The Evolution of Comparative Cognition: Is The Snark Still A Boojum?
The Evolution of Comparative Cognition: Is The Snark Still A Boojum?
The Evolution of Comparative Cognition: Is The Snark Still A Boojum?
Behavioural Processes
journal homepage: www.elsevier.com/locate/behavproc
a r t i c l e
i n f o
Article history:
Received 28 August 2008
Accepted 2 September 2008
Keywords:
Animal cognition
Comparative psychology
Memory
Numerical cognition
Theory of mind
a b s t r a c t
In The Snark is a Boojum, Beach [Beach, F.A., 1950. The snark was a boojum. American Psychologist.
5, 115124] famously asserted that animal psychology embraced too few species and too few problems
to deserve the name comparative. Later in the 20th century, others [e.g. Kamil, A.C., 1988. A synthetic
approach to the study of animal intelligence. In: Leger, D.W. (Ed.), Comparative Perspectives in Modern Psychology. Nebraska Symposium on Motivation, vol. 35. University of Nebraska Press, Lincoln, NE,
pp. 230257; Shettleworth, S.J., 1993. Where is the comparison in comparative cognition? Alternative
research programs. Psychological Science. 4, 179184] expressed similar concerns about the new subeld
of comparative cognition, suggesting that a more biological approach to choice of species and problems
was needed to balance a dominant anthropocentrism. The last 1015 years have seen many new developments, and a recent survey like Beachs reveals a very different picture. Not only are many more species
being studied, contributions by researchers from different backgrounds are increasing, and research on
comparative cognition is better connected with developmental psychology, behavioral neuroscience, primatology, behavioral ecology, and other elds. Contemporary research addresses three major aspects of
cognition about equally: basic processes, physical cognition, and social cognition. This article describes
a selected research program from each area, chosen to exemplify current trends and challenges for the
eld.
2008 Elsevier B.V. All rights reserved.
Fig. 1. Percent of all articles published in the given periods in each journal reporting data on rats (rat), mammals other than rats (other mamm), non-mammalian
vertebrates (other verts), and invertebrates (inverts). Beach = data from Fig. 2 in
Beach (1950) for 1946 + 1948; JCP = Journal of Comparative Psychology; JEP = Journal
of Experimental Psychology: Animal Behavior Processes; An Cog = Animal Cognition;
0507 = based on total for the three year period 20052007.
Fig. 2. Percent of all articles published in the Journal of Experimental Psychology: Animal Behavior Processes in 19911993 and in 20052007 reporting data on species
in the given groups. Multi species = contains new data from more than one species.
Multi species articles are also represented in one or more of the other categories.
They were counted once in each species group represented. For example, an article
comparing two or more monkey species counted as one article about other primates but one comparing monkeys with humans counted as one about humans
and one about other primates. See Dewsbury (1998) for an alternative approach to
this problem.
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which Beach and others (Dewsbury, 1998) might call simply animal psychology is considered in this article as part of the broader
eld of comparative cognition. Method and theory developed with
in-depth studies of a few species are indispensable for explicitly
comparative research, which in turn can feed back on the development of basic theory (for an example see Wright, 2006).
In itself the trend toward studying more species could represent just a mindless accumulation of data. But Beach (1950) also
complained about the limited number of problems and kinds of
behaviors being studied by so-called comparative psychologists.
Those criticisms were echoed over the years by people such as
Hodos and Campbell (1969), who added the complaint that the
comparisons that were being made were not well grounded in evolutionary theory (see also Papini, 2002). So what is important is
what this changing prole means, and to explore that I will focus
on comparative cognition, mainly on developments in the last 15
years or so. Not only does this time frame correspond to the age of
the Comparative Cognition Society, but also it is a little more than 15
years since Stu Hulse, one of the pioneers of the contemporary study
of comparative cognition, organized a symposium on the topic at
the meetings of the Psychonomic Society (Hulse, 1993). Echoing the
complaints of Beach (1950) and Hodos and Campbell (1969) about
the absence of biologically meaningful comparisons from so-called
comparative psychology, my contribution to it (Shettleworth, 1993)
was titled Where is the comparison in comparative cognition? It
contrasted biological and anthropocentric approaches to comparison and suggested that at the time most comparisons being made
by animal cognition researchers were implicitly with humans, i.e.
anthropocentric. More research was needed with an ecological or
adaptationist approach, testing for convergence and/or divergence
in cognitive abilities based on how cognition functions in the wild.
Comparisons of spatial memory in food-storing and nonstoring
birds provided an example. Other people, especially Al Kamil (e.g.
Kamil, 1988). were saying similar things at the time. Over the years
many others have made their own thoughtful assessments of the
eld of comparative cognition (Terrace, 1984; Wasserman, 1997;
Hulse, 2006; Church, 2001).
What follows is a personal view of what has been happening in
the eld in the past 1015 years, a view developed while preparing
an updated edition of my book (Shettleworth, 1998). Documenting
all the new developments makes clear that there really have been
some very big changes, so that complaints like those of Hodos and
Campbell about lack of sophistication regarding evolution, neglect
of natural behavior and more than a handful of species, or absence
of connections with other areas in the psychology and biology of
mind and behavior are becoming less and less appropriate. But
before surveying a few examples of these developments, let us go
back to a Beachian analysis of the proportions of articles on different groups of species in JEP:ABP (Fig. 2) and JCP (Fig. 3) at the
beginning and end of this roughly 15-year period. The changes in
JEP:ABP are most conspicuous. Although about the same number of
articles was published in 20052007 as in 19911993 (126 and 113,
respectively), the number of species studied doubled, from 10 to 20,
as did the proportion of articles reporting new data on more than
one species (multi species; see gure captions for further explanation). The increased number of species largely reects studies on
apes and monkeys and on more different species of birds. The trend
toward more studies of nonhuman primates is even more conspicuous in the data for the JCP, where the total number of species
hardly changed (66 species in 136 articles in 199193 and 73 species
in 151 articles in 20052007), but the species represented shifted
toward apes, monkeys, and humans. Indeed, a substantial number
of the multi species articles in the latter period were explicit comparisons of two or more primates, sometimes including humans.
Finally, as the simplied summary in Fig. 1 suggests, the journal
212
(Roitblat et al., 1984) with 33 chapters. New topics included number, evolution, and neuroscience. And the species contributing data
now included Clarks nutcrackers and other songbirds and many
more nonhuman primates. One might continue this survey and
extend it to textbooks, many of which reect the historical development of the eld with titles mentioning animal learning and
cognition and organizations with the chapters on cognition at the
end.
But it seems to me that if done without too many historical blinders, an inclusive survey of current work in comparative cognition
reveals that the eld encompasses three major sets of mechanisms
for the acquisition, processing, and representation of information
about the environment. Basic cognitive processes cut across all
kinds of content; these are the ones that were the main focus in
the 1970s. They include perception, attention, memory, associative leaning, category and concept learning. In addition, following
the taxonomy proposed by Tomasello and Call (1997), is research
on two sets of possibly specialized processes of acquisition, representation, and behavioral control, or cognitive modules, dened
largely in terms of their functions, i.e. what aspects of the world
they are about, namely physical cognition and social cognition.
Some aspects of physical cognition like time, space, and number
have been studied for quite a long time within experimental animal psychology, whereas others like tool using and causal learning
have emerged or re-emerged into prominence recently. Social cognition includes social knowledge, the kind of thing so beautifully
studied in the eld by Cheney and Seyfarth (2007), i.e. what animals
know about their social networks and how they come to know it.
It also includes theory of mind, imitation and other forms of social
learning, and the representational and other processes involved in
communication.
So part of what has changed since the 1970s is that the study of
cognitive processes in animals now encompasses a much broader
set of problems. They are also being studied by researchers from
a much wider variety of backgrounds. Behavioral ecologists, eld
biologists, developmental psychologists, and others are all contributing, and in some integrative research the lines between them
are nearly invisible. But more important are the major conceptual
and theoretical issues being addressed. The next part of the article briey reviews some key issues common to different aspects
of cognition by taking one topic within each of the three major
areas to exemplify some of the important new developments and
challenges.
3. Basic processes: memory
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216
Call, J., Tomasello, M., 2008. Does the chimpanzee have a theory of mind? 30 years
later. Trends in Cognitive Sciences 12, 187192.
Carruthers, P., Smith, P.K. (Eds.), 1996. Theories of Theories of Mind. Cambridge
University Press, Cambridge.
Cheney, D.L., Seyfarth, R.M., 2007. Baboon Metaphysics: The Evolution of a Social
MInd. University of Chicago Press, Chicago.
Church, R.M., 2001. Animal cognition: 19002000. Behavioural Processes 54, 5363.
Clayton, N.S., Bussey, T.J., Dickinson, A., 2003a. Can animals recall the past and plan
for the future? Nature Reviews Neuroscience 4, 685691.
Clayton, N.S., Dickinson, A., 1998. Episodic-like memory during cache recovery by
scrub jays. Nature 395, 272274.
Clayton, N.S., Yu, K.S., Dickinson, A., 2003b. Interacting cache memories: evidence
for exible memory use by western scrub-jays (Aphelocoma californica). Journal
of Experimental Psychology: Animal Behavior Processes 29, 1422.
Dally, J.M., Emery, N.J., Clayton, N.S., 2006. Food-caching western scrub-jays keep
track of who was watching when. Science 312, 16621665.
Darwin, C., 1871. The Descent of Man and Selection in Relation to Sex. John Murray,
London.
Dawkins, M.S., 1989. The future of ethology: how many legs are we standing on? In
Perspectives in Ethology 8, 4754.
de Waal, F.B.M., Tyack, P.L. (Eds.), 2003. Animal Social Complexity. Harvard University
Press, Cambridge MA.
Dewsbury, D.A., 1998. Animal psychology in journals, 19111927: another look at
the snark. Journal of Comparative Psychology 112, 400405.
Eichenbaum, H., Fortin, N.J., Ergorul, C., Wright, S.P., Agster, K.L., 2005. Episodic recollection in animals: If it walks like a duck and quacks like a duck. . .. Learning
and Motivation 36, 190207.
Emery, N.J., Clayton, N.S., 2004. The mentality of crows: convergent evolution of
intelligence in corvids and apes. Science 306, 19031907.
Emery, N.J., Clayton, N.S., Frith, C., 2007. Introduction: social intelligence: from brain
to culture. Philosophical Transactions of the Royal Society B: Biological Sciences
362 (1480), 485488.
Feigenson, L., Dehaene, S., Spelke, E., 2004. Core systems of number. Trends in Cognitive Sciences 8, 307314.
Fitch, W.T., 2005. The evolution of language: a comparative review. Biology and
Philosophy 20, 193230.
Galef, B.G., Heyes, C.M., 2004. Introduction: special issue on social learning. Learning
& Behavior 32, 13.
Galef, B.G., Laland, K.N., 2005. Social learning in animals: empirical studies and
theoretical models. BioScience 55, 489499.
Gallistel, C.R., 1990. The Organization of Learning. M. I. T. Press, Cambridge, MA.
Hampton, R.R., 2005. Can rhesus monkeys discriminate between remembering and
forgetting? In: Terrace, H.S., Metcalfe, J. (Eds.), The Missing Link in Cognition:
Origins of Self-Reective Consciousness. Oxford University Press, New York, pp.
272295.
Hampton, R.R., Schwartz, B.L., 2004. Episodic memory in nonhumans: what and
where, is when? Current Opinion in Neurobiology 14, 192197.
Hare, B., 2007. From nonhuman to human mind. What changed and why? Current
Directions in Psychological Science 16, 6064.
Hare, B., Call, J., Tomasello, M., 2001. Do chimpanzees know what conspecics know?
Animal Behaviour 61, 139151.
Hare, B., Tomasello, M., 2005. Human-like social skills in dogs? Trends in Cognitive
Sciences 9, 439444.
Hauser, M.D., Carey, S., Hauser, L.B., 2000. Spontaneous number representation in
semi-free-ranging rhesus monkeys. Proceedings of the Royal Society of London
B 267, 829833.
Hauser, M.D., Chomsky, N., Fitch, W.T., 2002. The faculty of language: what is it, who
has it, and how did it evolve? Science 298, 15691579.
Herrmann, E., Call, J., Hernndez-Lloreda, M.V., Hare, B., Tomasello, M., 2007. Humans
have evolved specialized skills of social cognition: the cultural intelligence
hypothesis. Science 317, 13601366.
Heyes, C., 2008. Beast machines? Questions of animal consciousness. In: Davies,
M., Weiskrantz, L. (Eds.), Frontiers of Consciousness. Oxford University Press,
Oxford, pp. xxxxxx.
Heyes, C.M., 1993. Anecdotes, training, trapping and triangulating: do animals
attribute mental states? Animal Behaviour 46, 177188.
Hodos, W., Campbell, C.B.G., 1969. Scala naturae: why there is no theory in comparative psychology. Psychological Review 76, 337350.
Hulse, S.H., 1993. The present status of animal cognition: an introduction. Psychological Science 4, 154155.
Hulse, S.H., 2006. Postscript: an essay on the study of cognition in animals. In:
Wasserman, E.A., Zentall, T.R. (Eds.), Comparative Cognition. Oxford University
Press, New York, pp. 668678.
Hulse, S.H., Fowler, H., Honig, W.K. (Eds.), 1978. Cognitive Processes in Animal Behavior. Erlbaum, Hillsdale, NJ.
Jeffery, K.J. (Ed.), 2003. The Neurobiology of Spatial Behaviour. Oxford University
Press, Oxford.
Kacelnik, A., 2006. Meanings of rationality. In: Hurley, S., Nudds, M. (Eds.), Rational
Animals? Oxford University Press, Oxford, pp. 87106.
Kamil, A.C., 1988. A synthetic approach to the study of animal intelligence. In: Leger,
D.W. (Ed.), Comparative Perspectives in Modern Psychology. Nebraska Symposium on Motivation 35. University of Nebraska Press, Lincoln NE, pp. 230257.
Kamil, A.C., 1998. On the proper denition of cognitive ethology. In: Balda, R.P., Pepperberg, I.M., Kamil, A.C. (Eds.), Animal Cognition in Nature. Academic Press, San
Diego, pp. 128.
217
Shettleworth, S.J., 1993. Where is the comparison in comparative cognition? Alternative research programs. Psychological Science 4, 179184.
Shettleworth, S.J., 1998. Cognition, Evolution and Behavior. Oxford University Press,
New York.
Silva, F.J., Page, D.M., Silva, K.M., 2005. Methodological-conceptual problems in the
study of chimpanzees folk physics: how studies of adult humans can help.
Learning & Behavior 33, 4757.
Smith, J.D., Washburn, D.A., 2005. Uncertainty monitoring and metacognition by
animals. Current Directions in Psychological Science (14), 1924.
Suddendorf, T., Corballis, M.C., 2007. The evolution of foresight: what is mental time
travel and is it unique to humans? Behavioral and Brain Sciences 30, 335345.
Terrace, H.S., 1984. Animal cognition. In: Roitblat, H.L., Bever, T.G., Terrace, H.S. (Eds.),
Animal Cognition. Erlbaum, Hillsdale, NJ, pp. 728.
Terrace, H.S., Metcalfe, J. (Eds.), 2005. The missing link in cognition: Origins of SelfReective Consciousness. Oxford University Press, New York.
Tinbergen, N., 1963. On aims and methods of ethology. Zeitschrift fur Tierpsychologie
20, 410433.
Tomasello, M., Call, J., 1997. Primate Cognition. Oxford University Press, New York.
Tomasello, M., Call, J., Hare, B., 2003. Chimpanzees understand psychological
statesthe question is which ones and to what extent. Trends in Cognitive
Sciences 7, 153156.
Tulving, E., 2005. Episodic memory and autonoesis: uniquely human? In: Terrace,
H.S., Metcalfe, J. (Eds.), The Missing Link in cognition: Origins of Self-Reective
Consciousness. Oxford University Press, New York, pp. 356.
Wasserman, E.A., 1984. Animal intelligence: understanding the minds of animals
through their behavioral ambassadors. In: Roitblat, H.L., Bever, T.G., Terrace,
H.S. (Eds.), Animal Cognition. Lawrence Erlbaum Associates, Hillsdale, NJ, pp.
4560.
Wasserman, E.A., 1997. The science of animal cognition: past, present, and future.
Journal of Experimental Psychology: Animal Behavior Processes 23, 123135.
Wilson, E.O., 1975. Sociobiology. Belknap Press, Cambridge, MA.
Wright, A.A., 2006. Memory processing. In: Wasserman, E.A., Zentall, T.R. (Eds.),
Comparative Cognition: Experimental Explorations of Animal Intelligence.
Oxford University Press, New York, pp. 164185.
Yonelinas, A.P., 2001. Components of episodic memory: the contribution of recollection and familiarity. Philosophical Transactions of the Royal Society B 356,
13631374.
Zentall, T.R., Clement, T.S., Bhatt, R.S., Allen, J., 2001. Episodic-like memory in pigeons.
Psychonomic Bulletin and Review 8, 685690.