Are We Smart Enough to Know How Smart Animals Are

by Frans de Waal

  Thorndike, E. L. 1898. Animal intelligence: An experimental study of the associate processes in animals. Psychological Reviews, Monograph Supplement 2.

  Thorpe, W. H. 1979. The Origins and Rise of Ethology: The Science of the Natural Behaviour of Animals. London: Heineman.

  Tinbergen, N. 1953. The Herring Gull’s World. London: Collins.

  ———. 1963. On aims and methods of ethology. Zeitschrift für Tierpsychologie 20: 410–40.

  Tinbergen, N., and W. Kruyt. 1938. Über die Orientierung des Bienenwolfes (Philanthus triangulum Fabr.). III. Die Bevorzugung bestimmter Wegmarken. Zeitschrift für Vergleichende Physiologie 25:292–334.

  Tinklepaugh, O. L. 1928. An experimental study of representative factors in monkeys. Journal of Comparative Psychology 8:197–236.

  Toda, K., and S. Watanabe. 2008. Discrimination of moving video images of self by pigeons (Columba livia). Animal Cognition 11:699–705.

  Tolman, E. C. 1927. A behaviorist’s definition of consciousness. Psychological Review 34:433–39.

  Tomasello, M.. 2014. A Natural History of Human Thinking. Cambridge, MA: Harvard University Press.

  ———. 2008. Origins of human cooperation. Tanner Lecture, Stanford University, Oct. 29–31.

  Tomasello, M., and J. Call. 1997. Primate Cognition. New York: Oxford University Press.

  Tomasello, M., A. C. Kruger, and H. H. Ratner. 1993. Cultural learning. Behavioral and Brain Sciences 16:495–552.

  Tomasello, M., E. S. Savage-Rumbaugh, and A. C. Kruger. 1993. Imitative learning of actions on objects by children, chimpanzees, and enculturated chimpanzees. Child Development 64:1688–705.

  Tramontin, A. D., and E. A. Brenowitz. 2000. Seasonal plasticity in the adult brain. Trends in Neurosciences 23:251–58.

  Troscianko, J., et al. 2012. Extreme binocular vision and a straight bill facilitate tool use in New Caledonian crows. Nature Communications 3:1110.

  Tsao, D., S. Moeller, and W. A. Freiwald. 2008. Comparing face patch systems in macaques and humans. Proceedings of the National Academy of Sciences USA 105:19514–19.

  Tulving, E. 2005. Episodic memory and autonoesis: Uniquely human? In The Missing Link in Cognition, ed. H. Terrace and J. Metcalfe, 3–56. Oxford: Oxford University Press.

  ———. 1972. Episodic and semantic memory. In Organization of Memory, ed. E. Tulving and W. Donaldson, 381–403. New York: Academic Press.

  ———. 2001. Origin of autonoesis in episodic memory. In The Nature of Remembering: Essays in Honor of Robert G. Crowder, ed. H. L. Roediger et al., 17–34. Washington, DC: American Psychological Association.

  Uchino, E., and S. Watanabe. 2014. Self-recognition in pigeons revisited. Journal of the Experimental Analysis of Behavior 102:327–34.

  Udell, M.A.R., N. R. Dorey, and C.D.L. Wynne. 2008. Wolves outperform dogs in following human social cues. Animal Behaviour 76:1767–73.

  ———. 2010. What did domestication do to dogs? A new account of dogs’ sensitivity to human actions. Biological Review 85:327–45.

  Uexküll, J. von. 1909. Umwelt und Innenwelt der Tiere. Berlin: Springer.

  ———. 1957 [orig. 1934]. A stroll through the worlds of animals and men. A picture book of invisible worlds. In Instinctive Behavior, ed. C. Schiller, 5–80. London Methuen.

  Vail, A. L., A. Manica, and R. Bshary. 2014. Fish choose appropriately when and with whom to collaborate. Current Biology 24:R791–93.

  van de Waal, E., C. Borgeaud, and A. Whiten. 2013. Potent social learning and conformity shape a wild primate’s foraging decisions. Science 340: 483–85.

  van Hooff, J. 1972. A comparative approach to the phylogeny of laughter and smiling. In Non-Verbal Communication, ed. R. A. Hinde, 209–41. Cambridge: Cambridge University Press.

  van Leeuwen, E.J.C., K. A. Cronin, and D.B.M. Haun. 2014. A group-specific arbitrary tradition in chimpanzees (Pan troglodytes). Animal Cognition 17:1421–25.

  van Leeuwen, E.J.C., and D.B.M. Haun. 2013. Conformity in nonhuman primates: Fad or fact? Evolution and Human Behavior 34:1–7.

  van Schaik, C. P., L. Damerius, and K. Isler. 2013. Wild orangutan males plan and communicate their travel direction one day in advance. Plos ONE 8:e74896.

  van Schaik, C. P., R. O. Deaner, and M. Y. Merrill. 1999. The conditions for tool use in primates: Implications for the evolution of material culture. Journal of Human Evolution 36:719–41.

  Varki, A., and D. Brower. 2013. Denial: Self-Deception, False Beliefs, and the Origins of the Human Mind. New York: Twelve.

  Vasconcelos, M., K. Hollis, E. Nowbahari, and A. Kacelnik. 2012. Pro-sociality without empathy. Biology Letters 8:910–12.

  Vauclair, J. 1996. Animal Cognition: An Introduction to Modern Comparative Psychology. Cambridge, MA: Harvard University Press.

  Visalberghi, E., and L. Limongelli. 1994. Lack of comprehension of cause-effect relations in tool-using capuchin monkeys (Cebus apella). Journal of Comparative Psychology 108:15–22.

  Visser, I. N., et al. 2008. Antarctic peninsula killer whales (Orcinus orca) hunt seals and a penguin on floating ice. Marine Mammal Science 24:225–34.

  Wade, N. 2014. A Troublesome Inheritance: Genes, Race and Human History. New York: Penguin.

  Wallace, A. R. 1869. Sir Charles Lyell on geological climates and the origin of species. Quarterly Review 126:359–94.

  Wascher, C.A.F., and T. Bugnyar. 2013. Behavioral responses to inequity in reward distribution and working effort in crows and ravens. Plos ONE 8:e56885.

  Wasserman, E. A. 1993. Comparative cognition: Beginning the second century of the study of animal intelligence. Psychological Bulletin 113:211–28.

  Watanabe, A., U. Grodzinski, and N. S. Clayton. 2014. Western scrub-jays allocate longer observation time to more valuable information. Animal Cognition 17:859–67.

  Watson, S. K., et al. 2015. Vocal learning in the functionally referential food grunts of chimpanzees. Current Biology 25:1–5.

  Weir, A. A., J. Chappell, and A. Kacelnik. 2002. Shaping of hooks in New Caledonian crows. Science 297:981–81

  Wellman, H. M., A. T. Phillips, and T. Rodriguez. 2000. Young children’s understanding of perception, desire, and emotion. Child Development 71:895–912.

  Wheeler, B. C., and J. Fischer. 2012. Functionally referential signals: A promising paradigm whose time has passed. Evolutionary Anthropology 21:195–205.

  White, L. A.. 1959. The Evolution of Culture. New York: McGraw-Hill.

  Whitehead, H., and L. Rendell. 2015. The Cultural Lives of Whales and Dolphins. Chicago: University of Chicago Press.

  Whiten, A., V. Horner, and F.B.M. de Waal. 2005. Conformity to cultural norms of tool use in chimpanzees. Nature 437:737–40.

  Wikenheiser, A., and A. D. Redish. 2012. Hippocampal sequences link past, present, and future. Trends in Cognitive Sciences 16:361–62.

  Wilcox, S., and R. R. Jackson. 2002. Jumping spider tricksters: deceit, predation, and cognition. In the Cognitive Animal: Empirical and Theoretical Perspectives on Animal Cognition, ed. M. Bekoff, C. Allen, and G. Burghardt, 27–33. Cambridge, MA: MIT Press.

  Wilfried, E.E.G., and J. Yamagiwa. 2014. Use of tool sets by chimpanzees for multiple purposes in Moukalaba-Doudou National Park, Gabon. Primates 55:467–42.

  Wilson, E. O. 1975. Sociobiology: The New Synthesis. Cambridge, MA: Belknap Press.

  ———. 2010. Anthill: A Novel. New York: Norton.

  Wilson, M. L., et al. 2014. Lethal aggression in pan is better explained by adaptive strategies than human impacts. Nature 513:414–17.

  Wittgenstein, L.. 1958 [orig. 1953]. Philosophical Investigations, 2nd ed. Oxford: Blackwell.

  Wohlgemuth, S., I. Adam, and C. Scharff. 2014. FOXP2 in songbirds. Current Opinion in Neurobiology 28:86–93.

  Wynne, C.D.L., and Monique Udell. 2013. Animal Cognition: Evolution, Behavior and Cognition. 2nd. ed. New York: Palgrave Macmillan.

  Yamakoshi, G. 1998. Dietary responses to fruit scarcity of wild chimpanzees at bossou, guinea: Possible implication
s for ecological importance of tool use. American Journal of Physical Anthropology 106:283–95.

  Yamamoto, S., T. Humle and M. Tanaka. 2009. Chimpanzees help each other upon request. Plos One 4:e7416.

  Yerkes, R. M. 1925. Almost Human. New York: Century.

  ———. 1943. Chimpanzees: A Laboratory Colony. New Haven, CT: Yale University Press.

  Zahn-Waxler, C., M. Radke-Yarrow, E. Wagner, and M. Chapman. 1992. Development of concern for others. Developmental Psychology 28:126–36.

  Zylinski, S. 2015. Fun and play in invertebrates. Current Biology 25:R10–12.

  GLOSSARY

  Analogy: Structurally and functionally similar traits (such as the streamlined shapes of fish and dolphins) that evolved independently as adaptations to the same environment. See also: convergent evolution.

  Anthropocentrism: A worldview revolving around the human species.

  Anthropodenial: The a priori denial of humanlike characteristics in other animals or animallike characteristics in humans.

  Anthropomorphism: The (mis)attribution of humanlike characteristics and experiences to other species.

  Behaviorism: The psychological approach introduced by B. F. Skinner and John Watson with emphasis on observable behavior and learning. In its more extreme form, behaviorism reduces behavior to learned associations and rejects internal cognitive processes.

  Biologically prepared learning: Learning talents and predispositions that evolved to suit a species’s ecology and assist its survival. See also: Garcia Effect.

  Bonding- and Identification-based Observational Learning (BIOL): Social learning primarily based on a desire to belong and conform to social models.

  Clever Hans Effect: The influence of unintentional cues by the experimenter in inducing an apparent cognitive feat.

  Cognition: The transformation of sensory input into knowledge about the environment, and the application of this knowledge.

  Cognitive ethology: Donald Griffin’s label for the biological study of cognition.

  Cognitive ripple rule: The rule that every cognitive capacity turns out to be older and more widespread than initially assumed owing to convergent evolution.

  Comparative psychology: The subdiscipline of psychology that seeks to find general principles of animal and human behavior or, more narrowly, to use animals as models for human learning and psychology.

  Conformist bias: The tendency of an individual to favor the solutions and preferences of the majority.

  Conspecific approach: The technique of testing animals with models or partners of their own species in order to reduce human influence.

  Convergent evolution: The independent evolution of similar traits or capacities in unrelated species in response to similar environmental pressures. See also: analogy.

  Cooperative pulling paradigm: An experimental paradigm in which two or more individuals pull rewards toward themselves via an apparatus that they cannot successfully operate alone.

  Critical anthropomorphism: The use of human intuitions about a species to generate objectively testable ideas.

  Culture: The learning of habits and traditions from others, with the result that groups of the same species behave differently.

  Delayed gratification: The ability to resist an immediate reward in order to receive a better one later on.

  Displacement activity: An activity irrelevant to the current situation that appears suddenly due to a thwarted motivation or conflict between incompatible motivations, such as fight an flight.

  Ecological niche: The role of a species within an ecosystem and the natural resources it relies on.

  Episodic memory: The recollection of specific past experiences, such as their content, location, and timing.

  Embodied cognition: A view of cognition that emphasizes the role of the body (beyond the brain) and its interaction with the environment.

  Ethology: The biological approach to animal and human behavior, introduced by Konrad Lorenz and Niko Tinbergen, that emphasizes species-typical behavior as an adaptation to the natural environment.

  Evolutionary cognition: The study of all cognition, human and animal, from an evolutionary perspective.

  Function: The purpose of a trait as measured by the benefits it confers.

  Garcia Effect: An aversion to a specific food develops after negative effects of ingestion, such as nausea and vomiting, even if these effects occurred after a long time interval. See also: biologically prepared learning.

  Homology: A similarity in traits of two species that is explained by the presence of these traits in their common ancestor.

  Hume’s Touchstone: David Hume’s plea to apply the same hypotheses to the mental operations of both humans and animals.

  Inferential reasoning: The use of available information to construct a reality that is not directly observable.

  Insight: The sudden combining (aha! experience) of past bits of information to mentally come up with a novel solution to a novel problem.

  Intelligence: The ability to successfully apply information and cognition to solve problems.

  Killjoy account: The deflation of a claim regarding higher mental processes by proposing a seemingly simpler explanation.

  Know-thy-animal rule: The rule that anyone who questions a cognitive claim about a species should either be familiar with the species or make an effort to verify the counterclaim.

  Magic well: The endless complexity of the specialized cognition of any organism.

  Matching-to-sample paradigm: An experimental framework in which the subject, after perceiving a sample, must find a matching one from among two or more options.

  Mental time travel: An individual’s awareness of its own past and future.

  Metacognition: The monitoring of one’s own memory in order to know what one knows.

  Mirror mark test: An experiment to determine whether an organism will notice a mark on its body that it can see only via its mirror image.

  Morgan’s Canon: The advice not to assume higher cognitive capacities if lower ones may explain an observed phenomenon.

  Object permanence: The realization that an object continues to exist even after it has disappeared from an individual’s perception.

  Overimitation: The imitation of all the actions shown by a model even if not all serve to reach the goal.

  Perspective taking: The ability to look at a situation from another’s standpoint.

  Pygmalion Effect: The way a given species is tested often reflects cognitive prejudices. Specifically: comparative testing favors our own species.

  Scala naturae: The natural scale of the ancient Greeks ranking all organisms from low to high, with humans closest to the angels.

  Selective imitation: Imitation of only those actions that lead to the goal while ignoring other behavior.

  Self-awareness: Consciousness of the self, which some interpret as requiring an organism to pass the mirror mark test, whereas others believe that self-awareness characterizes all life-forms.

  Signature whistles: Dolphin calls modulated so that each individual has a distinct and recognizable “melody.”

  Social brain hypothesis: The hypothesis that the relatively large brain size of primates is explained by the complexity of their societies and their need to process social information.

  Targeted helping: Assistance given by one individual to another based on perspective taking, such as judgment of the other’s specific situation and needs.

  Theory of mind: The ability to attribute mental states to others, such as knowledge, intentions, and beliefs.

  Triadic awareness: Individual A’s knowledge not only of its own relations with individuals B and C, but also of the relation between B and C themselves.

  True imitation: A subtype of imitation that reflects understanding of the other’s methods and goals.

  Umwelt: An organism’s subjective perceptual world.

  ACKNOWLEDGMENTS

  My interest in cognition as an evolved characteristic marks me as an ethologist. I
am grateful to all the Dutch ethologists, who influenced my early career. I began my graduate studies at the University of Groningen, in the Netherlands, under Gerard Baerends, who was Niko Tinbergen’s first student. Afterward I wrote my dissertation on primate behavior at the University of Utrecht with Jan van Hooff, an expert of facial expressions and emotions. My exposure to comparative psychology, the other approach to animal behavior, came mostly after my move across the Atlantic. Input from both schools has been critical to constructing the new field of evolutionary cognition. This book relates my own journey and involvement in this field as it gradually moved to the forefront of the study of animal behavior.

  I am grateful to the many people who have accompanied me on this journey, from colleagues and collaborators to students and postdocs. Just to thank those of the last few years: Sarah Brosnan, Kimberly Burke, Sarah Calcutt, Matthew Campbell, Devyn Carter, Zanna Clay, Marietta Danforth, Tim Eppley, Pier Francesco Ferrari, Katie Hall, Yuko Hattori, Victoria Horner, Joshua Plotnik, Stephanie Preston, Darby Proctor, Teresa Romero, Malini Suchak, Julia Watzek, Christine Webb, and Andrew Whiten. I am grateful to the Yerkes National Primate Research Center and Emory University for the opportunity to conduct our studies, and to the many monkeys and apes who have participated and become part of my life.

  This book was initially undertaken as a relatively short overview of recent findings in primate cognition but quickly grew in scope and size to what it is now. Inclusion of other species has been paramount, because the field of animal cognition has become much more varied in the last two decades. This overview is obviously incomplete, but my main objective is to convey enthusiasm for evolutionary cognition and to illustrate how it has grown into a respectable science based on rigorous observations and experiments. Since the book covers so many different aspects and species, I have asked colleagues to read parts of it. For their invaluable feedback, I thank Michael Beran, Gregory Berns, Redouan Bshary, Zanna Clay, Harold Gouzoules, Russell Gray, Roger Hanlon, Robert Hampton, Vincent Janik, Karline Janmaat, Gema Martin-Ordas, Gerald Massey, Jennifer Mather, Tetsuro Matsuzawa, Caitlin O’Connell, Irene Pepperberg, Susan Perry, Joshua Plotnik, and Malini Suchak.