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This book will review evidence of versatile thinking by animals, and of

cqual significance will be a representative sampling of the wide range
of scientific and scholarly opinion about animal minds. This spectmm
of strongly advocated views demonstrates the basic importance attached
to the nature of animal mentality by both scientists and philosophers.
Cognitive ethology, the analysis of cognitive processes in nonhuman
:rnimals, has attracted thoughtful and constructive contributions from
ficlds as diverse as behavioral ecology and the philosophy of mind. This
has led to many significant discoveries about animal behavior and cog-
nition. M*y students of animal cognition avoid consideration of
r,vhether animal cognition is ever accompanied or influenced by con-
scious thinking. But because conscious awareness adds so much to an
runconscious "sleepwalker" existence, it is important to consider the evi-
tlcnce suggesting both cognitive processes and conscious thinking.
Contemporary human thinking about animal mentality falls into
three carnps, although none is a monolithic dogma and all include many
shades of opinion. The first, cornmonsense view is that animals are
likcly to think about what they are doing and the results they expect
liom their actions, especially when these are adapted to varying and
oftcn unpredictable circumstances. In stark contrast was the second po-
sition, that of the strict behaviorists, who used to argue that subjective
nrcntal experiences are inconsequential side effects that should be totally
ignorcd by serious scientists. They attempted to explain all behavior,
.rnirnal and human, exclusively in terms of external influences and how
tlrcsc aftbct overtly observable behavior.
llchrrviorism was thc dominant school of psychology for many years,
lrut tlrrring thc p:rst gcncrltion psychology has undergone a "cognitive
rt'r,oluti<ln" :ls nr<)st psychoklgists ltavc adopted a third, intermediate
'l'lrt't, ll;rvt' .rlr.rrrtl,rrrt'tl tlrt' tllxxls of strict behaviorism and
t orrsitlt'r' l lrt'rrrst'lvt's ( ( )l,.nrt r\'(' ps1't lrologists lrcc:tttsc tltcy rcc<lgnizc that

vlll Prefare Prefnce lx

internal processes within brains or minds are of the utmost importance in rurn provide us with a promising sourcc ol'otrjcctivc data about the
in determining the behavior of men and animals. These cognitive pro- mental experiences of nonhuman animals. Wc crrn rccord and analyze
cesses entail, among other attributes, representations, including memo- them; and we can learn from the responscs of rccil'rients a great deal
ries, expectancies, and anticipations. Internal manipulations of such about what messages they convey. Expcrimcntal prlayback of recorded
representations are held to result in decisions, and classification of ob- signals is often helpful in identifying what spccific information they
jects in relation to desires and beliefs. That is, animals want some things, convey. Iust as human speech, along with nonverbal communication,
fear others, and expect that actions will lead to certain results. tells us most of what we know about the thoughts and feelings of other
Yet cognitive psychologists are very suspicious of claims that animals people, so the scientific analysis of animal communication provides us
are consclous, even when they recognuze that cognition must be as- with a useful window on animal minds.
sumed in order to explain the animal's behavior. Because the vast major- Furthermore, animals often behave in such a versatile manner that it
ity of human brain functioning occurs without our conscious aware- seems much more likely than not that they experience simple conscious
ness, it is possible that all animal behavior is unconscious. Because thoughts about their activities, even when these are not expressed by
evidence for or against animal consciousness has been difficult to evalu- specific communicative signals that we can recognize. Analysis of be-
ate by scientific methods, the contemporary view of many cognitive havioral versatility can certainly lead to improved understanding of an-
psychologists can be summed up as: "Animal cognition: yes of course; imal cognition. This cognitive approach to animal behavior can also
but animal consciousness: unlikely, or, if it does occur, impossible to serve as constructive compensation for the unfornrnate tendency of
detect, since whatever the animal does might be done unconsciously." many scientists to belittle nonhuman animals by underestimating the
This intermediate position of contemporary cognitive psychologists complexity and the capabilities of the animals they study.
is a great advance, but the reluctance to move ahead from cognition to There is considerable overlap with my two earlier books on the sarne
consciousness may well be a lingering residue of behaviorism. M*y general subject (Griffin I98I, 1984) because many examples of animal
cling to the positivistic view that, in the words of Latto (1986, 309, behavior suggesting cognition or conscious thinking are as pertinent
313), "Conscious awareness in other animals is a closed world about today as they were ten or fifteen years ago. But a number of additions,
which we can do no more than speculate. . . . Sadly for those of us who corrections, and revised interpretations are now needed to take advan-
agree (that studying the subjective experiences of animals would be a tage of significant new ideas and critical formulations which have clari-
desirable goal), there is no evidence that it is anything but unattainable." fied many relevant issues. The renewed interest in animal cognition and
This antipathy to consideration of consciousness threatens to become a intelligence is abundantly demonstrated by numerous recent books
sort of self-inflicted paralysis of inquiry, an obsolete hindrance to scien- and articles, many of which will be discussed in the following chapters.
tific investigation. For no one seriously doubts that human conscious llut this interest has produced far more scholarly books and articles than
thinking is real and important) or that it sometimes influences our be- can be adequately reviewed in one volume. I have therefore selected
havior. Why then is it out of the question to learn whether nonhuman primarily the more recent publications, especially those with appro-
animals think consciouslyf The usual answer to this question is that 1'rriate bibliographies.
other people can tell what they are thinking or feeling, but no such evi- I have been pleasantly surprised to find how enlightening it is to re-
dence is available about any conscious thoughts that might conceivably vicw the extensive published literature on animal behavior from this
be experienced by animals. cognitive perspective. As even two of the most severe critics of this ap-
Insofar as animals do experience conscious thoughts, it must often lrroach have recognrzed, "the development of cognitive ethology has
be important to convey them to companions, rivals, or even members hclpccl emphasize that animals routinely engage in behavior more com-
of other species. Charles Darwin and many other students of animal plcx than most cthologists or psychologists would have thought plau-
behavior have interpreted animal communication as expression of emo- sitrlc" (Y<rcrg anrl Krurril I 99 I ). Thus wc can at least hope to learn just
tions, but ethologists have recently discovered that some animals ex- Irow vcrs:rtilc rrnirtr:rls .tt'trr.tllt, .u'c lry c<lrtsiclcring what is known of their
press both feelings and simple thoughts. These communicative signals bch.rvior li'orrr u'lr.rt s('('nls likt'lv to lrc thcir ()wn pcrspectives (Griffin

1990, l99I). A.rd, furthermore, I expect that we will find it more and CHAPTER ONE
more plausible that animals are sometimes consciously aware of their
situation and of the likely results of their activities.
I am glad to acknowledge permission by the following authors and
publishers to quote from their publications: J. Diamond, md Macmil-
lan Magazines Ltd., Nature 297 (L982): 99-lO2; K. I. Friedmann for
Anirnnl Menta,lity
H. Friedmann, and Smithsonian Institution Press, U. S. National Mw-
seurn Bwlletin 208 (1955): 32-59; L. M. F{erman, and )ohn Wiley &
Sons, Inc., Cetacean behavior (1980), 402,406; A. I. Meyerriecks, and
the Nuttall Ornithological Club, Com.paratite breeding bebnvior of four
species of North Arnerican l'terons (1960), 8, 9, 89, 108-9; C. A. Munn,
and State University of New York Press, Deception in anirnals (1986), ental experiences are real and important to us, and in-
Va;|. R. Searle, and Cambridge University Press, Synthese 61 (1984): sofar as they occur in nonhuman animals they must be important to
14-15, andBeharioral nnd.Brain Sciences 13 (f 990): 585. them as well. They are certainly important to our appreciation of ani-
I am especially grateful to several colleagues who have allowed me to mals, for we can only understand other species fully when we know
draw on their recent work, including material not yet published or in what, if anything, they think and feel. It is therefore important for those
press. These include G. M. Burghardt, I. A. Fisher, B. Heinrich, H. E. interested in animals to learn as much as possible about whatever
Hodgdon, A. C. Kamil, P. Marler, T Natsoulas, I. M. Pepperberg, K. thoughts and feelings they experience. Unfornrnately, almost all of the
Pryor, C. A. Ristau, D. G. Reid, H. Ryden, P. Stander, and E. A. Was- scientists who study animal behavior avoid this subject; and many deny
serman. The recent symposia arranged and edited by C.A. Ristau the existence or the significance of animal consciousness. Because it is
(199t) and by M. Bekoffand D. )amieson (1990) have been most stim- so difficult to prove rigorously whether any given animal is conscious,
ulating and helpful. The detailed criticisms by three anonymous review- no maffer how ingenious its behavior, scientists have tended to cling to
ers of this manuscript have led to further clarifications and improve- the conservative assumption that all animal behavror $ anconscrous.
ments; and while not agreeing with all their recolrlrnendations, I am But recent discoveries about animal behavior have rendered this ten-
glad to acknowledge the beneficial results of their thoughtful efficrts. denry to minimizethe implications of animal versatility more and more
Finally, I wish to express my appreciation of the constructive editorial difiicult to maintain. The dilemma faced by the conservative "nothing
efforts of Susan Abrams and her colleagues at the University of Chicago but" position prefcrred by many scientists is illustrated by two ex-
Prcss. amples.
A hungry chimpanzee walking through his native rain forest in the
Ivory Coast, comes upon a large Pand,a oleosn nut lying on the ground
under one of the widely scattered Panda trees. He knows that these nuts
are much too hard to open with his hands or teeth, and that although
hc can use pieces of wood or relatively soft rocks to batter open the
more abundant Cowla edwlis nuts, these tough Panda nuts can only be
crackcd bv pounding them with a very hard piece of rock. Very few
st()ncs are availablc in the'rain forest, but he walks for about 80 meters
straight to anothcr trcc whcrc several days ago he had cracked open a
l)rurth nut with rr lrrrgc chtrnk of granitc. He carries this rock back to the
rrrrt hc hes jtrst lirrrntl. pl:rtt's it in:r crotch bctween rwo buttress roots,
.urtl t'r':rt'ks it olrt'rr u'itlr.r lctv u't'll ;tintt'tl blows. (Thc loud noises of
t'lrirrrP:urz,ct's t'r'.ltkrnl', nlrt\ \\'rtlr r,r, ks lr.rrl lt'tl t':rrly I')ttr<lPcatr explorers

2 Chapter One
Animal Mentality 3

to suspect that some unknown native tribe was forging metal tools in intruder's behavior. A parrot uses imitations of spokcn English words
the depths of the rain forest.)
to ask for things he wants to play with and t() answcr simple questions
such as whether two objects are the same or dillbrcnt, or whether they
In a city park in Irp.r, a hungry green-backed heron picks up a rwig,
differ in shape or color. Even certain insects, specifically the honeybees,
breaks it intb small piices, and cirries one of these to the edge of pond,

where she drops it into the water. At first it drifts away, but she picks it employ symbolic gestures to corilnunicate the direction and distance
up and bringsit back. She watches the floating twig intently until small their sisters must fly to reach food or other things that are important to
a.rapid thrusting the colony.
-inno*, r.ii- up to it, and she then seizes one by
gob with her tong sharp bitl. Another _green-backed heron from the These are only a few of the more striking examples of versatile behav-
I*. colony carrief bits of material to a branch extending out over the ior on the part of animals that will be discussed in the following pages.
pond and tosses the bait into the water below. When minnows approach
Although these are not routine everyday occurrences, the fact that ani-
mals are capable of such versatility has led to a subtle shift on the part of
thir brit, he flies down and seizes one on the wing'
scientists concerned with animal behavior from assertions that animals
Must we reject, or repress, ffiy suggestion thlt the chimpanzee or the
do not think at all to the view that their thoughts are very different from
heron thinks consciousiy about-the tisty food it manages- to obtain by
these coord,inated actions| Many animals adapt their behavior to
the ours. For example, Terrace (1987,135) closes a discussion of "thoughts
challenges they face either under natural conditions or in laboratory ex- without words" as follows: "Now that there are strong grounds to dis-
p.rim.its. This has persuaded many scientists that some sort of cogni- pute Descartes' contention that animals lack the ability to think, we
have to ask just how animals d.o think:' Because so many cognitive pro-
iio., -ort be required to orchestrate such versatile behavior. For ex-
cesses are now believed to occur in animal brains, it is more and more
*p1., in other pr.rc of Africa chimp-anzees.select suitable branches
fro- which they break offtwigs to p.odrr.e a slender probe, which they difficult to cling to the conviction that none of this cognition is ever
accompanied by conscious thoughts. The aim of this book is to reopen
.rrry some distance to poke ii into a termite nest and eat the termites
clinging to it as it is withdrawn. Apes.hav. ,lto learned to use artificial the basic question of what lifc is like, subjectively, to nonhuman ani-
mals, and to outline how we can begin to answer this challenging ques-
cor#nrinication systems to ask for objects and-activities they want and
ro answer simple quesdons about pictures of familiar things. vervet tion by analyzing the versatility of animal behavior, especially the com-
*rrk.y, employ diiferent alarm calli to inform their companions about municative signals by which animals sometimes appear to express their
particular tyPes of Predator. thoughts and feelings.
Such ingenuity is not limited to primates. Lionesses sometlmes co- M*y scientists feel that terms such as mind or consciousness are too
vague and slippery to be useful in scientific investigation; and they often
operare in iurrounding prey or drive prey toward.a comganion waiting
argue that these and other words describing subjective mental experi-
in a.on.ealed position.^Captive beaver have modified their customary
cnces cannot be defined with sufficient precision to allow objective test-
p"*..rrs of lodge and dam building behaviorby piling material around
vertical pole i't the top of which was located food that they could not ing of the presence or absence of whatever they designate. I will discuss
otherwise reach. They are also very ingenious at pl_uggilg water leaks, definitions in greater detail later in this chapter and in chapter 12, but it
is helpful to emphasize at the outset that the most basic and essential
somerimes cutting piices of wood io fiia particular hole throughwhich
aspect of consciousness is thinking about objects and events. The con-
water is escapinglUt d.. natural conditions, in late winter some beaver
cut holes ir thE dams they have previously constmcted, causing the tcnt of conscious experience may ordinarily be limited to what the ani-
mal perceives at the moment about its immediate situation; but some-
water level to drop, which allows them to swim about under the
tinrcs its awareness probably includes memories of past perceptions, or
without holding their breath.
rurticil'xrtions of firturc cvcnts. An animal's understanding may be accu-
Nor is apprJpriate adaptation of complex-behavior to changing cir-
cunstanc., , *^.*aliarmonopoly. Bowerbirds construct and deco- riltc ()r rnislcarlirrg, :urtl tltc cotttclrt of its thoughts may be simple or
out conrplcx. A corrst'ir)us ()r'll:lnisrtt tttrr.st ordinarily experience some feel-
rate bowers that help them affract females for mating._Plovers carry
injury-simulating distraction displays that lead predators ly"y from irrg :r[x)ul u/l).lt('\'('r ('n11.r1,.r's its .lll('ntirxt. Artilnll fc'clings, and espe-
thcir'cggs ()r y.ii,,.,g, ancl thcy ..tj.itt thcsc displays according to the t'i:rllt';tttitn:tl srrlli'r'rlr1,,,.tt('t('(,,1',tttz,t'tl lr1'lttosl sciclttists.ls rcal and
4 Chapter One

significant (Bekoffand |amieson 1990,1991; Dawkins 1990). Further- animals and men result entirely from cvc.ts ,r^r::::'r::n*.:
more, any thinking animal is likely to guide its behavior at least partly nervous systems. In other words, I will()pcratc orr thc basis of emergent
on the basis of the content of its thoughts however simple or limited materialism as defined by Bunge (1980, 6)., and assume that there are
such thoughts may be. Animals obtain most of the information that no immaterial, vitalistic, or supernatural proccsscs involved in the small
affects their behavior through their sense organs, including those that fraction of human or animal brain events that rcsult in conscious, sub-
signal conditions within their bodies. But some mental experiences are jective thoughts and feelings. This approach differs from that of Sperry
probably based on past sensory input; and some may arise through re- (1983), who appears to take the essentially dualistic position that con-
combination into new patterns of information already present in the sclousness is something different in kind from the physical world. But
central nervous system. otherwise his thoughtful and idealistic analyses are quite consistent with
One reason to suspect that nonhrunan urimals do experience con- the view that consciousness exerts a causal influence on brain function
scious thoughts is that the basic stmcture and functioning of neurons and behavior, and is not limited to our species. Because our own con-
and synapses are quite similar, as far as we kno*, in all animals with sciousness and thinking occur in an enormous variety of forms, these
organized central neryous systems. There is no convincing evidence that terms suggest different meanings to various people. Animal thinking
specific features of gross neuroanatomy are essential for conscious and feeling may also be much more varied and subtle than anything I
thinking. Therefore it is best to keep an open mind about the possibility will discuss in the following pages; but in trying ro ascerrain whether
of consciousness in all animals that exhibit versatile behavior or com- animals experience any conscious thoughts at all, it is helpful to concen-
municate in ways that suggest they may be expressing thoughts or feel- trate on simple and basic sorts of conscious thinking that are the least
ings. We are consciously aware of only a small fraction of what goes on difficult to detect.
in our brains, and there is no reason to suppose that this fraction will Recognizing our ignorance is a necessary first step toward reducing
prove to be larger in other species. The fact that we are unaware of it. The customary view of animals as always living in a state comparable
so much that occurs in our brains has led many scientists to neglect to that ofhuman sleepwalkers is a sorr of negativJdog*rtism. We know
consciousness because it is held to be an epiphenomenon or trivial by- far too little to judge with any confidence when animals are or are not
product of neural functioning (Velrnans t99l). But the component of conscious, ffid it is just as difficult to disprove as ro prove that a partic-
central nervous system activity of which we are conscious is of special ular animal is thinking consciously. Thus the question of animal con-
significance because it is what makes life real and important to us; and sciousness is an open one, awaiting adequate scientific illumination.
insofar as other species are conscious, the same importance may well be Many behavioral scientists dismiss this effort as idle speculation; but
manifest. Animals may carry out much, or even perhaps all, of their speculation is where scientific investigation begins, and I hope to srim-
behavior quite unconsciously, but insofar as they are conscious, their ulate new and enterprising inquiries that will significandy reduce our
consciousness is an important attribute. current ignorance and aversion. Regardless of the degree to which it
Whatever thoughts and feelings nonhuman animals experience may nray come to seem more or less probable that various animals experience
be quite different from ours) and presumably much simpler; but this particular conscious thoughts and subjective feelings, this approach
does not mean that they are insignificant. There is of course no reason should open up significant but largely neglected opporrunities to attain
to suppose that other animals are capable of the enormous variety of rr fuller and more accurate understanding of the other creatures with
thinking that our species has developed, largely through the use of our which we share this planet.
magnificent language-especially written language that allows the dis- There is little new about the basic question of what the menral expe-
semination and preservation of knowledge far beyond what can be ricnccs of animals may be ; that question was articulated and debated by
achieved by direct communication and individual memories. Animal Darwin, Romancs, l,loycl Morp5an, von Uexkull, and many other scien-
thoughts probably concern matters of immediate importance to the an- ti.sts of thc ninctccnth :rntl carly twcntieth centuries who were deeply
imals themselves, rather than types of thinking that are primarily rele- itrtcrcstctl irt rtrtirtr:rl nrt'rrl.rlit\,. 'l'lrt' historv of thc debate has been thor-
vant to human concerns. <rtrglrll' r't'r.'it'lvctl lrv nr.rrrv sr rcnrrrr*, irr.'lrrr.lirrg Schrrkz (1g75).Wasser-
I will take it for grantcd that behavior and consciousness in both rtt:ur (l()tll) lio:rkt's 1lt)tl'l;, l)r'rvsl'rn\, (l()ll4), I(it'lrlrcls (1987), and
6 Cbapter One

especially by Burghardt (1985a, 1985b). Indeed the nature of animal thinking; and scientific journals sometinrcs rclirs , ,r'r,;:::;K ,l-,
minds was a major subject of investigation and discussion uP to the
terpretations that support the infcrencc <>f rrrrirrr:rl consciousness (Searle
I920s and I930s, when it was repressed by behaviorism's restriction of I990b; Whiten and Byrne 1988).
scientific affention to overtly observable behavior, as discussed later in Some exceptions to this taboo against consiclcring mental experi-
this chapter. What ei new is the accumulated results of half a cenrury of ences of nonhuman animals have begun to appcar in recent years-for
active and trrc.essful investigation of animal behavior. This has now instance, Crook (1980, 1983, 1987,I988), Dcnron (1982), Barkow
provided a wealth of data about the complexities and versatility of ani- (1983), Staddon (1983), Burghardt (1985b, l99l), Oakley (1985),
mal behavior under natural conditions, and what they can learn to do in Knapp and Robertson (1986), Cheney and Seyfarrh (1990a), and
the laboratory. We can therefore return to the investigation of animal some) but by no means all, of the contributors to symposia edited by
minds with far better and more extensive factual evidence than what was Weiskrantz (1985, 1988). The neurophysiologist Eccles (1989) is per-
available to nineteenth-century biologists. suaded that at least simple mental experiences occur in birds and mam-
Comparative psychologists, ethologists, and behavioral ecologists mals, but not in insects. An importanr parallel development has been
have come to call themselves behavioral scientists, both because they what is often called the "cognitive revolurion" in psychology, by which
study behavior, and because they avoid. considering subjective mental the strict behaviorism advocated by B. F. Skinner has been largely re-
experiences. Therefore, most of the scientists who study animal behav- placed by concern with cognitive processes, that is, internal representa-
ioi have had little or nothing to say about the fcelings or thoughts of tions in the brain and how their interactions affect overt behavior, as
the animals thar interest them so keenly; and in their writing one almost discussed in more detail in chapter 6.
never finds any use of terms such as "thinki'"intend," "believe," and the The history of this cognitive revolution in psychology has been
like. Thus Colgan (1989) and Yoerg (199I) speak for many of their abundantly reviewed by Baars (1986, 1988), Gardner (1985), Miller
colleagues in adamantly eschewing any scientific concern with the men- (1988), and Riley, Brown, and Yoerg (1986), among others. An excel-
tal ex[eriences of animals. A primary reason for this avoidance of the lent perspective on contemporary thinking and controversies is pre-
subjeit is a belief that mental experiences) especially those of animals, sented in the book edited by Blakemore and Greenfield (1987). Numer-
are inaccessible to scientific investigation because they are private to the ous review articles, symposium volumes, and substantial books have
organism experiencing them. Hence it is claimed that no statement been devoted to the cognitive psychology that has largely replaced be-
about them Can be verified by others. But we do of course obtain useful haviorism-for instance, Anderson (1983), |ohnson-Laird (1983,
if incomplete and somewhat distorted information about other people's 1987, 1988), K."pp and Robertson (1986), Marcel and Bisiach
thoughti and feelings by making inferences from their behavior, and (1988), Newell (1990), and Whiten (I99I). Even Pavlovian condition-
cspeclaily their communicative behavior. Furthermore, the difficulty, or ing turns out to be much more complex than we used to take for
cven the impossibility, of conveying to others the exact nature of some- granted and to entail learning of relationships rather than simple linking
thing does not rule it out of existence or deprive it of significance' M*y of specific stimuli with specific responses (Rescorla 1988; Gallistel
thin[s have been profitably analyzed by scientists long before their na- ree0).
rure could be defined in complete detail. It can be questioned whether Analogies to computer systems have been central to this develop-
any important scientific entity can be described with I00 Percent coq- ment) and a major reason for abandoning the inhibitions of behavior-
pleteness. ism has been the ability of computer systems to perform many men-
^ tal operations that used to requr,ire human thinking, as discussed in
The taboo against considering subjective mental experiences of non-
human animals has become a serious impediment to scientific investi- dctail by Shallice (1978, 1988a, 1988b), among orhers. Since these
gation. Effective indoctrination-often accomplished by nonverbal sig- inforrlati()n-pr()ccssing clcviccs can do so much, the overwhelrning
rrrtr of disapproval-inhibits students and young scientists from tclnl'rtati<>tt hls bccn t<l rlssunlc that human and animal brains and minds
venturing into this forbidden territory, and those that do so encounter tllurit <lPcrlttc irr sintilrrr' \\':11,q. As srrnrrnrrrizccl by Riley, Brown, and
criticismlnd ridicule. One result is that students of animal behavior are Yocrg (l9tl(1, ll5), "tltt' t"ist'ol'tltt'('()nll)utcr :ls :l n)ctAphor has pro-
inhibited from reporting versatile behavior that suggests conscious t'itlt'tl :t l'itlt s()rn(('ol itk'.ts l,t lt,rr .,,11ttitivt's1,.11'11rs rrriglrt<lpcrate. If
B Chapter One Animal Mentality 9

such ideas are compatible with phenomenology, so much the better. . . . Krebs and Dawkins (1984) have disctrsscrl anirnal communication
Cognitive psychologists . . . are rnetbod.ological behaviorists." (Method- from an evolutionary perspective emphasizing its flnction in (a) per-
ological behaviorism is the reliance on observations of behavior as data mitting one animal to manipulate others t<> its r>wn advantage, and
about internal mental states and processes without following the strict (b) what they call mind-reading. By "mind-rcacling" they mean predic-
behaviorists in denying their existence or importance.) M*y cognitive tion of one animal's behavior by another on thc basis of the former's
psychologists are thus persuaded that, in the words of ]ohnson-Laird behavior, especially its communicative behavior. They emphasize the
(1988, 367), "the computer is the last metaphor for the mind." evolutionary advantages of manipulation and mind-reading by social
But this cognitive revolution in psychology has largely ignored the companions and by both predators and prey. They avoid committing
question which, if any, of the cognitive processes that are now freely themselves "to a view over the philosophical problems of animal mind
postulated to occur in the brains of men and animals are accompanied in the subjective sense." But they state that many ethologists have con-
by conscious awareness. A recent exception to this tendency is Baars cluded that "animals respond in mechanical robot-like fashion to key
(1988, 356), who writes at the conclusion of a chapter on the functions stimuli," and they contend that "we should not ask whether the stickle-
of consciousness: "Consciousness is special; but its wonderful qualities back 'thinks'the (red) mail van is a rival." (This refers to the well-known
are not isolated from other realities; nor is biological usefulness a special observation by Tinbergen that red-bellied male sticklebacks when
virnre. C,onsciousness is the vehicle of our individuality, something that highly motivated to court females display aggressively towards very
makes it of inestimable significance to us." I will return to this topic later crude models of other males provided they have a red color.) Yet Krebs
in this chapter, and in more detail in chapters 6 and 12; but first it is and Dawkins refer to animals as willing or unwilling participants in
necessary to consider some basic problems that have deterred many be- rnind-reading interactions. In a similar vein Guilford and M. S.
havioral scientists from seriously considering animal consciousness. Dawkins (199I) discuss the psychology of animals receiving and react-
M*y srudents of animal behavior are now quite willing to apply the ing to communicative signals but avoid mentioning any subjective men-
terms "cognition" or "cognitive" to a wide variety of animals that per- tal experiences of the animals whose psychology is under consideration.
form adaptive and versatile behavior without concerning themselves Like most biologists, Krebs and Dawkins acknowledge that many
with the question whether the animals are consciously aware of the in- rrnimals are probably often conscious of what they do, but they turn
formation being processed by their nervous systems. For example, Wit- rway from the implications of this recognition and limit their consider-
tenberger (1981, 48) has clearly expressed the prevailing viewpoint of :rtion to the evolutionary adaptiveness of animal behavior. A primary
most behavioral ecologists: rcason is the conviction that 'fue cannot monitor what goes on inside
their heads." Yet scientists have many ways of learning a great deal about
Cost-benefit analyses (are discussed) as a/ [italics in original] behavior results what goes on inside the brains of animals. Neurophysiological data of
fiom a conscious decision-mrkitg process. . . . This procedure is just a short- tlrc sort discussed in chapter 7 is one important source of relevant evi-
hand logic used for convenience. We cannot assume that animals make con- tlcnce. And mental imagery provides a good example of something that
scious decisions because we cannlt rnonitor wbat goes on inside tbeir heads. Never- cennot be observed directly, but which cognitive psychologists have
the less, it really d.oes not rnatter [italics mine] what the proximate bases of those sttrdied successfully by indirect methods, as reviewed by Hannay
decisions are when evolutionary reasons underlying the behavior are our prin- (1971), Haynes (1976), Finke (1989) and Kosslyn (1988). Similar ap-
cipal concern. . . . The question of whether those choices are conscious or un- proaches have begun to be employed to study imagery in animals by
conscious need not concern us, as long as we remember that our tacit assump-
llilling and Neiwonh (1987). Farah (1988) has reviewed strong evi-
tions about purposiveness are just that. . . . Particular stimuli or contexts elicit
tlcncc that the sarne areas of the human brain are active when subjects
particular behaviors. An animal need not know why those stimulus-response
relationships exist. It need onh,l<n.\tr' what the relationships are. This knowing
think a[-r<>ut something as whcn thcy are stimulated by it directly. Thus
need not involve conscious awareness, though in many cases animals are un- thc rcluctencc t() ['lcc<lnrc c()nccrnc(l with cognition or consciousness in
doubtedly conscious of what thev are doing; it need only involve the appro- :urinr:rls sccrns to rcsrrlt :tt lt':tst irt prtrt fiorn a philosophical aversion
priate neurological connections. . . . Animals can be goal-directed without r'.rllrcr tlt:ur irtsrtnlr()rtnl.rlrlt' b.rrri('r'ri to st'icntifr-c irrvcstig:rtion. Perhaps
being purposeful, and they can behave appropriately without knowing why. lrt't'.ltlst' llt'lt:tviol'.tl t'tokr1',tsts .ttt(l t'tlrokrgisls li'cl ltrorc conrfortable
10 Chapter One
Animal Mentalitl II
consciousness, but that reflective consciousncss is a trnique human ca-
dealing with evolutionary adaptiveness, they hav-e seldom moved ahead
pability. This view is often expressed in thc asscrtion that animals may
to con"cern themselves with oih.r equally significant asPects of animal
know certain things, but they do not know that they know. This wide-
life such as neuroPhysiological mechanisms or mental experiences.
spread view is shared even by those ethologists who are most inclined
to ascribe conscious mental experiences to animals, for example, Crook
Definitions (1983, 1987) and Cheney and Seyfarth (I990a). M*y who doubt or
deny that animals are conscious use the term to mean reflective con-
It is helpful to begin by recognrzing that conscious thinking is not a
sciousness. Reflective consciousness would be difficult to detect in ani-
neat, hornogen.o,ri .ntity; for there are obviously many kinds.and de-
mals, if it does occur. People can tell what they are thinking about, but
gr..t of coisciousness. Natsoulas (1978, 9f0_ Il) emphasized an im- animals are held to be incapable of doing so, although animal commu-
One widespread lganing
[ort*t distinction that is often overlooked. following th: Oxford' English nication may often serve the same basic function, as discussed more
i, *h"t he designates as Consciousness 3,
mentally conscious or aware of fully in chapters 8 to 12. This very difficulty of detecting whether ani-
Dictionnryr "the"state or faculty of being
of conscious- mals experience reflective consciousness should make us cautious about
anything." This Natsoulas calls "our most basic conce_Pt.
other being ruling it out. But most of the suggestive evidence that will be discussed
,r"rr, foi it is implicated in all the senses. One's con^scious,
being aware of some- in this book points towards perceptual rather than reflective conscious-
whaieve, more ii might mean, must include one's
is what Natsoulas calls ness, and those swayed by a visceral feeling that some important level of
thing" (p. 910). Antther important meaning
by the think- consciousness rnust be restricted to our species may cling to reflective
Coniciousness 4, as defined in the OED, "the recognition
consciousness as a bastion still defended by many against the increasing
ing subject of its own acts or affections." Natsoulas adds to this defini-
evidence that other animals share to a limited extent many of our mental
tiJn of Consciousness 4: "One exemplifies Consciousness 4 by being
aware of, or by being in a position to be aware of, one's own PercePtion,
Reflective consciousness entails a simple form of introspection, that
thought, or orher occurrenr mental episg{e'l (p^ ?I I). The otler shades
is, thinking about one's own thoughts. Introspection was once a very
of mEaning analyzed by Natsoulas (1983, I?85, 1986, 1988) are less
active and popular area of research in psychology, but was long ago
important-for our purposes although roT: of them might apply.to non-
abandoned under the influence of behaviorism. Even after the cognitive
human animals, but there two imfinge directly on the issues discussed
revolution, f.* if any psychologists have revived introspection as a
in this book.
Natsoulas's Consciousness 3 is essentially conscious PercePtion, and
method of studying the operation of mind or brain. It is therefore
somewhat ironic that many behavioral scientists who resist assigning
it cal conveniently be termed perceptual consciousness. Its content may
any significance to the notion of animal consciousness tend to fall back
cntail memories, inticipations, or thinking about nonexistent objects or
on introspection as a criterion of human uniqueness.
cvcltts as well as immediate sensory input. An animal may think con-
There is an intermediate category that is not clearly dealt with by
scir>usly about somerhing, as opposed to being-influenced by it or react-
Natsoulas's definitions. An animal might be consciously aware of some
ing to it without any conscious awareness of its existence or effects.
part of its own behavior-for example, of its act of eating food or
CJnsciousness 4, as defined by Natsoulas, entails a conscious awareness
fleeing from a predator. This would be a special case of perceptual con-
that one is thinking or feeling in a certain way. This is conveniently
sciousness. But such an animal might be incapable of thinking that it,
called reflective coniciousness, meaning that one has immediate aware-
itself, was eating or fleeing. If so, it would be capable of perceptual con-
ness of one's own rhoughts as distinguished from the objects or activi-
sciousncss about its own behavior but not of reflective consciousness
ties about which one ii- thinking. The distinction between perceptual
that it, itsclf, was thc actor. Yet if we grant animals perceptual conscious-
and reflective consciousness is crucial to the sometimes confused (and
ncss of thcir ()wn rctions, thc prohitriti<ln against conscious awareness
almost always confusing) debate among scientists about animal con-
<lf wh<l is c:rting <lr flccing bccorncs :r strrrincd ancl artificial restriction.
Art :utirn.tl c:t1l:rtrlc ol'pcrt't'plrt:tl r'ortst'ir)lrsncss nlr,rsf oftcn bc aware that
M*y behavioral scientists and philosophers such as Lloyd (1989,
it is likely that animals may sometimes experience perceptual ll [)llr'tirul:u't'onrIr:utiort is r'.ttirr1,. or llt't'irrg. tlr;tt is, it rnust be con-
186) feel
12 Chapter One Anirunl Mentality f3

sciously aware of both the action and of who is performing it. A percep- Loewer (L987), this additional attributc ncccl not bc anything apart
tualty ionscious animal could scarcely be unaware of its own actions of from the physical universe. A crude analogy is thc distinction between
eating or running away. Thus if we deny all reflective consciousness to the hardware and the sofrware of computer systcms; the latter is some-
such an animal, we are in effect proposing that its mental experiences thing different from the information-handling mechanisms, but not
entail a large "perceptual black hole" centered on its own activities. anything that is different in kind from other physical processes and re-
These .ot tid.titions call into question the strong tendency of many lationships.
scientists to hold that self-awareness is a unique human capability, as A major part of the perceived difficulty of providing a definition of
discussed in more detail in chapter 12. conscious mental experience acceptable to scientists has been their insis-
Philosophers strive to clari$, their own thinking and to h_elp others tence that such definitions must be based on objectively identifiable and
do likewiri. Thir leads them to refine and sharpen their definitions of observable properties. But consciousness is essentially a subjective at-
important terms like thinking and consciousness. A few philosophers tribute, as we know from personal experience. One of the most basic
have focused their attention on the possibility that animals may experi- aspects of conscious thinking is the contemplation of objects and
ence some sorts of thoughts, and in doing so they have proposed a va- events) and one of the major challenges of cognitive ethology is to learn
riety of definitions. But they do not all agree on such definitions, Per- to what extent other species experience something similar. It need not
haps because of differing emphases on what seem to each philosopher be identical to human conscious experience; indeed, it is likely to differ
to be the most important attributes of conscious thinking. The hetero- substantially in accordance with the animal's way of life, its sensory ca-
geneity of human consciousness may expJlln the variety of philoso- pabilities, and its capacity for learning, memory, and anticipation. This
asPects of conscious strong desire for tangible, objective criteria may explain why many phi-
[hers'definitions, because they emphasize differing losophers of mind refrain from proposing explicit definitions of the
ixperience. I have previously reviewed some of the more thoughtful and
pertinent attempt; to arrive at clear and useful definitions of mental mental states with which they are concerned. But some affempts at def-
i.r-r (Griffin I981, 1982,1984, 1986). But behaviorists find almost inition are of interest because of the way that recendy discovered facts
any definition inadequate because it does not point the way to specific about animal behavior can be related to them.
operational tests by which mental states can be identified. The materialist philosopher Armstrong (198I, 4-10) defined mental
- occurrences as states or processes in the central nervous system that are
These difficulties arise in large part because mental states aPPear to
be processes rather than tangible entities. Something goes on in a cen- potentially capable of producing behavior, that ir, he considered
trirr.*ous system when someone desires, believes, remembers, antici- thoughts to be dispositions to behave in certain ways. This definition
pates, or decides. To the best of our very limited knowledge, these.pro- allowed him to escape from the serious limitation posed for the behav-
i.rr., result from dynamic interactions between nulnerous excitations, iorist's definition of thinking as verbal behavior by the obvious fact that
inhibitions, and sPontaneous or endogenous activity at synaPses in the we can think and feel without speaking or otherwise expressing our
central nervous tytt.-. There is no reason to suPPose that a specific mental states. Armstrong defined consciousness as perception of one's
neurohumor for desiring, believing, or deciding permeates the brain own mental states-a definition close to Natsoulas's Consciousness 4,
and produces these mental states, nor are there specific PaTt of the brain or what I have been calling reflective consciousness. Another materialist
uniquely acive during anticipation or choosing of particular actions. philosopher, Bunge (f 980), begins his book about the nature of minds
Mriy behaviorists argue that to Postulate tt, conscious thinking t-rystating that "perceiving, feeling, remembering, imagining, willing,
affecis behavior is to claim that a norunaterial factor interacts with the urd thinking are usually said to be mental states or processes. (We shall
physical world. But Processes and relationships are in a sense im- ign<>re . . . thc quaint view that there are no such facts)." Bunge claims
material, yet effective and important. Conscious thinking is in all prob- tlut :rn ability to lcarn is ncccssary fbr mcntal states) and that such plas-
abitiry an"activity or attribute of central nervous systems,.a functional ticity is confirrctl to birds rurtl n'rrrrrrrrtrrls; lrtrt he overlooks extensive evi-
process by which a brain supports mental activities of which the person tlcncc of' lcarrring in :r witlc v.rrict1, ol'vcrtctrratc ancl invertebrate ani-
t. ,.,i-fl is corrsciotrsly awarc. Although mental experiences entail nrltls.
s()mcthing rrx)rc thrur infilrnr.lti()n 1'rroccssitrg, as argped cogently by l lrrll'll ('('t'rtur'1, ,*,r, tt'ltctt sYtttlroltt ,,,tttttturtit':ttiolt in lurinrals was
14 Chapter One
Anirual Mentality l5
people to be conscious of an event if (l ) thcy crrn srry inrmediately after-
unknown and generally believed to be impossible, Price (1938) con-
wards that they were conscious of it and (2) wc can indcpendently verif,
ceded that if animals did use symbols we would have to asstilne that they
the accuracy of their report." M*y of thc cxamplcs of animal corrunu-
have minds. And in a series of Gifford Lectures at Edinburgh,The De-
nication discussed in chapters 8 to 12 satisfy this requirement, since the
ueloprnent of Mind, the philosopher Kenny (1973,47) stated that "to
animal communicates some simple statement about what it is doing,
have a mind is to have the capacity to acquire the ability to oPerate with
and we can readily verify the accuracy of the statcment. If one requires
symbols in such a way that it is one's own activity that makes them
symbols and confers meaning on them." In emphasizing the importance
that true consciousness must be reflective, that is, Natsoulas's Con-
sciousness 4, the communication that there is a dangerous predator ap-
of symbolic communication as a criterion of mind, Kenny continues:
*The pursuit of self-selected goals that go beyond the immediate envi- proaching would fail to demonstrate such true consciousness unless it
included something equivalent to "I am conscious that a dangerous
.onrn.rrt in space and time is not possible without the use of symbols
predator is approaching."
for the distant, the remote, and the universal. And on the other hand,
The physicist Longuet-Higgins (L972, 136) in the same series of
the use of symbols itself involves PurPoses which go beyond the tem- (lifford lectures suggested that "the idea of a goal is an integral part of
spatial present."
- and
the concept of mind; and so is the idea of intention'. An organism
The examples of animal communication discussed below in chapters
which can have intentions I think is one which could be said to possess
8 to l l satis$, Kenny's criterion in a general way, but symbolic com-
.r rnind. . . . The concept of intention . . . involves the idea ofthe ability
munication is especially evident in the dances of honeybees described in
to form a plan, and make a decision-to adopt the plan. The idea of
chapter 9. For it is certainly the bee's own activity that makes her waggle
lirrming a plan, in turn, requires the idea of forming an internal model
danie a symbolic statement. The dances of scouts from a swarm of bees
of the world." Philosophical ideas about the importance of intentions in
that have visited cavities report their distance, direction, and desirability
cornmunication have been thoroughly reviewed in the book edited by
to their sisters in a situation where the symbolic communication is well (i>hen, Morgan, and Pollack (1990). Most of these philosophers take
removed in space and time from the objects it describes. Although the
lirr granted that human intentions are ordinarily conscious plans to do
separarion in time is ordinarily only a few minutes, in special situations
something in the future, but the possibility of nonhurnan intentions is
wiggle dances refer to a cavity or a food source that the dancer has not
sc:rrcely mentioned in such philosophical discussions.
visited for several hours (von Frisch1967,350).
Yet animals certainly seem to form at least simple plans and make
Some may object that we can voluntarily coin new words, or at least
tlccisions about what actions are likely to achieve what they want. Much
sclcct our symbols and thus endow them with meaning, while the goals
of'their learned behavior is necessarily based on some sort of acquired
of clancing bees may be assumed not to be self-selected but to be auto-
rcpresentation that models some important aspect ofthe external world.
rnaric ..r.ils of hunger or other internal physiological states. These in
Although anticipation and planning are impossible to observe directly
tunl arc oftcn assumed to set offgenetically programmed behavior pat-
nr rurother person or animal, indications of their presence are often ob-
tcnls that are held not to be accomPanied by conscious thinking. But,
st'rvable. Early ethologists such as Heinroth, and especially Lorenz
as cliscussed in chapter 12, the customary equation of instinctive with
irr thc 1930s, studied the intention movements of birds (reviewed by
unconscious rests on a very flimsy basis. The denial that the honeybee
communication system is truly symbolic alnounts to an a priori denial
llrrcnz l97l) and pointed out that these small-scale preliminaries to
rrurjor actions such as flying often serve as signals to other animals. Al-
that bees are conscious, which denial is then used to justi$r the rejection
t lr<rrrglr Lorenz interpreted intention movements as indications that the
of their communication as symbolic. In other words the definition of
lrirtl rvas planning and preparing to fly, the term "intention movemenf'
symbolic comes to have an unstated requirement of conscious selection
Ir:rs lrccn cluictly clropped from cthology in recent years, presumably
of signals along with an implicit assumption that this is something of
lrt't'rrrrsc l'rchaviorists fl'rrrcd th:rt thc tcrrn had mentalistic implications.
which insects are incapable. ( )rr tlrc othcr hlurtl, .s()nrc rttotlcnt crhokrgists rccognize that animals do
Baars (1988) suggests the following definition of consciousness
Ir.rvt'rrt lt'.rst sirrrPlc intcntiorrs (Krt'lrs .urtl l):rn,kirrs, 1984; Guilford and
from the viewpoint of a cognitive psychologist: "We will consider
16 Chapter One Ailimul Mentality 17

Dawkins, I99I), although they avoid describing such intentions as con- that its burrow is nearby, its resultant dash to thc firrniliar shelter results
scious. from combining these two beliefs into a bclicf thrrt ir should rush to the
Daanje (1951) described a wide variety of intention movements in burrow. Another distinguishing feature prop<>sccl by Millikan is that an-
many kinds of animals, but his primary interest was in the tendency of imal signaling does not seem to her to involve a scparation of indicative
such movements to become specialized communication signals in the from imperative functions of internal representations, whereas she em-
course of behavioral evolution. The possibility that intention move- phasizes that "human beliefs are not tied directly to actions." But cer-
ments indicate the animal's conscious intention has been neglected by tainly many, perhaps most, of our beliefs are related ro actions of some
ethologists during their behavioristic phase, but we may hope that the sort. And insofar as animals may entertain beliefs that are not related to
revival of interest in animal thinking will lead cognitive ethologists to rrny observable behavior, we would have difficulty gathering evidence of
reopen the study of the degree to which intention movements may in- their occurrence.
deed be signals of conscious intent. The very fact that they so often seem
to evolve into communicative signals may reflect a close linkage be- Significant Ideas about Animal Consciousness
tween conscious thinking and its communicative expression.
Later chapters will describe several suggestive examples, such as bea-
'fhe nature of consciousness and the
extent to which it occurs are major
vers piling material around sturdy fencing protecting a tree with the .rnd basic problems of psychology and the philosophy of mind. In ad-
apparent intention of reaching the unprotected trunk and branches, clition to the penetrating analyses of major philosophers of previous
which they then cut; cooperative hunting by lionesses; and honeyguides ecnruries, some contemporary psychologists and philosophers have re-
calling and leading human honey gatherers to distant bee nests. In all iccted the dogmatic pessimism that characterizes many behavioral scien-
these and many other cases it is difficult to deny that the animals form tists; and they have discussed the possibility that some animals do ex-
and execute simple plans. But the dance communication of honeybees Pcrience conscious thoughts. For instance, Dunbar (1988) finds it
discussed in chapter 9 provides us with one of the best windows likely that higher vertebrates at least "themselves do a great deal of their
through which we can discern signs of intentional planning. The scouts cost-benefit processing on a cognitive plane." Armstrong-Buck (1989)
that have found very desirable cavities seem to be urging their sisters to lrts reviewed recent developments in the study of animal cognition from
go tlrere, and according to Lindauer (1955, l97L) this urging can be t hc perspective of whitehead's philosophy. The "biophilosopher"

altcrcd by following dances of other bees describing better cavities. l(cnsch (L97L, 1985) recognized the likelihood that simple sorts of
Furthcnnore) a decision of great importance to the bees is reached on t'onscious experience occur in a wide variety of animals, and so do the
thc ['r:rsis of long series of communicative exchanges of information .rrrthors of several chapters in the recent books edited by Bekoff and
:rt'rout diftbrcnt cavities. These are only a few examples of animal behav- I.unieson (1990) together with other philosophers whose views are dis-
ior tl'rat satisfy Longuet-Higgins's criterion of mind. t'rrssed in chapte r 12.
-lo be sure, some
Millikan (1984, l9S9) doubts that bees and birds "have inner repre- philosophers "reject the concept of consciousness
scntations in the sarne sense that we do." This wording exemplifies a .rs otiose in the srudy of animal knowledge," in the words of Heyes
recent trend to shift from denying that animals experience any signifi- ( l9tl7)., u,ho argues that cognitive ethology is beset by muddled think-
cant thoughts to a more modest claim that their thoughts are different rrrg. Dore and Kirouac (L987) argue that cognitive ethology is mis-
from ours. Millikan goes on to list several ways in which she believes rlrriclccl because it depends on inadequare definitions. Yoerg and Kamil
that the internal representations of nonhuman animals differ from hu- t)91 objcct strongly to any ascription of conscious experiences
1I ) to an-
man beliefs. But many of these features do appear to be present in the tttt:tls, rrncl urgc that cognitive ethology restrict itself to an analysis of
memories and decision-making processes exhibited by animals. For ex- rrrgniti<ln thlt is as.sumcd to [-rc urrcon.scious. Dickinson (1980,5) saw
ample, she claims that only members of our species can "combine beliefs "n() r'c:ls()rt why nrcntlrl pr()ccsscs shoukl not bc inferred from behav-
with beliefs to yield new beliefs." But it seems likely, for example, that rour'"; ['rur Itt<lrc rccctttlv hc lt.rs ;u'grrt'tl rll:lt "n'rrlnifcst intentionality of
when an animal believe.s that a predator is threatening and also believes lrt'lt:tviour'" is rtot sttllit'it'rrt t,r tlt'rrx)nslr':lt(' rnt'ntll statcs (Dickinson
18 Chapter One Animnl Mentality 19

1988, 323). Most of the authors in the collection of papers edited by vant evidence concerning domestic animals w<>trkl rcquire another
Davey (1983) are reluctant to credit nonhuman animals with significant whole book.
mental states. And Dennett (1989) has asserted, without qualification To *y biologist it will be almost self-evidcnt that insofar as animals
or justification, that the attempt to study animal consciousness is a wild do experience conscious thoughts or subjective fbelings, these will not
goose chase or, at least, impossibly difficult (Dennett 199L,446). be unitary all-or-nothing phenomena. Certainly our own thoughts and
Mackintosh (L987) concludes that rats know about the conse- feelings vary enormously in their nature and complexity and in the rela-
quences of their actions, but feels that "this is not necessarily an apPro-
tive importance of conscious and unconscious processes, as emphasized
priate language for scientific analysis," thus expressing the intellectual by Shallice (1978,1988a, I988b). But before we can hope to analyze
ionflict experienced by many contemPorary students of animal behav- how the content and quality of consciousness varies from species to spe-
cies and from one situation to another, we must determine where and
ior. Recent symposia edited by Hoage and Goldman (1986) and by
when it occurs. The relatively simple content of animal thoughts and
|erison and |erison (1986) discuss animal intelligence from a variety of
subjective fcelings is almost certainly relevant to the animal's own situa-
viewpoints; and although the traditional inhibitions generally prevail,
the authors of some chapters edge closer than usual to considering ani- tion rather than to human concerns. This makes the quest for evidence
mal consciousness. Two books published in the 1980s exemplify this of consciousness more difficult than if we were searching for a single,
well-defined entity comparable, say, to color vision. But the lack of sim-
trend. The first, by a psychologist, concludes: "Our organ of thought
may be superior, and we may play it better, but it is surely vain to believe plicity does not render something unimportant or impossible to detect,
analyze, and understand.
that other possessors of similar instruments leave them quite un-
touched" (Walker 1983, 388). The second, by two philosophers, em-
phasizes that "in dismissing consciousness as superfluous, one sets limits Objections of "Inclusive Behaviorists"
on one's explanatory apparatus. It is important to realize that the limits
are set by choice, self-imposed, not dictated by any fundamental prin-
M*y people find it difficult to understand why so many behavioral
scientists are adamandy reluctant to consider animal consciousness. The
ciples of scientific methodology. There is room for consciousness if one
is willing to make room for it" (Radner and Radner 1989, 208).
historical reasons, thoroughly reviewed by Boakes (1984), Burghardt
(1973, L978, I985a, 1985b), Dewsbury (198a), ffid Rollin (1989,
Later chapters will explore what we can find in the extensive data on
1990), have involved a reaction against excessively generous interpre-
animal behavior when we do make room for animal consciousness. My
tations of isolated instances of animal behavior that suggested rational
approach will entail tentatively considering animals as conscious, mind-
ftrl creatures with their own points of view; and I will attemPt to infer,
thinking and insight. Coupled with this rejection of mentalism was an
cqually fcrvent rejection of the idea that genetic influences as opposed
as fhr as rhe available evidence permits, what it is like to be an animal of
a particular species under various conditions. As emphasized by Dretske
to individual experiences had a significant effect on human or animal
lrcl'ravior. Although genetic control of behavior is logically a wholly dif-
(1988), it is important to distinguish between what animals dn aurtd
ll'rcnt matter from the significance of subjective mental experiences, the
what happens to them; it seems likely that a considerable amount of
two issues have tended to be linked in theoretical consideration of ani-
animal behavior results from an animal's doing something rather than
nr:rl behavior and mentality, as discussed by Burghardt (1978). In psy-
being a passive object that is simply affected by the world around it.
t'hok>gy these distinct but closely coupled trends were combined in be-
This review of the published literature is by no means exhaustive. I have
lrrrvi<rrism, as advocated most influentially by Watson (L929) and
selected cases where versatile behavior patterns and apparendy inten-
Skirtrrcr (1974). l)uring the same period a strong reductionist tradition
tional communication are reasonably well understood, but many other
.rls<r rlcvclopcd in biology, typificcl by the views of Loeb (L9L2), who,
examples are equally suggestive. I will emphasize wild animals living
.rlth<ltrgh hc l-rclicvctl in tl'rc cxistcrrcc of human consciousness, argued
under reasonably natural conditions) not because Pets, domestic ani-
rlr.rt rrll :urirn:tl lrntl cvcrt rtttrclt hurn:rrr lrchlrvi<lr could be explained in
mals, and wild animals in captivity do not show equivalent evidence of
t('r'l)ls ol'tropisrns. In tlrt'ir zt':rl lirr olrjt't'tivc proof'<lf :rny claims about
conscious thinking, but simply because an adequate review of the rele-
Animal Mentaliry 2l
20 Chapter One
such cognitive states are real and necessary comp()ncnt.s o1'any adequate theory
animal behavior or mentality, most of the psychologists who established that seeks to explain animal behavior.
the long dominant behaviorist movement insisted on three major
points: These cognitive states "include learning, rcmcmbcring, problem solv-
ing, rule and concept formation, perception, (and) recognition" (Roit-
I. Learning and ind-ividual experience account for almost all behavior l"iat 1987,2).
not direltly controlled by the animal's structural capabilities' . Animal cognition has thus come to be accepted as real and signifi-
11. Only exteinal influences and directly observable behavior should cant, and its investigation is recognized as important, as reviewed in the
be considered in explaining what animals (or people).d9; behav- volume edited by Ristau (1991). Menzel and Wyers (1981) and Menzel
ioral scientists should fimit their concern to observable inputs to (1991) consider that the foraging behavior of animals entails cognition,
and outputs from the black box called an organism. And .urd Wyers (1985) concludes that cognitive concepts are useful in ana-
III. Subjective mental experiences, especially conscious thinking, lvzing the behavior of sticklebacks. But animal consciousness is still ta-
should be ignored for two reasons: lxro, both among biologists who study animal behavior and psycholo-
A. They .ri ,n -.asurable "private" phenomena, PercePtible only sists such as Terrace (1984, 7), who asserts that "both in animal and
by th. one who experiences them, so that statements about lrrrman cognition it is assumed that the normal state of affairs is uncon-
them carlnot be independently verified, and scious activity and thought."
B. They have no influence on behavior, and are thus incidental Although biologists have always tended to dissent from claim I of
bypioducts of brain function, or epiphenomena' lrchaviorism, they have generally concurred with psychologists in ac-
t cpting claims II and III. Therefore it will be convenient to refer to both
Claim I of behaviorism has been largely abandoned, although it used ttrl)ups collectively as "inclusive behaviorists." Despite renewed interest
,o b. vigorously defended by many 6ehavior.al scientists who reacted rrr :urimal cognition, the scientists who are willing to venture into this
against Irry r,rggestion that tehavior might be genetically influenced ,lifticult area have tended to cling tightly to the security blanket of con-
*"i.h muchth.iir. fervor as that currently directed against suggestions vcrrtional reductionism. Although most philosophers have long since
that mental experiences may occur in animals and exert some influence .rbuncloned logical positivism, ffid cognitive psychologists now reject
on rheir behavior. Extensivl evidence shows that what animals learn
rlrc negative dogmatism of the strict behaviorists, students of animal
strongly constrained by species-sPecific capabilities; some behavior pat-
l,t'lrrrvior are still severely constrained by a guilty feeling that it is un-
terns"aie learned much -o.. .arily than others that the animal is
quite st icntific to inquire about subjective feelings and conscious thoughts
capable of perfiorming. Furthermore, the widespread interest in socio-
r(.<rlgan 1989; Heyes 1987; Latto 1986; Snowdon l99I; and Yoerg
Uiif"gy nas tea to a strong emphasis on the adaptive value of behav- .urrl Kamil l99t). Although ethologists have recognized more and
ior--ht* it increases the like[Eood of an animal's survival and repro- nr()r'(: cornplexity and versatility in animal behavior, many have lagged
duction and, hence, its evolutionary fitness' lrt'lrirrrl the cognitive psychologists and continue to try dutifully to fit all
Claim II has also been greatly modified due to the cognitive revolu- tlrt' ncw knowledge about animal behavior into the salne old pigeon-
tion in psychology. As sirnrn arrzed by Roitblat, Bever, and Terrace Ir,rlcs that seemed sufficient years ago to Pavlov and Watson. Thus the
(1984,1): 1',h,rst of )acques Loeb (19I8) still makes its cold and clammy influence
It'lt rvhcn animal behavior is described solely in terms of stimuli, re-
Animal cognition is concerned with explaining anilal behavior on the
\l )( )r lscsr rurd adaptive advantages.
,i"t", as well ai on the basis of observable variables
of cognitiv. and processes,
Asitlc fionr Lorenz (1971) *d Hediger (1947,1968, 1976,1980),
such as stimuli ,.sponses. For a time it appeared, at least to some, that
"nd they were ex- r,'r v ll'w cthr>l<>gists havc discusscrl animal thoughts and feelings in re-
discussion of cognitiv. ,trt.t was not necessary' either because ( ('nt vcrlrs. Whilc sclclonr tlcrrying thcir cxistcnce dogmatically, they em-
environmental events, or because they were epiphen-
haustively deteniined by
omenal and withorra *y causal forcc. In any casc, it was assulned that a suffi- I'lr.rtizc tlr:rt it is cxtrcnrclr,<lillit'trlt. PcsllxPs inrpossible, to learn any-
for explanation' A rlrrn1,, ;rt :rll :rb<lut tlrc srrbjt't'tivt't'x1rt'r'icnt't's ol':urotlrcr spccics. But the
ciently detailed descripiion of ovcrt cvcnts w<>uld suffice
has made it clear, however' that
!r.rri.ul of thc rc..ar.l', into:rllinral bchavi<lr
Animal Mentality 23
22 CbaPter One
terns, too small to be resolved by terrestrial tclcsc()pcs, do indicate that
difficulties do not lustify a refusal to fhce uP to the issue' As
their there was once liquid water on Mars. Somc strict bcl"raviorists object to
({gig.,i1) put th. *"n.r, "of course to inteqpret the tho-ugh1s,.or
animal's behaviour is difficult, but this all hypotheses about conscious experienccs in animals, or even in
:a"i;;1.",,'*ni.f, determine an
people, on the ground that they cannot imaginc any procedure by
attemPt to do so. If it were not difficult,
is no reason for not making the
behaviour, and which such hypotheses can be confirmed or falsified. This may tell us
there would be very little [lterest in the study of animal
something about the limited imaginations of scientists, and outside of
very few books about it."
narrow scientific circles this argument is no more convincing than that
it is often claimed that human language is what makes conscious
capability, as of the solipsist philosopher who insists that he is the only conscious
thinking possible for us, but that no other spegles has this
geo/ Davidson 1984). This view is person in the universe . At early stages in the development of any branch
;;g""J"b'y Adler and 1lssz,
of science it is often necessary to do the best one can with fragmentary
*Ia.ty held euen by those who believe it probable that some animals cvidence and hypotheses that cannot be neady formulated into crisp al-
."p.ri.".e at least perceptu{_lgnsciousness (Natsoulas's Consciousness
con- tcrnatives for the very reason that the subject is poorly understood.
ayl r"r example, R..rr.rr G1TL) distinguished human from animal
sciousness on the gro,rrrd that the forrier but not the latter is normally
verbally.lut increasing understanding of the versatility of an- Limitations of the Objections
imal communication makes thetistinction between animal
'ltr claim that it is impossible to study subjective experience scientifically
cation and human language a less crucial criterion of human
is to overlook the fact that many scientific advances have begun by ex-
pkrratory probes into unknown areas where clearcut evidence is not ini-
As pointed out by the philosopher.Ytl P3yner (1978)' what
p..tottablyhelpful to animals in coping rially available. For example, Darwin and Wallace could not direcdy ob-
termed, "mental po#rs"
th.y "r.
face, and thereforJmust contribute to their sclve and measure the evolution of animals or plants in the remote past.
with the challerrg., I Iad they been inhibited from speculative inferences by the sort of par-
.uol rtiorrary fitnErs. He emphasized how useful it is to think
about al-
they are acrually .rlytic perfectionism that prevents inclusive behaviorists from investigat-
ternative actions and their tit<ety consequences before ing animal consciousness, one of the most far-reaching of scientific de-
error in the real
p.rf"r*.d. This of course serves to- ..pIt... trial and think- vclopments would have been severelv hampered if not prevented
world, where error may be costly or fati, with decisions based
inf about what orr" -"y_do. Popper seemed to imply that.such mental It is not correct to argue) as some have done, that even considering
of much
trial and error is a uniqul$ human capability, but the versatility .rnimal consciousness entails a lowering of scientific standards. This ar-
animal behavior ,rgg.r., ihr, ott , r.iy simple and elementary level
those they believe gument confuses critical standards with narrow-mindedness. Inquiring
sometimes think t63rr, possible acdons and choose
.rlxrut unknown or neglected subjects calls for questioning and explor-
will lead to desired results or avoid unpleasant ones. rng possible approaches, what is sometimes called pre-science. When
must be falsifi-
Scientists often insist that any significant hypothesis
to anticipate how it might be srrch explorations lead to suggestions and hypotheses, these should of
able, which means that we -rti be-able ( ( )rrrse be scrutinized and evaluated with the highest criticd standards.
procedures are not im-
.o.fir-"d or disconfirmed, even if the necessary llrrt to rule out a plausible possibility as unscientific is a sort of self-
mediately practicable. Scientists lose interest in a theory if no one can
not. Thus it was not nrrposcd handicap or even blindness. In the words of Kety (1960,
suggest n"* ," ascertain whether it is correct or
Lowell to that there were Iti(r2) "Narure is an elusive quarry and it is foolhardy to pursue her
entirely unreasonable for Percifal Postulate
u'ith onc cye closcd and one foot hobbled."
to him. This was clearly
canals on Mrrr, gi"* the timited data availabli
could readily lrtltrally mistakcn is the charge that to suggest animals may some-
a restable hypofiesis, and. Lowell or his contemPoraries
using improved telescopes or sPace- rrnrcs l'rc c<lnsci<>us smacks of postulating immaterial or supernatural en-
i*.gi"" that'future asffonomers not' As we now trtics. (ixrscious th<>trghts :rnrl srrtrjcctivc fbclings are generally agreed
*iirmight determine whether there were canals or
of the Martian surface became available'' to rt'strlt lirllrr:rctiviric.s ol't't'ttlr:ll rtt'r't,ou.s syritcrns, and there is no rea-
know, when suitable pictures .,on lo rkrulrt tlr:rt tlrcst':trt'f ,,ovcr ncrl lry tlrt'1u'inciPlcs <>f rratttralscicnce.
riverlike erosion pat-
they disconfirmed Lowell's hypothesis, although
24 Chnpter One
Animal Mentality 25

it for granted that consciousness exists in at least one species, it intelligent perficrmance of a trained horse namcd Hrns, whose devoted
trainer believed he could add, subtract, multiply, arrcl cven divide writ-
is a vJid andiignificant quesdon to ask to what extent it also occurs in
ten numbers. Flans gave his answers by tapping with his forefoot, eight
orhers. A related confusion is the implication that to suggest animals
taps when 2 x 4 was displayed, twenty-seven taps in response to 3 x
may consciously plan what to do in the immediate furure is somehow
akin to postulating a divine PurPose causing the diversity of anim* *d
9, and so forth. Some skeptics were troubled by the fact that Hans
solved difficult arithmetical problems about as rapidly and apparently as
the complexity of their st.oitui.. A moment's thoughtshould suffice to
casily as simple ones (Washburn L9L7). But he tapped correct answers
dispel this lingering vestige of the nineteenth-century debates about di-
cven when others beside his familiar trainer presented the problems,
vini creation versus evolution influenced by natural selection.
:urd many scientists were convinced that he understood the problems
rrnd arrived at correct answers by a sort of mental arithmetic.
Anthropomorphic Objection, and Conceit A psychologist, Oskar Pfungst, showed by careful experiments that
Hans was not watching the written numbers but the person who pre-
For many years any consideration of animal consciousness was strongly
scnted the problem. If no one was visible, or if the person did not know
discouraged by the accusation that it was anthroPomorPhic. This wide-
resulted from the recognition that many earlier_ascrip- the correct answer) Hans tapped his foot at random. What Hans had
tions of human thoughts to animals were wholly unjustified. But the
.rctually learned was to detect the small and inadvertent motions that
charge of anthropornorphism had been inflated to include even the 1rcople made while watching to see whether he stopped after the correct
thoughts by number of foot taps. Even when observers tried to avoid doing so they
-orit.ntative inference of the simplest kind of conscious the belief that a could not help revealing by subtle motions or facial expression when
animals. We were, in effect, brainwashed into equating
that a rabbit thc right number of taps had been produced. In his detailed account of
horse could carry our long division with the suggestion
down its. bur- these experiments Pfungst (191I) described many other complex pat-
consciously anticipates etciping from a fox by plunging
of anthroPomorphism, rcnls of behavior learned by Hans and showed that they all depended
row. When one carefully examines such charges
on inadvertent cues from human companions.
it turns out rhar they entail the implicit assumPtion that whatever it is
The saga of Clever Hans has been almost universally accepted by
suggested the animal might do, or think, really ls a uniquely human
scicntists as a definitive example of mistaken inference of complex men-
at[Ibute. Such an assunptiot begs the.ques.tion.being asked because it
rel abilities in animals. But this enthusiastic application of scientific
presupposes a negatrve answer and is thus literally a confession of pre-
This point has been emphasiz:d.bI Bennett t'rrution has mushroomed into denial that animals experience even the
'0924.1l),or pr.jrdice. (19rc: I985b, 1991) and especi4ly Fisher
iudg-.rrt sirnplest conscious thoughts. Inability to do arithmetic has been taken
Burghardt PV
.rs cvidence for the absence of any thinking whatever. What has been
itoSZ, I990) who has spelled out in considerable detail why there is no .rlmost totally overlooked is the real possibility that Clever Flans was
[',,,ri., philosophical basii for the taboo against anthropomorphism as it
( ()nsciously thinking something simple but directly relevant to his situ-
Irrrs l'rccn pcrclived by most scientists. When applied to the suggestion
.rtion-perhaps something like: "I must tap my foot when that man
r6i1r alimals might think about simple things that are clearly important
rrods his head." The horse's behavior was quite consistent with such an
ro them, this c-harge of anthroPomorPhism is a conceited claim that
intcrpretation, but scientists' enthusiasm for debunking unjustified in-
only our species is iapable of even the simplest conscious thinking'
ll'rcnces has trapped them for generations into a dogmatic dismissal of
t hc plausible alternative that animals may experience simple conscious

The Inverse "Clever Hans Error" r hotrghts, evcn though quite incapable of mental arithmetic.
'l'hc pcrccptual discrimination needed to detect inadvertent counting
Students interested in animal behavior have long been haunted by the
g('strlrcs has bccn recognized as remarkable and significant. Many ani-
specter of "Clever Hans errors." Suggestions that an animal might be
rrr.rls rrrc kn<lwn to hrrvc scns()ry rrbilitics cxcccding or differing from our
ctnsciou.ly aware of the tikely results of its behavior routinely elicit a ()\\,n. l)ogs crur srrrcll tlilli'rcrrct's lrt'twccrt cl<tthing worn by different
sort of knee-jerk reflex accusation that they result from Clever Hans er-
pt'opk', inst't'ts tlist'r'irrrirr.ttt'tlrt'pl.trtt'ol'pol:triz:ttiott <lf light, bats and
rors (Sebeokand Rosenthal, I98t). This hazardrefers to the aPParently
26 Chapter One Animal Mentnlity 27
other small mammals hear frequencies far above the human range, and tent of communicative signals, both human antl animal. To the extent
sharks are so sensitive to electric currents that they can detect buried that communicative signals convey conscious th<>ughts and subjective
prey by the electrical potentials from their heartbeats. But such "super- feelings, they can be used as objective, indcpcndcntly vcrifiable evidence
human" sensory capacities are simply different input channels to the about the mental experiences of the animals themselves.
central neryous system, and their refinements tell us little or nothing Additional indications of animal consciousness arise from the versa-
about any subjective thoughts that the animal may experience. tility with which they sometimes cope with novel and unpredictable
The detailed observations by ethologists under natural conditions, challenges in simple but apparently rational ways. While it islmpossible
reviewed in chapter 3, have shown that many animals monitor the be- to Prove with totally logical rigor that an animal thinks consciouslv
havior of predators and react to very slight changes in posture or behav- about what it is doing, even when it behaves intelligently, behavioral
ior that signal a likelihood to attack. Predators are also very adept at versatility does provide suggestive evidence that is too significant to ig-
noticing the slightest indications that potential prey are weak or sick, nore-though behavioral scientists have customarily done so.
which make them easier to capture. The sarne basic neurophysiological
mechanisms that underlie such finely tuned discriminations under nat-
ural conditions are probably employed by trained animals when they Reasons to Infer Animal Consciousness
learn to respond to inadvertent counting movements of their human Out of all these multiple crosscurrents of ideas, three categories of evi-
trainers. dence stand out as the most promising sources of significant, though
incomplete, evidence of conscious thinking by nonhuman animals.
'fhey will be reviewed in the following chapters:
Discredit by Exaggeration
Scientists often dismiss suggestions of animal consciousness by overin- I. Versatile adaptability of behavior to novel challenges (discussed in
terpreting them to include complex levels of thinking that are clearly chapters 2 to 6);
beyond the capabilities of nonhuman animals. This attitude was recently II. Physiological signals from the brain that may be correlated with
parodied on the cover of an issue of Newsweek which included a bal- conscious thinking (discussed in chapter 7);
anced review of the current revival of interest in animal thinking and III. Most promising of all, data concerning communicative behavior
intclligcncc. But the cover picture shows a dog with a balloon rising by which animals sometimes appear to convey to others at least
fi<xrr lris hcacl, and in the balloon the formula e : rnP. This is a typical some of their thoughts (discussed in chapters 8 to I l).
cxirggcration of thc suggestion that animals may think about simple Finally, after all this suggestive evidence has been reviewed, it will be
tr)rrttcrs th:rt arc important to them into an implication that they share .rlrpropriate to consider (in chapter 12) several general questions that
tlrc rnorc ct>nrplcx levels of human thought. Another example of this ,rrc relevant to the question of animal mentality.
tcntlcncy t() cxaggerate that which one wishes to deny is provided by
Ing<>ld's (1988) implication that those who suggest animals may some-
times think consciously are claiming that nll nonhuman animals always
do so, as discussed below in chapter 4.
It is important to recognize that we all make useful, and generally
correct, inferences about the conscious thoughts of other people by ob-
serving their behavior, especially their communicative behavior. The
sarne basic approach is equally applicable to animal minds. When ani-
mals communicate, as they often do, they may sometimes be expressing
conscious thoughts. M*y animals exchange rich repertoires of com-
municative signals, especially those that serve to regulate their social
behavior. Indeed, mental experiences may constitute the primary con-
Finding Food. 29
Foraging Decisions by Bumblebees
Bumblebees would not seem likely to employ a high order of thought-

Finding Food ful decision making, but when Pyi<e (L979) inalyiccl in detail the riays
in which a particular species of bumblebee (Bornbus appositws) gathered
nectar from clusters of monkshood flowers in the Colorado mountains,
he found that they followed fairly complex rules. These flowers vary
considerably in nectar content) depending in part on whether an in-
sect has already removed nectar from a particular flower. Pyke marked
bumblebees so that individuals could be distinguished, and recorded
their behavior when visiting clusters of flowers that had not been visited
.MocatingsuitablefoodisoneofthemoStwidespreadand by other insects. No one flower held enough to fill a bumblebee's stom-
pressing problemi faced by animals. Unlike pets and laboratory animals, irch, so that several had to be visited before she flew offto her nest. The
most *ild *i-als must spend a large fraction of their waking hours flower closest to the ground, or the next to lowest, was almost always
locating food and extracting it from their environments. In the case of visited first, and the bumblebee then moved upward, usually selecting
herbivores, this may seem simple at first thought; but it is seldom an the closest flower she had not already visited. Out of 482 observations,
easy mafter of wandering about nibbling whatever vegetation is en- the same flower was visited twice on only five occasions. Either the
countered. Not all plants are equally nutritious by any means, and even lrumblebee remembered for a short time which flower she had already
grazinganimals thal appear to need nothing but abundant grass do pick visited, or else she left a scent mark or some other indication that en-
*d .hoose just which patches are most worth cropping. Many herbi- .rbled her to avoid wasting her time on empty flowers.
vores musr pay considirable affention to signs that food is available The simplest rules that Pyke (1979, If70) could formulate to ac-
from particulai plants, and the tactics they employ often call for at least count for the foraging tactics of these bumblebees took the following
simpli levels ofiearning and perhaps conscious thinking. Active Pt+r- lilrm: "Start at the lowest flower on a given inflorescence, then move to
torr f... more obvious challenges because they must not only locate but thc closest flower not already visited, unless the last movement had been
also pursue and capture prey animals that seldom wait passively to be tlownward and was not in fact the first switch from one flower to an-
c:rtcrr but clcv<>te considerable effiort, and sometimes thought, to avoid- other on a particular inflorescence. In the latter case, move to the closest
ing that fhtc. lrigher flower not just visited." The formulation of these rules in English
l;or;rging lrchrrvior varics widely, and its versatility is not closely cor- rrrrry make them seem more complicated than they actually are, but even
rt'l.rtctl with thc prhylogcnctic group to which the animals belong; so- il'simplified into a set of actions within the capabilities of a foraging
t'.rllctl krwcr rurinurls often display ingenuity comparable to that of lrrrrnblebee, they are not the simple, stereotyped sort of reactions we are
Irrrurrrn:rls. 'l'his rcvicw of fbeding tactics that suggest thinking on the .rccllstomed to expect from insects.
:rnirrrrrl's plrt will trc divided rather arbitrarily into categories that can be Many other insects engage in equally ingenious foraging behavior,
rotrghly characterized as feeding on passive and active Pf1l. This chapter lrut most are difficult to study because they rely so heavily on olfaction,
wilibe devoted to the former category, in which the food consists of .urtl because it is extraordinarily difficult to monitor and experimentally
plants or of animals that are relatively inactive, so that the principal rn.uripulate the chemical signals that guide their behavior. Locating
problems are how to locate food and handle it. Chapter 3 will concen- lirorl rlay cntail searching for the odors that signal its availability, fol-
i.rt. on predation upon prey that exert effective efficrts to escape and k ru,ing graclicnts in the concentration of such odors, or simply moving
can be taken only by means of actively versatile tactics. In some signifi- rrpu,irrd whcn thcy arc clctcctcd. In othcr cases where insects use vision
cant situations these tactics include coordinated action by two or more to krc:rtc fixxl sotrrccs, :'rs rvhcn bccs :rntl othcr insects that feed on pol-
individual predators, and such cases are often very suggestive of simple It'rr.urtl ncct:lr.sc:trclt lirr lL)\\'('r's, tlrt'1, "1'.' s<l snrlll and move so rapidly
conscious thinking on the part of the cooPerating animals. rlr.rt it is vt'r'\,tlillir'rrlt lo tlt't('rnul(' jrrst w'lt;rt sclrrclrirr;1 nl()vcnlcnts they
30 CbapterTwo l;iiliinq Food 3I
employ. But I suspect that when cognitive ethnologists become suffi- eral kinds of aquatic insects were abundant. At a prrrticular dung pat the
ciently disinhibited from the mindset that views all insects as genetically wagtail would usually caprure only one of thc lrrrgcr flics, and this dis-
prograrnmed clockwork, they will devise effective methods to monitor turbance would cause the others to scaffer inro thc grass. The bird
how insects go about searching for food. This in turn might disclose would then search for and catch many flies in thc inrnrcdiate vicinity.
that many species are at least as versatile as the bumblebees studied by At the start of a feeding session each bird hacl to dccide where to
Pyke. search for food, whether to join a flock of wagtails or hunt by itself, and
whether to concentrate on dung pats or on aquatic insccts at the shallow
pools of water on low-lying areas. The wagtails madc their choices with
Prey Selection by Starlings and Wagtails
considerable efficiency, so that they obtained approximately the maxi-
Birds rely primarily on vision to locate and capture food, and they are murn possible arnount of food with minimum expenditure of time and
easier to observe than many other animals. As a result, we know more cffort. This entailed concentrating their efforts where food was most
about their behavior in general, and their foraging in particular. In some plentiful and moving on when it became depleted. But these shifts were
cases they are obliged to make choices in their search for food that not rigidly programmed; they did not wait until every last fly had been
would seem likely to be facilitated by a linle simple thinking about the captured, but moved to richer sources rvhen the effort required to catch
possibilities available to them and the probable results of various alter- another fly became greater than that needed to move on. The shifts were
native courses of action. For example, a thorough study of a group of not random; the wagtails moved to other areas where insects were plen-
starlings in the Netherlands by I. M. Tinbergen (1981) revealed that tiful. These decisions seemed to be based on seeing the larger flies on
when feeding nesdings, they concentrated primarily on two species of fiesh dung pats. But the birds may well have also been influenced by
caterpillars, which were to be found in opposite directions from their memories of locations where they had found plentiful food in the recent
nests. This made it possible to tell from their initial flight direction past.
which of the two kinds of caterpillar they intended to gather. One of the Behavioral ecologists who analyze feeding tactics such as those of the
two species was preferred under most conditions, but the parents Oxford wagtails ordinarily avoid speculating about any possible think-
switched to the other when there was a pressing need for food, and ing on the bird's paft as it makes these decisions, which are important
especially when their broods were experimentally increased by placing lirr its survival and reproduction. But the multiple factors that must be
additional nesdings in their nest. These choices were made at or near t'r,aluated, ffid the unpredictable details of the feeding situations, would
the nest, where neither type of caterpillar was visible ; the starlings had sccm to render a little sirnple thinking helpful and therefore adaptive.
to remember in which direction to fly for each tyPe .
A clcar and reasonably representative example of the choices and de-
Illackbirds' Decisions about Feeding Ecology
ci.sions involvcd in feeding behavior stems from the studies of rwo spe-
cics <>f wagtails feeding on Port Meadows along the banks of the Isis A dctailed study of the behavioral ecology of marsh-nesting blackbirds
Rivcr in Oxford (Davies, 1977; Krebs and Davies, 1978). The pied hl, g.irrrr (1980) has revealed how many subde factors influence both
wagtail (Motacilla albo ya.ruellil) is a year-round resident of southern En- thc sclection of insect prey and the choice of mates and nesting territo-
gland, and the yellow wagtail (M. fl'ava f.awssima) is a migrant Present r ics. Thc redwinged blackbird (Ageloius pboeniceus) and the somewhat

only during the sulrlrner months. They were srudied early in the spring l;rrgcr yellowheaded blackbird (Xantbocepbnlus xanthocephalas) are
before they started to breed. At this time they were gathering food only .rlrundant breeding birds in the marshes of northwestern United States
for themselves, but were probably also putting on weight in preparation .urtl wcstcrn Canada, and they nest in sufficiendy open areas that most
for the nesting season that would follow in a few weeks. They were ,,1'thcir ft'cding behavior can bc observed relatively easily. Orians and
easily observed because the grass was heavlly grazed by catde and lris collclgucs c()rrc(:ntratcd on thc ncsting season when the parents are
horses, and the ntunerous dung pats provided food for the flies on rnrrlo'i{rc:lt prcssrrrc to otrt:rirr t'rtotrglt lixxl fbr thcir nesdings. This of
which the wagtails fed. Only one bird at a time fed on insects from a ( ( )lrrs(' is :r sitrrlrtiort rvltcrt' tt.tt ur'.tl sck'r't iort <lpcratcs p()wcrfully on the

single dung pat, but small groups often hunted at the pools where sev- lrrrtls'llt'lt.rvior'; lirr tltc rttuttlrt'r ol ltr'.tltlt1, l,orutg tlt;tt crut bc raiscd de-
32 Chapter Two hinding Food 33

pends directly on the alnount and quality of food their Parents caPture they are selecting territories. When the fcmalc.s :rrrivc they seem to ig-
and bring back to the nest. nore the vigorous displays of the males and instcad spcnd a great deal of
Both species of blackbirds nest in vegetation growing in shallow time at the edge of the water. Perhaps they arc l<xrking for the aquatic
larvae and nymphs of insects that will later cmerge as adults, but Orians
warer. The redwing is strongly territorial; in the spring the males arrive
first and establish territories that include an area of marsh or adjacent (1980) interprets his observations more conservatively in terms of veg-
upland. Up to a dozen females arrive later, and, after visiting several ctation patterns that indicate where aquatic insects are most likely to
male territbries, each female settles in one, mates with the territorial cmerge as adult forms. Few insect larvae occur where the stalks of
male, and builds her nest within his territory. The females do all the nest aquatic plants are closely spaced, but many can be expected to emerge
rrt the outer edges of such areas. Female blackbirds may be looking for
building, incubation of the egBS, and almost all the feeding of the nest-
signs of future food sources as they decide where to settle and build
Iings, although after the young have left the nest the males also feed
them. The yellowhead males do help feed their nestlings, but otherwise their nests.
the habits of the two species are similar. Both feed heavily on adults of Behavioral ecologists tend to assurne that some genetically deter-
aquatic insects that have just emerged from the water, but the redwings nrined action pattern guides these choices. They seldom allow them-
sclves to speculate about any possible thoughts of blackbirds that ex-
alio feed on insects they find on the dry upland areas. The larger yellow-
heads exclude redwings from both their nesting territories and from the
.rmine several marshy areas, and choose one only after devoting a
considerable amount of time. Might the birds think that certain types
richest sources of aquatic insects.
Marshes vary greatly in the abundance of the insects on which the of marshy vegetation are more likely than others to provide abundant
insects a few weeks laterl While we have at present no way to answer
blackbirds feed, and the density of nesting birds is roughly correlated
srrch a question, it is important to realize that it remains open and that
with insect abundance, although other factors also play a role. For ex-
ample, the yellowheaded blackbirds avoid areas with a continuous stand lirture investigations might provide at least a provisional answer.
of trees extending more than about 30 degrees above the horizon or, in For example, it might turn out after appropriate investigation that
one case, a marsh where tall cliffs rose abruptly from the water's edge. p:rrt of the male's display behavior communicates to females some such
nrcssage as "Lots of insects here." How could ethologists hope to test
The tendency to avoid nesting in such areas, even when insect food is
abundant, is probably related to the danger that hawks may select such rhis hypothesis| Experimental procedures have been developed that in-
tlicate which of several stimuli pigeons recognize as similar or different,
trccs tor thcir nests.
.rs will be discussed in detail in chapter 6. Although such experiments
lt is inrl'rorranr to recognize that the male blackbirds make extremely
Ir.rvc so far been limited to restricted laboratory siruations, they might
intlxrrr:rnt choiccs about nesting territories well before their young
h:rtch rurtl rccluire an abundant source of insect food. At this time very
lrc nrodified and extended to inquire of blackbirds whether certain as-
fl'w acluatic insects have emerged, so that the choice of a territory must pccts of a male's displays were judged to be similar to representations of
.rlrrrndant insects. If such experiments should yield positive results, cog-
bc guided by something other than the contemPorary abundance of in-
,..1r. Somehow they do ordinarily make appropriate choices, selecting nitivc ethologists would have obtained suggestive but significant evi-
tlt'ncc that the displays in question did convey a message relating to
out of extensive areas of marsh those localities that later produce the
ur,scct abundance.
richest harvest of aquatic and terrestrial insects. One might suppose that
these choices are guided by memory and tradition, the blackbirds After the young blackbirds have hatched, the mother, and in the case
simply remembering where they nested last year or where their Parents
,l'thc ycllowheads sometimes the father as well, have an extremely de-
rrr;urtling task of finding, catching, and carrying back to the nest a suffi-
raisid them. But these marshes change rapidly from year to year due to
( r('nt nr.rrnbcr <lf insects to feed their hungry young. The actual selection
ecological changes-such as variation in water level and invasion of
.rrrrl c:rptrrrc of inscct prcy is diflicult to srudy in detail, because many of
lakes 6y."rp-that drastically reduce the populations ofaquatic insects.
It seems thit they must have some mental rePresentation of a future tlrt' irrsccts rlrc snlrrll arrtl tlrc lrirtls crlnn()t always be approached closely
,'rr, rrrglr wlrilc tltcy rtrc li't'tlirrg l( ) ri('(' irrst whrrt thcy arc doing even with
Newly arrived blackbircls <>ftcn forage at the air-water interface whcn tlrt' .ritl ol'birtot'rrlrtrs. ( )ri.rrrs ,rrrrl lus tollt':tgut's ttsctl .scvcral ingcnious
34 Chapter Two Fiildinq Food 35

methods to determine what quantitics of different insects were taken. that on the coast of Cumbria they usc rw() prirrcip:'rl tcchniques for
One method was to place around thc neck of a nestling a loose collar opening mussel shells. When the musscls arc firlly cxposed the birds
formed from a soft pipecleaner, not tight enough to Prevent breathing scize them with their sturdy bills, pull thcm kxrsc from the substrate,
but sufficient to prevent swallowing of insects. The accumulation of in- rrnd carry them to a patch of sand where thcy turn thc shell so that its
sects in the nestling's mouth was then removed for analysis after it had flat ventral surface is uppermost. Even though this is not the most stable
been fed. This procedure showed that as many as ten insects might be lrosition, the oystercatcher maneuvers the musscl so that it remains ven-
delivered to a nestling on one return visit by its mother. tral surface up while hammering open the shcll. To determine what
Orians and his colleagues also learned by tedious observation and firrces were necessary for this operation, Norton-Griffiths built a
long practice to identify through binoculars many species of insects as rnussel-cracking machine, using a close copy of an oystercatcher bill as
they were captured by the blackbirds. Sometimes a bird carrying a large the pick. The flat ventral surface of the shell proved to be the most easily
load dropped what it had while pursuing and usually catching an addi- broken part. Each oystercatcher learned where the sand was suitably
tional insect, but in such cases it always picked up the previously gath- hard for this operation and brought nrunerous mussels to the sarne spot.
ered prey and then carried the whole lot back to its young.The foraging When mussels were covered by shallow water the oystercatchers
behavior of these blackbirds conformed at least approximately to exPec- ()pen them in an entirely different way. They search for slightly open
tations based on optimal foraging theories. These predict, for example, shclls and stab their bill into the opening. They do this in such a manner
that when gathering food close to the nest) birds should return more rhat they cut the large adductor muscle that closes the shell. After thus
often with smaller loads than when they are obliged to search for food rcndering the fleshy body of the mussel accessible, the oystercatcher
at greater distances. In the former case the return trips require less time rc:trs the shell loose from the substrate and carries it to some convenient
and energy. spot where it picks out the body of the mussel and eats it. At first this
The adult blackbirds must also feed themselves, and they usually ,liflcrence in fceding behavior appeared to be an adaptive adjustment to
swallow the first few insects captured on any one foraging trip before t ircumstances and opporrunity; if the mussel shell is tightly closed, as it
beginning to gather food for the young. The utilization of specific tyPes rs when fully exposed, it must be hammered open; but when the shell is
of insect prey differs to some extent according to the circumstances. slightly opened underwater, the stabbing technique is easier. When
When they are not feeding young, these blackbirds often eat dragon- Norton-Griffiths marked individual oystercatchers and observed their
flies. The available dragonflies were quite large and provide excellent lccding behavior, it turned out that each one specialized in one or
nutrition for the youngi and even when they were the first insect caught tlrc other procedure. Further study strongly indicated that the young
on a particular sortie the parent bird did not swallow them but carried ,r1'stcrcxtchers learned which technique to use when they began feeding
them back to the nest. What, if anything, do these busy Parents think as rvirh tl'reir parents. It seems clear that each bird learned only one of the
they devote most of their waking hours to gathering food for their hun- rrvo tcchniques, rather than simply playing out a genetically prescribed
gry young| Perhaps "Those youngsters need food," or "That dragonfly l).rrtcrn of behavior. In many other circumstances, however, birds and
will stop its squawking for a while." We cannot say, as yet; but these are .rlrcr active animals must employ a variety of food gathering and pro-
plausible inferences that should be kept in mind as hypotheses awaiting ( ('ssing actions according to the circumstances.
an adequate test.

l).rrwin's Finches
Oystercatchers' Mussel-opening Techniques
I lrt' linchc.s that inhabit the Galapagos Islands provide a classic case of
The oystercatcher (Haematopws ostralegus) is a large shore bird with a cvolrrtiorrrrry clivcrsification. Sometime within the past million years or
conspicuous red bill; it is rclatccl to thc sandpipers and plovers. Mussels \( ) .u'r :rnccstral poptrlati<>n cst:ttrlishcd itself on these dry volcanic is-
exposed at low tidc arc onc of thcir principal foods, but they also feed l.rrrrls, :rnrl its tlcsccntlu'rts cvolvt'tl irtto thirtccn species that range in size
on othcr shcllfish arrd orr curtl)w()rrns cxposed in plowed fields. The lr()nr k'ss th:rn l0 t<) nl()r'('tlr.rrr 40 gr:ulls. "l-lrcy wcrc collected by
Irnglish bch:rvior:tl ccok rgist Nortolt-(iriffi ths (1967 ., 1969) discovered (,lr.rlt's l).rrwirr:urtl tlrcir rtr'.ulr'(()ntnlrotts r':u'irrti<ln lcft him some-
36 Chapter Two l;inding Food. 37

what confused, so that it is not clear just how influential they were in several species of small birds have devclopctl thc hatrit of feeding on
his recognition of evolution by natural selection. The history, ecology, parasites that they pick offthe skin of largc nranrnrrrls.
and evolutionary biology of these birds has been recently reviewed au- These "vampire finches" direct their vig<>rous 1-rccking selectively at
thoritatively by Grant (1986). There are three groups of Galapagos the base of boobies' feathers, most often ncar thc elbow of the folded
finches, which can conveniendy be categorized as ground finches of the wing, drawing enough blood to drink. The b<xrbies try to dislodge the
genus Geospizn, tree finches of three genera, and the warbler finch Cer- birds, but the latter usually succeed in obtaining a blood meal by re-
thidae olivocea. The species differ most conspicuously in the size and peated attempts. This habit is well established on Wolf Island, but on
shape of the beak, and these differences are clearly correlated with feed- other islands where the same species has been thoroughly studied nu-
ing habits. Finches with short thick beaks feed on seeds, many of which merous boobies also nest without any sign of its occurrence. On Wolf
are too hard and tough to be cracked by the more slender beaks of other Island G. d.ifi.cilis also "push and kick seabird eggs against rocks, widen
species that specialize on insects. cracks that form in the she[, and then consurne the contents" (Grant
Darwin's finches live in a harsh environment where food is often very I986,393).
difficult to obtain, except after the occasional rains when vegetation While Galapagos finches are not the only birds with diversified and
and insects become much more abundant than during the usual dry per- ingenious feeding habits, they demonstrate rather clearly how much
iods. Their diet tends to be opportunistic; as Grant (1986, 393) sum- versatility is required to make a living under difficult conditions. The
marizes it: use of twigs as proving tools, and the selective pecking at the bases of
booby feathers to obtain a drink of blood are especially suggestive. It is
As a group, Darwin's Finches rip open rotting cactus pads, strip the bark off important to recognize that the same individual finches employ a wide
dead branches, kick over stones, probe flowers, rolled leaves, and cavities in variety of food-gathering techniques according to the circumstances, al-
trees, and search for arthropods on the exposed rocks of the shoreline at low though no one species exhibits the full range of feeding specializations
tide. They consurne nectar, pollen, leaves, buds, a host of arthropods, and seeds clisplayed by the Darrvin's finches as a group. We can only speculate
and fruits of various sizes. . . . By virtue of their deep beaks, and the masses and rbout the origin of feeding on booby blood, but when a finch pursuing
clispositions of the muscles that operate them, ground finches crush seeds at the cctoparasites that crawled deeper into the thick feathers perhaps acci-
basc of thc bill. In contrast, tree finches apply force at the tips of their bills to dcntally pecked hard enough to break the skin, was it pleasantly sur-
tlrc w<xx'ly tissucs of rwigs, branches, and bark, and thereby excavate hidden
prised to find a source of nutritious fluid| Did this perhaps remind it of
rrrtlrrol'r<xl prcy. . . . The warbler finch, cactus finches, . . . woodpecker finch,
ihe fluids to be found and eaten from inside cracked seabird eggsl
rurtl rn:ur11rovc linch have relatively long bills which they use to probe flowers
lirr ncctrrr or holcs in woody tissues for arthropods. To an inclusive behaviorist these are idle and foolish speculations, but
tlrey call to mind the extensive experiments of Tolman (1932, 1937)
In addition to these general tendencies to specialize on foods for rvith laboratory rats that seemed to be surprised when food they had
which their beaks are adapted, some of the Galapagos finches have c\rcry reason to expect to find at the end of a well-learned maze was not
highly specialized feeding habits. Woodpecker finches (Cnoospiza pal- lirrthcoming. Here we would be dealing with pleasant surprises rather
lid.n) artd mangrove finches (C. heli,obotes) hold twigs, cactus spines or than disappointments, but if and when methods are developed to test
r hc hypothetical inference of such simple but probably vivid mental ex-
the petioles of leaves in the beak and use them as tools to Pry arthropods
of various kinds out of crevices. On two small islands, Wolf (or Wen- pcriences, we will have learned something important about the animals
man) and Darwin (or Culpepper), about 100 km from other islands of r'onccrned.
the archipelago, the sharp-beaked ground finches (Geospiza d.fficilis)
have developed the most unusual habit of feeding on the blood of boob- Sc:rrching Imagcs
ies (genus Swln). This habit probably began as a mutually advantageous
feeding on ectoparasites; a related species of ground finch commonly Whcn l hrrngry rrnirrurl is scrrrching lirr fixrd under natural conditions it
eats ticks from the skin of marine iguanas some of which have ritualized n'orrltl u/:lstc :l grcllt tlc:tl ol'tirttt'rrrrtl t'lli)rt t() scrutinize every detail of
displays to solicit tick removal by the birds. In other pafts of the world tts sut'tlnrrrtlirrgs. lkrtlr t'r'olrtlr()n.rt 1' st'lt't'liott utrd lc:rrning ntust exeft a
38 ChapterTwo l.ind.ing Food 39

strong influence on searching behavior. Animals concentrate their atten- these shells, but gradually paid less and lcss :rmcntion to them. When
tion not only on things that look, sound, smell, or feel like food but also they were only occasionally turning ovcr nlu.sscl shclls, Crozr placed
on quite different things that are signs showing where food may be bait under some. When a crow found onc rhar was thus baited, itbegan
available. Specialized sensory systems are sometimes employed in rurning over many more. Under narural cr>nditions it is .o--orr-fot
searching for food. For example, some sharks detect the weak electric something to be a sign of food only some of the time. Animals learn
currents from the contractions of the heart or other muscles of prey that it pays to inspect such objecrs even though they yield food only
animals that would otherwise be very difficult to locate (Kalmeijn occasionally, md, when they do yield food, to search for similar objects.
1974). And insectivorous bats distinguish the sonar echoes of edible Similar behavior has also been observed in other animals, as reviewed in
insects from the many other echoes returning to their ears (Schnrlo'ler et the symposium edited by Kamil and Sargent (1981).
al. 1983; Osmrald et al. 1988). But most searching is based on vision, The signs of food availability may be difficult to recognize, for it is
olfaction, or hearing. obviously advantageous for porential prey to avoid easy detection. But
The basic idea of a searching image, or its equivalent, was discussed locating food is so crucial that many animals have developed not only
t-ry n'rany early ethologists, and in recent years detailed studies of forag- cfficient sensory mechanisms for distinguishing signs of food from very
ing birds have shown that thev look for particular patterns that reveal similar objects, but an ability to learn what is a fruitfirl searching image.
'fhis is well illustrated by the experiments of Pietrewic, arrd Kamil
whcrc fbod is to be found, such as the barely PercePtible oudine of a
crypticallv colored moth resting on the bark of a tree trunk (Pietrewicz (I9qI), who applied to bluejays instead of pigeons the type of operanr
:rrrrl Kirmil I98f ). In a wide variety of laboratory exPeriments, rats or conditioning procedures developed by psychologists. Naive bfuejays
ordinarily have nothing to do rvere adept at learning how to pick out cryptically colored moths resting
1'rigct>ns lcarn that visual pafterns which
with f<>od are now signals that food can be obtained. Somewhere in the on backgrounds very similar to their own appearance .
animal's brain there must be a mechanism for recognizing what are Animals cannot ordinarily predict what objects are likely to indicate
termed searching images. the presence of food, ffid an ability to learn about novel signs of food is
One of the most thorough and significant studies of searching im- useful to many species. An interesting example gre\,\,, out of the marking
ages was carried out by Harvey Croze (1970). On a sandy beach where ,f nest locations by ethologists. Ground nesting birds often lay eggs
carrion crows were gathering mussels at low tide he laid out a row of that resemble the substrate on which they are laid, and some conCeal
t hcir nests very effectively under vegetation. Having laboriously located
empty half mussel shells, convex side up, and beside each shell he placed
a small piece of beef. After five hours the crows had taken all the pieces. srrch nests, ethologists often mark their location by placing stakes a
The next day Croze laid out twenty-five mussel shells and under each short distance to one side, in order to facilitate finding them again. In
one he hid a similar piece of beef. When the crows rerurned they turned ,,nc study of nesting phalaropes and semipalmated sandpipers near
( lhurchill, Manitoba) many nests were marked by 50 cm stakes placed
over twenty-three of the shells and ate the meat. They had learned 2
quickly that mussel shells lying on the sand, which would ordinarily be to 3 meters southeast of each nest (Reynolds 1985). At least one sand-
empty, had suddenly become sources of tasty food. On the third day the lrill crane learned that these novel objects were signs of tasty food.
meat was buried in the sand underneath the shells. The crows turned l(cvnolds observed this bird searching diligently near nest markers, and
these shells over, but finding nothing directly under them dug with .rlthr>ugh nest predation was not observed directly, eggs were missing
their bills in the sand until they found and ate the meat. Although olfac- li',rrr ncsts ncar which there were perforations in the ground almost
tion is not well developed in birds, one cannot rule out the possibility t t'r't.rinly made by the bill of a probing crane. This use of completely
that crows could smell meat at close range, especially since pigeons can ttrtvcl scerchiltg images indicates how versatile birds can be in leaming
discriminate between different odors in laboratory experiments rvlr.rt tr> l<x>k fi>r u,hcn foraging.
(Schmidt-Koenig L979). But regardless of the sensory channel em-
ployed, these carrion crows had obviously learned quite rapidly that '
'it 'l rtctics
food might be buried in the satrd ttnclcr emPty mussel shells.
Crctze now continucd to phcc sinrilar musscl shells on thc bcach, bttt l'lrt' gt'rtrs l\rnrs int'ltrtlt's tlrt' Nortlr Arrrt'r'it';rrr chick:rrlccs and titmice,
witlrorrt llny rrrc:rt. For tilttc tltc cr()ws c<ltttitrttctl f() ttlrll ()vcr
s()r'r'lc llt,,st' .tt tolr.tlit .ttrtl ('!tt('rl.unrnll \'rsrtors t() tlrous.urrls ol-lrirtl fccders,
40 CbapterTwo Finding Food 4L

along with several European species known in England as tits. Because Except for failing to distinguish barkics conccaling mealworms or
these birds do well in captivity and display ingenious foraging behavior, bits of string, the great tits learned to foragc in thcse new types of insect
I. R. Krebs and others have studied the nanlre and efficiency of their hiding place; if mealworms were provided in one type of container but
feeding tactics when they search for insect prey. The stated purpose of not the others, they concentrated their fbraging on the type that had
these investigations was to test mathematical theories about optimal yielded food. Individual great tits speciahzed in particular methods of
foraging behavior. Although the investigators did not admit to any in- extracting the mealworms. Some concenrrated on the hoppies, rurning
terest in whatever thoughts and feelings the birds might have experi- over the pieces of paper much as wild birds rurn over leaves lying on rhe
enced, their findings provide suggestive hints. ground, and peering into the container. Others wallowed in the con-
In one set of experiments Krebs, MacRoberts, and Cullen (L972), tainer and threw out the pieces of paper. one discovered that by peck-
Krebs and Davies (1978), and Krebs (1979) studied how great tits (Pa- ing through the masking tape he could peer into the container and see
rus rnajor) coped with the challenging problems of foraging for con- whether a mealworm was present. Some opened the milkies by ham-
cealed food. In order to standardize experimental conditions Krebs and mering through the tape, while others pulled away one edge of the tape.
his colleagues did not study the capture of normal insect prey hidden on These individually varying panerns showed that foraging is nor a
natural vegetation. Instead they used mealworms (larvae of the flour fixed, stereotyped pattern, ffid suggest that each bird was trying various
beetle), which are about 3 mm in diameter and about 25 mm long. rrctions in its efficrts to find concealed food. When one bird was allowed
M*y insectivorous animals eat them avidly in captivity. To analyze to discover that a particular container contained a mealworm, others
both how the tits would learn to find mealworms hidden in different housed in the sarne cage also began to look in similar places or similar
ways, and how several hungry birds foraging in the salne area would containers. In short, these great tits learned a great deal about where to
interact, four types of hiding places were employed: plastic cups called find concealed food in this novel situation both by remembering where
"hoppies"; pingpong balls cut in half, called "pingies"; 7.5 x 4.5 x .urd in what sort of hiding place they had found mealworms, and by
4.5 cm blocks of wood termed "milkies" with I.5 cm holes drilled 2 cm observing where other birds found them. Once a food source had been
deep into their tops; and "barkies," consisting of small strips of masking itlcntified, the dominant bird of a group would chase others away from
tape stuck on trunks of artificial "trees" constmcted from wooden dow- it and take more food in a given time than the subordinates.
els. Under the tape there might be a mealworm forming a small b*p. The versatility of insectivorous birds in finding hidden food items
The milkies were designed to simulate milk bottles, which wild tits had lcrl to a spectacular development in the 1930s, when nvo species of tits
learned some years earlier to open by tearing offthe thin metal foil used tliscovered that milk botdes delivered to British doorsteps could be
to cover their tops, as discussed below. ,pcned by pulling the metal foil off the tops of the botde (Fisher and
The first three types of container were filled with sawdust or bits of I Iinde 1949; Hinde and Fisher 1951). At that time the milk was not
paper and the openings were covered with masking tape. Only some Ir<rnrogenrzed, and the tits could drink the thick crearn from the top of
contained mealworms, so that the birds had to open them to find t hc l'rottle. Careful studies were made of the gradual spread of this be-

whether they were or were not sources of food. To prepare the birds for lr.rvior throughout much of England until a change in the technology
this new type of foraging they were first given uncovered mealworms, ,l'covering milk bottles eventually deprived the birds of this source of
then mealworms buried in sawdust in the sarne containers but not cov- lootl. While the matter was not studied direcdy, it seemed at the time
ered with masking tape, and, finally, covered containers. They learned vt'r1' likely that increasing numbers of tits took up this habit by obser-
surprisingly quickly that they could sometimes find food by pecking r .rt ion:rl lcarning-seeing that another bird had found food in a novel
through and tearing offthe tape. Some of the barkies consisted of short sort of 1'rlacc, just as the experiments of Krebs and his colleagues showed
pieces of thick string covered with tape, but the birds never learned to tlrt'y cottkl tlo under contr<>llcd conditions. Many behaviorists are sus-
discriminate between masking tape with bumps formed by mealworms l)tr iotts of-sttch suggcstivc cvitlcrrcc filr observational learning, however,
or bits of string. All these experimental arrangements were designed to .rs t't't't'ntlv rcvicwctl hy (ielcl'( lgttlt) rvlro corr.sidcrs it "an onerous con-
simulate the task faced by birds when they search through large areas of .t'1tt":rrrtl PI'clt'rs rcnns sttt'lr .rs sot'i:rl lircilitetiorr uscd by many of the
vegetation fbr thosc fcw s1'r<lts whcrc somcthing cdible can be uncov- r',rr lv ct lrologists :rrrtl .rtlr', rt'.rtt'tl r ('( ('nl11, lr1, ( )l.rytorr ( l97tt). S<lcial fhcil-
crccl by prot'ring or ptrllirrg offlrtycrs of-t'rerk. tl.tll()n is tlrt'slirttttl.tliott lr1'otlrt'r .rrrrrrr.rls tlr.rt t.lus('s.t givcn lurirllrl t<>
42 CbapterTwo t"inding Food 43

perform a paftern of behavior that it had already performed on other food source. other tits presumably pickcd tr1'r thc habit by watching
occasions. It differs from observational learning in that no new or mod- their companions, as in the experiments of Krclrs and his colleagues.
ified behavior is learned by observing another animal, ffid it seems to This is probably typical of innovation by animals; they learn that appty-
avoid the implication of conscious copying, although either effect ing familiar motor patterns to new objects or in novel situati,ons
might be facilitated by conscious realization of its appropriateness. It is achieves a desired result or avoids an unpleasant one.
difficult, however, to dismiss some evidence for learning by observation, To what extent does the novelty in applying well-established actions
such as examples discussed in chapter I I involving cetaceans and pri- to new situations indicate conscious thinkingf The degree of novelry is
mates, and especially the observations of Boesch (199I) of active teach- surely an important factor, for the essence of the distinction benveen
ing by chimpanzees. Palmeta and Lefebvre (1985) and Lefebvre and social facilitation and true observational learning is that in the former
Palmeta (1988) have demonstrated that pigeons can learn a novel food- case the presence, or sometimes the food getting, of one or more other

gathering technique by watching other pigeons obtain food in this way. rrnimals elicits a form of behavior already familiar to the animal in ques-
The basic motions used by tits to open milk botdes were much the tion. Although inclusive behaviorists are so averse to considering con-
sarne as those used to pull layers of bark from vegetation. Recognition scious thinking that they seldom phrase the distinction in such terms,
of this similarity has led many to disparage the discovery that milk rvhat they seem really ro mean by true imitation, which Galef finds "an
botdes were a source of food as not so novel after all. Indeed it was not onerous concept," is the conscious copying of another animal's behav-
the development of a whole new motor pattern, but it was a case of ior. How might one hope to detect conscious imitationf Possibly this
versatile application of a previously well-developed type of action to a rnight be accomplished by some form of communication in which the
new and wholly different situation. This is typical of the interplay of irnitating animal conveyed to others (and thus potentially to eavesdrop-
ideas about animal behavior that has characterized advances in ethology. ping cognitive ethologists) the basic thought of getting food by some
Some see novel behavior as evidence of radical inventiveness) a sudden rxrvel form of behavior. Nothing of the kind has been observed ro date,
insight that some completely new type of behavior will yield a desired but it would be worthwhile to keep an open mind about such possibili-
result. Others note that the same limbs are moved in ways that are not t ics.
very different from other long established pafferns of behavior, and
pooh-pooh the animal's performance as nothing new. Sherry and Galef
(1984, 1990) have studied the acquisition of very similar milk-botde- l)ropping Shellfish on Hard Surfaces
opening behavior in captive chickadees (Paras atricnpillws), close rela-
tives of the British tits studied by Fisher and Hinde. They found that An cnterprising sort of behavior carried out quite often by herring gulls
some chickadees learned this novel method of obtaining food on their is t() carry clams, whelks, or other shellfish to some hard surface on
own, but that they are more likely to do so if they could see another rvhich they are dropped from a height of several merers. Similar behav-
chickadee in an adjacent cage. But they were about equally likely to ac- r,r' has been observed in other birds, including crows; but it has been
t horoughly srudied in herring gulls. This process is quite different from
quire the new behavior whether or not the other bird opened a milk
bottle. This supports Galef's general view that learning by imitation is lirrrling food, seizing it, breaking it up, and swallowing. A potential
rare or nonexistent in animals, and that social facilitation is a more par- lrxrtl itcm must first be recognized as something that becomes edible
simonious explanation of cases like the milk bonle opening by British ,rrl1, q,[sn its outer shell is broken. Then the bird must pick it up, fly
tits in the I930s. *'ith it to a suitable place, and drop it from a sufficient height. In some
There are elements of accuracy to both views. The tits certainly did .rr(':ls cthologists have reported that gulls are not selective and drop
not comprehend the nature of milk bottles, the properties of glass and slrt'lllish on s<lft surfaccs whcre they do not break. But it is a corunon
, rlrst'r'r':ltion th:rt hcrring gtrlls drop the great majority of the shells they
metal foil, or the nature and source of cream. But in hungrily exploring
the envirorunent of village streets, sidewalks, and doorsteps, they found t.rn'\'on r<>cks, rrxttls, p:rrking l()ts ()r othcr placcs where the shells do
that pulling off a sheet of shiny, pliable stuff allowed them to get at a l,rt'.tk. 'l'ltc :tcctttttullttiott ol'lrt',rkt'rr slrt'll li.rgrncnts can often be found
r ollt('nlt'.tlcrl .tkllrg
new and tasty sort of licluid f<xrd; ancl they went on to exploit tl'ris new l).ltlr( ttl.u strt'tr lrt's ol'.r p:tvctl rrxrtl. In tidal estu-
44 Cbapter Two r^inding Food 45

aries consisting of sand flats and salt nrarsh with very few rocks, those between approximately three and eight nrctcrs. ()nly about one in four
few are sometimes surrounded by a hal<> of clamshell fragments. drops broke the shell, so that many had to bc ;rickcd up and dropped
Beck (1980, l9S2) srudied shell dropping by herring gulls on the over and over again. Unless they were disturbcd, the crows persisted
shores of Cape Cod, Massachusetts. These birds picked Yq :lTt, until the shell finally broke, which sometimcs took as many as twenty
whelks, or empty mollusk shells inhabited by hermit crabs which they drops. Why didn't they fly higher so that shclls would be more likely to
found at low tide, and carried them for distances on the order of 30 to break? Zach's observation suggested that the crows had some difficulty
200 meters to rocky areas, sea walls, and paved roads or parkinB areas. in seeing where the whelk had fallen, md after dropping one they de-
scended in such a way that it seemed that they were watching the trajec-
Beck observed that the gollt usually flew quite low over the beaches so
that during all but the lait part of each flight they could not see the hard tory of the falling shell. \Mhen an occasional whelk was dropped from a
surfaces tJward which they were flying. They had evidently learned greater height it also seemed more likely to shatter into several frag-
where to take shellfish for this PurPose. In one area 90 Percent of the ments, making it more difficult for the gulls to locate and pick up all the
drops were directed at a Particular sea wall which occupied only about soft parts. Perhaps it was less pleasant to eat whelks containing small
I percent of the area over which the gulls flew. bits of broken shell. This was indicated by the fact that crows sometimes
Beck also observed that when dropping shells on this relatively small dipped broken whelks into freshwater pools before eating them, appar-
sea wall the gulls dropped them from lower altitudes than when using a
cntly removing fragments of shell.
large parkinlg lot. Perhaps they realized that there was no danger of Only a small fraction of the crows collected whelks and dropped
likely to break them on rocks, so that this specialized feeding behavior had presumably
-iirirrg this-larget trtg.i and that the shells were more developed quite recently. The initial stages of crows' discovery of this
from a"greater height. Shells did not always break, and the gulls often
picked ip * unbroken shell and tried $ai*. Beck also observed that type of feeding and its spreading to other birds have not been studied.
yor,rg herring gulls were less successfirl than adults; they dropped llut Zach did observe some individual differences. For example, one
iath.i few shellfish, but often carried up and dropped other objects, crow picked up and dropped rwo whelks simultaneously, although all
rhe others carried only one at a time. Such individual variability sug-
apparently in play. We have no detailed data, however, concerning th"
development of shell-dropping behavior. scsts that the birds had tried different tactics and were gradually learn-
Other studies by Zach (19i8) showed that a particular population of ing which ones were most effective.
crows nesring on an island near the coast of British Columbia had de-
veloped the f,abit of gathering whelks at low tide and dropping them ( )rrches
on particular rocky wheri they often broke so that the crows could
".""r M:rny animals store excess food when it is abundant. Curio (1976,22-
eat the soft parts. Each pair of crows foraged at one section of beach
and dropped whelks on I particular rocky area. Not all rocks were aP- 25) describes how numerous predators store captured prey for later
t onsumption. Often when a hungry animal finds an abundance of food
propriate, b.."or. if they were too close to the water the whelks would
boor.. off and sink. If the rocks were not fairly level, edible fragments it stores more than when the sarne food is located after it has eaten its
fetl into deep crevices where they were also lost._From a range of sizes lill. might be due to thinking about future needs even when satis-
of whelks tli. .ro*t selected the larger ones and they did not pick up Iyirrt its immediate hunger. Under natural conditions much of this
srorcrl ft>od is recovered and eaten later, but by no means all. Other
dead whelks or emPty shells.
.rrrinr:rls takc some, ffid the animal that stored it in the first place does
Zach studied the'selection process by sruffing emPty whelk shells
either with very tight material or with something similar in density to rrot :rlrv:rys rctrieve it. But a substantial fraction is recovered, by some
\l)t't'ics rrt lcast, often aftcr itrtervals of weeks or months.
the tiving motlusk. He then glued back in place_ the horny op_erculum
that closls the shells and found that the crow selected shells of normal .\tluirrcls arc thc rl()st fhnriliar arrimals that store food, but there has
weight or density. Presumably a lightweight shell would ordinarily Irt't'n t'onsitlcrltrlc unccrt:rinl1, 1* t<l how thcy recover buried nuts.
(..rlr.rl.urc (1942) conr'ltrtk'rl tlr.rt \\'('st('r'n lirx srluirrcls do not retrieve
*.it, a shriveled corpse rathcr than a frcsh ancl edible morsel.
Zach obscrvcd that thc cr()ws tlr<>prpcd whclks from heights ranging l,urrt.rl rrrrts lrY nr('nlory lrrrt lrl,srrrcllirrg rlrt'rrr. Lcwis (1980) rcached
46 Chapter Two I;inding Food. 47

similar conclusions, and it has also been suggested that, rather than re- irt a large aviary had to be remembered. [n firrthcr cxpcriments of the
membering where they stored nuts,, squirrels notice signs of the ground sarne general type Shettleworth and Krcb.s fotrnd that marsh tits re-
having been disturbed. More recently, however, McQuade, Williams, rncmbered quite well where they had storcd scccls. F'urthermore, when
and Eichenbaum (1986), Jacobs (1989), and ]acobs and Liman (1991) storing additional seeds they usually avoidcd thosc hiding places where
found that captive gray squirrels did remember the location of some of rlrey had recendy placed a seed. Evidently marsh tits specialize instoring
the food they had stored in a large cage. It remains to be determined :urd retrieving seeds, and they are probably much better at this task than
what role memory plays under natural conditions. r)lany other species.
Birds have provided stronger evidence of recovery of stored food by An even more impressive example of memory for food caches has
means of a detailed memory (Kallander and Smith 1990). Experimental bcen provided by studies of ClarlCs nutcracker, a relative of the crows
studies of marsh tits by ethologists at Oxford University have been es- .rnd jays, which lives in alpine environments in western North America.
pecially revealing. These birds are very similar to North American Ir<rcd is very scarce during long cold winters, but during the aununn
chickadees but at bird feeders they must compete with more species of thcse birds gather enormous numbers of pine seeds and store them in
birds that eat similar foods. As reviewed by Shettleworth (1983) ard ,'rcvices or bury them in the ground. This behavior has been srudied in
Sherry (1984), two other tits of the genus Parus, the great tit and the tlctail by Balda (f980), Vander Wall and Balda (1981), Vander Wall
blue tit tend to eat rapidly when peanuts or other desirable seeds are 1 1990), and Balda and Tirrek (1984). When seeds are plentifirl a single

available. Marsh tits, on the other hand, tend to grab single seeds, fly hird may hide as many as 33,000 during the fall. Each cache conrains
away, store them, and quickly return for repeated storing of individual ,,rdinarily two to five seeds. To obtain enough food to survive through
seeds in different places. They do return to the hiding places and recover .r typical snowy winter it is estimated that the Clark's nutcracker must
r t'l<rcate approximately a thousand of its caches.
many, but not all, of these seeds.
Cowie, Krebs, and Sherry (I98I) studied the caching behavior of In order to study this remarkable type of memory under better con-
r r'olled conditions, captive nutcrackers were allowed to bury pine seeds
marsh tits under natural conditions by radioactively tagging sunflower
seeds and detecting their hiding places with a scintillation counter. They rrr sand spread over the floors of a large aviary cage. After being kept
found that stored seeds disappeared much more rapidly than control ,trt of the cage for a month, a nutcracker recovered and consumed a
seeds stored in very sirnilar sites by the experimenters. This suggested, srrtr.stantial fraction of these seeds. To be sure, some seeds could be
although it did not rigorously prove, that the birds were recovering l,und by random searching, and when the experimenters buried nu-
seeds with reasonable efficiency. nrcr()us seeds themselves, the bird found a few. But the nutcracker
Turning to laboratory experiments where conditions could be better l,rrrnd many more of the seeds it had stored itself. Had it been using
controlled, Sherry, Krebs., and Cowie (I98I) allowed captive marsh tits ,,,krr or some other cue than its memory, it would presumably have
to store several hundred seeds per day in a large aviary. The birds recov- I't'crr cqually able to find both kinds of seed. The cage was provided with
ered stored sunflower seeds at far higher than chance levels after being ,,,ns1'ricuous logs and stones on the floor. The nutcracker buried most
, rl' its seeds in the sand near such landmarks, and its success at finding
kept out of the aviary for twenty-four hours. To control for other Pos-
sibilities, such as having preferred types of place to store seeds and look- tlrt'nr was greater than when no such landmarks were made available.
ing for such places when searching, these experimenters took advantage lhrt whcn the stones or logs were shifted during the month that the bird
of the fact that in birds visual information is processed and stored al- rr'.rs n<)t allowed in the cage, it would usually search near a certain part

most exclusively on the opposite side of the brain from the eye where it ,,1 .r log as if it remembered the location of each cache in relation to this

is received. They covered one eye of experimental marsh tits and found l.rrgc rrnd conspicuous object. Its recovery rate was verylow after the
that this treatment did not affect their rate of recovering stored seeds. l.rrrtlrrurrks had been shifted.
But if the blindfold was shifted from one eye to the other after seeds had I lntlcr tratttral conditi<>rts thc cnvironment where seeds are hidden
been stored, the birds located seeds only at approximately a chance level. ,lt.ttt11t's rlr:rstically drrrirrg tlrc wintcr rrs lcavcs fall and the ground is
This greatly strengthened the cvidence that they were remembering spe- ,llt'rl t'ovcrcd with sttow.'l'lrt'rtutt'r':rt'kcr nrust rcmcmbcr at least ap-
cific locations whcrc scccls \.\,'crc storccl cvcn when dozens of strch places l,t oxirtt:llt' k x':ttiolts wit lt n'lt'r ('n( (' to r t'l.rt ivcl1, llrrgc rurtl constant land-
48 Chapter Two

marks such as trees or sizable rocks. Ficld studies have shown that nut- CHAPTER THREE
crackers do search even under the snow in more or less the right general
Iocations where they have stored seeds. Presumably they remember a
large number of such locations, and they may lookat them from time to
ti1{e as leaves fall and snow arrives to reinforce their maplike memories. Predntion,
When it is important for birds and other animals to remember a large
number of deiails, th.y are often able to do so. To what extent they
rhink consciously about this task is another and more difficult question.
They can be regirded as thoughtless memory machines, but, as in other
.*r., of this sort, simple conscious thinking about the task may well be
he complex and often dramatic interactions of actively mobile
predators and their elusive prey provide many suggestive insights into
what life is like for the participants in this all-important phase of their
lives. For the predator, the location and pursuit of appropriate prey calls
tirr tactics that can be rapidly adjusted to changing and often unpredict-
:rt'rle circumstances. Although success or failure in a particular hunt is
rt<>t ordinarily crucial for the predator, its survival and reproduction de-
pcnd on succeeding reasonably often. Prey animals must adjust their
bchavior in many ways, especially to balance rhe need for food against
the dangers of predation. For them, each encounter is literally a matter
,rf life or death. The challenges of catching prey and escaping caprure
.rrc just the sort of situations where conscious thinking may be most
Itclpful. When predation is studied carefully under natural conditions it
oltcn turns out that the animals adjust their behavior with an adaptive
vcrsatility that suggests simple thinking about the likely results of vari-
( )us behavior patterns among which they must make split-second

behavior of predators and prey has come under strong selective
l)r'cssure in the course of their evolutionary history. Predation and ef-
lirrts to escape are widespread among animals, and some of the most
r lrought-provoking examples suggesting conscious thinking have been

,lcscribed among animals that we do not ordinarily consider especially

r t't'srrtile or intel[gent. Out of the thousands of speiies of predators that
( .t[)turc cven larger numbers of other animals under natural conditions,

rt lr:ts bcctr nccessary to select for this discussion a few specific cases
rvlrcrc thc bchavior of both prcdators and prey has been described thor-
, rrrglrll, cnough to pr<lvidc :l rci'ls()nlbly clear picture of their respective

t.tttit's. Mtrclt of this sct'tiort is l'r.tsctl on rrn cxccllcnt monograph by

( 'ttr ir t ( l()76).

50 Chapter Three Predation 5l
school, which usually then moved farthcr frorn thc pikc than it had been
Pike and Minnows before the inspection. When a single minnow contluctcd an inspection
The predator avoidance behavior of small fish, especially species that it usually moved from the edge to the cenrcr of rhc school on rejoining
aggregate into compact schools, has often been interpreted in terms of it. Earlier experiments had shown that minnows havc some difficulty in
stereotyped instinctive reactions. These interactions between predatory recognizing pike; they approach both realistic and crude model pike,
fish and their prey has been reviewed by Noakes (1983) and Helfman but resume feeding if the model does nor resemble a real pike . During
(1988). As emphasized by Magurran (1986), there is actually a great inspections, the minnows avoided the most dangerous zone immedi-
deal of individual variability in fish behavior, and this variability often ately around the pike's mourh. This behavior strongly suggesrs that the
involves adaptation to specific local situations. Variation is the raw ma- inspecting minnows are aware the pike is a danger and are seeking to
terial on which evolutionary selection operates, and recent sociobiol- find out whether it is acrually a predator and also how likely it ii to
ogical theories have accounted for alternative behavioral strategies that attack.
are effective and adaptive for different members of a given species. For In these experimenrs the pike often began ro stalk the minnow
example, sticklebacks from lakes where pike are present are much more schools by slowly approaching them. In addition to simply swimming
timid in the presence of pike than others from waters that have no large ilway from the pike, the minnows react to a stalking or attacking pike by
fish predators (Huntingford 1982). In waters where herons are impor- cmploying several quite different tactics. One response is for one or
tant predators the sticklebacks spend more oftheir time near the bottom rnore members of the school to "skitter" by accelerating rapidly for one
(Huntingford and Giles 1987). Coho salmon also adjust their feeding to five body lengths, often moving away from the school and then re-
behavior in accordance with the availability of food and the risk of pred- turning to take up a new position. Sometimes there is a more vigorous
ation (Dill 1983). Groups of goldfish tend to search for food near to :urd synchronized "group jump" during which the school moves rapidly
where other goldfish are feeding, but not near to groups that are not .urd vertically to a new position. It seemed unpredictable to the investi-
gathering food (Pitcher and House 1987). gators (and presumably also to the pike) which of these tactics would
The interactions of pike and minnows involve especially significant lrc employed in a given instance, a kind of "protean behavior" discussed
adaptive variability, as revealed by the detailed field and laboratory in- lry Driver and Humphries (1988). Another form of antipredator behav-
vestigations of T ]. Pitcher, A. E. Magurran, md their colleagues. i.r performed by large schools is to open up a space roughly five min-
These minnows are about 8 cm in length, and they spend much of their now body lengths in size around the pike as ir moves into the school,
t hcn close around it as it enters the open space and thus form a minnow-
tirrrc fbeding singly or in small groups spaced some distance apart.
l'itchcr (1986) advocates using the term "shoal" for groups of fishes lcss "vacuole" surrounding the predator.
that rcn'lain together for social reasons, and "school" for those shoals in Still another comrnon maneuver is for the school of minnows to
which swimming movements are synchronized and polarized, that is, srvim rapidly ahead of the approaching pike, then separare inro rwo
all fish head in nearly the same direction. tlr()ups that turn toward the predator's tail as it passes. This "fountain"
When a 20-30 cm pike was introduced into a 1.5 x 2 meter tank r)lrll)euver may also occur if the school meets a diver or fishing gear. As
where twenty minnows had been living for some time, the minnows' Mrrgurran and Pitcher (L987,453,460) describe the behavior, "escap-
first response was to stop feeding and come together into a compact rng fish keep one eye on the object or predator they are avoiding while
school, each fish about one-half to two body lengths from its neighbors rrrlintaining a swimming track of approximately I55 degrees to its cur-
r cnt position. This causes the school to split into two. By then reducing
(Pitcher, Green, and Magurran 1986). Earlier investigations had dem-
r lrt' :rnglc of their swimming track to maintain visual contact with the
onstrated that minnows in such schools are less vulnerable to predators.
But then, at intervals of three or four minutes, some individual min- ,lricct, thc fish automatically come together in a shoal behind it." When
nows or small groups began inspection behavior. They swam away from . k rscly apprr>achccl or actullly amacked by the pike the schools some-
the school and approached to within four to six body lengths of the rirrrcs cxhit'rit l "fla.sh cx1'r:ursior'r" in which thc fish appear to explode by
pike, paused for about a second, and then swam back to rejoin the srvirnnrirrg r:rPitllv irr .rll tlirt't tiorrs :rrv:ry liorn thc ccntcr of the school.
52 Chapter Three Pred.ation 53

Finally, after a school has split up, individual minnows often seek cover Drowning Prey
between pebbles at the bottom of the tank or under vegetation. Pike
counter this tactic by "vigorous affemPts to flush minnows out from Predatory birds strike or seize their prey and in almost all cases kill it
their hiding places by directing jets of water towards them." with the beak or talons. But in a fcw rare cases when a prey animal is
Similar interactions between other predatory fish and the smaller too large to be subdued easily it is held under water unril it drowns.
fishes on which they feed have been observed under natural conditions. Meinertzhagen (1959, 48) described such behavior by white pelicans
For example, Helfman (1989) has recently reported a series of experi- (Pelecanws onochrotnlws) in the zoological gardens near Cairo "where
ments on the responses of a small Caribbean reef fish, the threespot many wild duck take refuge by day, this pelican can be seen sidling up
damselfish, to presentations of models of a local predator, the Atlantic to a teal, suddenly seizing it, holding it under water until drowned and
trumpetfish. These experiments were conducted at depths of two to ten then swallowing it."
meters near coral reefs by Scuba or snorkel divers who moved a large or Two firsthand observations of prey drowning by hawks have been
small model trumpetfish toward the damselfish in either a vertical or supported by published photographs. In the first case a fcmale marsh
horizontal orientation. Tirrmpetfish were observed to strike at Prey hawk or marsh harrier flying low over a marshy area stmck a common
more often when in a head-down vertical position. Large and vertically gallinule and fastened her talons in its back. As described by Fitzpatrick
oriented models were more likely than smaller or horizontally oriented (1979), "instead of carrying the gallinule off, she pushed it down into
models to elicit escape behavior, including entering refuges in the coral. the water which varies in depth from 2 to I0 inches in this particular
Helfman describes several other cases where prey animals exhibit what area. After submerging the gallinule, the Marsh Hawk remained up-
he calls a "threat-sensitive predator avoidance." As a conventionally cau- right with the water midway up her breast . . . for approximately the
tious ethologist he refrains from any speculations as to conscious intent; next ten minutes. She occasionally flapped her wings and brought the
but the fish he and others have studied certainly behaved as though gallinule up out of the water. Each time it was brought up while still
aware of differences between threatening and nonthreatening predators :rlive, the gallinule thrashed about, whereupon the hawk would sub-
and reacted appropriately. rnerge it." Only after it ceased moving did the marsh hawk drag her prey
The overall impression that can be drawn from this series of appro- about four feet to an exposed stump and eat portions of it.
priate maneuvers by predatory and prey species of fish is that the former In the second case a Cooper's hawk had seized a starling but had
ire actively trying to catch the latter, and that the potential prey are well difficulty in killing it. As described by Grieg (L979), "I had watched the
aware of the danger. On seeing a real or model pike, minnows stop feed- hawk struggle with the Starling for several minutes no apparent
ing and aggregate into schools; individual minnows approach and in- success rn some underbrush. The hawk was aware of my presence and
spect the pike from what seems to be a relatively safe distance; and when u,as moving away from me and staying well hidden, but then to my
approached or attacked the minnows adopt a variety of evasive maneu- surprise it carried the violently struggling Starling out into the open
vers that are often effective. Damselfish also approach model tnrmPet- tlirectly in front of me, no more than 40 feet away, and into a depression
fish on some occasions, but both Prey sPecies avoid the head and mouth rvhere several inches of rainwater had collected. Once in the water with
regions of the larger fish. One can posnrlate a complex network of in- rhc Starling, the hawk merely stood on top of it, and when the Starling
stihctive reflexes to account for the observed behavior, complete with n,ould struggle to raise its head and a wing out of the water, the hawk
random noise generators at strategic points to explain unpredictable se- u'ould shift its feet so that it would push the Starling's head back under
r lrc surface." After the starling had ceased struggling the hawk carried it
quences. But the "ad hocery" of such schemes increases in ProPortion
tb the completeness of our understanding of the natural behavior. It .r\v:ly. In this case the observer's presence may have disturbed the hawk
thus becomes increasingly plausible, and more parsimonious, to infer r() s()nlc cxtent, but not enough to prevent it from dispatching and car-
that both pike and minnows think in simple conscious terms about their rvirrg offits prey.
all important efficrts to catch elusivc food or to escape from a threaten- (irccn, Ashfirrcl, end I Irrrtridgc ( 1988) obse rved a sparrowhawk that
ing predator. ,lroppctl to tlrc srrrl:rcc ol'tlrc \\':llcr':rltcr scizing a lapwing in flight. The
54 ChapterThree
l'nirrtirtrt 55

watching for approaching predators. As rcvicwctl lry Hg.rr' ([989;, 1xr-

lapwing was held under water for about three minutes and then carried
dead. Knowing nothing of the previous history of these
tential prey animals such as torrunies spcnd nl()rc tilrrc aplxlrct)tly
"pi'rrently watching for predators when they are in small gr()u[)s thrrn whcn nrany
hawks, we can only speculati about how such behavior might l.rave
are within view of each other. Elgar stresscs that mlny othcr fhct<>rs
arisen, or how, ot *t.tner, they calne to realize that holding a bird
underwater would quiet or kili it. But it does provide a thought-
influence time spent in "predator vigilancei' but it sccrns clcar that such
watchful behavior helps avoid predation and that othcr gr()up mcmbers
provoking exampt. of u.ttrtile inventiveness. An anon-ymous reviewer
benefit when one notices a sign of danger.
tf .ni, bSok hai raised the interesting quesdon whether a hawk that When a tommy sees something unusual or suspicious it becomes ob-
customarily captures both fishes and air-breathing birds or mammals
viously alert; it holds its head high, the ears pointed forward, muscles
might know enough to subd,ue the latter but not the former by holding
tensed, and it looks toward whatever has aroused its attention. Some-
th; underwat...i k ro* of no data bearing on this possibility, but en- times a tornmy in this siruation stamps on the ground with a foreleg,
terprising ethologists might keep it in mind for future investigations'
:rnd often it emits a soft snort which Walther describes as a "quiff."
Quiffs seem to occur only or at least primarily when something has
Predation on the East African Plains :rlerted the tommy, and they cause others to assune the alert posture
.urd look in the sarne direction.
The most abundant antelopes of East Africa are the Thompso.n's. ga-
zelles, or tommies, which aie p..yed uPon by m{Y carnivores,
indud- When a serious attack does occur, the tommies flee at a steady gallop
rvhich can attain speeds of 45 to 60 km per hour. This is faster than any
i.g t."ptrds, lioni, cheetahs,-hyenas, ffid wild do-g:' Ytlfitr (1969) of their predators can run except for a very short distance in an initial
*? o,n..s have been able to observe many details of the behavior of the t'harge. But tommies often run in other ways, including stotting, in
l0 to 15 kitogram tonrmies, because they live in oPe.n country where
of rvhich they jump a meter or so into the air, holding their legs relatively
they can be w-atched througirout the day without serious alteration
they migrating, thty stiff. Stotting usually occurs at the start of a chase, but only when the
their normal activities. Ouiing periods when are
live in mixed herds with torrghty equal numbers of males and females' l)ursuer is not too close, and at the end when the predator has given up.
When a herd of tommies is closely pursued, most or all of them bounce
But when they remain in ori most herds consist of femdes and
"..", .rbout in an irregular fashion, and this behavior seems to confuse many
their young together with subadult males or "bachelors'" The adult
bucks'defe"a i"liuiaual territories roughly I00 to 200 meters in diam- lrrcdators and hinder their concentration on a single gazelle so that
ctcr; these are approximately contiguous with little unoccupied sPace '{tcn they all escape. But when closely pressed the tommies always gal-

k rp. The type of gait also varies according to the type of predator; stot-
bctwcetr them. C.o.rpt of femalet irou. through these territories and
But rirrg is much more corrlrnon when tommies are chased by hyenas or wild
arc tolcrated even *[r.tt no courtship or mating is taking place'
around r k rgS, but is employed rarely with lions, cheetahs, and leopards, which
bachclor males are chased. away, and ipend most of their time
.rt hicve higher speeds in their initial charge. Caro (1986a, 1986b) has
the edges of the adult males'territories'
f)es"pite the fact that tommies are an important portion of
the diet of .rrr:rlyzcd stotting in detail and concludes that its rnost probable function
to their lives in a constant r\ r() warn predators that they have been detected or, in the case of
several predators, they do not aPPear spend
odt.r.or. Their principal -."t r of escape is simply running away,
l.rn'r)s, to alert the mother that the fawn needs protection. FitzGibbon
.rrrtl Fanshawe (I988) have provided additional evidence that stotting
and this is almost always effective, provided the prld1t9r is seen at
the tommies ,,lrorvs the tommy to be in good physical condition and likely to outmn
sufficient distance. But e,oen when fibns are ptainly visible
states that .r rr rstring prrcdator-
d.o not flee unless the lion seems likety to attack. walther

than Jrrst bcfirrc tommies are actually caprured they often change direction
tommies seem less disturbed by predators at a reasonable distance
are far from complacent, however' r.r;ritll1,, clotrbling back likc :l llrlrc. lrut irr all such cases closely obsened
by healy rainstorms. The tommies
I'r Wrlthcr thc Prcdator crrrrglrt tlrc g:rzcllc in thc cnd. When a mother
They watch for dangers at intervals, although any one may concentrate
.rn,l l.rn,n wcr-('.rPPrrxrt'ltc'tl lr1,.r j:rtk:rl, rvlrich is:rbotrt thc size of a fox,
o^ groing fo, m*"y minutes at a dme. The members of a herd look
tlrr'1' u'orrltl :rt lirst rrrn oll lr,1,,r'tltcr lltrt sornt'tirt'rcs rltc ln<lthcr would
aroind at"different times, so that there is almost always at least .trc
56 ChapterTltree l'rrdstion 57

aftempt to defend her fawn by charging at the jackal and striking it with uttering loud moaning calls and is torn apart l'ry thc lrycn:rs. It appears
her horns. Occasionally a second female, perhaps an older sister of the to be in a state of shock." Although cow-sized wiklctrccst sornctimes try
threatened fawn, would join in this kind of attack. Mothers with young to escape by running into a lake or strearn, thc hycnls rrlnrost irrvariably
fawns somerimes attack quite harmless animals and birds. But when the manage to kill them. They may hope, although vainly, that thcy can
fawn is chased by a larger and more dangerous predator, such as a lion escape by running into the water.
or cheetah, the mother moves about excitedly at a considerable distance Mother wildebeest often attack hyenas that arc thrcatening their
without intervening directly. calves, but those without calves hardly ever do so. Yet Kruuk observed
Hans Kruuk (1972) describes a sort of distraction behavior by one striking exception on the part of a cow that was in the process of
mother tommies directed at hyenas that were chasing their fawns. They giving binh. Her calf's front feet had already emerged, but she never-
would run between the two, crossing in front of the hyena and staying theless went to some lengths to attack a hyena that was walking past and
very close beside it but just out of reach. Although usually only one that seemed not to be paying any attention. Shortly afterwards this cow
female, presumably the fawn's mother, would engage in this sort of be- appeared to be avoiding the hyenas in the vicinity as she selected a quiet
havior, iometimes as many as four would run close to the hyena at the spot, surrounded by other wildebeest, where she lay down to complete
sarne time. Yet all these efficrts seemed to be ineffective. On twelve oc- the birth. Might such a cow realize that her soon-to-be-born calf was in
casions fawns were aided by distracting efficrts of adult females, but six danger of attack by a hyenaf We cannot tell, but perhaps it is best to
of them were caught. In nineteen cases observed by Kruuk the females keep an open mind and not dismiss such possibilities out of hand.
made no attempt to distract the hyena, yet only five of these fawns were
taken. Possibly the females could discriminate between more and less Mutual Monitoring by Predators and Prey
serious dangers to a fawn and engaged in the distraction effcrts only
when the danger to the fawn was acute. If so., the two sets of data may Potential prey animals are almost constantly on the watch for dangerous
not have been strictly comparable. predators, ild once one appears they keep it under close observation.
Such seemingly hopeless behavior as that displayed by * adult fe- Only on rather rare occasions does the predator become serious about
male tommy eniails a real risk that the hyena will capture her as well as attacking, md only then, ordinarily, do the prey animals become seri-
the fawn. In strictly evolutionary terms, these attemPts to save the fawn ously alarmed. When predators and prey can see each other, they spend
appear to be maladaptive inasmuch as they do not seem to lower the most of their time monitoring each other rather than in attacking or
tikllihood that the fa-wn will be killed. Likewise the final frantic efforts fleeing. This involves making subde distinctions; predators notice
of a tommy to escape have no statistical survival value if they are ineffec- slightly abnormal behavior that signals weakness or r,rrlnerability. And
tive. This appa.enilack of any survival value leads inclusive behaviorists prey animals notice the changes in the behavior of predators that signal
to disparage the significance of such behavior, because their concern is likelihood of attack. It would be advantageous for predators to conceal
limited to *"yr in which behavior contributes to the inclusive fitness of such signals; therefore, they are probably unavoidable and inadvertent.
the animals in question. But when we broaden our horizons by consid- When Thompson's gazelles detect a predator, they often do not flee
ering what life may be like to the animals themselves, it is not surPrising but move closer. They appear to be much interested and to be inspect-
to find that they make strenuous efforts to avoid being killed, or having ing the dangerous creature. Walther sometimes saw a herd of tommies
their offspring killed, even when such efficrts have litde or no chance rccognize a predator at 500 to 800 meters and then approach within
of succesi. This is an example of how our theoretical concePts can I00 to 200 meters. Under these circumstances the herd contracted into
be broadened bv a consideration of how life may seem to the animals :r smaller area than when feeding, the individuals remaining closer to
themselves. ()nc anothcr. When the predator moved, the herd followed it, evidently
Wildebeest attacked by a pack of hyenas make surprisingly few and :rwArc of thc danger ancl rcady to dash off at the first sign of an actual
ineffective affempts to dcfcncl thcmsclves. Kruuk (1972, I58) statcs rtttack. Thc prcclat()rs :rlso sccrn t<l undcrstand the situation and rarely
that a wildcbccst bcsct t'ry rr grotrp of hvcnas makes some aftemPts t() .rtt:rck :r gr()up ol' lrlcrt lorrrttit's. l)rctl:rtor monitoring by territorial
btrtt its rrttrrckcrs, btrt thrrt "gcrtcntllv spclrking, the qttarry itrst statrtls rrr:rlcs \\':rs ('sl)c('i:rlly cl'itlt'rtt At tlrt' .r1t1rrrr:tt'lt of'l prcclator in day'time
58 Chapter Three l't'rirtl ittrt 5()

the females generally moved away, while the buck stayed in his territory predators often try to identi$, and attack tlrosc Prt'y:rrrinr:rls rlr:rr urc
and kept the predator under close watch. As it moved he usually fol- most easily captured.
lowed at a safe distance until it reached the territorial boundary. Then This ability to perceive very minor changcs in thc lrhlvior of'un-
one of the neighboring territorial males would take over the monitoring other animal appears to be widespread among ['r<>th prctl:rtors rurd prcy.
of the dangerous intruder. This sort of predator monitoring was so ef- The same basic neurophysiological mechanisms tlurt pcrrnit such subtlc
fective drat predators captured only one of fifty territorial males that discriminations are probably called into play whcn animals such as
Walther studied intensively during a two-year period. Clever Hans learn to respond to minor and inadvcrtcltt c()unting move-
George Schaller (1972) describes other examples of prey animals ments of their human trainers, as discussed in chaptcr I. Recognizing
monitoring the behavior of predators and not aPPearing to be fright- how basically important such discriminative perccption is to ,"ild *i--
ened unless the predator rushes at them direcdy. When a lion is walking mals under narural conditions helps us to understand how a horse or a
along steadily, tommies, zebras, wildebeest, and other Potential Prey rlog can notice when a man stops counting as he watches the perform-
usually face the danger in an erect Posture but do not mn away. Wilde- rrnce of an animal that is supposed to be solving arithmetical problems.
beest usually keep up an incessant grunting, but when a lion approaches Kruuk observed that predators whose home area was close to that of
they stop, so that the predator is surrounded by azone of silence, which tcrritorial tommies never hunted these familiar neighbors. Some hyenas
undoubtedly warns others of the danger. A group of wildebeest may rrsually rested from midday until late afternoon in dens located within
even approach a predator and line up to watch it pass. But if a lion stops tcrritories of male tommies. When they left their dens in the early eve-
and turns in their direction, the grazing animals usually flee for a short ning they were presumably hungry; but, although they were often sur-
distance, then turn and stand watching again. Roughly thirty meters r'<>unded by tommies, they passed between them and hunted in other
from a lion seems to be considered a safe distance in open country, but .rreas. Perhaps the hyenas knew that the local tommies were alert and
when potential prey animals move into thick vegetation they behave tli{ficult to catch. Regardless of that possibility, these hyenas were
much more cautiously. These sensible adjustments of Prey monitoring clcarly distinguishing some tommies that were neighbors and were not
behavior suggest a conscious understanding of the relative dangers of .rttacked from others that were treated as prey. Thus their behavior was
various predators and how these dangers vary with circumstances) es- lirr from being a stereotyped set of responses to a particular species.
pecially with the behavior of the predator itself. A special case of predator monitoring that involves an unusual sen-
Predators are thought to select for attack metnbers of a herd that are
weak, sick, very young or very old, although an extensive review of the
'ory mechanism has been described by Westby (1988) in the course of
('xtcnsive field studies of electric fishes. The electric eel (Electrophorus
evidence bearing on this question showed that the results of many in- it:ctricu.s) is well known for its powerful electric organs that can stun or
vestigations failed to support this widely held belief (Curio 1976,1t3- kill other animals. It has been customary to consider these as defcnsive
I7). Even when all members of a herd aPPear to be healthy and vigor- nrcrlsures, but it has also been known for some time that electric eel are
ous, hungry predators still manage to caPture some. Much other evi- Prcdators, ffid that their strong discharges help them to catch prey.
dence reviewed by Curio (ll7-28) does indicate that unusual or con- Wcstby had placed recording electrodes in a strearn and was monitoring
spicuous members of a group of prey are more likely to be taken by tlrc social behavior of a small species ofweak electric knifefish, Cryrnnotus
predators. Kruuk observed that hyenas aPPeared to be quite adept at rrtrapl, which uses its weak pulses both for orientation and for corrunu-
noticing slight differences in an individual prey animal's posture, loco- rrrc:rtion in courtship. While he was thus monitoring electric activity in
motion, or other behavior indicating weakness or l'ulnerability. He re- llrc strcam, the pulses of a 1.8-meter-long electric eel could be detected
ports that when a gazelle had been anesthetized for study or marking, ,rl,prorrching the location of the knifefish. The laner stopped emitting
he had to stand by in his automobile to Protect it from attack by hyenas rts lrtrlscs nlost <>f the tinrc, but was detccted and devoured by the elec-
even after it seemed to have recovered completely and to be behaving trit ccl, which prot'rablv loc:rtctl it by rccognizing its occasional weak
normally. Thus while the tcnclcncy to select more I'ulnerable Prey may clt't I ric sigrr:rls.
havc only a small ovcrall statistical cffect., it seems reasonably clcar that Irt:t l:ttxlrrlf()r'\/ tltttk .t r'.tPtit'r'r'k'tlrir't't'l cntittctl its str<lng "preda-
60 Chapter Three l>redation 61

tory" shocks when stimulated either by a live knifefish or by electrodes Cooperative Hunting
generating signals recorded from the same knifefish and played back
into the water at normal intensity levels. Although such electric signals M*y carnivorous mamnals sometimes hunt in groups, although it is
are unfamiliar to us, they are easily monitored and reproduced, so that not clear how much this increases their total foodlntake over wh-at each
the investigation of social communication and electric shock predation could_capture individually. Sometimes group hunting succeeds in sur-
can be conducted with more precise control of the signals than is pos- roundin-g_or concentrating prey that would otherwisJbe more likely to
sible with most other animals. This offers a potentially exciting oppor- escape. This type of simple cooperation has been observed when peli-
tunity to cognitive ethologists to analyze not only predatory shocks and cans, cormorants, South American otters, dolphins, or killer whalei are
efforts to avoid them but also a whole range ofsocial communication of pursuing fish (Curio 1976, L99-20L). The behavior of large cooperar-
weakly electric fish by electrical recording, analysis, and playback, as is ing. groups is. quite different from that of individualr p.rrriring fish on
already being done by several investigators including Westby (1988) their own or in smaller groups. For example, Bartholomew
116+zy ob-
and Bratton and Kramer (1989). .served that double-crested cormorants (Phala,crocora,x aaritws) fished in
a different type of formation when in very large groups of 500 or more

Playing with Prey than wllen only 50 or so were pursuing fish togeth.r. k such cases the
individuals modifi their behavior only enougli to maintain an appro-
Foxes, like many other predators, sometimes play with caprured prey; priate position in the formation.
while our human sympathies go out to the tormented victim, the pred- Meinertzhag:n (1959, 47) vividly describes this type of cooperarive
ator seems to enjoy this sort of behavior. Henry (1986, 136-40) de- by Dalmatian pelicans (Peleconws tispas) as-follows: ..There
scribes a highly suggestive incident in which a six-month-old red fox \r/ere over a hundred birds forming line, diving towards shore in shallow
that he had observed extensively appeared to release a captured shrew water, two ends of the line advancing in perfect order and not very fast.
intentionally and return it to the vicinity of its burrow. This fox had A crescent was eventually formed, every bird keeping his correct station,
caught and immediately eaten one mouse, then caught another with .urd then, as water barely 18 in. deep was reached, the rwo horns of the
which he "played vigorously for several minutes." After killing it, the crescent increased speed, closed in, and formed a complete circle, the
fox carried it some distance and cached it. Although this showed that birds almost touching. Within the circle the warer boiledwith small fish,
the fox was no longer very hungry, he soon captured a shrew, which he hc'ads were rapidly plunged in simultaneously and pouches filled with
carried some distance to an open roadway where he began to play with lish, the circle closing in all the time and feet paddling hard ro prevent
it. As Henry described the fox's behavior in his field notes, "the fox is lish escaping below body-line." wi.irsig (1983) hai described how
leaping around, dancing about the shrew who runs over to one side of tlusky dolphins herd anchovies in the open ocean, diving and swimming
the road before the fox herds it back to the center. After 45 seconds of .rt them from below and from the sides while vocalizing loudly. Thii
playing with this animal, the fox then does an extraordinary thing. He r csults in a tight ball of anchovies; and the dolphins
take rurns swim-
picks the shrew up in his mouth, walks back down the slope to where rrring into the aggregation and seizing fish while others conrinue the
he captured the prey, and then with a toss of the head spits the shrew hcrding from outside the ball.
out directly at a small burrow. In less than a second, the shrew disap- chimpanzees ordinarily feed on fruit, leaves, flower blossoms, seeds,
pears into the hole and is out of view." Shrews have an unpleasant odor, .rnrl insects. But on occasion they actively hunt, kill, and eat monkeys,
and though they are eaten by hungry foxes, they are more often cached. lrtrshpigs, small antelope, rodents, and even human babies. In some
As Henry suggests, this fox may have returned the shrew to the burrow (.rscs thcy prepare to hunt monkeys by watching them for some time,
a fcw inches from where it was caprured with the anticipation that it ,rrrtl apparc'ntly communicating with each other by low intensity sounds
might provide food or furr ()n s()nlc firrurc occasion. Of course, we can- ,rrrtl touching cach othcr. Thcn thcy approach and pursue particularly
not be at all surc <lf strch rr suggcsti()r'1, [-rut, rrs Hcnry concludes, "if wc r rrlrrcr:rlrlc inclivicltr:rl rrrorrkcl,s. strch as fbmales or young, with many
arc going t<l urrrlcr.starrtl rcrl firxc.s corrtplctcly, in all their dcpth and \rlltts ol' itttctttirnal ('()()lx'r'.rlion, :ls tlcscril'rcrl in dctaii by Goodjl
l'rrcrrtlth, wc (':lnnot sttrtll, .urrl .rrlrlyzc jrrst thcir c()mnr()n hchavi<lrs." 1 |()lt(r) :ttttl b1, lkx'st lt .uttl lk,r's. lr A. kt-l'rrr:rlrlr ( l99l
62 Cbapter Three Predatinn 63
In many cases the advantage of group hunting seems to be that it rccorded one relay chase that continucd firr:rt lc:rst ti00 m and involved
permits the killing of a large prey anirnal that would be able to defend rnore than 20 stoops and hence switchcs in thc lcad."
itself against a single attacker. Hawks and eagles that prey on birds have Another clear advantage of cooperativc hunting is the ability ro take
been suspected of cooperative hunting, but when such hunting has been very large prey that a single predator could not subdue unaided. one
studied carefirlly it has often been unclear whether it was adr,'antageous, intriguing example is the hunting behavior of the South American giant
or whether the sarne birds obtained just as much food when hunting offer Pteronura brasiliensis studied in the Manu National Park of Peru
singly. In the case of Aplomado falcons (Falco fernoralis) in Mexico, by Munn (1988). These otters are six feet long and weigh about 30
however, Flector (1986) found that there was some division of labor kilograms. Their principal diet consists of fish caught singly by individ-
and simple coordinative signaling. Bednarz (1988) has both reviewed tual otters, but they often hunt in groups when pursuing large prey. A
earlier studies suggesting cooperation and reported his observations of corrunon cooperative fishing tactic is to swim together in a loose phd-
Flarris'hawks in New Mexico, which engaged in effective teamwork lnx, and dive together for ten to twenty seconds, with much thrashing
rvhen hunting cottontail rabbits and jackrabbits. lnd churning of the water. Sometimes groups of giant otters kill and eat
These hawks, which average about 850 grams in weight, hunted dur- l'rlack caimans from 0.6 to I.5 meters in length, md even anacondas up
ing the nonbreeding season in groups of two to six, probably members r<> 2.7 meters long. They attack caimans almost simultaneously from
of a genetically related family. They captured both cottontail rabbits, scveral directions, and when attacking a large anaconda two or more
somewhat smaller than themselves, and also jackrabbits that weighed ()tters would bite the snake at different points along its body, holding
about 2100 grams. Bednarz had previously attached radio transmiffers lirst and bashing it
against fallen treerrunks in the warer. These group
to at least one hawk in each hunting groupr and he could observe the .rttacks are coordinated to at least a limited degree, and some quick and
others visually during most of thirty successful hunts in which a group scnsible thinking about where and how to bite in relation to where
of hawks captured seventeen cottontails and nine jackrabbits. Coopera- one's companions are attacking a large antagonist would seem helpfirl.
tive hunting seems to be advantageous for Flarris' hawks, since single Kruuk (1972) summarized the results of his extensive observations
hawks were not seen to attack large prey during these observations. Es- ,rf hyenas hunting wildebeest calves both individually and in groups.
pecially with jackrabbits that are more than twice the size of the hawk, ()nly about one third of I08 attempts by one or more hyenas ro caprure
it seems unlikely that a single bird would have much success. The firll t':rlves were successfril. Single hyenas were almost always driven off by
sequence of hunting behavior was observed in thirteen cases. thc mother, but when two hyenas were involved one often seized the
At the beginning of a hunt a group of five or six hawks would split celf while the mother was attacking the other. It is also clear from many
up into smaller groups of one to three that appeared to search for prey ,lrservations that hyenas and wild dogs are more successful in hunting
during 100 to 300 meter flights from one conspicuous perch to another. tommies in groups than singly. George Schaller's extensive studies of
In seven of the thirteen well-observed hunts several converged from li.ns showed several cases in which a group of four or five lionesses
different directions on a rabbit that was away from cover. In four cap- sprcad out as they approached one or more gazelles, those in the center
tures of a cottontail rabbit "a flush-and-ambush strategy was employed. , rl- the group approaching more slowly than those at the edges, thus
Here, the hawks surrounded and alertly watched the location where the r r-cating a U-shaped formation that tended to surround the prey on
quarry disappeared while one or possibly two hawks attempted to pen- tltrcc sidcs. Some prev animals escaping from lions in the center of the
etrate the cover. When the rabbit flushed, one or more of the perched Iormation seemed to be more easily caught by those advancing on the
birds pounced and made the kill." The two remaining hunts that could ,'rlgcs of thc fbrmation. Yet both Schaller and Kruuk and more recendy
be closely observed were relay attacks. which Bednarz describes as fol- St'lrccl and Packer (1991) are vcry cautious about inferring conscious
lows: "This technique involved a nearly constant chase of a rabbit fbr rr)tcnt <ln thc part ()f thc c<lclpcreting predators. For example Schaller's
several minutes while the 'lead'was alternated among Party members. A rrrtlcx d<rcs not inclr"rtlc thc r.l,ortl "c<>{r1'rcrAtion."
switch occurred when the lead hawk stooped at the prey and missed, at Schrrllcr c<xrclttrlctl th:rt c.rt'h liont'ss bch:rvcs morc or less indepen-
wirich point the chase was continuccl by anothcr member of the party. I .lcnll1, :rltlrouglr ol't'ottt'sr' (llrtl(' rr'.rrl1, to t:rkc atlv:rrrt:rgc of another's
64 Cbapter Three Predation 65

hunting efforts, as when a gazelle fleeing from a companion runs close fiom the woods directly toward the wildcbcc.st that were located be-
to the lioness in question. But Schaller did note that when hunting in tween the woods and the road, and thcy thundcrccl off direcdy away
groups the lionesses look at each other and seem to be trying to main- fiom her toward their companions on thc opcn plain. This route took
tain an effective formation, such as the U-shaped pattern. Groups of them across the ditch close to where we had last seen the lioness slinking
lionesses that hunt together routinely for months at a time are often furtively a few minutes earlier. As the herd bounded over the ditch she
sisters or mother and daughters, md they certainly know each other lcaped up and seized one of the fifty or so that were galloping all around
intimately. Yet like so many other ethologists, Schaller and Kruuk seem hcr. As the dust settled she was busy killing this wildebeest by covering
to be leaning over backwards to avoid any suggestion that lionesses or its mouth with hers as it lay on its back, legs kicking gendy in the still
other predators intentionally cooperate by coordinating their hunting tlusty air.
tactics. The two lionesses that had been sitting quiedy on their mounds and
I once had the good fornrne to observe a grouP lion hunt involving the one that had chased the wildebeest towards the ditch walked slowly
more definite evidence of coordination. While I was briefly visiting towards the downed prey, but arrived only after its kicking had ceased.
Robert Seyfarth and Dorothy Cheney Seyfarth during their studies of All four then began to eat their prey in a leisurely fashion, and after a
vervet monkeys in the Amboseli National Park in Kenya, they drove me ll'w moments a jackal joined the scene. Meanwhile the whole group of
along a dirt road at the edge of a forested area bordering a large oPen rvildebeest returned from the open plain where they had all fled and
plain. At a place where the woodland receded for a few hundred meters, stood in a line watching the lionesses and her victim from a distance of
the road ran between a semicircular area of grassland on one side and .rbout a hundred meters.
the open plain on the other. A large herd of wildebeest had split into A single observation such as this one cannot be taken as conclusive
rwo groups; fifty to sixty were grazing on the woodland side of the 1',roof of intentional cooperation, but it is certainly very suggestive.
road, while the remaining hundred or so were feeding on the oPen plain Why else should the first nvo lionesses have climbed to conspicuous
about I50 to 200 meters from the road. positions and waited where the wildebeest could easily see that they
As we paused to watch the wildebeest, four or five lionesses aP- 1',resented no serious dangerf \{Ihy should a third lioness sneak so fur-
proached with a businesslike gait along the edge of the plain, roughly r ivcly along the ditch to a position about midway benveen the rwo

parallel to the road and within a few meters of it. Both groups of wilde- sroups of wildebeestf And was it a pure coincidence that a fourth lion-
beest obviously saw them, for they stopped feeding and watched the css disappeared from the group and that a lioness just happened at the
lionesses intently. Because the ground was irregular we could not see the .rppropriate time to rush out from a suitable point at the edge of the
lionesses all the time, but when about 200 meters from the two grouPs lorcst so as to chase the wildebeest over the ditch where one of her
of wildebeest two climbed slowly to the tops of two adjacent mounds .'ornpanions was waitingf The individual elements of group hunting be-
where they sat upright, and remained stationary but conspicuous. After lr:rvior I have described have been observed by others, but we were re-
a few minutes had passed we could make out a third lioness slinking, rrrlrkably fornrnate to see so much of this sequence. Yet the ethologists
her belly pressed close to the ground, along a ditch that paralleled the rvlto report detailed observations of lion behavior have been so reluctant
road. Although she was visible to us only occasionally, it was clear that to infer conscious intent to cooperate that they seem to have refrained
she was moving toward a position roughly midway between the rwo lirrrn reporting as much of this type of behavior as they have actually
groups of wildebeest. She soon crall4ed out of our view and for several , rtrscrved.
minutes nothing seemed to be happening at all. Standcr (1992) has observed ciozens of group lion hunts in very
Suddenly a fourth lioness rushed out of the forest behind the wilde- ( )l)cn c()untry of Namibia. He studied these lions so intensively that he
beest on the woodland side of the road. Although we had not seen her ..,,rrltl rccognize individuals, somc by natural markings, ffid some by
do so, it seemed almost certain that she was a member of the sarne t.rgs :rrrtl rrrcli<> transnrittcrs thrrt wcrc attached to them when they had
group; and that she moved into the wooded area out of our view, and Irt't'rr r':rl'rtrrrcd antl iurcsthctizctl. In nunlcr()us group hunts of large prey
presumably also that of thc wildebcest. Irr any event a lioness rushcd P.rrtit'rrl.rr lirxrcsscs trxrk tlrt's.uttt'Position withirr a r<lughly linearhunt-
66 Chapter Tbree

ing formation night after night. Individual lionesses occupied the same CHAPTER FOUR
po-sition (center o. o.. of the wings) on-successive nights. These for-
matlons approached prey in a coordinated fashion before the group at-
tacked at ibout the iame time from different directions' But hunting
tactics were varied according to the situation, with smaller prey hunted Con struction of Artofncts
by individuals in many cases.

wide variety of animals display considerable ingenuity in

the construction of shelters and stmctures that serve other purposes,
such as capturing prey or attracting mates. These activities require ad-
justment of behavior to the local situation, to the materials available,
and to the various stages of construction. This necessary versatility often
suggests that the animal is thinking about the results of its efficrts and
anticipating what it can accomplish. For acting to attain an intended
objective is a more efficient process than blindly following a rigid pro-
gram. This chapter discusses selected cases where animals build more or
lcss fixed stmctures that benefit them or their offspring; chapter 5 de-
scribes the construction and use of tools. Although there is no sharp dis-
tinction between artifacts and tools, the details of the behavior involved
in their constmction and use make it convenient to discuss them separ-
The many types of structures built by animals are often characteristic
of the species to which they belong, and in some cases such as the ter-
rrrites and the larvae of caddis flies the stmctures may be more usefi.rl for
identifying species than is the morphology of the animals that build
thcm. This species specificity suggests genetic programming of a rela-
r ivcly stereotyped nature; but when analyzed carefully the animals often

rlisplay considerable versatility in adapting the details of the artifact

(()nsrruction to the particular situation. Karl von Frisch (1974) re-
vicrvcd many significant examples in a delightful book,AnirnalArchitec-
ttrc. It is no accident that the sarne brilliant scientist who discovered
tlt:tt hotrc),bces communicate symbolically, as discussed in chapter 9,
.rls() trrn)cd his attcntion to thc irrgcnious variety of shelters constructed
1,1, r,:lrior.rs :rnirrr:rls. I'or it i.s rlillicult t() rcprcss onc's admiration for the
cllt'ctivcncss, :urtl [rc:rrrty, ol'rtt:trrY ol'tllc stntcturcs built by cven rather
srrrrplr':rnirtr;rls. ()rrr':trlrttit'.ttiott nl.rv st('r'rt irr p:trt fi<lnr thc suspicion
tlr.rt llrt'.rrrirrr:rls nr.r\/ tLr llrt'rr Irrrrltlrrrl,, rvitlr .rt lt':rsl s()nlc rtrdittrcnts of

()nttrtrrttort ol'Artifitcts
68 Chapter Four 69
intention. A very thorough survey of animal architecture has been pro- Topoff 1977; Heinrich 1984, l4f-51). Whcn :ur :urt or othcr small
vided by Hansell (198a); this adds much detail and many new discov- prey animal falls into the pit, the predat<>ry arrt lion ()r ilnt w()rnl seizes
eries to von Frisch's more general book. The examples discussed below it with its mandibles and injects a poison which kills thc victim. Often
are based largely on these two books. active prey such as ants crawl about activcly cnough that they are not
Even some of the protozoa build simple cases, usually by secreting seized on the ant lion's first attempt. The ant li<xr thcn throws grains of
material from the cell surface. A fe*, such as the amoebas of the genus sand in the general direction of the prey, and this sccms to increase its
Dffiugia add external grains of sand to their outer surfaces, so that they chances of capturing an ant. Recendy Lucas (1982, 1989) has studied
ir-r detail one species of ant lion Myrrneleon crud.elis in Florida. The pits
come to resemble tiny croquettes. These particles are transported
through the cytoplasm and distributed fairly evenly at the cell surface. are not perfecdv conical but have walls that slope more gradually in the
But the processes involved appear to have more in common with cellu- parts of the pit where the ant lion waits for prey. The walls are steeper in
lar functions such as pinocyosis, where the cell membrane bulges out fiont of it, and these front walls also tend to be lined with finer grains
and engulfs an external particle than with active manipulation by the r>f sand.
organism of objects outside of its body (Netzel 1977). Since Protozoa These predatory insect larvae thus constmct a very simple artifact,
lack anything at all comparable to a central nervous system capable of the pit with somewhat different walls on different sides and also throw
storing and manipulating information, it seems highly unlikely that .sand grains as a very crude form of tool. The details of their prey-
they could be capable of anything remotely comparable to conscious catching behavior are difficult to study because everl'thing happens too
thinking. first for the human eye to follow easily. It is not clear how adaptable the
Hansell (1984) reviews several scattered examples of multicellular rrnt lions are, but they do alter their behavior to some degree according
annelids and molluscs that build simple stmctures, such as the burrows to the type of prey the kind of soil in which their pit is dug, and occa-
of marine polychaete worms. Impressive stmctures are built primarily sionally they show interesting interactions. Wheeler reviewed earlier
by arthropods and vertebrates. Several species of crabs dig burrows, and r>bservations in which two ant lions dug pits so close together that an
some fiddler crabs of the genus Uca add hoods near the burrow en- insect escaped from one pit only to fall into the other. In this case the
trance, apparently as a part of their courtship and affraction of females lirst ant lion emerged from its pit and pursued the prey into its neigh-
(Crane 1975; Christy L982). Several species of fish build nests to shel- [ror's pit.
ter their egBS, the most thoroughly studied being the European stickle-
back, whose courtship behavior has been analyzed by Tinbergen and (,addis Fly Cases
nrany others. A less well-known case is the weakly electric fish Cryrnnar-
()ne of the more impressive examples of complex structures built by
chus niloticus, the species used by Lissmann in his classic experiments
clcmonstraring the use of weak electric fields for orientation. These rel- vcrv simple animals are the cases and nets built by the larvae of caddis
atively large freshwater fish build a nest from floating vegetation which llics. These are abundant animals in freshwater strearns and ponds and
has a corridor leading to a chamber at the end where the eggs are laid nrirny of them constmct shelters of various types attached to vegetation
(Bullock and Heiligenberg 1986). or the bottom of whatever body of water they occupy. They develop
lionr eggs laid in the water by winged female caddis flies which emerge
.rntl mate after a long period as aquatic larvae. The larvae of North
Ant Lions r\rncrican caddis flies and the cases they constmct have been described
groups of rrr dctail by Wiggins (1977), who illustrates nurnerous variations in cad-
Simple pitfall traps are constructed by two distantly related
insect larvae, the ant lions and worm lions. Both dig shallow, roughly tlis fly casc and net constnrcti()n characteristic of the numerous genera
-fhc larvac tlrcnrsclvcs arc rather nondescript
funnel-shaped holes in loose soil and wait with their bodies almost en- .rrrtl s1'rccics. and difficult
tirely buried at the bottom of the cavity for other small animals to fhll to itlcntil\,. btrt thc shcltcrs :lr'(' so t'h:rmctcristic tl'rat they are often used il

in. The corunonest prey are ants, which generally attemPt to escaPc lrl' s1,stcln:rtit' crrtorttokrgrsts lor s1x't'11's itlcntificatiorr. Tl'rc cases built
from the pit by climbing up thc stccply slopring walls (Whcclcr 1930; lr1't;rtltlis llt' l:rn':tc rtt,t1'r'tttPl,r1' lrtts ol lr'.tvt's, P:trtit-lcs ol'serttl, or<lther
70 Chapter Fowr ( )nstrtrr I ttttt ol'rlrt tlirrtt 7 I

available materials including the empty shells of very small snails. They f-asten it there. On a very small size scalc thi.s lrchrrvior is llcxiblc rrrrrl
are cemented together by silk secreted from glands on the larva's head. adapted to the available particles and thc stagc ol'crrsc ('()n.\trrrction.
Sometimes caddis fly larvae crawl out of their cases, and they may fight Hansell (1972, L974) also studied anothcr spccics <>l'c:rrltli.s fly lrrrva,
over cases or one may evict the occupant of a case and take it over (Otto Lepidnstorno hirturn, which constructs cut pancls liorn bits of'lclvcs t<>
1987a, 1987b; Englund and Otto I99l ). form a floor, roof, and two sides. All of thc pancls urc lpproximatcly
Like other insects, these larvae grow through successive stages in rectangular pieces, one or two millimeters in sizc hckl togcthcr at the
which the exoskeleton is shed. In early stages the small larva uses minute cdges by secreted silk. The resulting case is strcngthcncd by a staggered
and ordinarily homogeneous particles to form a roughly cylindrical case xrrangement of the pieces. Each joint betwecn two sicle plates intersects
around its body. These cases may increase the flow of water over the with the middle and not the edge of a roof platc. When Hansell cut
gills (Williams, Tavares, and Bryantl9ST), and also protect the other- away the front end of a case to form a continuous, smooth front edge,
wise vulnerable soft bodied larva from small fishes or other predators rhe larva cut leaves of different shapes from those normally used and
such as immature dragonflies. The case is not totally impervious; it has an glued them into place so as to restore the staggered arrangement. These
opening at the posterior end to allow feces to pass out, and uater cir- simple insect larvae thus exhibit a considerable degree of versatility not
culates freely from an anterior opening to the posterior one so that the onlt, in the initial constmction of their cases but in repairing them. De-
gills can extract oxygen from the water. In many species the case is port- spite our customary assumption that insect larvae exhibit only stereo-
able and is carried about as the animal moves by pushing its head and typed behavior, they have highly organized central nervous sysrems
thoracic segments carrying the six legs out through the front opening. with hundreds of neurons and synapses that appear quite capable of
The case is held close to the body by hooklike projections from the ab- organizing relatively complex and flexible behavior.
dominal segments. In constructing their cases, caddis fly larvae are Yet another species of caddis fly larvae constmct a more elaborate
somewhat selective about the materials used. Some species cut pieces casc, which provides not only a shelter but a food-gathering mechanism
from the leaves of aquatic plants and others constmct fine meshed nets as described in detail by Wallace and Sherberger (1975). This case is a
that serve to strain minute animals and plants from the flowing water. chamber considerably larger than the animal's body and roughly oval in
The case building behavior of a few species of caddis fly larvae has shape. From the upstream end rises a tubular extension with a roughly
been studied carefirlly in the laboratory by Hansell (1984, 1968). He ninety-degree bend and an opening facing into the direction from
conducted detailed observations and experiments with Selo palltPa rvhich water is flowing. From the other end of the oval chamber rises a
which begins its larva life by constructing a simple rylindrical tube of shorter outlet tube. The entire chamber is only two or three centimeters
sand grains cemented together. This species passes through five instars in length, but the flow of water by the surrounding stream serves to
between which the animal sheds its external skeleton and grows a larger vcntilate it fairly well due to its construction. Opening into the side of
one. In its first instar the Silo larva occupies a roughly cylindrical case thc main chamber is a separate tubular structure corresponding to the
composed of particles about one-half millimeter in diameter. But norrnal caddis fly case. But both ends of this open into the larger cham-
toward the end of this instar it adds two larger sand grains at the sides bcr. The end u,here the larva places its head opens into the upstream
of the front end. During the second instar it adds two more larger par- sitlc of the main chamber, and water flows through this side chamber
ticles, and through the three succeeding instars it selects at each molt p.r.st the larva's gills and out a posterior opening into the downstream
Iarger grains of sand for the anterior opening. At the end of the fifth p.rrt <>f the main chamber. Finally, the larva constmcts a fine mesh net
instar the case is about ten millimeters long and the larger anterior .r('r-()ss thc middle of the large chamber. Small animals and plants are
grains are two to five millimeters in diameter. Throughout this growth ...rrrght ()n this net and serve as food. The entire stmcture is roughly
the larva enlarges its rylindrical case by adding more small particles. ,, rrnparat'rlc in complcxity to thc ncsts of many birds.
Hansell's observation showed that the larvae reach out of their cases It h:rs l'rccrr cu.st()rurlry to vicw such artifacts as caddis fly cases in
and fcel particles in the immediate vicinity with their anterior appen- rrrut'lr tlrc srunc light th.rt lriokrgists vicw thc clabclrate structures of an-
dages and reject many that arc cithcr too large or too small. Having fl'lt rrn.rl Ixrtlit's lr:lftcrrrs rt'11rl.rtt'tl prirrr.rrilv lry gcrrctic irrstructions. But
onc of appropriatc sizc tlrcy nrovc it irrt<l p<lsition anc-l sccrctc silk r<> ,lrtk,st't'x.urtitt.tlion rl llrlnsolrl tlr.rl cvcrrsirrrlrlt'('r('.ltlrrc.ssttchascad-
72 Chapter Four Oonslnrrtiort ol'rlrtilhrts 7.\

dis fly larvae adjust their building behavior in ways that would seem to portion of the tapering spiral cavity of thc srrail slrcll with clrcwctl rr1-r
be aided by simple thinking about what they are doing. Such thinking pieces of leaf. Nearer the outside she deposits crrotrgh snr.rll pctrblcs t<r
might be limited to seeking to match some sensory or perceptual pat- fbrm a fairly rigid wall. Neither the leaf fragnlcnt.s nor rhc ptrtrlcs pro-
tern that was itself produced by genetic instructions. But, as I have vide a totally airtight seal, and air can still circulatc cvcn :rftcr a scct>nd
pointed out elsewhere (Griffin 1984), th" fact that a central nervous wall of leaf pulp is added outside of the pebblcs. As though thcsc prcp-
system operates in a certain way because of genetic instructions does not ilrations were not enough, the mason bee adds clry stalks <>f grass, tiny
necessarily mean that its operations may not also lead to cognition and rwigs, or pine needles, piling them over the snail shcll in a large irregular
perceptual consciousness. clome.
These elaborate sequential actions may well be genetically pro-
Insect Nests
grammed to a considerable extent, but experimental evidence is not
rrvailable to indicate how much individual experience may affect this be-
Numerous species of insects constmct a wide variety of nests or shelters havior. Might such an egg-laying female think consciously about what
as reviewed by von Frisch (1974). Often, as in the conspicuous nests of she is doingl She will die long before her offspring emerge, so rhat she
wasps and hornets, nulnerous females contribute by gathering bits of has no direct information about the eventual result of her complex ef-
vegetation, chewing them, and mixing them both with saliva and with lirrts, although she did of course begin life as a larva in a similar nest.
silky secretions from specialized glands or with their own feces. The While a female Osruia may have no possibility of understanding the
resulting daubs are then applied to some solid substrate, and other l()ng-term advantages of her elaborate efforts, she might nevertheless
daubs are added to build up a multichambered nest much larger than think consciously about the immediate present or very short-term fu-
the individual insects. In some ways the nests built by solitary bees and t ure. She might strive to close the snail shell after laying eggs and feel
wasps are even more impressive, because they result from the work of a sood about hiding it, even though she has no understanding that oF
single female. When ready to lay eggs she searches widely for suitable spring will evenrually emerge.
materials and brings them from a considerable distance to prepare a Other wasps dig tunnels in the ground or into solid wood and lay
place where she builds a nest. cggs in them. The tunnel opening is then plugged, and some species
The mason bees of the genus Chnlicod.orna. morsten with their saliva sclcct material for the plug that matches the surroundings so well that
particles of sand and dirt they have gathered and form these into small tlrc burrow opening is very difficult to detect. In the sand wasps (Arn-
oblong pellets. The female then carries each such pellet to a spot on a rnophila carnpestris) srudied by Baerends (1941) the burrows are dug in
large rock, where she cements them together into a roughly cylindrical s,rndy ground with an enlarged chamber at the lower end. These wasps
cell open at the top. In each cell she lays one egg and regurgitates liquid r krse the opening with small stones, which they bring from some dis-
honey around it. Then she closes the top with additional sand grains, l.u)ce if none are available in the immediate vicinity. Then the wasp
cementing it securely with saliva. Next she applies dust particles to the scrrrches for and captures a caterpillar, which ordinarily is as large as
outside of a group of such cells with the result that they come to look lrcrsclf. She paralyzes it by stinging it in several places and carries it on
almost exactly like the surface of the rock to which they are attached. rlrc wing to the burrow. There she opens the entrance, drags the cater-
The mixture of fine dust particles and saliva dries into a stmcture almost 1,ilhr down ro the nest chamber and only then lays an egg. Paralyzed
as hard as the rock. t:rtcrpillars survive well enough that the growing larvae can eat them.
A different species of mason bee, Osrnia bicolor, seeks out an emPty As rcvicwed by Thorpe (1963) and described in detail by van Iersel
snail shell and deposits both her eggs and food for the larvae that will .urtl vun clcm Assem (1964), the sealing of wasp burrows is accom-
hatch from them in the narrow inner parts of the spiral chamber. Somc l,lislrcd vcry skillftrlly, so that aftcr it is completed it is virnrally impos-
of the food thus deposited is a semisolid mixture of pollen and regurgi- srlrlc to scc rlrry signs of tlistrrrl):lncc. Whcn cligging a burrow, the wasp
tated stomach contcnt known as "bcc bread." After depositing numcr- llttrru's s:trttl grltins s()nl('tlisl.urr't'.lu':t\/ so thtrt thcy d<l not create a re-
ous eggs and a quantity of bcc brc:rcl tl'rc fcmale Osrnia fills thc midcllc vr'.rling pilc ol'ttt:ttt'ri:tl.'l'lrt'lt'rrr.rlt'. on rt'trrrrrirrg witlr a catcrpillar, re-
74 Chapter Four ( )ortstrtrr t ttttt ol' tlrt tlitt l t ,,!

locates her hidden burrow by remembering the appearance of sur- from the entrance over the forest floor in srrch cn()r'nrotrs nrurrlrt.r's tlr.rl
rounding landmarks. If these are experimentally altered she may be they quickly wjar down the vegetation and lirrrrr lrt':rtt'n l):rtlrs.'l'hcy
unable to find the concealed burrow entrance. climb plants of all sizes, cut pieces of lcaf roughly rlrc sizc ol'rhcir orvrr
This type of complex burrow construction and provisioning has bodies, and carry these back to the cok>ny. ()ficn rlrcy crrrr lrc sccn lry
been studied experimentally by intervening in the process in ways that the hundreds walking methodically along tlrcir tmil.s, c:rch :rnr crrrrying
a- tiny green fragment. When they attack flowcr bcrls, rhc clisnraycd gar-
would not normally occur. For example if a paralyzed caterpillar is
moved after the wasp has dropped it near the burrow entrance while dener may be startled by a busy trail of fivc-millinrctcr fiagnrcnts of col-
reopening the hole, she hunts about for the missing prey and drags it orful flower petals being carried to the undergr<>uncl runncl system.
back to the entrance. But in many experiments she then repeats the en- Inside the colony the workers carry leaves or flower pctals into spe-
tire behavior of depositing the caterpillar near the entrance and digging cial chambers containing masses of fungus. These chambcrs may be as
even though the burrow has already been opened. This has often been l1rg. as-a-meter in diameter, and the fungus grows rapidly, nourished by
taken as evidence that the entire pattern is rigidly programmed geneti- the leaf fragments as well as by feces of the ants. The leaf cutters, like
cally, and the further assumption is customarily added that for this rea- certain other species of ants, are in a very real sense engaging in a form
son the wasp cannot possibly think consciously about what she is doing. of agriculture. They collect particular food planrs, bring them into the
Similar examples have received a great deal of emphasis. When some colony, and manipulate the fungus in appropriate ways to facilitate its
insects have constructed a nest they may fail to alter their behavior if an growth and the processing of the food, which the ants themselves could
experimenter opens a hole in the wall or bottom of the nest so that the not digest unaided. In addition to gathering food and tending the fun-
eggs fall out as soon as they are laid. We can immediately see what the gus "gardens," the ants devote much effiort to caring for eggs and larvae .
insect ought to do to accomplish her general objective; and when she While much of the behavior of leaf-cutter ants is relatively predictable,
fails to do this, and instead repeats what would ordinarily be appro- tl-re workers vary their activities according to the needs of the colony to

priate behavior in this abnormal situation, we tend to conclude that she some degree. It has not been practicable to rear such ants in isolation in
is a mindless robot. But in other cases insects do behave sensibly and .r way that would serve to tease apart the relative contribution ofgenetic

repair damaged nests. Undue emphasis has been placed by inclusive be- constmctions and individual experience, but, as in so many other cases
haviorists on the examples of stupid behavior, and because many insects of complex animal behavior, it would seem that a little elementary con-
often fail to adjust their behavior after abnormal experimental distur- scious thinking would be helpful. For example, when suitable food has
bances, we have overgeneral:z,ed such inefficient behavior into a dog- r)r>f $sen found in one area, the leaf-cutter ants shift their foraging acdv-

matic conclusion that no insect ever thinks consciously about its activi- ity to other places. They cenainly exploit newly available food sources
ties. by'massive invasions that can be totally destructive to human gardening
The leaf-cuffer ants of the genus Atta are in many ways one of the cfk>rts.
most successfi.rl species in the world if judged by the number of well- Another group of specialized ants, the African weaver anrs (oeco-
nourished individuals and their impact on the immediate environment. phyla longinoda.), exemplify the capabilities of millimeter-sized cenrral
The general behavior of these ants has been well reviewed by Weber ncrvous systems (Holldobler and Wilson 1990). Weaver ants live pri-
(1972) and by Holldobler and Wilson (1990). They live in enormous nrarily in trees, but instead of digging a burrow or nesting cavity they
underground colonies consisting of many chambers interconnected by ('()nstruct nests by joining together leaves. The edges of the leaves are
tunnels. Each colony is founded by a single queen, but she lays eggs that .rttrrchcd with sticky silk, to form closed chambers considerably larger
develop into thousands of nonreproductive workers. Males and virgin tlrln thc bodies of the ants that btrild them. Nest construction is carried
queens are produced only after such a colony has grown to a substantial orrt [-ry ltonrcproductivc fcmalc workers, like most of the activities of
size. The workers are adapted both in anatomy and behavior for differ- rot'irtl in.sccts. Thc lirst pr<lblcrn irr con.stmcting a nest is to bend leaves
ent ftlnctions such as caring firr cggs, larvae, and pupae, gathering food, ottt ol'tltcir rt<lrtnrtl llrrt slrrrpt's .rntl join thc cdgcs to form the walls of an
<lr clcfcncling thc c<llony rrgainst intruding insects ofother species as wcll t'rtt'k r.st'tl t':tvity. Sorttr't it'ttt's , )t)(' .u)t ('.lr) llr':r,sl) orrc lc:rf with hcr rear legs
as against r,,crtctrr:rtc prctl:rtors. 'l'hc fixxl-gathcrinpS workcrs m()vc ()ut .tlttl lltt'otltt'r witlr lrt'r'i.trt's.trr,l Irr'lrt'rrtlirr[ lrt'r'u,lrolc botly antl flcxing
76 Chapter Four ()ntstntrt iort ol'rlrt ilirrts 77

her legs can pull the edges of the leaves together. But since the individ-
ual ants are much smaller than the leaves, numerous workers must line
Bird Nests
up along the edges of two leaves and all pull in a roughly coordinated The nests of birds are larger and more familiar t() r.r.s tlurn thosc <>f in-
fashion. Even this degree of cooperation is not sumcient when the sects, but when one takes into consideration thc tlifll'rcncc in sizc of the
leaves are separated by more than an ant's body length. This problem is builders many bird nests appear rather small and sirnplc conrpared to
solved by the ants forming chains, one seizing the edge of a leaf in her the elaborate structures built by some of the social insccts. Yet other
jaws, another holding her by the abdomen, while a third holds rhar ant's bird nests, such as those of orioles, are covercd structures with long
abdomen, ffid so on until at the end of a chain of several ants one grasps entrance tubes. The elaborate nests of African weaver birds have been
the second leafwith her hind legs. Numerous chains of ants pulling and studied extensively by Collias and Collias (1962, L964, 1984) and by
bending leaves in rough coordination form them into an enclosure that Crook (L964); these and other complex bird nests are also described by
will later be occupied as a nest. von Frisch (1974) and Hansell (1984). The nest of the village weaver
This shaping of leaves and bringing their edges together by the co- (Tbxtor or Plocews cwcwllatws) of Africa is an ingeniously complex woven
operation of numerous individual weaver ants is only part of the pro- structure, and the detailed observations and experiments of Collias and
cess. Once brought together, the edges of leaves must be joined with Collias have provided a more complete understanding of how it is built
silk. But the adult workers cannot secrete this silk themselves. It is ob- than is available for other species.
tained by carrying larvae of appropriate age from another nest and hold- The finished nest of the village weaver is a roughly spherical structure
ing them first against one leaf edge and then the other. Thus the with an opening leading downward from one side of the bottom. The
younger sisters of the workers are used as a sort of living tool in nest nest is constmcted from strips of grass or similar material, which are
constmction. woven by a series of fairly complex motions. When coufting a female,
The queen weaver ant lays her eggs, and larvae grow and are fed by the male weaver begins nest building by forming a roughly vertical ring
workers that bring food into these nests. The food consists mosdy of :rttached at two or three places to a small branch. The ring is then en-
fragments of other animals the foraging workers have killed or scav- larged at the top forming first a partial roof and later the walls of a
enged. But one leaf nest is seldom large enough to hold a growing col- roughly spherical chamber. The entrance is completed last. The actual
ony, so that while the queen remains in the first nest the workers con- building operation consists of grasping a strip of grass near one end and
stmct others nearby and then carry food, egBs, and larvae back and forth poking it with a vibratory motion, at first alongside some object such as
between them. Sometimes these colonies grow to consist of dozens of .r twig, and later into the mass of previously placed strips. When the end
nests extending over several trees. of the strip sticks in place, the bird releases its grip, moves to the other
All this social behavior, which is necessary for the survival and repro- side of the twig or nest mass, and seizes the strip again with its bill. It
duction of the colony, would seem to be facilitated if the workers were thcn pulls it through or around whatever material is already present,
capable of simple conscious thinking. When starting nest constmction trcnds or winds it about the original rwig or another piece of nest ma-
they might intentionally work to pull the edges of leaves closer together. tcrial and finally pokes the end of the strip back into the accumulating
When leaves have been bent into approximately an appropriate shape, nlASS. A constant feature of the stitching process is that, with successive
some workers might consciously realize that it is now necessary to glue lxrkings of the strip, the bird reverses the direction in which it is wound
them together and fetch larvae of a suitable age to secrete the necessary .rround some preexisting object. Different parts of the nest receive dif-
silk. Coordination of this building activity must require some sharing li'rcnt arnounts and kinds of material, so that the end result is a structure
of information about what needs to be done. But this is probably car- u,ith a virtually waterproof roof, thicker than the walls, and a short,
ried out in large measure by chemical signals which are very difficult to rorrghly cylindrical cntrance tube. When a female accepts the male's
analyze.In the case of food gathcring, however, corununicative behav- ,'otrrtship displays, antl thc ncst hc has constructed, she adds a soft, thick
ior of weaver ants ancl othcr spccics has bccn studied in sufficient dctail lirrirrg:rt tlrc l'rottonr ol'thc cgli t'h:rnrtrcr, first covering it with a thin
that wc can urrdcrstuntl rrt lcrrst tlrc lr:rsic pr()ccsscs by which cooperativc l,rvr'r'ol'strills tlr:rt slrt'tr'.rrs lionr lt'.rvcs ol't:rll gr:tsscs <lr palm fronds.
crrtlcrvors irrc c()()r'tlirr:rtctl. :rs u'ill hc tliscusscd irr chaptcr 9. r\licr'.rt't'orttplislring tlus t.rsk, slrc rnscrls nl;ulY solt grlrss t<lps with the
(ittt-slrtrrl tttrt ul' tlrl tlircts 7<)
78 Chapter Four
start building many nests in some artificial strrrctrrrc llrrrt lr:rs rrr:rny
stem end down, so that their feathery toPs Provide a soft cup. When
similar-looking cavities. The birds apparcntly l'rccorrrc corrlirsctl rrs t<r
feathers are available the female gradually begins to use them until there just where the nest is to be and never succcctl in conrplcting any onc
is a thick layer of fbathers on toP of the grass heads.
nest. As in so many cases of this kind, we tcnd ro infl'r :l t()trrl lack of
The tailor bird (Ortbotonr.us sutorius) of India constructs its nest by
thinking when animals do something foolish and wrstcful t>f cflbrt. But
stitching together leaves to form a Protective cuP-. Plant fibers or_ spider we do not apply the same standard to membcrs of our ()wn spccics, and
silk are ir"dm threads, and these are sometimes threaded through holes we never infer a total absence of thinking when pcoplc behave with
made by the bird at the edge of the leaves. While many species of birds
comparable foolishness. It is impoftant to realizc that to postulate that
.orrrt*tt their nests by a viriety of motor actions that serve to produce an animal may engage in conscious thinking is bv no means the same as
a stnrcture that is sturdy, and often is camouflaged to make it less con-
to say that it is infinitely wise and clever. Human thinking is often mis-
spicuous, the weaving and stitching procedures are especially suggestive
guided, and there is no reason to suppose that animal thinking always
of conscious thinking about the process and its results. corresponds perfectly to external reality. Our thoughts may be inaccu-
It is customary to view nest building by birds as geneticalll Pro- rate or quite different from what others see as correct and sensible. But
grammed behavior. In some species such as canaries, which build rela- crror is not the same as absence of thought.
tively simple cup-shaped nests, naive females that have never seen a nest Events in our own lives show that stupidity does not preclude con-
do construct a reasorriUty normal one when ready to lay eggs' But in the sciousness. If our usually dependable automobile fails to start, in our
case of the village weavers a considerable alnount of learning seems to
impatience many of us do something totally irrational, such as kicking
be involved. Young males build partial and irregular nests, but these are
the tires or swearing at the machine. We know perfecdy well that such
nor accepted by females. Their nest building skill-is increased if they can clisplaced aggression will not start the car, but we are probably thinking,
warch adult males building nests. Thus the male that builds the rela- "Why won't the damned bus start this morningl" or "What will happen
tively complex structures 6as ordinarity had a- lo1g period of.practice rvhen I am late at the officel" or "I should have bought a new battery
and iras ahb had abundant opportunity to watch older males build more
last fall."
complete nests. While the general pattern of a village Yeater nest is
This leads us to another challenging question about nest building
fairly constant, each male adtptt his building efforts to the immediate .urd other complex reproductive behavior of birds. When they are at an
situation, especially to the shipe and position of the rwigs where he carly stage of nest building, do birds have any concept of the finished
starts nest building.
product they are working to achieve I We might go one step further and
Birds generally-repair damaged nests in a reasonably sensible fashion .rsk whether a bird beginning to build a nest has any idea of the eggs
and do ,iot go tlrrough the entire sequence of building unnecessarily. .rnd young that will soon occupy the nest. Such speculation may be
When Collia-s and Collias removed parts of a nearly completed weaver nrore plausible in species where the females do the nest building, for
bird nest, the male rebuilt those Parts and did not go through_wasteful rhcy will lay the eggs and fced the young. M*y will feel that it is out-
repetitions of other portions of the building se.quence. The only Partid r.rgcously far-fetched to suggest that a female bird rnight think about
to this ruie involved the entrance rube. If this was damaged, ,'ggs and young as she begins to build a nest, but there might be some
the male generally built an abnormally long tube' .rtlvrrntages to such thoughts. Even a simple concept of the function the
Nestin"g birds behave in many appropriate and rational ways when
rrest will serve could help birds constmct it appropriately. But again we
raising yo".rrrg. Even simple nests are often concealed in vegetation, that
.rr c stymied by our inability to gather convincing evidence.
is, are-cbnstructed in plales where they are difficult to see. Furthermore
What can wc say about the possible conscious thoughts and feelings
the parents arrive *d d.p"rt from their nests quietly and inconspicu- , rl'ncst-building birdsl Thc conventional assumptions of inclusive be-
orrrfy. This is obviously advantageous, because many predators eat eggs lr.rviorist.s lurs bccn that ncst llriltling is a complex but predetermined
and young, and either the nest or the arriving and departing parent arc l,r'nr of'trch:rvi<lr. 'l'ltc prctlctcrtttirt.ttion n):ry stcm from genetic infor-
obvious signs that food is availablc. rrr.rtit)n ()r lc:rrrring; rlrtlirr:rril\/.s()nr('rnixtrrrc ot-thc tw<1. One clear ex-
This is i-r.rt t., say drer bircls ncvcr clo fbolish things in thc coursc ol' .rrrrPll' ol'gt'nt'tit' irrllrrt'rr((' on rrt'st lruiltlirrg h<'lt.rvi<)r stcnls fi<lm the
rrcst l-rui1lilg. V1r i,rirclr (1974) tlcscritrcs how hhckbirtls occ:rsiotr:rlly
80 Chapter Four (itrtstrurtiort ol'tlrtilirrt: tll
experiments of Dilger (1960, L962) with two species of lovebirds of of Vellenga (L970, 1980) and Warham ( 1962),:urrl conrirrrring with
the genus Agnporwis which hybridize in captivity. One, A. personntnf.s- increasingly ingenious methods in the snrdies of'llorgia ( I 9tl5a, l9ti5b,
cherc, builds its nest from pieces of bark that it carries in its beak. An- 1986), Borgia, Kaatz, and Condit (1987), antl c.s1'rcci:rlly t)iarnond
other, A. roseicollis, cuts strips of nest material from vegetation, which it (1982, 1986a, 1986b, L987., 1988).
carries by tucking them into feathers on its back before flying to the Fourteen of the eighteen species of bowerbircls btrilcl bowcrs or at
nest. In the experiments, hybrid birds cut paper strips but were ineffi- least make small clearings on the ground, which thcy dccorare to some
cient in transporting them, apparently attempting both to tuck strips extent. Bower style varies with the species. It is convcnicnt to begin
and to carry them in the bill. They improved with practice, however, with the relatively simple avenue bower built by the satin bowerbird
and most ended by carrying strips in the bill after initial and incomplete (Ptilonorbynchws violacews). Adult males are glossy bluish-purple and the
tucking movements. This is a classic example of behavioral genetics females and immarure males are green. This species has been more thor-
where there is clearly a strong inherited tendency to behave in a certain oughly studied than any other because it is common in eastern Australia
way and yet the animal does not follow the genetic instructions slavishly and sometimes builds its bowers in suburban areas where it can be ob-
but gradually modifies its actions on the basis of experience and suc- served more easily than its relatives that are found only on uninhabited
ceeds in obtaining an apparently desired and intended result. mountains of New Guinea. Vellenga (1970., 1980) took advantage of
Despite the lack of completely conclusive evidence, it seems plausible this oppornrnity by color banding 940 satin bowerbirds captured in her
that nest-building birds have some simple conscious desire and inten- garden over a period of five years. One of these individually identified
tion to produce an appropriate structure. Genetic influences may deter- birds could be traced to a park half a mile away where he maintained
mine the general pattern of the desired result, but birds certainly vary and defended his bower for fifteen years. Her observations of known
their behavior as they work to achieve this goal. Although their efforts individuals confirmed several aspects of bowerbird behavior that had
are not always totally efficient, and human observers can often imagine previously been inferred by Marshall and others on the basis of less di-
how they might do somewhat better, the birds give every indication of rcct evidence.
trying to achieve an anticipated goal. As summartzed by Diamond (1982, 99-100), largely on the basis of
Vellenga's observations :

Bowerbird Bowers 'l'[re

bower is a woven platform about I0 feet square, supporting an avenue of
\\'oven sticks, with walls a foot high nearly joining in an arch over a floor, and
In many ways the most impressive structures built by *y animals are tlccorated with blue or green natural or man-made objects. Perishable decora-
the bowers constructed by male bowerbirds of Australia and New t ions such as flowers are replaced daily. Some bowers are left unpainted, but
Guinea. Displaying males attract females to these structures, ffid mating ,thers are painted daily either blue, black, or green by the male, using a wad of
takes place in them. Darwin placed considerable emphasis on the brrrk as a paint brush and using crushed fruit, charcoal, or (nowadays near civi-
bowerbirds in his discussion of sexual selection, and more recent inves- lization) stolen blue laundry powder as paint. The long axis of the bower is
tigators have discovered many important facts about their behavior. The scnerally within 30 degrees of north-south, possibly so that the male and female
Australian biologist Marshall (1954) described and analyzed the behav- ('iul face each other during early morning displays without either having to stare
ior of bowerbirds in great detail, emphasizing physiological and endo- rttto the rising sun. When Marshall picked up a bower and reoriented it, its
crine influences on their courtship displays and bower building. Gilliard .rrchitect promptly demolished it and rebuilt it in the correct orientation. . . .
(1969) pointed out that among bowerbirds and their relatives there is l'hc bower-owning male Satin Bowerbird continually tries to entice females
rrtto his bowcr by picking up in his bill an object such as a flower or snail shell,
an inverse correlation berween striking plumage and elaborate bowers.
.rntl posturing, dancing and displaying to the female.
Species with conspicuous colored feathers used in courtship displays
build simple bowers, if any, whilc the most elaborate bowers are con- 'l'hc rlr:rlcs also call loutlly. As clcscribed by Borgia (1986, 98) the
structed by specics with rclativcly tlull plumage. More recently intcnsivc rtt.tlc "f :rccs rhc fl'ntrrlc rvhilc lrc st:rrrrls <ln thc platform. He gives a whir-
snrdics of irrclivitlu:rlly nrarkcd birtls has added new dimensions to ()rrr r irtli t':rll n'hilt' prrurt'irtg, llrrllirrg rrp lris li':rthcrs :rrrtl flapping his wings

runtlcrst:rnding of'tlrcir s<ri:rl lrch:rvi<lr, bcginning witlr thc ol'rscrvrrti<lrts to llrt'lrt'.tt ol'tlrt't'.rll. ( l.rlls.rr(' l)urrt trt.ll('(l u'itlr pcriorls of'silclrcc, quict
(itnslrtrttitttt ol'rlrttlirrtt lt.l
82 Cbapter Four

chortling buzzing, or mimicry of other birds. The female's initial re- that were orange, pitk, or red. Furthernr()rc thcv slrolvt'tl :r prt'lt'r't'rrt't'
, for blue and purple flowers that were unc()n'rn'lorr in tlrc krc:rl crrvinn-
sponse is to enter the bower and'taste,'or nip, at a few sticks. Then she
intently watches the courtship. If she is ready to copulate, she crouches
and tilts forward." Diamond (1982,I00) emphasizes the fact that
Borgia (I985b) also studied the effects <xr rtr:rting succcss ol'txrwcr
destruction by other males. He found that thc nunrlrcr of'tlcstructivc
many courtships are interrupted at a crucial stage by the intrusion of other in- attacks on bowers, and the amount of destmcti<)rrr wcrc invcrscly c<>r-
dividuals. However, another reason for the low success rate may be the invar- related with the quality of the bowers, that is, tl'rcir .symmmryr size of
iant sequel to successful mating: the male bowerbird savagely attacks the female, sticks used, density of stick packing, and general quality oflthc bower as
pecks and claws her, and chases her from the bower. Mating itself is so violent judged by the investigators. Bower destruction occurred only when the
that often the bower is partly wrecked, and the exhausted female can scarcely
bower owner was absent, ordinarily to feed, and on his return the owner
crawl away. The courtship display can appear litde different from the male's
almost always drove offthe raider. Since bower quality had been shown
aggressive display. When a courted female is won over and starts to solicit cop-
ulation, the male often changes his mind and chases her away. Thus, a female to be correlated with mating success, it is clear that the comperirive
may have to make many visits to a bower before she overcomes her fear of the bower raiding has a direct effect on the evolutionary fitness of the males.
aggressive male. After mating, the female constmcts a nest at least 200 yards In addition to partial or complete wrecking of bowers, neighboring
from the bower and bears sole responsibility for feeding the young. males often steal feathers and other decorations to improve their own
Bowers, like flags of possession, may serve as symbols of males' ProPerty l'rowers (Borgia and Gore 1986).
rights in their wars with other males. An adult male spends much time repairing All this complex interaction of competing males using elaborate
his own bower, protecting it from raids by rivals, and attempting to steal orna- bowers to affract females suggests that some simple conscious thinking
ments or destroy rivals' bowers. The batdes and territorial shifts that Vellenga rnay be involved when bowers are being constmcted or decorations
recorded among her 426 banded adult males make the European Thirty Years'
sathered and set in place . Advocates of the "sleepwalker" view of animal
War seem straightforward by comparison. . . . Dominant males directly prevent
lrchavior may be tempted to argue that because all this behavior has
other males from rvooing females by the destruction of their bowcrs. Young
srrch an obvious effect on the birds'evolutionary fitness it must be ge-
males continually try to erect rudimentary bowers in the territory of an adult
male but the latter patrols his property several times a day and wrecks them. nctically fixed and therefore mindless. But as has been found to be the
When Marshall placed 100 pieces of numbered blue glass into these rudimen- c:rse with many behavior patterns, the generally similar actions per-
tary bowers one night he found 76 of the pieces transferred to the bowers of lirrmed by members of the sarne species do not preclude a major role for
dominant males by noon the next day. Similarly, Vellenga observed a blue cel- inclividual experience and learning. Early in the mating season, as surn-
luloid band to be transferred between bowers several times a day, until one malc rrrrrrized by Borgia (1986), "young males visit the bowers and the
firmly wove it into his bower. lro$,er owners often display to them . . . fbut later] the bower owners
lrccome less tolerant of male visitors." Vellenga's earlier studies had
Borgia (I985a) and several collaborators observed the mating suc-
slrown, as sruilnarized by Diamond (1982, l0I), that
cess of many individually marked male and female satin bowerbirds,
using an automatic recording camera to monitor 207 copriations at28 nrilnv skills related to bower building and use have to be learned. Young males
bowers during one season. The number of copulations at each bowcr nr srccn plumage spend about two years building rudimentary but increasingly
varied from zero to 33, with five of the 28 males achieving 56 percent ( ( )nr[)lex bowers before acquiring blue adult plumage and building complete
of the matings. There was also a statistically significant tendency firr Ir,rvcrs. These "practice bowers" are the joint efforts of several young males,
males with well-constructed and highly decorated bowers to mate with rr lriclr takc turns placing and rearranging sticks, often clumsily and without
more females. The most attractive bowers were more symmetrical, irt- ',u( ('css. occasionally with the cooperation of more skilled older males. The
cluded larger sticks more densely packed, and were decorated with morc 1.ung nrrrlcs clo not pr:rint thcsc bowcrs and are less discriminatingthan adult
blue feathers, yellow leaves, and snail shells. In another investigation ol' ,rr.rk's irr clroicc of'colour firr bowcr tlccorations. Thc young males spend much

flower preferences Borgia ct al. (t987) found that male satin bowct'- rrnrt'u,.ltr'lrinq thc tlispl:tys, tttrttirrg:trttl othcr lxrwcr activitics of adult males,
.ul(l .lr'(' tlislll.rt,t'tl to ll1' lrtltrlt ltt.tlt's.
birds sclcctccl prirnarily l"rhrc lntl purplc flor,vers and ncvcr usccl thosc
84 Cbnpter Four ConstructionofArtifacts 85

Other species of bowerbirds build quite different types of bowers, and political obstacles. In the Wandarnen Mountains the bowers arc
but all seem to serve the same basic function of attracting females. For truly impressive huts 40 to 80 cm high and from 90 to 220 cm in di-
example, the stagemaker or tooth-billed bowerbird (Scenopoeetes d.enti- arneter formed by weaving sticks together. On the downhill sidc of thc
rostris) of North Queensland clears a roughly circular area of the forest hut is an opening 18-58 cm wide and20-28 cm high. As describcd by
floor. As described by Gilliard (L969,276),largely from the observa- Diamond (1987,189), "the hut was built around a sapling at whose
tions of Warham (L962) and Marshall (1954), base was a green moss cone 20-23 cm in diameter and I5 cm high, with
a low stick tower joining the cone to the ceiling of the hut. The hut
the male clears all the fallen debris from this space of earth as if with a broom. rested on a green moss mat."
He then decorates it with fresh green tree leaves of one or more favoured species In the Kumawa Mountains, about 200 km from the Wandarnen
. . . the leaves may be up to twice as long as the male which carries them to his range, the same species builds much simpler bowers, which lack any
bower. These leaves are almost always placed upside down on the "meticulously roofed hut but consist of maypoles, moss mats, moss cones, and stick
clean" court and are replaced with fresh leaves when they wither. The tooth-
towers similar to those located inside the huts of the Wandarnen birds.
cdged bill (for which the bird is named) serves as a specially modified tool for
In both cases small, conspicuous decorations are added by the birds.
scvcring fresh leaves. . . . At one bower Warham found 56 leaves. He removed
all of them . . . [after which] almost every day the male carried in from 2 to I0
The moss mats are "woven tightly from fine, clean, dry, dead fibers of a
lcavcs and placed them carefully on the ground couft. moss that grows abundantly on trees" (Diamond 1987, I82). These
mats at some bowers were almost perfect circles; when the diameter was
Within a week 25 leaves had been gathered to replace those that had measured across the circle in several directions it varied by only a few
bccn removed. percent. The "maypoles" were saplings I to 3 cm in diameter without
Archbold's bowerbird of the New Guinea highlands (Archiboldinpa- lcaves or branches up to 1.5 to 4 meters above the ground. The moss
puensis) makes a display ground of flattened ferns and other vegetation cones were formed from the same moss used to make the mat. Stick
but decorates it with piles of snail shells and sometimes black beetlc towers consisted of hundreds of 20 to 90 cm sticks piled against each
wing covers. MacGregor's bowerbird (Arnblyorru.is rnacgregoriae), als<t nraypole. Around the base of the tower the sticks lay horizontally, ra-
found in the New Guinea highlands, clears a roughly circular area ancl diating neatly in all directions. In both areas there was also some varia-
forms at its center a "maypole" consisting of "a column of sticks erectcd tion in size and details of construction between individual bowers.
around a thin sapling" (Gilliard L969). Moss is gathered and placed orr Most of the Kumawa bowers were decorated with dead pandanus
the cleared area around this vertical pile, which may be as much as :t lcaves 20 to 150 cm long, often leaning against the maypole sapling.
meter in height. The golden bowerbird (Prionod.wra newtoniana) <tl Some of these leaves weighed half as much as the bird, who must have
Queensland constructs a double column of sticks, each somewhat likc ,lragged them for many meters from the nearest pandanus tree. Other
the "maypole" ofMacGregor's bowerbird but with a roughly horizontrrl (()rrunon decorations were the brown shells of land snails, dark brown
stick connecting them. The male perches on this stick during Parts ()l .re()rns, brown stones, beetle elytrae, and piles of 22 to 90 brownish
his displays. All of these styles of bower construction show considerat'rlc sticks 8 to 100 cm in length. The Wandamen bowers were decorated
(f uitc differently. Most corrunon were 20 to 50 cm piles of black bracket
variation from place to place and from one individual to another, incli
cating that they are not fixed, stereotyped building behavior Pattern.s. lrurgi or groups of 4 to 32 dark brown or blackish beetle elytrae. Red
Perhaps the most impressive of all bowers are some of those cott- .rrrtl orange fruits were also present at most bowers, along with red
structed by certain populations of the Vogelkop gardener bowcrtrirtl It'.rvcs and black fungi other than bracket fungi, plus black fruits. Partic-
(Amblyornis inornotus). These have been studied by Diamond (l9tl2, rrl.rr dccorati<lns wcrc preferentially placed in certain areas relative to the
1986b, L987,1988), who not only has described how they vary bc lro\\,cr', firr instancc black and orange bracket fungi downhill from the
r L ror'. ( irklrctl flowcrs, rctl lclrrrcs, rcd, ()renlcr or green fruits were usu-
tween populations of the same species, but has demonstratcd ['ry ilrgc
nious experiments how the birds select decorations of prefbrrccl col<tt's. .rllt' outsitlc tlrc l'rowcr <lrt tltc rn.lt, :rntl otrjccts chosen infrequently as
These birds are confinccl t<l ruggccl, uninhabitccl moutrtains of-wc.slcnl ,k'tor'.llions \l,t'r'c usurllt'irrsitlt'tlrt'lrut.'l'lrt'sc rlrrc itcrns included but-
Ncw (ltrinca which rrrc vcry tliflicult t<l rcrrch [rcr':tttst' ol-lxrtlt ph1,si,.11 tr'r lltt's. lrt't't lt' ltt':ttls. .uttlrt'r lrt'r't lt's. .l( ( )r n\1 .uttl r )r-:lrtgc 1'ricccs <lf bark
86 Chapter Four (hnstnrtiort ol'Artilirctt 87
or jellylike fungus. In some cases decorations of the same color were comPanying it, Marshall relognized that thc birrls rn:rv rvcll crrjgl, thc.
grouped more or less together. When Diamond altered these arrange- bowers they build. As von Frisch (L974) pointccl out iir his lr<xrk,4zi-
ments by shifting decorations to atypical locations the birds usually put rnal Architecture, it would be difficult to deny that inrprcssing fcn"ralcs
them back where they apparendy belonged. motivates much human artistic creation. Unless .,rn^rniitt.d a-priori to
All of these observations suggest that individual Wandamen bower- an absolute human/animal dichotomyr we have no basis fbr rejeiting out
birds were expressing preferences for certain patterns of decoration. <f hand he hypothesis that a male bowerbird thinks in simple ,i.*,
Given the fact that young male bowerbirds practice bower building and rrbout the bower he.is building and decorating, the other malei comper-
watch experienced adult males building bowers and courting females at i.g with him, and the females he hopes to for mating.
them, it seems like\, that these local and individual preferences in deco- "niic.
rating bowers are learned manifestations of what Diamond (I986b,
lJeaver Engineering
3042) calls a "culturally transmitted trait, like human art styles." To test
this interpretation Diamond (1988) placed poker chips of seven bright When we consider the kinds of animal behavior that suggesr conscious
colors in or near the bowers of both Kumawa and Wandalnen bower- rhinking, the beaver comes narurally to mind. These larE. aquatic ro-
birds. In the Kumawa area, where the birds do not naturally use colored tlcnts manipulate their environment in rather spectacula. irryr io obtain
objects to decorate their bowers, most males removed the poker chips l<nd and shelter. They fell trees and construit conspicuous lodges as
placed in their display areas, and did not bring any in from nearby. At rvcll as digging less obvious bank burrows. They also deepen shillow
Wandamen bowers, however, the birds gathered many poker chips and stretches of water to form channels where they can swim and. tow
arranged them in their bowers, showing a hierarchy of preferences with branches that would otherwise drag on the bottom. Beaver carry mud
blue collected in largest numbers, followed by purple, orange, red, [av-
ilyg up from the bottoms of these channels to piles that may fo.ni small
ender, yellow, and white in that order. But these relations differed rslands. This behavior may extend to digging canals through dry land
among individual birds, and whichever color was preferred was gath- that are also used to float branches to food rtor.g. piles. fh"r. canals
ered first, stolen from other bowers first, and removed from the bower .rrld channels are not dug helter-skelter but alongioutes the beaver use
least often. Poker chips of the salne color tended to be grouped close to r, trxvel between alodge or burrow and food supplies. Finally, as every-
each other, and also close to narural objects of similar color. Two or ,,ne knows, some beaver create ponds by buil&ng dams ,iros small
three poker chips of the sarne color were sometimes stacked on top of \trcams. While they are far from being perfectly effiCient engineers, their
each other; occasionally a chip of a preferred color was piled on top of a .rctivities have a more cbvious and substantial impact on their surround-
less favored color. In general poker chips were treated in much the samc rngs than those of most other mammals
ways as naturally occurring decorations. This review of beaver behavior is based primarily on the detailed
This panopty of construction and decoration strongly suggests that o_lMorgan (1868), wilsson (r9zr), Richard (1960a, 1960b,
the bird is consciously thinking about what it is building. Of coursel It)67,1980, 1983), Hodgdon (L978), patenaude (r9g3), patenaude
determined behaviorists can always dream up complex sets of genetic ,urtl Bovet (1983, 1984), and Ryden (1989). wilsson and Richard
instructions that might operate to generate whatever behavior may bc sttrtlicd captive beaver for the mosr poft, while Hodgdon and Ryden
discovered. In the case of bowerbirds, this exercise will require morc ( ( )llccntrated on extensive observations
of wild beaver under nanrral
ingenuity than in many other cases. Ifwe allow ourselves to speculate as , , rrrtlirions. Patenaude succeeded in arranging an observation
to what these birds might be thinking as they work at their bowers, thc rlr.rt 1'rcrmined video taping of beaver behavioi inside the lodge.
god of luring a female ready for mating may well be prominent in thc Ilcrvcr typicaily live in family units consisting of a monogamous pair
content of their thoughts. Marshall (1954) and others have argued thrrt ,,1 .ttlttlts and their young. Onc litter of three or four kits aie born each
because bower building and decorating are so clearly part of the birds' ',1,r ing, rurtl thcy ustrally srey wirh rhcir parenrs for two years. The
reproductive bchavior, tlrey wcrc not accompanied or influenced by acs- lrrrlis hcJP bv fl'cdirrg rrntl gr<xrrrirrg rlrcir v()ur-lgcr sibiings, and iome
tl'rctic fcclings. Yct t<>w:rrcl thc cntl of his monograph, which cmphasizctl '.t.rr'.rvit.h tlrcir l)urcrrrs lor rr rlrirtl vt..rr'(ll<xlgtlon l97B). Alth.rugh the
thc horrn<>nal corrtr<ll <ll'[r<lwcrl'rirtl rcproclucti()n lrtttl tltc lxltrvior :tt' .r,lrrlts tkr nlort'tl;urr;uttl krtl1,,t. lrrriltlirrg tlr:ur thcir olllllrilrg, thc:ycar-
88 Chapter Four Constnrctiortol'Artifhrts ll9
lings participate to some extent. M*y aspects of beaver behavior seem rcpeated several times, always at night, after we hacl rcltrovctl thc stick.s
to vary from one siruation or population to another, so that there are no in the morning and restored the water in the po<>l t<> its nonn:rl lcvcl.
absolutely fixed patterns of behavior that occur under all natural condi- lrvery night the beavers made new calibrated sticks and bl<>ckcd up the
tions. Scientists concerned with animal behavior have paid relatively holes. . . . [Finally they] changed their technique. In addition to the
little attention to beaver despite the impressive scale and scope of beaver sticks they used grass and whole piles of leaves mixed with mud."
works. One reason is the difficulty of observing a largely nocturnal ani- M*y scientists disagree with Richard's conclusion that beaver know
mal that spends much of its time out of sight in a lodge or burrow. rvhat they are doing, claiming that all their constmction of burrows,
Furthermore, most of its body is submerged a great deal of the time,, lodges, canals, and dams result from genetically programmed action
and some of its most interesting behavior occurs underwater or even l)atterns that involve no conscious thinking or anticipation ofthe results
under the ice in midwinter. of these activities. For example, after one of the most thorough srudies
As emphasized by Richard ( 1960b , 1967, 1980, 1983), it is difficult ,f beaver behavior involving both free and caprive animals, Wilsson
to repress the inference that beaver could scarcely accomplish what they (1971,240-54) concluded that even those acrions that seem most in-
do without some awareness of the likely results of their activities. He tclligent can be explained as the result of genetically programmed motor
snrdied captive beaver in a fenced "Parc i Castors" about I80 x 60 l)atterns. He specifically disputes the conclusion reached by Richard
meters in size with a small strearn flowing through it. They built dams (1967) that beaver exhibit some degree of forecasting and "unformu-
and lodges, and Richard was able to observe many details of their be- l.rted thought."
havior and to perform experiments that tested their ability to solve
problems quite different from the normal experience of their species. I'he examples he [Richard] gives as evidence for "forecasting," "intelligence"
Some individual beaver learned to open pazzle boxes to obtain food, ,rnd "some kind of unformulated thought" can . . . just as well be interpreted as
even when this required manipulating different types of latch. When \rcreotyped phylogenetically adapted reactions. For example, the fact that a
lrcaver often thoroughly investigates a leak in the dam, then leaves it for some
confronted with food out of reach on a small platform at the top of a
Itours and later brings different kinds of material with it when it returns ro
one-meter pole, some beaver piled branches around the pole until they
r cpair it, does not necessarily mean that it is able "to forecast in the choice he
could climb up this pile to reach the food.
rtt.rkes of building materials which depends on the use made of them as well as
Richard's Parc i Castors contained nurnerous willows on which thc rlrc shape his construction will take." . . . Dam building behaviour is activated
beaver were free to feed, except for a few trees that were declared off rvltcn the animal has received stimuli from the dam for a certain time and a
limits "as in the Garden of Eden" to preserve the appearance of the park ,k'hved response is not unusual in phylogenetically adapted behaviour. (Wils-
and to provide shade. These trees were protected by a cylindrical fencc .,,tn 1971,247)
of heary netting firmly anchored in the ground and wired securely t<>
branches above the beavers' reach. But the beaver solved this problem Yet, despite this insistence that their behavior is stereotyped, Wilsson
by piling a pyramid of branches and mud around the tree, and climbing 11971, 187-89) describes how some of his caprive beaver first piled
up this pile to reach the unprotected trunk, which they then cut in their rrr:ttcrial at a water outlet, but when this did not raise the water level in
usual fashion. They did this to similarly protected trees on several differ- rlrcir tank,, they changed their tactics to a more appropriate placing of
ent occasions. sticks and mud at the inlet. Thus, as pointed out by Richard (1983),
Pilleri (1983, 99) reports an ingenious response to a novel situation ,l.rrrr l'ruilding behavior is sometimes modified as the beaver learns that
by t'wo beaver confined in an enclosure where the water level of a 3.5 x , rrrc plircement of material is ineffective in raising the water level.

2.5 meter pool 1.6 meters deep was regulated by * outlet pipc A vivicl rcccnt example of the strong tendency to deny conscious in-
equipped with a cap perforated by three holes 8 mm in diamctcr rt'nt hrs rcccntly becn exprcssccl by the anthropologist Ingold (1988,
through which the water escaped. After about two weeks the two bca- It(r, 90). I Ic p<>int.s out that orrc ol-thc carlicst scientific studies of beaver
ver began to plug thcse thrcc holcs with "peeled twigs which had bccrr .'rrgirrccring \vxs contluctctl h1, Lcs,is Ilcnry Morgen (1868), who was
gnawecl offobliqucly at both cncls by thc bcavers and whittled down irr .tls, r. in Irtgoltl's wortls, "()n(' ol'tlrt' lirurrtlt'r's ol'tlrc disciprlinc of anthro-
srrclr :r rvrry, th:rt tlrcy cxactly fittcd tlrc lrolc.s. . . . Thc pcrfirntrallcc \\/:ls l',,1,,g\':ts \t/('krltttv il lo,l.t1,''Altt'r (tlr()tinl,, Mor'11:ur's o1'riniorr tlrat bca-
90 Chapter Four Oonstnrtiurt ol'rlrttlirrl: ()

ver fell trees and build dams with at least some rudimentary anticipation doing, yet feel so strongly committed to dcnying th:rt :urirrr.rls urc c:r-
of the results of their activities, Ingold vigorously denies the correctness pable of any foresight, even for a short timc into thc lirttrrci ()r rlny
of any such infcrence . He cites approvingly the assertion by the Ameri- thoughts about the likely results of their own activitics.
can anthropologist Kroeber (1952) that (in Ingold's words) "the beaver Given this basic uncertainty and disagrecmcnt, c:ln wc throw any
dnes not artd canno, construct an imaginary blueprint of his future ac- light on these questions by considering the actual bchavior of bcavcrf A
commodation, whereas this is something ofwhich even the most'p.i-- good place to begin is their digging of burrows and c()nstruction of
itive'human is capable [italics are Ingold's]. The human engineer con- lodges. Under natural conditions most beaver dig burrows into the
structs a plan in advance of its execution; the beaver lives merely to banks of whatever strearns or lakes they occupy. Burrows start under-
execute plans designed-in the absence of a designer-through the water) and then turn upward until it becomes possible to constmct a
play of variation under natural selection." In all fairness to Kroeber, it reasonably dry chamber. Beaver seldom if ever start digging burrows
should be mentioned that he expressed this view originally in where the ground slopes too gradually to provide space for a beaver-
l9l7,long before ethologists discovered how versatile animal behavior sized tunnel above the water level. This implies that they recognize that
can be. some shores are too low to make burrowing worthwhile. As far as I
Ingold goes on to support his assertions by appealing to the author- have been able to learn from published accounts of beaver behavior or
ity of Karl Mam: "What from the very first distinguishes the most in- liom my own observations, beaver do not start useless burrows. But
competent architect from the best of bees, is that the architect has built .rborted burrows would be difficult to locate, so that lack of reports of
a cell in his head before he constructs it in wax." Proving a global nega- their occurrence is not conclusive evidence of their absence. Perhaps
tive statement, that something never happens under any circumstances, rhey make this selection on the basis of steep underwater banks, but it
is notoriously difficult; but Ingold and others deny that beaver might scems more probable, pending appropriate investigation of the ques-
be aware of the results of their actions, without presenting any convinc- tion, that beaver explore shorelines and select for burrowing only places
ing evidence to support such a sweeping and dogmatic assertion. u,here the ground rises far enough to provide space for a dry chamber
Ingold reiterates his conviction that "anirnals have no thougbts," and, rvithin a reasonable distance of the water.
"rather than thinking without corrununicating, the animal cornrnwnicntes Burrow constmction by beaver and other animals is an interesting
withowt thinking; so that the signals it transmits correspond to bodily sort of goal-directed behavior. It may even be directed toward the con-
states and not to concepts" (94 and 95; italics are Ingold's). It is difficult sciously perceived goal of providing a dry shelter. But the fact that bur-
to reconcile this vehemently negative assertion with the evidence I shall rowing occurs underground and sometimes also underwater greatly re-
be reviewing in later chapters, especially the experiments showing that stricts the sort of observational or experimental evidence that can be
pigeons can be taught something closely resembling concepts. Yet in a , rtrtained without difficult and costly special procedures. Animals can be

section titled "Thinking, feeling and intendingi'Ingold recognizes that ,,trserved starting to dig a burrow, and completed burrows can be exca-
animals are probably conscious of "doing and feeling." "Morgan in his r.rtcd and mapped; but the actual behavior of digging them, deciding
time, and Griffin in ours, are suggesting that . . . beavers . . . plan things rrr what direction to progress, and coping with obstacles such as rocks
out, or envisage ends in advance of their realization. I do not think they ( )r' trce roots remains almost totally unstudied.

do; but more than that, I do not think human beings do either, excePt When beaver burrows begun under water turn upwards as they pro-
intermittently, on those occasions when a novel situation demands a l,,r'css under and beyond the shoreline they often reach the surface and
response that cannot be met from the existing stock-in-trade of habitual l,r t'rrk through to the air. Beaver sometimes pile sticks and mud over this
behavior patterns" (95-97). No one has ever suggested that animals (,lx'ning and continue burrowing upward through the material they
nlrryt think consciously about what they are doing or the likely results lr.rvr rrtklcd. Sincc their tccth can easily cut branches and shred woody
of their activities (although on page 96 Ingold accuses me of that rr['r- rrr.rtcrirrl int<> srift bcclcling, thcy can l'rurrow from below into a pile of
surd claim, a typical example of discredit by exaggeration). What is str tlrt'ir own nrlrking rrt lc:rst rrs c:rsilv :rs thr<lrrgh r naftrral bank, where the
ptzzling is how Ingold and others can recognize the likelih<x>tl thet r'.rrtlr is olit'rt sttrtltlt'tl witlr roots;ttttl st()tr('s.'l'lris atklition of newma-
animals arc s()mctinrcs, cvcn if <lnly rarcly, c<lnsciotts of wlrat thcy rrrt' tcrr.rl nr:l\/ ()('('ur-citlrt'r':tltt't .ut .ttttt.tl oPt'rtirt11 to rltc rrir <lr shrlrtly bc-
92 Chapter Four (hnstnrctiort ol'rlrtrlirrtt 9.1

forehand. As with many other aspects of beaver behavior, different pop- five to ten meters long, and their remains can ['lc rccognizctl yc;rrs l:rtcr'
ulations seem to differ in this respect. But in either case the beaver even though grass, bushes, and even trees may havc gr()wrr u[) ()tr thclrr.
brings mud and branches from some distance to a spot on the shore Abandoned lodges are sometimes reoccupied and rcconstnrctcd.
where its burrow is close to openinB, or has already opened to the air. In many cases, except when there are very y()ung kits in a fhnrily
Bank lodges formed by adding material above a burrow often be- lodge, the beaver move about from one burrow ()r l<ilgc to anothcr in
come island lodges when the construction of a dam raises the level of the same pond or strearn, so that a shelter occupicd onc day may be
the water. But some island lodges are also built a short distance from the cmpty the next. One pleasant day in mid-May I came upotl a pair of
shore of lakes where the beaver build no dams and where the water level adult beaver and at least one youngster in a sort of "bower" under a
does not fluctuate appreciably. Hodgdon (L978) observed cases in fallen tree partially screened by surrounding vines and small branches
which the beaver started an underwater burrow at a place where the but clearly visible from my kayak as I paddled down a small stream in
water's depth varied steeply although all the immediate area was under the New ]ersey pine barrens. The nearest lodge was three or four hun-
water. When the burrow broke through the earth, still below the water cired meters away, and the very gently sloping shoreline provided virnr-
surface, they piled branches and mud over the opening and thus created ally no opportunity for burrowing. These beaver had presumably come
an island lodge. out or stayed out after daybreak although they must have had some
The beaver that Hodgdon observed extensively at close range always other shelter. This "bower" was later converted into a typical small
began lodge building by at least starting to dig a burrow under water. lodge by adding sticks, leaves, grass, and mud to the walls.
When the bottom was too rocky for burrowing, these beaver went Beaver vary their lodge and dam building in different situations, and
through the motions of digging before piling up material that eventu- they use many sorts of material according to what is available. Some i

ally became a lodge. But Richard (1980, 95, fig. 53) describes a large beaver adapt their building behavior to atypical situations, such as ones
lodge that had been constructed when a flood inundated the beaver's tlrat built lodges inside caves (Grater 1936; McAlpine 1977; Gore and
burrow and which was later exposed after falling water level left it high llaker 1989). They may modify human artifacts-for example, adding
and dry. The lower portion was entirely composed of sticks piled up by sticks, mud, and even stones to a concrete dam and thus raising the
the beaver, through which an access tunnel had been excavated. This led water level above what the human dam builders intended. Or they may
into a chamber above the highest water level large enough for two per- truild nesting chambers inside abandoned, or even occupied buildings
sons to squeeze into. Since the actual constnrction of this lodge was not ck>se to strearns, such as unused mills (Richard 1980). These modifica-
observed, there is no way of knowing whether the beaver began with an t ions of behavior suggest sensible use of available resources rather than

attempt at burrowing. rhe unfolding of rigid, stereotyped genetic programs. l

Aeschbacher and Pilleri (1983, 98) found that when captive beaver One of the principal foods of beaver is the bark of trees, but they also
built a lodge, they "cut sticks of rwo different lengths from the branches t'rrt other vegetation such as tubers of water lilies dug up from the bot- i

provided, peeled them and inserted the longer ones into the roof of thc tom of their ponds. They may totally consume small branches up to i

main chamber and the shorter ones into the chamber entrance, in a .rtxrut a centimeter in diameter; but from larger branches or the trunks
more or less radial pattern which was afterwards plastered with mud, , rl' saplings they strip off only the bark and leave a shiny bare surface

wood shavings and small twigs." Richard also describes cases where thc rrrottleC by characteristic tooth marks. Their digestion is aided by sym-
beaver gathered appropriate material before starting to build, suggest- lriotic microorganisms, and their intestine, like that of most herbivo-
ing anticipation of the constmction. r( )us nlarnmals, has large branches or caecae where slow digestive pro-
( ('sscs takc place . Beaver produce two kinds of fcces, one of which they
Under natural conditions beaver add to and alter lodges and bur-
rows, so that these shelters are in a constant state of enlargement ancl t'.rt rrncl thus rccirculate somc foodstuffs, presurnably accomplishing in
modification, somewhat like medieval cathedrals. Lodges and burrows tlris wrrv a nr()rc complctc digcstion of otherwise intractable materials.
are often abandoned, even when the beaver remain in the vicinity antl Orrrtirrg trccs is pcrlrrtps tlrt' lrcst known <>f bcaver activities. Most
build new shelters. Even aftcr they are abandoned, beaver lodgcs rrrc tr('('s ('ut b1,[rs111,1'1':trc n() rlt(]r'('tlr.rrr l5 to 20 crn irt clianrctcr, butocca-
substantial pilcs of nratcrial, somctimcs rwo or thrcc nrctcrs higlr urtl '.rort.rll1,:t tnutk.rs tlrit'k.ls ()n('nr('t('r ts st'r,t'r't'tl. Wlrcn thc trcc fhlls,
94 Chapter Fowr (itttslrtrtlrottol';lrttlirtt ()5

most or all of the branches are cut into smaller sections that the beaver as a small stick or a rocky ledge on the bottorrr ol'tlrc slr'('.u'rr. As rlrc
can tow through the water. The bark may be eaten immediately, or sec- water level rises more material is added, ustrally with rrrost ol'it pl:rccrl
tions of tree trunk and branches may be transported to underwater food where the water is flowing most vigorously. lticlurrtl poinrs otrr thrrr
piles near the lodge or burrow. Beaver tend not to use tree trunks or laying sticks roughly parallel to the directiorr in rvhich thc wlrtcr is flow-
branches with edible bark for building lodges and dams. For these they ing gradually produces, as the dam grows highcr, iu'r arrily of'.sticks rlri-
usually employ sticks or logs from which the bark has been stripped, cnted at increasing angles to horizontal. But many sticks arc oricnrcd in
dead trees or fallen branches, and portions of trees whose bark is ined- other directions, so that the eventual dam is a tanglc of branches and
ible or is eaten only rarely. When accumulating unden /ater food piles or rnud. Manmade objects are sometimes also incorporatcd into beaver
building dams, beaver sometimes actively thrust one end of a stick into dams, such as pieces of sawed lumber or plastic. Although beaver apply
the mud or the previously accumulated tangle of branches; this prevents rnud and soggy vegetation to the upstream face of their dams, this does
the stick from floating to the surface or being carried away downstream not produce a watertight stmcture, and usually more water trickles
by the current. through or under a beaver dam than flows over the top. But beaver
Although these activities seem directed toward an end result that is rlams do commonly maintain a pond that may be a meter or more deep
useful to the beaver, they are by no means perfecdy efficient. Some trees on the upstream side of the stmcture.
are cut halfivay through and then abandoned, others lean against neigh- Wilsson (L971) and Richard (1967,1980) have tested the hypothe-
boring trees as they begin to fall, so that the beaver obtains no food at sis that the sound of running water is a stimulus to placing material on
all. Beaver do not seem to realize in such cases that by felling the tree rvhat will eventually become a dam. Playbacks of recorded sounds of
against which the first tree has lodged they could obtain a double supply running water did elicit piling of material close to the loudspeaker; but
of bark rather than nothing at all. Occasionally one finds tree trunks that often this response occurred only after a considerable period of time.
have been cut partway through at two or more levels. Beaver of different lUchard (1967) found that playbacks of the sound of running water
sizes can chew effectively at different distances above the ground, or :lttracted the beaver's attention, but that lowered water level and inspec-
such multiple cuts may result from activity with and without an appre- rion of the leaking dam led to the placement of most material where it
ciable depth of snow. But they sometimes occur in areas such as the New rvas needed to stop the leak. When pipes were inserted through the
Jersey pine barrens where there is not enough snow to account for them tlam, the beaver initially tried ineffective measures, such as placing mud
on this basis. on the dam itself near the noisy outflow from the pipe. In many cases,
Inspection of areas where beaver have been working shows that they lrowever, they eventually discovered the place where water was entering
expend more effort than what we can see would be necessary. Even after thc pipe, and plugged this opening, even when it was several meters
branches or tree trunks are brought to ground level they may be cut into upstrearn from the dam and near the bottom of the pond. In one exper-
sections as short as 15 to 20 cm, although sticks as long as two or three irncnt a long pipe with a strainer at its entrance was arranged so that
meters can be transported; these short sections may be taken into the rvrrter entered the pipe well above the bottom of the pond and far up-
lodge where the bark is eaten, or the whole piece may be shredded to strcarn from the dam. The beaver evenrually piled material under the
form bedding. It is easy for us to judge from inspection of beaver works srrrtiner to create an underwater shoal, to which they then added
that they could have accomplished their apparent objective with much t'rrough mud and vegetation to plug the strainer and stop the escape of
less work than was actually expended. But lack of perfect efficiency in \\':ltcr.
accomplishing an operation does not Prove the lack of any conscious Altlrough sounds are clearly lne strrltrlus to dam building, these ex-
plan. pt'rinrcnts show that adding of material to a dam is by no means a rigid
Beaver dams are built by gradually adding sticks, mud, and occasion- r('slx)nsc to this particular stimulus. Most material is added on the up-
ally stones to some relatively narrow portion of a flowing strearn. I havc \t r'('ilnl siclc of tl'rc clam cvcrr th<ltrgh thc loudest sounds of running water
weighed stones up to 3.3 kg from a small dam, and Richard (1983) .rrt' ustr:rlly orr tlrc dowrrstrcrrrtt lltcc. Llndcr narural conditions beaver
reports use of rocks as hear,y as l0 kg. Ordinarily the dam is bcgtrrt l,ilt' rrr:rtcri:tl ortl1, ltt .t li'u,ol'rrt.ur1' Pl:tt't's wltcrc w:ltcr is nrn'rbling nois-
whcrc thcrc is alrcady s()nlc small <>bstruction t() thc flow <lf watcr suclt rlt'. Wlrcn lrt':lt't'r':trr':ttl.lttt1,, srn.rll .un()unts ol'rtuttt'rilrl r<l somc of the
96 Chapter Four Oonslnrrtiort ol',,lrltlitttt ()7

places where water is flowing out of the pond they are occupying, they used for food if he cut it at all. Three othcr bc:rvcr lirxrr rlrc r'o[1rv
often bring nothing at all to larger leaks where a much noisier flow is ioined in relatively fruitless efficrts to fix branchcs r<> rlrc rop ol'rhc r.,ci<
occurring. If the sound of running water were the only stimulus for dam pile_over which the water was cascading, although durirrg nl:lny rrights
building, one would expect to see piles of sticks and mud at many places of observation they had seldom been obsencc'l at rhc tlarn.
where the sound of running water was present; but this is far from being adding branches to the top of the largcly subrncrgctl r<rck pilc
^ ..w-h."
the case. The view that dam building is a simple, fixed action pattern failed to slow the torrent that was draining thcir pond, thc beaver
released uniquely by the sound of running water is a typical reduction- changed their tactics within a few minutes. Instcad <>f towing more
istic oversimplification. branches to the hole in the dam, they dove to the bortom of the pond,
Beaver dams are often damaged by strong currents after heavy rains gathered mud and vegetation such as water lily stems, leaves and ioots,
and snowmelts, and beaver usually repair breaks in actively maintained and used them to plug the underwater gaps between rhe rocks. This
dams; but this may not happen for hours or days. Dam building and slowed the escape of water from the pond, ffid in time the combined
repairing is more prevalent in late srurrmer and fall than earlier in the cffcrts of the beaver and their human helpers stabilized rhe warer level,
year. Occasionally, however, an especially disastrous break elicits strik- but at a much lower level than that of the original pond. Beaver ordinar-
ingly energetic and appropriate behavior. One of the best examples of ily gather mud and underwarer debris and apply such material to the
such emergency responses is described by Ryden (1989) in the course rrpstream face of the dam after they have piled sticks at one of many
of extensive observations of a beaver colony whose members were cut- places where water is flowing. But in this case they seemed to recognize
ting only a few trees because they were feeding primarily on water lilies. that stick piling was ineffecrive and rurned instead to plugging unde.-
These beaver were relatively habituated to human observers whose pres- water gaps between the stones, even though the noise of flowing water
ence did not seem to alter their normal behavior. For several weeks the carne from the top of the rock pile.
adult male had been doing most of the dam maintenance. At nearly the Ryden watched the beaver work for most of the night at this dam-
sarne time every evening he inspected it and added small arnounts rcpairing endeavor, leaving only in the early hours of the following
of mud here and there; but his mate and the yearlings rarely visited rlrorning for a brief rest. When she returned, the beaver had retired to
the dam. their lodge . Late in the afternoon, at his customary time of emergence
Then one day in late )une, human vandals tore open a large hole in liom the lodge, the adult male's first act was to remove a large stick?om
the dam, causing a torrent of water to rush out of the pond. The water r hc lodge itself and tow it 100 merers to the dam for further repair

level dropped at a rate that clearly threatened to drain the pond within t'flbrts. Ryden had been watching the beaver pond conrinuously for rwo
a matter of hours. Ryden and a companion were naturally outraged at Itours beforehand, and in all probability this beaver had not visited his
this wanton destruction and sought to reduce the damage by piling ,lrm since retiring some twelve hours earlier. Yet he performed this most
large stones in an arc upstream from the opening in the hope that this unusual action of removing a branch from the lodge and towing it to
would slow the flow of water and help the beaver repair their dam, even t lrc dam, presumably because he remembered the need for material to

though almost all of the stones were underwater. When the adult malc n'pair the damaged dam. Other beaver also removed sticks from the
emerged from the lodge at the normal time in the late afternoon and k xlge when they emerged and brought them to the dam.
made his customary visit to the dam, he immediately responded to this while the beaver were inside the lodge, Ryden and her companion
emergency with drastically altered behavior. He first cut a few small lr.rtl brought many dead branches to the pond to provide the beaver
branches and towed them to the gap in his dam where he succeeded in u'itlt matcrial for dam repair. They did this because there was so little
pinning some into the newly placed rock pile, although others washctl ,rr':rilrrt'rlc ncar the shores of this pond. On finding this floating tangle of
away downstream. lrr.urchcs, thc beaver began ar once to use them for dam repair, piling
At this pond there were very few dead trees available for the beavcr' nr.rrr)/ of'tltcsc branchcs ()n t()p of thc nraterial they had added to the ar.
to gather as dam building material, primarily because human picnickcrs .l sltxtcs ths: night lrclirrc. In tirnc thcy succccdcd in restoring a func-
had used them for fircwo<>d. In this crncrgency situation thc bcavcr ctrt Itotl.ll tl:tttt. Mcrurrvltik' tlrc \\'.ll('r' lr:rtl l:rllt'rr so low that thc cntrances to
anc'l brotrght to thc cllnr grccrr vcgctrrti<ln that ltc worrkl <lthcrwisc hlrvt' tlrt'kxlgt'sltt'ltt'rirrg.r lrttt'r ,l ktts lt.r,l lrctornt't'x1'rosctl. Sonrcclays later
98 Chapter Foar (itnslnrrtirm ol'rlrttlircts ()1)

the beaver reconstructed the entranceways so that these were again un- use in dam repair observed by Ryden is an cxtrcnrc cxlrrrplc. I',r,cn thc
derwater. dams are sometimes modified by removal of rnatcrial :r.s wcll :rs lry atltli-
Further dam building with sticks and mud gradually raised the water tion of sticks, mud, or stones. In winter bcavcr;ronrls in northcrn lrrti-
level, but only slowly over many days. During this period, despite the rudes are often frozenover for many weeks. I)uring thi.s tinrc thc bcavcr
lack of any very noisy flow of water, the beaver added material to the must either remain in the lodge or swim undcrwatcr l'rcncath the ice,
top of the dam, and above the water level. This is something they do holding their breath, to reach their food storage pilcs or to travel to
not ordinarily do when building a dam, although Hodgdon (1978, <rther partsof the pond. Several observers, including Wilsson (1971),
209) describes other instances of "over compensation of repair effcrts Hodgdon (L978), and Ryden (1989), have noted that beaver some-
. . . where repaired dam segments became higher than the normal dam times open holes in their dams, thus causing the water level to drop and
crest"; and similar behavior is reported by Wilsson (1971) and Richard creating an airspace under the ice. Such holes in the dam have not been
(1967). Ryden, however, has observed many repair efficrts in which the rcported under other circumstances, to the best of my knowledge . Ot-
top of the dam was kept almost perfectly level and is no higher at the tcrs also make openings in beaver dams, as described by Reid, Herrero,
point where a break had been repaired. In these situations when beaver rrnd Code (1988), but their openings are usually trenches at the top of
adapt their behavior to changing circumstances) are they perhaps hope- the dam rather than tunnels.
fully anticipating a higher water level that would restore their pond to Opinions differ as to why beaver cut holes in the dams they have so
its former depthl Of course one cannot be at all sure of such a specula- lrrboriously constructed and maintained in previous weeks or months.
tive inference, but it is a possibility worthy of further investigation. One One possibility is that the resulting air space under the ice makes it un-
way to learn more about this behavior would be to inquire whether such llccessary to swim under water to reach their food stores or to travel
"overcompensation" occurs only, or primarily, when the break being re- lirrther from the lodge and perhaps reach openings in the ice through
paired had lowered the water level below its former level. Or is it just as rvhich they can come out on land to seek fresh food. Hodgdon (1978,
likely to occur after a relatively small break that has not resulted in a 124-25 and209-I0) observed twenty-two beaver families during long
significant drop in water level? pcriods in midwinter when they were confined under thick ice for weeks
Ingold (1988, 97) claims that only members of our species ever plan .rt a time. Eighteen of these family groups cut thirty-one holes in their
things out'(on those occasions when a novel situation demands a re- tlrrms, six being "beaver-sized tunnels completely through dams." Most
sponse that cannot be met from the existing stock-in-trade of habitual ,rf these beaver-created breaks were made in the late winter when rising
behaviour patterns." Such drastic breaks in a beaver dam as the one de- u,rrter levels probably began to flood the lodge. They lowered the water
scribed by Ryden are fornrnately rare events, and it is highly doubtful lo,e[ by as much as half a meter, although usually they produced a l0 to
that these beaver had ever before encountered a problem of this magni- 15 cm air space under the ice. The important point is that the beaver
tude. They certainly had never experienced human helpers placing large rcvcrsed their normal behavior with respect to their dams, cutting holes
stones in an arc upstream from a major break in their dam. Their first r.rthcr than adding material. It seems reasonable to suppose that they
response was to bring branches to the damaged dam and try to pin lrrrcl some objective in mind, unless, like Ingold, we refuse to consider
sticks into the stone pile. But they soon changed their behavior to dig- rlrc possibility of any sort of conscious intention on the part of beaver.
ging up mud and vegetation from the bottom of the pond and using it 'ltl account for such reversal of their customary behavior of adding
to plug underwater spaces benveen the stones. Later they transferrecl rrr:rtcrial to dam or lodge as the thoughtless unfolding of a genetically
material from lodge to dam. These were novel and appropriate rc- (l('tcn"ltiltcd program requires that we postulate special subprograrns to
sponses to a wholly new situation without precedent in their expcri- ( ( )\1cr nurrcrolls special situations such as rising water in midwinter

ence. u'lrcrr thc 1'roncl is covered by icc. Such posrulation of a genetic sub-
Beaver often rework material they have built into their lodgcs, not l)r'( )Fr:lnr crrn rrlwrrys bc advatrccrl as urt cxplanation of any behavior that
only adding new branchcs and mud but shifting material to ncw 1'rosi- rs otrscrvctl; [rrrt tlrc Pl:rrrsitlilitt,ol'sttt'lt "utl hoccry" fhdcs as their ntun-
tior-rs. Thc taking of l'rrlnchcs fionr thc lodge sheltering young kits lirr l,t'r .rrrtl intri(':r('\/ irrt'r'c.rst's. A sirnPlt'r' .ttttl rtt<lrc P:trsint<lttiotts cxplana-
I00 Chapter Four

tion may well be that the beaver thinla consciously in simple terms CHAPTER FIVE
about its situation, and how its behavior may produce desired changes
in its environment, such as deeper water when there is no pond, or an
air space under the ice in midwinter under the conditions where Hodg-
don observed that a large majority of beaver families cut holes in the Tools a,nd Specinl Devices
dams they had previously constmcted.

he use of tools by nonhuman animals has often been considered

a sign of intelligence, and at one time it was believed to be limited to
our closest relatives, the apes and monkeys. But prolonged and inten-
sive observation of animal behavior has revealed many instances of tool
use, and even of preparation or construction of simple tools, in a wide
variety of animals ranging from insects to birds and mammals. Some
scientists such as Hall (1963) have reacted against the trend to interpret
tool use as especially telling evidence of rational behavior by arguing
that it is not so special after all. Beck (1980, L982) and Hansell (1984,
1987) have both reviewed the many known cases of tool use by animals,
but they have also expressed the opinion that the use or even the prepa-
ration of tools does not necessarily indicate greater mental versatility
than many other kinds of behavior.
Other types of animal behavior, such as the shell dropping by gulls
tlcscribed in chapte r 2, arejust as strongly indicative of thinking as tool
trsing. But the latter is certainly one important category of behavior in
rvhich it would appear especially valuable for an animal to think con-
sciously about what it is doing. Even in relatively simple cases of tool
trsc, the object used as a tool is something different from whatever the
.rrrimal uses it for. In an especially impressive type of tool preparation
.urd use, a chimpanzee breaks offa suitable branch, strips it of nvigs and
lcrrvcisr carries this probe some distance to a termite nest, pokes it into
tcrnlite burrows, and then pulls it out and eats with apparent relish the
tt'rrnitcs that cling to it. Such tool use differs significantly from digging
rrp l'rurrowing prcy or otherwise capturing it by direct action, because
.rll lrut thc final stcps requirc sceking out, modifting and manipulating
sonrcthing vcry dillcrcnt fionr thc f<xrd tl'rat is thus obtained.
Altlrotrgh othcr typcs ol-trch:rvior rrlso cntril acting on objects quite
,lilli'r'crrt lrrxtr tlrosc irtvolvt'tl irr tlrt' lirr:rl t'r)nsun)nllltr>ry l-rchavioq tool
rrst', llntl t'spt't'ilrlll,tltt';rrr'1t.rt,rtr()rl ol tools. tonstitrrtcs:ut c.s1'rcciallyclis-

102 Chapter Five Tools and Special Dnices 103

tinct separation of specialized behavior from the goal attained. To be close a burrow
w_h_ere they have laid an egg, as rcvicwed by Evans and
sure, when a rat runs through a maze or a pigeon pecks a lighted key, west Eberhard (1967) and Beck (1980). Ar .*r..,ple of this type of
these actions also differ from obtaining food from the end of the maze behavior has recently been described in detail by Haeseler (l9gi). ri-
or from the magazine of a Skinner box. But selecting a suitable object nally, the use of silk secreting larvae by the *.ru., ants, described in
to use as a tool entails a more independent action on the animal's part, chapter 4, involves the use of these living tools during rhe construcrion
the adaptation of an otherwise unimportant object such as a branch or of the leaf nests.
t*ig to a specific purpose. Therefore it is appropriate to retain much of An .especially striking case of complex rool use is presented by
the commonsense view that tool use, and especially tool manufacrure McMahan's discovery that certain neotropical assassin bugs ..fish,, for
or preparation, are rather special, although of course not uniquely in- termites with the corpses of previous victims. These insects-acrually em-
dicative of conscious thinking on the animal's part. This chapter will ploy two different-types of tool when capruring termires. First they pick
review not only significant cases of tool use in the customary meaning up articles from the outer surface of the t.r-it. nest and apply'them
of that term) but two other cases of specialized behavior by birds that liberally to the ourer surface of their own bodies. This rpprr*ity pro-
are akin to tool use in strongly suggesting simple thinking about some- vides as an effective sort of camouflage, whether tactile,^olfactory, o.
thing the animal is trying to accomplish. both. Then, having caught one termite at an opening into the nesi and
Although tool use is relatively rare, it does occur consistently in sucking its internal juices, the assassin bug dangles iir. .orpre into the
many groups of relatively complex animals. The suggestive examples opening, where it attracts other termites thrt .r. captured in rurn. One
mentioned below, as well as many others, are clearly reviewed by Beck assassin b^ug was observed to consume thirty-one iermite workers
(1980). Certain crabs pick up anemones (which give off stinging ne- means of this combination of camouflage and baiting (MacMahan
matocysts when disturbed) *d either hold them in their claws to ward t982,1983).
offattackers (Duerden 1905; Thorpe 1963) or hold them close to parts M*y cases of tool use by birds have been reviewed bv chishorrn
of their exoskeletons so that the anemones attach themselves and form (1954, L97L, and 1972). usually these involve using some small object
a protective outer covering (Ross l97l). Ant lions and worm lions were such as a mig or piece of bark to remove an edible iisect from a crevice
mentioned in chapter 4 because the pits they constnrct are functional where the bird cannot otherwise reach it. The bird may simply pick up
artifacts. But their prey-catching behavior also includes the throwing of a suitable probe or it may break off a rwig and bring it to'the^.reuice
small grains of sand at the ants or other small insects that fall into their fiom which it evidently wants ro remov. * it.m oifood. sometimes
pits, and this constitutes a simple form of tool use, as described by birds such as the marabou srorks observed by Marshall (19g2) seem to
Wheeler (1930) and Lucas (1989). But the ant lion does nothing to be trying unsuccessfully to probe for food *itt sticks. Cjne olthe best-
modify or improve the grains of sand or other small particles that it known elamgl_es of such tool-assisted food gathering is practiced by
throws. It is not even clear that the throwing is particularly directed at rwo species of Darwin's finches, discussed in chapter z withreference to
the prey. tlre specialized habit of feeding on the blood of boobie s. cactospiza pal-
Other insects, however, carry out more specialized tool-using behav- lid'a pries insect larvae, pupae, and termites from cavities l, d.rd
ior. Ants of the genus Aphnenognster \se crude sponges to carry back to lrranches with the aid of cactus spines or rwigs held in its beak, and
their nests semiliquid foods such as fruit pulp or the body fluids of prey, lteliobates uses similar tools to remove prey from crevices in mangroves
as described by Fellers and Fellers (1976). They pick up bits of leaf, (Ourio 1976, 164-65; Grant 1986, 3,- 372).
wood, or even mud and hold them in the liquid long enough for appre- Bowman (1961) ,r,d Mitlikan and Bowman (1967) srudied the
ciable arnounts to be absorbed before carrying back the wetted, sponge- of such tool-using behavior by captive Galapagos finches, and
like object to the colony. This enables them to transport as much as ten f<rrrcs and Kamrl (L973) observed that a ciptive utuelay learned to use
times as much of the liquid food as they could otherwise carry. Wasps of Prot'rcs and pieces of paper to obtain otherwise inaccessi"ble food. Some-
the genus Arnrnophila and Sphex hold in the jaws a small pebble, a piecc *'h:rt sirr"rilar tool use by green jays in Texas has also been reported by
of wood, or other small object and usc it to tamp tl<>wn soil usccl to (i.ryorr (1982). Sonrc of thc l'rtrngry blucjays tore pieces
of paper of
I04 ChaPter Fhte
Tbok and Special Devices I05

roughly appropriate size and shape from the sheets of newspaper lining
with rwo horizontal poles well above the ground. The ravens had been
"bonom fcd for many months with road-killed animals and other pieces of meat
the of their cages and used the pieces as crude tools to rake into
placed on the ground within the cage. During the experiments Heinrich
the cage food pellets that they could not otherwise reach. The behavior
provided the hungry ravens with only a small piece of meat suspended
varied"consideiabty among individuals; some did not learn it even when
from one of the horizontal poles by a piece of string. At first the ravens
given abundant oppotn t ity to observe other birds obtaining food in
flew to the suspended food but were unable to detach anything edible
Ihir *"y. It is thus anyhing but a stereotyped fixed-action plttern. It is
from it; they also seized the string while perched on the horizontal pole,
possible that after faiiing to reach a food item with its bill a bird inten-
and pulled at it from time to time. But the string was too long to allow
iionally picks up and.rs.r nvig or other object to aid in this endeavor.
" a single pull to lift the meat within reach. After six hours one raven
But many randbm movements seem to precede even the crude and oc-
suddenly carried out a complex series of actions that did bring the sus-
casional use of toot-like objects by captive jays'
pended meat within reach. This entailed reaching down, grasping the
Crows and their relatives are versatile and ingenious birds that some-
times use tools to a limited degree, as reviewed by Angell (1978)' Reid string in the bill, pulling it up, holding the string with one foot, releas-
captive rook used a standard drain Plug ing it from the bill, reaching down again to grasp the string below the
(1982) reported that a younf-depression
in in its aviary cage and thus to pole, and repeating the sequence four or five times.
io .tor. the drain hole a
that would otherwise have escaped. )anes (L976) de- For a few days only this raven obtained suspended meat in this way,
rerain rainwater
of nesting ravens dislodged small stones that fell in but in time all but one of its companions began to pull up the string,
scribes how a pair
nvo who had ctimbed close to their nest hold it with one foot and repeat these actions until the food could be
the general diriction of people
Heinrich 1989) observed similar behavior by reached directly. They performed this feat in slightly different ways; two
and"young. But 1ilSA,
believes that it may be "displacement b.ehav- birds moved sideways during successive stages of holding the string
wild and claptive ravens and
ior when they are angry or frustrated." When ravens are disturbed near with the foot so that the string was held at different points along the
*d yort often strike at all sorts of available objects, so horizontal perch. The other two piled the string in loops, standing in
their n.rt g, they
from-b.anih.t ot which they are but, as Hein- roughly the same spot while holding the string. All but the first raven
that twigs fall -perched; to perform this string-pulling action could have learned it by observing
rich poiirs our, the dropped objects have never been observed to strike
the successful bird, but Heinrich's impression was that each bird solved
the intruder.
Another type of tool use that has been observed in a few species of the problem for itself, using slightly different maneuvers, although its
efficrts to do so may well have been encouraged by watching its compan-
birds is throwing stones or other hard objects at eggs that are too strong
ion obtain food in this unusual manner.
to be broken by-pecking or other direct attack. The best-known example
Heinrich also observed a further indication of real understanding by
is the dropping bf ,torr., on ostrich eggs by Egyptian vultures, as de-
the ravens that had learned this specialized form of food gathering.
scribed f"i, UV Goodall and van Lawick (1966). Just how this behavior
When a raven is startled while holding a small piece of meat in its bill, it
is acquired is-not clear, although Thouless, Fabshawe, ffid Bertram
typically flies offwithout dropping the food. But all four of Heinrich's
(1980) suggest that rulrures firsi learn to associate small eggs that.they
ravens that had obtained their food by the string-pulling maneuver al-
ian breakirlitt the food they obtain in this way, and then, recognizing
ways (in more than one hundred trials) dropped the meat before flying
Iarge ostrich eggs as potential food, learn that these can be broken by
haiing srones I[pp.i on them. Flowever this sort of tool use develops,
to another part of the cage. They apparently realized that the string
rvould prevent the meat from being carried away. One raven never did
it seeirs likely thai-the vulrures are thinking about the edible contents
they pick uP stones and drop them' lcarn to obtain food by string pulling, although it had obtained food
of the ostrichegg as
fiorn its string-pulling companions. !\rhen this less talented bird was
Heinrich (iri"preparaiibn; his recently studied a specialized.form of
.stertlcd while holding a piece of meat still attached to a string, it did fly
tool use by ravens t^hat suggests insight into novel and somewhat colll-
plex relatibnships. Five rivlns were captured as ncstlings a'd hcld i.
offwitl'rout rclcasing the meat-which was jerked from its bill when the
srring lrcc:rrnc trrrrt.
-[ko cr()ws failed to obtain suspended meat by pull-
i..g" outdoor.rg"r until rhc1,1vc.. wcll grow.. Tlrc crtgc wrts ccltrippctl
106 Chapter Fr,ue Took and Spuial l)uicrs 107
ing up and holding string; and they initially flew offwith meat attached They sometimes keep a favorite stone tucked undcr thc
urrnpit filr re-
to a string, although they learned not to do so after five and nine trials peated use' Some ofters use discarded bottles as anvils
in.stcad <>f str>nes
resPectively. (Woolfenden 1985). others have learned that small
oct.1-ri ..t..rt i,rto
Small caged birds have been trained to obtain food by pulling on empty aluminum cans; these ofters have been obscrvcd
,,i b.i,rg,h. o._
strings, as snrdied in detail by Vince (196I). But in all cases a consider- cupied can to the surface, where they tear it ope.
wirh the tecth to ex-
able time of trial-and-error behavior was necessary before the trick was tract and ear the.
learned. In Heinrich's experiment the four successful ravens seem to r.:T 9.jgp.^ (Mcclenighan *d' A-" s 1976). It wourd
helpful ro think in simple terms about the fbod rrr.yi"f"
io ob_
have had the insight that pulling and then holding the string would by these specialized procedures.
bring the food within reach, Each bird carried out the whole sequence some species of primites engage in tool use quite often,
. but others
the first time it was attempted, holding it with the foot, and repeating do.so rarely-if at all, as revieweJ ii
a"tail by Beci (I9g0). Mo* of the
the process at least four times. Heinrich had watched the ravens at all objects used as tools are stones or pieces of *ood,
wtricn are used to
times when food was suspended from a string in their cage, and they break open nuts or to throw ,t otir.. animals or
peopre. parker and
did not engage in partial or incomplete actions that gradually developed
$iu:o.1 Qllo),^wgstergaard and Fragaszy (r9g7), and chevalier-
into a successful food-gathering procedure. They had never had access skolnikoff (1989) have-provided ,e,ri.*, of tool use and
to strings or stringlike objects such as vines; and in his extensive obser- "*..irir,.
manufacture of simple too! by monkeys and apes. chimpanzees and
vations of wild and captive ravens Heinrich has never seen them pulling capuchin monkeys (genus cebus) are cliarly
on vines or other stringlike objects to obtain food. use tools than other species. some but not.all captive
inclined to make and
capuchin monkeys
Tool use by mammals is not widespread; except among primates and display considerable inventiveness in fashioning probes
used to obtain
elephants it is scarcely more prevalent than with birds. Beck (1980) de- otherwise inaccessible food and sponge-tike ,Joi,
to take up riquids.
scribes simple cases of tool use by three species of rodents, tool-assisted Ritchie.and Fragaszy (1988) des.rib.s"ho\ry a mother
capuchin ..rianu_
digging by a pocket gopher that held small stones or other hard objects facrured, modified, and used simple tools to manipulJte
h., irirrrt,,
between the forepaws, the leaning of an oat stalk against the wall of a head wound, and applied modified plant materials
to the wound.,, wes-
glass aquarium by a captive harvest mouse that used it to climb to the tergaard and Fragaszy conclude thai they are almost
as versatile in this
top of the enclosure, and the throwing of sand at snakes by ground type of behavior as chimpanzees. chevalier-skolnikoft- (irrti^.or_
squirrels. Rasa (1973) has described how the dwarf mongoose breaks cludes from her review of tool use by capuchins
that in some individuals
eggs by throwing them backwards between its hind legs against some this behavior conforms to all six of piaget's stages of ..rrrorimotor
intel- i'

hard object. Elephants are trained to hold various objects with the ligence. The mury conmentarors on hZ..revi"ir e*p."ss
a wide range of
trunk, and wild elephants have been observed to use sticks to scratch at murually contradictory interpretarions, but it seems clear,
on balance,
parts of the body that are difficult or impossible to reach directly. They that regardless of theoretical debates, these monkeys, ,,
also throw things held with the trunk, although this is apparently not a Great Apes, must think about the objectives they ari
*.ti ,, ,rr. l

achieving by the
cofiunon occurrence. use of tools.
The clearest case of tool use by mammals other than primates and It is imporranr to emphasize that although some individual
elephants is the use of stones by sea otters, as described by Kenyon and apes become.very proficient makerc *i users of
tools, others rr.u.,
(L969), Calkins (1978), Houk and Geibel (L974), Riedman and Estes do anything_of the kind, even under virnrally the same
(1990) and Riedman (1990). Stones are carried to clams, abalones, or conditions. Furthermore, the details of tooi making and
,rirrg *.y
other molluscs at the bottom and used to hammer them loose from thc widely among individuals, and across populations oith.
For example, the well-known manrfacturi and use of
substrate. Stones are also carried to the surface and used as anvils rcsting sticks to ..fis'h,, for
on the otter's chest as it floats on its back and hammers shellfish ()r scA tcrmites varies in^detail among populations of chimpanz..,
in ain-.._
urchins against the hard surface. Ricclman h:rs obscrvcd nruch indivitl- crrt rc:gions of Africa, as revieweq_br Sugiyama *d Ko-
an 1tsis1,
ual variability in thc ways in which scu ()ttcrs us('st()n('s ()r otltcr <llrjccts Mc(ircw, Tlrti,. r,tl li:rltrwirr (lg7g),,,ia coodall (I9g6t. brf,i""
strch as shclls as rrnvils rrg:rinst n,ltit'lt to lr.tttrrttcr rct.tltitr'.rrrt slrclllish. :l[)q.5 f1'1t'. bcclr fu':rirrt'tl t<) usc :r witL. v:rricty
of huma, devices from
f 08 Chapter Five
Toob and Special l)eyices 109

probably reduces predation on eggs and young by mongo()scs, which

socket wrenches to bicycles. An.orangutan has even been taught to
apparently do not venture into even shallow water, as some nests wcre
make stone tools (Wright 1972), although of course this is not some-
on islands separated from the shore by only about a meter with the in-
thing that they do under natural conditions.
tervening water depth only about I0 cm. Both male and female Egyp-
,( descriula in chapter I, Boesch and Boesch-Ackermann (1984, tian plovers make several scrapes before eggs are laid in one of them. As
l99f ) have observed that chimpanzees use different kinds of stones for
Howell (L979,24-37) describes this behavior "A pair may make doz-
cracking different sorts of nuts, and remember where both stones and
ens of scrapes before finally setding on a nest site, and a small islet may
,ot, ,rJto be found, so that when a Particularly tough species of nut is resemble a miniature battlefield pocked with bomb craters."
gathered they know where to find an aPProPriate type and size of stone
As soon as an egg is laid it is covered with sand by use of the bird's
i"i,f, which io op.r, it. They use stones in a variety of well-coordinated
bill. Both parents take turns sitting on the nest during most of the day-
ways to open different rypes of nuts. Indeed their manual dexterity in
light hours; while incubating eggs they sometimes remove the sand and
this activiiy has led to likening them to early hominids.
bring the egg in contact with the incubation patch (an area on the ven-
Like alt the instances of versatile behavior discussed in this book, one
tral surface where the feathers are much thinner than elsewhere so that
can postulate that whatever tool making and tool use may be displayed
the egg can come in contact with the skin). Incubation is almost contin-
Uy a"imds, it need not necessarily be accompanied by, much less be
uous during the night, and the eggs are about rwo thirds covered with
influenced by, any conscious mental activity. But, as pointed^out in
sand. During the six hottest hours of the day, when the temperature in
chapter I, this is avery difficult question to answer with any confidence)
the shade rises to 45 degrees Centigrade and over 50 degrees in the sun,
*d th"r.fore negatiye assertions are just as questionable as positive each adult frequendy soaks its ventral feathers in the river and returns
ones. One can invert the customary reason for doubting the Presence or
to settle on the buried egBS, thus surrounding them by wet sand which
influence of conscious thinking when animals behave in a versatile and
keeps the eggs distinctly cooler than they would otherwise be .
ingenious fashion by asking how one can Prove that they are not con-
The action of wetting feathers is distinctly different from wading in
scious of what they do.
the river in search of food, which involves wetting only the feet and
lower legs. Quoting Howell again, "to soak, an adult Egyptian plover
Burying and Cooling Young wades into quiet, shallow water at the river's edge until its ventral body
surface is immersed. The bird then rapidly rocks up and down, alter-
Egyptian plovers (Plurianws aegypticas) resembl: .h. migratory plovers
nately lowering and raising its fore- and hindparts in an antero-
oiiriorrh America, but nest on sandbars on the shores of African rivers.
posterior plane. . . . On reaching its nest, the bird fully extends the wet
Herodotus, who called this bird the Tiochilos, and others more recently,
ventral feathers and settles on the substrate, often with widely spread
have stated that it picks leech-like parasites from the teeth of crocodiles.
of climatic and legs. . . . As the ambient temperatLrre rises and nest-soaking behavior
It is no longer found in Egypr because ecological
corrunences, the parents quickly shorten the intervals between change-
changes sincJ ancient times. 7n- 1977 Thomas Howell (1979) srudied
overs (from one to several hours when it is cooler) and may relieve each
Egyitian plovers that were nesting along the Baro fuver in southwest
other every few minutes."
EIft"pia. Wnit. he and other recent observers have not seen them pick-
The chicks are precocial and do not rerurn to the nest after their first
ing the teeth of crocodiles, the behavior Pafferns th.y use to.conceal
day. The parent birds bring food to them and expose food for them by
ttrEir eggs and young and to protect them from overheating are in many
rurning stones. Howell describes the response to approaching preda-
ways more striking and significant.
'Egyptian tors: "The chicks crouch down and are completely covered with sand
plovers nest only on sandbars exPosed during the dry sea-
by a parent in the sarne manner that eggs are covered. Buried chicks are
,on."Vvh.n nesting they are very aggressive towards predators.ol tggt
llso wctted with soaked ventral feathers. . . . Even juveniles up to three
or young and towards other Egyptian plovers as well as other birds that
u,ccks <>f agc may bc covcred with sand by a parent.' If an approaching
."ith. ri-" rypes of food. Theirnest is a simple depression in thc satrcl' kitc <lr pictl crow is s1'rottcrl rrt a consiclerable distance, the parents man-
known as a scrape. Only island sandbars are selected for ncstirtg,.l'his :tlttl
:rgc t() c()\,('r tlrt' t lrit'k so tlrorouglrlv that Howcll f<lund it nearly impos-
very similar sanciy areas conncctcd to the maitrLurtl :tt'c :tv<litlctl.
tI0 Chapter Flve Tools and. Special Deyices l l l
sible to locate it. When human or other predators approach a nest on counts of heron behavior is that they obtain their food by standing still
very hot days the parents continue the soaking behavior even though and watching intently until they see a fish or other prey and then strike
they act nervously when doing so. This of course risks disclosing the at it so fast that the human eye cannot follow details of the motion. Bur
nest location, but apparently the danger of overheating is so great that the prey is seldom so obliging as to make itself readily available, and
this behavior is worth the risk. herons often spend long periods waiting or searching before they strike,
Other species ofwaders related to the plovers are known to soak belly and sometimes succeed in seizing an edible morsel. In an apparent effcrt
feathers and wet their eggs or young when the temperature is very high to improve their chances of success, some herons display a degree of
(Maclean 1975). But this habit reaches an extreme form in the sand- versatility in their feeding techniques that suggests that they are think-
grouse that nest in the Kalahari desert of southern Africa (Cade and ing about what they are doing.
Maclean 1967; Maclean 1968). These birds nest far from the few riv- Several specialized fishing techniques of North American herons
ers where water is available, and they concentrate there in large flocks have been described by Meyerriecks (1960), and recent observations by
even when raising young at nests that are far away-in extreme cases as Higuchi and others demonstrate that one species occasionally uses bait
far as 80 kilometers. The males, but not the females, have specialized to attract fishes. Because they have been observed to use a variety of
feathers on the ventral surface that can hold up to 25 to 40 ml of water. feeding techniques, I will consider here primarily the green-backed
Even after flying for miles these feathers still retain I0 to f 8 rnl. When heron (now known as Ardeoln striata although other scientific narnes
it is very hot, the chicks go to males, which squat over them and wet have been applied to it in the past) and the reddish egret, Dichrornanassa
them with the water-carrying feathers. rufescens. But most of these special techniques are also used by other
Egyptian plovers wet their eggs or young only when the temPerature species on some occasions. The simplest procedure adopted by hungry
rises above roughly 40 degrees. They need only go a short distance to herons is to stand and wait with the neck retracted and to stab at small
the river to gather water for this purPose; but the male sandgrouse must fishes or other prey when they appear within striking distance. While
add to its own drinking behavior the special action of wetting its ventral herons typically feed in shallow warer, they also sometimes hunt for in-
feathers and then flying many miles to where its chicks are located. The sects on land or snatch flying insects from the air. Often no prey is
end result of the specialized behavior is far removed in space and time sighted during long periods of standing and waiting, and the heron be-
from the situation in which the belly feathers are weffed. Although we gins to walk slowly, usually wading in shallow warer. As Meyerriecks
cannot accept this displacement as conclusive evidence that these birds (1960, 8) describes this behavior of green-backed herons: "As the bird
think about keeping their eggs and young cool when they wet their stalks closer to its prey, its steps become slower and longer; each foot is
feathers, the whole pattern is at least suggestive. brought forward, placed, and then lifted so slowly that the movements
are barely perceptible. . . . The bird may rerracr its head and neck or
hold them extended over the water or ground; or rarely the head and
Fishing Techniques of Flerons neck are held momentarily in an extended'peering over' attitude ."
Flerons are specialized for catching fish and other prey by a very rapid F{erons sometimes add "wing flicking" to their slow and carefirl
stabbing motion of their long thin bills. This action consists of an exten- walking in search of prey. As Meyerriecks describes this in the great blue
sion of their elongated necks, which have been curved back into a com- heron, Ard.ea herodiws, the bird "suddenly extends and withdraws its
pact resting position beforehand. Prey are ordinarily seized in the wings about a foot in a short, rapid flick. Such wing-flicks may be re-
slightly opened bill, although the motion is so fast that the heron seems peated as many as five or more times, but usually two or three flicks in
to be stabbing, and on rare occasions it may actually impale a fish. Her- rapid succession are made, md then the bird resumes wading. I have
ons have excellent vision and aim quite accurately at fish, crayfish, or sccn wing-flicking only on bright days, in open, shallow water, when
other prey even when they are underwater. They usually forage in quitc cach wing-flick created an obvious sudden shadow on the surface of the
shallow water, so that refraction of light at the surfacc is probably not rt wrrtcr. Thc fiurction of wing-flicking is ro srarrle prey" (Meyerriecks
serious problem. The impression one gathcrs fr<lrrt rt':ttling gcltcrll rtc- 1960, tt9).'l'hc rctltlish cgrct s1'rcnds lcss of its feeding time standing
Tools and Special Deyices I13
ll2 ChaPter Five
scrapes the mud or aquatic vegetation with one foot. This behavior is repeated
and waiting or walking slowlY, and wing-flicking is quite corunon' while the bird continues in flight. The strike is made from the hovering posi-
Again quoti.rg MeYerriecks (1960, I08t its most colrunon

is a lurching, weaving type of half-run, half-jump Progression' As the bird reels Foot-stirring is also used by snowy egrets, Leucopboyx thula and other
forward,, it stabs ."ffii" the right and left, to seize any prey dis- herons (Meyerriecks 1959; Rand 1956). Another variation on this
primarily in very shall'ow water' ' ' ' theme is vibrating the bill while it is in contact with the water. Kushlan
;a.4 by its ,.ti.,it'i.s.ihis metliod is used of rafescens'The
itdwi.g Feeding is another characteristic^feeding technique (L973) has found that this also attracts small fish which the heron then
slowly, wings.partly-extended' Then at the sight
feeding bird beginriy.rrrrring captures.
of the prey it.*,,riiaf/*f,.*r.nir,t.i"i"gs fully As the prey dash about, All of these specialized types of feeding behavior suggest that the
the egret turns *i d;irir, wing.s still extended
fuly, and the bizarre perform-
heron is actively trying to detect or aftract small fishes or other prey.
rriinrt"r. On occasionthe bird may halt suddenly
ance may conunue for several
Nothing is known about the development of these feeding techniques
and retract the other
in the middle of a run, retract one wing, rapidly extend in the individual birds, or the degree to which they involve learning or
wing, and then resulne its forward run' genetic influences. A behavioristic interpretation would be restricted to l

open feeding noting that the obtaining of food would have reinforced immediately
Reddish egrers frequently changg from the s^o19f YiF
described above . i"f,", ir
."UEa canoPy feeding. f:. Yl"rriecks preceding actions, and an evolutionary view would emphasize the ob-
(ilOO, f08-f09) describes canopy feeding by the reddish egret, the vious adaptive value of obtaining food by these techniques. But the ver- It
bird satility of the behavior also suggests that the heron thinks consciously
about these uses of its wings and feet to affract or startle prey and thus
and peers into the water' and
runs forward with the wings extended, then halts make them visible and catchable.
then brings both *irrg, foivard _or., i,. head,
forming a canoPy over the.head
As discussed in chapter l, the extreme example of specialized, and

and neck. This pose iJheld for a few moments to ,.'e'"1 minutes' I could clearly
the bird made under the canopy of the perhaps purposeful, feeding techniques of herons is occasionally exhib-
.' fish-catching
see the rapid
ited by the green-backed herons, Ard.eola s*iata. While most of these
;id;, -. *v ou..*rti!ns of rufescens at extremely close range (three feet) birds feed in relatively simple ways, they have occasionally been ob-
ind.icate that the r;;";pt;vides a false refuge for the.fish startled into motion
hold their wings in served to use bait to attract small fishes (Lovell 1958; Sisson L974;
;yA. previous arrfri"g lctivities. Reddish .Igt.tt typically
a strike' I could clearly
the canopy attirude for-a minute or two beforithey -f: Norris 1975; and Walsh et al. 1985). Higuchi (1986, 1987, I988a,
see many fish enter the shade of the .*opy
i".s: shallow waterr and when a l9S8b) has studied this behavior intensively, both in |apan and in Flor-
preV had thus "fallen for the^ruse," the egret would stab rapidly ida. The herons pick up some small object, which may or may not be
number of
under its extended wings' edible, carry it to an appropriate sPot on the shore, drop it into the
Me- water and watch it intently. When small fish approach the bait the heron
This is also colrunon behavior Paffern of the African black heron'
extensively, and seizes them with its usual rapid neck extension. A wide variety of small
lnnophoyx *d.oi*, which .-pioy, canoPy
when can- objects are used as bait, including twigs, leaves, berries, feathers, insects,
wir,Ll.r (1982) found that thry att.acted mot. small
earthworms, pieces of bread or crackers dropped by human visitors to
- the park, and even bits of plastic foam. If the bait drifts away, the heron
Meyerriecks (1960,
Another food-gathering procedure observed by may pick it up and drop it again within reach.
109) in the reddish egrets is foot-stirring: Adult birds are more successful than juveniles, which suggests that
vibrate its feet over the
As the egret waded forward rather slowly, it would learning plays a role in the acquisition of bait fishing behavior. Small
would stol'r
the feet; then it
surface of the mud, imparting a scraping motion.to fishes often come to the surface to nibble at such floating objects, and
and peer at the ,r*"..tf &"t.,
,t irrd".ith.. strike at Prey
*"*:1;t].ttttll, thc heron scizes onc with its characteristic stabbing motion. In some
motions- Hovering-stirring is an acritrl vrtrirurt of tvpricll
resuming the scraping situlrti<lrrs tlrc lrcrorr rnlrv wait on a branch somewhat above the water
sl.rvlv, thctt stttltlcrtlv
stirring o, ,..upilg-.'ilr. fcctling bircl rirovcs fiirwrrrtl lcvcl rrltcr t lrrou,irrg tlrt' brrit <ltrt fiom thc shorc ancl thcn fly out to seize
hunchcs irra, nifi',?, l',.ru.r, ,rt'.r''tlr. strrfhcc
,l' thc w'll('t ' 'ttttl 't't'\' 1il''rt't'ltrllv
I14 Chapter Five

fish attracted to the floating object. In Higuchi's initial observations

only a few out of a colony of twenty or thirty green-backed herons nest-
ing near a city park engaged in this type of fishing. He suspected that
thEy had first observea smU fishes attracted to pieces of bread dropped
into the water by children, but he was unable to induce bait fishing by
dropping crumbs near other birds of the sam: species. Further investi-
grti,rr, rriitt U. necessary to learn just how ft* individual herons ac-
(uire this specialized and enterprising behavior.
When nb suitable small objects are available near the shore herons
sometimes gather small bits of vegetation and bring them t9 the water's
edge. They may even break twigs into smaller lengths for this PurPose.
It i"s important'to recognize that only a very tT"ll fraction of the green-
.l-he previous. chapters have revi:*.g suggestive evidence that on
some occasrons animals may be consciously aware of objects and events,
backed herons have been seen to use bait for fishing, but a bird that has
and that they experience perceptual consciousness, roughly correspond-
acquired the habit does engage in bait fishing repeatedly. As with yit--
ing to what Natsoulas calls Consciousness 3. But do they grasp any soft
Afy * cases of enterprising behavior by animals, a behavioristic inter- of generalizations, or is each perception experienced in total isolation
pretation is quite poriibl.. But it does seem more parsimonious to infer from all othersf For example, do animals ever think in terms of cate-
that the birdlnin[s about its behavior and the probable results.
gories such as food, predators, or members of their own groupl This is
a difficult question to answer, like most of those discussed in this book,
but it is an important one. The ability to classify and think about cate-
gories as well as specific individual items is a powerful facet of conscious
thinking, and if it lies within the capabilities of various animals, this
ability is an impoftant attribute that must be appreciated to understand
the animals adequately. Some evidence points in the direction of a ca-
pacity to think in terms of simple concepts) and this chapter reviews a
few especially clear examples.
The natural world often presents animals with complex challenges
best met by behavior that can be rapidly adapted to changing circum-
stances. Environmental conditions vary so much that for an animal's
brain to have prograrnmed specifications for optimal behavior in all sit-
uations would require an impossibly lengthy instruction book. Whether
such instructions stem fiom the animal's DNA or from learning and
environmentd influences within its own lifetime, providing for all likely
contingencies would require a wasteful volume of specific directions.
Concepts and generalizations, on the other hand, are compact and effi-
cient. An instructive analogy is provided by the fact that the official rules
for a familiar game such as baseball run to a few hundred pages, al-
though once the general principles of the game are understood, quite
sirlplc thinking sullices to tell even a small child what each player
sh<>ukl d<l in :rlrrro,st :rll grrnrc situations.
It is ol'c()urs('olrviorrs th:rt wc c.ln chssify stimuli into groups to
I ls
Concepts lL7
I 16 Chapter Six
psychologists largely abandoned the effcrt to understand human con-
which an animal gives the same or a very similar resPonse. But such sciousness, replacing introspection with objective experiments. While
evidence does not"suffice to indicate that the animal thinks in terms of
experiments have been very helpful in analyzing learning and other hu-
caregory that includes all these stimuli. For example, hungry an^imals
man abilities, the rejection of any concern with consciousness and sub-
.ppio..f, and eat a wide variety of foods and flee from a variety of d-an- jective feelings has gone so far that many psychologists virnrally deny
gl;, but they might think about each one quite independently of all their existence or at least their accessibility to scientific analysis.
5ah"rt and nevet thirrk about the categories of edible or dangerous In one rather extreme form of this denial, Harnad (1982) has argued
things. In social grouPs, individual animals often recognize other mem- that only after the functioning of our brains has determined what we
bers"of their g.6rP,^ or at least react differently to kin and nonkin will do does an illusion of conscious awareness arise, along with the
(Fletcher rrra tli.f,iner 1987; Hepper 1?99) For instance, honeybees mistaken belief that we have made a choice or had control over our
.r. -or. tikely to deliver food to their full sisters than to the half sisters behavior. The psychologists who thus belittle and ignore human con-
that result from the queen having mated with more than one drone sciousness can scarcely be expected to tell us much about subjective
(oldroyd, Rinderer, and Buco I99t). In an especially telling.1rt., thoughts and feelings of animals, still less the degree to which thev
iro*., (Lg79) observed that in a captive colony of the neotroPic.al fruit think in terms of concepts. If we cannot gather any verifiable data about
calls from
bat Caiollin perspicillata, whenthe harem male heard distress
our own thoughts and feelings, the argument has run, how can we hope
a baby thrt t.d failen to the floor, he would frequendy yaw.l 1o the
her to retrieve her infant' to learn anything about those of other species|
-oth., of that particular baby and stimulate A long overdue corrective reaction to this extreme antimentalism is
But do any animals think in t..-. of such categories as "one of us"?
well under way. To a wide range of scholars, and indeed to virnrally the
Differential reaction to group members or close relatives as compared
whole world outside of narrow scientific circles, it has always been self-
with others of the t*. tp..i.t ^*y might be based
on familiarity versus
evident that human thoughts and feelings are real and important (see,
sffangeness and not entail .o.rrJious thinking about the categories
of the best evidence that animals can for example, MacKenzie L977; and Whiteley L973). This is not to
of gr6rp member or kin. Some underestimate the difficulties that arise when one attempts to gather ob-
think in terms of categories or concePts has become available from what
*tly- jective evidence about other people's feelings and thoughts, even those
at first thought -ry r..- an unlikely rort.., the detail*
1*:ly that have been re- one knows best. But it really is absurd to deny the existence and impor-
ses of animi learning by experimental psychologists
r (1975), Dickinson tance of mental experiences just because they are difficult to study, and
viewed by Mackinro;h itOi+1, Hilgard a1d Boye
because it is very difficult to distinguish conscious from unconscious
(1980), *d goll"s and Beecher (1988).T" explain how these experi- cognition in animals.
ments came to be developed, it will be necessary to digress into a rather Why have so many psychologists appeared to ignore a central area of
i."$hy consideration of what life is like for the experimental animals their subject matter when most other branches of science refrain from
used to study learning.
such self-inflicted paralysisl The usual contemporary answer is that the
cognitive revolution discussed in chapter I has led to a newly dominant
Behavioristic Inhibitions school of cognitive psychology, based in large part on the analysis of
of human and animal behavior in terms of information processing (re-
The investigation of the possibility that animals might,hi"k in terms viewed by Baars (1986, 1988), Blakemore and Greenfield (1987), and
conceprs or even categ6ries of important o.bjects has been seriously
|ohnson-Laird (1988) among others). Analogies to computer pro-
impeded because .o-["trtive psychologists have seemed to be
by Bttrg- grarns play a large part in this approach, and many cognitive psycholo-
peirified by the notion of animal consciousness, as reviewed gists draw their inspiration from the success of computer systems, feel-
'hrrdt (1985b). Historicatly, the science of psychology has beln rcactirlg
ing that certain types of programs can serve as instructive models of
for fifty years or more ,gri.r.t earlier affempts to understand thc work- hrnnln thirrking. Tcrnrs that used to be reserved for conscious human
i.g, oi th. hrr-"n minl by intro^spectivc sclf-cxami.ati.tt-tryi,g t<r
bcirrg.s rrrc n()w r'orrrrrrorrly trscd to clcscribe the impressive accomplish-
learn how we thirrk by tlririking al'rout our thouglrts. Tltis cflirrt
lctl t<r
cxPcrittlctlt.tl n'rcnts ol'trx'nprrlt'r's. l)cspitc thc optirnisrn <lf conrputcr cnthusiasts,
c<xrflicting lnd corrtratlictorv i'csrrlts; so, itr litrstr:ttiott,
IL8 Chapter Six Ooncepts I 19

however, it is highly unlikely that any comPuter system can sPonta- guished career did he confess to having been a "cryprophcnomenolo-
neously generate subjective mental experiences (Boden 1977; Dreyfus gist" (Tolrnan 1959).
1979; Baker 1981; Searle 1990; Churchland and Churchland 1990). Tolman's ideas were not widely accepred by behavioristic psycholo-
Conspicuously absent from most of contemPorary cognitive psy- gists, although in recenr years he is often acknowledged as having anric-
chology is any serious attention to conscious thoughts and subjective ipated the developmenr of cognitive psychology in the l95bs and
feelings. For example, Wasserman (1983) defended cognitive psychol- 1960s, as reviewed by Burghardt (1985). A few other psychologists
ogy to his fellow behaviorists by arguing that it is not subjective or men- such as Mowrer (1960a, 1960b), Bolles (1972, 197\: and Wilker
talistic; but, as described below, some of his own exPeriments have (1983) have rather cautiously ventured to suggest that processes more
come to indicate that animals can think in simple concePtual terms. or less equivalent to conscious thinking must occur in cirtain animals.
Analyzing people as though they were computers may be useful as an But they have almost always avoided explicit consideration of animal
consciousness. Yet the learned behavior patterns srudied by comparative
initial, timited approach, just as physiologists began their analysis of
hearts by drawing analogies to mechanical pumps. But it is important psychologists can be appropriately viewed as versatile behaiior by
to recognize the limitations inherent in this approach; it suffers from which the animal adapts ro a novel and challenging siruation, and does
the danger of leading us into what Savory (1959, 54) called by the apt what it has learned will get it food or enable it to avoid something un-
pleasant. Rather than tediously pointing out that the experimentJ ani-
but unfornrnately tongue-twisting nalne of "the synechdochaic fallacy."
This means the confusion of the part of something with the whole, or, mal may have understood perfecdy well that it had to do certain things
as Savory put it, "the error of nothing but." Information Processing is to get food or avoid electric shocks, I will concentrate on some recent
experiments that are even more strongly suggestive of simple conscious
doubtless a necessary condition for mental experience, but is it suffi-
cientf Human minds do more than process information; they think and thinking. These are usually referred to in terms of concepti that the an-
imals appear to have acquired.
feel. We also experience beliefs, desires, fears, expectations, and many
other subjective mental states.
Psychologists have analyzed learning in animals by means of a host Experimental Analysis of Animal Cognition
of ingenious experiments, and whole books such as those by Dickinson
(1980), Mackintosh (L974), ard Roitblat (1987) are required to re- The criticism that behavioristic psychologists have neglected animal
view them adequately. But these discussions of what animals learn and thoughts has begun to elicit a promising new response. Several psychol-
ogists concerned with animal learning and problem solving und"r corr-
remember are couched almost entirely in behavioristic terms. The psy-
chologists who have conducted and reviewed these sorts of experiments trolled laboratory conditions now claim that they and thelr colleagues
have been investigating animal minds all along, even when behavioiism
concentrate almost exclusively on what animals do, and avoided like a
was dominant (Masonl976; Roitblat, Bever, andrerrace 1983; Walker
plague any consideration of what they might think or feel as they carry
out the sometimes complex patterns of behavior they have learned will 1983). But in the salne breath they are likely to assure us that all animal
get them food or allow them to avoid unpleasant experiences. One thinking, and even mosr human thinking, is quite unconscious. Mind is
redefined as information processing; an analysis of how information is
notable exception was Tolman (1932) who emphasized that animals
acquired, stored, and retrieved, and how it affects behavior, is felt to be
often appear to expect certain outcomes when they perfiorm various
all that is required to understand animal minds. But beyond this defen-
learned behavior patterns, such as running mazes. Tolman called his
sive reaction to the charge that a central aspect of psychology has been
viewpoint purposive behaviorism, and he clearly believed that rats and
other animals intentionally try to obtain desired things such as food and ncglected, there is a positive and hopeful aspect to these discussions.
to avoid unpleasant experiences like receiving electric shocks. But thc This is the increasing recognition that when animals learn to perform
rrcw tasks, thcy presumably think, consciously or unconsciously, about
positivisttc Zeitgeist of his times was so influential that he refrainctl
from explicit suggestions that animals might consciously thirrk at-xrttt thc problcrns thcy facc arttl thc solutions they attempt or achieve. As
what they were doing. Orrly towarcl thc crrrl of l'ris long :urt'l tlistirr- cxpcrilttctrt:tl ps1,r'llologists bccorrrc incrcasingly concerned with mental
l2O CbaPter Srx Concepts l2l
experiences in animals, their ingenious experimental methods can be less it does what it has learned will prevent this unpleasant experience.
adapted to the study of animal consciousness, once the taboo against its But psychologists carefully avoid describing conditioned avoidance as
consideration is laid aside. evidence that the animal expects a painful shock following the warning
This process has been under way for some time, but it has remained signal and anticipates that it will be hurt unless it takes the avoidance
hidden behind a smokescreen of behavioristic terminology. Many ofthe action it has learned to be effective.
experimenrers really do seem quite interested in the possibility of think- M*y students of animal learning have noted that animals often act
irg, .r.n of conscious thinking, in the animals they study. But they have as though they are expecting something, and if it does not become avail-

bin inhibited from saying so directly, even to themselves; and the re- able they appear surprised or disappointed. Tolman (L932, L937) em-
sult has been what I call semantic behaviorism (Griffin 1981)' As the phasized this sort of behavior in rats that were required to learn complex
behavioristic taboos are relaxed or ignored, the ingenuity that has en- mazes in order to obtain food. In a typical experiment, after the rat had
abled psychologists to discover so much about learning and informa- learned a moderately complex maze and was performing almost per-
tion piocessing-can be redirected toward animals' subjective thoughts fbctly, choosing correcdy a long series of right or left rurns, the experi-
and feelings. This is a very hopefut prospect, and the chief barriers to its menter withheld the reward. On reaching the goal box and finding no
realizatiot li. itt the current mindset of many experimenters. reward, the rats would appear confused and search about for the food
There is a significant, though still largely unrecognrzed., intellectual they had reason to expect.
underworld of ethologists and psychologists who often susPeff that One of the most dramatic examples is still one described by Tinkle-
their subjects could scircely do *hat they do without some conscious paugh ( 1928, 224, also quoted in Tolman 1932, 75) . He trained mon-
thinking and subjecrive feeiing about their situation and their efforts to keys to watch the experimenter place a favorite item of food, such as a
solve pioblems. Hundreds of talented scientists are actively studying piece of banana, under one of two inverted cups that remained out of
how animals solve problems, the extent to which they deal in generaliza- reach until a barrier was removed. The purpose of the experiment was
tions and conc.ptt, and whether they employ simple plans. or exPecta- to measure how long the monkey could remember which cup hid the
tions. We can tike full advantage of the rich body of data about animal piece of banana. When a monkey had learned to select the correct cup
problem solving under both nanrral and laboratory conditions, without almost every time, provided it did not have to remember the situation
teing unduly ioubled by the scientists' stated reasons for conducting for too long, the banana was replaced by lemrce during the short wait-
their"investigations. Even though semantic behaviorism still frowns on ing period when the monkey could not see the cups or the experimenter.
terms with mentalistic connotrtiot t, the results and interpretations of As Tinklepaugh described the results, the moderately hungrv monkey
experiments are continually providing 1ew. and stronger evide11l that now "rushes to the proper container and picks it up. She extends her
*^i^"lt sometimes think consciously (Honig and ThomPson 1982)' In hand to seize the food. But her hand drops to the floor without touch-
short, while most of the scientists who study animal cognition deny any ing it. She looks at the letnrce but (unless very hungry) does not touch
concern with animal consciousness, the fervor of these denials seems to it. She looks around the cup . . . stands up and looks under and around
be slowly waning. her. She picks up the cup and examines it thoroughly inside and out.
Rats and othEr laboratory animals easily learn that a certain light or She has on occasion turned toward the observers present in the room
sound will be followed by * electric shock. They may cringe or show and shrieked at them in apparent anger."
other signs of expecting the unpleasant shock- before it is delivered. Numerous other experiments have confirmed Tolman's thesis that
They .ri leain how to p.event the shock by taking some specific animals expect a particular outcome at certain times. For example, Ca-
action, such moving to a different Part of the cage or pressing a lever.
as paldi, Nawrocki, and Verry (1983) have demonstrated that rats antici-
After iearning this solcalled conditioned avoidance, the animal contin- patr: thc patterns of reinforcement they have experienced in ways that
-periods supp()rt what thcv tcrm "a cognitive view of anticipation." As summa-
ues for long to react to the warning signal by taking the same
avoidance i.iiot, even though it no longer receives any shocks (rc- rizcrl ['r1, 1y.1O.r (l9tt3): "S<)r'nc kincl of mental activity is being attrib-
viewed by Mackintosh 1974)-.It scems rcasonable to concludc that thc utc('l t() tlrc.urirrr:rls: tlr.rt is, tlrcrc is cr>rr.sirlcrccl to be some internal sift-
animal kriorvs it will ['rc htrrt a fl'w scc<xrtls :rftc:r thc wrtntilrg siglrrrl trtt- irrg ruttl sclt'ttiorr ol irrlirnrr:tliott rrttltcr tltrut simplv thc release of
122 Chapter Sm Concepts 123
responses by a certain set of environmental conditions. Knowledge of gest conscious thinking. In a typical experiment of this type a rat is
goals, knowledge of space, ffid knowledge of actions that may lead to trained to recognize that a triangle marks the location of food but that
goals seem to be independent, but can be fitted together by animals an equally conspicuous circle does not. After the rat has been respond-
when the need arises" (p. 8l). Naturalists and ethologists have gathered ing appropriately to these rwo stimuli quite accurately for some dme,
abundant evidence that such needs do arise very corrrmonly in the nat- the experimenter suddenly changes the rules of the garne, so that the
ural lives of animals, and the resulting behavior strongly suggests that circle now shows where food is available and the triangle yields nothing.
they understand in an elementary fashion what the problems are and In time the rat learns the reversed rules and again perfiorms almost per-
how their behavior is likely to solve them. Animals appear to think in fectly; it has changed its searching image from triangle to circle. But an
"if, then" terms. "If I dig here, I will find food," or "If I dive into my interesting difference results from overtraining some rats on the first
burrow, that creature won't hurt me." Likewise in the laboratory, "If I problem by letting them make the correct choice dozens or hundreds of
peck at that bright spot, I can get grain," or "If I press the lever, the times, while giving others just enough training that they have barely
floor won't hurt my feet." become proficient. One might expect that the overtrained rats would
A relatively simple case of expectation is demonstrated by the ability have the "triangle marks food" rule so thoroughly drilled into their
of numerous animals, including many invertebrates, to learn that food brains that it would be more difficult to learn the reversed problem. But
is available in a certain place at a certain time of day. They typically re- careful experiments have shown that under some conditions overtrained
turn to this place at or shortly before the appropriate hour on subse- rats learn more easily than others to reverse their choice (Mackintosh
quent days and may continue, though with decreasing regularity, even 1974). Perhaps during the numerous reversals and relearning of rules in
after many days when no food has been found there. It seems reasonable dozens of trials after the problem is initially solved, they begin to think
to infer that these animals really do expect food at a certain time and consciously about the two patterns or even about the possibility of rule
place and that they experience disappointrment, annoyance, or other reversal and thus find it easier to grasp the new relationship. No one can
subjective emotions when their expectations are not fulfilled. say for sure, but communication with rats via such reversal learning ex-
There is also increasing evidence that many animals react not to periments might be telling us somerhing important.
stereotyped patterns of stimulation but to objeos that they recognize Mackintosh (L974) *d Walker (1983) have reviewed several other
despite wide variation in the detailed sensations transmitted to the cen- types of experiments showing that laboratory animals can learn rela-
tral nervous system. As reviewed in chapter 3, a Thompson's gazeLle tively abstract rules, such as oddity or the difference between a regular
recognizes a lion when it sees one. The lion's image may subtend a large and an irregular pattern. In oddity experiments the animal is presented
or small visual angle on the retina, and it may fall anywhere within a with a number of stimuli or objects, one of which differs from the oth-
wide visual field; the gazelle may see only a part of the lion from any ers in some way; it must learn to distinguish this "oddball" from the
angle of view. Yet to an alert tommy, a lion is a lion whether seen side or other members of the set. For many animals, learning a single case of
head on, whether distant or close, standing still or walking. Further- this sort is not difficult. Chimpanzees, however, have learned to gener-
more, its perceptions of lions are obviously separated into at least two alize oddity as such, ffid having learned to selecr a red disk placed with
categories: dangerous lions ready to attack, and others judged to be less rwo blue disks, and a blue disk accompanied by rwo reds, they also se-
dangerous on the basis of subtle cues not obvious to a human observer lected the oddball when it was a triangle with rwo squares. pigeons have
without considerable experience. Comparable behavior is so corrunon much greater difficulty with comparable problems, but, surprisingly,
and widespread among animals living under natural conditions that it they do better than cats and raccoons.
seems not to call for any special scientific analysis. Yet the ability to ab- Variations on this experimental theme have led to other unexpected
stract salient features from a complex pattern of stimulation, often in- rcs'rlts. For instance, Zentall and colleagues (1980) compared the per-
volving more than one sense, requires a refined ability to sort and eval- forrnancc of pigcons faced with rwo types of oddity problem. In bne
uate sensory information so that only particular combinations lcaci t<l c:rsc thc bir,ls srlw l fivc-by-fivc array of rwenty-five disks, one of which
the appropriate responsc. tlifli'rctl ilt cokr lirrnt tltc rcrtrrrirrirrg twcrrtv-four. In the other problem
Laboratory cx1'rcrinlcnts on wltlrt is clllctl rcvcrsll lcarnirrg :tls<l srrg- tltcrt'\\'('t'('tltt't't',,lrlt'tlisks itt:t r<)\\/. tw():rlikc:rp( tftc tfuird a diftbrent
124 Chapter Six Concepts 125
color. In that case, if the positions of the odd-colored disk was varied to manipulate. For rats this is a lever close to the floor which they can
randomly, or if the actual colors were changed, for instance from one depress with one forepaw, and for pigeons it is a key, or small back-
green and two reds to two greens and one red, the pigeons failed to lighted piece of translucent material flush with the wall at a height easily
solve the problem. But with the array of twenty-five they quickly reached by the bird's beak. A third fixture of the Skinner box is a me-
learned to peck at the disk that differed from the rest in color, even when chanically operated food hopper which provides access to food, or
the colors were shifted randomly from wenty-four reds plus one green sometimes water, but ordinarily only for a few seconds at a time. Both
to twenty-four greens and one red. levers and backlighted keys are attached to microswitches connected so
In a related type of experiment, Delius and Habers (1978) trained as to control the food hopper or produce changes in the stimuli pre-
pigeons to distinguish pairs of visual patterns according to their relative sented to the animal. General illumination in the box is also provided;
syrnmetry or asyrrunetrv. Ffaving learned this task, they were also able and since pigeons rely heavily on vision, turning off this "house light"
to make the correct distinction on the first try when given new pairs of tends to inhibit most activities including key pecking.
shapes, some of which were symmetrical and others not. Bowman and Studies of learning in Skinner boxes have ord.inarily been conducted
Sutherland (1970) trained goldfish to distinguish benveen a perfect and analyzed in strictly behavioristic terms; but some of the results pro-
square and one with a bump in the top edge . In one of many variations, vide significant though limited evidence about what the rats or pigeons l

goldfish that were trained to swim toward a square having a small tri- may be thinking as they work for food or water. The most revealing
angular extension from its top, rather than a perfect square, also selected evidence of this type has been obtained with pigeons, which rely much
a circle with a small semicircular indentation in the upper edge in pref- more than rats on vision. This facilitates complex types of experimental
erence to a plain circle. They seemed to have learned to distinguish stimulation, th.at we, as equally visual animals, can more easily apPre-
simple shapes from the same shape complicated by either an indentation ciate. Psychologists who study this sort of learning emphasize what they
or outward bulge. Walker (1983) expressed surprise that "even a verte- call contingencies of reinforcement) that is, the rules relating what the
brate as small and psychologically insignificant as a goldfish appears to apparatus does in response to the animal's bar pressing or key pecking.
subject visual information to such varied levels of analysis." Why should A very simple rule would be for the food hopper to make food acces-
this be surprising, when it is well known that fish can discriminate many sible for a few seconds whenever a pigeon pecks the key. Or the bird
types of pattern that signal food or dangerl We should be on guard rnay be obliged to deliver two, ten, or some other number of pecks to
against the feeling that only primates, or only mammals and birds, have obtain food. An early discovery in this type of investigation was that
the capacity for learning moderately complex discriminations. For the animals work harder if the food hopper operates only occasionally after
narural life of almost any active animal requires it to discriminate among a variable and unpredictable number of pecks or bar presses. This vari-
a wide variety of objects and to decide that some are edible, others dan- able ratio reinforcement elicits a very high and sustained rate of re-
gerous, and so forth. sponding. In this situation the hungry pigeon might think something
like: "Pecking that bright spot sometimes gets me food, but not always.
It's easy-almost like picking up sssd5-5s I'll keep trying until every
Lifc in the Skinner Box
now and then that box clanks and I can get some food."
M*y laboratory snrdies of learning and discrimination between stimuli In these experiments, pigeons are ordinarily deprived of food or
employ the Skinner box, in which a very hungry animal, typically a rat water long enough to make them very hungry or thirsty; a standard
or pigeon, is isolated from almost all stimuli except those under study. proccdure is to hold the bird's weight at 80 percent or even 70 percent
To obtain food the animal must manipulate something in the box when of what it would be with food available at all times. When first put into
a particular stimulus is presented to it. Opaque walls prevent it from :r Skinncr box most hungry or thirsty pigeons peck the key before too
seeing anything outside the box; and a broadband hissing noise is ofterr It>ngi rrftcr all thcrc i.s nothing else to do, and pecking is a narural action
provided to mask any outside sounds. Thus the animal has almost noth- lor hungr-1, 1'rilgcon.s which prick trp scccls or other small objects as a rou-
ing to do but operate deviccs within thc box that rvcrc origirr:rlly sc- rirrc prrrt ol'tlrt'ir tl:rilt, livcs.'l'lrc ncw. lcarncc-l bcl'ravior is to peck at the
lected becausc they wcrc things thrlt nrctltbcrs <>f its s1'rcri1'* t'.tsi11, lc:rrrt lrr iglrt slx)l orr llrc n'.rll instr';rtl ol'.rn :rcrrr:tl trit of grairr. Since this causcs
L26 Chapter Six Concepts 127
the food hopper to open and gives the bird a chance to pick up edible light is on, but never with the green panel illuminated. A plausible in-
seeds for a few seconds, it is not surprising that most pigeons soon learn ference is that the pigeon might think something like : "When that spot
the basic rules of the game. is red I can sometimes get food by pecking the white spot." But how
After this stage has been attained, the experimenter may change the can we test such an inferencef Perhaps it is quite wrongi the bird may
rules so that the food hopper operates only some of the time, or only be thinking about something entirely different, such as the perch where
when some other information is supplied. One or more additional keys he spent last night, or the hen he was courting when last given an op-
may be provided and their microswitches connected to circuits that op- pornrnity to do so. Or perhaps he does not think about anything at all.
erate the food hopper only when this key is lighted. The pigeons then Straub and Terrace (1981) trained pigeons to peck at colored keys in
learn to peck much more often when this second light is on, though the wall of the Skinner box and to do so while following a parricular
they usually try occasional pecks at the food-gening key at other times sequence of colors. To get its food, one pigeon might have to peck first
as well, perhaps thinking that it might still work. Or the apparatus may red, then blue, yellow, and green, while another was required to peck in
provide food only when a certain color or a specific pattern is displayed, the sequence yellow, red, green, blue. These pigeons were faced with
and endless variations on this theme have been used to measure sensory two rows of three spots that could be illuminated with different colors.
capacities and the ability to discriminate between similar stimuli. In the most significant experiments four of the six spots were illumi-
These procedures were originally developed by psychologists who nated simultaneously, each one a different color, but the positions of the
denied any interest in whatever subjective, conscious thoughts or feel- colors varied from trial to trial; the pigeon had to ignore the position of
ings their experimental animals might experience. They had been con- the spots and select the appropriate colors in the correct sequence in
ditioned by the intellecrual, Tr-itgeist of behaviorism to restrict their order to obtain food. Several pigeons solved this problem and per-
concern to overtly observable behavior and how it could be altered by formed at a level far above chance, indicating that they had learned a
learning. Indeed one of the main advantages of the Skinner box is that sequential rule that guided their decisions about which spor ro peck. It
the animal's behavior can be recorded mechanically and objectively as seems plausible that they thought something like : "I must peck first at
numbers and rates of bar pressing or key pecking. Any other behavior red, wherever it is, then blue, next yellow and then green."
is ordinarily ignored, and the opaque walls of the Skinner box prevent One set of experiments with pigeons in Skinner boxes has provided
the experimenter from seeing what else the animal may be doing. The a significant though incomplete indication ofwhat the birds were think-
psychologists who conduct these experiments almost never speak of the ing about. Jenkins and Moorc (1973) departed from custom by acrually
animals in Skinner boxes as hungry: they are food deprived, or main- watching what their pigeons were doing. They expanded upon earlier
tained at 80 percent of free feeding weight. And they never let them- observations by Squier (1969) that fish "reacted to response keys with
selves be caught saying, in print, that such a pigeon might want the species-specific fceding movements" and the report by Wolin (1968)
food-hopper to open or believe that pecking the key wilt get the food it that "the form of the pigeon's operant key-contact response depends on
must crave. When the animal learns to do what gets it food or water, the nature of the reinforcer." Close observation and photography
such behavior is said to be "reinforcedj' rather than rewarded. This showed that when pecking a food-getting key, pigeons held their bills
choice of terms reflects the behavioristic insistence on ignoring any in a position closely resembling that used in picking up actual seeds. But
mental experiences of the experimental subjects. thirsty pigeons held and moved their bills in ways that were much like
Once we allow ourselves to escape from what the philosopher Daniel clrinking. (Pigeons swallow water with a distinct set of movements that
Dennett (1983) called "the straitjacket of behaviorism," we can ask our- differ from those used to swallow seeds.) To avoid observer bias and
selves what it may be like to be famished or very thirsty in a closed box cxpcctations, ten judges who did not know whether the birds were hun-
where a litde food or water can be obtained by playing the Skinncr box gry or thirsty, or whether they were rewarded with food or water, were
game. Consider a typical experiment where the box contains rwo back- shown t'n()ti()lt 1'ricturcs or video tapes of pigeons pecking keys in a Skin-
lighted panels in addition to the white key that sometimcs, but t'tot rrl- ncr b<lx. ltightf,-scvct'l l)crccnt <>f thcir judgments were correct, and two
waysr activates the food hoppcr. ()nc pancl is rccl whcn turrrctl ott. tltc ol'tlrc itrrlgt's ttt:ttlt' n() ('rr()rs .rt rrll. As sunrmarized by fenkins and
other lyccn, antl thc fi><lcl hoppcr ()pcr:ltcs occ:rsi<lltrtllY rvltclt tltc rctl Moorr', "lltt' lr,tsis lor jrrtlgt'nrt'rtl n)()s[ c<lrtrrnr>rrly ntctrtioncd was that
I28 Chapter Six Concepts 129
eating-like movements were sharp, vigorous pecks at the key. In con- figure might be large or small, dressed in different sorts of clothing or
trast, the drinking like movements, it was said, involved slower, more engaged in a variety of activities, sitting, standing, walking, with or
sustained contacts with the key (or other object) and were often accom- without other people or animals present. In some pictures only part
panied by swallowing movements." of a human figure such as the face was included. The negative pictures
Later investigations have confirmed and extended these results. varied just as widely. When pigeons were pecking significantly more
LaMon artdZ-,eigler (1988) have reported detailed measurements of the often when shown picrures containing people, a series of wholly new
pigeon's behavior when pecking at a key located on the floor of the positive and negative pictures were shown, ones that varied as much as
Skinner box, and when actually taking grain or water. The most obvious the original set but which the birds had never seen before. Surprisingly,
difference between key pecks for food and water was that the beak was some of the pigeons mastered this task and pecked significandy more at
opened much farther for food reinforced keypecks (about 5.5 mm com- the new pictures containing people. It is imporranr ro appreciate that
pared to 0.4 mm). Whether pecking the key or actually eating and the pigeons do not perform perfecdy in these resrs; typically they may
drinking, the hungry pigeons used brief pecks with a relatively high peck at perhaps 70 to 80 percent of the positive pictures and only 20 to
force, while thirsty pigeons employed sustained contact movements of 30 percent of the negatives. But the numbers of pictures used in such
the head and beak. Although the scientific papers describing these ex- experiments are so great that these differences are extremely unlikely to
periments are constrained into orthodox behavioristic terminology, it is occur by chance.
clear that hungry pigeons peck the key as though eating, thirsty birds as Herrnstein termed this concept learning, for the pigeons had learned
though drinking. Since food and water were of the utmost importance not specific pictures or patterns, but categories. In other experiments of
to these birds, it seems quite reasonable to infer that they were thinking the same general type pigeons learned to distinguish: (l) oak leaves
about eating or drinking when operating the Skinner box mechanism from leaves of other trees (Cerella 1979), (2) scenes with or without
to satis$r their hunger or thirst. trees, (3) scenes with or without bodies of warer, (4) pictures showing
In another series of experiments Richard Herrnstein and several a particular person from others with no people or different individuals
other psychologists have presented pigeons with truly challenging (Herrnstein, Loveland, and Cable 1976), and (5) underwarer scenes
problems of memory and perception. In a pioneering experiment by containing fish as contrasted with similar underwater pictures contain-
Herrnstein and Loveland (1964) the standard Skinner box was modi- ing no fish (Herrnstein and de Villiers 1980). This last task was selected
fied so that in addition to the customary food-gening key there was a because pigeons would never in their individual or species experience
small screen flush with the wall on which colored slides could be pro- be obliged to discriminate among underwater scenes.
jected. The screen also served as a key which closed an electrical switch In other experiments by Poole and Lander (197L) pigeons learned
when the pigeon pecked it. A wide variety of photographs were pro- to distinguish pictures of pigeons from other animals and birds. After
jected on this miniature screen, indoor and outdoor scenes, pictures of having been trained with positive photographs of normal pigeons they
people, animals, buildings, trees, flowers, and street scenes. In all these treated as "pigeon" picrures of "weird" pigeons described as "fancy
experiments some slides, designated positive, signaled the availability of varieties having heavily feathered feet, abnormal head, body, or tail
food; pecking them sometimes caused the food hopper to open for a stmctures." This suggests recognition of a variety of pigeons as some-
few seconds. Other pictures, termed negative, were not reinforced; thing equivalent to "one of usj' although it has not been demonstrated
pecking them had no effect, or it might turn offthe "house lights," leav- that pigeons can learn more easily to recognize pictures of pigeons than
ing the pigeon in darkness. othcr animals such as dogs or hawks. It is important to bear in mind
!\rhen the pigeons had learned to peck much more frequently at the that in all cases the crucial tests were carried out with brand new pic-
positive pictures, the rules of the game were made even more challeng- tur.cs, ncvcr shown to thc pigeons before. Herrnstein et al. (1989)
ing. They were now shown a large number of miscellaneous scenes, and trlincd pigcons to tirllow "an Abstract relational rule" by pecking at pat-
key pecking obtained food only when the picrure included a Person or tcnls in wlriclt ortc otrjcct rv:rs insiclc, rathcr than outside of a closed
part of a human figure. All otl'rcr picturcs wcrc unrcwardctl <lr ncgativc. linc:u'(igrrrt'. Ilt'r'r'rrstt'irr (l()t14. 1990) d<;cs nor claim that these con-
Thc positivc picttrrcs might show nlcnl w()nrcn, <lr chiltlrcn; tltc httttr:rtt ('('l)ts:tt't't't;utr'.tk'ttl l,r tlrt'r'it'lr rnt':urirrg colrvcvctl lry w<lrcls in human
130 Chnpter Sm Concepts l3I
language, but some elementary classification of very diverse scenes is much more difficult for a pigeon than selecting pictures containing a
clearly accomplished by the pigeons. certain feature such as a tree) person, or fish when the actual appearance
This type of experiment has been further elaborated recently by of these objects varies enormously in prominence and other ittributes.
Wright, Cook, Rivera, Sands, and Delius (1988) to test whether pi- Distinctions that seem elementary to us may nor be at all obvious to
geons could master the concept of same versus different. In several pre- another species. And, conversely, tasks such as recognizing an important
vious experiments, pigeons had failed to make this distinction in a reli- class of object even when it differs widely in size and othlr attributes is
able and convincing fashion. Wright et al. developed a modified Skinner probably of crucial importan_ce in identifying edible foods or detecting
box in which three pictures 5 x 6 cm in size were projected side by side dlngerous predators at a sufficient distance to permit successful escape.
on the floor instead of the wall of the Skinner box. The pictures were Noticing rvhich two of three objects are the sarne does not have any
cartoons produced by a computer graphics program. When the pigeon particular salience in the real world, where animals live under natural
pecked at the correct picture a simple mechanism dispensed seeds di- conditions. But learning to recognize some category of important ob-
rectly on the screen where the picture was projected; thus the associa- jects such as food or predators is often a maner of life and diath. When
tion of a given picture with food was closer than in the standard Skinner a new type of food becomes available, it is imporrant for many animals
box. In each trial three pictures were projected on the three screens, and to recognize rt whenever possible without expending enormous time
either the righthand or the lefthand picture was identical to the central and effort trying and rejecting a huge range ofobjects. The sarne consid-
one. If the pigeon had grasped the rule that the correct picture to peck eration is even more important with respect to dangers. A similar sirua-
was the one that was the sarne as the middle picture, it should perform tion is indicated by the experiments of Roberts and Mazmanian (I9gg),
correctly when presented with wholly new sets of pictures. who found that pigeons could more easily distinguish one kind of bird
Two pigeons were trained by repeated trials with two cartoons-a from another than-make more general diitinctiois such as birds versus
duck and an apple. Sometimes the duck was the central picrure and at other kinds of animal. The results of these experiments make excellent
other times the apple, ffid the matching picture varied irregularlv in sense from the perspective of a naturalist. Experiments on animal learn-
position, left or right. After 1,216 presentations during seventy-six ing will probably become more significant when they employ stimuli
trials, the pigeons were making the correct choice 75 percent of the and discriminations comparable to those that are importani in the nat-
time. But when tested with new sets of picrures they performed onlv at ural lives of the animals concerned.
the chance level. It proved very difficult to train these birds to make the It seems reasonable to suppose that when the pigeons are working
correct choices with a third and fourth set of pictures even after many hard in Skinner boxes to solve these challenging problems, they are
sessions. Two other pigeons were shown I52 different sets of pictures thinking something like: "Pecking that thing gets me food"; that is, it
in each day's testing session, and each picrure was shown only once in seems most plausible to suppose that they classi$, things simply as rhose
the seventy-six trials. Learning was slow and uncertain, but after 360 that do and don't produce food. In any event) it is difficult to imagine
training sessions over eighteen months they were making 75 percent learning to solve such problems without at least basic and elem.ri".y
correct choices. When these pigeons were presented with new sets of percePtual consciousness. To be sure, strict behaviorists reject *y ru.h
pictures, however, they did slightly better, 83 percent correct. Evidently interpretation, and insist that it is unscientific to speculate about even
the lengthy training with I52 sets of pictures had enabled the pigeons the simplest sorr of subjective thoughts of other species. While we can-
to recognize that the correct picture, whatever its nature, was the one not prove conclusively whether or not a pigeon making these categori-
that matched the central image. Wright et al. (1988) conclude that "the cal discriminations thinks consciously about the pictures or the fearures
ability to learn a concept (same-as-the-center-picture), however, does that lead it to peck or not, its brain must, at rhe very least, classi$, com-
not mean that this is the pigeon's preferred learning stratgy. Quite the plcx visual stimuli into one of two categories.
contrary, it is clear from the vast arnount of research with pigeons that Thc.sc cxpcrinrcnts stimulated a number of further investigations, be-
they prefer to attend to absolute stimulus properties and to form item- cett.sc tltcl' .1.,'t't()nstmtc(l tlrrrt pigc<>ns could learn not only specific stim-
specific associations." trli lrtrt gt'ltt't'.tl (.tl('llorit's. 'l'lrc lr:rsic firrtling ha.s bccn replicatcd in other
lt is intcrcsting that tl'ris problcm of nratchirrg to .r s:un1'rlc sccnrs l:rllx':rtont's rrsirr1,, s,,rrrr'u'lr.rr tlillt'r'cnt pnlcctltrrcs. F..<lr cxamplc Siegel
132 Chapter Six Concepts I33
and Honig (1970) repeated the Herrnstein and Loveland experiment of positive and negative categories did not look very much alike, and
using a Skinner box but varying the procedure by either showing the from the pigeon's point of view they did fall into nvo functional cate-
positive and negative pictures (with and without people) simulta- gories-those that yielded food and those that did not.
neously on adjacent parts of the screen or sequentially, as in the original Lea (1984) doubdess spoke for many psychologists when he worried
experiments. Again the pigeons transfcrred their discrimination to about just what we mean by acquisition of a concept, and whether the
brand new exarnples, and they performed above chance levels when the experiments of Flerrnstein and others suffice to show that these birds
pictures were upside down and when the negative pictures were photo- have the concept of person, tree, or whatever object was present in a
graphs of the sarne scene as the positives but without a human figure. variety of forms in the positive picrures at which they learned to peck
In another replication Malott and Siddall (1972) used a modification more often than at negative pictures lacking such objects. He and others
of the Wisconsin General Test Apparatus developed for training mon- seem to agree that the best definition of concept recognition, in contrast
keys and other animals to discriminate arnong various objects. The pi- to learning to respond to a stimulus attribute such as color or shape, is
geons poked their heads through an opening in the wooden box where that recognition of a concept can only be inferred 'khen there is no
they were confined, and looked at two wooden cubes. On the faces of simple single perceptual feature on which a discrimination could be
the cubes visible to the bird were glued colored photographs clipped based." This definition is unsatisfying because it rests on a negative cri-
from an illustrated magazine. When the bird pecked at a positive picture terion, and proving negatives is notoriously difficult; strictly speaking,
containing people, the cube was pulled away, uncovering a shallow well it is impossible. Thus one can always posrulate that some simple feature
containing a kernel of corn; pecking negative cubes with miscellaneous that has escaped the notice of the investigators but has been recognized
pictures of geometric shapes, machinery, landscape, furniture, or ani- by the pigeons as a signal meaning "pecking that gets me food." But this
mals yielded no food. Each positive picture was presented until the pi- idea avoids granting that pigeons can understand simple concepts only
geon had made five consecutive correct choices, and then t'wo new pic- by postulating a literally "superhuman" ability to discern some simple
ture cubes were presented. After somewhere between three and but single feature that is present in the positive but not the negative
seventeen such problems had been solved, the pigeons very seldom pictures.
pecked at cubes with negative pictures that contained no human figures. Another complication in interpreting these experiments stems from
Then, in the critical tests, wholly novel pairs of pictures of the sarne the remarkable ability of pigeons to learn and remember hundreds of
general sort were presented, ild the pigeons performed almost per- specific pictures, and to respond appropriately to most of those that
fectly. yielded food even weeks or months after they were last seen (Skinner
These results were so surprising to those who had tended to view 1960; Greene 1983; Vaughan and Greene 1984). For instance Wilkie,
pigeons as stupid "learning machines" that alternative, simpler interpre- Wilson, and Kardal (1989) have trained pigeons to recognize airplane
tations have been advanced to explain these findings. M*y psycholo- views of a particular geographical location. Other birds have compa-
gists have been reluctant to agree with Herrnstein that pigeons can learn rable abilities, as demonstrated, for example, by the experiments re-
a concept. Yet something in the pigeon's brain must correspond at least viewed by Balda and Turek (1984) showing that Clark's nutcrackers re-
roughly to what we call the concept of person, tree, or fish. In a review member where they have stored hundreds of seeds. But the ability of
of animal cognition, Premack (I983a, 358-59) expressed frustration pigeons to respond correctly to most if not all of nnu positive or nega-
because of "the inability of the reader (of these papers)-who is shown tive pictures they have never seen before rules out an explanation based
only a few of the test photographs-to judge for himself the author's on a sirnple memory of specific pictures.
claim that the concepts could not be formed on the basis of 'simple As might be expected, behavioristic psychologists have been very re-
features."'Premack had "never found this claim entirely convincing. Pi- lLlctant to intcrprct thcsc cxperiments as evidence that pigeons might
geons have never been shown to have functional classes-furnirurc, rhink corrsciously rrbout thc catcgorics that they learn to distinguish.
toys, candy, sports equipment-where class members dt> not l<>ok alikc; Ilor cxrunplc l'rcrrr:rt'k (l9tl3a) rlcscribes experiments by Epstein,
they only recognizc physical classcs-trecs, htrntlrrs, birtls---rvlrcrc clrrss L:lnz;r, :rrrtl Skirrrrt'r ( l()l'lO) in tlrt' lirlkxving tcrnrs: "The lrasic approach
mcnrbcrs tl<l l<xrk rrlikc." IJut in nt:uly <lf tltcsc cxpcritttt'nts t lrt' cx.ttttplcs Irlts lrt't'lr to llrtl Pt'rlolrr.rrr.t's ilr:lIr1'.5 1rr ln<lnkcvs tltat Arc rccom-
134 Chapter Six Concepts I35
mended as proofs of mind and then demonstrate the sarne performance Initially the pigeons had no way ofknowing these rather complicated
in the pigeon. Although this could backfire (and be taken as showing rules of the Skinner box game, md they were equally likely to peck at
mind in the pigeon) . . . the opposite conclusion is drawn: what need is any one of the four corner keys, so that their choices were correct only
there for mind when there are contingencies and reinforcement?" In about one quarter of the time. Every day the pigeons were given forty
this exchange Epstein and his associates were expressing doubt that ex- trials, ten with each type of picture, md after ten days they were per-
periments on self-recognition by chimpanzees (discussed in chapter 12) forming better than chance. By thirty days they were making, on aver-
demonstrate that they had minds, using as an argument the fact that age,76 percent correct choices. By this time they had had ample oppor-
somewhat similar performances could be elicited from pigeons by tunity to learn all fony pictures, each of which they had seen thirty
means of operant conditioning, apparently taking it for granted that times. Since pigeons can learn and remember dozens or hundreds of
pigeons are mindless. Premack's use of the term "backfire" captures pictures and identify at far better than chance levels those that get them
nicely the widespread reluctance of psychologists to credit even as com- food, at this point the experiment had only shown that pigeons can
plex animals as pigeons with any soft of mental experience. learn four sets of pictures at the same time and respond to them by
A recent extension of the pioneering experiments of Herrnstein and pecking the correct one of the four colored keys. The critical stage of
Loveland has strengthened the case for something approaching the con- the experiment consisted of mixing in among the ten familiar pictures
scious awareness of simple concepts or categories, although, to judge by of each type entirely new and different pictures containing one of the
some of their other publications, the psychologists who conducted the four key features. The pigeons still made primarily the right choices,
experiments would probably dispute this interpretation of their find- although they were correct a somewhat smaller fraction of the time . But
ings, as discussed below. E. A. Wasserman and several colleagues trained they did generalize to new examples of these four types of picture at
pigeons to recognize and distinguish four categories simultaneously much better than chance levels. In another experiment of the same type
(Bhatt, Wasserman, Reynolds, and Knauss 1988; Wasserman, Kiedin- the pigeons learned to classify stimuli into four types without ever
ger, and Bhatt 1988). Their apparatus and procedures are of interest, seeing the same slide twice.
because they provide additional hints about how the situation may ap- In later experiments Wasserman and his colleagues (in preparation)
pear to the pigeons. The Skinner box was provided with a 7 x 7 cm have trained pigeons to discriminate between pictures of human faces
viewing screen and four circular keys I.9 cm in diameter and located expressing strong emotions such as anger or sadness. The pigeons re-
2.3 cm diagonally from the four corners of the picture screen. When sponded correctly at better than chance levels to new pictures of differ-
activated, these keys differed in color. In preliminary training the pi- ent persons displaying the sarne emotions. Of course, the training could
geons learned to get access to food by pecking first the picture screen not teach the birds anything about the emotions of the people photo-
and then whichever one of the colored corner keys was illuminated. At graphed when sad or angry. But these experiments do show that fairly
this stage the picture screen was a uniform white. subtle categories of visual patterns can be learned by birds. This ability
After this task had been mastered, the pigeons were presented every probably stems from the very widespread need to evaluate the likeli-
day with a series of forty pictures, ten of which included a cat, ten a hood that a predator will attack or that a given spot is or is not some-
flower, ten an automobile, and the other ten a chair. As in earlier exper- thing edible.
iments of this type, the pictures varied widely in content and the cats, Wasserman and his colleagues conclude from these and many related
flowers, autos, and chairs also varied widely in size, color, and position findings that "the conceptual abilities of pigeons are more advanced
in the picture. Along with these pictures all four of the corner lights tlran hithcrto suspected" (Bhatt et al. 1988, 219), and that "these results
were turned on, and the pigeon was required to peck a different corner suggcst that many worcls in our language denote clusters of related vi-
light if the slide on the central screen contained a cat, a flower, an auto- sual stirntrli which pigcons rrlso scc as highly similar. To the degree that
mobile, or a chair. The pigeons obtained food only if they first peckcd r-cirrfirr-ccnrcnt contirtgt'rtt'ics t'orrclrttc with these human language
at the picture about thiny times and then pecked at the correct or-rc of gr<rtrpin61s, pigcorts'tlisr'r'irttirt.ttiort lc:trning is l'rastcncd and generahza-
the four colored keys. Only this key activated thc f<xxl ho1'rpcr :rntl pro- li<lrt t<) rt('\\' .uttl .tllt'r't'tl t'x.uttlrlt's is t'rtlr:u'rt'ctl" (ffisscrnran, Kiedinger,
vidcd somcthing for thc hungry bird to cat. :rrrtl lllt:rt1 l()llll, -2.15 t lrr kt'r'1,rrr1q u'itlr tlrt' lrt'h:rvioristic traditi<tn, thc
136 Chapter Six Concepts 137
papers describing these impressive achievements of pigeons are titled understand other relatively simple concepts as unnarned thoughts.
"Conceptual Behavior in Pigeons." Presumably this wording was cho- There is little reason to suppose that thinking about unnamed rr..rrib.r,
sen to reinforce the behavioristic insistence that any mental terms be had been useful enough in the past for nrr,rral selection to have favored
scrupulously avoided. Animals may behave as though they utilized it specifically. Yet when it became important to think in this way to ger
simple concepts, but behaviorists are constrained to ignore or deny the food, ravens and a few other birds learned to do so, apparently emplJy-
possibility that they might consciously think about the categories or ing general ability to learn simple conceprs. To be r*., seibt 1r^laiy
concepts that must be postulated in order to explain their behavior. has argued that since pigeons can learn as easily to peck three times
It is significant that Wasserman (198I, L982,1983, 1984, 1985) has when shown two lighted spots as to peck rwice when rlio*, three, there
argued vigorously in favor of the behavioristic taboo against any impli- is no basis for the claim that birds have an unnamed number concept in
cation of consciousness despite the recent revival of research on animal the sense claimed by Koehler. But these data can just as easily be inter-
cognition to which he has made important contributions. For example: preted by crediting pigeons with the ability to learn r*o .ori.lated un-
"I, for one, have tried to steer clear of the possibility of subjective expe- named numbers, that of the stimulus and that of the required response.
rience in my animal subjects; the more prudent of my professional col- Davis and Memmon (1982) have pointed our that although several
leagues have as well; . . . cognitive psychology need not be construed as birds and mammals have been able to learn to count in the sense of
mentalistic. Those cognitive processes that are said to mediate behav- responding selectively to different numbers of objects, this is a relatively
ioral relationships are the public behaviors of scientists, not the private unnatural sort of behavior that has only been elicited by "relatively ex-
experiences of their subjects" (Wasserman 1983, fO-II). And, more treme experimental conditions." Capaldi and Miller (l9gga, lgggb)
recently: "No statement concerning consciousness in animals is open to and Davis, Mackenzie, and Morrison (1989) have demonstrared thar
verification and experiment. Isn't it time we set aside such tantalizing, rats are capable of a simple form of discriminating what is somerimes
but unanswerable, questions and direct our energies to more productive called "numerosity" to distinguish it from the sort of counting by men-
pursuitsl" (Wasserman 1985). Perhaps as psychologists come to recog- tally assigning successive numbers as we usually do. Numeiosity is a
nize such similarities between human and animal cognition, they will rudimentary type of concept that lies within the capabilities of ai least
gradually begin to suspect that human and nonhurnan mental experi- some birds and mammals.
ences may also have much in common. Hediger (1968, L976) has reviewed evidence that many mammals
In a fcw special situations animals give evidence of thinking in terms can recognize their narnes when these are used by zoo keepers. Of
of simple concepts such as numbers or even narnes of individuals. The course, domestic animals and pets routinely learn to come when called
German ethologist Otto Koehler and his colleagues at Freiburg in by the narnes given them by their human owners. Hediger suspected
southwestern Germany carried out nurnerous experiments on the abili- that certain animals had "unnamed names" for other animals and for
ties of birds to solve problems that required what he called "wordless familiar human cgmpanions. But although many animals undoubtedly
thinking," meaning that they thought about objects and relationships recognize individually other members of their species, there is no con-
but not in terms of words (Koehler 1956a,I956b, 1969). In one of the vincing evidence that one animal addresses another by some individual
most impressive of these experiments, birds were trained to select from ,-r1r.,, although rhe recent investigarions of Tyack discussed in chapter
a number of covered vessels the one having a certain number of spots I I suggest that the individual-specific "signarure whisrles" of dolphins
on the lid. The spots varied in size, shape, and position, but a well- rnight be used as something roughly equivalent of narnes for familiar
trained raven could reliably select the pot with any number from one to c<lmpanions.
seven sPots. Davis (1989) has reported that rats learned that they could obtain
From the results of many such experiments Koehler concluded that fixxl in rr ccrtain siftration, lrut only when the experimenter was not
these birds had the concept of numbers from two to seven, which hc l)rcscltt t() Prc\/cnt tltcltt lr-<lnr otrtrrining it. The rats carne to refrain from
called unnamed numbers. This ability may be comparable in somc weys cllirrts to t'crtch tlrt' lixrtl u'ltt'rr tlrc cxpcrimcntcr was present but took it
to the very earliest stages of undcrstarrdirrg of numbcrs in prcvcrt'ral chil- rt'ltt'lt ltt'tt':ts.tlrst'ttl.'l'lrr'r'lr.rtl tlrrrs lc:rrnctl thlrt thc prcscncc of an ob-
drcn (Gclman and Gallistcl 1978). Kochlcr rtlso helit'r,t'tl tlr.rt .rrrirrr:rls it'tt tpritc tlillt'rcrtt ltoru tlrc loorl nrt'.urr rlrr'\,rvorrkl lrc prcvcntcd fi<lm
138 Chapter Six Ooncrpts l..lrt
obtaining it. This is so simple a relationship that it scarcely deserves to that they had been visiting for some time. They were carriccl irr tl;rr.k
be called a concept, but it is an example of the softs of contingencies closed boxes to another location, released, ffid their initial flight tlirct.-
that animals often learn. tions observed. The hive, the food site, and the experiment'al rclc:r.sc
The directional orientation of honeybees provides further examples point were located-at the apices of an equilateral triangle, so that t6c
of moderately complex integration of information derived in different direct route from the new location to thi food source ivas 60 degrccs
ways and at different times. M*y of the relevant experiments have been different from the original flight direction from hive to food. Mo"st of
conducted by Dyer and Gould (1981), md by Gould (1980, 1982, the bees started in this new direction, ancl to judge by the time needecl
1986, 1990), and the general subject has been reviewed by Gould and to reach the food.they flew quitg directly. This exferiment was repeated
Gould (1988), Gould and Towne (1988), and Gallistel (1990). M*y with similar results at hive-to-food disiances or roo and 350 ,ir.t..r,
of these experiments were possible only because honeybees employ a and with the location of food source and release point interchanged, so
symbolic communication system, discussed in detail in chapter 9, that that the new direction of flight deviated from thi normal hive-tl-food
allows them to convey to their sisters (and to eavesdropping etholo- direction by 60 degrees clockwise and counterclockwise. But when the
gists) the direction in which a desirable source of food is located. Ordi- bees were carried 4,425 meters away, they departed randomly in
a wide
narily this direction is indicated relative to the azimuth direction of the variety of directions, as would be expected since it is rare for honeybees
sun. This of course changes during the day, and if bees are prevented to forage this far from their hive. Gould inrerprers these data as d.--
from communicating about a desirable food source for some time, they onstrating that honeybees employ what are called ..cognitive maps,,, that
indicate not the direction in which the food was located when they vis- is, they have some sort of internal representation of tle g.o-.*i.al
ited it, but a different direction that results from at least a rough com- lationships of impoftant objects and major landmarkr, i,d use this to
pensation for the sun's apparent change in direction. The rate of change orient their flight when displaced to a novel location within rhe area
in sun azimuth varies considerably with season, latitude, and time of with
_which they are familiar. Similar experiments with rats and other
day, so that bees face a problem in achieving this compensation. The vertebrates have been carried out by Tolman and others, but insects had
results of experiments reported by Gould (1980) indicate that the com- not been believed capable of this level of cognition.
pensation is probably based on the rate at which the sun's azimuth was
changing when the bee flew to and from the food source.
_ Menzel (1989), Menzel et al. (1990), w.ht.. and Menzel (1990),
wehner and wehner (1990), wehner er al. (1990), and Dyer
When the sky is completely overcast, bees still communicate the di- have conducted similar experiments with honeybees but th. i.srrlis have
rection in which they must fly to reach it, at least under some condi- indicated direct orientation toward familiar landmarks rather than the
tions. Earlier experiments reviewed by von Frisch (1967) indicated that use of cognitir,'e maps. Gould (1990) has presented evidence that in
bees remember the food location with reference to landmarks. But experiments the local terrain did not provide specific landmarks that
Gould (198I) found that after displacement to a new location under a were within the resolution of honeybee panern iirior. perhaps differ-
completely overcast sky their directional communication is still ex- ..1:.r in local ropography or in the of the be.s .rnderly this
pressed relative to the sun even when this direction must be remem- difference in experimental results. At "*p"ri"nce
present the question ,.mrin, ,n
bered. Furthermore, this memory must include at least an approximate oPen one, and further experiments are needed to clarify the situation.
compensation for the time of day. This sort of directional communica- But whether or not honeybees are capable of using cognitive maps, they
tion cannot help to recruit completely naive bees, but in many cases the are certainly able to integrate more than one type of iensory input
active foragers from a particular colony are likely to be familiar with storcd parterns in determining in which direction to fly.
major local landmarks, so that the information that food is available in An<>thcr s.rt of cvidcncc suggesting that honeybles may think in
a particular direction can presumably be interpreted as meaning to fly tcrnrs of c<lrrccpts strch :rs tlrc naturc r>f flowers and where within a
along a conspicuous linear landmark such as the edge of a wooded arca (lowcr thc nccr:rr is ro bc obr:rincrl hrrs l-rccn rcvicwcd
by Gould (1979,
bounding an open field. l9tt2). I Ittltt.tlt .tglit'rrlttttt' ol'lt'rr [)r'('s('r]rs honcybccs witlr challenging
In later experiments, Gould ( I986) ot'rscrvccl thc flight tlircctions ol' problcrrrs.'l'lrt'.rrrtlrr.rs ol .rll,rll.r lk)\r,(.r.s rlrr-ipg li:rck vig6r<ltrsly., iir_
bees capturccl as thcy lcfi thc hivc t() rctrrnr to rt tlcsirrrlrlc lirotl st)rrrcc itilrg iltst'tl, tlttts (lltsttltli rt rr rtlr ;rollt'rr 'l'1,.'i.. ll,,u,t.ri,rrc,r,l,r1-,tctl filr
I40 Chapter Six Concepts 141

pollination by larger insects such bumblebees. When honeybees enter

as area where flowers open and make nectar available may expand with the
them they are knocked about so violently that they learn very quickly to sunlight under some such conditions, so that a similar exirapolation of
avoid alfalfa. But when no other flowers are available, honeybees learn expected food locations might be advantageous. Perhaps the repertoire
to enter only alfalfa flowers whose anthers have already been tripped by of genetically programmed foraging ractics encoded in honeyb.t oxa
another insect, or, when the colony is in extreme need of food, they bite provides for this special situation. But even if we accept this rather far-
a hole in the back of the alfalfa flowers to reach the nectar. This atypical fetched explanation, we must still credit the bees withadapting a ractic
method is also used in other situations, as reviewed by Inouye (1983). ordinarily used in the early morning near steep mountains io flit terrain
A final thought-provoking type of behavior that suggests conceptual and to other times of day.
thinking has been observed by several investigators of the symbolic
communication of honeybees that will be discussed in chapter 9. To
observe communication about distant resources, investigators must in-
duce bees to visit controlled food sources at distances of several hundred
meters. To accomplish this, often in the face of serious competition for
the bees' attention from natural flowers, a concentrated sugar solution
is first provided in a small dish right at the hive entrance. After many
bees have begun to gather sugar solution from such a feeder it is gradu-
ally moved farther and farther from the hive. At first it can be moved
only a few centimeters, later a meter or so, without losing the bees. But
when it is about 30 meters from the hive, the experimenter can move it
by much larger jumps, and the sarne bees return to it after carrying
stomachs full of sugar to their sisters in the hive. When the feeder is
more than 100 or 200 meters from the hive, it can be moved 20 or 30
meters at a time, and many bees that have visited it at previous locations
begin to search for it beyond where they found it last. Thcy seem to
have realized that this splendid new food source moves, and that to find
it again they should fly farther out from home. If so, they may be think-
ing in terms of the simple but abstract concept of a moving food source.
There is some doubt whether this conclusion is justified by the avail-
able evidence, for adequate experiments have not yet been reported that
would rule out other interpretations, such as a tendency to scatter in all
directions around the former location of the food, so that a few bees
would happen to arrive at its new location. Nevertheless this possibility
deserves further investigation, because if bees do extrapolate the posi-
tion of food sources in such a situation, this ability would represent an
unusually enterprising versatility of behavior and perhaps of conscious
thinking. Of course, real flowers do not ordinarily move 20 or 30 mc-
ters in a few minutes, so that it is difficult to imagine how natural sclcc-
tion would have prepared honeybees to extrapolate the position of a
moving feeder. Yet one can imagine natural situations where somcthillg
similar could occur. Ncar stccp mountain ridgcs thc rrrca of nronring
sunshinc gradually cxpancls as tlrc ntourttairt's shrrtkxt' tlirttirrislrcs. 'l'hc
Physinhgical Indices oJ"l'hirtkittr, | ,t.r

CHAPTER SEVEN Later alizarion of B rain Mechanisms controlling

Communicative Signals
The investigation of animal communication discussed
below in cha,rcr.s
P hysi,ologicnl In d;ices 8 to 11 hal yielded unexpected evidence that particularup..io
constituted that specific ttp_es of sounds o. othei signals
,." ,,,
are mrch morc
imponant to them than other physicaly compara6re
of Thi,nhirug cases
signatr- r, , r"*
this has led to the proceriir^rq of iuch importanr types
of signal
being concentrated in one side of lhe brain. Th'is is best
known in the
case of human speech, ffid indeed it.was
lateralization of rguea until quite ...lrruf ,nr.
:peech conrrol, ordinarily"in the left tempo.J-.1*"*,
,ki.g it for granted that both behavior and conscious thinking was. a qualitatively unique human attribuie
and formed a ihysiologicar
result from the functioning of brains or central nervous systems, we may basis for our superior mental abilities based o., lrngJrg.. B;i,hi,
appropriately inquire whether the extensive srudies of brain function all-or-nothing"m.dl
dichotomy is no longer tenable, because several cases
have provided any evidence concerning the particular processes that have been discovered in which animll brains alro con.entrate
the pro-
produce conscious thought. Although a thorough review of the cogni- cessing of communicative signals in one side of the
brain. The clearest
tive neurosciences is far beyond the scope of this book, a few especially example is the lateralization of control of singing in songbirdr,-*hi.h
also shows other intriguin^g parallers to late.ji ,oitionof
salient experiments provide significant evidence that conscious thinking lio-*'rf"..h
control (Nottebohm 1979; Konishi l9g5; Arnold *a n"rg.r-igss,
is not a monopoly of our species, or even of our close relatives. )ohn (in
Thatcher and ]ohn 1977), among others, has equated consciousness McCaslan d L987).
with a sort of internal feedback whereby information about one part of Other instances of lateral specialization of brain mechanisms
for the
a paffern of information flow acts on another part. This may be a nec- control of communicative signals have recently been discovered
in mon-
essary condition for conscious thinking, but it is not sufficient, for it is keys. one of the clearest halbeen demonstraied by Hamilton
and ver-
also an aspect of many physiological processes that operate without any -..i.: (1988), who studied rwenty-five monkeys (Macaca rnwlatto) in
conscious awareness on our part. yhl+ the corpus callosum connecing the t o ..r.urJ r,.#rprr.r.,
Human speech depends heavily on certain areas of the temporal cor- had been.surgically cut. In such animis, or in human
patients whose
tex (principally Broca's and Wernicke's areas); but this localization of corpus callosum has been cut in order to control severe
the two
function is not precise and absolute, for damage to particular parts of halves of the brain operate more or less separately.
tn tt"pit"pry,
the speech control areas does not always produce the same effects, as monkeys the hippocampal and anterior iommirrrr", "r"'t*".rty_fi,u.
and the ootic
chiasm were also cut in the midline, thus separating
reviewed by Lecours et al. (1984). Furthermore, as far as neuroanatom- rr,.
cerebral correx more completely than in many othJ. ,.split
*",iJ., #,rr"
ical evidence goes) these areas of the brain are not unique to our species. br"i'i.*.r_
Homologues of Broca's and Wernicke's areas are present in other marn- iments of this genglal type. The monkeys rrad recoveied
fully and be-
mals, but they are not called by the salne nalnes since the animals are haved quite normally that when allowed to see things with only
one eye, only one cerebral cortex received visual input.
incapable of human speech. Nevertheless a few recent discoveries about This allowed the
brain mechanisms controlling communicative behavior in monkeys ancl cxPerlmenters to train them to make various visual
birds do throw some light on these questions because these mechanisms .scparatelv with either the right or the reft cortex.
when ,.qrir.Jio air-
share some properties with those that control human speech. crimirarc lrcrwccrr ^straigrrt lincs differing in slope by l5'a.gr..r,
Ittonkcys pcrfirrlttcd significrrrrtly bcttc. *1.., .rrirrg
tn! t.t rr.firirprr".".
llttt rt'ltt'll thc Prolrlcrlr \\':ls to tlist'rirrrirr:rtc [-rcr*c.I pictures of
thi faces
ol-illtliVitltl:tl ttlotlkt't's. tlrt'ri1,,lrt ('()t'r('x w:lri su[)crior. Thc.sc
\\'crc (lll.llllit.tttvc .ttttl ttol .llrs,lrrtt'; lrotlr Irt.rriislr6crcs c.tr1l
lcar. t.
144 Chapter Swen Pbysinlogicallndices ofThinhing I45
perform both discriminations, but the superiority was clear and statisti- second was the frequency at which the coo began. one of the other
cally significant. species, the vervet monkey cercopithecus oethiopi, does not use coos in
The recognition that primate vocalizations conveyed specific infor- its social communication; the other two do have coo-like sounds, but it
mation in addition to levels of emotional arousal began with very de- is not known whether they have any special significance to the animals
tailed studies by Green (1975) of the sounds exchanged by |apanese themselves. The /apanese macaques consistenily learned the discrimi-
macaques (Macam fuscata) in relatively relaxed social situations. He nation of peak position more easily than the other three species, but
found that a group of sounds most readily described as "coos" differed they were Poorer at learning to discriminate on the basis oi th. initial
in acoustical details, even though they had at first seemed much the frequency. Thus the perceptual capabilities of these species of monkeys
sarne to human listeners. Furthermore certain types of coo-like sounds appe-ared to be correlated with the acoustic features of tfr. sounds they
were used most often in specific situations. For example, "smooth early use for social communication.
highs," which began at a fairly high frequency, rose slightly, and then In related experiments these coo-like sounds were presented to |apa-
declined in pitch, were usually emitted by infants sining apart from nese macaques and to five other species of monkeys th.ough earphones
their mothers. On the other hand, "smooth late highs," in which the that allowed the experimenters to present the stimuli to eilher the right
frequency rose steadily to peak near the end of the call before dropping or the left ear (Petersen et al. 1978,1984). since most of the auditory
slighdy, were most often used by sexually receptive females. This and neurons of mammals cross the midline before reaching the cerebral cor-
other observations indicated that these cooing sounds were especially tex, a right ear advantage means that the left auditoryiortex is playing a
important in the social communication of )apanese macaques. This led larger role than the right in processing such signals. when ,o,rrd, .r.
Tnloth and Gree n (1979) to suggest similarities to human speech. presented to the human right ear, we can usually discriminate small dif-
The coos are not the only vocalizations used by |apanese macaques ferences better than with sounds arriving at the ieft ear.
to corrununicate with their social companions when they are close to- All five. /apanese macaques showed i significant right ear advantage
gether and interacting amiably. Another type of sound, called "girneys" ^ detecting
for the position of the frequency pe*, whil-e only one of the
by Green, have been studied in detail by Masataka (1989). These are monkeys showed this effect. when the monkeys, task was to make
sounds with multiple harmonics that rise in frequency and fall toward discriminations based on the initial frequency of the sound, one
the end of each vocalization. Masataka distinguished two general sorts nese.macaque showed a left ear advantage, while another monkey of this
of girney, those in which the peak frequenry occurred during the first species and rwo of other species showed no difference betwe.r, "th" *o
third of the sound, and others that peaked in the final third. The first ears. It is.importan-t to recognize that these right or left ear advantages
type was often followed by the caller grooming the receiver, while the are not absolute; the monkeys and human listeners can make the dis-
latter type usually resulted in the receiver grooming the caller. Thus criminations with either ear, but more often perform better when the
these rwo types of sound seem to mean something like "I'[ groom you;' sound is delivered to one of the rwo ears. This evidence that
and "Groom me." This interpretation was supported by the results of
Ta:agu:s, but not the other sp-ecies tesred, process coos primarify with
playbacks of tape-recorded sounds, which were followed by motions their left auditory correx was further supported by the &p".irrr.rrts of
and gestures that strongly indicated that the hearer expected to be Heffner and Heffner (1984), who trained animjs to make the same
groomed or to groom the companion nearby. This is an additional ex- discriminarion berween coos on the basis of the position of the peak
ample of the subtle differences in animal signals that used to seem mean- fiequency. Then parts of the brain were surgically removed, a.rd afte.
ingless but have been shown by careful experiments to convey different rccovery the monkeys were tested again in the sarne way.
messages. when thc auditory correx on both sides of the brain was removed,
Building on these findings, Zoloth et aL. (1979) trained fapanesc ma- thc nl<lnkcvs c<>ulcl tr<> longcr make this discrimination even after addi-
caques and three other species of monkeys to discriminate bcrwcctt tiort:tl trrrining. llrrt tlrc1, Pcrlirrrnctl normally when only the right audi_
tape-recorded coos on the basis of two acoustic fcaftrres. Thc first wls t()rv c()rtcx \,\1:ls rcnrovt'tl. Alit.r' thc lcfi :rtrclitory cortex had Leen de-
the position of the frequency ;lcak, early <lr Lrtc irr thc sourtd. which slrrrl,ctl. tlrt' rrronkl'1,.' lrcr li,r rrr.rn('(. \virs initially p(x)r; but with further
sccms to convcy clilll'rcrrt nrcrnings t() thc )rr1'r.utt'sc r)lrlcrl('lucs. rrntl tltc tr':rillilrg it irrrprrrvr'tl .tntl rr'.rtlrt',1 rts li)nn('r'lt'vtl. Il,itlcrrtly t6csc nlon-
146 Chapter Seven
Tbinhirut l.l
Physi.ologtcal Ind,ices of

keys had been using the left auditory cortex before the operation but spond to pictures faces, whether these be actual simian
faces or pictures of-of
or hrrrr.rr
could relearn the discrimination with the right cortex when necessary. them. The extensive literarure on this sort
of sclcc-
This result is intriguingly similar to the localization of human speech responsiveness has been reviewed uy rur.*sell
ly^.^ and Newsonrc
perception in the left auditory cortex) more specifically in Wernicke's (1987), and representarive recenr experiments
on face ...ojrLirrg..u_
area. rons is described and analyzed by peirett,
Rolls, and caan (r9g2). Bay_
These experiments indicate that recognition of at least one type of lis, Rolls, and T eonard (ilssl reporr evidence
thatsome neurons are
sound used in social communication is concentrated on one side of the selectively sensitive to partic.rlai mont.f
a..r. we do not know
brain in one species of monkey. Lateralization of speech perception and whether a monkey is moie or lesslikely a u..""scious
of recogn izing
control used to be considered a unique brain mechanism underlying the face of a known companion when th.r.
neurons are active. But the
human speech and thought. The finding of similar lateralization in fact that a central t.*oir. system can be so organized
thai p#..rtr.
songbirds and in ]apanese macaques is reminiscent of the nineteenth- cells respond to very specific types of patternef;
stimuli does demon_
century controversy between Owen and Huxley over the former's claim strare what refined types of diicrimination
are possible for p.i-rt.
that there was no hippocampus in the brains of nonhrunan primates. brains. It would be of great interest to carry
out comparable experi_
Fluman mental superiority, enormous as it is, does not seem to be based ments with other groups of animars, using
p#erned stimuli that are of
on any single, unique feature of neuroanatomy. special importance to them.
Recent technical developments have allowed noninvasive procedures
to depict which parts of a brain are most active, but these methods are Physiological Indices of Conscious Thirkirg
complex and expensive and have so far been employed for the most part
in human clinical investigations and diagnosis, as reviewed by Posner et Inasmuch as cognition is obviousry an acdve
process carried out by cen-
al. (1988) *d Scheibel and Wechsler (1990). Kosslyn (1988) has re- tral nervous sysr:m:,. neurophysiologists rltt.."pti"g
to understand
viewed evidence that both hemispheres of the human cortex are acti- brain function seek objectirr" data thatlrn b.;;;i"red
when brains are
vated when subjects experience mental images-a clear example of how engaged in their complex and enormoys]y
significant activity. Thefrin_
supposedly unobservable mental experiences can be studied. But most cipal data available are electrical potentiali. Tf,ese
clearly r..J-p*i ro,
of these procedures are limited in spatial resolution, so that they would only the conductio, of impulses along ,r.rror*
trr, ,rr. .1-irirfo'.t*t
be difficult to employ with brains as small as those of many animals. In modulating processes that o..,r. at sy.rapres. Ideally,
, ,,zu;;;iiyrioto_
one important recent investigation, however, Georgopoulis et al. gist prefers to record with microelecirod.s from
individual neurons or
(1989) have recorded the action potentials of neurons in the motor cor- synapses, or at most a few at a time. But
when dealing with the
tex of a monkey while it moved a lever to follow the motion of a spot of t9-pl.T
Td rr.s. progesses of cognition, monit6rirrg the -or.
light. The activity of these neurons occurred in the sarne spatial pattern ties of single cells":fic.ant
is clearly of limited rr.."Thi, is because
wharever activ-
as the hand motion that followed after a fraction of a second. This sug- ities of central nervous ryit.-r lead to.ogritior,
*d.orrr.ious thinking
gests that the monkey was perhaps thinking about the movement it was require complex interactions of large.r.rrib.r,
of cells.
about to carry out. But the time interval by which this patterned activity One general type of electrical signal that can be
recorded from central
of the motor cortex preceded the actual movement was a fraction of a nen/ous systems reflects the massed activities of
hundreds or thorrr*d,
second; so one could interpret these data as simply reflecting an early of neurons and synapses. Relatively weak .t..ui.rt signals
stage in the physiological process leading the monkey to move its hand known aselectro.n..phrlo{aqh 1ricl potentials, or, more
as it had been trained to do. as brain waves, can be r..ord.d both fi;; electrodes inside brain tissue
A related area of exciting progress in neurophysiology is the identifi- and als<> fr.rn <>.tsidc a. animar or human skull.
These ppc p"*",irr,
cation of neurons that are selectively responsive to particular classcs of h:rvc bcc, rcc.rtlctl cxtcrrsivcry fr.m thc human
scalp ,"a dra.., gi".
stimuli. Monkeys recognize the faces of known companions, etttl ctlt trscfirl sigrrs ol't'lirrit'.rr :rhnorin.rrirics. N.,r',;;;thyri.,r.,girt.
have been
readily be trained to respond sclcctivcly to skctchcs of rnonkcv frrccs tctnl)tc(l li'olrr tilnt.r,) tln(.to lropt.rlr.rr wirft'r.ifii.i.,rily
clctailed and
(Dittrich 1990). Sonrc t'lcur()ns in thc tcn)lxrr'.rl t'ot'tt'x ol'nronkcvs rc- ilrgcltiorls :tll.tlYsts tltcst' sr1,,rr.rt ,r,r1ilrt lrt.t'or.r-t.llrtctl
witlr spccific..rg,ri-
I48 Chapter Snen Physinlogicallnd.ices ofTbinhing 149
tive activities going on within the brain. These hopes have generally over the left cerebral cortex, as one would expect from the well-knowp
been disappointed, and the prevailing opinion of leading neurophysiol-
fact that the left side of the cortex is much ^-o.. heavily involved in
ogists is that EEG Potentials are too coarse and too gross an index to processing and recognizing speech. But this evidence does not add any-
reieal more than the most general sorts of activity. Nevertheless certain t"g of great importance to what was already known from data on the
efllects of damage to differenr pafts of the human brain.
recent developments in the analysis of electrical potentials recorded
from both human and animal brains offer a tantalizing suggestion that Ne-urophysiologists have found that a different type of electrical po_
with much further refinement this approach might throw some light on tential can be recorded from the human scalp after disirete sensory stim-
the questions under consideration in this book. ulation such as flashes-of light or brief sounds. Ordinarily these .r. ,oo
First it witl be necessary to digress briefly to emphasize that neuro- lo1,^rn.vok"s: to be detected reliably against the backg.ound of other
physiologists are generally cautious scientists who refrain from inter- EEG signals, but this difficulty has been surmounred b| repeating such
preting their data beyond their immediate and clear-cut relevance to discrete stimuli and averaging the EEG porentials. Although this lan be
well-defined questions. Thus they almost never exPress any opinions done.by a variety of methods, the most convenient and effective proce-
about such elusive phenomena as conscious thinking, even though they dure is to use a digital compure-r to average the potentials and display
are concerned with the neurophysiological mechanisms that are gener- them graphically as a function of time after the prir".rtrtion of the ,ii-_
ally agreed to underlie all tyPes of information processing, cognition, ulus. Typically several hundred or even a few thousand stimuli must be
and even consciousness. Conscious thinking has simply aPPeared to be a.velaged to- obtain a clear graphic display, which sets obvious limits
a slippery subject that is considered beyond the immediate reach of con-
the kinds of stimuli that can be studied-. They must be brief-otherwise,
temporary experimental analysis. But behind the respectability blanket excitation from a later part would compli.ai. ,.sponses from the earlier
of siientific caurion, neurophysiologists dare to dream that their science portions-and they musr be repeated many timei.
is gradually building a foundation uPon which an understanding of ..
T!:t. potentials resulting fiom discrete sensory stimulation are or-
conscious thinking will eventually be attained. It is therefore necessary dinarily called evoked potentials, ffid they are described in terms ofelec-
to extrapolate somewhat beyond the tangible evidence and stated con- trical polarity and time or latency after the stimulus. Those poftions of
clusioni in our attemPt to discern how the neurophysiological mecha- the evoked potentials occurring within less than abou. o.r.-t.nth of a
nisms underlying conscious thinking may come to be understood. second are clearly reflections of the sensory impulses traveling from the
peripheral sense organs ro successively
The predominant EEG potentials recorded from an intact brain are -o.. Lterio, porti5ns of the
brain. These are usefirl indices of sensoiy input but.erreal relatively little
of relatively low frequency. They are also ordinarily only a few micro-
volts when recorded from the human scalp. The most prominent are the about cognition, let alone consciousness.
alpha waves with a frequency on the order of 5 to 8 Hz that are most A subset of evoked potentials, usually having ronger latencies are
.uid.rt when the human subject is lying quiedy with closed eyes and is clearly correlated with moderately in6rm"iio., processing.
not engaged in any particular mental activity. If the subject perficrms There are tantalizinghints that under rom. conditions thire -.y d"
related to decision
some mental task such as solving arithmetic problems, these alpha waves Saking or orher simple types of conscious thinking.
diminish in amplitude and merge into more irregular, noisy signals cov- They are usually called evenr related pot.rrtirlr, abbreviated ERps, be-
cause they are not a direct function of the sensory input but are also
ering a broad frequency band. This is a disappointing fact for those who "
*orrld hope to extract from the EEG signals a direct correlate with men- rrftbcted by internal processes within the brain, inciuding previous
tal activity.
Nevertheless, one indication of localization of function has been ob- There is an cnormous literature describing a wide variety of event
r-clatccl pr<ltc'r-rtials, ancl this tliscussion will concentrate only on a fcw of
tained by anatyzing EEG waves from the two sides of the human brain.
While the electrical signals are present over both cerebral cortices, thcrc thc t'tl<lrc clcar-cttt typci which provirlc significant ..rgg.rtions about
are small quanritative differences when the subject engages in thinkirrg
tltc occttt'rctlcc ol'const'i()us rlrirrkirrg. l)oirchirr ct al.-[e83), picton
about different types of subject matter. Verbal problctns, stlclt as sclcct- ruttl Strr.ss (l9tl4). Srrrss. t'itron..rrrtl ocrr-i (1986) antl S<>mmcir, Marr,
ing synonyms fi<>m a scrics of w<>rtls, prtltlttcc sliglrrlt' l:rrgcr lx)tctlti:lls .rntl Lctttlloltl 1l()()0) lt.tvt'r('\'r('\\'('(l tlrc cvitlt.rrt't.r'cl:rtirrg tlrcsc p()tc.-
150 Chnpter Scven Pbysi.ohgr.cal Indices ofThinhing 15l

tials to human consciousness. The whole subject has been reviewed in count the number of times the rare stimuli were heard. In all cases there
two articles by Verleger (1988) and Donchin and Coles (1988) in the were prominent P300 potentials, but the rare stimuli elicited, on the
journal Beha.yioral nnd. Brnin Sciences, which also publishes nlunerous average, larger ones with longer latency. The difference in latency was
coffrrnents by other interested scientists and resPonses to these com- greater when the subject's task concerned semantic meanings. It takes
menrs by the authors. Almost all of the papers and discussion of event the brain longer to deal with the problem of deciding whether the
related potentials has been concentrated on those recorded from human sound was a word synonymous with "prod" or rhyming with "cake"
brains, in a few experiments quite similar potentials have been re- than to simply distinguish benveen the corrunon and the less common
corded from the brains of laboratory animals, primarily cats and mon- of two words.
keys. To appreciate the significance of the latter potentials, it is neces- Cautious neurophysiologists tend to limit their interpretations of
rriy to r.rri.* briefly the data from human subjects that point toward a such data to the conclusion that a substantial portion of the brain is
correlation between ERPs and conscious thinking. active when responding to these stimuli and that the summated electri-
From a wide variety of components of ER?s, much of the experi- cal effects or their time course differ when the response is more compli-
mental attention, and the most interesting implications, come from cated. This is, at least, a significant opening, a sort of entering wedge
what is usually called the P300 wave. This is a positive Potential occur- that might lead to more detailed and significant analyses. It is therefore
ring about 300 milliseconds after a stimulus. Actually it lasts in many pertinent to inquire whether animal brains show comparable potentials.
.mEr 100-200 msec and the Peak varies somewhat, but is ordinarily in The answer is that those of cats and monkeys certainly do, although the
the range of 300-400 msec. The defining characteristic of the P300 detailed form of the ERPs may differ from the human P300 waves to
wave is not so much its electrical or temporal properties as its relation- some extent. Wilder, Farley, and Starr (1981), Buchwald and Squires
ship to at least simple types of cognition. (1982), and Harrison, Buchwald, ffid Kaga (1986) have recorded
One of the mosr widespread experiments suggesting this relationship evoked potentials from cats which were very similar to the human
involves presenting a long series of uniform stimuli, usually sounds, one P300. These electrical responses were prominent, however, only after
of which- is occasionally omitted. P300 waves occur after all of these either the brief tone or light flash had been associated with the delivery
sounds, but the one following the omission of an expectable signal is of an electrical shock to the cat's tail. In other words, the stimulus did
often as large or larger than those following actual stimulation. Since not produce a significant P300 initially, but did so after the cat had been
there *"r tto stimulus at all preceding the P300 waves for an omitted conditioned that it signaled an unpleasant event. In one experiment a
stimulus, these waves must reflect some sort of activity in the brain re- cat learned that a light flickering at7.7 times per second signaled that it
lated to the general paftern that had been established by the repeated would receive an electrical shock turless it made a simple response, but
stimuli. A somewhar similar experiment is to present a train of stimuli that 3.I flashes per second meant it could obtain food. The ERPs in-
including two types, one much more colrunon than the other. The rela- creased in amplitude and changed their waveform after the cat had
tively rare stimulus has come to be called the "oddball" stimulus. Under learned what to expect.
many conditions all stimuli produce P300 waves, but the oddball stim- In a similar experiment with monkeys (Ma,caca fascicalaris), two
uli generate larger ones) as reviewed by Galambos and Hillyard (f 98I). tones of 500 and 4,000 Hz were presented, the latter occurring less
Mor. closely related to possible thinking is a variation on this exPer- often than the former. The rare stimulus was accompanied by * electric
iment in which the common and rare sdmuli differ in semantic mean- shock. After the monkey learned that the rare tone would be followed
ing. In one intriguing experiment of this type the subject heard the spo- by a shock, its brain showed a clear P300 wave in response to it but not
ken name David 80 percent of the time and Nancy in the remaining 20 to the other sound. Neville and Foote (1984), Glover et al. (1986) and
percent (Donchin tlStl. Inanother experiment 80 percent of thc l'irrccla ct al. (1988) showed that in squirrel monkeys (Sairniri sciures)
narnes were masculine and 20 percent feminine. In still another varia- rrn <xlclt'rall t<lnc clicitcd :r l:rrgcr P300 wavc.
20 percent of thc words rhyme'cl with 'l'hcsc rurtl othcr conrp:tr:tlrlc cxpcrinrcnts showcd that the brains of
tion on this experimental theme
cake and 80 percent did not. In a final cx;rcrintcrrt thc ocltlb:rlls wcrc t':rts :rntl lu<llrkcvs givc k rrrg l.rtt'nt'v lxrsitivc w:tvcs similar to the human
.synonyms of 1'rr<ld and thc othcrs wcrc rtof . 'l'ltt' sttlrict'l's frlsk w:ts ttl I'.3(X) irr thcir t'on't'l.rtiorr u'rtIr tlrt' rxrvt'111, :uttl rrrc:uringfitlncss of thc
152 Chapter Snen Physiologtcallnd.icesofThinhing 153

stimulation. This can be interpreted conservatively as showing onlv that In this sense, P300 can be used to index the occurrence of conscious
meaningful stimuli activate larger numbers of neurons and synapses in processing." Nevertheless, there are exceptions, and the presence of a
both human and animal brains, which is scarcely surprising since the P300 wave does not demonstrate with absolute certainty that the hu-
animals clearly learn to respond appropriatelv to stimuli they have man subject is aware of the stimuli. Verleger (1989) and Donchin and
learned have a particular significance. The behavioristic interpretation Coles (1988) and numerous corrunentators on these rwo papers debate
of these data is simply that the experiments have monitored electrical at length and in almost excruciating detail just what these potentials
activity correlated with information processing, but that this tells us ab- reveal about the activities of the human brain.
solutely nothing about the presence or absence of conscious thinking. Despite such uncertainties, the presence of an electrical potential that
Nevertheless, as the functioning of some animal brains is found to re- correlates with task relevance and the unexpectedness of stimuli is at
semble to a greater degree the comparable functions in human brains, least suggestive evidence that the subject is consciously thinking about
the possibility of conscious awareness certainly does not diminish. It is the meaning of the stimuli. The requirement that stimuli must be re-
therefore appropriate to consider what is known about the relationship peated many times in order to measure ERPs means that only certain
between the human P300 wave and the conscious thinking that can be types of situation can be studied in this way. But it does seem that ERPs
reported by human subjects. from animal brains deserve much more intensive study than has yet
Sommer, Matt, and Leuthold (1990) found that conscious exPecta- been reported. It would be of great interest to arrange experiments in
tions modified the human P300 to some extent, although the subjects which the stimuli had clear semantic meanings or required that animals
were not conscious of most of the factors affecting these event related make important decisions on the basis of information thereby con-
potentials. Donchin et al. (1983) addressed this question directly, ac- veyed. Certain types of ERPs may be necessary though not sufficient for
cepting verbal reports as relevant objective data about the conscious ex- conscious thinking; and their occurrence, magnitude, latency, and cor-
periences of human subjects. While there is a rough correlation between relation with relevance to the animal might provide very helpfirl indica-
the presence of a P300 wave and the subject's awareness of the stimulus, tions of the likelihood that it was indeed thinking consciously about the
the two do not always occur together. Some P300 waves have been re- information conveyed by the experimental stimuli.
corded following stimuli that the subjects did not consciously notice, The reluctance of behavioral scientists to become enmeshed in the
and the absence of P300 waves has been recorded following stimuli the complicated problems of consciousness may have discouraged attempts
subjects did notice. Given the complications of recording P300 waves to study experimentally the correlation between human conscious
and the numerous other electrical events that often obscure them, the awareness and ERPs recorded from the human scalp. It would seem
occasional mismatch benveen their occurrence and conscious awareness possible to arrange conditions under which human subjects made the
of the stimulus is not altogether surprising. sarne or very similar discriminative responses to stimuli that produce
The general conclusion, after many detailed studies of human P300 ERPs but did so under rwo sorts of conditions, one in which they were
waves) is that they are endogenous in the sense that they are not direct clearly aware, consciously, of their responses and the other in which they
results of stimulation. They are elicited by stimuli that are unexpected were not. The avoidance of conscious awareness might be achieved
and yet are relevant, stimuli that signal something important, whether through long repetition and overlearning, or by distraction of compet-
leasant or unpleasant, or signals informing the subject of something he ing stimuli. But experiments of this type do not seem to have been car-
or she is expected to do. This has led to the general interpretation that ried out with the care and ingenuity required. Thus we do not yet have
the P300 results from an updating of the internal representation of more than rather general and uncertain correlations between human
some important aspect of the subject's situation. When the process of ERPs and cr>nscious awareness. We should not, however, be discour-
updating is more complex, there tends to be an increase in the P300 agcd fronr firrthcr cx1'rcrinrcntal investigation of ERPs from animal
latency, but this is not invariable. Donchin et al. (1983, I l2) concluded tlrlins whcn rhc :urinrrrls :rrc cngrrgcd in cliscriminations that are impor-
that "a consideration of the circumstances in which thc P300 c()lllP()- tilnt t() thcrrr rrrrtl th.rt rrriglrt pl.rusitrly lrc supposccl to be accompanied
nent is observed suggests that whcncvcr P300 ()ccurs, thc srrtricct is c<ltr- [ry const'iorrs t lrirrkirrg.
sciou.s of thc task-rclcvant inf()rrnatiotr carrictl h1' tltt' t'lit'itilrg stilttttltts.
Cornmunication as Epidence ofThinhing I55
CHAPTER EIGHT cation provides objective, verifiable data on animal feelings and
thoughts are so far-reaching and so significant for cognitive ethology
that they call for thoughtful consideration. Ethologists seldom inquire
whether an animal may want or intend to attack, or whether another
C oruq,%l,un icntiovl, a,s may fcar injury. But if we recognize that such basic subjective feelings
and thoughts may occur in animals) we can often make much better,

Eyidence of Thinking and more parsimonious, sense out of their behavior. Russell (1935) in a
thoughtful discussion of the basic challenges of investigating animal
mentality concluded that "perception or imagery which does not issue
in action must remain unknown to us, unless of course the subject can
in some way communicate such perceptions and images to us." This is
t is much more effective for one animal to anticipate another's just what communicative behavior may sometimes do. Yet psycholo-
actions than to wait until they are underway. This is especially obvious gists have paid little attention to the communicative behavior of ani-
in the case of aggressive encounters. When a dominant animal signals mals, for reasons that are not entirely clear. Could this lack of interest
its intention to attack it is much better for a subordinate to perceive this stem from the pervasive inhibitions of behaviorism for the very reason
as a threat than to wait until it is actually injured. For threats can be that communication does suggest thinkingf
dealt with in several ways, including retreat, counterthreats that may One reason that has discouraged ethologists from using the commu-
deter the attack, or submissive behavior. Insofar as animals ever experi- nicative behavior of animals as a source of evidence about their feelings
ence conscious thoughts and feelings, these are very likely to accomPany and thoughts is a conviction that all animal communication is a direct
social behavior and interactions betrveen predators and prey. Many, if result of internal physiological states that are not under any sort of con-
not most interactions between animals may well involve at least simple scious control. Animal communication is thus held to be comparable to
feelings and thoughts about the situation. If so, other animals with human eye blinks, blushing, gasps of surprise, or groans of pain. These
which signals are exchanged will benefit by correcdy understanding do of course serve to coffIrnunicate to others the state of irritation of the
what the communicator feels or wants, as emphasized by Krebs and eye, embarrassment, surprise, or pain. But they are not intentional sig-
Dawkins (1984). Communication is often a two-way Process, a re- naling employed for some perceived purpose. I have called this general
peated exchange of signals by which two or more animals can perhaps view of animal communication the "groans of pain" or GOP interpre-
ivaluate each other's feelings and thoughts as well as their likelihood of tation (Griffin 1985). A related view is that threats are not signals that
behaving in various ways. an animal wants or intends to attack but predictive information that
Animal communication can therefore provide a usefi.rl and signfficant leads to an appropriate response on the part of the animal that is threat-
'fuindow" on animal minds, that is, a source of objective evidence ened. This viewpoint considers animals to be simple-minded "behavior-
about the thoughts and feelings that have previously seemed so inacces- ists" who care onlv about what other animals do. On the other hand,
sible to scientific investigation. Experimental playbacks of communica- insofar as conscious thoughts and subjective feelings affect subsequent
tive signals are of crucial importance because they allow a limited but behavior, it must be more efficient for both sender and receiver to rec-
revealing sort of panicipatory dialog between animal and scientist. ognize them by means of communicative signals that report them.
Sounds are the most easily simulated signals, but other sensory channels How can we hope to tell whether a given sort of communicative be-
can also be employed in playback experiments provided only that tech- havior does or docs not fhll into this GOP categoryf One impoftanr
nical means are available to reproduce the animal signal with adequate inc'licati<ln is thc cftr'ct of rrrr :tudicncc. Since GOPs are assruned to de-
fidelity. This has even been effective with electric fish, which use weak pcnd tlircctly ()n s()n)c irttt'r'nrtl plrysiol<lgical statc, it should not matter
electric signals not only for orientation but in social and predator-Prey wltctlrcr rutv otltcr':utirn:rl is Pr'1'51'111. Iivclids lrlink when the cornea is
interactions (Bullock and Heiligenberg I986; Kranrcr 1990). irrit:ttctl rt'g.tt'tllt'ss rtl .ltt\' .lttrltt'lttt'. llrrt lltt'cotttttttuticltivc signals of
The implications of this gcncral prop<lsitiotr tlt,tt .trtittt:tl t'<xttttrttni- ttllltlV soti;tl .tttittt.tls.ttt'ollt'lt rlt'Pt'11rk'ttl ott lltt'l)t-cscncc <tf'othcr ani-

156 Chapter Eight Cornrnwnicntion as Epid.ence ofTbinhing I57
mals, and they are often modified in response to communicative signals Although it is clearly advantageous for vervet alarm calls to convev
received from others, as discussed below. The important basic point is the information that one of the three rypes of predator had been
that reasonable and appropriate interpretation of communicative sig- sighted, many scientists did not accept the differences in the alarm calls
nals exchanged by animals may provide significant though not conclu- as proof that an animal can convey semantic information about the na-
sive evidence about their thoughts and feelings. Analysis of this evi- ture of the danger rather than merely its state of fear or arousal. For
dence can) at the very least, provide an entering wedge into what has example, Montagna (1976) stated, "With one cry, the monkeys take to
previously been held to be inaccessible territory beyond the reach of the ground; with another, they climb trees; but in neither case do they
scientifi c investigation. know what predator they are escaping from." Vervet monkeys are ordi-
narily close to each other, and their first response to an alarm call is to
look at the caller. Like many other animals they are adept at judging the
Semantic Alarm Calls direction in which a companion is looking, so that they can usually see
One of the clearest examples of narural animal communication that sug- for themselves what has caused the alarm and respond appropriately.
gests conscious thinking stems from studies of the alarm calls and other Also the caller is likely to flee from the danger quickly, so that the other
vocalizations of vervet monkeys (Cercopitbecws aetltiops). These mon- monkeys might simply do what he is doing. In view of the deep-seated
keys, about the size of a small dog, live both in forests and in open areas conviction that animal communication could not convey semantic in-
of Africa where they can be observed more easily. They spend most of formation, it had seemed more parsimonious to interpret Struhsaker's
their lives in stable groups consisting mosdy of close relatives, who rec- observations as evidence that the three alarm calls conveyed only the
ogntze each other as individuals. When they see dangerous predators degree of fear, or that they were a scale of intensity rather than having
they emit at least three types of alarm call, originally described by specific meanings about the nature of the threat. Yet the three calls vary
Struhsake r (1967). One type is elicited by the sight of a leopard or other in intensity with the degree of the caller's arousal, so that this interpre-
large carnivorous mamnal. One of the few flying predators that preys tation seemed somewhat strained.
on vervets, the martial eagle, calls forth an acoustically quite different Carefully controlled experiments by Robert Seyfarth, Dorothy Che-
alarm call. And when the monkeys see a python they give a third call ney Seyfarth, and Peter Marler (1980) resolved this uncertainty. The
that is clearly different from the other rwo. first step was to become so thoroughly familiar with groups of vervets
This differentiation of alarm calls according to the type of danger living under natural conditions in East Africa that all individuals could
leads to clearly distinct responses. The immediate response to the leop- be recognized. The next was to habituate the monkeys to the presence
ard alarm call is to climb into a tree; and since leopards are good climb- of human observers and their recording equipment. Then they played
ers, monkeys can best escape from them by climbing out onto the small- back alarm calls that had previously been tape recorded when a member
est branches. But this would make them vulnerable to a martial eagle, of the group had first seen a predator. M*y precautions were necessary
and the response to eagle alarm calls is to move into thick vegetation to obtain convincing data. The monkeys might well respond abnor-
close to a tree trunk or at ground level where they would not be at all mally, if at all, to playbacks of a known companion's alarm calls when he
safe from a leopard. In response to the snake alarm call, the vervets was in plain view and obviously not frightened. Therefore the loud-
simply stand on their hind legs and look around at the ground. Once speaker had to be concealed in vegetation, and since monkeys recognize
they can see a snake they can easily mn away from it, although pythons the calls of individual group members, playbacks were attempted only
do take vervets by surprise. Thus the best ways to escape from the three when the monkey whose calls were to be reproduced had just moved
principal predators of these monkeys are murually exclusive, and it is out of sight of his companions into the general vicinity of the concealed
very important that the alarm calls inform other members of the group speaker, r.l,hcn the nr<lnkevs were not actively engaged in other behavior,
wbich danger threatens. A generalized escape response would be ineffi- atrtl u,hctr thcy wcrc rx)t rcacting to real dangers. Their behavior before,
cient; there is no need wasting time climbing into a tree if thc danger is tlttriltg, :tltcl alicr- thc pl:r1,[r:rcks w:'ts rcc<>rclccl by means of motion pic-
from a python, and mistaking a martial eagle f<rr a lc<11'rrrr(l ()r vicc vcrs:r turcs, .uttl tltc t'r'.tlrr.rliort ol'r't'spr)nscs wlls rnaclc ['ly <>bservers who
could casily causc thc nronkcys t() d<l itrst thc wron11 tlrirrg. vicrt'crl t ltt' liltns rvtl lt, rttl kttorvilt1,. tt'lt.tt t':rll lr:rtl lrcclt Pllyctl.
I58 Cbapter Eight Comrnunication as Eyidrnce ofThinhing 159

These playbacks elicited the appropriate responses in most cases. The played." They therefore selected recordings of grunts emitted in five dif-
vervets climbed into trees on hearing playbacks of leopard alarm calls, ferent social contexts, using only cases when they had been able to re-
and dove into thick bushes in response to the eagle alarm calls. Play- cord all the interactions that preceded and followed the vocalization.
backs of the snake alarm call caused them to stand on their hind legs and Only grunts of each type that were similar in duration and amplitude
look all around for a nonexistent snake. Somewhat similar results have were used for playbacks, and grunts that were responses to other grunts
been reported for lemurs by Macedonia (1990) and Pereira and Mace- were excluded. Numerous playbacks were made of grunts to a dominant
donia (I99I). Yet many inclusive behaviorists remain reluctant to ac- male, to a dominant female, to subordinate females, to a monkey mov-
cept the straightforward interpretation that these three types of alarm ing into an open area) and to another group of vervet monkeys.
call convey information about the type of predator the caller has seen. The monkeys showed some revealing differences in their responses
One alternative is that the alarm calls are injunctions rather than state- to these playbacks of gmnts. One of the clearest differences was that
ments about the kind of danger. The leopard alarm calls might mean grunts directed at dominants caused none of twelve monkeys hearing
something like "Go climb a treel'the snake alarm call "Stand up and the playback to move away from the loudspeaker; they apparently con-
look around," and so forth. Even this somewhat strained interpretation veyed an appeasing rather than a threatening message. But gmnts to
recognizes that the calls are more than expressions of arousal. Their subordinants produced movements away from the speaker in five out of
meaning might be what to do, rather than what danger threatens, but twelve cases. The venets spent more time looking towards the speaker
such injunctions are also semantic messages. after playbacks of grunts to dominants than grunts emitted on seeing a
Vervet monkeys emit many other types of sounds during their social monkey move into the open, and there were similar quantitative differ-
interactions. Cheney and Seyfarth (1982) have analyzed by experimen- ences between some of the other types of grunts used in these experi-
tal playbacks, comparable to their studies of alarm calls, the "low- ments. Although these experiments do not indicate just what meaning
pitched, pulsatile grunt, originally described by Stmhsaker (L967) . . . the grunts conveyed, they do show that they were not interchangeable.
given in a variety of social contexts." To human listeners these gmnts As summarrzed by Sefanh (f 984), "When a monkey hears a grunt, he
seem rather nondescript sounds, and like many other animal sounds is immediately informed of many of the fine details of the social behav-
they were commonly interpreted as a graded series conveying only some ior going on, even though he may be out of sight of the vocalizer, and
emotional state of arousal. Close analysis of their acoustic properties even though the vocalizer himself may not be involved."
showed very slight differences that could be distinguished by human In other recent investigations Seyfarth (1987) *d Cheney and Sey-
listeners only after considerable practice. When different responses to fanh (1990) used selective habituation of responses to repeated play-
grunts were observed, it had been customary to assume that this was backs of vervet calls to learn something of their meaning to the monkeys
due to differences in the situation or context in which an essentially themselves. They concenffated on three calls given only in the presence
unitary type of sound was emitted. Cheney and Sefanh suspected, of another group of vervets: a gnrnt, a chutter, and a call designatednryz
however, that subtle differences alnong the grunts might be recognized Playbacks of any of them caused the monkeys to orient towards the sig-
by the monkeys as conveying different meanings. Unlike predator alarm naler and to look in the same direction as the signaler. When such play-
calls, gnrnts did not elicit any vigorous responses from other vervets, backs were repeated in the absence of another group, the duration of
except that they often looked at the companion who grunted. these responses gradually diminished. After such habituation had oc-
In planning their experiments, Cheney and Seyfanh reasoned that "if curred to repeated playbacks of the wrr of a particular monkey, not only
the grunts were really one vocalization whose meaning was largely de- his utr"t's but also his intergroup chutters elicited a much weaker re-
termined by context, subjects should show no consistent differences in sporlsc. Yet when thc same experiment was repeated using the nws or
response to the calls. Instead, resPonses to playback should be a func- chuttcrs of arr<>thcr rnonkcy, this clicited a normal intensity of response.
tion of the variable contexts in which they were presented. On the other In orhcr rvortls thc nronkcvs tcndccl to ignore both the type of inter-
hand, if each of these gmnts was different, and if each carriecl a specific gr()u[) r,oc:rliz,:rtion th.rl lr:rrl lrt'crt rcpc:rtctl witl'rout the presence of an-
meaning, we should expect consistent differcnccs itt rcsp()nscs t<> clch otlrt'r' gr'( )ul), :urtl t lrr' .r,, oust i. .tllv tlilli'r't'rrt sotutcl trsccl by thc same mon-
grunt typcr rcgarc'llcss <>f thc varying circtrnrstrutt'cs itt n,ltit'lt tltc1, 1v.t-. kc1, 11,,, lrrt'srnrr.rlrly ton\'('\'('(l tltr'',.trttt'()r';l sirrrillrr nrclurirtg. Thtrs thc
f60 Chapter Eight Cornrnunication as Evidance ofTbinhing 16I

habituation was specific to the individual caller, regardless of the cate- nated as noisy, arched, tonal, pulsed, and undulating screarns. The noisy
gory of call used by that animal. The vervets seemed to recognize that if screarns had a broad frequency spectmm from about 2 to 5 kllz.
one type of intergroup call by a given companion had proved inappro- Arched screarns had narrow frequency bands which rose and fell one or
priate, his other intergroup calls also deserved less attention. On the more times. Tonal screarns had a wavering but gradually descending fre-
other hand, when the same experiment was repeated with alarm calls quency from about 5 or 6 to 2 or 3 kLIz. Pulsed screarns were similar to
elicited by leopards or martial eagles the result was significantly differ- noisy screarns but broken up into pulses each lasting only about 0.1
ent. Although the vervets did habituate to the groundless leopard alarm second. Finally, the undulating screarns consisted of a series of four or
calls of a particular companion, played back from a tape recorder, they five harmonics which wavered up and down several times during a du-
still responded to playbacks of the eagle alarm calls of that individual. It ration of roughly 0.7 to L.2 seconds. Although these screarns varied
seems likely that predator alarm calls are such serious matters that the considerably in detail, these five categories could easily be distinguished
monkeys cannot afficrd to ignore them even when the caller has previ- by human listeners.
ously "cried wolf " about a different type of danger. These screarns tended strongly to be used selectively toward different
categories of opponent. With some exceptions, noisy screarns were di-
rected at higher-ranking adversaries when there was physical contact-
Semantic Screams
including biting. Arched screarns were given almost exclusively to
Another type of semantic information conveyed by animal calls is the lower-ranking opponents when no physical contact was taking place.
social relationship between the caller and another member of the group Both tonal and pulsed screams tended to be given more often to rela-
to which he belongs. This has been most clearly demonstrated in rtodi.i tives of the caller, while undulating screams were directed almost en-
of the free-ranging rhesus macaques (Atlatncn rnwlntta) that have been tirely to higher-ranking opponents when no physical contact was in-
studied for many years on Cayo Santiago Island offPuerto Rico. When volved. Thus the screams contained information about the severity of
these and other monkeys engage in aggressive encounters, they often the encounter and the social status of the opponent.
call loudly, and this calling sometimes serves to enlist the aid of others The mothers of callers also responded differendy to these screarns, as
against the antagonist. Gouzoules, Gouzoules, and Marler (1984) se- demonstrated by playbacks of tape recordings. The basic procedures
lected a well-studied group of these monkeys for detailed studies of the employed in these playback experiments were the same as those used by
screarns given by immature males when exchanging threats or fighting Seyfarth, Cheney, and Marler in the experiments with vervet monkey
with other members of the group. These monkeys could all be recog- alarm calls. The first response of the mothers was to look towards the
nized individually, and both their maternal ancestry and social status concealed loudspeaker; they did so for I00 percent of the noisy screarns
was known from extensive previous studies. It was thus possible to dis- given to higher-ranking opponents with physical contact, but less con-
tinguish whether a young male was interacting with a close relative or sistently in response to the other types. The duration of their gaze to-
not, and whether his opponent was higher or lower in dominance rank. wards the speaker was much longer for noisy and arched screams than
The screams of these young males often brought the screamer's mother for tonal and pulsed screams, and they reacted more quickly to these
to his aid. types than to the others. The responses of mothers to screarns that were
M*y previous studies of monkeys'calls had indicated that they var- repeated for several seconds included threat displays and charging from
ied continuously in their acoustic properties. This has been interpreted a considerable distance uttering loud calls of their own.
as a fundamental difference between monkey calls and human lan- In other cxperiments the sarne investigators found that mothers re-
uage, because the latter consists of discrete words while animal calls spond m()rc strongly to th<: screarns of their own sons than to those of
have been viewed as merely emotional signals devoid of any meaning <>thcr y()ung nralcs ((iorrzoules, Gouzoules, and Marler 1986). Similar
except to convey the state of arousal of the caller. It was therefore a sturlics <rf rr largc gr()rrl) ol'captivc pigtail macaques (Macncanernestrinn)
surprise to find that 90 percent of 56I recordings of thc agonistic by (iotrzotrlcs:urtl (iouzorrlcs (l9tt9) sh<>wcd that in this species differ-
screams of these juvenilc malcs fbll into orrc of tivc rlistirtct c:rtcgorics. cnt tvlx's ol'st'r'r'.urrs \\'('r.(' t'rnittt'tl wlrcn fightirrg or thrcatcning oppo-
On thc basis <lf s<lurrcl s[)cctr()gr:ulrs thcsc fivt' t:rtt'1,,orit's rvcrt' tlcsig- ncnls ol'tlilli'r't'nt s(x i.rl r.lrrk. llttt st'r't':utts ol'pigtrril tl)rlcll('lLrcs c'licl not
162 Chapter Eight Cornrnunication as Eyidence ofThinhing 163

seem to differ according to matrilineal relatedness, as they did with rhe- tam cockerel lived for long periods in a large outdoor cage. Models of
sus monkeys. hawks were presented by pulling them along overhead wires, much as
The results of these investigations show that the screarns of these Lorenz and Tinbergen had done in their classic studies of avian re-
monkeys, unlike groans of pain, convey considerable information about sponses to hawk-like patterns. Under these conditions the cockerels
the caller's situation, information that affected their mothers' behavior. emitted 509 aerial alarm calls in 400 presentations of moving hawk
It seems likely that the monkeys think about these highly emotional models, but no ground alarm calls at all (Marler, Dufty, and Pickert
situations in simple terms of the degree of threat and danger and the 1986a, 1986b; Gyger, Marler, and Picke rt 1987; Karakashian, Gyger,
social relationships of the opponent or, in the case of the mother, of and Marler 1988; and Marler, Karakashian, and Gyger 199I). The
their offspring's situation. cockerels gave significandy fewer aerial alarm calls when alone than
when their mate or another familiar female was clearly visible and au-
Audience Effects dible in an adjacent cage; but when this experiment was repeated with
unfamiliar females the male called no more often than when he was
As mentioned above, one way in which ethologists might be able to alone. Familiar males elicited almost as many alarm calls as familiar fe-
distinguish communicative signals that do or do not fall into the males. Young chicks were almost as effective an audience as familiar fe-
"groans of pain" category is to study the effect of an audience on the males in eliciting alarm calls, but the presence of bobwhite quail did not
production of communicative signals. Marler and his colleagues have increase the frequency of alarm calling. Evans and Marler (199I) have
been aftempting to do this with the calls emitted by domestic chickens. recently refined these experiments by showing that video tapes with
Chickens emit a wide variety of calls, as described by Collias and )oos sound tracks have the sarne effects as live birds. This allows improved
(1953) and Collias (1987), ffid they are of course convenient animals experiments in which possibly confounding effects, such as variation in
to study. Marler and his colleagues concentrated on two types of call activity of the quail and chicken could be experimentally controlled.
given by adult males of a small strain, the golden Sebright bantam, that Cockerels also give other calls when food becomes available, and in
seems to be quite similar to the ancestral jungle fowl from which do- the experiments they called more when presented with preferred foods
mestic chickens derived. Because some of the most interesting calls are such as mealworms or peas than for peanuts or inedible nutshells. Fe-
rather faint, they were recorded by temporarily attaching to a cockerel's males approached males giving these food calls more than noncalling
back a 2 x 2.5 x 5 cm radio microphone weighing 16 grams. The males, and they were more likely to approach a male calling about a
birds became accustomed to wearing these instruments and their behav- preferred food. Males also called more when hens were present, ffid
ior did not seem to be appreciably altered by them. hardly at all when another adult male was in the adjacent cage. This is
Chickens, like several other species of birds, have two types of alarm doubtless related to the fact that courting cockerels often bring food to
calls, a series of short, narrow band whistles commonly given when they females in which they are interested. The amount of food calling by the
see aerial predators such as hawks, and a pulsed broad-band cackle elic- males also varied with the nature of the conspecific audience. When no
ited by ground predators such as dogs or foxes. But the type of danger other chickens were present, males gave food calls 13 out of 18 times
is not the only factor affecting which call is produced, so that they are tl'rat mealworms were presented, ffid only once in 18 presentations of
not a highly specific form of signal. The so-called ground predator call incdible nutshells. When another male was present, they gave no food
is also given to hawks at close quarters, and the aerial alarm call is often calls at all for either mealworms or nutshells, although they ate 15 of the
given to small and harmless birds or other objects seen against the sky. Iti mcalworms. When either familiar or unfamiliar females were pres-
Yet despite much variability and many calls given when the observers cnt, thc cockcrcls ncvcr atc thc nrcalworms and gave food calls in 35 of
could detect no danger or other appropriate stimulus, there is neverthe- 36 prcscntrrtions. 'l'lrtrs tltc prcscrtcc and narure of an audience had a
less a strong tendency for the aerial alarm calls to be given for hawk-like rttrtrkctl cllL'ct ort lirotl r':rllirrg.
objects seen in the sky and the ground predator alarm crrll for moving It is sigriilit':rrrt tlr:rl llrt'st' .rrrtlit'rrt't' clli'ctsi irrc clilll'rent for food calls
objects at ground level. :uttl llrrrrtt t':tlls. Alrttost .rs nl.urt'.tl.trnr t;tlls u,t'r-c givcn in the presence
Marlcr and his c<>llcrrgtrcs :rrrangctl cortditi<ltrs irr u'lrit lt .r singlc lrlrt- ol'llrrrrili.u'nt.tlt's.ts l.tttttlt.tt lcttt.tk's, lrttt rto lixrtl t'.tlls ltt lrll wcrc givcn
L64 Cbapter Eight Cornrnunicntion as Evid.ence ofThinhing 165

to males. Although Marler et al. are cautious about interpreting these sionally a honeyguide has been reported attempting to lead a mon-
data, and carefully consider other factors that might cauie tnJain'er- goose, monkey, or baboon; but only baboons have been observed to
ences they observed, their experiments cerrainly support the hypothesis follow the bird. Most of the detailed observations of the guiding behav-
that cockerels are appropriately selective about their use of both alarm ior have involved human cooperators, and several recent students of
calls and food calls according to the nature of their audience . To be sure, honeyguides suspect that they never cooperated with ratels and that the
other considerations such as the whole context in which communica- idea they did so arose because the nocturnal ratels were seen feeding on
tion takes place are also important in interpreting these experiments, as honeycomb after it had been exposed by human honey gatherers.
discussed in detail by Smith (I99I). But, at the very least, the experi- Friedmann believed that the guiding habit had decreased markedly
ments demonstrate that as more is learned about communicative behav- from earlier years as European ways of life have provided more easily
ior of animals, it becomes increasingly difficult to fit such behavior into obtained sources of sugar than the opening of wild bees'nests. He also
the procrustian bed of GOPs. suspected that ratels had become more nocturnal, under increased hu-
man hunting pressure, so that honeyguides had less opportunity to ob-
tain wax by this type of cooperative behavior. The guiding behavior
seems always to have been limited to certain areas within the honey-
An intriguing type of foraging that suggesrs intentional planning and guide's range, so that it is far from being a rigidly fixed behavior pattern.
communication of simple thoughts is the guiding behavior of the Afri- Regardless of this question, there is no doubt that, in many areas of
can greater honeyguide (Ind.icator ind.icator). These birds feed on insects Africa, honeyguides lead human searchers for bees'nests to their loca-
but are also fond of the wax from honeycombs, and they are able to tion, and that after the honey gatherer has opened the nest the birds
digest beeswax. They cannot open bee nesrs, but in an apparent efficrt profit by obtaining honeycomb.
to obtain wax and honey they cooperate with men or perhaps animals As Friedmann (1955, 32-33,39-4L) describes typical guiding be-
that tear open bee nests to take honey, leaving a considerable amount of havior:
honeycomb available to rhe honeyguides. The several species of honey-
guides and their behavior were srudied intensively by the ornithologist When the bird is ready to begin guiding it either comes to a person and starts a
repetitive series of churring notes or it stays where it is and begins calling these
Herbert Friedmann and described in his 1955 monograph. His analysis
notes and waits for the human to approach it more closely. . . . If the bird comes
of the cooperative behavior is significant as a classic example of the re-
ro a person to start leading him, it flies about within 15 to 50 feet from him,
ductionistic Zeitgeist that was so prominent in srudies of animal behav- calling constandy, and fanning its tail, displaying the white outer rectrices. If it
ior for many decades and led even the most experienced field naturalists waits for the potential follower to approach it for the trip to begin, it usually
to underestimate the versatility of the animals they studied. More re- perches on a fairly conspicuous branch, churring rapidly, fanning its tail, and
cently Short and Horne (1985) have thoroughly investigated the be- slighdy arching and ruffiing its wings so that at times its yellow "shoulder"
havior and ecology of honeyguides with special emphasis on their roles bands are visible. As the person comes to within 15 to 50 feet from it, the bird
as nest parasites that lay their eggs in the nests of other species. The flies off with an initial conspicuous downward dip, with its lateral rectices
following review of honeyguide behavior is based on Friedmann's widely spread, and then goes off to another tree, not necessarily in sight of the
monograph, substantially supplemented (and in important respects follower, in fact more often out of sight than not. Then it waits there, churring
modified) by the recent work of Short and Horne, and especially that of loudly until the follower again nears it, when the action is repeated. This goes
on until the vicinity of a bees' nest is reached. Here the bird often (usually in
Isack and Reyer (1989) discussed in detail below.
my experience) suddenly ceases calling and perches quietly in a tree nearby . . .
Honeyguides are widely believed to lead the ratel or honey-badger
and thcrc waits . . . until the pcrson has departed with his loot of honeycomb,
(Mellivora capensis) to bees' nests. They also engage in the same sorr of whcn ir conrcs tlown to thc plunclcrcd bees' nest and begins to feed on the bits
cooperative behavior with people, and in some areas African natives of corrrtr lclt strcrt,rt ;ql'rout. . . .
seek out honeyguides to obtain honey from rhc ncsrs of wikl bccs. (irritlinli nr.l\,('()\'('r'il tlrrr.tfiort ol'liorn rr fl'w scconds to half an hour, or
Some,, according to Fricdn'rar"u1, imitatc thc gnrntirrg sorurrls ol'mtcls, p<lssiblt,('\,('ll .ln lrorrr. ,rrrrl rtr.tv ittr',rlvt'rt tlistrurcc ol'fiont I fl'w fcct to ovcr half
or ch<lp ()n trccs t<l sinrulatc thc sorrntl of-<11'rclrilr1,,.r lrt.r.s'rrt.st. ()t-cl- .r lnilt',.rrrtl lx,ssrlrl\', .rl tllrr('\, ('\'('n .r nrik'. . . . (itrirlilrg lc.ttls to thc vicinity of a
166 Chapter Eight Coynrnunication as Eyidence oJ'Thinhing L67
bees'nest, not to the exact spot. . . . If a person does not'follow a honey-guide episode as evidence that the honeyguides were not leading intentionally
that has apparendy come ro "lead" him, the bird may increase the tempi and
to a bees' nest whose location they knew beforehand:
excitement of its behavior as if to urge and entice, or it may give up easily and
leave. . . . A would-be_ "guidirrd'birimay sometimes follow ip.rron fo. a u.ry
Captain Davison . . . had a group of his natives at one of the rest camps in the
long distance (five miles is the maximum known to me) or foia very consider- Reserve when a honeyguide came to them and chattered and went through all
able period of time (half an hour is the maximum I know ofl) to aftempt ro ger
the motions of trying to get them to follow it. Davison refused to let any of his
him to follow it.
boys go, but got them all on a truck and drove off to the next camp some five
Recent students of honeyguide behavior have reported somewhar dif- miles away. The bird followed them all the way and then Davison told one of
ferent patterns, and these may well vary from plice to place and from the natives to get an axe and follow the bird. The honey-guide "led" this native
time to time. But there is no doubt that the birds exerr considerable to a bees'nest less than half a mile from the second camp, but which must have
been at leasr 4Vz miles from where the bird first began calling to them. (59)
r, in amemprs to anract the anention of people, rhat they do fly with
to the vicinity of bees' .rests, and that if someone opens Elsewhere in his 1955 monograph, and especially in later reviews of
the nest they do ear honeycomb. the same material, Friedmann claimed that these observations prwe that
After describing this cooperative behavior in some detail Friedmann the guiding behavior is carried out without conscious intention on the
oPens a section of his monograph (5a-64) tided "Behavioristic level of bird's part. For instance: "It is now known that this guiding behavior,
the habit''as follows: which looks so purposive, is actually a form of excitement reaction on
Use of the term "guiding," with respect to the behavior pattern that usually the part of the bird when meeting a potential foraging symbiont, md
resuls in the follower arriving at a bees'nest, is unfornrnati in that it implies a that the excitement dies down when the bird, with its symbiont near at 1

preexisting PurPose or plan on the part of the bird, an intelligent activiry far hand, sees or hears swarming bees" (Friedmann and Kern 1956, 19).
beyon{ the psychological capacity of any bird. . . . The word pidi.,g" has a His 1955 monograph includes the statement: "The releasers of the in-
purposive connotation which is applicable to the species but not to *y of its stinctive behavior constituting 'guiding' are the sight or sounds of
members. . . . There are several features of "guiding" which further indicate its ratels, baboons, and humans (away from villages). The stimulus which
:Tr:gtyPed nature. One is the fact that guiding is ordinarily not direct. The apparendy brings these actions to a halt is the sight or sound of bees"
bj$ frg9uendy leads in a most erratic course, often actually going a consider- (p. 59). And, later: "There is no occasion whatever to assume anything
able distance beyond a bees' nest and then coming back to it. . . . tr griai.,g
involving planning or intelligence on the bird's part. The behavior is
were PurPosive in the individud this would be difficult indeed to explain, espe-
cially since there were no obstacles or barriers such as hills, ravin.r, .i. to be 6y- wholly on an instinctive level, but it is something sought for by the bird,
passed. (54) not merely something it does automatically when the necessary stimuli
are present" (p. I63).
Friedmurn illustrates several very indirect roures taken by honeyguides These statements are representative of the widespread effcrts on the
between the place where the leading began and the beesl nest wf,ere it pan of both Ps),chologists and biologists to account for all animal be-
ended, and he found he could cover the direct distance benveen these havior without allowing any role for conscious thinking or intentional
nvo points in half the time he had taken when following the bird. yet, planning. The observation that honeyguides do not go directly to a
as pointed out by Isack and Reyer (1989), these birds did not move ar bees'nest is important and certainly argues against a detailed and accu-
random, and tended toward the location of the bees'nest, though their rate memory of the most direct route to the goal. But it scarcely proves
approach was indirect. the absence of any conscious intention. One obvious alternative would
Friedmann advanced as another reason for concluding that the guid- be an imperfect memory of where a bees' nest was located, even though
ing is not intentional "tJre fact that on occasions the biid will lead not the bird might recall that there was one in the vicinity. Or the bird might
to a bees'nest but to a dead animal or to a live snake, leopard, rhinoc- wait until it hacl cnlisted a follower and then begin searching for a bees'
eros, etc." One reason for this may be the numerous flic.s or <lrhcr insct.t.s ncst. 'l'lrc .rv;ril:rblc tl:rta rrrc fhr from sufficient to confirm or disconfirm
that-are often present near animals such as thosc ncrrr whit'lr thc lroncv- strch lrypotltt'st's; lrtlt thc inrp6rtant p<lilt is that scientists have been
gtride ceases its lcatlirrg bchavi<lr. Frictlllt:ll'tn :rlso titt's rlrt' lirllowirrg vo'v t;rrir' k to st'izc lrl)( )n .rrrv l.rilrrrc ol-arr lrnirnal tr> pcrft>rrrr with perfect
168 Chapter Eight Cornruwnication as Evid.ence ofTbinhing 169

efficiency and to offer such failure as evidence that it is a totally thought- terested in the guiding." When it has reached the vicinity of a bees'nest
less robot. the bird emits an "indication call" which is softer in tone than the calls
In a truly revolutionary paper Isack and Reyer (1989) describe an during guiding, with longer intervals between successive notes.
intensive field study of the greater honeyguide in norrhern Kenya, ex- Isack and Reyer observed the vicinity of bee nests from "camou-
tending over three years, in an area where honey from the nests of wild flaged observation positions occupied before dawn," and they saw
bees is an important paft of the diet of the Boran people. This is dry honeyguides inspecting the nests, remaining only for about a minute
bush country quite different from the forested areas where Friedmann before flying away. On cloudy and cool mornings when the bees were
had conducted most of his observations of the same species, but the not aggressive, "the bird would fly straight into the entrance of the nest
guiding behavior was very similar to the displays and calls Friedmann and peer into it." Isack and Reyer could not gather data adequate to test
had described. Some of the Boran people are professional specialists in two additional claims of the Boran honey gatherers: "(i) that a bird,
honev gathering, md they rely on honeyguides to a considerable extent. flying lower than the treetops, will guide to a colony close to the
Considering only days when they did find at least one bees'nesr in an ground, and (ii) that when nest distances become very long (about 2
unfamiliar area Isack and Reyer ( 1989) repoft that "their search time km or more), the birds'deceive'the gatherers about the real distance by
per bees'nest was, on the average, 8.9 hours when not guided and 3.2 stopping at shorter intervals. F{owever, having found all the other
hours when guided." Very few of the bees' nests are located where the Boran observations to be true, we see no reason to doubt the statements
unaided birds can reach them, so that the guiding, and following, be- of these excellent'ethologists."'
havior is an effective form of behavioral symbiosis which has important These recent discoveries by Isack and Reyer are most revealing, and
benefits for both participants. The extensive observations of these birds show that Friedmann's interpretations, reached in the heyday of behav-
by Short and Horne (1985) are quite consistent with the behavior de- iorism, clearly failed to do justice to the versatility of which the honey-
scribed and analyzedby Isack and Reyer. guides are capable. The close correlation of the birds' initial directions
The Boran honey gatherers interviewed in their own language by of flight and the straightness of the routes along which the honey gath-
Isack, who is himself a Boran, stated that the guiding behavior of the erers are led, demonstrate clearly that the birds knew the location of the
honeyguides "informs them about the direction of, the distance to, and nest to which they were leading their cooperators. Whether the varia-
their arrival at the colony fof bees]." Isack and Reyer tested this surpris- tions in perch height and length of flights between perching are in-
ing statement by mapping several routes followed by honeyguides while tended to inform the follower is more difficult to ascertain. But even if
guiding the professional honey gatherers. The results clearly confirmed they are not, they provide evidence that the bird is paying attention to
that the starting direction was indeed almost always correct within 20 its memory of the nest location. Behaviorists can translate these obser-
or 30 degrees, *d th" mean direction of all initial flight directions was vations into a series of stimulus-response contingencies, but the result-
within less than one degree of the bearing of the bees' nests to which ing positivistic account becomes more and more unwieldy as more is
they eventually led their human cooperators. As the bird travels toward learned about the details of the birds' actual behavior. To assume a
the bees'nest, three properties of its guiding behavior decrease progres- simple conscious intent to lead the follower to the bees' nest and get
sively: the distance between perches where it lands and waits for the food after he has opened it seems a more parsimonious and reasonable
man to catch up, the height of these perches above the ground, and the interpretation.
duration of periods when the bird flies off toward the bees' nest and
then returns. This period varies between about half a minute and two
minutes, and while it was not possible to follow the birds, it seems likely A Parrot Who Means What He Says
that they fly part or all of the way to their objective and then rerurn ro "Parroting" has bcc<lmc a tcrm for imitation of speech without under-
the man they are guiding. st:rnrlirrg whrrt it nrcrrrr.s. Afiicln gray parrots (Psittacws eritlta.cws) are es-
The human honey gatherers communicatc with thc horrcvgtridcs. ryci:rllv prolit'it'rrt ;rt nrinrit'kirtg ltunrrur spccch, but other parrots, my-
They use a loud whistle to attract thc birrls, rntl as tlrt't, lolkxy thcnr Ir.rh lrirtls. sl.lrlinf,,si,.urtl otlrt'r'sPccics r::ttt:rlsr> mimic words well
"thcv whistlc, bang ort wor>tl, arrtl trrlk lotrtllt,to tlrt'lrir,l t,r kt'r'p it ilr- t'rtouglr tJr.rt tlrt'\'..ur t'.rsrlv lrt'rt't,,p,,niz,t'tl lry ltttttt:ut listctrcrs. Thc cftL'c-
l7O Chapter Eight Cornrnwnication as Evidence ofThinhing l7l
tiveness with which parrots and other mimetic birds can imitate a wide proof boxes, and there periodically heard a tape-recorded word or phrase which
was then followed by a pellet of food. . . . These subjects should have learned to
variety of words, as well as other sounds, has led their owners to teach
reproduce the "conditioned stimulus" (word), that is, to imitate. They did
them whatever comes to mind. The results are often entertaining; but
not. . . . Perhaps we get a clue from the fact that there were rwo or three mynahs
the meanings of the words imitated are mosdy so remote from anything around GrosslighCs laboratory which his assistants had converted into "pets,"
a bird could possibly comprehend as to reinforce the widespread con- and they were all fluent talkers. (1980, 5l-54)
viction that avian mimicry entails no understanding whatever. If it has
not already been done, an African gray parrot could undoubtedly be It is characteristic of the behavioristtc Tr-itgeist of the mid-twentieth
trained to say "Read my lips!" just as one trained by Stevens (1888) century that Mowrer's work has since been cited primarily as evidence
learned to say "Hurrah for Blaine and Logan" during the campaign of that because birds cannot be trained to imitate speech by means of stan-
r884. dard operant conditioning methods, their imitation cannot entail any
Yet some words that parrots learn do have a simple and direct rele- understanding of the meanings conveyed by the words they mimic. This
vance to their situation, as when they learn to ask by name for particular was clearly not what either Mowrer or Grosslight and Zaynor con-
foods. Although this is grudgingly recognized, a sort of simplicity filter cluded. Instead they recognized that interactive exchanges of sounds
has tended strongly to rule out of scientific thinking the notion that a with companions was probably a necessary condition for the develop-
bird might understand that a simple meaning is conveyed by a sound it ment of "talking" i, birds. Ethologists proceeded to study the use of
has learned to imitate. This type of simplicity filter was made to seem complex vocalizations by parrots, Indian Hill mynahs and other birds
more plausible by the failure of several efficrts to train parrots to emit under natural conditions and found that imitation of companions plays
particular sounds in order to obtain a food reward. The most often cited a large role in their social behavior. Young birds pass through a stage
examples of such efficrts are those of Mowrer (1950, I960a, I960b, when they emit varied and imperfect versions of the sounds they will
1980) and Grosslight andZaynor (1967). use as adults, and they seem to enjoy repeating and imitating sounds
It is perhaps no accident that in the I950s when behavioristic learn- they hear around them. The social context, and the responses of other
ing theory was dominant in psychology it was O. H. Mowrer who be- birds are important factors in song learning, as demonstrated for ex-
carne interested in "talking" birds. For he was sufficiently uninhibited ample by West and King (1988) with cowbirds. Females of this species
by behaviorism to write: "If . . . we sometimes speak of 'consciousness' respond to a small subset of male songs with a rapid wing flick, and this
(a tabued word for the behaviorists), this is not just a friendly gesture is apparently recognizedby the males as a sign of readiness for copula-
to the past or concession to cofiunon sense; it represents instead the tion.
growing conviction that the objective study of behavior has now An important advance was made by Todt (1975), who developed an
reached the point where some such concept is essential . . . if conscious- effective training procedure called the modeVrival approach. His proce-
ness were not itself experienced, we would have to invent some such dure was much closer to the natural social exchanges by which birds
equivalent constmct to take its place" (Mowrer 1960,7). learn their vocalizations, although with human companions rather than
Mowrer later (1980) describes how he "acquired a collection of par- other birds. He exposed a mimetic bird such as the African gray Parrot
rots, mynah birds, parakeets, magpies and crows, and set about learning to a cooperative human trainer who talked in the bird's Presence to an-
how to teach them to'talk."'It is not clear ftom his publications to what other person acting as a rival, in effect competing with the parrot for the
extent he actually tried to elicit vocalization by means of operant condi- trainer's attention. Irene Pepperberg (198I) improved this procedure
tioning with food as a reward, but his efficrts were apparendy unsuccess- by having two trainers talk about objects in which their parrot seemed
fuI. For he continues: intcrcstcd, orlc asking for one of these objects, the other giving it to her
or withhokling it eccorrling to the correctness of her verbal requests.
'l'hc trrrincrs cxclrrrngctl rolcs tionr time to time. Using this method she
The only systematic and extensive investigation of this problcnr thus fhr rc-
ported, in so far as I am aware, is that of Grosslight rrntl Zrl\,rror'119(r7). 1'lic strcccctlctl irr tr'.rinirrg .r rrr.rlt' Ali'icrrn gray parrot named Alex to use im-
mynah birds which wcrc usctl as cxpcrinrcnt:rl sul'rjt'r'ts \\'('r('l)ul rrtto sotntl- it.rtions ol'scvt't'.tl lrrrl,,lislr n'ot.tls ilt :tlt :tppropri:rtc fhsl'ri<ln. In his first
L72 Chapter Eight Cornrnwnication as Epidence ofTbinking 173

26 months of training Alex acquired a vocabulary of nine narnes, three and use this understanding to select the correct reply from his vocabu-
color adjectives) two phrases indicating simple shapes, and he carne to lary (Pepperberg 1990, 199I).
use "no" in situations where he was distressed and seemed unwifling These findings consdrute a truly revolutionary advance in our under-
to do what his trainers wanted, or when rejecting something offered to standing of animal mentality, comparable to von Frisch's discovery that
him. honeybees use symbolic gestures to cornrnunicate direction and dis-
Alex has subsequently learned numerous uses of his imitated English tance to their sisters, as discussed below. Because they are such startling
words. V\rhen shown familiar objects and asked "What color)" or "What extensions of what we had previously believed possible for any bird, it
shapef " Alex learned to answer correcdy more than 80 percent of the is very important to consider carefully whether there might be some
time, which is far better than chance because he had to select one of five flaw in these experiments. In short, can we really believe that a parrot
colors or four shapes (Pepperbe rg 1987b). L further experiments he can make such judgments and express them by using words he has
learned to say the numbers 2 to 6 plus the name of the objects when learned to imitatef
presented with sets of two to six familiar things. His overall accuracy in It is unfornrnate that Pepperberg's pioneering work is based on the
these tests was 78.9 percent correct, but more than half of his errors behavior of a single bird. To date no one else has apparently attempted
were responses in which he named the objects correctly but omitted the to replicate Pepperberg's experiments, but she has begun to extend her
number. In such cases the further query "How manyl" produced the experiments to include another parrot. Both steps are highly desirable;
correct response 95 percent of the time (Pepperberg L987a). but pending such essential replication we can inquire as critically as pos-
In other experiments Alex was shown two objects (which might be sible what flaws might have escaped our notice. The first thought of any
either familiar or things he had never seen before) and required to say student of animal behavior is that some sort of inadvertent cuing may
what was the sarne or different about them (Pepperberg L987b, 1988, have taken place, that Alex responded not to the actual properties of the
I99I). They differed in color, shape, or material, and Alex usually gave objects he was shown but to some unrecognized behavior of the trainer
the correct respon5s-((s9l9rr" "shapej' o. "maffer" (which he pro- who presented the objects and asked the questions, something analo-
nounced "mah-mah")-to designate the material of which the object gous to the cuing that explained the apparent ability of Clever Hans to
consisted (paper, wood, cork, or rawhide). His responses to "What's perform feats of mental arithmetic. Such inadvertent signals would have
samef" or "What's different)" were 82-85 percent correct when there to be quite subtle, some gesture that Alex took to mean he should say
were three options-color, shape, or material-so that a chance score "samel' "bluer" "woodr" "noner" or any of the several other words he
would be only 33 percent correct. In further tests of _this general type, had learned.
some pairs were identical, while others were totally different. In the for- Alex was initially quite sensitive to the presence of his familiar train-
mer case Alex learned to respond to the question "\4rhat's differentf" by ers. FIe acted frightened in the presence of strangers, so that to assure
saying "None." When the test objects were very different and Alex was his attention and cooperation his principal trainer, Pepperberg, had to
asked "What's same|" he would also answer "None." His accuracy in be present during critical testing of his discriminatory responses. Dur-
these tasks was about 90 percent. ing all tests, as opposed to training sessions, Pepperberg, who is keenly
In still more recent experiments Alex is shown any collection of ob- aware of the dangers of inadvertent cuing, sat in one corner of the room)
jects and asked any of the following four questions: "What color is Xf" did not look at Alex, and did not know what was presented to him by a
"What shape is Xl" "What object is Yf" or "What object is shape Z|" so-called secondary trainer. The latter was familiar to Alex but had not
where X might be the narne of any of several familiar objects, Y might l'rccn prcscnt when he was trained in the task under investigation. In
be any of seven colors, andZ any of five shapes. He had learned all these othcr worcls, this sccondary trainer was not present when a primary
words and used them correcdy in previous experiments. His accuracy in traincr hrrtl prcscntcd thc tcst objects and trained Alex to say "samef'
responding was about 8I percent. These questions were mixed with "clifli'rcrrt," "n{)nc" or whlrtcvcr wAs the correct response . Thus Alex had
other tests, so that each one was presented only at lrlng intcrvals. Ti> n() ()l)l)()r'rrrnilv to lt'.rnr .utv itt:rtlvcrtcnt cucs that might accompany the
answer correctly Alex had to undcrstand all thc wortls irr thc tprcsti<ln l'rr-csr'nt:rlion ol' r'.rriorrs olrit't'ts ()r ('oIrtbinltiotrs try thc sccondary
174 Cltapter Eight

trainer. If he was responding to some unrecognized cue speci$ring CHAPTER NINE

which of numerous words in his vocabulary he should utter on a given
occasion, it must have been one that any person would exhibit when
showing Alex various objects. This seems highly unlikely, to say the
least. More recently Alex has demonstrated that he can answer correctly Sy*b olic Cornvn uvt icntion,
about 80 percent of questions asked by relative strangers when Pepper-
berg is not present.
Thereforc it seems reasonable to conclude that a parrot can learn
both to understand and to corrununicate about several simple properties
of familiar objects (color, shape, material) as well as such basic relation-
ships as sarne or different. Pepperberg makes no claim that Alex has
learned anything approaching the versatility or complexity of human xploiting newly discovered sources of food is a very comnon
language; but he does seem to have demonstrated some of the basic problem for animals that live in cooperating groups. To consider a
capabilities that underlie it. More important is the strong indication simple example involving the smallest possible group, when insectivo-
that Alex thinks about colors, shapes, sarnenessr and so fonh. To be rous birds are feeding a nesrful of young, they need to locate and cap-
sure, those inclined toward a sleepwalker view of nonhuman animals ture quite large numbers of insects. They are not alone in this search;
may insist that he is an unconscious robot so contrived that he gives the other birds and other insectivorous animals are also busy hunting, and
correct verbal responses. But this insistence must be based on other con- the insects themselves are not exactly cooperative in making themselves
siderations than his ability to use words meaningflrlly. In short, he gives available. When both parents are feeding nestlings, one parent some-
every evidence of meaning what he says. times finds an aggregation of edible insects at some distance from the
nest when the other is less successful. In this situation it would clearly
be advantageous for the former to convey to its mate the location of this
newly discovered source of food. We do not know whether this happens
()r not. It has not been observed, but the types of observation that
rvould be necessary to reveal it are difficult and have not been seriously
undertaken, to the best of my knowledge. One would have to follow
[;oth foraging parents, note when one ofthem was having better success
than the other, see whether they interacted back at the nest, and, if so,
rvhether the less successful parent then flew to the food source discov-
crcd by its mate.
This would be a special case of an "information center" where ani-
rnrrls may learn from their companions where to locate food, as sug-
gcsted by Ward and Zahavi (1973). M*y recent srudies (for example
l{icl'rncr and Marclay I99I) have failed to support the hypothesis that
.rninrals lcarn in this wav about the location of food. Perhaps as etholo-
gists bcgirr to clcvotc nlore attention to animal cognition and inten-
ti<,rrrrl c<lnrrnunicrltion, thc nc:ccssary studies will be carried out and will
rc,u,clrl whctlrcr ()r n()t this sort of-cflicicttt communication about newly
tliscovcr t'tl lixrtl s()ur-('('s tkrcs r)('('ur in lrirtls.
()tlrcr sot'i:rl .utirn:tls t<'r.t.rittlV tkr slrrtrt' irrlirrrrt:rti<ln atxrttt rrcwly dis-
r'ovt'r't'tl lixrtl st)ur'(('s. .rs r('\'r('\\'t'.1 l,\, Ilolltkrtrlct':uttl Wils<ln (1990).

176 Chapter Nine Symbolic Cornrnwnication 177
One of the best examples involves the weaver ants, whose ingenious especially clear-cut. The gestures used in recruiting for fighting re-
cooperative construction of leaf nests was described in chapter 4. Gath- semble in some ways the movements employed in actual combat. This
ering the food needed by -y large colony of ants requires a great deal may be a ritualized imitation of actual fighting, a sort of intentional
of effort on the part of many of the nonreproductive workers. They pantomime. Whether intentional or not, this differential recruitnrent is
often search a relatively wide area and after they have found food return effective, and numerous workers are induced to move rapidly out either
to the nest and recruit many of their sisters to join them in gathering to gather the recendy discovered food or to fight the intruders.
this food. Most species of ants lay odor trails along the route from the Why are different gestures used for these two purposes? If the only
food source back to the nest. But this in itself may not be enough, be- function of the communication were to recruit nestrnates, it would
cause workers that have not been to the food must be induced to follow seem unnecessary to use a different gesture in the two situations. Per-
the odor trails. Chemical signals are transferred from returning foragers haps the recruited ants are better prepared for either food gathering or
to other members of the colony as they feel each other with their anten- fighting if informed which to expect as they move out from the nest.
nae . The forager often regurgitates food from her stomach which others These recruiting gestures are undoubtedly accompanied by the trans-
take up in a behavior pattern known as trophallaxis. mission of odors and chemical signals, and for all we know these may
In some ants the returning forager moves her body rapidly from side also provide information about what is located at the end of the odor
to side while engaging in mutual palpation and trophallaxis with one of trail.
her sisters. In Carnponotus serviceus this behavior induces the recruited Another feature of weaver ant recruitment also suggests thinking
ant to grasp the abdomen of the forager, and the latter then moves out about the need to recruit nestmates. Some of the ants receiving the re-
along the odor trail she laid down on her return to the colony (Holl- cruiting gestures do not follow the odor trail but turn to other workers
dobler 1974, 1977). This results in tandem running out to the food and repeat the recruiting gestures even though they have not been di-
source. Another very impoftant form of recruitment occurs when the rectly stimulated by intruders or newly discovered food. This sort of
colony is threatened by aggressive or competing members of other col- chain communication whereby one original recruiter indirectly stimu-
onies or other species. The weaver ants show a significant difference in lates large numbers of nestmates is almost unique in animal communi-
their recruiting behavior according to whether recruitment is for food cation. If we allow ourselves to postulate, tentatively, that these ants
gathering or fighting offintruders. rnight be thinking in simple terms about such impoftant matters as
Holldobler and Wilson (1978) have studied in detail the behavior of gathering food or fighting intruders, these somewhat specialized ges-
weaver ant workers after they have returned to the colony either from tures may be interpreted as evidence of what they are thinking about.
food sources or from encounters with intruders. The intruders may be 'l'he practice of chain communication is especially significant, because
members of another colony of the sarne species that are more nrunerous thc ant that has been stimulated by recruiting gestures and then repeats
and aggressive, or they may b-e other insects. The recruiting weaver ant thcse gestures may bc expressing a simple thought that has been con-
engages in a series of face-to-face encounters with nestmates at or close vcycd to her through the communicative process itself rather than by
to the leaf nests. The recruiter makes lateral movements of her head, s( )mc external stimulation.

which often induce the other ant to follow the odor trail she has just 'fhcse two kinds of recruiting gestures are an extremely limited form
laid down. These recruiting gestures differ according to what it is the of'somcwhat symbolic communication. The similarity remarked upon
recruiter has returned from. The principal difference is that when re- by Hdllcloblcr and Wilson between the gestures used to recruit for
cruiting to food sources, they move the head in lateral wagging mo- liglrting ancl thc acnral motions of fighting suggests that the communi-
tions. But when they are returning from an encounter with intruders, r'.rtion is iconic rathcr than symbolic. In this usage iconic means that the
they recruit other workers by jerking their bodies back and forth toward sigrrrrl rcscrrrt'rlc's thc :rctiorr <lr tlring that it represents. Thus making a
and away from the nestmate rather than from side to side. Holldoblcr s,rtrnrl ch.rr':rctcristic ol':r p:rrtictrLlr s()rt of'ruritnal as a symbol to repre-
and Wilson also describe other communicativc gcsturcs uscd whcn st'rrl llrltl :rrtirttrtl, srrr'lt:ls "llr)\\'-\vo\\," lot-tklgs, is iconic, whereas the
stimulating nestmates to movc to anothcr l<rrrtiorr, l'rut thc tlistincti<lrr rr',rrtl "tkrg." r.r,ltit'lt lt:ts tto lr.trlir ttl.tt't't'st'lttlrl:u)('c t() thc lutitnal in ques-
bcwccrr gcsturcs firr rccrtriting t<l f<xxl:rrrtl lir rotnlr.ttirrg irrtrtrtlcrs is Irorr, is lrot. ( )rr tltc olltcr lr.rrrtl, tltt' t('( nrilirrg gt'strrrt's lirr lixltl s()urccs
L78 ChapterNine Syrnbolic Cornmunication 179

do not seem to be iconic. It will be of great interest to learn more about such as flowers that have just come into bloom, many other bees from
these processes of communication when they can be studied with atten- the same colony may arrive a few minutes later, so rapidly that they
tion to their possible significance as indications of the thinking of the could not all have found the food by individual searching. This sug-
communicating animals. gested that some sort of recruiting communication occurred, but how
Humphrey (1980) has extended an earlier suggestion by |olly this was achieved remained almost totally unknown until the work of
(1966) that consciousness arose in primate evolution when societies de- Karl von Frisch, whose work has been mentioned several times in earlier
veloped to the stage where it became crucially important for each mem- chapters. F{e was a brilliant Austrian zoologist who carried out most of
ber of the group to understand the feelings, intentions, and thoughts of his research at the University of Munich, beginning about f9f0. Quite
others. When animals live in complex social groupings, where each one early in his career he proved by elegant simple experiments that bees
is critically dependent on cooperative interactions with others, they were capable of discriminating hues. He was led to this discovery by the
need to be "natural psychologists," as Humphrey puts it. They need to simple naturalist's belief that the striking colors of flowers must be per-
have internal models of the behavior of their companions, to feel with ceptible to the insects that visit them to obtain nectar and pollen. Early
them, and thus to think consciously about what the other one must be in the twentieth century, prevailing scientific opinion was strongly neg-
thinking or feeling. Following this line of thought, we might distin- ative about color vision in invertebrates. But von Frisch developed
guish between animals' interactions with some feature of the physical simple and ingenious experiments demonstrating conclusively that
environment or with plants, on the one hand, ffid interactions with honeybees have excellent color vision.
other reacting animals, usually their own species, but also with preda- In the I920s, when studying the sensory capabilities of honeybees,
tors and prey, as discussed in chapter 3. While Humphrey restricted his von Frisch noticed that the agitated dances were carried out by workers
criterion of consciousness to our own ancestors within the past few mil- that had visited sources of food. In order to see what bees did on return-
lion years, it could apply with equal or even greater force to other ani- ing to the hive, he constructed specialized beehives with glass windows
mals that live in mutually interdependent social groups. that allowed a clear view of their behavior as they crawled over the ho-
neycomb. To study foraging behavior he set out dishes containing con-
centrated sugar solutions, which bees visit and take up eagerly just as
The Symbolic Dances of Honeybees they take nectar from flowers. To identify individual bees he marked
The most significant example of versatile communication known in any them with small daubs of paint on the dorsal surface while they were
animals other than our own species is the so-called "dance language" of sucking up sugar solution. The bees he had marked at his dishes of sugar
honeybees. This type of communicative behavior is so strikingly differ- solution danced in circles, alternating clockwise and counterclockwise
ent from all other known kinds of animal communication that it has motions. At the sarne time he noticed that others returning with loads
been difficult for inclusive behaviorists to integrate it into their general of pollen were carrying out a very different type of dance. He could tell
understanding of animal behavior. The difficulty is exemplified by the that they had gathered pollen because honeybees carry substantial
behavioral ecologist Krebs (L977), who called these dances an "evolu- amounts of pollen grains packed between hairs on their legs. These pol-
tionary freak." The versatility of honeybee learning has been reviewed len gatherers perfiormed what are called Schwonzeltanzen in German,
by Gould and Towne (1988); and many of the complex effects of over- customarily translated as waggle dances. In a waggle dance the bee walks
learning and extinction studied by psychologists in rats and pigeons rapidly in a straight line while moving her abdomen back and forth lat-
have also been found in honeybees, for example by Bitterman (1988), crally at about thirteen or fourteen times per second. Then at the end of
Shinoda and Bitterman (1987), Couvillon, Leiato, and Bitterman this straight wagging mn she circles back and repeats the straight part
(I99I) and Lee and Bitterman (1991). of thc d:rncc, firllowctl by lltcrnating clockwise and counterclockwise
Beekeepers and students of bee behavior had noticed for centuries rctunls to thc st.lrting poirtt of a scrics of straight wagging runs. Al-
that worker honeybees sometimes move about ovcr thc surlace of thc tlrorrgh thc llcc nrily nlovt' .r slrort tlistlrtrcc lrctwcen successive cycles of
honeycomb in agitated pattcrns callcd clarrccs. [t rv:rs also u,cll knowrr tlrt'rv:rgglt'tl:urt'c. tlrc lr.rsit l).rtt('r'n is rclrrtivcly c<>nstant under given
that oncc a singlc forlging workcr has tliscovcrctl .r r it lr sr )ur'('(' ol'lixrtl, t'olttlit iolrs. \t lr l;r'rsr lr t lrus r ortt lrtrlt'tl t h.rt tltc two tyl)cs of thtrcc wcrc
180 ChapterNrne SyrnbolicCornrnunication l8l
somehow related to the sort of food being brought back to the colony, watching them whether their leisurely moving about the hive is idle
a reasonable interpretation of the observations he was able to make at loafing or whether they are sampling odors and other conditions in
the time. ways that will later affect their behavior. The workers often take food
Only much later, during World War II, when his laboratory in Mu- from partially filled cells, into which other workers are still adding
nich had been seriously damaged and he was studying bees at his coun- honey or pollen. Thus the food stores of a beehive are in a constant state
try estate in the Austrian Tyrol, did he have occasion to move the artifi- of flux, with new material being added after foragers have brought it
cial feeding dishes to a considerable distance from the observation hive. back, but also constandy being drained by workers, which obtain much
When he did this he discovered that the bees gathering sugar solution of their food in this way.
from more than about one hundred meters performed waggle dances When a forager returns to the hive with a stomach full of nectar, she
rather than the round dances he had always associated with sugar gath- ordinarily finds other workers ready, after a brief period of mutual pal-
ering (von Frisch 1950, 67-72;1967,57-235). This had escaped his pation, to take her stomach load by trophallaxis. These other workers
notice previously, because for reasons of simple convenience he had set then store the somewhat modified nectar in pardy filled cells, or they
out his dishes of sugar solution relatively close to the observation hive may transfer it to third parties before it is finally stored. This widespread
so that he or his assistants could remain in touch while marking bees at process of mutual palpation and trophallaxis serves also as a sort of
the feeder or observing them in the hive. communication, because the ease or difficulry with which a returning
It is very important to appreciate that these dances occur only under forager can transfer her load provides information about the general
rather special conditions. They are part of an elaborate nexus of social situation in the colony. This is panicularly important when conditions
communication that goes on almost continuously in a beehive, as de- are not optimal and when something is in short supply. The most com-
scribed by Lindauer (1971) and Seeley (1985, 1986, I989a, I989b). mon shortage is of carbohydrate food. The workers are informed of this
The workers move about a great deal and interact with their sisters by by the relative emptiness of storage cells, and when conditions are truly
feeling them with their antennae and being felt in return. There is a sort severe, capped cells may be opened and the honey consumed. This re-
of mutual palpation in which the two bees face each other and feel sults in an eagerness to receive regurgitated nectar during trophallaxis
each other's antennae and head region. At this time one of the bees with rerurning foragers. When, on the other hand, honey is abundant
often regurgitates a small portion of her stomach contents, which is but pollen is in short supply, foragers returning with stomachs full of
taken up by the other. This is very similar to the trophallaxis of weaver nectar have more difficulty finding a sister to whom they can transfer
ants and other social insects. It is very widespread among social insects their load. Whether there is some chemical or other signal that conveys
and serves to convey not only food material but also the odors that ac- more than a reluctance to receive one type of material is not clear. But
company it. In colonies of specialized social insects such as honeybees somehow foragers are induced to change what they seek outside the
the queen, the larvae, and younger workers obtain their food in this way. hive .

Tiophallaxis is so widespread that a given molecule of sugar ordinarily This distil'rction becomes all the more clear under special conditions
passes through several stomachs before it is finally reg;urgitated into one of overheating. When the hive temperature rises above approximately
of the cells in the honeycomb. By this time the original nectar gathered 35 degrees C, workers returning with either sugar or pollen have diffi-
from the flowers has been modified into honey. Pollen grains trans- culty unloading. But workers that have gathered water regurgitate it in
ported in specialized pollen baskets formed from stiff hairs on the legs small droplets, and other workers fan vigorously with their wings, pro-
are also transferred to other workers before being stored. During round tlucing a circulation of air that cools the hive by evaporation. Under
and waggle dances other bees cluster around the dancer and follow her thcsc conclitions f<rragcrs shift from gathering nectar or pollen and visit
movements. From time to time they make a brief sound that seems to plrrccs whcrc thcy c:rn takc up water. It is not clear just how this transfer
cause the dancer to stop and engage in trophallaxis with one or more of ()ccurs, whcrlrcr thc high tcrnpcrrrturc ciircctly stimulates the returning
her sisters. lirr:rgcr, rrkrng rvitlr lrt'r' rlillir rrltv in rurlo:rtling whatever she was bring-
In spite of all this activity, wrlrkcr honcytrccs sccnt to lrt'tkrirrg noth- irrg irr prt'r'iousl\,. (,r \\,1)('tltt'r s,)nl(' sot't ol'irrfilrrtr:rti<ltr is transferred
ing at:rll nrrrch of thc tirnc, llrt ir i.s dil]icrrlt lo tlt'tcrrtrint'hv sirrrplv li'ottr ot ltcr rvorkt'l s.
L82 ChapterNr.ne Symbolic Cornrnunication f 83

The important point is that the older workers that fly outside the hive Round dances are performed when food has been discovered rela-
searching for things needed by the colony shift their searching behavior tively close to the hive, and waggle dances are used for desirable things
between different commodities accordi.g to the needs of the colony. located at a greater distance. The transition from round to waggle
This network of social communication conveys to the older workers not dances is gradual, ffid it occurs at different distances ranging from nvo
only what is required by the colonv but how badly it is needed. Thus or three meters in the Indian species Apis dmsnta andA. f.orea to 50-
when a forager leaves the hive, she has been induced to search for some I00 meters in the widely used Carniolan strain of European honeybees.
particular thirg, and this motivation clearly varies in intensity. The most In a typical round dance a bee circles alternately clockwise and counter-
corrunon need is for carbohydrate food, so that the nectar of flowers is clockwise, although occasionally nvo cycles may be executed in the
the usual target of this searching activity. But sometimes it may be pol- sarne direction. When von Frisch originally discovered that round
len grains or water. Under other special conditions the need may be for dances were used for food sources at relatively short distances and
waxy materials used in building honeycomb. This need is relatively rare waggle dances for those farther from the hive, he concluded that the
in agricultural beekeeping practice because beehives have been built to round dances contained no directional information and simply in-
provide a waxy foundation, but under natural conditions honeybees and formed recruited workers to search in all directions close to the hive. He
other bees must build their own wax foundation or plug holes in a nat- also found that bees stimulated by round dances arrived in approxi-
ural cavity. Dances do not occur at all when everydling is going nicely mately equal numbers at experimental feeders located in different direc-
and nothing is in short supplv. Foragers return with nectar or pollen, tions within a few meters of the hive. M*y interested scientists have
these substances are transferred to other workers, and the net stores of observed and made motion pictures of round and waggle dances over a
both carbohydrate and protein food are either constant or slowly in- forty-year period, but only recently has it been noticed that even at very
creasing. Under these favorable conditions it seems that workers can short distances the point at which the circling reverses does contain di-
find adequate supplies of nectar and pollen by individual searching ef- rectional information of the same kind conveyed by the waggle dances
forts. discussed below (Kirchner, Lindauer, and Michelsen 1988). The fact
Under the special conditions when something has been in short sup- that it took so long to appreciate this simple fact indicates how easily we
ply, older workers ready to fly outside the hive somehow receive the overlook matters that do not readily fall into our preconceived patterns
message that sugar, or something else, is very badly needed. When they of expectation.
have discovered a rich source of nectar they return to the hive and en- The transition from round to waggle dances begins by a very brief
gage in communicative dances. After walking a short distance in from lateral vibration ofthe bee's body just at the moment when she has com-
the entrance of the hive, and usually after antennal contact with other pleted one circle and is about to begin circling in the opposite direction.
workers, the returning forager begins either round dances or waggle As the distance to the food increases this lateral wagging motion lasts
dances. Dancing is not something the bees do mechanically and auto- longer and the bee walks in a straight line for a gradually increasing
matically, but only as part of the larger social nexus of communication. distance. This can be observed with the same bees by inducing them to
This point is often overlooked in elementary discussions of the bee gather concentrated sugar solution from an artificial feeder which is
dances. The durces are entirely dependent on the Presence of an audi- gradually moved away from the hive. This experimental procedure is
ence ofother bees. cffective only when the colony is seriously in need of additional sugar.
Wirh this background we can better appreciate the symbolic naulre When the distance is gradually increased, beginning at a very few meters
of the honeybee communication system. It is partly a chemical colrunu- fiom the hive, it is possible to see the gradual transition from an almost
nication system, for the odors of flowers are conveyed along with the instantancous latcral vibration at the moment when the round dance is
nectar or pollen. And when bees visit desirable things, they often mark rcvcrsctl irr dircctir)n t() arr increasingly long straight wagging run. At
their location with secretions from certain glands that produce a long- distanccs <lf'rr kil<lnrctcr ()r nl()rc rhc wagging run is ten or eleven milli-
lasting odor which serves to attract searching foragers. But in addition nlctcrs irr lcrrgth.
to these specific odors that are transmitted, thc tlattccs c()rtvcy thc dircc- 'l'lrt' rnost sigrrilit:rnt ( )l vorr l;r'ist'lt's tliscovcrics was that the direction
tion and distancc to thc fboc'l [-ry .l s()rt r>f gcolnctricrtl svlttlx rlisltt. ol tltt'sll':riglrt w.U',1',tll!', llttl \v.ls tot't.t'l:tlt'tl witlr fhc tlirccti<lrr that thc
f 84 ChapterNine SyrnbolicCornmunication 185

dancer had flown from the hive to the source of food. This insight was for the complicating effects of odors. The majority of the recruited bees
possible only when he was able to observe waggle dances perficrmed by calne to feeders within about plus or minus L5-20 degrees and plus or
that had returned from known food sources lying at considerable minus about f 0-I5 percent of the distance indicated by the dances.
distances in various directions. Ordinarily this is not possible, because Thus the system is far from perfect, but the waggle dances corrrrnu-
honeybees are too small and fly too far and too fast to permit direct nicate three types of information that are all important to the bees.
observation. In his early experiments) von Frisch saw no reason to move These are (I) the direction toward the food, expressed relative to the
his artificial food sources more than a few meters from the hive. In the position of the sun, (2) the distance to the food which is correlated with
1920s it would have required a truly superhuman level of enterprising the duration and perhaps length of the wagging run, and (3) the vigor
imagination to suggest that an insect might indicate the direction to a of the dances which conveys the desirability ofwhatever the bee is danc-
food source by some form of communicative behavior. Even a brilliant ing about. The detailed nature of distance corrrrnunication has been dif-
scientist who had already challenged some of the established "nothing ficult to determine. The number of waggling movements is correlated
but" dogmas of his time did not make the leap of inference necessary to with the distance a bee must fly. But since the rate of waggling and the
imagine that the waggle dances which he and many others had observed rate of forward movement are quite constant, both the length of the
.oold conceivably serve to corrununicate direction toward a source of waggling run and its duration are also closely correlated with distance.
food. This leads one to wonder what other versatile ingenuities of ani- While statistical analysis suggest that the duration is a better indication
mals might be staring us in the face but waiting to be correctly inter- of distance, it is not possible from currently available data to be certain
preted. which property of the waggling run is actually perceived by other bees
The specific correlation between direction of the wagging run and and used to determine the distance they will fly.
direction toward the food takes the following form: When the food is The vigor or intensity of waggle dances is easily recognized by expe-
in the direction of the sun, outside the hive, the waggle dances are ori- rienced observers, for some dances seem clearly more energetic than
ented straight up on the vertical surface of the honeycomb. If the food others, and these ordinarily result when foragers have found a rich
is located in the opposite direction from the sun, the dances point source of sugar solution or something else that is important to the bees.
straight down, and under other conditions the angle between the direc- The concentration of sugar in an artificial feeder can be more easily ma-
tionio the food and the azimuth bearing of the sun corresponds to the nipulated by experimenters, so that it has been studied more thor-
orientation of the wagging run relative to straight up. If the food is 90 oughly. But it is clear that under relatively constant conditions when
degrees to the right of the sun, the dances are 90 degrees to the right of carbohydrate food is scarce and dancing is actively under way, the
vertical. clances are much more intense when the foragers have visited sugar so-
This relationship between a direction taken by a flying bee outside Itrtions with a high concentration. One difference is that dances from
the hive relative to the sun and the direction of its communicative wag- rich sources are continued for a long time while dances from less con-
ging run inside the pitch dark hive is more truly symbolic than any other ccntrated sugar solutions may be continued only for a few cycles and
krro*r, communication by nonhuman animals. But one should not take thcn broken off, as discussed by Seeley and Towne (in press).
this correlation to mean that the directional communication is perfectly Another important point about the waggle dances is that they serve
precise. At gradually increasing distances, as the bees change from t() convey information to other bees inside the totally dark beehive
iound dances to waggle dances, the straight runs do not at first point rvhcn thc subject of the communication is something entirely different
directly in the appropriate direction. Instead they alternate between lirrrn thc immediate situation, namely the direction a bee should fly out
being several degrees to the right or to the left of the correct distance in thc ()pcn air. Thus thc communication has the property of displace-
r..oiding to the rule stated above. As the distance increases this devia- n)cnt; thc l'rccs cornnrurricatc about somcthing displaced in both time
tion diminishes, so that by several hundred meters each waggle run :urtl s1'r:rcc lirrrn thc irtutrctlirrtc situ:rti<ln whcrc the communication takes
points in almost exactly the same direction. The accuracy of information pl.rt'c.
iransfer has been measured by Tkrwne ancl (lotrld (lgttti) bv sctting ottt Wcnnt'r'(1959, l()(r2lr),.rrrtl lrst'lr (19(rl, 1964) cliscovcrcd thatfaint
tcst fcc{crs in a vlrricty <lf tlircctiotrs:uttl tlist.tllt't's rvitlt t'.trclirl cotrtr<ll sottlltls:l((()ll)l).lllit'tl tlrt'u'.r1',1',lt'tl.tlttt's.'l'ltt'st':ll'c t'l()t.rtli,urily l<ltrd
186 ChapterNine Syrnbolic Comrnunicat'ion L87
enough to hear through the glass window of an observation hive and leagues (Michelsen, Kirchner, and Lindauer 1986; Michelsen, Kirch-
require that the glass be removed so that the dances can be observed ner, Andersen) and Lindauer 1986; and Michelsen, Towne, Kirchner,
direcdy. This is obviously somewhat hazardous, since several hundred and Kryger L987). The most important point clarified by these recent
bees are completely free to fly out. But if the glass is gently removed experiments is that the changes in air pressure which we detect as
most of the bees stay in the honeycomb, and many detailed experiments sounds, either by hearing them direcdy or via microphones, are only
have been carried out with observation hives that can be opened. Ordi- one physical aspect of the signals generated by dancing bees.
narily this is done with a darkened room around the hive, but even this When any solid object oscillates against the air, whether it be a danc-
is not entirely necessary, and quite bright lights can be used for photog- ing bee or a loudspeaker diaphragm, air in the immediate vicinity moves
raphy or video recording, provided that the bees are not disturbed ex- back and forth at the frequenry of the movement. Close to the vibrating
cessively. The sounds accompanying waggle dances are brief pulses with object this motion of the air is the primary physical process, but mag-
a fundamental frequency of about 250-280 Hz; each lasts only for a nitude of air movement falls offwith distance very rapidly. The oscillat-
few waves but the pulses are repeated as a sort of interrupted buzzing. ing movements of the air also generate traveling sound waves which are
The fundamental frequency is nearly the same as the wingbeat fre- areas of very slight compression and rarefaction that spread outward at
quency when the bees are flying, but the wings move only a fraction of the speed of sound (approximately 3M meters per second in air). It is
a millimeter. The sounds and waggling movements are not always syn- of course qualitatively tru9 that in order to produce a region of higher
chronous; in long-duration dances reporting highly desirable food, the pressure some air molecules must move into such a region, but the
sound may be delayed by a substantial fraction of a second (Griffin and arnount of air that moves back and forth in a traveling sound wave is
Thft, in press). very small compared to that which moves about close to the vibrating
Esch (1963) concluded the desirability of food or other commodities source. This difference leads to the physical distinction benveen near
seems to be conveyed, at least in part, by the intensity or temporal pat- field and far field sounds. In the near field the air motion is large and in
tern of these dance sounds, which seem to vary with the desirability of the far field it is very small, because its magnitude falls off rapidly with
the food being gathered. But Wenner, Wells, and Rohlf (1967) did not distance from the source.
find such variations, ffid it remains unclear whether the dance sounds The bees that are stimulated by a dancer are ordinarily within less
convey information about food quality. One possibility is that the tem- than one body length, and this is definitely in the near field. The sounds
poral relations between waggling movements and sound emission with which we are most familiar are far field pressure waves. Bees and
might convey this or other types of information. Further evidence of rnost insects lack speci alized auditory receptors for sound pressures, al-
their importance has recently been provided by Towne (1985), who though a few specialized insects such as some of the moths that respond
srudied two closely related species of bees in India, Apis dmsata and A. to the orientation sounds of bats do have sense organs adapted for re-
f.orea, which use waggle dances but nest in places where light is avail- sponding to sound pressure. What bees and many other insects have
able. They make no dance sounds, although in other aspects of their instead are very sensitive hair-like sense organs that respond well even
dance communication they are similar to European Apis rnellifern. It to feeble air movements, whether these be unidirectional or oscillating
seems clear that only honeybees and their close relatives that dance in- at frequencies of a few hundred Hz. Thus it is not surprising that
side dark cavities make sounds during their waggle dances. honeybees do not respond to far field sounds, but such insensitivity
Interpretation of these observations was initially difficult because tclls us nothing about their sensitivity to near field acoustic stimu-
honeybees appeared to be deaf. Despite several attempts to do so, no lution which consists primarily of oscillatory air movements.
one had been able to demonstrate any responses to airborne sounds. Michcl.scrr, ltrwnc, Kirchncr, and Kryger (1987) measured the near
This suggested that the sounds heard by human observers might be an lickl conrp()ncnt of thc dancc s<>unds and found these to be quite in-
incidental by product of a mechanical signal that was transmiffed either lcrr.scr provitlcd tlrc lrrce.srrrirrg rlcviccs wcrc within a few millimeters of
by vibratory motions of the surface on which thc l'rccs wcrc standing or tlrc tl:rnt'cr. In lirrtlrcr cxlx'rirrrt'nts'lirwrtc and Kirchner (1989) *d
in some othcr manncr. TIris .sinratiorr lra.s bccrr t'onsitlt'r:rblv clerificd Kirtlurt'r, l)n'llt'r'. ;urrl 'liru,rtr' (l()()l) lixrnrl that h<>ncybccs rcspond to
throtrgl'r quantitativc rtc<lustic:rl cxpcrinrcrtts Iry Mitltr'lst'rt :ttttl ltis c<ll- tlrt'rtt'.rr lit'ltl,;tit'rttr)\,('rn('!rl (()nrl)()n('nl ol'sourttl sintihr to thc dance
188 CbapterNine Syru.bolic Coru.rnwnication f 89

sounds. Using sound sources that generated either primarily near or far vinced that the system really functions as von Frisch described it (Rosin
field sounds of either 265 Hz or 14 Hz, they were able to show clear 1978,1980, 1984, 1988; Wenner 1989; Wenner and wells 1990). Both
responses to the near field signals but not to the far field sound pressure Rosin and Wenner consider von Frisch's discoveries susPect because
stimulation. The latter had been used in previous attempts to learn they imply, for Wenner (1989, II9), that bees are "capable of human-
whether bees could hear. like communication (language)," ot because, according to Rosin (L978,
The situation is further complicated by the fact that honeybees also 589) "a hypothesis which claims a human-level'language'for an insect
transmit acoustic signals as vibrations of the substrate . With appropriate upsets the very foundation of behavior, and biology in general." These
vibration detecting sensors Michelsen, Kirchner, Andersen, and Lin- critics, and doubtless others, are so certain that symbolic communica-
dauer (1986) showed that the dance sounds are transmitted only very tion is a unique human capability that they go to great lengths to_ deny
feebly into the honeycomb. But another sound at about 320H2 is emit- the signifi.*t. of the many experiments demonstrating mT m:9ances
ted by bees following a dancer; this is believed to serve as a request for .o.rury information about distance, direction, and desirability. They do
the dancer to stop and regurgitate food samples. These sounds are trans- nor deny that the paftern of the dances is correlated with the location of
mitted through the substrate. When the honeycomb was set into vibra- a food ,o.rr.., bui claim that recruited bees simply search for the odor
tion by artificial devices at this frequency dancing bees stopped dancing they have learned from the dancer is associated with the food. In some
as they do when this so-called begging signal is generated by other bees ingenious experiments by Gould (reviewed by Griffin l98l), bees were
clustered around a dancer. induced to point their dances in a direction different from the actual
Another quite different type of acoustical signaling is carried out by clirection from which they had returned. Test feeders were set uP in the
honeybee queens. When larvae have been fed appropriately by workers fbrm of traps that allowed counting of the number of recruits arriving
they develop into queens, and often several queens are present in sepa- at different places, but prevented them from leaving and possibly intro-
rate cells. At this time, it has long been known that the queens emit two clucing cornplications. The results were that most of the recruited work-
kinds of sounds called tooting and quackirg. These are transmitted crs flew to i.st feeders in the direction indicated by the dance rather
through the honeycomb substrate and are sensed by other queens. The than the direction from which the dancer had returned. The more re-
tooting is produced by a queen who has emerged from her cell and the cent experiments with an effective model bee, which certain\ did not
quacking signals come from queens still confined within cells. Usually convey location specific odors, abundantly confirm that information
the original queen together with a very large number of worker bees lbout distance *d di...tion can be conveyed from the dancer to her
departs from the hive and forms a new colonv. One of the new queens sisters.
then cuts a hole in the side of the other queen cells and kills the occu- The accuracy of this distance and direction information has been
pants. Thus this exchange of acoustical signals is an important sttrclied by von Frisch ( L967) and more recendy by Towne and Gould
part of the social behavior of a honeybee colony around the time of (1988). The basic approach was to set out test feeders with the same
swarming. otlor as that associatid with a rich source of concentrated sucrose and,
Michelsen, Kirchner, and Lindauer (1989) have succeeded in con- .rftcr removing the original source of food about which bees had been
structing a model honeybee that can transmit signals which direct re- tlurcing, to -ir.,rre how many recruits arrive at the test feeders. In both
cruits to search for food in particular directions. This exciting develop- r,,r1 Fr]sch's original experiments and these more carefully controlled
ment is still at a very early stage, and all that can be said is that in a tcsrs, rhc majoriiy of the recruits went to feeders in approximately the
general sense the model does work. The reason it has worked better s:lnrc clircction and at approximately the same distance as the location
than previous attempts is probably that the near field acoustical signals irrtlic:rrctl by thc clanccs. Thcrc is, however, considerable variation and
r lrc sirrntion is cornplicrrtcd lry thc possibility that the odors
have been reproduced more accurately. It will be of great interest to
follow future developments in this new technology for studying the rlrc loc:rrion ol'thc origin:rl ll'ctlcr or thc tcst fccdcrs may diffirse widely
symbolic dance communication of honeybees. t-rrorrgh tlrrrr becs .lt'r :tltr'.I('t('(l lo tltctn cvcn th()ugh they may not have
It has been so astonishing to find insccts c<lt'trttrrrricrrting in strch a ll,,ryrr yr.t'1r;11,',,r':il1l1, to lltt'tlist.tltt't'ltrttl tlirccfi<ln inclicated by the
versatile and symbcllic fhshion that s()nrc skcptit's lr;rvc rt'rrr:rirrctl unc()n- ,l.tttt'<'s lltt'\'lt:tvt'lollou't'tl. lrr 1',t'lrt't.tl lt't'ltts, it sccltls th:rt thc clirec-
f90 ChapterNine SyrnbolicComrnunication I9f
tional indication is accurate within approximately plus or minus 20-30 warmer months when they are active. While the queen may have partic-
degrees and the distance indication perhaps plus or minus I0 or 15 per- ipated in swarming many months before, the workers have never expe-
cent. Evidently the finding of the exact location requires response to the rienced anything remotely like the movement out of the old hive and
odors conveyed at the time of the dancing. But the symbolism of com- the aggregation of thousands of bees in the open.
municating direction and distance is very significanr) even though its It is not easy to find an appropriate cavity. It must be of roughly the
accuracy is not all that one might ideally desire. right size and have only a small entrance near the bottom. It must be
One misunderstanding of the dance communication of honeybees dry and free from ants or other insects. In one of the few investigations
that is very widespread is the belief that it is rigidly linked to food. As that has followed from Lindauer's discovery Seeley (1977) has studied
mentioned above, the dances are also used to corilnunicate about water how the scout bees investigate cavities. He established colonies on small
needed to cool the colony by evaporation, but water can be viewed islands where no suitable cavities were present and induced swarming
simply as a very dilute sugar solution. Wary materials are sometimes by the simple procedure of shaking the queen and numerous workers
collected and their location indicated by waggle dances. But the mosr out of the old hive and leaving them to their own devices in the open
enterprising use of the dance communication system occurs when bees air. He then provided experimental cavities of different types at some
are swarming. Although these dances were discovered many years ago distance. The workers found these and eventually induced the colony to
by Lindauer (1955), ethologists have devoted very little anenrion to occupy one of them. In their preliminary visits these workers crawled
them despite their implications concerning cognition. back and forth through most of the interior of the cavities and spent
Swarming occurs when a colony of honeybees increases to the point considerable time investigating them.
that the hive is crowded. Workers then feed some larvae a different soft When Lindauer studied swarming bees he observed that workers car-
of food, which causes them to develop into queens. Under ordinary ried out waggle dances on the surface of the swarm. These are similar in
conditions the bees also prepare to swarm, md part of the behavioral some ways to dances that are occasionally carried out on a horizontal
changes that accompany this sort of preparation is a change in the surface in front of the hive entrance. When bees are dancing on a hori-
searching images of the older workers that have previously been garh- zontal, surface in the open they point direcdy toward the food or what-
ering food. They now begin to investigate cavities. As new queens de- ever the dances are about. The symbolic transfer to graviry with upward
velop, the older queen stops lryrrg eggs and usually moves out of the pointing dances meaning toward the sun apparendy does not occur
hive along with a large portion of the workers. Initially these aggregare when the dancer and any of her sisters who follow the dances are on a
in a ball of bees clinging to the surface of the hive or ro vegeration. In horizontal surface and can see the sun.
normal bee keeping practice the beekeeper either enlarges the hive at The waggle dances executed on the swarrn indicate the distance, di-
the first sign of swarming so that the colony can grow further or else he rection and desirability of the cavity which the dancer has visited. This
provides a new hive immediately below the swarm. A beehive is an ideal rneans that the dance communication system, with all its symbolism, is
cavity and the bees usually move directly into it. cmployed in this totally unprecedented situation. The same code indi-
M*y colonies of bees flourish away from carefully tended apiaries, cates the location and quality of something as different from food or
and when they swarm no beekeeper provides an ideal caviry in the im- water as one can imagine. Worker honeybees that have been gathering
mediate vicinity. Under these conditions many of the older workers, ncctar from flowers during the past few days, and which may even con-
rather than searching for flowers or other sources of food begin to tinuc to do so to provide food for the swarm, utilize the totally different
search widely for cavities. Often they must search over a very large area, scarching image of a dry dark cavity of appropriate size to guide both
crawling into innumerable crevices in trees, rocks, or buildings. Their thcir scarchcs f<rr such cavities and their communication about one that
central nervous systems must recognize a searching image for an appro- thcy lravc visircd. If wc acccpt specialized communicative behavior as
priate sort of cavity. A cavity is Jf course ,o*.t-hi,',g Iotally diff.i.c,',t suggcstivc cvitlcncc ol'thinking on thc part of the communicating ani-
from food, and these workers that now scarch f<rr cavitics h:rvc ncvcr in nr:ll, wc nr:ry inli'r' tlr:rt tltt'sc w<lrkcr hccs think about either food
their lives done anything of thc kind. Swanninli ortlirr:rrilv ()ccrrrs :rt s()rtr('('s ()r-('.tvilit's,.lrtor.lirrg to lltt'rrcctls thcy havc pcrceivcd at the
intcrvals of many nl()nths, atrrl workcrs livr'ortly .t lt'rv u'r't'ks tlrrrirrg the t irrrt'.
192 ChapterNme Syrnbolic Communication 193
In his classic experiments during the 1950s, Lindauer discovered bees do not reach this crucial decision until dancers have been) so to
that the waggle dances executed on a swarm lead to a group decision on speak, singing the praises of a particular cavity for a considerable period
the part of the colony about where they should move to establish a new of time. M*y factors probably play a role in the evaluation of cavities
colony. Ordinarily dozens of scout bees that locate cavities dance on the by individual scout bees. In addition to size, dryness, and a dark interior
swarm about different locations. Furthermore, the intensity of the with a small opening, distance from the original colony is important. It
dances is correlated with the quality of the cavity. Small, damp, or ant- seems that other factors being equal the bees prefer a cavity a few hun-
infested cavities produce only a few feeble dances whereas others that dred meters from the old colony. This presumably has the advantage of
are dark, dry, and of suitable size lead to prolonged and vigorous waggle avoiding competition for food sources with the thousands of bees that
dances. Since different scouts have visited different cavities, a wide va- remain in the original cavity and continue to search vigorously for food.
riety of locations are described by the numerous dances that go on over Although we can only speculate about what, if anything, these danc-
the surface of a swarm. ing bees and their sisters who follow the dances on swarms are thinking,
Lindauer spent many hours in laborious observations of the dances their vigorous communication suggests that they are thinking about a
on the surface of numerous swarms, climbing ladders, or doing what- suitable cavity, perhaps similar to the one from which they have recently
ever was necessary to reach a suitable observation point. He found that emerged. Lindauer also observed another feature of the communication
although a wide variety of locations were signaled in the first few hours on swarms that has significant implication for a cognitive interpretation
after a swarm emerged from the original hive, the dances gradually came of the communicative behavior. In the first day or two, after the swarm
to represent a progressively smaller number of locations. As time had emerged and a number of different cavities were being described by
passed, the few cavities described by the dances that were carried out by various returning scouts, one might suppose that the less desirable cav-
increasing numbers of bees were those that had originally elicited the ities dropped out of the communication process because scouts that had
most vigorous dances. In other words, the cumulative effect of extensive visited them simply stopped dancing, while those returning from the
dance communication was a progressive reduction in the number of better cavities continued. Yet the individual bees return repeatedly to
cavities described. And those that continued to be danced about were the cavities after a bout of dancinB, so that the sarne individuals con-
the best ones available. tinue to describe the cavities they have located over many hours or even
In further experiments Lindauer varied the suitability of particular a few days.
cavities. If their quality was lowered, the dances became less enthusias- By marking individual dancers, Lindauer discovered that something
tic; and in some situations at least, dances about other cavities became even more interesting was going on. Bees that had visited a cavity of
more nurnerous. This process of repeated dancing about the more desir- mediocre quality sometimes became followers of more enthusiastic
able cavities went on for a few days, and finally almost all dances were dances than their own. Then some of them visited the better cavity they
about a single cavity. After this had been going on for several hours, a had learned about as followers ofvigorous dances) rerurned, and danced
different sort of behavior occurred, which Lindauer describes as rrppropriately with respect to the superior cavity they had now visited.
a"buzzing run." The bees making these buzzing runs moved for fairly I.indauer was only able to observe this in a handful of cases, and it is not
long distances over the swarm while emitting abtzzing sound. When clcar how large a role this change of reference of the dances of individual
this had been going on for some time the swarm took wing and flew l'rccs plays in the whole process of reaching a group decision. Neverthe-
fairly directly to the cavity that had been described by the concentration lcss thc fact that any bees change from dancing about one cavity to an-
of enthusiastic dances over the past day or so. othcr, aftcr switching roles from dancer to follower) means that the
These dances on the swarm lead to a sort of consensus whereby the wholc proccss of communication by means of waggle dances is not a
colony selects out of many possible cavities the one that has been judged ril4itl onc linkcrl tightlv to thc stimulation received during visits to the
by the scout bees to be the best. There seem to be adaptive advantages lirst c:rvit), :r P:rrtit'rrllr intlivitlrr:tl hrrs located. It seems reasonable to
to prolonging this process of evaluation, bccausc c:rvitics nrlrv changc irrlt'r'tlr:rt rrrrtlcr lltt'st't'otttliliotts lrccs lrrc thinking about cavities, and
their desirability as cr>ncliti<lns changc. F-or cxrrtnlllt', ottt'tlt;tt ltrts lrcclt .rrt':rlrk'lo t'lt:utgt'tlrt'ir ".rllt'girrrrt'r"'lir)rt'l ()nc thcy havc discovcrcd
'l'lrrrs il st't'ttts th:rt tlrc
dry in g<xlcl wcathcr rnrry ['rc rllunp ott rr rltinV tl:l\'. tlrt'rrrst'lvt's lo.l lrcttcr ont'tlrt't'lr.rvc lr',rnrt'tl :tlxxrt:ts rccipicnts()f sym-
194 ChapterNrne

bolic information from the dances of one of their sisters. Unlike the CHAPTER TEN
weaver ants studied by Holldobler and Wilson, however, Lindauer did
not see any signs of chain communication. When dancers changed the
cavity about which they danced they did so only after visiting the sec-
ond cavity. D eception, a,n d Mnn opulntion,
AII this communicative versatility certainly suggests that the bees are
expressing simple thoughts, as I have argued elsewhere (Griffin 1981,
1986). One significant reaction to von Frisch's discovery was that of
Carl ]ung (1973). Late in his life he wrote that, although he had be-
lieved insects were merely reflex automata,

this view has recendy been challenged by the researches of Karl von Frisch; . . . n the previous chapters animal communication has been consid-
bees not only tell their comrades, by means of a peculiar sort of dance, that they ered as a straightforward transmission of information from one animal
have found a feeding place, but they also indicate its direction and distance, to another, and it has been tacitly assumed that this information is rea-
thus enabling beginners to fly to it direcdy. This kind of message is no different
sonably accurate. That is, when one animal, the sender, emits a signal,
in principle from information conveyed by a human being. In the latter case we
this signal is taken as some indication of its intentions, or at least of its
would certainly regard such behavior as a conscious and intentional act and can
hardly imagine how anyone could prove in a court of law that it had taken place disposition to behave in a certain way, that can be reliably interpreted
unconsciously. . . . We are . . . faced with the fact that the ganglionic system by one or more other animals, the receivers. (The terms "actor" and
apparendy achieves exactly the same result as our cerebral cortex. Nor is there "responder" are sometimes used instead of "sender" and "receiver"; but
any proof that bees are unconscious. the latter are preferable because they do not i-ply anythi"g about be-
havior of the receiver, which may not react at all.) I have emphasized
the possibiliry that the production of communicative signals may be
consciously intentional, that the sender may want to transmit informa-
tion to the receiver because it wishes to affect the receiver's behavior in
some way. Inclusive behaviorists have avoided any such inferences, pre-
ferring to concentrate attention on the functional effects of the com-
munication, especially its contribution to evolutionary fitness, rather
than on any mental experiences of either sender or receiver.
Dawkins and Krebs (1978) in an eloquent and influential paper have
argued against what they call the classical ethological analysis of animal
communication, which emphasizes cooperation benveen individual an-
imals facilitated by transmission of accurate information about the
scndcr's dispositions to behave in particular ways. Instead they empha-
sizc the struggle between individuals, both between members of the
.sllnrc and different species. This emphasis stems from a strong prefer-
cncc f<lr thc "picturc of an animal as a machine designed to preserve and
[)r()ptgatc thc gcrrcs that ridc insidc it" as argued forcefrrlly by Dawkins
(1976). l)awkirrs rrrrrl Krctrs intcrprct communicative signals as means
to rn:rniprrl:rtc otlrcrs, r:lllrt'r'th:ur to inlirrrn thcnr. From this perspective
il st't'rrrs likcly tlr;rt tlrc irrlr)r'rr):ltiorr lr';utsttrirtcrl lry c<lmmunicativc sig-
rr.rls is oltt'rr in;rt t rrr..rtt', .urtl s('r \'('s to rrrisirrlirntt thc rcccivirtg urimal.

f 96 Cbapter Ten Deception and Manipulatiott l()7

As pointed out by Hinde (I981) the diftbrence between the two ap- by Mitchell and Thompson (1986), and I will draw on several spcc-ific
proaches is not as fundamental as Dawkins and Krebs assert. Etholo- examples of deceptive behavior described in that volume.
gists studying animal communication have almost always considered Some discussions of deceptive behavior include in this category mor-
that communicative behavior is adaptive, that it has resulted from nat- phological mimicry, in which the colors or shapes of animals resemble
ural selection, and that it often enables one animal to alter the behavior dangerous or inedible objects, as well as cases where their behavior con-
of another to the former's advantage. The difference is one of emphasis: veys inaccurate information. Clearly the former type is of little or no
Dawkins and Krebs conclude that most animal communication has interest in relation to the possibility of conscious deception. Animals
been selected for its effectiveness in manipulating others for the sender's ordinarily have no choice about their body coloring, although in a few
benefit, while other ethologists point out that mutual benefits to both cases, such as chameleons, chromatophores in the skin are under
sender and receiver are widespread, as discussed by Smith (1986). For, nervous control and the animal does change its color to some ex-
in the long run, "cheating" by transmitting inaccurate information tent to match its background and make itself less conspicuous (Winkler
works only if most signaling is reasonably accurate. Otherwise receivers 1968). This behavior seems not to have been studied thoroughly
will be selected to ignore) or even perhaps "see through" the inaccurate, enough, however, to provide much indication of the degree to which it
manipulative signaling, as reviewed by Wiley (1983). The evolutionary might entail conscious thinking. Cryptically colored moths tend to land
significance of honest and dishonest signaling has been extensively dis- selectivell, on surfaces where they will be less conspicuous (Kettlewell
cussed by ethologists, and recently reviewed by Guilford and M. S. 1955, Ketdewell and Conn 1977, Sargent 198I, Partridge 1978), but
Dawkins (I99I). it is difficult to tell from available evidence how much versatility is re-
M*y ethologists and behavioral ecologists have found the approach quired in making these selections of landing places.
espoused by Dawkins and Krebs a congenial one. One reason is that it Some animals make definite effcrts to display pafferns that look like
tends to appear consistent with the "selfish gene" approach to animal dangerous objects, although they have no control over the presence of
behavior, but another possible reason may be that it seems to avoid the these patterns, they do expose them on appropriate occasions. For ex-
need to suppose that communicating animals might consciously mean ample, many species of butterflies and moths have eye spots on the dor-
what they say. This viewpoint has been advanced as a reason to reject sal surfaces of their hind wings which look remarkably like two eyes.
the suggestion that animal communication could serve as an effective These are not visible when the wing is folded, but are suddenly exposed
source of data about animal thoughts or feelings. The fact that animal by spreading the wings when the moth is attacked. Experiments by
signals sometimes convey inaccurate information detrimental to the re- Blest (L957) showed that these starding displays often scare off attack-
ceiver but beneficial to the sender complicates their interpretation, since ing birds. When the scales forming the pattern on a moth's wings were
we must consider that they may be either accurate, inaccurate, or some removed, it spread its wings normally, but the display had a much re-
mixture of tire two. But in either case the signals are expressions of duced effect. Moths without eyespots elicited only about one quarter as
something going on within the sender's nervous system, and they may many escape responses from birds as normal moths. Blest was also able
convey the sender's feelings or thoughts whether these are cooperative to show similar effects when artificial eye-like patterns were presented
or competitive, honest or devious. In fact, deceptive communication to birds along with mealworms. But we know too little to judge how
may be more rather than less likely to require conscious thinking than flcxible and versatile these antipredator displays of moths actually are.
accurate expression of what an animal feels, desires, or believes. More
recently Krebs and Dawkins (1984) have modified and elaborated their
l.'ircfly Communication and Deception
analysis by adding "mind-reading" to their evolutionary analysis of ani-
mal communication, as discussed in chapter I. 'l'hc cxtcnsivc invcstigati<>ns of Lloyd (1986) have revealed that these
This chapter will review several cases where animal communication Irnrrincsccnt l'rcctlcs cr)grlgc in fhntastically complex social communica-
does not appear to convey accurate information, and where thc flexiblc tion rrrctli:rtctl b1, tcrttPor':rl Prtttcr-tts of their self-generated flashes. Nu-
versatility displayed suggcsts conscious thinkirrg on tlrc part ()f .scrrtlcr, r)t('l'()us sPt't.it's ol'lirt'llit's .lt'(' \'('t'\/ sirtrilrrr tnt>rpholttgically, so much so
rcccivcq or b<>th. This sut'ljcct hrrs ['rccrr rcvicwctl irr :t syt111'r115iturr crlitetl tlr.rt t'lrtorrrok,g,ists (.ur ()lt('rr rtk'rrtil\'tlrcrrr n'l()rc rcadily by their flash-
198 ChapterTbn Deception and Manipulatilm lt')<)

ing patterns than from examination of caprured specimens. Of the I30 whether each firefly has a relatively constant pattern but such pattcrns
species Lloyd has studied under natural conditions, the most intriguing vary widely among individuals of the sarne species. There is certainly
patterns have been analyzed in the American genera Photinas and Pho- great variability and complexiry but not enough is yet known to distin-
turis. Male Photinus pyralis typically begin to search for females by emit- guish random variation from systematic and possibly rational, even Ma-
ting a half-second flash about every six seconds while flying near bushes chiavellian, competition. It has been traditional to assume that insects
where females are likely to be perched. A responsive female waits about behave in rigid, stereotyped ways that are genetically predetermined.
two seconds and then emits her own half-second flash. The male turns But recent advances in our understanditg of insect social behavior have
toward her and they exchange similar flashes until he reaches her posi- provided abundant evidence that this view may well be a serious over-
tion, where mating often takes place. Females usually find a mate within simplffication.
a few minutes, and then return to their burrows to lay eggs. Males, on
the other hand, may search for several nights before finding a responsive
female of their own species. Mantis Shrimps
Life is complex and hazardous for male Photinus pyralis fireflies. Their Mantis shrimps of the genus Gonodacrylus are predatory marine cnrsta-
flashes are answered only about half the time by females of their own
ceans equipped with appendages that serve, in different species, as clubs
species. At other times very similar answering flashes come from females
or spears. They occupy cavities and burrows in coral reefs and where
of the larger genus Photuris, which are predatory and may catch and eat
they are protected from predators. They use cavities as ambushes from
males that come too close. Yet the predatory "femmes fatales" actually
which to seize prey, and for mating and egg-rearing. Cavities are essen-
capture only about 10-15 percent of the males that approach them,
tial for survival, and mantis shrimps often fight over them (Caldwell and
suggesting that at close range the male Photinus pyalis can detect differ-
Dingle 1975). Larger animals can usually evict smaller ones from cavi-
ences between the flashes of conspecific females and those of the preda-
ties, but much of this fighting is rirualized posruring and gesturing.
tory Photuris.It is also possible that other information such as species- Although they can seriously damage each other, they seldom do so
specific odors might play a role in these close encounters. Sometimes (Dingle and Caldwell 1969). Experiments by Caldwell (1979., 1984,
the predatory females also fly aggressively towards Potential prey and 1986) with adult G. festai 40 to 47 mm in length demonstrated that
capture some in this way.
they can recognize other individuals of their species by chemical cues.
This sounds complicated enough, but the actual situation is much They avoid empty cavities with the individual odor of a mantis shrimp
more intricately hazardous for the males. Several other species of fire- that has defeated them in a previous encounter, but enter cavities con-
flies are often present flashing in somewhat different Pafterns. And even
taining the odor of one they have bested. M*y encounters involve a
one well studied species such as Photinus pyralis changes its flashing sort of bluffing, and as Caldwell puts it, they are able both to recognize
drastically under some conditions when aggressive mimics are active. other individuals and to remember their "reputations" as fighters.
Sometimes several males approach a female but land far enough away
It used to be taken for granted that individual recognition was im-
that escape is possible if she turns out to be a fcmme fatale. They seem
possible for invertebrate animals, but this relatively complex behavior is
to be probing with their light flashes to determine from her responses typicd of the surprises that have resulted from detailed investigations of
whether she is a conspecific female or a dangerous aggressive mimic. In ethology. Yet Caldwell is also typical of inclusive behaviorists in closing
this situation Lloyd found some indication that males may mimic flash- his review of these ingenious and revealing experiments with the fol-
ing signals of predatory fireflies, as though to deter rivals long enough lowing disclaimer:
to reach a responsive female themselves.
Unfornrnately we do not know enough about the histories and ex- Thc usc of rcptrtation and bluff in stomatopods should not be viewed as con-
periences of individual fireflies to judge how versatile all this communi- sciorrs acts. I{rrthcr, tlrcy :rrc thc product of natural selection operating on prob-
carive interaction actually is. They are not readily raiscd in captivity and etrilitics ol'1x's'liy1slr:urtt' :rrrtl r('slx)nsc. Thc sclcctive equation has balanced over
studied under controlled conditions, so that it is tliilictrlt to tlctcnrtinc nl:lny l-1('n('t'rltiorrs tlrc rosts.rrttl lx'ttclits ()lgcncrating, as well as accepting or
whcthcr thcir t-rchavi<lr varics in rcsl'xrnsc t() ch:rrrgirrg. t it't'ttlttst:ttl('cs, ()r tlistorrrrliltl,,, sr1',rr.rls tlr.rl t,rrrcl.rlc rt'itlr tlrt'llroblblc ()tltconlc of a contest. The
200 Chapter Ten Deception and Manipulation 201

resulting product is further runed by experience and by the degree to which to itself. Because it is vitally important to escape predators announced
information so derived is available and accurate. I hope that by demonstrating by alarm calls, such escape responses are likely to be resistant to habiru-
the occurrence of such supposedly complex mechanisms as rePutation and bluff ation, as Cheney and Sefarth found to be the case in their experiments
in relatively simple animals such as stomatopods, I can suggest the existence of described in chapter 8.
similar processes producing "deceptive" interactions in more sophisticated ani- Other cases of this type have been observed in mammals, birds, and
mah whose sensory and integrative capacities make objective analysis much even ants, as reviewed by Munn (1986a). Most of these instances have
more difficult. (Caldwell 1986, I43)
not been studied in sufficient detail to tell us how consistendy false
This is a prime example of the strong inhibiting effect of inclusive alarms are sounded or to provide very helpful hints as to the likelihood
behaviorism. Adaptiveness is a completely seParate matter from the pos- that this behavior is carried out with conscious intent. Recendy, how-
sibility of conscious thinking. Because mantis shrimp are cmstaceans a ever, Moller (1988) has demonstrated that great tits (Parws rnajor) give
few centimeters in length, it is assumed npriori that they cannot possibly false alarm calls when no danger was threatening to disperse sparrows
be conscious. Even wlien they are shown to engage in moderately com- that were monopolrzing a concentrated food source. When food was
plex and versatile behavior, these data are forced into the procmstean scarce and the tits had to feed at a high rate in winter, they also gave
6ed of mindless automatism. Yet mantis shrimp have well-organized false alarm calls to frighten other birds of the sarne species away from
central nervous systems, and while their neurophysiology has not been restricted and desirable food sources.
it is unlikely to be very different from that of cra1fish,
studied in detail A striking instance ofwhat appears to be complex deceptive behavior
which have all the basic mechanisms of synaptic interactions that are by a hummingbird has been reported by Kamil (1988, 257-58). A male
found in the central nervous systems of all comPlex animals (Bullock Anna's hummingbird named "Spot" because of a white spot on his face
and Horridge 1965, I187-89; Schram 1986). had detected a mist net in his territory because a heary dew had made
The central nervous system of a mantis shrimp is larger than that of a the black threads conspicuous.
bee, and it is well known that honeybees and other social insects display
a variety of versatile behavior patterns, including symbolic colrununica- Spot saw [the net] immediately. He had flown along it, and even perched on it.
Experience had taught us that once a hummingbird has done this, it will never
tion, as discussed in chapter 9. It is quite reasonable to speculate that
fly into the net. . . . Sudderly * intruding hummingbird flies into the territory
mantis shrimps may exPerience very simple conscious fcelings or
. . . and begins to feed. Male Anna's hummingbirds are extraordinarily aggres-
thoughts about the fights by which they gain or lose the cavities that are sive animals. Usually they will utter their squealcy territorial song and fly di-
so important to them and the antagonists whose odors they learn to rectly at the intruder, chasing it out of the territory. But that is not what Spot
...ogrrir" from previous encounters. Perhaps they do no more than feel does. He silently drops from his perch and flies around the perimeter of the
fearful on sensing the odor of a larger shrimp that has defeated them territory staying close to the ground, until he is behind the other bird. Then he
previously. But we have no firm basis for dogmatically denying any sub- gives his song and chases the intruder-directly into the mist net.
iective experience at all when behavioral evidence suggests versatile
aprarion of behavior to challenges that are important to the animal it- Although Yoerg and Kamil (1991) argue against inferring conscious
self. intention in animals, Spot's behavior is certainly suggestive of inten-
tional planning.
In the course of detailed srudies of mixed flocks of neotropical forest
Deceptive Alarm Calls birds, Munn (I986a, I986b) has documented a type of false alarm call-
M*y animals have calls that signal danger from predators, ffid these ing that is highly suggestive of intentional deception. He studied two
sometimes differ according to the type of predator, as in the case of the gr()ups of bircls in thc Amazon basin of Peru that live in permanent
vervet monkeys and domestic chickens discussed in chapter 8. Thc re- rrrixccl-s1'rccics fl<rks, ()r'lc [lr()up is mostly found in the forest canopy,
sponses of animals that hear alarm calls are usually to flee from thc in'r- l5 -45 nrctcrs rltrovc tltc grotrnri, thc othcr in thc understory below 15
mediate arear so that the possibility exists that a sctttlcr lrtight ttsc rtl:trnt n)ctcrs. Wltilc st'r't'r'.tl sl)t't'it's s< xttctirrrcs j<lin thcsc flocks, mated pairs of
calls to frightcn <>thcrs rrway fi<ltn rr placc thc sctttlcr u'otlltl likc to ltrtvc lirttr to tt'rt spt't it's lorttr tlrt'(()r'('ol'tlrc llock lrrrtl rcrrurin witl'r it ntostof
202 Chapter Ten
Decepti.on and Manipulation 203
the time. The understory and canopy flocks may even join together at give the false alarm call as it flew or t after a falling insect
times and occasionally as many as 6O-70 species may be assembled in a that was being
chased byanother bird, but once it became clear ihat
single flock. th. other bird had
caprured the insect, the calling antshrike immediately graded
In the understory flocla one species, the bluish-slate antshrikes itr.ril irrto
a wider-frequgncy nonalarm rattle call, which funcii6ns fike
Thnrnnnrnanes schistogynas tend to lead the others when the flock moves a rallying
call for other birds. The bird apparently realized that the alarm
for distances of more than about 20 meters. They give loud calls which call was
no longer appropriate and switched to the nonalarm call in mid_
seem to help maintain flock cohesion. In the canopy flocks the white- vocalization. Additionally, the fact that both sentinel species
winged shrike-tanagers Lon'i,o versicolor play the sarne role as the lead use the
false alarm calls more frequently when.feedirg fledglingskgti
species. These two species spend more time perched than the others, *gg"r,
and obtain most of their food by flying out to snatch insects off leaves $a| they are 'saving' thii trick for a situatioi i" #rri.fi *,"f ...j.r.r-
ilely desperate for extra food. The behavior of receivers ,.rgg"rri m.,
and from the air; the others spend more time searching for and flushing they recognize that one_potential meaning of the alarm callr"Is
insects from the forest vegetation. The lead species in both canopy and the ap-
proach of a predator. These birds .r" .oI simply startled by
understory flocks also serve as flock sentinels; they are almost always the * alarm
call-rather, often they look in the direction of rfr. call. This reacdon
first or even the only members of the flock to give loud alarm calls when is
especially obvious when birds already in thick cover jerk
they see one of the several hawks of the genera Mirnstur, Accipiter and their heads
quickly and look in the direction of an alarm. This looking impliesthat
Leucoptemls that are serious predators on these insectivorous birds. alarm calls are interpreted as meaning something more like .hawk!,
On hearing these alarm calls the other members of the flock look up, than
like Jump!"'
freeze, dive downward, or move into thick vegetation. This division of Inclusive behaviorists can of course interpret the results of
labor in mixed species flocks seems to be murually advantageous. The Munn,s
observations in terms of natural selection fortehavior that increases
leader-sentinals obtain at least 85 percent of their food from insects the
birds' evolutionary fitness or learned behavior reinforced by r""a.-g",
flushed by other species, and in retLlrn they provide timely warning of the flexible versatility with which false alarming occurs primarily
danger from hawks so that the other birds can spend more time search- under
ap.plopriate conditions suggests that these biids are i.rrenti""luy
ing for edible insects. Typically the sentinel-leaders sit near the center or a"-
ceiving their compedro.s. As in other cases of this sorr, the
beneath a group of actively foraging members of the flock and when an n"o ir,..-
pretations are not nlutuary excrusive. Behavior reinforced
insect is flushed by one of the latter, they fly out and downward in hot by .ith.,
learning or natural selection may also entail conscious intent.
pursuit of the quarry. Since they are faster and more acrobatic fliers they Indeed the
capability of such conscious intention may be an importanr
often catch the insect first. paft of what
is selected or reinforced.
In the course of these multi-bird tumbling and competitive chases of
insect food, the sentinel-leaders often give hawk alarm calls very similar
to those elicited by real hawks. Playbacks of alarm calls recorded either Predator Distraction Displays
on sighting a real hawk or in one of these competitive insect chases when animals are fright"":q by the close approach of a larger crearure
clearly startle other flock members. The sentinel-leaders give alarm calls thcy sometimes exhibit striking forms of bihavior that inv6lu"
significandy less often when they are the only bird chasing an insect ceasing
rnost bodily activity, becoming immobile, or acing as though
than when others are also pursuing it, indicating that the deceptive urary irr:
irrrcd or even dead. The ada[tive fi.rnction of 1n5r, irrstan"c., of such
alarm calling is employed primarily when it is helpfirl in competition for bchavi<>r is unclear, for it is difficult to understand why
a predator about
food, and not whenever insects are being chased. r() c.lt a. animal would bc deterred by its suddenly u".omirrg
Munn (1986a, L74) concludes by intelpreting his observations in immobile
:ritl c-casilrg all cfl.rt.s r().c.scapc. Btrt some of these displays ir. ."-.rt_
terms of possible thinking by the birds involved: "Certain facts suggest .rblc i, rhc tlcgrcc t, wlriclr rlrcy.sinrtrlarc dcath. Burghardt
that some arnount of thinking is involved both in sending and rccciving (199I) dis_
('u.ssc.s rlrc tlclrth sirnrrl;rriorr <,i'trr. rrogn<lscd ,,-,ok."
the alarm call. That the sender thinks about whrt its clll inrplics is sug- lttrtrroaon-'ptrr;
rltiu2s\, rvlrit'lr rvrittr<'s t't'r'.rtit:rrty, tlt.li'-t:rtcs, ts1.1rs ,vcr
-l'ltamnomfin(s srli.rtttt1.vnu.r lrcgrrn and remains
ge.sted by onc occa.si<>n irr wlrich a to tlrli<'t witlr :tlr ()lx'll ttl(,ullt, lolrllrrt'lr.urging out, cvcn blccclipg
at thc
204 Chapter Tbn Deception and Manipulation 205

mouth and without appreciable breathing. This bizarre behavior has Ioung. The displays rhemselves vary widely, but usually involve expos-
typically been viewed as an uncoordinated, instinctive response. But mg consprcuous patterns and moving in atypical ways.
Burghardt reviews old and new evidence that even in this state of appar- . one type of display is called a crouch run; the bird holds its body
ent death, the hognosed snake watches the animal that stimulated it. If close
!9 the ground, lowers its head, and runs in a way that makes it
this animal goes away, the snake recovers, and it remains in the state of resemble a small rodent such as a vole. Sometimes the plover even emits
death simulation longer if a human intruder looks at it. Thus even in an rodentlike squeaks during these crouch runs. Mosi predators that
extreme state of a death-simulating display, the snake monitors the ani- would be likely to.ear plover-eggs or chicks are probabiy also likely to
mal that stimulated it to perform this display. pursue a vole, so that the rodent-like crouch run- seemr iik.ly to divert
Various birds employ a wide range of antipredator behavior, ranging attention from a search for eggs or plover chicks. similar diqplays have
from direct attacks to maneuvers that tend to deflect an intruder's atten- also been observed in a small passerine bird by Rowley (l962i.At times
tion to the bird itself instead of its vulnerable eggs or young, as reviewed plovers threatened by an approaching intruder settle down into a small
by Armstrong (1942) and by McLe an and Rhode s ( 199 I ) . When small depression in the sand as though incubating eggs. Such false incubation
birds attack larger predators they often call loudly, dive at the intruder, may lead a predator to search at the empty depression rather than the
empty on it the contents of the stomach or cloaca and sometimes even actual nest.
strike it with the legs or bill. Such attacks are usually quite effective in Other comnon distraction displays involve postures and movements
driving the intruder away, even against hawks that occasionally rurn on that render the bird conspicuous or cause it to appear injured. The tail
their tormentors and kill them. An especially significant and suggestive may be spread abnormally, one or both wings
-iy u. exiended or even
dragged on the ground as the bird moves ou". an irregular course. In
form of deceptive communication takes place when certain ground-
nesting birds perform elaborate displays that serve to distract predators the extreme form of this display, called the broken wing-clisplay, the bird
that might otherwise destroy their eggs or young. Plovers and sand- falls over and flops about as though badly injured, p.rt rpi with a bro-
pipers typically lay their eggs in simple nests on the ground where they k5n wlng.- It looks just like a bird that has been wingedby a hunrer,s
are especially r,ulnerable to predation. Their many and varied types of shot. Predators are especially alert for signs of weak]r.r, o, injury in
antipredator behavior, reviewed by Gochfeld (f984), include maneu- potential. prey, and these displays musr make the bird appear .rp..ir[y
vers that are more complex and devious than direct attacks. Although ,uulnerable.
their eggs are cryptically colored and resemble the substrate on which The customary explanation of these distraction displays has been that
they are laid, many plovers and sandpipers respond to intruders with the bird is in severe conflict behavior, being motivated both to flee and
specialized distraction displays. t() attack, with the result that it is thrown into a state bordering on an
The most striking type of predator distraction behavior is displayed rrrrcoordinated conr,.ulsion (Skutch L954; Simmons 1955; Anistrong
by several species of small plovers, such as the Nonh American killdeer 1949). The strong influence of inclusive behaviorism has led most or-
(Cbnradrius vociferws), piping plover (C. rnelodas), and Wilson's plover ,ithologists and ethologists to deny emphatically that a bird might in-
(C. wilsonla). Killdeer typically nest in open fields, and the piping and tcntionally anempt to deceive a predator and lead it away fr6m its
Wilson's plovers lay their eggs on sandy beaches. The nest itself is little \'oung. For example, Armstrong (1949, 179) asserted that i.it i, ludi-
more than a shallow depression. When a larger animal approaches the (rl)Lrs to suppose that injuly-simulation arose through birds deciding
nest of a plover, one conunon response is for the incubating bird to thc trick was worrh trying." Although Armstrorrg *.i speaking of evo-
stand up and walk slowly away from the nest for a few meters. Then it Itrtionary origins, he and other ornithologists seem equally ceiain that
may begin calling, in the case of the piping plover a plaintive peeping t hc t'rirtls cl<> trot individually display with the intention
of leading the
that has given the bird its name. Often the parent bird then walks or lrrctlltor ewe-y. ()nc rcas<)n t() qucstion whether the displaying birJs are
flies closer to the approaching intruder and begins a conspicuous dis- t'rrrsciousll, trvirrg to lcrrd rr Prci'l:rtor awav is the fact that th.y,o*.-
play. This behavior contrasts with the ordinary behavior of flying di- tirrrcs t'ontirrtrc rlispl.rvirrg cvcrr rrltcr it h:rs killcd thcir young, as de-
rectly away from a frightening intmdcr whcn thc lrirrl hls n<> cggs ()r st rilrt'tl lrv l)r'it'slt'irt :tntl llt'rrnt'l t (l()79\.. Such contirruati.r,-t ,if
Deception and Manipulation 207
206 ChapterTen
convulsions is that the bird frequendy looks at the intruder. Even when
tion d.isptay after the predator has taken the egg: ol young may indicate
moving away it repeatedly turns its head and looks back. During
that the bird is not ionsciously intending to lead the predator away. broken-wing or other distraction displays the plover does not ordinarily
Although obviously not completely rational,-this continuation of the stay in one spot but moves slowly and somewhat erratically over the
displayinay be comparable to other emotional expressions that are car-
ground. If the intruder does not follow, the bird typically stops display-
ried on aftir they can no longer achieve a desired effect.
ing and moves to a different position where it repeats the display, often
Broken wing displays provide an especially suitable situation where
with increased vigor. Significant indications of intentional, rather than
new observations and experiments can throw some light on the possi-
chaotic or unplanned, displaying also resulted from Ristau's analysis of
biliry that the birds are atting intentionally. Not that any evidence yet the spatial relations benveen the intruder, the nest or yomg, and the
coni.mplated can settle r,r.li a question conclusively; brrt certain fea- displaying bird. If the displays result from a simple mixture of motiva-
rures of th. birds behavior strengthen the plausibiliry of inferring con-
tion to attack and to flee, one would expect the parent bird to approach
scious intent. Such an analysis has been carried out by Ristau (1983a,
the intruder, then withdraw, and perhaps approach and withdraw alter-
I983b, 1983c, and 1991) with piping plovers and Wilson's plovers nately as one or the other motivation carne to predominate. But there
nesdng on beaches in Virginia and Long-Island. Almost all data that are
would be no reason to expect that the location of the nest would play
available about the details of predator distraction displays have so far
any signfficant role in such movements, except that, having come from
come from encounters with human intruders, because it is only rarely
somewhere near the nest, a plover that simply approached the intruder
possible to observe natural encounters between plovers and mammalian
and then withdrew would often move back toward the nest.
predators. The few observations that have been rePorted indicate that
Intruders are ordinarily detected at a considerable distance, and the
th. pr"dator distraction displays in response-to natural predators are parent bird usually walks slowly and inconspicuously away from its nest
very similar to those elicited by human intruders who approach a nest
before flying fairly close to the intruder while it is still many meters from
where plovers are incubating eggs or areas where young chicks are Pres-
the eggs or young. As the intruder comes close, the displrying plover
ent. Aimsrrong (1942, tl-9t) reviewed several observations of an ot-
moves a bit faster, and although appearing crippled and easy to catch, it
rer, foxes, *.ri. k, dogs, and cats being led away from younq bild: Uy
always manages to stay just out of reach. On one occasion a displaying
p"i.rr,, acting as though iniurgd. Sullivan (1979) observed a black bear Wilson's plover led me along a beach for about 300 meters with almost
being success-firlly tured away by a blue grouse hen. Pedersen and Steen
constant displays.
(f98"5) arralyzrd, the effectiveness of predator distraction displays of When fustau mapped where the intruder would have been led if it
ptr.-ig*. And Brunton (1990) observed that distracdon displays of firllowed the plover throughout its broken-wing displays, she found
i.i[d".i*.re almost always effective in leading potential predators away that in 44 out of 45 cases the intruder was led away from the nest. Since
from eggs or chicks. rhe displays began at positions that varied widely with respect to the
Sonlira (1988) has recently described direct observations of foxes line connecting the nest with the initial position of the intruder, some
that apparently "saw through" the injury-srmulating displays of grouse r()utes might be expected to lead initially a litde closer to the nest before
*d ..rp"nded by searching the immediate vicinity-for grouse chicl<s corrtinuing off in a quite different direction. But in only 39 of the 45
rather tiran following the &splaying adult. He develoPs a theory that ('ilscs would an intruder have moved closer to the nest at any time while
when small -^-*Jprey is abundant, young foxes do not learn that it was following the displaying bird.
distraction displays mean young birds nearby, but that in years when Anothcr indication of something other than mechanical and random
small mammali ,."r..,-fbxei are more likely to learn that such dis-
".. lkrpping ab<>ut in chaotic conflict behavior is the degree to which plov-
plays are a sign of available prey in the vicinity. Thus there may well be ('r's urc sclcctivc abotrt which intruders will elicit full-blown displays.
i of cofrritive interaction benveen parent birds and predators by l'lrcy hrrbitr,r:rtc to fhrrriliar pcoplc, cspccially on heavily visited beaches.
which disuaition displays are reduced or eliminated in situations where Skrrtclr (1976);urtl Ann.str()ng (1949, 1956) both observed that when
the predators are clever inoughto interpret them. as signs of cdiblc cggs t:rttlt' or otlrt'r' lrrxrlt'rl :tttirtt.rls :rl)l)r1r:rt'h thcir ncst, instcad of behaving
.r..^hi.kt nearby rathcr than an iniured bird w<>rth prrrsrrirrg' ,rs tltorrglr irrjurcrl, plt)\'('r':i riornt'titttt's st:urtl rrp c<>rrs1'ricrr<usly, closc to
Onc indicati<ln that thcsc clisplays Arc s()tll('lltirrg, otltt'r tlt:tlt ch:rotic
208 CbapterTen Deception and Manipulation 2Og
the nest with spread wings, and may actually fly direcdy at an approach- and carrying out distraction displays, which may be wasted
effcrt at
ing cow This is sensible behavior, because the danger from cattle is not best, or under adverse weather ctnditions may lower
the chances that
that they will eat the eggs but that they may step on them. the eggs will develop normally.
Ristau (1991) carried out systematic experiments to analyze this se-
lectivity of response to different kinds of intruder by having human in-
Deceptive Behavior of Monkeys and Apes
truders behave in two clearly different ways towards an incubating
plover. One category, termed "dangerous" intruders, walked to within Several other examples of deceptive or manipulative communication
two meters or less of the nest, looked about, and acted as though search- described in the book edited by Mitcheu ana Thompso" lrqgJi. or
ing. They must have appeared to the parents as more likely to destroy particular interest is an illustrated Fnglish translation of thl
paplr by
the eggs than others, designated "safe" intruders, who walked past the Ruppell describing deceptive use of uiararm call by a mother
nest tangentially but did not approach closer than 12 to 32 meters. The whose y""lg *:re snatching foo{ and kept the mother away
i*i. ro*
by rri.,.t-
two categories of human intruders dressed as distinctively as possible. ing.at her. Elephants (chapler ll) and dogr (chapter 12)'show
Both before and after being exposed to one to four such dangerous and evidence of deceptive behavior, although it"is u.ry difficuit
to be sure
safe approaches the plovers were tested by having the previously safe how much conscious intent is involvel. witt, ,pir, however, the
and dangerous intruders walk past at a constant, moderate distance. crunstantial evidence of conscious deception is considerably
stronger, as
In 25 out of 31 tests the plovers reacted more strongly to the intruder described in detail by. Miles- (chapter 15) for an orangutan
who had
who had previously acted dangerously than to the one who had played been trained to use a.simple foragf sign language, and"especialry
by de
the "safe" role. Stronger responses entailed looking up or moving away waal (chapter 14 and de waal L9g2),*hor. ior,[.r., r*di., oflaptive
from the nest at a greater distance, staying offthe nest longer, and per- chimpanzees documented nurnerous cases of deieptive behavior.
forming more active displays. In three of the remaining six experiments cially revealing were de waal's observations of suLordinate
males who
there was no appreciable difference. In the other three cases the re- sought, and sometimes obtained, sexual inrercourse with adult
sponse was the opposite of what would be expected if the birds had females, but only when the more dominant adult males
did not see them
learned which person was the more likely to threaten the nest, that is, cooulating. Both Paftners in these surreptitious liaisons acted.
the response was stronger to the safe intruder than to the one who had and seemed clearly to be keeping out of iight of the dominant
males. If
behaved dangerously. Thus in the great majority of these tests the plov- discovered in the act of close sexual advan"ces, such a subordinate
ers learned in the course of a fcw exposures to safe and dangerous in- hastily covered his erect penis with his hands. This is in effect
truders which one posed the greater threat and called for the more vig- noncommunication.
orous resPonse. B_yrne and whiten (1988), whiten and Byrne (l9gg),
and whiten
In other experiments Ristau had human intruders either look at the (1991) have reviewed published descriptioni of .pp.."rrtly
nest or turn their heads artd gaze in the opposite direction as they lrchavior in many species ofprimat"r, *h they have *gg.rt.d
ho# thi,
walked past at a moderate distance. Again, the plovers reacted more subject can be
-gr." adequaiely studied in thl fur,rr..They emphasize
strongly to the distinctively dressed persons who were looking direcdy the-degree to which even experienced primatologists have
been inhib_
at their nests than to those that looked the other way. All these observa- ircd, or even embarrassed, a6out ..po.tirrg beharlor that sugge*,
tions and experiments indicate rather strongly that plovers learn quickly scions deception. The review by white, irra Byrne is
folloild by nu_
which types of intruder are dangerous and respond more strongly to rltcrous comlnentaries from other scientists and scholars,
some of*hose
them than to others that have previously behaved in a less threatening t'riticisms clcmonstrate how strongly the residual influence
of behavior-
manner. Byrkjedal (1991) has concluded that conflict of motivations is isnr still linrits acccPtancc of overwhelming circumstantial
evidence that
not an adequate explanation ofnest-protection behavior in golden plov- Prilttrttcs arc tlrritc t'rrp:rl'rlc of what Whiten and Byrne call ..tactical de-
ers. They and other birds performing predator clistraction displays may t't'P1i1111." Yct ilr tlrcir rt'ply t() c()n)n)cr)t.s ()r'l thcir
paper they deny that
well be thinking in simple rational tcrnrs atrorrt lr:rlrrrrcirrg thc risks of lltt'1' 11,'. ('()t)('ct'ttc(l rvitlr tlrc "plrcrrorrrcrr:rl w<>rltlsi ,if th. animals
nest prcdation against thc cftilrt rurd risks irrvolvt'tl irr lt':tvittg thc ttcst \t lt(l\,.'I'lrt' bclr:tviol'ist it t.rlrrxr still litrgr.r.s on.
2lO Chapter Ten

on balance, it seems clear that on many occasions animals coEunu-

nicate inaccurate information or intentionally woid conveying certain
rypes of information to others (cheney and- s-eyfafth 1988, I990a,
rggou, I99I). In many cases the versatitity of deceptive or misleadi.g
behavior provides even more suggestive evidence of conscious intent
Aprt a,nd Dofuhirus
than the transmission of t.rtotttbly accurate information' Although
is difficult to liken such deceptive communication to involuntary
of pain, the deceptive tacticJ o!1onk9ys inconsistent. For ex-
T.e 9ften
,..ipt. Cheney *d s.yf"rrh (1990a) describe hoy a veryet monkey may
.#, t leopari alarm.rtt drrtit g a territorial confrontation with a neigh-
boring ,toop. This causes the oppott.t ts to flee, but the caller may move he Great Apes and the whales and dolphins engage in so much
irrto fi. op.n himself, .ontr"ry io normal, prudenl behavior when a real
versatile behavior that whole books would be required for each group
predator is approaching. Intentionally deceptive behavior may thus
the task of ascertaining whether it to document the evidence that suggests conscious thinking. I will there-
!*..ot.d i".ptly, which"complicates
fore select only a few of the most striking examples, with emphasis on
results from conscious Planning.
communicative behavior that provides compelling evidence about what
these animals are thinking and feeling.
The world's largest brains are found in cetacean and not human
skulls, and the toothed whales or dolphins have brains that are roughly
comparable in size and complexity to our own, although Morgane, ]a-
cobs, and Galaburda (1986) point out that the large cerebral cortex of
the cetaceans lacks some of the organizational complexities of the pri-
mate cortex. Furthermore these marine mammals produce a wide va-
riety of sounds, and engage in complex and versatile behavior, both
when trained in captivity and spontaneously under natural conditions.
lt is as counterintuitive to deny that they think consciously about some
of their activities as it would be to advance such an absurd claim about
the Great Apes. One of the best examples of mental versatility displayed
by captive dolphins is imitation of both sounds and actions. For ex-
rrmple, Herman (1980, 402) summarizes observations by Thyler and
Saayman (1973) of a botde-nosed dolphin (Tursi.ops trancatus) who im-
itated the behavior of a seal, rurtles, skates, penguins, and human divers
in its aquarium, employing behavior patterns not seen in this or other
tlolphins under other circumstances :

'l'hc bchaviors imitated included the seal's swimming movements, sleeping

l)()strtrc, antl conrfi>rt rl()vcmcnts (self-grooming). The dolphin, like the seal, at
tinrcs sw:rnr lry sculling with its flippcrs while holding the tail stationary. The
slccpirrli p()sturc inritltetl w:rs lying ()n ()nc siclc at the surface of the water,
('xtcn(linl-l tlrt'llippcrs, rrrrrl tryirrg to lili thc lhrkcs clcar <if thc water. The com-
l()tt trx)v('rrrcrrt rrrirrrr,kt',1 rr'.rs vi1,,,trrrrts rrrhhinli of'thc [rclly with thc undcr
srrrl.rt'r'ol onc or lxrtlr llrpl'r'rs ArLlttiort.tl irttit.rtivc lrcltlviors lry this dol-

Apes andDolphins 213
2L2 ChnPter Elcven
of turdes, skates, and for echolocation and longer duration sounds, usually of lower fre-
phin included the swimming characteristics and Posntres
attempted to remove algae from an underwater quency, by which they communicate; and they can be trained to imitate
il*in;. The dolphin a]sJ. a hymal diver a wide variety of whistle-like sounds (fuchards, Wolz, and Herman
window with a sea'gull feather, in imitation of the activity 9f
the window. The dolphin, while."cleaning" the window, 1984). They often produce a medley of sounds when engaged in social
*fro ..gurarly cteane?
valve of the
,.po*"laty pioduced sounds resembling d".t:.fro3 the demand interactions, but the physical properties of underwater sounds make it
6f brrbbl.t in apparent imitation of the extremely difficult to determine which sounds come from a particular
d.iirer,s ,.grrlr,o, and emitted a stream
dolphin using
.*pt[!d by the i"'' nan also.observed a a
Tayler and Saal, animal when they are close to one another. This is because underwater
pi...lr uroken tile .o ,.rrp. seaweed from the tank bottom, a behavior appar-
sounds have much greater wavelengths than the same frequencies in air,
'ently derived from observing a diver cleaning thegnk with a vacutun hose' The
dolphin' and they are affenuated scarcely at all over distances of several meters
,.r"pi.,g behavior of this aJtpnm was then copied by a second while being strongly reflected from most surfaces they encounter, in-
also describes spontaneous observational learn- cluding the air-water interface. The sounds emitted by most terrestrial
Herman (1980, 406)'large
ing by dolphins in the tanks wheie ,h.y trained to perficrm a animals are audible to human ears, and a listener can usually judge the
to entertaln
sPectators: direction from which they arrive with considerable ease and accuracy.
u"ii.ty of complex gymnastics
But underwater sounds cannot be localized nearly so well, even when
In some cases., the animals may even train themselves. In one interesting to converted to airborne sounds by hydrophones connected to earphones,
.pir"a. iuustrating self-training, 9ne animal of the grouP had been taught primarily because multiple reflections are often at least as intense as the
leap to srrrpe.rd".d ball, gr.ip it with its teeth, and pull it some distance
" sound waves arriving directly from the source .
thlough the wate, in ori.ito raise an attached flag' This
animal was subse-
was trained One important type of sound emitted by dolphins is the so-called
[".",iy removed from the show and a second animal in the group
flag by striking repeatedly at the ball signature whistle, a frequency and amplirude modulated sound that is
in the same task, but learned to raise the
by pulling it. This second animal, a female, subse- characteristic of each individual. These were studied in detail by Cald-
with its snout rather than
and another female of lhe grouP immediately took over the per- well and Caldwell (1965, 1968, L97L,1973,1979) and Caldwell, Cald-
;";"dy died ball with the snout' well, and Tyack (1990). The Caldwells were obliged to record them
for-*.., without training, and, continued to strike at the during a rwo-day
Later when this new femal"e refused to participate in the show primarily from dolphins that were isolated out of the water, because of
in the grolp. immediitely performed the behavior, but the difficulties of separating sounds from various sources underwater.
period, a young male
*a piU.a the ball i"i.rt-rrit teeth, in the manner of the originally
But it was nevertheless clear that more than 90 percent of the whisdes
trained animal' were specific to the particular dolphin, and could easily be distinguished
companions from the signature whistles of other dolphins. Tyack (1986) has devel-
During the several days when these dolphins watched their oped a small and harmless device that can be attached to a dolphin's skin
and, iriso doing, learned the novel t.qr.tt.. of actions, they must have
by a suction cup and picks up that animal's sounds much more strongly
thought about these specialized- behavior Pafferns'
than those of others in an aquarium tank. This has enabled him to dis-
Pr"yor, Haag, ,nd o'R.itly (1969) andPryor (1975) describe how a
perfiorm a tinguish signature whistles from two animals, Spray and Scotty, that
captive roughltoothed dolpiin lsttno bred'anensls) learnedto
fbod, another sort of enterprising had lir,,ed together in the sarne tank for about seven years. Two types of
new trick.,i.ry day in ordei to obtain
some conscious rvhistle predominated in their vocal exchanges, and each type was pro-
behavior th.t ,..ms likely to have required at least cltrced primarily, but not exclusively, by one of the two animals. Spray
Reilly (1989) tiave.demonstrated that pigeons
,t int irrg. MacPhail and
can lea."n to discriminate between novel and familiar stimuli, but creat- lrrodtrced 73 percent of one whisde type, while Scony emitted 74 per-
task' ccnt of the other type . Tyack suggests that perhaps the whistles of the
,"j and moderately complex actions is a more demanding
""r.rfurther experimlnt, .omp"rable ,?..1rot. of Pryor et it is
al. othr:r aninral's characteristic pattern resulted from imitation. It is even
n"nairrg possit'rlc tlurt thcsc two clolprhins were calling the other by name. But
difficulito judge wh"th"r other animals could learn to do this' nruclr ltltlitionul cvitlcncc woukl bc nccdcd to demonstrate that such
Thebottle-.or.d dolphin is the most commt>nly trainc'd pcrfirrnrcr rrsc ol'rvltistlcs .rs tltt' t'tlrrir':rlcttt ol-rt:rrrtc.s w:ls :rcttrally occurring.
t'y scictrtists'
in oceanaria, and it has air., bcc,-t snrcliccl n)()st tlr.rtltrg5ly l'ryor' :uttl Stlt.tlk'rtlrt'r'gt'r' (l()()l) lr.rr,c :tls<l dcscribctl how ;lclagic
tr:lins ttsctl
Thcse ancl <>t6cr 4<llphins crnit u vlricty ol-sotrtttls, lxrtlt
Apes andDolphins 215
214 ChaPter Elewn
Fferman (1986, 1987) and his colleagues have approached the ques-
spotted dolphins (Stenella attenuata) have learned about th9 purse tion of dolphin cognition by * intensive training program designed to
seines used ro ,or-*d and caPture runa in the tropical
Pacific' The
assess the degree to which they can understand not only individual sig-
tuna tend to stay below schoois of dolphins, which therefore afi
nals but combinations of signals that are related to one another in a
markers for the presence of the tuna. These dolphins of the oPen
manner resembling the grammatical rules of English. This emphasis
do not ordinarily encounter any large solid objects, and when this rype stems from the widespread conviction that combinatorial productivity
ornrrr-g was initiated, hund.r"a. p*i.ked and became entangled in the based on the use of rule-governed combinations ofwords constitutes an
nets. But in recent years they have learned to remain far{y quiet
essential feature of human language. Herman's experiments concen-
wait until the crew maneuvers to lower a small portion of the net and
trated on comprehension or receptive competence of dolphins rather
allow them to escaPe. Shortty after escaping fronlthe net the dolphins
than on their ability to produce coffrrnunicative signals. He trained one
often leap repeatediy into the air, as though in.ioyful celebration. female bottle-nosed dolphin, Akeakamai (or Ake), to respond to ges-
The behavior oi th. dolphins strongly indicates that they have tures from a trainer at the edge of the tank, and another, named Phoe-
do when
learned a great deal about thehshing vessels and about what to nix, was trained to respond to underwater whisde-like sounds. Both
Experienced fisher-
.nrr.a by"speedboats and ,ur.oorrd.d by,the net. dolphins learned vocabularies of about thirty-five signals, which in-
men beliir" th"t dolphins recognize the fishing vessels from a consider-
the sur- cluded the names of objects in the tank and actions such as toss, swim
able distance, and th"t ot seeing one they often rest quietly at under, j.r-p over, fetch, and put something in or on top of something
face without conspicuous blowing. If the ship approl+.t, they may
else. There were also a few modifiers such as right and left, surface and
swim rapidly in #apparent effortio keep on.its right side; presumably
bottom. A typical combination of signals was RrcHT prpE TArL-ToucH,
b..ror.^th.y h",u. leained that the cranes and other machinery used to meaning that the dolphin should touch the floating pipe to her right
handle the nets are usually on the left side. But the tuna fishermen with her tail.
ploy speedboats ro chase and herd the dolphins into a position where
Both Ake and Phoenix learned to respond appropriately to muner-
fur.jr.'"" be surrounded by the net, which may be as much as a mile in ous combinations of these commands, which could be as complex as
length. five-unit sequences such as pr,ACE BorroM prpE rN suRrACE Hoop,
Another sort of versatile behavior of dolphins that suggests con- where pr"acE rN is a single command. This much was not especially
sick or injured'
scious thinking is their aiding of other dolphins that are novel, as many dolphins have been trained to carry out sequences of
it been observed in detail in several
This is relativJly uncorrrmorlbrrt has
behavior of greater complexity. But in their training, these rwo dolphins
of the kind occurs occasionally under
captive grorrpr, and something were never presented with more than a small proportion of the possible
natural conditions. Aid.ing behivior is not limited to d9l.nh1t, *l clear
and meaningfi.rl combinations of commands; the others were reserved
by Rasa (1976,
.**pt., in the dwarf -6rrg99re have been described
for tests of their comprehension of the rules that governed the combi-
1983). The instances of dotlphins aiding h*P swimmers presumably nations. These rules were similar to those of English, in that the order
sinks below
result from similar behavior. If a dolphin is visibly weak and of the words or corlrnands determined which would be the direct or
the surface, its companions may swim down and push it.from below,
indirect object, and which modifier applied to a particular narne. After
lifting it to the surface so that it can breathe air. The dolphins are
ar much the dolphins were responding quite well to these sequential combina-
what selective in this behavior; females and young
"idirrg left tions, they were presented with new combinations that they had never
;;r. [kely to be assisted in Ihis w"y, are sometimes
T9 "d..-1es carries this aiding rcceived before.
at the bottom of the tank. Occasionrlly dolphin
" babl Phoenix responded correcdy to 7L to 87 percent of the rwo- and
behavior to extremes, such as a mother who carried her stillborn thrcc-clement combinations, diminishing to 60-68 percent for three-
to or the botde-nosed dolphin
fo. d.y, until it had begul decomPose,
to-(ivc-"wr)rd" scrics; and Akc averaged 65 percent correct on all the
that carried a dead shar'k for eight dJys without stoPPing to
eat' Some
cvcn t'orrrbirurtions, tloing rrtxlrrt rrs wcll (74 percent correct) on two- and
conscious thoughts seem likely to accomPany this aiding bchavi6r, (ivc-clcrncrlr c()ntl)iruttiotts ;urtl lcss wcll (56-65 percent correct) on
when the effort is misguided'
216 Chapter Elewn
Apes and Dolphins 217
two-) three-, and four-unit combinations. The overall success of these
rwo dolphins on 405 novel "sentences" was 66 percent correct. While . The great emphasis on syntactical rules as a fund,amental property of
language has been annunciated primarily by scientists and icholars
66 percent correct may not seem very close to perfection, it should be whose native language English, one of the few human languages
realized that the chance score was very low indeed, since there were a .is
where word order provides almost all of the syntax. But in mo-st lan-
very large number of possible actions among which the dolphins had to guages inflection of words is used to convey the grammatical relation-
choose. Thus these nvo dolphins had clearly learned not only the mean-
ings of the individual commands but the sequence rules governing $ips between them, and English does retain a fewluestiges of inflection,
for example the possessive iorm of nouns and the diherent forms of
which was direct and which was indirect object, ild which modifier pronouns such as "her" "hisr" and "him." The fact that so many human
applied to a given object narne. languages rely heavily or primarily on inflection ofwords ,o.oru.y
Schusterman and Krieger (1984) trained rwo sea lions (Zalophus cal- tax suggests that inflection may be a more basic and, perhrpr, ,'rnor.
ifornianus) to respond correctly to 64 and I90 gestural signs displayed easily utilized w.al ro express grammatical relationships. If so, ,*.-pr.
by human trainers. Schusterman and Gisiner (I988a, I988b, 1989) to teach a combinatorially. productive languag. to .rri-als might be
have trained sea lions to comprehend combinations of commands- more successful if they employed inflection iattr.r than word ordJ..
demonstrating that this ability does not require the brain volume of Fouts (1989) has found by- analyzing videotapes of signing chimpan-
dolphins or Great Apes. But they and also Premack (1986) deny that they sometimes "afilbcr th-e meaning oi a sign"by riodulating
this ability to learn combinatorial rules is remotely equivalent to the it." This has entailed gesturing and gazing ai objecti of interest while
versatility of human language. They point out that understanding the also signing about them. But it is possibl. th.t apes might modify the
following two rules would appear sufficient to account for the perficrm- sign itself in ways that would indicite whether it ii meanl to denote the
ance of both F{erman's dolphins and their sea lions (1988a, 346): direct or indirect object, for example. The customary eflbrts to train
t. If an object is designated by one) two, or three signs (an object sign apes to standardize their-signs would probably discourage such inflec-
and up to rwo modifiers), then perficrm the designated action to that tion, unless it were specifically encouraged. Thi Gardner(l9g9b) have
object. indeed observed that their chimpanz..Jdo modulate the signs they have
2. If two objects are designated (again, by one to three signs each) and learned and convey additional meaning by dorng so. weLay p.rhup,
the action is rnrcH, then take the second designated object to the anticipate that in furure.investigations the possibfity of inflectior,"l ry.r-
first. tax will be analyzed explicidy.
A more fundamental distinction between human language and what
Comprehension of these rules would seem to require some signifi- dolphins and sea lions have accomplished, at least so f..ir fie ability to
cant thinking, as discussed by Herman (1988). Of course this compre- switch back and forth between comprehension and production of .o*-
hension of both individual commands and the meaning conveyed by municative signals. This is obviously a key attribute of hr** language,
their sequential relationships falls far short of the rich versatility of hu- and is ability that has been attained-at least by Kanzi ,-oig tt .
man language. But these dolphins and sea lions have learned to compre- .an
(ireat Apes, as described below. But experiments with marirr.
hend rule-governed combinations of word-like signals. While human have not yet even attempted to test whether or not they can learn
languages obviously involve far more than two rules, this is the first comprehend and produce signals interchangeably, and therefore this
demonstration that animals can comprehend nny syntactical rules at all. rluestion must remain open. obviously dorphins and sea lions cannot
In short, two is significantly greater than zero. Furthermore, if dolphins lrc cxpected to produce human gestures; bui phoenix, who learned
and sea lions think in terms of these rules, they must be capable of think- cr>mprehend the rules relating commands presented to her as under-
ing in correspondingly complex terms about the relationships berween w:rtcr sotrnds, could almost certainly learn to i-itrt" those sounds. Ap-
signals and the actions or objects for which they stand. It woulcl bc Pn4rriatc cx1'rcl-iltrctrts with Pl'rocnix or other dolphins or sea lions sim-
unwise to allow our preoccupation with thc qtrantitativcly uniquc cil- il.rrly trrtirtctl t() ('()t)ltt'ttttticrttc ['ry souncls might riveal whether they are
pabilities of human lanp;uage to obscurc thc fhct tlr:rt tlrcsc cxpcrirncnts t':tPeble r.rt'ttsilrg il('(.)ltsli.' sign,rls irrrcrcharrg'cably in both the receitive
rcvcal at lcast part of what tltc rlolphins wcrc tlrinkirrg. ;llttl ptr rtlttt'l iyt' ttr,tl.s
218 Chapter Elmen Apes andDolphins ZLg

Pldy by demonstration-use of the sign by t-rer trainers in the presence

Ape Language of the object or acriviry for which the iign itood-and partly by mold-
One of the most exciting advances in cognitive ethology was achieved ing,- a procedure in which a trainer ,"o.rld gently hold her hands and
by B. T and R. A. Gardner at the University of Nevada (1969,I97L, guide them through_ the appropriate motions. In three years she learned
1984, I989a, 1989b) when they succeeded in training a young female t^o u:e a1{
lespond appropriately to eighty-five signs (Gardner and
chimpanzee named Washoe to use more than a hundred signs derived G.ardner I97L). subsequ.ldy several other chimpanzees and a few go-
from American Sign Language (ASL). These signs are gestures devel- rillas and orangutans have been taught to use signs derived from ASt,
oped for communication by the deaf. Based on English, it is one of and vocabularies of over a hundred iigns have bEen achieved by several
several sign languages for the deaf adapted for manual gesturing. The of these animals, as revie_wed by fusiau and Robbins (19g2), and by
Gardners based their plans for this ambitious aftempt to teach a gestural Gardner, Gardner, and van cantfort (1989). scarcely'any behavioral
language to a chimpanzee on three previous investigations, among oth- scientists expected that Yerke s' l92s prediction would ev.i b. so abun-
ers: (I) the extensive studies of the Great Apes by R. M. and A. W dantly frrlfilled.
Yerkes (L925,1929); (2) the detailed observations of natural corrunu- . The implications of the discovery that chimpanzees and other Great
nication between chimpanzees described by )ane Goodall (1968, Apes could communicate in even a rudiment..y fo.- of language were
1986); and (3) the almost totally unsuccessfirl attempts by the Kelloggs truly shattering q. deep-seated faith in language as *i[r.itunan
l" " a heated se-
(1933) and the Hayes (l95la, I95lb) to train chimpanzees to use spo- attribute separating humanity from the beasts. As a result,
ken words, partly at least because their larynx is anatomically unsuited ries of controversies continues to rage over the degree io which the
for producing the sounds of human speech. communicative behavior learned by apes is acruaily a simple form of
Yerkes (1925, 179-80) had suggested that chimpanzees might be
l*go1g... Y*y criticisms of the earlier experiments with apes have
able to learn a gesrural communication system. His and many other been significantly constructive, and have led to a sharpening of scientific
studies involving both laboratory experiments and the home rearing of understanding language and its acquisitibn by*young chil-
young chimpanzees by the Kelloggs and the Hayes had abundantly dren. have
"falso. 1"1 ,". improved and bette, .orrtroiled invEstiga-
tions of the communicative behavior of the apes, and these in rurn have
demonstrated that our closest nonhuman relatives can learn nurnerous
complex discriminations. Under natural conditions some populations served to overcome many of the criticisms bf tft. earlier srudies. On
of chimpanzees use simple tools, and in laboratory studies they can balance, it now seems clear that apes have learned to communicate
learn to use many human tools. Similar use of human tools by orangu- simple thoughts.
tans has been described in detail by Lethmate (L977). They communi- Anticipating the appropriare concern that the signing apes were nor
cate with each other by sounds and simple gestures; and captive apes, really communicating-lingrristically, the Gardn.r, "r.qriir.d th"t quite
like many other birds and mammals, learn to recognize simple spoken stringent criteria be satisfied before they accepted a sign as reliably used
commands. But until the Gardners'work with Washoe, chimpanzees by washoe. It had to have been "reporred by three d.iFerent human ob-
had seemed almost totally incapable of anything even suggestive of lin- as having occurred.in an appropriate context and spontaneously
(that is, with no__prompdng oth& than a [signed] queition such as
guistic communication. The intensive and at times heatedly controver-
sial investigations that have followed in the footsteps of the Gardners 'what is it|'or'wha_t do you wantl') . . . each d"y ou.. a period of 15
(and Washoe) are reviewed in detail by Savage-Rumbaugh (1986) *d consecutive day_s" (Gardner and Gardner L969)'. In latei vocabulary
in the volumes edited by Heltne and Marquardt (1989) and by Parker tcsts, pictures of objects for which the chimpanzee had learned to AsL
and Gibson (1990). sigtr werc projected on a screen visible to her but not to either of nvo
Washoe was acquired by the Gardners at about one year of age , and .bscrvcrs who did not know what picture was shown. one observer was
she was cared for by friendly and familiar people who communicated irr thc sanlc r()()r'r'r, and if thc chimpanzee did not sign spontaneously
exclusively in American Sign Language whcn shc was prcscnt. Thcy Yl]-.-t,
thc plq1111'c wils lrnrjccrcd on thc screen, she sifned the question
signed to her about things likely to intercst hcr, rntrch rrs ltutnan percnts "Wllrtt is itf" ()t's()!tl('ctlrriv:rlcrrt.'l'hc othcr obscrver watched from a
talk t<l thcir l'rabics. Wash<lc wrs tuugltt sintplt' \'t'r'siorrs ol'A.SL sigrrs, sr'[r;t1;1t1'r'(x,ilt tlrrrrul,,lr.r ()n(.rr,.r1,gl:rss wiptl<lw. I]<lth gbscrvcrs noted
220 Chapter Eleven Apes andDolphins 221

what sign they judged the ape to have produced, but they could not of the training. Afrer this was accomplished, Ally was shown the objects
communicate or influence each other's reading of the signs until after and he identified them by means of the signs he had learned from their
the test was completed. spoken narnes (Fouts, Chown, and Goodm an 1976) . Signing chimpan-
The two observers agreed in their interpretations of 86 to96 percent zees sometimes transfer signs to new situations, different from those in
of both correct and incorrect signs produced by three of four chimpan- which they had been trained to use them. For instance, Washoe learned
zees. The fourth animal yielded only 70 percent interobserver agree- the sign for "open" to ask that doors be opened, but she then used it to
ment, probably because she had not mastered signing as thoroughly as request her human companions to open boxes, drawers, briefcases, or
the other three. The chimpanzee's signs were correct tnTL to 88 percent picture books, and to turn on a water faucet. After she had learned the
of the trials, and this was far above chance levels because many signs sign for flower, she used it not only for different kinds of flowers but
were in use by these animals, so that if they were merely guessing at also for pipe tobacco and kitchen fumes. To her, it evidendy meant
random, the expected percentage of correct signs would have ranged smells.
from 4 to 15 percent (Gardner and Gardner 1984). These "blind" tests Stimulated by the Gardners'success with Washoe, other investigators
seem to rule out the possibility that the data could have been seriously have achieved similar levels of communication not only by several other
distorted by inadvertent cuing or Clever Hans errors, because neither chimpanzees but also by gorillas (Patterson and Linden l98I) and an
observer could see the projection screen, and also because any such in- orangutan (Miles 1990). Still other investigators have studied the com-
advertent cuing would have had to convey which of numerous signs the municative abilities of apes by quite different procedures. Premack and
chimpanzee should produce in response to the projected picture. his colleagues concentrated on a type of symbolism based on plastic
Nevertheless some critics have pointed out that apes are very adept tokens, which chimpanzees learned to arrange on a sort of bulletin
at detecting inadvertent cues from their human companions, and that it board in order to request desired objects and answer simple questions
is conceivable that even in these blind tests the ape could have received about them. These plastic symbols were arbitrary in that they did not
information about which sign to produce from unintentional sounds or resemble the object for which they stood. Premack's star pupil, Sarah,
movements of the observers. It is also conceivable that they could have learned not only to select the correct symbol when shown the object for
inadvertently conveyed information to each other about what sign was which it stood, but to use the symbols to request things she wanted. She
appropriate, as claimed by Sebeok and Rosenthal (I98I) and by could also arrange plastic tokens in strings resembling rudimentary sen-
Umiker-Sebeok and Sebeok (1981). Although every sort of Precaution tences) and answer simple questions presented to her through similar
and repeated checking of all possible sources of error are always aPPro- arrangements of the tokens. She could answer such questions as "What
priate, these criticisms seem quite far-fetched, and later experiments of is the color ef about the plastic representations of objects, even
Savage-Rumbaugh and her colleagues described below render explana- when the colors and other properties of the tokens were quite different
from those of the objects for which they stood (Premack1976,,1983b;
tions based on inadvertent cuing extremely implausible.
Washoe and other apes who have learned to use comnunicative ges- Premack and Premack 1983).
tures based on ASL seem to use these signals more or less as very young In another ambitious project Rumbaugh, Savage-Rumbaugh, and
children use single words. They sign spontaneously to request simple their colleagues at the Yerkes Laboratory in Adanta, Georgia, use a key-
things and activities, and they sometimes sign to themselves when board connected to a computer that records which keys are activated by
alone. Washoe and other signing chimpanzees sign to each other to at cither a human experimenter or the ape that learns which key it must
least a limited extent (Fouts 1989; Fouts and Fouts 1989; Fouts, Fouts, touch to obtain specific objects or to express simple desires. Each key
and Schoenfeld f984). A three-year-old chimpanzee named Ally was lights up when pressed, and each has a characteristic pattern to help the
trained by the Gardners' methods to use about seventy signs, and he rrpcs recognize and select it; but these pafferns are not iconic represen-
also learned to understand several spoken words and phrases. Ncxt hc trrtions of the objects for which the key stands. This system permits two-
was taught to use new signs corresponding to tcn of thcsc wortls that wrly c()r)rnrunicatiorr; and it has the great advantage that an objective
referred to familiar objects, but only thc sigrrs :uttl rtot tltc obiccts thcrtr- rcc<lrtl clur lrc kcpt ol'cvcry kcy prcss.
'l'lrc initi:rl t'xpt'r'irn('nts u,ith
sclvcs wcrc prcsc'r'ltcd along with thcsc spokt'tt tvortls tltlrilrg tlris plutsc [rl:rstic t<>kcns and kcyboards were inter-
222 Chapter Elnen Apes and Dolphins 223

preted as showing that the chimpanzees were using a simple type of of the words, rather than by word order. But regardless of how it is
linguistic communication, including a rudimentary sort of grammar in done, rule-governed combinations of words .oru"y a much wider array
which the tokens or key presses were used in a specific sequence to ex- of meanings than.*"++ be possible if each word were entirely indepen-
press relationships between the individual symbols. But, as reviewed by dent, and its relationship to other words did not convey any additi,cnal
Savage-Rumbaugh (1986), these apes may have learned only to per- meaning. Sugh glamnarical or syntactical rules .." ro important in
form specific actions to obtain particular things or activities. They may Tfilg possible the richness and versatility of human languages that
linguists and many others often maintain thar syntax is a sini qul. non of
have been thinking something like "If I do this, he will give me some
candy," or "If I do that, she will play with me." They seldom, if ever, languagg, and that the use of words or their equivalent is noi sufficient
tried to use their newly acquired skills to initiate communication with to quali$r as rrue language. This view must o? co.rrse entail denial of
their human companions or with each other, partly because the experi- trug]anguage to young children with vocabularies of only a few words.
mental arrangements in these early investigations allowed rather litde The importance assigned to syntax led to great interest in the com-
opportunity for such spontaneity. On the other hand, Washoe and other binations of signs used by Washoe and other rigrring apes, and to effcrrs
apes taught to communicate by manual gestures did often initiate com- by Premack and his colleagues as well as the scGntists it the Yerkes Lab-
municative exchanges by spontaneously asking for things they wanted. oratory to determine to what extent chimpanzees could communicate
All these approaches to teaching language-like communication to syntactically. Terrace (L979) replicated the Gardners, rraining of a
chimpanzees have been successfirl in the general sense that the apes have yoYlg cfimpanzee rouse signs derived from American sign Lan-guage,
learned to make requests and to answer simple questions. They have and he devoted special attention to series or combinations of sign-s used
also learned to give the appropriate gestural sign, to press the correct by this animal, named Nim chimpsky. The resuks were disapplinting.
key, or to select the right plastic symbols to label familiar objects. Seri- A few combinations of two or three signs were used, but onlyio a very
ous theoretical questions have been raised, however, about the degree limited extent did Nim attain anything like the combinatorial produi-
to which such apparent conununication entails any true understanding tivity of human language. when two-o. more signs were ,rr.i, there
on the animal's part of the meanings of the signals and symbols. The was little consistenry in their order, and in only a few cases was sign
alternative interpretation that has been suggested by many critics is that combination AB y:.q differently from BA. Most series of signs were
the chimpanzee learns merely to perform certain actions in order to ob- repetitious, with third or later signs adding almost nothing toih. mes-
tain things it wants, including activities or actions on the part of the sage convgyea Furthermore, many of Nim's signs were repetitions of
human companions, such as opening doors or going for a walk. These