou, M. and Groves, R. H., eds.
PlantAnimal Interactions in Mediterranean-Type
Ecosystems, pp. 2536. Kluwer Academic Publishers,
Netherlands.
Blondel, J., Dervieux, A., Maistre, M., and Perret, P. (1991).
Feeding ecology and life history variation of the blue tit
in Mediterranean deciduous and sclerophyllous habi-
tats. Oecologia, 88, 914.
Blondel, J., Dias, P. C., Maistre, M., and Perret, P. (1993).
Habitat heterogeneity and life-history variation of
Mediterranean blue tits (Parus caeruleus). Auk, 110,
511520.
Blondel, J., Dias, P. C., Perret, P., Maistre, M., and
Lambrechts, M. M. (1999). Selection-based biodiversity
at a small spatial scale in a low-dispersing insular bird.
Science, 285, 13991402.
Blondel, J., Maistre, M., Perret, P., Hurtrez-Bousscs, S., and
Lambrechts, M. M. (1998). Is the small clutch size of a
Corsican blue tit population optimal? Oecologia, 117,
8089.
Blondel, J., Perret, P., and Maistre, M. (1990). On the genet-
ical basis of the laying-date in an island population of
blue tits. Journal of Evolutionary Biology, 3, 469475.
Braillet, C., Charmantier, A., Archaux, F., Dos Santos, A.,
Perret, P., and Lambrechts, M. M. (2002). Two blue tit
Parus caeruleus populations from Corsica differ in social
dominance. Journal of Avian Biology, 33, 444450.
Castelln, T. D. and Sieving, K. E. (2006). An experimental
test of matrix permeability and corridor use by an
endemic understory bird. Conservation Biology, 20,
135145.
Cooper, C. B. and Walters, J. R. (2002). Experimental
evidence of disrupted dispersal causing decline of
an Australian passerine in fragmented habitat.
Conservation Biology, 16, 471478.
Davies, K. F., Gascon, C., and Margules, C. R. (2001).
Habitat fragmentation: consequences, management,
and future research priorities. In: Soule, M. E. and
Orians, G. H., eds. Conservation Biology: Research
Priorities for the Next Decade, pp.8197. Island Press,
Washington, DC.
Dhondt, A. A., Adriaensen, F., Matthysen, E., and
Kempenaers, B. (1990). Nonadaptive clutch sizes in tits.
Nature, 348, 723725.
Dhondt, A. A., Kempenaers, B., and Adriaensen, F. (1992).
Density-dependent clutch size caused by habitat het-
erogeneity. Journal of Animal Ecology, 61, 643648.
290 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
Dias, P. C. (1996). Sources and sinks in population biology.
Trends in Ecology and Evolution, 11, 326330.
Dias, P. C. and Blondel, J. (1996). Breeding time, food
supply and fitness components of blue tits Parus
caeruleus in Mediterranean habitats. Ibis, 138, 644649.
Ekman, J. B. and Lilliendahl, K. (1992). Using priority to
food access: fattening strategies in dominance-structured
willow tit ( Parus montanus) flocks. Behavioral Ecology, 4,
232238.
Ficken, M. S., Ficken, R. W., and Witkin, S. R. (1978). Vocal
repertoire of the black-capped chickadee. Auk, 95, 3448.
Fort, K. T. and Otter, K. A. (2004a). Territorial breakdown
of black-capped chickadees Poecile atricapillus, in
disturbed habitats? Animal Behaviour, 68, 407415.
Fort, K. and Otter, K. A. (2004b). Effects of habitat disturb-
ance on reproduction in black-capped chickadees
(Poecile atricapillus) in Northern British Columbia. Auk,
121, 10701080
Gascon, C., Lovejoy, T. E., Bierregaard, R. O., Jr, Malcolm,
J. R., Stouffer, P. C., Vasconcelos, H. L., Laurance, W. F.,
Simmerman, B., Tocher, M., and Boges, S. (1999). Matrix
habitat and species richness in tropical forest remnants.
Biological Conservation, 91, 223229.
Godfrey, J. D. (2003). Potential use of energy expenditure
of individual birds to assess quality of their habitats.
Science for Conservation, 214, 1124.
Gosler, A. G. (1996). Environmental and social determin-
ants of winter fat storage in the great tit Parus major.
Journal of Animal Ecology, 65, 117.
Hansen, I. J., Otter, K. A., and van Oort, H. (2005).
Communication breakdown? Habitat influences on the
communication networks in black-capped chickadees.
Acta Ethologica, 8, 111120.
Lambrechts, M. M., Caro, S., Charmantier, A., Gross,
N., Galan, M.-J., Perret, P., Cartan-Son, M., Dias, P. C.,
Blondel, J., and Thomas, D. W. (2004). Habitat quality as
a predictor of spatial variation in blue tit reproductive
performance: a multi-plot analysis in a heterogeneous
landscape. Oecologia, 141, 555561.
Laurance, W. F. (2000). Do edge effects occur over large
spatial scales? Trends in Ecology and Evolution, 15,
134135.
Mennill, D. J., Ramsay, S. M., Boag, P. T., and Ratcliffe,
L. M. (2004). Patterns of extrapair mating in relation to
male dominance status and female nest placement in
black-capped chickadees. Behavioral Ecology, 15,
757765.
Noss, R. F. and Cooperrider, A. Y. (1994). Saving Natures
Legacy: Protecting and Restoring Biodiversity. Island Press,
Washington, DC.
Nour, N., Currie, D., Matthysen, E., Van Damm, R., and
Dhondt, A. A. (1998). Effects of habitat framentation on
provision rates diet and breeding success in two species
of tit (great tit and blue tit). Oecologia, 114, 522530.
Ots, I., Murumagi, A., and Horak, P. (1998).
Haematological health state indices of reproducing
great tits: methodology and sources of natural vari-
ation. Functional Ecology, 12, 700707.
Otter, K., Chruszcz, B., and Ratcliffe, L. (1997). Honest
advertisement and singing during the dawn chorus of
black-capped chickadees, Parus atricapillus. Behavioral
Ecology, 8, 167173.
Otter, K., Ratcliffe, L., Michaud, D., and Boag, P. T.
(1998). Do female black-capped chickadees prefer high-
ranking males as extra-pair partners? Behavioral Ecology
and Sociobioliology, 43, 2536.
Otter, K. A., Atherton, S. E., and van Oort, H. (in press).
Female food solicitation calling, hunger levels and habi-
tat differences in the black-capped chickadee. Animal
Behaviour.
Perret, P. and Blondel, J. (1993). Experimental evidence of
the territorial defense hypothesis in insular blue tits.
Experientia, 49, 9498.
Remes, V. (2003). Effects of exotic habitat on nesting suc-
cess, territory density, and settlement patterns in the
blackcap (Sylvia atricapilla). Conservation Biology, 17,
11271133.
Ricketts, T. H. (2001). The matrix matters: effective isola-
tion in fragmented landscapes. American Naturalist, 158,
8799.
Riddington, R. and Gosler, A. G. (1995). Differences in
reproductive success and parental qualities between
habitats in the great tit Parus major. Ibis, 137, 371378.
Seki, S.-I. and Takano, H. (1998). Caterpillar abundance in
the territory affects the breeding performance of great
tit Parus major minor. Oecologia, 114, 514521.
Smith, S. (1988). Extra-pair copulations in black-capped
chickadees: the role of the female. Behaviour, 107, 1523.
Smith, S. (1991). The Black-capped Chickadee; Behavioral
Ecology and Natural History. Comstock Publishing
Associates, Ithaca.
Stauss, M. J., Burkhardt, J. F., and Tomiuk, J. (2005).
Foraging flight distances as a measure of parental effort
in blue tits Parus caeruleus differ with environmental
conditions. Journal of Avian Biology, 36, 4756.
Tabarelli, M. and Gascon, C. (2005). Lessons from frag-
mentation research: improving management and policy
guidelines for biodiversity conservation. Conservation
Biology, 19, 734739.
Thessing, A. (2000). Growth and final size of willow tit
Parus montanus under different environmental condi-
tions. Ardea, 88, 215224.
Thomas, D. W., Blondel, J., Perret, P., Lambrechts, M. M.,
and Speakman, J. R. (2001). Energetic and fitness costs
 H A B I TAT Q UA L I T Y A N D R E P R O D U C T I V E B E H AV I O R
of mismatched resource supply and demand in season-
ally breeding birds. Science, 291, 25982600.
Tobias, J. A. and Seddon, N. (2002). Female begging in
European robins: do neighbors eavesdrop for extrapair
copulations? Behavioral Ecology, 13, 637642.
Tremblay, I., Thomas, D., Blondel, J., Perret, P., and
Lambrechts, M. M. (2004). The effect of habitat quality
on foraging patterns, provisioning rate and nestling
growth in Corsican blue tits Parus caeruleus. Ibis, 147,
1724.
Tremblay, I., Thomas, D. W., Lambrechts, M. M., Blondel,
J., and Perret, P. (2003). Variation in blue tit breeding
performance across gradients of habitat richness.
Ecology, 84, 30333043.
Tubelis, D. P., Cowling, A., and Donnelly, C. (2004a).
Landscape supplementation in adjacent savannas and
its implications for the design of corridors for forest
birds in the central Cerrado, Brazil. Biological
Conservation, 118, 353364.
291
Tubelis, D. P., Lindenmayer, D. B., and Cowling, A.
(2004b). Novel patch-matrix interactions: patch width
influences matrix use by birds. Oikos, 107, 634644.
van Oort, H. and Otter, K. A. (2005). Natal nutrition and
habitat distribution of male and female black-capped
chickadees. Canadian Journal of Zoology, 83, 14951501.
van Oort, H., Otter, K. A., Fort, K., and Holschuh, C. I.
(2006). Habitat quality affects the reliability of a condi-
tion-dependent signal in black-capped chickadees.
Ethology, 112, 772778.
van Oort, H., Otter, K. A., Fort, K., and McDonell, Z. (in
press). Habitat, dominance, and the phenotypic quality
of male black-capped chickadees. Condor.
Verhulst, S. and Tinbergen, J. M. (2001). Variation in food
supply, time of breeding, and energy expenditure in
birds. Science, 294, 471.
Weise, C. M. and Meyer, J. R. (1979). Juvenile dispersal
and development of site-fidelity in the black-capped
chickadee. Auk, 96, 4055.
This page intentionally left blank
 SYNOPSIS IV
Landscape ecology, behavior,
and conservation issues
Andr Desrochers, Ken A. Otter, Marc Blisle, and
Jennifer R. Olson
Introduction
Conservation does not require landscape ecology,
nor the study of behavior. Given the frequent focus
of conservation on landscapes, however, and the
fact that population patterns in landscapes can be
difficult to interpret without an understanding of
the behavior of individual animals, the synergy
between those fields also cannot be denied. We
believe that, as a result, landscape ecology and
behavior contributed greatly to the advance of
science-based conservation, especially in the last
two decades. For example, empirical and simula-
tion studies of individuals responses to landscapes
demonstrated the influence of habitat loss on
dispersal, metapopulation dynamics, and species
viability. Conversely, conservation issues have
contributed greatly to the study of landscape ecol-
ogy and behavior, simply because they fed those
fields with a rich variety of problems to solve, and
substantial amounts of money to address those
problems.
Among its trickle-down effects, the synergy
between landscape ecology, behavior, and conser-
vation has spurred advances in the study of Parids,
in areas that were not previously investigated in
detail in this family, especially landscape and
matrix use. In return, Parids may hold much
promise for the fields of landscape ecology, behav-
ior, and conservation because of their potential as
a model system. In this synopsis, we highlight
some key points of the latter three chapters, and
propose further thoughts to not only advance the
study of Parids, but also to emphasize the value
and relevance of Parids for students of landscape
ecology, behavior, and conservation. We proceed
under two frameworks. First, we will look at Parids
as a system with its intrinsic value for the advance-
ment of ornithology, with a focus on dispersal and
habitat selection. Second, we will consider the
value of Parids as a model group for those inter-
ested in broad conservation issues.
Focus on the Parids
Global perspective
Ornithologists are still just breaking ground in
understanding landscape level issues with North
American and other Parids. We saw from a broad
range of geographic locations that Parids studied
in the Eurasian and in the North American often
respond to edges, patch size, forest fragmentation
and habitat heterogeneity, especially in landscapes
dominated by agriculture (Chapter 15). The Parids
themselves may not differ much in their response to
Eurasian versus North American landscapes, but
the studies of Parids landscape ecology does differ
greatly between those regions, at least in emphasis.
Work in the Eurasian is much farther along in
understanding habitat effects on breeding than it is
in North America, even though Eurasian studies are
largely limited to comparing birds among different
oak species forests. The fact that North American
Parids seldom opt for nestboxes in most areas (rela-
tive to Eurasian ones at least) remains a major
obstacle for the study of reproductive responses of
these birds to phenomena such as habitat loss or
293
294 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
degradation. However, work on black-capped
chickadees at Northern British Columbia shows that
those obstacles can be overcome. In contrast to the
work on breeding Parids, North American studies
of movement by individuals or flocks (Ohio,
Alberta, and Quebec) are farther ahead than those
from the Eurasian. Yet, as is the case with studies
on breeding Parids, some key questions remain
unanswered, such as, whether habitat fragmen-
tation impacts Parids more through reducing
access to habitat or by altering habitat quality.
As this book illustrates, there is a very strong
legacy of experimental work with all aspects of
Parid ecology. In the next couple of decades,
researchers working on Parids will evidently fill
many of the knowledge gaps pertaining to north-
ern/temperate locations. However, we need to put
things in perspective, and this requires taking into
account all regions of the geographical distribution
of Parids. Even though North American Parids
seem to respond to landscapes in much the same
way as Eurasian ones, this does not guarantee that
Parid responses to landscapes will be similar in
other parts of the World, where most Parid species
occur but where landscape issues remain largely
unaddressed in this family (Fig. VI.1). Studies of
African and south-east Asian Parids hold much
promise not only for the advancement of compara-
tive or meta-analytic studies, but also as opportun-
ities to measure the geographic scope of landscape
ecology hypotheses with fresh, independent
evidence. Our understanding of Parids as a family
will remain grossly incomplete until we tackle
several unstudied species in Asia and Africa.
Additionally, new studies in Africa or Asia may
uncover unsuspected threats to populations of rarer
Parids, or point to potential solutions for vulnerable
or threatened species. Fortunately, only four of the
Worlds ca. 65 Parids are currently listed by the IUCN
(2004). All four listed Parids (Parus holsti, P. nuchalis,
P. semilarvatus, Periparus amabilis) are little-known (for
this family) and endemic to south-east Asia.
Dispersal
As with most animals, the biggest period of move-
ment in Parids is also the most poorly understood,
and that is the period during natal dispersal. It is
during the first fall that these birds make their
primary, large-scale movement and we have little
idea how they do this, let alone how this is affected
by things such as fragmentation and disturbance to
the environment. Further, we do not understand the
significance of sudden influxes of juvenile chickadees
from outside local populationstypically called
irruptionsseen at banding stations, and whether
these relate to factors associated with landscape dis-
turbance (e.g. forest fires) and/or with (cyclic) vari-
ation in habitat productivity (Fig. VI.2). The detailed
studies of Parid movement and occurrence patterns
discussed in this section of the book show that minor
gaps in forests do constrain Parid movements, but at
the same time, they clearly indicate that Parids can
eventually reach even remote patches of forest. As a
result, it is impossible at the moment to infer just how
much impediments to individual movements scale-
up at the population level. That is especially true in
North America, as reflected by the lack of a thorough
discussion of dispersal and its outcomes in this book.
North American research on Parid dispersal basically
amounts to an old study of black-capped chickadees
in Wisconsin (Weise and Meyer 1979), and a handful
of banding studies mostly on irruptions by Parids
of unknown origin and destination. By contrast,
European researchers have produced numerous pub-
lications, led by landmark studies of Wytham Woods,
UK, and Northern Belgium. Yet, very few of these
publications addressed the influence of landscape
structure on dispersal processes and their resulting
occupancy patterns.
Although the latter studies in Europe benefit from
their extraordinarily long durations and associated
large number of band recoveries and reobservations,
there is no reason to believe that there is a European
monopoly on the study of Parid dispersal. Long-
term studies of Parids are becoming well established
in North America (Ohio, Massachusetts, Ontario,
British Columbia) and should offer nice avenues for
the data-hungry topic of natal dispersal. At the same
time, exciting new avian research tools, such as
microscale telemetry equipment and stable isotopes,
or clever low-tech experiments, may provide more
efficient methods to tackle natal and breeding dis-
persal questions without the need for long-term
datasets, thus bridging a knowledge gap between
Parid studies of different parts of the World.
 H A B I TAT Q UA L I T Y A N D R E P R O D U C T I V E B E H AV I O R 295

(a)

Species
1625
1015
69
15
0

(b)

Studies
721
56
34
12
0

Figure VI.1 Geographic patterns of Parid diversity (a) and landscape studies including Parids (b). Geographic regions in North America are
divided by states (US) and provinces (Canada) in (b) so as to more directly compare spatial distributions of the number of active studies on
landscape issues among Parids in relation to species distribution.

700

600

500
Individuals/100 h

400
Figure VI.2 Southward irruptive movements of black-
300 capped (black dots) and boreal (white dots) chickadees recorded
visually between August and November in Tadoussac, Quebec.
200
Observation effort averaged ( 1 SD) 913 142 h/year. The
100 proportion of juveniles (i.e. birds in their hatching year)
averaged ( 1 SD) 97 3% (n 7 banding years) and
0 86 13% (n 6 banding years) for black-capped and boreal
1994 1996 1998 2000 2002 2004 2006 chickadees, respectively. These data have been generously
Year provided by the Observatoire doiseaux de Tadoussac.

Until we collect direct evidence on movements of

juvenile Parids during the dispersal periods
(mostly in fall but also in spring, after flock break-
up), we will have to contend with weak inference
on dispersal processes, based on postdispersal
habitat selection (i.e. occupancy patterns).
Habitat selection at the individual level
Like dispersal, the problem of habitat selection has
generated much literature, but again with an
emphasis on occupancy patterns rather than
processes. From a pattern point of view, dispersal
296 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
and habitat selection may appear as very different
problems (typically with the latter focusing on
distribution patterns, and the former focusing on
dispersal distances). But from a process point of
view, those two problems are closely linked and
face the same difficulties. In the case of Parids,
flocking, when it occurs, makes things even more
complex, for habitat selection becomes a two-stage
process: first joining a flock (and its range), and,
second, partitioning the flock range into breeding
territories. As a result, dispersal activity probably
occurs not only in the fall, but also in the spring, as
in cases where subordinate individuals are expelled
from the flock home range altogether.
Contrary to the study of dispersal, the study of
Parid habitat selection has flourished both in the
Eurasia and in North America. If the selection of a
place to spend the autumn and the winter has been
the focus of earlier work (e.g. marsh tit in Sweden,
Nilsson and Smith 1988, and great tit in Japan,
Saitou 1979), Chapter 17 illustrates renewed
emphasis on the consequences of habitat selection
on breeding. Current evidence portrays the choice
of flocking locations (in the fall) largely as
determined by social factors (social dominance,
floating, and the availability of potential mates).
Dispersal decisions made in the fall are likely of the
utmost importance to temperate and boreal Parids.
Consider Olson and Grubbs outlined microclimate
effects on thermoregulatory physiology in winter-
ing Parids (Chapter 16)this illustrates the fantastic
challenges that birds wintering in temperate/north-
ern areas face. In fact, the potential of Parids to help
us understand how birds cope with extreme
weather remains largely untapped. Significant
advances on the physiological front (e.g. corticos-
teroid hormone levels, Chapter 3) are beginning to
show just how stressful disturbed habitats can be to
Parids (Lucas et al. 2006).
If habitat change is altering the evolved physio-
logical response mechanisms to deal with already
harsh environmental conditions, these can have
knock-on effects well beyond the direct challenges
posed by winter weather. For example birds
coming out of the winter in poorer body condition,
faced with reduced food availability, may burn
themselves out in egg laying and the provisioning
of nestlings, or simply abandon breeding altogether
(Chapter 17), only to enter the subsequent winter
again in poor condition, following an extra cost of
molting. Furthermore, low access to food mediated
by social dominance has been shown to constrain
individual Parids, such as black-capped chicka-
dees, entering the breeding season to settle in
lower-quality territories (Smith 1991). In habitats
that are relatively productive (such as deciduous
oak forests in Europe or the mature forests
mentioned in Chapter 17), the difference in quality
between territories of dominant and subordinate
pairs may be negligible, and allow opportunity for
success among young and subordinate pairs. As
subordinate pairs often constitute the majority of
a local population, the effect of their gaining oppor-
tunity to breed successfully is not a minor consid-
eration. However, in lower quality habitats
(evergreen oak, or young forestsChapter 17), the
dichotomy in quality between territories secured by
dominants and subordinates may be more extreme,
especially in low productivity years. The result may
be a larger contrast in reproductive success and
condition of birds based on rank in marginal
habitats, which may be even more exacerbated in
highly fragmented habitats because of the travels
costs imposed by multiple patch use (Hinsley
2000). As a consequence, Parids of contrasting
social ranks may adopt differing long-term repro-
ductive strategies in different habitats to compen-
sate for variation in habitat quality, but these
studies are still in their infancy.
Whether habitat selection processes with strong
demographic consequences occur mostly in the fall
or in the spring remains unknown in Parids, just as
with most songbirds. However, as with dispersal,
Parids lend themselves well to experiments on
habitat selection, for example they sometimes use
nestboxes and generally accept supplemental food,
at least at certain times of the year.
Parids as a model group
Although Parids as a group do not strike us as
requiring specific conservation measures, we argue
in this section that they could offer key knowledge
to address avian landscape and conservation
issues. First of all, they are typical passerines
in the sense that they are small, short-lived, and
 H A B I TAT Q UA L I T Y A N D R E P R O D U C T I V E B E H AV I O R
use all-purpose territories. Of course, the fact they
are short-lived is a blessing and a curse: one can
track differences over the course of individuals
lifetimes, but at the same time one cannot track
changes to individuals associated with longer scale
changes in the environment (e.g. rebounds associ-
ated with restoration projects, etc.) using individ-
uals as their own beforeafter controls.
What landscape/conservation problems could
Parids help us solve? Although the last two decades
have provided a plethora of information on bird
conservation issues, most of it is idiosyncratic and
therefore of limited value for those in search of
general patterns. The effect of landscapes on birds
is a case in point. Although we have solid evidence
that birds do not generally use forest patches inde-
pendently of what happens outside those patches
(based on presence/absence patterns), we have not
yet developed a solid understanding of the
processes underlying patch use. Several processes
undoubtedly lead to the frequent avoidance of
small or isolated forest patches, but it would be
useful to know under what circumstances edge
avoidance, movement issues, conspecific attraction,
other unsuspected factors, or a synergy among
those factors is the driving force behind landscape
occupancy patterns in most birds.
One of the major impediments to generalization
here is the overwhelming diversity in the life
history of the bird species investigated. In this
regard, Parids can offer huge insights to working
on larger issues associated with alteration to the
landscape (and climate), because they offer a
diversity of responses to landscapes, but at the
same time share a lot of life history traits, making
the diversity of landscape response hopefully more
manageable.
Parids have several things to offer as a model
group:
They are extremely well studied, and there is a lot
known about their behavior, evolution, and
ecological requirements.
There are large numbers of long-term studies
in areas that have undergone changes to the
landscape during the course of monitoring.
They use a variety of forested habitats, inter-
specifically, but more importantly, at the species
297
level, even within a locality. The fact that they also
take to habitat islands and can be experimentally
removed to look at recolonization rates, etc., makes
them a nice species for testing ideas about island
biogeography and the utility of different matrixes
and corridors for facilitating movement.
They lend themselves well to field experiments,
particularly because of their frequent use of feeders
(and sometimes nestboxes), but also because they
are not cryptic and they are generally easy to cap-
ture and mark. For example the fact that they are
easy to track (relative to other birds) has resulted in
them being one of the best studied groups for small
scale movement in relation to habitat gaps and
edges.
To illustrate the potential role of Parids as a
model group for the study of avian landscape
ecology, conservation, and behavior, consider the
effect of urban development on birds in North
American. There are a few studies on urbanization
effects on birds, but many of the results are con-
flicting, as are a lot of the studies on the effect of
habitat fragmentation. Most forest birds tend to
desert developing suburbs, but chickadees will
generally remain in those areas, thus providing
good opportunities to understand new opportuni-
ties and challenges posed by urbanization (which
are easier to interpret at the intraspecific than at the
interspecific level). Unlike most forest birds, chicka-
dees persist in towns and cities (either through
immigration or reproduction), thus offering inter-
esting opportunities for comparisons between town
and forest. Being cavity-nesters, chickadees get
heavily hit by urbanization in terms of nest-site
limitation, which presumably explains why they
appear to take more readily to nestboxes in sub-
urbs. At the same time, they benefit from bird feed-
ers. Fragmentation and other urban sprawl also put
Parids much more directly in competition with
exotics (house sparrows) for cavities, and also
exposes them to nest predators, such as house
wrens, that they do not contend with when living
away from edges. However, the difficulty of setting
up long-term studies in urban settings has probably
limited these studiesfocus on urban parks or
large campuses (such as the University of British
Columbia, Canada) may help remedy this.
298 L A N D S C A P E E C O L O G Y, B E H AV I O R , A N D C O N S E R VAT I O N
References
Hinsley, S. A. (2000). The costs of multiple patch use by
birds. Landscape Ecology, 15, 765775.
IUCN (2004). 2004 IUCN Red List of Threatened Species.
www.iucnredlist.org.
Lucas, J. R., Freeberg, T. M., Egbert, J., and Schwabl, H.
(2006). Fecal corticosterone, body mass, and caching
rates of Carolina chickadees (Poecile carolinensis) from
disturbed and undisturbed sites. Hormones and
Behaviour. 49, 634643.
Nilsson, J.-. and Smith, H. G. (1988). Effects of dispersal
date on winter flock establishment and social domi-
nance in marsh tits Parus palustris. Journal of Animal
Ecology, 57, 917928.
Saitou, T. (1979). Ecological study of social organization in
the great tit, Parus major L. II. Formation of the basic
flocks. Journal of the Yamashina Institute of Ornithology,
11, 137148.
Smith, S. (1991). The Black-Capped Chickadee; Behavioral
Ecology and Natural History. Comstock Publishing
Associates, Ithaca.
Weise, C. M. and Meyer, J. R. (1979). Juvenile dispersal
and development of site-fidelity in the black-capped
chickadee. Auk, 96, 4055.
 CHAPTER 18
What drives differences between
North American and Eurasian
tit studies?
Andr A. Dhondt
18.1 Introduction
In comparing studies of Parid ecology, evolution,
and behavior that have been carried out in Eurasia
and North America it becomes clear that there
seem to be two essential factors that have driven
differences: differences in species biology and
the possibility to carry out long-term studies.
Differences in Parid evolution and natural his-
tory between North America and Eurasia
have often dictated the types of research questions
that can be addressed. Long-term studies, many
of which have now gone on for 20 or more
years, have made it possible to obtain answers
before questions were asked.
The phylogeny of the Paridae that Gill et al.
(2005) have developed (see Fig. 2.1) can be used
to map different traits on the cladogram,
making it possible to determine which traits
are ancestral and which traits are derived.
Based on this, the two main species that have
been studied in Eurasia (great and blue tit)
are at the base of the Parid tree, while all
North American species are the result of two
invasions 3.5 and 4 MBP (million years before
present) (Gill et al. 2005, see also Chapter 1).
North American Parids, therefore, belong to more
derived clades. Great and blue tit, the primary
study species that European scientists have been
studying as model species for more than 50 years
may, after all, not be representative for all tits and
chickadees.
18.2 Natural history traits determine
the ease of study and the questions
asked
The types of research questions addressed by North
American and Eurasian Parid researchers often do
not coincide. Rather than differences in interests
across continents, this may simply reflect the kinds
of studies that are possible with the Parids that
occupy the different regions. In Table 18.1, I have
briefly summarized important differences between
great and blue tit against the more derived tits, such
as those more prominent in North America. Note
that excavating a hole (rather than using an existing
one), caching food in the fall to be used during
winter (requiring an enlarged hippocampus), and
living in pair or group territories during winter
(which leads to winter limitation) are all synapo-
morphies. Caching food and remaining territorial
year-round evolved before the Baeolophus,
Lophophanes, Periparus, and Poecile split off from the
Parus group. One can speculate that both traits
evolved simultaneously to enhance winter survival
in response to a period of colder climate, and that
taxa that developed these traits would have been
preadapted to invade North America across the
Bering Strait.
Among the Baeolophus, Lophophanes, Periparus,
Poecile group, cavity excavation evolved multiple
times independently. Lhrl (1966) pointed out that
excavation among Poecile-tits (and nuthatches)
occurs among smaller taxa. He suggested that the
299
300 N O RT H A M E R I C A N A N D E U R A S I A N T I T S T U D I E S
Table 18.1 Some differences between great and blue tit, and the more derived Parid clades
Ancestral
(great, blue)
Breeding territory
General purpose territory (Type A), usually 0.51 ha (35 ha in Bialowica) General purpose territory (Type A), usually 110 ha
Winter social organization
Winter flocks with site-specific dominance
* leads to summer limitation, and high breeding density
Winter ecology
Non-hoarding
* migrates or uses human-provided food in cold winters
Nesting
Secondary cavity nester; non-excavator
Mostly single loader, many feeding visits by adults per hour
Song
Song with individual repertoire and multiple song types with small-scale Limited song repertoire but complex vocalizations, limited geographic
geographic variation of song types found in populations;
song output high
*many studies of song and male quality
inability of the somber tit, one of the larger species
among these, to excavate limited its distribution to
areas where great tits are rare, and therefore natural
cavities available. Although this might explain why
somber tits have a limited distribution, I would sug-
gest that the selective pressure that has led smaller
Poecile tits and nuthatches to excavate (or frequently
excavate) their nests is more likely the result of
interspecific competition with larger species for lim-
ited numbers of cavities. Note that these excavating
species did not develop adaptive morphological
changes for excavation, thereby limiting their ability
to excavate to locations in soft or rotting wood, so
that cavities are not really safe from predation
(Christman and Dhondt 1997).
Great and blue tit never excavate their own cavity,
and therefore rely on existing cavities (and are part
of a cavity guild; see Chapter 8). They prefer nest
boxes to natural cavities for breeding. Furthermore,
in winter they usually flock in large groups that
roam over an area an order of magnitude larger
than a breeding territory. As a result, breeding
Derived
(willow, marsh, black-capped, Carolina, crested,
tufted, boreal, etc.)
Winter group territory: local breeding pair usually joined by non-kin
juveniles in 1:1 sex ratio
* leads to winter limitation, and low breeding density
Hoarding; leads to enlarged hippocampus
* allows survival in extreme winter conditions
Some taxa excavate, but no adaptive morphological traits; excavation
has emerged multiple times, typically in smaller taxa in a
branch (Lhrl 1966)
Multiple loaderusually few visits by adult per hour
variation; song sometimes lost (crested tit, boreal chickadee,
chestnut-backed chickadee, Siberian tit)
* many studies of syntax
density of, especially, great tits can be very high
when excess numbers of nest boxes are provided in
high-quality, food-rich study plots. In a 12.5-ha
study plot inside a large woodland near Antwerp,
up to 58 pairs of great tits and 48 pairs of blue tit
nested in a given year. The highest combined
density in a single year was eight pairs per ha (52
great tit and 48 blue tit pairs). When birds use nest
boxes, nests can be found by simply checking these,
and observations on the content is easy. This has led
to numerous, long-term studies with large or very
large sample sizes, whereby hundreds of breeding
pairs were studied by one investigative team.
Furthermore, nest boxes make manipulative experi-
ments relatively easy, leading, for example, to
experimental studies of optimal clutch size, effects
of interspecific competition, effects of food manipu-
lation, etc.
By comparison, North American studies
have often focused on wintering and flocking
behavior, foraging, vocalizations, dominance,
with fewer long-term breeding studies, and few of
 N O RT H A M E R I C A N A N D E U R A S I A N T I T S T U D I E S 301

Table 18.2 Number of publications from Science Citation Index Expanded of North-American (N. Am.) and
Eurasian (EU) titmice; more ancestral clades are at the top, more derived clades at the bottom

Genus Species name Region Number of publications

Cyanistes blue tit EU 343

Parus great tit EU 1307
Lophophanes crested tit EU 43
Baeolophus bridled titmouse N.Am. 6
oak/plain titmouse N.Am. 5
juniper titmouse N.Am. 10
tufted titmouse N.Am. 39
Periparus coal tit EU 71
Poecile willow tit EU 193
marsh tit EU 94
Siberian/gray-headed EU N. Am. 25 1
somber EU 2
black-capped chickadee N.Am. 193
Carolina chickadee N.Am. 44
mountain chickadee N.Am. 40
Mexican, chestnut-backed, boreal N.Am. 10

Search was carried out on 28 December, 2005.

those addressing questions of optimal nesting
behavior.
Vocalizations are quite different between great
and blue tit, on the one hand, and the more derived
clades on the other. Great and blue (and coal) tits
sing a lot, both in spring and in the fall. Each
individual uses many different song types, and song
is sung in strophes. This has led European scientists
to study, primarily, variations in repertoire size and
in song production, and to relate this variation to
differences in male quality (McGregor et al. 1981;
Lambrechts and Dhondt 1986; Kempenaers et al.
1997). The song of North American chickadees is
less variable, but other types of vocalizations are
more variable leading to many fascinating studies of
syntax (Chapters 1014).
Another difference between North American and
Eurasian studies is related to the number of Parid
species with overlapping geographic distribution.
In Europe there can be six sympatric species, while
in North America there are rarely more than two,
but many species have parapatric distributions.
This difference has led to studies on interspecific
competition being frequent in Europe, while
studies of interspecies hybridization being more
common in North America.
Another factor that may influence the choice of
study species and number of studies is simply
relative abundance of ones study species. Great
tits are one of the best-studied species because they
are abundant, secondary-cavity nesters living in
diverse habitats. When searching in the Science
Citation Index Expanded (ISI Web of Science) for
publications that mention any of the titmice that
can be found in Eurasia or in North America more
papers mention the great tit (1307) than all other
species combined (1119) (Table 18.2). The blue
tit, another species that is mostly studied using
nest boxes, is the second most frequently studied
tit. Clearly the ease of studying a bird species
that readily breeds in nest boxes at high densities is
one of the factors driving the large number of
studies. Note that the importance of these studies
goes way beyond just understanding Parid
biology, as will be illustrated below. Among the
derived species the largest number of publications
mention willow tit (193) and black-capped
chickadee (193).
302 N O RT H A M E R I C A N A N D E U R A S I A N T I T S T U D I E S
18.3 The value of long-term studies:
Providing answers to questions not
yet asked
David Lack started his long-term studies of great
tits in Wytham Woods near Oxford with the explicit
assumption that what was true for great tits would
be true for other species as well. Lack was primarily
interested in what factors regulated numbers (Lack
1954) and adaptive explanations for clutch-size
variation. Lack was inspired by Kluyvers studies
in the Netherlands that had started in 1937.
Kluyver also had access to data that had been
collected by Wolda who had the foresight to initi-
ate nestbox inspections as early as 1912 (Kluyver
1951, p.3). Kluyvers work, in its turn, must have
been influenced by the pioneering studies of
Margaret Morse Nice (1937, 1943), as there are
many similarities in the questions addressed in her
papers on song sparrows and Kluyvers 1951 great
tit monograph. In 1959, Jan Hubl in Belgium
started collecting the data that I later analyzed in
many of my publications. Hubl explicitly modeled
his studies on Kluyvers work, to the extent that he
used the same Wageningen nest boxes.
I guess this is where the funding comes in. Long-
term studies cant be done without long-term fund-
ing. By 1970, Hubl had distributed about 800 nest
boxes, in eight study sites in and around Ghent. All
boxes were monitored for breeding by himself, two
university paid technicians, and students,
wherebyas in other studiesdetailed informa-
tion was obtained on nesting through weekly visits
to all nest boxes, all young were banded and most
adults caught. Furthermore, all boxes were checked
for roosting birds twice per winter. When I started
my own population studies near Antwerp in 1979,
I hung as many boxes as needed for the field experi-
ments on competition with the caveat that my
university-paid technician and I would be able to
collect all information (including individual
weights of nestlings, and identity of all adults).
The fact that I knew that I would have full-time
assistance for tens of years made it possible to start
a study that needed to be long-term and is still
ongoing under the leadership of Erik Mathyssen
and still involves the same technician who started
with me in 1978.
Note that in his book, Lack (1966) described all 13
bird population studies that had continued for at
least 4 years. Today, we have a few studies that have
continued for 50 years, and a large number that have
studied great and blue tit for 20 years. This makes it
possible to study, for example, how birds respond to
environmental changes (Visser et al. 2003).
In the next sections, I illustrate the fact that long-
term data sets make it possible to answer questions
that were unanticipated at the outset of data collec-
tion using three examples: (1) changes in spring
phenology; (2) dispersal and local adaptation; and
(3) effects of habitat fragmentation.
18.3.1 Spring phenology
When Lack and Kluyver began their studies on
great tit breeding biology more than 50 years ago,
questions on possible effects of global warming, or
of large-scale climate fluctuations (NOA or El Nino)
where not on the agenda of biologists (see also
Chapter 5). However, when in the 1990s evidence
for important changes in phenology arose, both the
English and the Dutch studies provided important
information.
McCleery and Perrins (1998) showed that between
1947 and 1970 spring temperatures had gradually
become colder and that great tits initiated laying
gradually later; after 1970 however, as spring
temperatures warmed up the tits began to lay earlier
and earlier. The interesting part of the story here is
that the relationship between spring temperature
and lay-date (or first-egg-date) was not different
during the cooling period, 19471970, and the warm-
ing up period, 19711997. Visser et al. (1998), using
the Dutch data, confirmed that from 1972 onwards
great tits began to lay earlier, that this was an adap-
tive response to the temperature-driven earlier cater-
pillar peak, but that nevertheless the tits were not
able to fully follow this change in phenology and
that the magnitude of selection differential
representing the extent to which great tits mistimed
layinggradually increased over a 20-year period.
Taking advantage of the large number of long-
term studies, Visser et al. (2003) compared changes
in lay-date over a 20-year period in 24 populations
of great and blue tit in 14 study sites between
Corsica in the south and Finland in the north,

and between the UK in the west and Russia in
the east. They found very large differences
in changes in lay-date between sites, whereby in
some sites lay-dates did not change, while in
others lay-dates advanced on average as much as
0.67 days per year. The analyses showed that, in
general, lay dates changed where spring tempera-
tures had changed, while they did not change
where there had been no increase in spring
temperature (for example in Russia and Finland),
or where the phenology of the entire food chain
(evergreen treescaterpillarsbirds) is less tempera-
ture sensitive (Corsica). One of the more surprising
results was that in two neighboring sites just
50 km apart (Antwerp, N. Belgium; Breda, S.
Netherlands), where the patterns of spring
temperatures changes had been very similar,
changes in lay-dates were very different: the
Belgian population showed the strongest change in
lay-date over the 20-year period (0.667 per year
for great tit and 0.594 for blue tit), while the
Dutch population showed one of the weakest
(0.177 great tit, 0.337 blue tit). Further analyses
suggested that another life-history characteristic
(% second broods) seemed to have a major effect on
changes in first-brood lay-dates. In populations
with few second broods, first-brood lay-dates
rapidly changed with changes in spring tempera-
tures. In contrast, among populations in which
second broods were frequent, first-brood lay-dates
did not respond to changes in spring temperatures,
but the % second broods declined.
18.3.2 Dispersal and local adaptation
Dispersal, causing gene flow, counteracts local
adaptation through natural selection via its hom-
ogenizing effect. Long-term studies on great and
blue tit in four countries have greatly contributed to
refine our understanding of this central theoretical
concept in evolutionary biology. Inspired by Chris
Perrins concluding remarks at the 1989 Corsica
meeting on hole-nesting birds (Perrins 1990),
Dhondt et al. (1990) analyzed their data and docu-
mented that, in high-quality habitat, great and blue
tits laid clutches that were smaller than what would
be most productive, while in low quality habitat tits
laid clutches that were larger than what would
N O RT H A M E R I C A N A N D E U R A S I A N T I T S T U D I E S 303
be most productive. The inability of the tits to
evolve to an optimal clutch in a heterogeneous
landscape was caused by the high proportion of
females that immigrated into each study plot, often
from sites with a different optimum. If gene flow is
low and local selection pressures very strong, then
strongly differentiated populations may arise as
illustrated by Blondel et al.s (1999) studies on
Corsican blue tits living in evergreen and decidu-
ous oak habitats. On Vlieland, another island, the
optimal clutch size is lower than that on the adja-
cent mainland 20 km away. Kluyver selected
Vlieland to study the role of density-dependent
survival in population regulation and started a new
study there in 1955, because it was the most remote
of the Dutch Frisian islands and few immigrants
were to be expected. The island comprises one large
wood of 214 ha, and four smaller ones covering
78 ha together (Kluyver 1971). Postma and Van
Noordwijk (2005) showed that the clutch size in the
large area was significantly smaller than in the
smaller ones. In the large area, low immigration
(13%) combined with strong selection against
immigrant genes maintained that subpopulation at
its adaptive value, while in the smaller areas the
proportion of immigrants from the mainland
(which carry genes for large clutches) was too
high (43%) and the higher immigration rate pre-
vented local adaptation. In contrast to these three
examples, the fourth study in Wytham Woods,
UK, showed that dispersal was non-homogenous,
thereby enhancing evolutionary differentiation at
surprisingly small scales (Garant et al. 2005).
Because great and blue tit breed in nest boxes it
was possible to collect, in all four long-term studies,
very detailed information (lay-date, clutch size,
fledging success, individual nestling weight and
size at fledging, identity and survival of parents,
and recruitment of fledglings to breeding) over
extended periods for large numbers of breeding
pairs, providing sufficient power for all these
analyses.
18.3.3 Effects of habitat fragmentation
Habitat fragmentation is a hot topic today, with
several chapters in the book addressing aspects of
this topic. According to the ISI Web of Science the
304 N O RT H A M E R I C A N A N D E U R A S I A N T I T S T U D I E S

first paper that mentions this term was published
in 1984, with more than half being published in the
4-year period 20022005 (1055 of 2009 or 52.5%)
(Fig. 18.1). Clearly, when the long-term studies
were initiated the question as to possible effects of
habitat fragmentation on populations and commu-
nities had not been asked. One of the advantages
of studying woodland birds in northern Belgium is
that most wooded areas are small and isolated. So
250
Number of publications
when a Dutch colleague visited me in Belgium in
the late 1980s and asked me if I had any data on tit
populations in fragmented habitats I said: Sure,
about 20 years worth of data. I realized only after
establishing a new set of nest box plots near
Antwerp in 1979 that the reason the birds I had
studied near Ghent did not behave like the birds I
had read about in the literature was that they
lived in isolated habitat fragments. In the Ghent
fragments, nestling mortality tended to be high and
nestling weights tended to be low even in high-
quality oak habitat (Table 18.3). Furthermore, the
most productive clutch size was much larger in
plots within large woodlots than in plots in
fragments. We also found that during winter, birds

200 that lived in fragments tended to flock less, leading

to a lower divorce rate (Dhondt et al. 1996).
Fragment size and isolation also greatly impacts
150
local recruitment rates (Matthysen et al. 2001).
The study system described in Chapter 8 was
100 established as a long-term study in the 1990s about
200 km south of Prince George in central BC. The
50 intent was to look at fragment size and logging on
nest-web communities. As one of the unexpected
0
outcomes, Kathy Martin suddenly found herself
1985 1990 1995 2000 2005 with a picture of community structure and nesting
Year published success of various cavity nesters (chickadees,
woodpeckers, nuthatches, etc.) before and after
Figure 18.1 Number of publications mentioning fragmentation
a pandemic attack of mountain pine beetles. The
according to a search on the ISI Web of Science on 28 December
2005. The first paper that mentions this term appeared in 1984; current infestation is unprecedentedwithin
more than half were published in the 4-year period 20022005 the next 10 years it is anticipated that 80% of the
(1055 of 2009 or 52.5%). lodgepole pine in an area about the size of England

Table 18.3 Effect of woodlot size on great tit and blue tit reproduction

Great tit Blue tit

F/E 15-day mass (g) Most productive F/E 15-day mass (g) Most productive
clutch size clutch size

Plots in large woodlot near Antwerp

B 0.90 17.64 12 0.85 11.15 14
TL 0.90 17.58 12 0.97 11.16 14
Isolated fragments near Ghent
Z (G for blue tit) 0.79 15.65 8 0.85 n.d. 12
H 0.80 16.02 11 0.75 10.6 9

Data from Table 1 in Dhondt et al.. 1990. F/E: fledglings per egg in successful first broods. All plots are predominantly oak, except plot H which is
predominantly beech.

will be completely decimated. Because she had
10 years of breeding data of all species before the
pandemic hit her site, Kathy Martin can now look
at how chickadees respond to changes in other
species densities. Long-term studies, wherever
they are carried out, always contribute to answers
of questions not asked at the onset. As landscapes
become more and more fragmented, through what-
ever cause, a deep understanding of factors that
influence habitat quality gain in importance and
the older data from long-term studies combined
with more recent studies focusing on fragmentation
effects (Chapters 1517) may help us alleviate some
of its effects.
18.4 Winter group territoriality: A
derived trait that leads to winter
limitation
A marked difference between great and blue tits
and the species belonging to the Periparus, Poecile,
Lophophanes, and Baeolophus clades concerns winter
social organization (Ekman 1989). Great tits, and
probably also blue tits (although not well studied!)
have a relatively loose organization characterized
by semistable basic flocks which often intermin-
gle and live in overlapping home ranges (Saitou
1978). The other species live in discrete units (pairs
or small groups) with a linear dominance hierarchy
and high coherence among members. These winter
flocks reside within non-overlapping territories
that are actively defended. In Ekmans (1989)
review of non-breeding social behavior in Parids,
he lists just eight studies involving great and four
involving blue tits (together 18.5% of 65 studies),
compared to 53 (81.5%) in the more derived clades.
These latter are about equally divided between
Eurasian and North American species. Studies of
non-breeding social organization are thus rare in
great and blue tit, but much more frequent in win-
ter-flocking species, especially when compared to
the proportions mentioned in Table 18.2 (68% of all
studies refer to great and blue tit). It is also interest-
ing to underline that 26 of 42 studies in Europe
were carried out in Scandinavia (primarily
Sweden). In North America, black-capped
chickadees and tufted titmice were studied
most frequently and fascinating questions were
N O RT H A M E R I C A N A N D E U R A S I A N T I T S T U D I E S 305
addressed concerning cost and benefits of flock
joining and flock switching, effects of winter food
and temperature on over winter survival, and more
recently effects of fragmentation, winter food and
temperatures, and interspecific competition
(Chapter 16).
In that context, a large number of experiments
have been carried out to determine the extent to
which the winter flock territories actually limit
breeding population density. The first removal
experiment with a winter-territorial species
(Cederholm and Ekman 1976) was carried out just
before the breeding season and, to the surprise of
the authors, showed no replacements (Table 18.4).
The authors concluded that there were no surplus
birds and wrote (p. 212): As our removals were
done late in spring they do not, however, exclude
the possibility that territorial behaviour limits
numbers earlier on. the question should be pur-
sued by further removal experiments outside the
breeding season. With the exception of Otter and
Ratcliffe (1996) all other removal experiments in
this group of species were done in fall and winter,
and nearly all showed that in these winter-
territorial titmice very few, if any, surplus birds
remained alive by the beginning of the breeding
season. Hogstad (1989b) carried out a series of
removal experiments between September and
February. In each instance, he removed a single
bird from territorial groups and after a few days
released the removed birds back into their flock. In
October and November all removed birds were
replaced by non-territorial floaters and the
rereleased birds expelled the replacement birds
showing that floaters were subordinate individu-
als. Later in the season removed birds were no
longer replaced, indicating that no non-territorial
birds remained in the population. His data,
graphed in Fig. 18.2, showed very clearly how the
number of floaters, available to replace vacancies,
declined throughout winter, so that there remained
no surplus birds by the time the breeding seasons
began.
In stark contrast to these results, all removal
experiments involving great tits (none were done
with blue tits) resulted in rapid and often complete
replacement of the individuals removed. In the
Polish study, which was carried out in primeval
306 N O RT H A M E R I C A N A N D E U R A S I A N T I T S T U D I E S

Table 18.4 Results of removal experiments in Parids

Autumn/ winter removals

Ekman et al. 1981 Crested tit Removed birds partially replaced by birds from neighboring flocks,
suggesting no floaters
Hogstad 1989a Willow tit Birds removed in September all replaced by floaters
Hogstad 1989b Willow tit Birds removed in January not replaced
Hogstad 1990 Willow tit Replacement declined from 100% in Sept to 0 % from the end of December
onwards (see Fig. 18.2)
Ekman et al. 1981 Willow tit Fall removed birds more than replaced by known non-territorial individuals,
showing floaters
Alatalo et al. 1985 Willow, crested No (few) replacements
Alatalo et al. 1987 Coal tit No (few) replacements
Samson and Lewis 1979 Black-capped chickadee No September birds replaced
Smith 1987 Black-capped chickadee High-ranking winter removed birds replaced by floaters
Dolby and Grubb 1998 Carolina chickadee No (few) replacements
Samson and Lewis 1979 Tufted titmouse Some September birds replaced
Cimprich and Grubb 1994 Tufted titmouse No (few) replacements
Dolby and Grubb 1998 Tufted titmouse No (few) replacements
Spring removals
Cederholm and Ekman 1976 Willow tit, crested tit No replacements
Otter and Ratcliffe 1996 Black-capped chickadee Female movements between territories; no replacement by floaters
Krebs 1971, Krebs 1977 Great tit Rapid replacement; in 1977 study twice within 3 weeks
Wesolowski et al. 1987 Great tit Rapid replacement in natural habitat without nest boxes
Lambrechts and Dhondt 1988 Great tit Rapid replacement

100
80
% replaced

60
40
20 Figure 18.2 Seasonal variation in the percentage of willow tits
0 that were replaced after removal of single individuals from flocks at
different times during fall and winter. The results clearly show that
6 Oct

17 Oct

9 Nov

25 Nov

10 Dec

29 Dec

16 Jan

17 Feb

the number of non-territorial birds available to replace removed

birds decreases rapidly in late fall and early winter. (Data from
Date of removal Hogstad 1990.)

forest in which the breeding density was five to ten
times lower than in the other populations, the
authors still found evidence for territorial exclu-
sion. In one of Krebss (1977) experiments all birds
were replaced in two successive removals at the
onset of the breeding season.
Winter group territories with a clear dominance
hierarchy provide an interesting system to address
the generally important question concerning causes,
correlates, and effects of dominance, and the
cost/benefit analysis individuals must make when
deciding to join an existing group as a subordinate,
or to wander around as a floater until it becomes
possible to insert oneself at a higher dominance
level with a good chance to breed (Smith 1984). In
that context, very exiting work has been carried out
by Susan Smith and by Laurene Ratcliffes group at
Queens University (Chapters 1 and 9).
When comparing North American species with
Eurasian ones, one wonders why black-capped

chickadees, for example, live in larger winter flocks
than willow tits, their Eurasian counterparts, and to
what extent black-capped chickadees, in areas in
which winter feeding is extensive, would be winter
limited as I concluded above. Well-timed removal
experiments could provide an experimental answer
as to the effect of winter feeding on the size of
chickadee breeding populations (Brittingham and
Temple 1988).
18.5 Studies of hybrid zones
Studies of hybrid zones provide important insight
in evolutionary dynamics. Among Parids, many
hybrids have been described both among Eurasian
and among North American tits (Harrap and
Quinn 1995). Some hybrids have even been given
names because they were frequent, such as
the Pleskes tit, a hybrid between blue and azure
tits. Nevertheless, detailed studies of causes
and effects of hybridization and studies of hybrid
zones in titmice have been carried out primarily
among North American species (Chapter 7), deep-
ening our understanding of factors that contribute
to shifts in hybrid zones. In Eurasian studies, obser-
vations on hybrid pairs have remained mainly
anecdotal. In his review, Randler (2002) pointed
out that various mechanisms might be involved in
hybridization including one species being rare,
mistakes in mate recognition, and supernormal
stimuli resulting in females selecting the male of
the wrong species. Very elegant and probing North
American studies (Bronson et al. 2003a, b, 2005;
Chapter 7) have shown that this latter mechanism
(female choice) seems to drive hybridization
in the black-capped/Carolina chickadee system.
Equivalent studies in Europe involve primarily the
cavity-nesting Ficedula flycatchers (Alatalo et al.,
1994; Saetre et al. 1997).
It is interesting to underline that black-capped
chickadee females prefer the dominant male as a
partner, regardless of whether the male is a conspe-
cific or a Carolina chickadee. The strong attraction
of black-capped females for dominant males has
been shown in diverse ways by Ratcliffes group:
females prefer dominant males as extrapair part-
ners (Otter et al. 1998), will excavate their nest
closer to the territory boundary of a dominant male
N O RT H A M E R I C A N A N D E U R A S I A N T I T S T U D I E S 307
(Mennill et al. 2004), and will desert their own part-
ner if more dominant males are experimentally
widowed (Otter and Ratcliffe 1996).
A comparison of North-American and Eurasian
Parids suggests that hybridization is more frequent
when species have parapatric rather than when
they have sympatric distributions.
18.6 Conclusions
To a large extent differences in questions studied
among great and blue tit (largely studied in
Europe) on the one hand, and other Parids on the
other hand (largely studied in North America and
in northern Europe) are driven by the fact that
when entire populations breed at high densities in
artificial nest boxes it becomes much easier to
collect detailed information, especially on repro-
duction, on large number of pairs. Although any
study we carry out has the ambition to obtain
insights that are generally applicable, it has been
questioned to what extent this is true for all aspects
of studies on great and blue tit, and what they are
representative for.
Thus Wesolowski et al. (1987) found that in the only
study on great tits in a primeval forest in Europe,
birds defended territories of 3 to 5 ha rather than of
0.3 to 1 ha as found in western Europe in mostly
secondary or planted woodlands. Even in those low
density conditions, however, removal experiments
during nest building or egg laying showed that terri-
torial behavior still limits great tit breeding density,
implying that great tits are also summer limited in
native habitat. Tomialojc and Wesolowski (2004)
showed that in Bialowica forest bird species diversity
was larger, but overall bird breeding density lower
than in Western European woodlands, and suggested
that predation played a larger role there and limited
breeding density overall.
Mller (1989) made the point that most people
who study nest box populations remove old nests,
and that therefore nest box studies largely ignore
the role of nest parasites. Richners elegant experi-
ments have confirmed the important role of hen
fleas and documented dramatic effects on the birds
(Richner et al. 1993; Fitze et al. 2004). Mller was
thus correct in stating that by removing old nests
selection pressures are changed.
308 N O RT H A M E R I C A N A N D E U R A S I A N T I T S T U D I E S
Although numerous studies showed that nest-
box size, and the size and location of the nest box
and of its entrance hole, influences which species
use them (e.g. Wille 1967, Lhrl 1977), most pro-
fessional studies have used boxes with a single
entrance-hole size only, thereby favoring the great
tit. In a situation with variable entrance holes,
interspecific competition pressures may be relaxed
so that combining boxes with different entrance
hole sizes can have dramatic effects on the breeding
density of smaller species (Dhondt et al. 1991).
Thus although studying cavity nesters in natural
cavities (as in most studies in this book) entails high
costs, the benefit could be that they study the birds
in their natural environment in which they are
exposed to diverse selection pressures. Even with
these challenges, there exist a fair number of long-
term studies in North America (as described in this
book), but sample sizes are often problematic
because of the enormous effort required to find and
access nests, trap adults, or even band young.
Furthermore, because of the large territory sizes,
the probability to recapture Poecile juveniles after
dispersal is lower (Weise and Meyer 1979), so that it
is difficult to know which traits favor survival. In
great and blue tit, juvenile survival data are also
less than perfect, but enough data are available in
some studies to draw very strong inferences on
selection pressures (Garant et al. 2005; Postma et al.
2005).
References
Alatalo, R. V., Eriksson, D., Gustafsson, L., and Larsson, K.
(1987). Exploitation competition influences the use of
foraging sites by titsexperimental-evidence. Ecology,
68, 284290.
Alatalo, R. V., Gustafsson, L., Lindn, M., and Lundberg,
A. (1985). Interspecific competition and niche shifts in
tits and the goldcrestan experiment. Journal of Animal
Ecology, 54, 977984.
Alatalo, R. V., Gustafsson, L., and Lundberg, A. (1994).
Male coloration and species recognition in sympatric
flycatchers. Proceedings of The Royal Society, London Series
B-Biological Sciences, 256, 113118.
Blondel, J., Dias, P. C., Ferret, P., Maistre, M., and
Lambrechts, M. M. (1999). Selection-based biodiversity
at a small spatial scale in a low-dispersing insular bird.
Science, 285, 13991402.
Brittingham, M. C. and Temple, S. A. (1988). Impacts of
supplemental feeding on survival rates of black-capped
chickadees. Ecology, 69, 581589.
Bronson, C. L., Grubb, T. C., and Braun, M. J. (2003a). A
test of the endogenous and exogenous selection
hypotheses for the maintenance of a narrow avian
hybrid zone. Evolution, 57, 630637.
Bronson, C. L., Grubb, T. C., Sattler, G. D., and Braun, M. J.
(2003b). Mate preference: a possible causal mechanism
for a moving hybrid zone. Animal Behaviour, 65, 489500.
Bronson, C. L., Grubb, T. C., Sattler, G. D., and Braun, M. J.
(2005). Reproductive success across the black-capped
chickadee (Poecile atricapillus) and Carolina chickadee
(P. carolinensis) hybrid zone in Ohio. Auk, 122, 759772.
Cederholm, G. and Ekman, J. (1976). A removal experi-
ment on crested tit Parus cristatus and willow tit P.
montanus in the breeding season. Ornis Scandinavica, 7,
207213.
Christman, B. J. and Dhondt, A. A. (1997). Nest predation
in black-capped chickadees: How safe are cavity nests?
Auk, 114, 769773.
Cimprich, D. A. and Grubb, T. C. (1994). Consequences for
Carolina-chickadees of foraging with tufted-titmice in
winter. Ecology, 75, 16151625.
Dhondt, A. A., Adriaensen, F., Matthysen, E., and
Kempenaers, B. (1990). Non-adaptive clutch-sizes in
tits: evidence for the gene flow hypothesis. Nature,
London, 348, 723725.
Dhondt, A. A., Adriaensen, F., and Plompen, W. (1996).
Between- and within-population variation in mate
fidelity in the great tit. In: Black, J.M., ed. Partnerships in
Birds, pp. 235248. Oxford University Press, Oxford.
Dhondt, A. A., Kempenaers, B., and De Laet, J. (1991).
Protected winter roosting sites as a limiting resource
for blue tits. Acta XX Congressus Internationalis
Ornithologici, pp. 14361443.
Dolby, A. S. and Grubb, T. C. (1998). Benefits to satellite
members in mixed-species foraging groups: an experi-
mental analysis. Animal Behaviour, 56, 501509.
Ekman, J. (1989). Ecology of non-breeding social-systems
of Parus. Wilson Bulletin, 101, 263288.
Ekman, J., Cederholm, G., and Askenmo, C. (1981).
Spacing and survival in winter groups of willow tit
Parus montanus and crested tit P. cristatusa removal
study. Journal of Animal Ecology, 50, 19.
Fitze, P. S., Tschirren, B., and Richner, H. (2004). Life
history and fitness consequences of ectoparasites.
Journal of Animal Ecology, 73, 216226.
Garant, D., Kruuk, L. E. B., Wilkin, T. A., McCleery, R .H.,
and Sheldon, B. C. (2005). Evolution driven by differen-
tial dispersal within a wild bird population. Nature, 433,
6065.

Gill, F. B., Slikas, B., and Sheldon, F. H. (2005). Phylogeny
of titmice (Paridae): II. Species relationships based on
sequences of the mitochondrial cytochrome-b gene.
Auk, 122, 121143.
Harrap, S. and Quinn, D. (1995). Chickadees, Tits,
Nuthatches and Treecreepers. Princeton University Press,
Princeton, NJ.
Hogstad, O. (1989a). The role of juvenile willow tits,
Parus montanus, in the regulation of winter flock
size: an experimental study. Animal Behavior, 38,
920925.
Hogstad, O. (1989b). Subordination in mixed-age bird
flocksa removal study. Ibis, 131, 128134.
Hogstad, O. (1990). Winter floaters in willow tits Parus
montanusa matter of choice or making the best of a
bad situation? In: Blondel, J., et al.., eds. NATO ASI
Series, Vol. G 24, Population Biology of Passerine Birds, pp.
415421. Springer-Verlag, Berlin Heidelberg.
Kempenaers, B., Verheyen, G. R., and Dhondt, A. A.
(1997). Extrapair paternity in the blue tit (Parus
caeruleus): female choice, male characteristics and off-
spring quality. Behavioral Ecology, 8, 481492.
Kluijver, H. N. (1951). The Population Ecology of the
Great Tit, Parus m. major L. Ardea, 39, 1135.
Kluijver, H. N. (1971). Regulation of numbers in popula-
tions of great tits Parus m. major. In: Den Boer, J. and
Gradwell, G. R., eds. Proceedings of the Advanced Study
Institute on Dynamics of Numbers in Populations
Oosterbeek 1970, pp. 507531. Pudoc, Wageningen.
Krebs, J. R. (1971). Territory and breeding density in the
great tit Parus major L. Ecology, 52, 222.
Krebs, J. R. (1977). Song and territory in the great tits Parus
major. In: Stonehouse, B. and Perrins, C. M., eds.
Evolutionary Ecology, pp. 4362. University Park Press,
Baltimore.
Lack, D. (1954). The Natural Regulation of Animal Numbers.
Clarendon Press, Oxford.
Lack, D. (1966). Population Studies of Birds. Clarendon
Press, Oxford.
Lambrechts, M. and Dhondt, A. A. (1986). Male quality,
reproduction and survival in the great tit. Behavioural
Ecology and Sociobiology, 19, 5763.
Lambrechts, M. and Dhondt, A. A. (1988). Male quality
and territory quality in the great tit Parus major. Animal
Behaviour, 36, 596601.
Lhrl, H. (1966). Zur Biologie der Trauermeise (Parus
lugubris). Journal fur Ornithologie, 107, 167186.
Lhrl, H. (1977). Nistkologische und ethologische
Anpassungserscheinungen bei Hhlenbrtern. Die
Vogelwarte, 29, 92101.
Matthysen, E., Adriaensen, F., and Dhondt, A. A. (2001).
Local recruitment of great and blue tits (Parus major,
N O RT H A M E R I C A N A N D E U R A S I A N T I T S T U D I E S 309
P. caeruleus) in relation to study plot size and degree of
isolation. Ecography, 23, 3342.
McCleery, R. H. and Perrins, C. M. (1998) temperature
and egg-laying trends. Nature, 391, 3031.
McGregor, P. K., Krebs, J. R., and Perrins, C. M. (1981).
Song repertoires and lifetime reproductive success in
the great tit (Parus major). American Naturalist, 118,
149159.
Mennill, D. J., Ramsay, S. M., Boag, P. T., and Ratcliffe,
L. M. (2004). Patterns of extrapair mating in relation
to male dominance status and female nest placement
in black-capped chickadees. Behavioral Ecology, 15,
757765.
Mller, A. P. (1989). Parasites, predators and nest boxes
facts and artifacts in nest box studies of birds. Oikos, 56,
421423.
Nice, M. M. (1937 and 1943). Studies on the life history of
the song sparrow I and II. Transactions of the Linnean
Society of New York, 4 and 6, New York.
Otter, K. and Ratcliffe, L. (1996). Female initiated divorce
in a monogamous songbird: Abandoning mates for
males of higher quality. Proceedings of The Royal Society,
London Series B-Biological Sciences, 263, 351355.
Otter, K., Ratcliffe, L., Michaud, D., and Boag, P. T. (1998).
Do female black-capped chickadees prefer high-
ranking males as extra-pair partners? Behavioral Ecology
and Sociobiology, 43, 2536.
Perrins, C. M. (1990). Concluding remarks: dispersal and
gene flow. In: Blondel, J., et al., eds. NATO ASI Series,
Vol. G 24, Population Biology of Passerine Birds, pp.
475480. Springer-Verlag, Berlin, Heidelberg.
Postma, E. and van Noordwijk, A. J. (2005). Gene flow
maintains a large genetic difference in clutch size at a
small spatial scale. Nature, 433, 6568.
Randler, C. (2002). Avian hybridization, mixed pairing
and female choice. Animal Behaviour, 63, 103119.
Richner, H., Oppliger, A., and Christe, P. (1993). Effect of
an ectoparasite on reproduction in great tits. Journal of
Animal Ecology, 62, 703710.
Saetre, G. P., Kral, M., and Bures, S. (1997). Differential
species recognition abilities of males and females in a
flycatcher hybrid zone. Journal of Avian Biology, 28,
259263.
Saitou, T. (1978). Ecological study of social organization
in the great tit, Parus major L. I. Basic structure of
the winter flocks. Japanese Journal of Ecology, 28,
199214.
Samson, F. B. and Lewis, S. J. (1979). Experiments on
population regulation in two North American Parids.
Wilson Bulletin, 91, 222233.
Smith, S. M. (1984). Flock switching in chickadees: Why be
a winter floater? American Naturalist, 123, 8198.
310 N O RT H A M E R I C A N A N D E U R A S I A N T I T S T U D I E S
Smith, S. M. (1987). Responses of floaters to removal
experiments on wintering chickadees. Behavioral Ecology
and Sociobiology, 20, 363367.
Tomialojc, L. and Wesolowski, T. (2004). Diversity of the
Bialowieza Forest avifauna in space and time. Journal of
Ornithology, 145, 8192.
Wesolowski, T., Tomialojc, L., and Stawarczyk, T. (1987).
Why low numbers of Parus major in Bialowieza Forest
removal experiments. Acta Ornithologica, 23, 304316.
Visser, M. E., Adriaensen, F., van Balen, J. H., Blondel, J.,
Dhondt, A. A., van Dongen, S., du Feu, C., Ivankina,
E. V., Kerimov, A. B., de Laet, J., Matthysen, E.,
McCleery, R., Orell, M., and Thomson, D. L. (2003).
Variable responses to large-scale climate change in
European Parus populations. Proceedings of the Royal
Society, London, Series B-Biological Sciences, 270, 367372.
Visser, M. E., van Noordwijk, A. J., Tinbergen, J. M., and
Lessells, C. M. (1998). Warmer springs lead to mistimed
reproduction in great tits (Parus major). Proceedings of the
Royal Society, London Series B-Biological Sciences, 265,
18671870.
Weise, C. M. and Meyer, J. R. (1979). Juvenile dispersal
and development of site-fidelity in the black-capped
chickadee. Auk, 96, 4055.
Wille, H. (1967). Selectieve nestkasten in Belgi. Vogeljaar,
6, 435448.
 Index
Note: The terms Eurasian Parids and North American Parids have not been indexed as they appear throughout.
A note 168, 238
information and chick-a-dee
call:
basic note types 200
identity 205
signal redundancy 204
syntactical information
205, 206, 207, 208, 209
variability in note types 201, 202,
203
vocal production and perception
160, 161, 163
aberrant song 1034, 105
absolute pitch 155, 156, 157, 158
acoustic plasticity 193
adaptation, local 303
adaptive specialization hypothesis
26, 28
Africa 86, 87, 89, 238, 259, 294
age 2, 57, 134
photoperiodism and annual cycle
49, 51
postdispersal social environment
and acoustic variation in
birdsong 192
social dominance and fitness 141
alarm notes 211
Alaska 1, 75, 147
behavioral aspects of hybridization
106
caching, spatial memory and
hippocampus 278
corticosterone in chickadees 345
phylogeography of chestnut-
backed chickadee 78, 79, 80,
82, 83, 84, 85
winter adaptations and habitat
fragmentation 264, 265, 268
Alberta 11516, 139, 2456, 254, 294
AMPA receptors 17
AP5 17, 18
area parahippocampalis 17
Arizona 86, 106
Asia 87, 88, 89, 107, 238, 259, 294
aspen (Populus tremuloides) 229
azure tit (Parus cyanus) 86, 87,
106, 107
B note 161, 163, 171, 238
information and chick-a-dee call
200, 201, 202, 204, 205, 206, 207,
208, 209
Baeolophus vivii, ix, x, xi, 151
differences between North
American and Eurasian
studies 299, 305
information and the chick-a-dee
call 210
neurobiology of spatial behavior
9, 10
status signaling and
communication networks 229
Balkans 878, 89
banded wren (Thryothorus
pleurostictus) 222
bark beetle 120, 149
barrier effect 247, 252, 257
bee note 157
begging C 202
behavioral aspects of chickadee
hybridization 95108
behavior and genetics,
relationships between 1023
chick-a-dee calls across hybrid
zone 104
chick-a-dee calls beyond and within
hybrid zone 1012
confounding variables (potentially)
in vocal patterns analysis
1045
Eurasian Parids 1067
field methods 967
genetic composition of study
populations 989
genetic methods 97
hybrid index scores 978
Pennsylvania 103
song and call recordings 98
song patterns beyond and within
hybrid zone 99101
song patterns in Pennsylvania
contact zone 1034
songs and calls, lack of congruence
between 102
sound analysis 98
study sites 96
behavioral modifications 2669
Belgium 123, 252, 294, 300,
302, 303, 304
between song 193
between-bird diversity values
1889, 190
bilingual songs 2, 96, 100, 101, 103,
104, 105, 107
birch (Betula papyrifera) 229
black tit 238
black-capped chickadee (Poecile
attricapillus) vi, x, xi, 15, 71,
75, 1489, 1512, 238
behavioral aspects of hybridization
95, 103, 104, 105, 106, 107
background and methods
96, 97, 98
results 99, 100, 101, 102
caching, spatial memory and
hippocampus 26, 27, 28
corticosterone in Alaska and
Colorado chickadees 345
differences between North
American and Eurasian
studies 301, 305, 3067
dominance, corticosterone, spatial
memory and hippocampus 35
edge, patch and landscape effects
2445, 2478, 2512, 2549
female eavesdropping 2247
global perspective 294
habitat quality and reproductive
behavior 283, 284, 286
311
312 INDEX
black-capped chickadee (Cont.)
habitat selection at individual
level 296
information and the chick-a-dee
call 199200, 202, 20410
irruptive movements 295
male eavesdropping 2223
methodological advances 237
neurobiology of spatial behavior
1117
neurogenesis in hippocampus
1819
phylogeography 77, 78, 79, 85, 86,
89, 90
postdispersal social environment
and acoustic variation 183,
1856, 1902, 1945
reproduction 556, 58,
603, 65, 67
status signaling and communication
networks 215, 230
communication networks 222,
223, 227, 228, 229
context of singing 218, 219, 220,
221
fee-bee song 216, 217
unpredictable food, corticosterone,
spatial memory and
hippocampus 30, 31
vocal communication complexities
235
vocal production and perception
153, 154, 155, 156, 157, 15860,
161, 162, 164
winter adaptations and habitat
fragmentation 263, 264, 265,
268, 269, 270
see also demography; gargle call;
photoperiodism; social
dominance and fitness
black-crested titmouse (Baeolophus
atricristatus) x, 106, 107
black-lored tit (Parus xanthogenys)
238
blackbird (Turdus merula) 16, 219
blood parasites 59
blue tit (Cyanistes caeruleus) 4, 71, 149
behavioral aspects of hybridization
106, 107
caching, spatial memory and
hippocampus 26
comparison with great tit 282
demography, nest web
communities and changing
habitat 116
differences between North
American and Eurasian
studies 299305, 307, 308
edge, patch and landscape effects
245, 247, 24950, 252, 253, 259
in evergreen versus deciduous oak
forests 2802
habitat quality and reproductive
behavior 284
neurobiology of spatial behavior
9, 17
phylogeography 86, 87, 88, 90
postdispersal social environment
and acoustic variation 194
reproduction 55, 56, 61, 67
climatic variations 63, 64, 65
extrinsic factors 57, 58, 59
future effects on adult fitness
components 62, 63
offspring production and
recruitment 61
population adaptations to
habitat 60
social dominance and fitness 132,
136, 139
status signaling and
communication networks
219, 230
winter adaptations and habitat
fragmentation 267, 270
bokharensis group 86
boreal chickadee (Poecile hudsonica)
1, 106, 230, 238, 295
edge, patch and landscape effects
247, 251, 255
phylogeography 77, 78, 79, 83,
845, 86, 89, 90
breeding 2834
costs, future 623
density 300
territory 300
see also reproduction
bridled titmouse (Baeolophus
wollweberi) 16, 26, 106
British Columbia 1, 2, 76, 147, 149,
255, 294
demography, nest web
communities and changing
habitat 111, 112, 113,
116, 117
differences between North
American and Eurasian
studies 3045
habitat quality and reproductive
behavior 283, 284, 286
phylogeography 78, 79, 80, 81, 82,
83, 84, 85, 90
reproduction 58
broken dee note 202, 286
brood parasitism 288
brown creeper (Certhia americana)
79, 210
brown-capped chickadee vi, 75, 77,
106, 238
bushtit (Psaltriparus minimus) 79
bushy-tailed woodrat (Neotoma
cinerea) 115
C note 161, 163, 238
information and chick-a-dee call
210
basic note types 200
signal redundancy 204
syntactical information 205, 206,
207, 208, 209
variability in note types
201, 202, 203
caching 3, 325, 268, 299
interspecific differences 256
intraspecific differences 269
seasonality 29
see also food storing
California 78, 82, 83, 106, 112, 251,
255
calls 95
see also vocal production and
perception
Canada 60, 65, 75, 77, 78
see also specific places
Canary Islands 867, 88, 89, 90
canary (Serinus canaria) 179
cannabinoid receptors 18, 19
Cardueline finch 44
Carolina chickadee (Poecile
carolinensis) 1, 2, 4, 75,
148, 151
behavioral aspects of hybridization
95, 103, 104, 105, 107
background and methods 96, 97,
98
results 99, 100, 101, 102
caching, spatial memory and
hippocampus 29
call characteristics, sharing
of 174
differences between North
American and Eurasian
studies 307
dominance, corticosterone, spatial
memory and hippocampus 35
edge, patch and landscape effects
245, 251, 255, 256, 258
information and the chick-a-dee
call 199, 210
basic note types 200
identity 205

signal redundancy 204
syntactical information 206, 207,
208, 209
variability in note types 201, 202,
203
phylogeography 77, 85, 86,
87, 89
postdispersal social environment
and acoustic variation 194
reproduction 56
social dominance and fitness 139
status signaling and
communication networks 229
vocal production and perception
160, 161
winter adaptations and habitat
fragmentation 264, 267, 270,
271, 272, 273
caterpillars 2801
cavity:
characteristics 11820
excavation 299300
roosting 2689
and singing behavior 2279
cell proliferation 367, 38
chestnut-backed chickadee (Poecile
rufescens) 1, 75, 106, 1478,
230, 238
edge, patch and landscape effects
251, 255
see also phylogeography
chick note 202, 208, 209
chick-a-dee call 2, 4, 148, 151, 236, 238
behavioral aspects of hybridization
96, 98, 102, 105
call characteristics, sharing of 167,
168, 171
photoperiodism and annual
cycle 48
postdispersal social environment
and acoustic variation
186, 191
status signaling and
communication networks
215, 220, 222, 230
vocal communication complexities
235
vocal production and perception
15960, 161, 162, 163, 164
see also chick-a-dee call and
information
chick-a-dee call and information
199211
across hybrid zone 104
basic note types 200
beyond and within hybrid zone
1012
context 2078
identity 2045
note types, variability in 2004
playback studies 209
signal redundancy 204
syntax 2057
chick-a-fee-bee note 186
chip note 202, 208
cinereus group 86, 107
climatic variation 55
cyclical 634
directional 645
clutch size 556, 60, 303
coal tit (Periparus ater) 25
behavioral aspects of hybridization
106, 107
caching, spatial memory and
hippocampus 26
differences between North
American and Eurasian
studies 301
edge, patch and landscape effects
244, 245, 247, 249, 253
neurobiology of spatial behavior
11, 12
reproduction 59, 64
winter adaptations and habitat
fragmentation 267, 270
Colorado 278, 345, 115
see also Fort Collins
communication networks see status
signaling and communication
networks
condition 1356, 287
condition-dependent behaviors
2858
conformity 194
Connecticut 249, 251
conservation 4
context 2078
continuous assessment hypothesis
138, 139
Corsica 55, 59, 65, 2802, 3023
corticosterone 19, 2938, 73
Corvids 9, 16, 26, 236
crested tit (Lophophanes cristatus)
1, 9, 25, 62, 106, 123
edge, patch and landscape effects
244, 245, 247, 250, 252, 253
winter adaptations and habitat
fragmentation 267, 270
cross-fostering 107
Crossbill (Loxia species) 44
crow 236
Cyanistes ix, 1
cynomolgus monkey (Macaca
fascicularis) 13
INDEX 313
D note 160, 161, 163, 171, 238
behavioral aspects of hybridization
96, 98, 102, 104, 105
information and the chick-a-dee
call 200, 204, 205
syntactical information 205, 206,
207, 208, 209
variability in note types 201,
202, 203
dark-eyed junco (Junco hyemalis)
1314, 16, 17, 26
dawn chorus 2202, 2856, 288
deciduous downy oak (Quercus
pubescens) 2801, 282, 283, 284,
296, 303
dee call 2, 148, 202
demography of sympatric mountain
and
black-capped chickadees under
changing habitat condition
11128
excavation history, nest tree and
cavity characteristics 11820
facilitators 115
interspecific interactions 11516
nest web, Parids as members of
11115
population growth models 118
predators 115
site level changes using population
growth models 1208
study area and habitat change
11617
Denmark 229
density of species 270
dialects 195
disjunct populations in
chestnut-backed chickadee 90
dispersal 90, 2945, 303
diurnal countersinging interactions
21720
dominance hierarchy 358, 75, 296
call characteristics, sharing of 174,
179
habitat quality and reproductive
behavior 287
photoperiodism and annual cycle
456, 49, 51
reproduction 62
see also social dominance
Douglas-fir (Pseudotsuga menziesii)
112, 116, 119, 283
downy woodpecker (Picoides
pubescens) 111, 11315, 11823,
1267, 149
winter adaptations and habitat
fragmentation 271, 272, 273
314 INDEX
eastern bluebird (Sialia sialis) 56
eastern whipbird (Phsophodes
olivaceous) 215
ecological adaptations 2669
edges 2437, 271
avoidance 248
food abundance 244
habitat quality and reproductive
behavior 277
microclimate 2445
movement corridors 2457
predator avoidance 245
egg dumping 288
El Nio Southern Oscillation 63
energy limitation hypothesis 59
estradiol 51
Eurasian starling (Sturnus vulgaris)
59
European nightingale (Luscinia
megarhynchos) 216
European nuthatch (Sitta europaea)
270
European robin (Erithacus rubecula)
219
European starling (Sturnus vulgaris)
434, 48, 49, 115, 179, 183
evergreen holm oak (Quercus ilex)
2802, 284, 296, 303
excavation history 11820
faint fee-bee call 48, 221
fee-bee song 4, 151, 152, 236, 238
behavioral aspects of hybridization
96, 99, 100
call characteristics, sharing of 167,
168, 171
information and the chick-a-dee
call 199
photoperiodism and annual
cycle 48
postdispersal social environment
and acoustic variation 183,
186, 191, 194
social dominance and fitness 137
status signaling and
communication networks
220, 222
variation on two-note theme 21517
vocal communication complexities
235
vocal production and perception
153, 154, 155, 162, 164
fee-bee-bee call 99, 156
fee-bee-ee call 100
fee-fee-bee call 156
female eavesdropping in
black-capped chickadees 2247
finch see Cardueline; gray-crowned
rosy; house; zebra
Finland 106, 252, 253, 270, 3023
first fight hypothesis 137, 138, 139
first-order uncertainty 206
fitness see social dominance and
fitness
flycatcher (Ficedula) 307
food availability 567, 65, 66, 244
food solicitation calling 2867, 288
food storing 914, 723
cache sites, memory for 11
caches, memory for versus other
spatial locations 1112
seasonal changes 4950
spatial memory in versus
non-storing birds 1214
in the wild 911
food supply, fluctuating 2
food supply, unpredictable 2932
food/energy limitation 589
foraging behavior 268
forest:
mature 2834
patch size 24951
young 2834
fragmentation 27880
see also habitat fragmentation
France 55, 57, 5960, 645, 86, 88,
2801
frequency matching/shifting 217,
219, 220, 229
gargle call 4, 151, 236, 238
behavioral aspects of hybridization
96
information and the chick-a-dee
call 205
photoperiodism and annual cycle
48
postdispersal social environment
and acoustic variation 191
status signaling and
communication networks
215, 220, 221, 230
vocal communication complexities
235
vocal production and perception
155
see also gargle call of black-capped
chickadees; sub-gargle
gargle call of black-capped chickadees
16780
aviary experiments on gargle
changes 1756
combined analysis of interactive
playback tests 1778
contexts of use 1745
description of call 168
features of call and population
patterns 1714
persistence and change in calls
over time 173
year-to-year changes in
repertoires of individuals
1734
interactive playback experiment I
175
interactive playback experiment II
1767
ontogeny of call 16871
synthesis of theory and empirical
results 17880
genetics 57, 8890, 989, 1023
genotyping 80
geographic location of population 3
Germany 107, 282
glacial refugia 89
global distributions vivii
global perspective 2934
glucocorticoids 25, 33
glutamate 17
golden-crowned kinglet (Regulus
satrapa) 210
gonad development 44, 45, 47, 48, 49,
51, 57, 65
gonadotropin-releasing hormone
(GnRH) system 44, 45
gray jay (Perisoreus canadensis) 270
gray-crowned rosy finch (Leucosticte
tephrocotis) 162
grey-headed chickadee (see also
Siberian tit) x, xi, 25, 238
behavioral aspects of hybridization
106
phylogeography 77, 85, 86, 87
great horned owl (Bubo virginianus)
210
Great Marsh 967, 98, 99, 101, 103
Great Plains 194
great tit (Parus major) x, 71, 149, 237,
238
behavioral aspects of hybridization
106, 107
call characteristics, sharing of 179
comparison with blue tit 282
demography, nest web
communities and changing
habitat 116
differences between North
American and Eurasian
studies 299305, 307, 308
edge, patch and landscape effects
244, 250, 252, 253, 254

habitat quality and reproductive
behavior 280, 281
Japan 296
neurobiology of spatial behavior 9,
12, 16, 17
photoperiodism and annual cycle
43, 47
phylogeography 86, 88
postdispersal social environment
and acoustic variation 194,
195
reproduction 5562, 65, 67
social dominance and fitness 132,
135, 136, 139
status signaling and
communication networks 217,
219, 221, 223, 226, 229
vocal production and perception
164
winter adaptations and habitat
fragmentation 264, 267, 270
green alder (Almis crispa) 283
grey tit 238
Groundpecker (Parus humilis) 9
habitat:
fragmentation 3035
see also winter adaptations and
habitat fragmentation
management 4
quality and reproductive behavior
27789
fragmentation, matrix and halo
effects 27880
matrix: habitat of similar species
but dissimilar age 2828
matrix of similar age or structure
but dissimilar species
composition 2802
matrix, use of in conservation
planning 2889
selection at individual level 2956
hairy woodpecker (Picoides villosus)
83, 114, 118
halo effects 27880
Harris sparrow (Zonotrichia querula)
216
harsh dee note 202
hatching/fledging success 61
Hawk Mountain Sanctuary 967, 98,
99, 101, 103
hermit warbler 84
hierarchy formation and maintenance
1379
high zee note 168, 171
hippocampus 3, 9, 1419, 20, 328,
45, 71, 723
comparative studies 16
interspecific differences 256
intraspecific differences 269
neurogenesis in black-capped
chickadee 1819
seasonal changes 4950
spatial information, neural
processing of 1618
volume and seasonal variation
2930
house finch (Carpodacus mexicanus)
265
house sparrow 19
house wren (Troglodytes aedon) 270
HVC 18, 29, 45, 48, 49, 71
hybrid spruce (Picea glauca x Picea
engelmannii) 116, 119, 283
hybrid zones 307
hybridization 756
see also behavioral aspects of
chickadee hybridization
Iberian Peninsula 87, 89
Idaho 81
identity 2045
Illinois 251
immediate early genes 17
India 238
internal information 204
interpatch movement 2734
irruptions 294, 295
island populations and
chestnut-backed chickadee 90
Islands North see Fort Collins
Italy 86, 88
Japan 249, 250, 251, 296
Japanese chinquapin (Castanopsis
cuspidata) 11
Japanese quail (Coturnix japonica
japonica) 44, 265
Japanese tit 107
jay 16, 236
gray 270
ground 9
Stellers 83
juniper titmouse (Baeolophus ridgwayi)
x, 60, 106, 264, 266
Kentucky warbler (Opornis formosus)
216
kinglets (Regulus spp) 79
landscapes 248, 2527
lay-date 3023
laying, timing of 72
leader-follower patterns 2578
INDEX 315
lidocaine 17
lifetime reproductive success 132
lodgepole pine (Pinus contorta) 112,
116, 11922, 124, 149, 283, 304
long-tailed tit 248, 249, 252, 253, 256
long-term potentiation 15, 17
long-term studies 299, 3025
Lophophanes viii, 9, 299, 305
Louisiana 258
low fee-bee note 186
LRS 143
luteinizing hormone 65
Machlolophus ix
magpie 236
Maine 254, 258
mainland populations and
chestnut-backed chickadee 90
major group 86
male eavesdropping in black-capped
chickadees 2223
marsh tit (Poecile palustris) 11, 25
behavioral aspects of hybridization
106
caching, spatial memory and
hippocampus 26
dominance, corticosterone,
spatial memory and
hippocampus 35
edge, patch and landscape
effects 247, 248, 251, 252,
254, 256
information and the chick-a-dee
call 207
marsh tit (Cont.)
neurobiology of spatial behavior
11, 16, 17
photoperiodism and annual
cycle 47
reproduction 57, 60
social dominance and fitness 135
status signaling and
communication networks
229
Sweden 296
unpredictable food, corticosterone,
spatial memory and
hippocampus 31
Maryland 253, 254, 255, 258
Massachussetts 132, 194, 249, 251,
294
matrix 4, 27880
habitat of similar species but
dissimilar age 2828
of similar age or structure but
dissimilar species composition
2802
316 INDEX
matrix (Cont.)
use in conservation planning
2889
vulnerability index 2789
Melaniparus viiiix
metabolic adjustments, seasonal
2635
methodological advances 237
Mexican chickadee (Poecile gambeli)
1, 5
behavioral aspects of hybridization
106
caching, spatial memory and
hippocampus 26
information and the chick-a-dee
call 199, 202, 207, 208, 210
neurobiology of spatial
behavior 16
phylogeography 77, 86, 89, 90
status signaling and
communication networks 229
Mexico 86
Michigan 251
Michoacan 86
microclimate 2445
Minnesota 139
minor group 86
Missouri 96, 1034
mitochondrial DNA 77
mixed songs 105
mobbing calls 208, 209
mountain chickadee (Poecile sclateri)
2, 1489
behavioral aspects of hybridization
105, 106
caching, spatial memory and
hippocampus 29
corticosterone, food caching,
spatial memory and
hippocampus 32, 33, 34
dominance, corticosterone, spatial
memory and hippocampus 357
edge, patch and landscape
effects 255
information and the chick-a-dee
call 202, 204, 206, 208
neurobiology of spatial
behavior 17
phylogeography 77, 789, 86, 89
reproduction 56, 67
status signaling and
communication networks 229
unpredictable food, corticosterone,
spatial memory and
hippocampus 30, 31
winter adaptations and habitat
fragmentation 264, 266
see also demography of sympatric
mountain and black-capped
chickadees
mountain pine beetle (Dendroctonus
ponderosae) 76, 117, 1214,
1267, 3045
movement corridors 2457
natural history traits 299301
Nepal 106
nest density 1218
nest tree characteristics 11820
nesting 300
Netherlands 56, 57, 249, 250, 251, 253,
254
differences between North
American and Eurasian
studies 302, 303
reproduction 55, 61, 64
winter adaptations and habitat
fragmentation 270
neurogenesis 3, 2930
neuron number and seasonal
variation 2930
neuropeptide Y 17
neurophysiology 3
New Jersey 2445, 249, 251, 253, 254,
255, 268
New Mexico 115
New York 264
Newfoundland 86, 89, 90
nightingales 219
NMDA receptors 17, 18, 19
nocturnal hypothermia 2635
Nolde Forest 96105passim
nomenclatural distinctions viixi
normal song 215
North Atlantic Oscillation 55, 634
North Carolina 249, 251, 253, 254, 255
North Cascades 81
northern flicker (Colaptes auratus)
114, 118
northern flying squirrel (Glaucomys
sabrinus) 115
northern mockingbird (Mimus
polyglottos) 179, 236
northern pygmy owl (Glaucidium
gnoma) 210
Norway 211, 264
Nova Scotia 86
novel song 1945
novelty score 191
nutcracker (Nucifaga caryocatactes) 16
nuthatch 16, 115, 116, 266, 270,
299300
see also red-breasted;
white-breasted
oak forest 282
see also deciduous downy oak;
evergreen holm oak
oak titmouse (Baeolophus inornatus) x,
60, 106, 229
offspring food supply,
synchronization with 601
offspring production and recruitment
602
Ohio 245, 256, 270, 294
Oklahoma 253, 255
Ontario 14950, 294
edge, patch and landscape effects
251, 255
habitat quality and reproductive
behavior 288
photoperiodism and annual cycle
456
postdispersal social environment
and acoustic variation 1945
reproduction 58, 63
social dominance and fitness 132, 139
status signaling and
communication networks
216, 217, 229
Oregon 79, 80, 82, 83, 85, 255
over-wintering in heterospecific
flocks 2667
overlapping geographic distribution
230, 301
owl 210
pygmy 245
Palearctic Parids 86
paper birch (Betula papyrifera) 283
parahippocampalis 15
Pardaliparus viii
parental feeding effort 287
pair formation 46
parrot 236
Periparus amabilis 294
Periparus ater 10
Cyanistes caeruleus 10
Parus major affinis 86
Parus major weigoldicus 86
Poecile rufescens barlowi 79
Poecile neglectus 79
Poecile rufescens 79
Periparus venustulus 10
patches 2478, 24951, 2778, 279
penduline tit 211, 237, 238
Pennsylvania 1034, 148, 244, 258
Periparus viii, 9, 10, 299, 305
photoperiod 34, 301, 579,
65, 66, 72
photoperiodism and annual cycle of
black-capped chickadee 4352

reproduction 468
seasonal changes in food storing
4950
seasonal changes in song and
song-control system 489
seasonal neural plasticity 445
seasonal reproduction 44
seasonality 434
photorefractoriness 44, 45, 47, 48, 50,
51, 71
photosensitivity 44, 50, 65, 71
photostimulation 44, 47, 48, 50
phylogeography of chestnut-backed
chickadee 7791
Alaska 82
biogeography 789
comparison to other Parids 868
interior and coastal populations
812
origin 78
population genetics, factors
influencing 8890
private alleles 835
Queen Charlotte Islands 823
recolonization patterns 856
samples and genotyping 80
physiological adaptations
2636
physiology 3
pigeon (Columba livia) 13, 15, 265
pileated woodpecker 114
pine forest 117, 282
see also lodgepole pine
pine grosbeak (Pinicola enucleator)
83
pitch:
absolute 155, 156, 157, 158
ratio 157
relative 154, 155, 156, 157, 158
variation 230
pj call 211
place cells 15
Pleskes tit 307
plumage 4, 1367
Poecile vi, vii, viii, x, xi, 151
call characteristics, sharing of 180
differences between North
American and Eurasian
studies 299, 300, 305, 308
information and the chick-a-dee
call 199
neurobiology of spatial behavior
9, 10
phylogeography 77
status signaling and
communication networks
229, 230
vocal production and perception
153
see also black-capped;
brown-capped
Poland 3056
population adaptations to local
habitat 5960
population genetics, factors
influencing 8890
population growth models 118
and site level changes 1208
postdispersal social environment and
acoustic variation in birdsong
18395
ages of adults since 2004 191
bottleneck, effect of 18990
data analysis 1889
empirical results, synthesis of
1914
Fort Collins and Islands North
1901
model and hypothesis 1845
novel song and reproductive
fitness 1945
origin and maintenance of dialects
and repertoires 195
sampling procedure 1878
song development 194
study system 1857
variation across space and time
194
variation within juveniles 191
postglacial colonization and
chestnut-backed chickadee 89
postural signals 4
predator avoidance 245
private alleles 835, 86
proactive interference 13
proximate environmental cues 43, 46
Psittaciform 236
ptilochronology 267, 271, 273, 284
Puget Sound 183
pygmy owl (Glaucidiium passerinum)
245
quaking aspen (Populus tremuloides)
112
Quebec 246, 247, 255, 256, 294, 295
Queen Charlotte Islands 79, 81, 823,
85, 90, 147
RA 71
rank acquisition, variation in 13940
rasp call 175
rat 13
recolonization patterns and chestnut-
backed chickadee 856
INDEX 317
recruitment 612
red knot (Calidris canutus) 323
red squirrel (Tamiasciurus hudsonicus)
115, 120, 121, 122, 123, 127, 149
red-breasted nuthatch (Sitta
canadensis) 79, 11114, 11823,
1258, 149
red-naped sapsucker (Sphyrapicus
ruber) 11315, 118, 1214,
126, 149
relative pitch 154, 155, 156, 157, 158
Remizidae 211
removal experiments 3057
repertoires 170, 195
reproduction 5567
adult fitness components, future
effects on 623
behavior see habitat quality and
reproductive behavior
black-capped chickadee 468
climatic variation, cyclical 634
climatic variation, directional 645
extrinsic factors 579
fitness 1945
instrinsic factors 57
offspring production and
recruitment 602
population adaptations to local
habitat 5960
research, history of 567
success 1413
timing in males 656
Rhode Island 251
richness of species 270
Rocky Mountains 60
Russia 303
samples 80
San Juan Islands 90
Saskatchewan 251, 254, 255
seasonal changes 1819, 38
in food storing 4950
hippocampus 4950
in song and song-control system
489
seasonal metabolic adjustments
2635
seasonal neural plasticity 445
seasonal reproduction and
photoperiodims 44
seasonality 434
see also photoperiod; winter
second broods 303
see-bay-see call 99
see-bay-see-bay-see call 99
see-bee-see-bay call 96, 99, 100, 101
see-see-bay-bay-bay call 96, 101
318 INDEX

semi-Markovian model 206, 207
seniority 135
settlement 2834
sex 2, 135, 141
Shannon-Wiener species diversity
index 178, 188
sharp-shinned hawk (Accipiter
striatus) 285
shifted song 215
shivering 2656
si-t call 211
Siberia 106, 107
Siberian tit (Poecile cincta)
caching, spatial memory and
hippocampus 29
dominance, corticosterone,
spatial memory and
hippocampus 35
edge, patch and landscape
effects 253
neurobiology of spatial
behavior 11
reproduction 62
status signaling and
communication networks 230
winter adaptations and habitat
fragmentation 267, 268
Sierra Nevada 60, 127, 149
signal redundancy 204
singing see song
site level changes using population
growth models 1208
Sittiparus ix
size 1356
snow cover 271
social dominance 19, 38
winter 23
see also social dominance and
fitness in black-capped
chickadees
social dominance and fitness in
black-capped chickadees
13144
age 134
future research 1434
hierarchy formation and
maintenance 1379
plumage 1367
rank acquisition, variation in
13940
reproductive success 1413
seniority 135
sex 135
size and condition 1356
spring field methods 133
survival 1401
vocalizations 137
winter field methods 1323
soft dee note 202
somber tit (Parus lugubris) 300
song 300
aberrant 1034, 105
behavior and nest cavities 2279
and call, lack of congruence
between 102
and call recordings 98
control nuclei 712
control system 45
frequency, variations in during
countersinging interactions
21819
patterns beyond and within hybrid
zone 99101
patterns in Pennsylvania contact
zone 1034
photoperiodism and annual
cycle 49
and song-control system, seasonal
changes in 489
sparrow (Melospiza melodia)
85, 193
timing, variation in during
countersinging interactions
21920
types 95
versus call distinction and social
complexity 2367
see also postdispersal social
environment and acoustic
variation in birdsong; vocal
production and perception
sound analysis 98
South Carolina 249, 251, 253, 255
South Dakota 264
Spain 86, 88, 245, 248, 249, 250, 253,
254
sparrow 16
see also Harris; house;
white-crowned
spatial behavior, neurobiology of
920
food storing 914
hippocampus 1419
spatial memory 328
interspecific differences 256
seasonality 29
species biology 299
spitt notes 211
spring field methods 133
spring phenology 3023
spruce 112, 117
SR141716A 17
status signaling and communication
networks 21531
fee-bee song: variation on
two-note theme 21517
female eavesdropping in
black-capped chickadees
2247
male eavesdropping in
black-capped
chickadees 2223
nest cavities and singing behavior
2279
singing context 1: diurnal
countersinging interactions
21720
singing context 2: dawn chorus
2202
Stellers jay (Cyanocitta stelleri) 83
stress 3
stripe-breasted wren (Thryothorus
thoracicus) 215
sub-gargle 168, 169, 171
sub-Saharan Africa vi
sub-song 168
subalpine fir (Abies lasiocarpa) 283
substance P 17
suppression hypothesis 3, 138, 139
survivorship 62, 1401, 206, 207,
2701
Sweden 65, 2457, 24951, 2534,
267, 296, 305
Switzerland 58, 61
syntax 2057, 235
target of selection argument 200
taxonomic distinctions vivii
temperature 268, 269, 270
effects of on isolated woodlots
2713
and reproduction 58, 65, 66
Tennessee 206, 255
territoriality 287, 299
testosterone 51
Texas 106
thermogenesis by shivering 2656
three-toed woodpecker (Picoides
dorsalis) 114, 118
thrushes 16
Townsends warbler 84
tree swallow (Tachycineta bicolor) 56
trembling aspen (Populus tremuloides)
116, 119, 283
triangle fights 138
tropical antbirds 65
true calls 2
tufted titmouse (Baeolophus bicolor) x,
4, 5
behavioral aspects of hybridization
106
 INDEX 319

caching, spatial memory and warbler 16 winter adaptations and habitat

hippocampus 29 hermit 84 fragmentation 264, 265,
differences between North Kentucky 216 267, 268
American and Eurasian Townsends 84 wind:
studies 305 warbling song 230 effects on isolated woodlots 2713
dominance, corticosterone, spatial Washington 80, 83, 85 intensity 264
memory and hippocampus 35 whistled songs 2 speed 268, 269
edge, patch and landscape effects white spruce 116 winter:
244, 245, 249, 252, 253, 257, 258 white-breasted nuthatch (Sitta adaptations and habitat
information and the chick-a-dee carolinensis) 209, 258, 271, fragmentation 26374
call 209 272, 273 behavioral modifications and
postdispersal social environment white-crowned sparrow (Zonotryicha ecological adaptations 2669
and acoustic variation 194 leucophrys) 434, 183 effects on wintering permanent
status signaling and white-fronted tit (Parus semilarvatus) resident birds 2704
communication networks 229 294 physiological adaptations 2636
winter adaptations and habitat white-naped tit (Parus nuchalis) 294 responses to fragmentation
fragmentation 267, 268, 269, wild canary 49 26970
270, 271, 272 willow species (Salix spp.) 283 ecology 300
Turkestan 107 willow tit (Poecile montana) 25 field methods 1323
behavioral aspects of hybridization fitness 2
under-represented groups xi 106, 107 group territoriality 3057
United Kingdom 55, 56, 57, 601, caching, spatial memory and limitation 3057
294, 302, 303 hippocampus 29 social organization 300
edge, patch and landscape effects corticosterone, food caching, Wisconsin 255, 294
249, 250, 251, 253 spatial memory and within bird diversity measure 1889,
Utah 116, 264 hippocampus 32 190, 191
differences between North within song 193
Vancouver Island 90 American and Eurasian woodlot:
variable see note 48, 221 studies 301, 306, 307 connectivity 2734
varied tit (Poecile varius) 106 dominance, corticosterone, edge effect 270
Virginia 1034 spatial memory and isolated 2713
visual signals 45 hippocampus 35 size 2701
vocal communication 4 edge, patch and landscape effects woodpecker 116, 266
vocal patterns analysis, confounding 244, 245, 247, 250, 252, 254 pileated 114
variables (potentially) in 1045 habitat quality and reproductive see also downy; hairy; three-toed
vocal production and perception behavior 280 wren see banded; house;
15364 information and the chick-a-dee stripe-breasted
call perception 1613 call 202, 207, 208, 211 Wyoming 255
operant conditioning studies neurobiology of spatial behavior
1623 11 yellow tit (Parus holsti) 294
playback studies 1612 phylogeography 77, 85, 86, 88, 90 yellow-bellied tit (Periparus
call production 15961 postdispersal social environment venustulus) 106
song perception 1559 and acoustic variation 194
operant conditioning reproduction 65 zebra finch (Taeniopygia guttata) 15,
experiments 1579 social dominance and fitness 131, 59, 162, 193
playback experiments 1567 135, 139, 141 zero-order uncertainty 205, 206
song production 1535 status signaling and zi note 211
vocalizations 95, 137, 301 communication networks 229 Zipfs Law 206