Oikos 000: 000
000, 2008

doi: 10.1111/j.2008.0030-1299.16232.x,
# 2008 The Authors. Journal compilation # 2008 Oikos
Subject Editor: Kenneth Schmidt. Accepted 11 February 2008

Density-dependence by habitat heterogeneity: individual quality

versus territory quality

Javier Balbontı́n and Miguel Ferrer

J. Balbontı́n (jbalare@unex.es), Grupo de Investigación en Comportamiento Animal, Área de Zoologı́a (Biologı́a Animal), Facultad de Ciencias,
Univ. de Extremadura, Avda. de Elvas s/n., ES
06071 Badajoz, Spain.
M. Ferrer, Dept of Biodiversity Conservation, Estación Biológica de
Doñana, CSIC, Avd/ Marı́a Luisa, Pabellón del Perú, ES
41013 Seville, Spain.

The aim of this comment is to review the ecological issues concerning the role of individual and habitat heterogeneity as
possible mechanisms explaining density-dependent fecundity in animal populations. Our intention is to discuss different
approaches to determine whether or not studied populations are subjected to density-dependent processes and which
mechanisms are involved. We show that because individual quality (e.g. measured in terms of age of breeding individuals)
and territory quality can be correlated, untangling both effects on fecundity is frequently a difficult task. We discuss the
misuse of statistical methods and other problems related to the specific characteristics of the studied populations that can
have a strong influence on the conclusions reached by researchers working in this field.

In many populations, density affects reproductive or
survival rates (Sinclair 1989, Pulliam and Danielson
1991, Newton 1998, Both 2000, Rodenhouse et al.
2003). However, density-dependent effects are not uni-
versal, being found in some populations (Kluyver 1951,
Dhondt et al. 1992, Both 1998) but not in others (Atatalo
and Lundberg 1984, Török and Tóth 1988, Dhondt et al.
1992, Soutullo et al. 2006). When detected, negative
density-dependent fecundity is a population regulating
mechanism that operates by reducing the population
growth rate as density increases (Soutullo et al. 2006).
Multiple mechanisms can produce negative relationships
between population density and reproductive rates. Dhondt
et al. (1992) proposed that density-dependent fecundity
occurs because as density increases, breeding habitats are
occupied in a sequential order with respect to its suitability
(e.g. quality). If high quality territories are occupied first
and poor quality ones (those that yield lower than average
fecundity) later, average fecundity decreases as population
size increases (Brown 1969, Rosenzweig 1991, Sutherland
1996, Rodenhouse et al. 1997, Gill et al. 2001, Sutherland
and Norris 2002). In this situation, individual behavioural
decisions with respect to habitat selection and dispersal have
important consequences in the regulation of animal
populations (Fretwell and Lucas 1970, Lomnicki 1988,
Ferrer and Donázar 1996, Rodenhouse et al. 1997, Ferrer
et al. 2006). This particular mechanism has been named the
habitat heterogeneity hypothesis, also known as the buffer
effect (Brown 1969, Rosenzweig 1991, Dhondt et al. 1992,
Sutherland 1996, Gill et al. 2001, Sutherland and Norris
2002) or site-dependent population regulation (Roden-
house et al. 1997).
Increasing density could also lead to lower breeding
performance due to antagonistic encounters among indivi-
duals. Specifically, the interference hypothesis or the
individual adjustment hypothesis, proposes that as popula-
tion density increases, fecundity declines through an
increase in interference that in turn leads to a relatively
uniform decrease in site suitability (Dhondt and Schille-
mans 1983, Fernández et al. 1998, Newton 1998, Krüger
and Lindström 2001, Sillett et al. 2004).
In the last several years researchers have tried to discern
which density-dependent mechanism was best supported in
their own study system (Holmes et al. 1996, Ferrer and
Donázar 1996, Petit and Petit 1996, Fernández et al. 1998,
Krüger and Lindström 2001, Penteriani et al. 2003, Kokko
et al. 2004, Carrete et al. 2006a, 2006b). However, across
these studies researchers have applied different and incon-
sistent criteria to reach their conclusions. Thus, our
intention is to clarify criteria on this topic in order that
appropriate conclusions can be reached.
Recently, Carrete et al. (2006a) analyzed the effects of
intra- and inter-specific competition (e.g. density), indivi-
dual quality (e.g. age) and habitat heterogeneity on
fecundity using four eagle populations, two of Bonelli’s
eagles Hieraaetus fasciatus, and two of golden eagles Aquila
chrysaetos, from southeast Spain. Their main aims were to
test some predictions of the ‘habitat heterogeneity hypoth-
esis’ that provides one potential mechanism linking density-
dependence declines in fecundity. The authors of this study

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concluded that age, but not territory, affected breeding
success in both species. First, it is important to state that
whatever the mechanism in question, density-dependent
declines in fecundity can only be detected in either an
increasing or stable population (close to carrying capacity).
By definition, the habitat heterogeneity hypothesis or buffer
effects cannot otherwise be detected (Wyllie and Newton
1991, Dhondt et al. 1992, Begon et al. 1996, Ferrer and
Donázar 1996, Rodenhouse et al. 1997, Ferrer et al. 2006).
For example, this is violated in the case of some of the
populations analyzed by Carrete et al. (2006a), particularly
those which are referred to as ‘low density areas (LDA)’. In
this situation, no relationship between territory quality and
productivity would be found if low-quality territories are
avoided in a low-density situation (Ferrer and Donázar
1996, Rodenhouse et al. 1997, McPeek et al. 2001).
When trying to test the habitat heterogeneity hypothesis
or buffer effects, researchers should determine if, within an
increasing population, a negative relationship between
fecundity and population density exists. For this aim,
only the information about the change in population size
with time and measures of the annual fecundity distribution
(e.g. mean, variance or skewness) are needed (Ferrer and
Donázar 1996, Ferrer et al. 2006, 2008). However,
researchers typically use alternative information, such as
individual quality (e.g. measured in terms of age of breeding
pairs) or intra- or inter-specific interference (e.g. distance
between neighbouring conspecific pair, numbers of floaters,
etc.) to investigate their effects on fecundity with the aim of
trying to better understand the underlying process (Soutullo
et al. 2006, Carrete et al. 2006a, 2006b). In some of these
cases, relying on inconsistent or inappropriate criteria, it
might be hard to distuinguish whether or not their study
populations are subjected to density-dependent processes.
For instance, when trying to test the habitat hetero-
geneity hypothesis, one of its assumptions is that habitat is
heterogeneous, and hence in territorial species, territory
must have an effect on fecundity. In many situations,
individual quality (i.e. age of the bird) and territory quality
are correlated, with young birds often observed in poor
quality territories more frequently than expected by chance
alone (Newton 1991, Forslund and Pärt 1995, Ferrer and
Bisson 2003, Ferrer and Penteriani 2003, Penteriani et al.
2003, Espie et al. 2004, Ferrer et al. 2004). In these cases, it
is very difficult to accumulate sufficient samples to
statistically detect the independent contributions of age
and territory on fecundity. Hence, there is a high
probability of committing a type II error, because the
critical sample size required to detect an effect of age while
controlling for territory quality would be the number of
occurrences in which breeding pairs formed by individuals
of different age bred in the same territory in different years.
Frequently, the number of territories occupied by differ-
ently aged parents over the course of a study is small (Ferrer
and Bisson 2003, Penteriani et al. 2003). Therefore, we
encouraged those researchers working with average sample
sizes to perform power analyses on their data to evaluate
precisely the risk of committing a type II error. We have to
take into account that failure to adequately control for
breeding age can result in reaching incorrect conclusions.
For example, Carrete et al. (2006a) reported immature
birds breeding in some territories more frequently than
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expected by chance and concluded that differences in
fecundity among territories simply arose from variation in
parental age, not in territory quality per se. In this study
there was an attempt to disentangle the effects of age and
territory using a mixed model analysis in which territory
was included as a random effect and age and other
covariables were included as fixed effects. They concluded
that age, but not territory, affected breeding success. As
mentioned above, if individual quality (e.g. age) and
territory quality are correlated then the two effects should
be included as fixed effects in a multivariate approach in
order to determine the effect of one of them (e.g. territory)
while controlling for the effect of the other (e.g. age).
Because territory was included as a random term, this
approximation was statistically incorrect if the aim was to
separate the effects of age and territory on breeding success.
Therefore, the conclusion Carrete et al. (2006a) reached is
questionable and a re-analysis of their data will help to find
out if the conclusions still uphold.
In addition, an eagle’s age is an individual trait, whereas
difference in the probability of territory occupancy by
immature birds is arguably a territorial characteristic.
Hence, the differences in fecundity Carrete et al. (2006a)
detected may be a consequence of differences in territory
quality, specifically in differences amongst territories on the
replacement of breeding individuals amongst years. Regard-
less, we think the relevant question from a density-
dependence point of view is not why adult individuals
perform better than immature ones, but why immature
eagles appear more frequently than expected in certain
territories than others, usually in those with low-quality
features. Whatever the reason, the observed decrease in
mean fecundity in those populations subjected to a density-
dependent process is most probably due to the character-
istics of the territories themselves, independently of
the quality of their occupants. Furthermore, untangling
the contributions of territory and individual quality will
require multiple years of manipulative studies; at least on
those ones involving species without conservation concerns
(Rodenhouse et al. 2003).
Ferrer et al. (2006, 2008), proposed that in populations
subjected to an habitat heterogeneity regulation mechanism,
a negative correlation might arise between annual repro-
ductive rates (e.g. productivity) and variation (e.g. measured
as the coefficient of variation, CV) or skewness on annual
productivity, as population size increases. It should be
emphasized that age instead of density could also represent a
mechanism regulating population growth rates. Specifically,
an increase in the proportion of young breeders (those with
a lower than average fecundity) could explain a decline in
average fecundity at the population level as shown in birds
(Rodenhouse et al. 1999, Penteriani et al. 2003) and
mammals (Rödel et al. 2004). In these cases, the same
predictions formulated for the habitat heterogeneity hy-
pothesis, concerning the relationship between mean annual
fecundity and variation in annual fecundity or its skewness,
could be expected (Penteriani et al. 2003).
It has been also suggested that site-dependent variability
in adult survival instead of site-dependent variability in
reproductive performance, may be an important trait to be
seriously considered for the site-dependent population
regulation framework (Dhondt et al. 1992, Rodenhouse
et al. 1997, Sergio and Newton 2003). This is because
habitat heterogeneity could be explained by differences
among territories in (1) breeding performances or (2)
turnover rates, caused by either mortality or emigration
(Ferrer and Bisson 2003). In fact, most of the ‘‘classic
papers’’ on regulation by heterogeneity clearly establish the
importance of variation in turnover rates among territories
(Ferrer and Donázar 1996, Rodenhouse et al. 1997,
Balbontı́n et al. 2003, Penteriani et al. 2003, Ferrer et al.
2006). Not only could adult mortality affect the frequency
and duration of vacancies, but also different emigration
rates (Ferrer and Bisson 2003, Ferrer and Penteriani 2003,
Penteriani et al. 2003, Ferrer et al. 2004). Furthermore,
territories with high turnover rates could be less productive
not only due to the age of the breeders (under the
assumption that young birds produce less nestlings), but
also because in those species in which both members of the
pair are necessary for successful reproduction, the loss of
one member of the breeding pair during the breeding cycle
could result in reproduction failure (Ferrer and Penteriani
in press). Consequently, it is difficult to detect the
proximate causes generating a decrease in fecundity under
a density-dependent situation due to interacting factors
such as age of the components of the breeding pairs, the
quality of territories occupied by them and the variation in
survival rates they experienced under these circumstances.
In summary, our understanding of density-dependence
fecundity and the underlying mechanisms involved in this
process must consider multiple factors that may influence
breeding performance, e.g. territory and mate choice, or
territory and individual quality. Variability in these factors
also differs among territories and time and hence they are
difficult to control statistically in observational studies.
Therefore, in those studies with sufficient sample sizes,
statistical models should be correctly defined to confidently
test the hypotheses set a priori by the researchers of this
particular ecology area. Lastly, to disentangle the contribu-
tions of territory and individual quality will likely require
multi-year manipulative studies, at least on those systems
involving not endangered species on which researcher could
perform their experimental studies.
Acknowledgements
Thank you very much to K. Schmidt for their
valuable suggestions that helped improving this manuscript
throughout the reviewing process and also thanks to L. Svensson
for editorial assistance. JB was supported by the Spanish Ministry
of Education and Science through the post-doctoral program
‘‘Juan de la Cierva’’.
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