Intelligence in Corvids and Apes: A Case of Convergent Evolution?

Intelligence is suggested to have evolved in primates in response to complexities in the environment faced by their ancestors. Corvids, a large-brained group of birds, have been suggested to have undergone a convergent evolution of intelligence [Emery & Clayton (2004) Science, Vol. 306, pp. 1903–1907]. Here we review evidence for the proposal from both ultimate and proximate perspectives. While we show that many of the proposed hypotheses for the evolutionary origin of great ape intelligence also apply to corvids, further study is needed to reveal the selective pressures that resulted in the evolution of intelligent behaviour in both corvids and apes. For comparative proximate analyses we emphasize the need to be explicit about the level of analysis to reveal the type of convergence that has taken place. Although there is evidence that corvids and apes solve social and physical problems with similar speed and flexibility, there is a great deal more to be learned about the representations and algorithms underpinning these computations in both groups. We discuss recent comparative work that has addressed proximate questions at this level, and suggest directions for future research.

[1]  L. Lefebvre,et al.  Feeding innovations and forebrain size in Australasian birds , 1998 .

[2]  N. Emery,et al.  Investigating Physical Cognition in Rooks, Corvus frugilegus , 2006, Current Biology.

[3]  Christian Rutz,et al.  Development of tool use in New Caledonian crows: inherited action patterns and social influences , 2006, Animal Behaviour.

[4]  J. Martin Marcos,et al.  COOPERATIVELY BREEDING GROUPS OF CARRION CROW(CORVUS CORONE CORONE) IN NORTHERN SPAIN , 2002 .

[5]  Bernd Heinrich,et al.  Mind of the Raven , 1999 .

[6]  R. Connor Dolphin social intelligence: complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  J. Yamagiwa The Evolution of Thought: Diet and foraging of the great apes: ecological constraints on their social organizations and implications for their divergence , 2004 .

[8]  Nicola S. Clayton,et al.  The social life of corvids , 2007, Current Biology.

[9]  A. Kacelnik,et al.  Shaping of Hooks in New Caledonian Crows , 2002, Science.

[10]  P. Godfrey‐Smith Environmental complexity and the evolution of cognition. , 2002 .

[11]  Richard W. Byrne,et al.  Machiavellian Intelligence II: Machiavellian intelligence , 1997 .

[12]  W. McGrew Chimpanzee Material Culture: Implications for Human Evolution , 1992 .

[13]  S. Uehara,et al.  Natural Diet of Chimpanzees (Pan troglodytes schweinfurthii): Long-Term Record from the Mahale Mountains, Tanzania , 1983 .

[14]  Gavin R. Hunt,et al.  Tool Use by the New Caledonian Crow Corvus moneduloides to Obtain Cerambycidae from Dead Wood , 2000 .

[15]  Derek C. Penn,et al.  Darwin's mistake: Explaining the discontinuity between human and nonhuman minds , 2008, Behavioral and Brain Sciences.

[16]  F. D. Waal Chimpanzee Politics: Power and Sex among Apes , 1982 .

[17]  Anne E. Russon,et al.  Machiavellian Intelligence II: Exploiting the expertise of others , 1997 .

[18]  L. Lefebvre,et al.  The Biology of Traditions: Social learning about food in birds , 2003 .

[19]  Brian Hare,et al.  Can competitive paradigms increase the validity of experiments on primate social cognition? , 2001, Animal Cognition.

[20]  M. Tomasello,et al.  Chimpanzees know what conspecifics do and do not see , 2000, Animal Behaviour.

[21]  M. Bitterman PHYLETIC DIFFERENCES IN LEARNING. , 1965, The American psychologist.

[22]  Nathan J Emery,et al.  What do rooks (Corvus frugilegus) understand about physical contact? , 2006, Journal of comparative psychology.

[23]  A. Kacelnik,et al.  Behavioural ecology: Tool manufacture by naive juvenile crows , 2005, Nature.

[24]  Josep Call,et al.  Gorillas (Gorilla gorilla) and orangutans (Pongo pygmaeus) encode relevant problem features in a tool-using task. , 2005, Journal of comparative psychology.

[25]  Michael Tomasello,et al.  All great ape species follow gaze to distant locations and around barriers. , 2005, Journal of comparative psychology.

[26]  G. Hunt Manufacture and use of hook-tools by New Caledonian crows , 1996, Nature.

[27]  G. E. Woolfenden,et al.  Social learning of a novel foraging patch in families of free-living Florida scrub-jays , 2000, Animal Behaviour.

[28]  B. Heinrich,et al.  Influence of competitors on caching behaviour in the common raven,Corvus corax , 1998, Animal Behaviour.

[29]  N. Emery,et al.  Cooperative problem solving in rooks (Corvus frugilegus) , 2008, Proceedings of the Royal Society B: Biological Sciences.

[30]  C. Darwin The Descent of Man and Selection in Relation to Sex: INDEX , 1871 .

[31]  B. Heinrich,et al.  Ravens, Corvus corax, differentiate between knowledgeable and ignorant competitors , 2005, Proceedings of the Royal Society B: Biological Sciences.

[32]  C. M. Heyes Anecdotes, training, trapping and triangulating: do animals attribute mental states? , 1993, Animal Behaviour.

[33]  Á. Miklósi,et al.  Comparative social cognition: what can dogs teach us? , 2004, Animal Behaviour.

[34]  M. Tomasello,et al.  Chimpanzees Recruit the Best Collaborators , 2006, Science.

[35]  A Dickinson,et al.  Scrub jays (Aphelocoma coerulescens) form integrated memories of the multiple features of caching episodes. , 2001, Journal of experimental psychology. Animal behavior processes.

[36]  David Marr,et al.  VISION A Computational Investigation into the Human Representation and Processing of Visual Information , 2009 .

[37]  P. Hammerstein,et al.  Economics in nature : social dilemmas, mate choice and biological markets , 2001 .

[38]  David R. Shanks,et al.  Instrumental action and causal representation , 1995 .

[39]  P. Marler Social Cognition: Are Primates Smarter than Birds? , 1996 .

[40]  A. Dickinson,et al.  Planning for the future by western scrub-jays , 2007, Nature.

[41]  D. Griffin Prospects for a cognitive ethology , 1978, Behavioral and Brain Sciences.

[42]  C. Perrins,et al.  Birds of the Western Palearctic , 1978, Nature.

[43]  K. Milton Distribution Patterns of Tropical Plant Foods as an Evolutionary Stimulus to Primate Mental Development , 1981 .

[44]  L. Lefebvre,et al.  Feeding innovations and forebrain size in birds , 1997, Animal Behaviour.

[45]  Andrew Whiten,et al.  The evolution of animal ‘cultures’ and social intelligence , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[46]  L. Rapaport,et al.  Social influences on foraging behavior in young nonhuman primates: Learning what, where, and how to eat , 2008 .

[47]  Nicola S. Clayton,et al.  The Mentality of Crows: Convergent Evolution of Intelligence in Corvids and Apes , 2004, Science.

[48]  M. Tomasello,et al.  Cues that chimpanzees do and do not use to find hidden objects , 2000, Animal Cognition.

[49]  K. Laland,et al.  Social intelligence, innovation, and enhanced brain size in primates , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Russell D. Gray,et al.  Direct observations of pandanus-tool manufacture and use by a New Caledonian crow (Corvus moneduloides) , 2004, Animal Cognition.

[51]  A. Jolly,et al.  Lemur Social Behavior and Primate Intelligence , 1966, Science.

[52]  A. Dickinson,et al.  Scrub jays (Aphelocoma coerulescens) remember the relative time of caching as well as the location and content of their caches. , 1999, Journal of comparative psychology.

[53]  B. Heinrich,et al.  Ravens, Corvus corax, follow gaze direction of humans around obstacles , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[54]  Robin I. M. Dunbar Neocortex size as a constraint on group size in primates , 1992 .

[55]  Joanna M. Dally,et al.  The Comparative Cognition of Caching , 2009 .

[56]  Sue Taylor Parker,et al.  Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in cebus monkeys and great apes , 1977 .

[57]  Louis Lefebvre,et al.  Tools and brains in birds , 2002 .

[58]  Richard W. Byrne,et al.  Evolution of primate cognition , 2000, Cogn. Sci..

[59]  L. Barrett,et al.  The social nature of primate cognition , 2005, Proceedings of the Royal Society B: Biological Sciences.

[60]  Edwin Hutchins,et al.  Machiavellian Intelligence II: Why Machiavellian intelligence may not be Machiavellian , 1997 .

[61]  J. Lockie THE BREEDING AND FEEDING OF JACKDAWS AND ROOKS WITH NOTES ON CARRION CROWS AND OTHER CORVIDAE. , 2008 .

[62]  T. Bugnyar,et al.  Leading a conspecific away from food in ravens (Corvus corax)? , 2004, Animal Cognition.

[63]  G. A. Sonerud,et al.  Ignorant hooded crows follow knowledgeable roost-mates to food: support for the information centre hypothesis , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[64]  Richard W. Byrne,et al.  Complex leaf‐gathering skills of mountain gorillas (Gorilla g. beringei): Variability and standardization , 1993, American journal of primatology.

[65]  F. Waal,et al.  Reconciliation and consolation among chimpanzees , 1979, Behavioral Ecology and Sociobiology.

[66]  R. Potts Paleoenvironmental basis of cognitive evolution in great apes , 2004, American journal of primatology.

[67]  L. Marino Convergence of Complex Cognitive Abilities in Cetaceans and Primates , 2002, Brain, Behavior and Evolution.

[68]  B. Heinrich,et al.  Raven roosts are mobile information centres , 1996, Animal Behaviour.

[69]  D. Goodwin,et al.  Crows of the world , 1976 .

[70]  M. Tomasello,et al.  Chimpanzee gaze following in an object-choice task , 1998, Animal Cognition.

[71]  A. H. Taylor,et al.  Do New Caledonian crows solve physical problems through causal reasoning? , 2009, Proceedings of the Royal Society B: Biological Sciences.

[72]  Robin I. M. Dunbar,et al.  Neocortex size and social network size in primates , 2001, Animal Behaviour.

[73]  W. McGrew,et al.  Chimpanzee use of a tool-set to get honey. , 1990, Folia primatologica; international journal of primatology.

[74]  Sabine Tebbich,et al.  The ecology of tool-use in the woodpecker finch (Cactospiza pallida) , 2002 .

[75]  Amanda M Seed,et al.  Cognitive adaptations of social bonding in birds , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[76]  J. Goodall,et al.  Tool-Using and Aimed Throwing in a Community of Free-Living Chimpanzees , 1964, Nature.

[77]  Jason P. Mitchell Mentalizing and Marr: An information processing approach to the study of social cognition , 2006, Brain Research.

[78]  R. Bernard,et al.  The Chimpanzees of the Taï Forest. , 2001 .

[79]  L. Sorkin,et al.  Food-Caching Western Scrub-Jays Keep Track of Who Was Watching When , 2006 .

[80]  A. Dickinson Contemporary Animal Learning Theory , 1981 .

[81]  R. Waite Local Enhancement for Food Finding by Rooks (Corvus frugilegus) Foraging on Grassland , 2010 .

[82]  P. Bednekoff,et al.  Social Caching and Observational Spatial Memory in Pinyon Jays , 1996 .

[83]  Donald R. Griffin Prospects for a Cognitive Ethology , 1978 .

[84]  N. Humphrey The Social Function of Intellect , 1976 .

[85]  M. Tomasello,et al.  Chimpanzees (Pan troglodytes) conceal visual and auditory information from others. , 2006, Journal of comparative psychology.

[86]  Russell D. Gray,et al.  Species-wide manufacture of stick-type tools by New Caledonian Crows , 2002 .

[87]  R. Byrne,et al.  Machiavellian intelligence : social expertise and the evolution of intellect in monkeys, apes, and humans , 1990 .

[88]  L. Lefebvre,et al.  Comparing cognition across species , 2005, Trends in Cognitive Sciences.

[89]  N. Emery,et al.  The role of food- and object-sharing in the development of social bonds in juvenile jackdaws (Corvus monedula). , 2007 .

[90]  Alex H. Taylor,et al.  Spontaneous Metatool Use by New Caledonian Crows , 2007, Current Biology.

[91]  Jackie Chappell,et al.  Selection of tool diameter by New Caledonian crows Corvus moneduloides , 2004, Animal Cognition.

[92]  Glen E. Woolfenden,et al.  The Florida scrub jay : demography of a cooperative-breeding bird , 1986 .

[93]  R. Byrne,et al.  Neocortex size predicts deception rate in primates , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[94]  Richard W. Byrne,et al.  Why are animals cognitive? , 2006, Current Biology.

[95]  B. Rensch,et al.  Spontanes Öffnen verschiedener Kistenverschlüsse durch einen Schimpansen , 2010 .

[96]  Paul H. Harvey,et al.  Primates, brains and ecology , 2009 .

[97]  G. Roth,et al.  Evolution of the brain and intelligence , 2005, Trends in Cognitive Sciences.

[98]  J. Call,et al.  Chimpanzees solve the trap problem when the confound of tool-use is removed. , 2009, Journal of experimental psychology. Animal behavior processes.

[99]  E. Wasserman,et al.  Comparative cognition : experimental explorations of animal intelligence , 2009 .

[100]  Hiroko Kudo,et al.  Neocortical development and social structure in primates , 1990, Primates.

[101]  Robin I. M. Dunbar,et al.  Understanding primate brain evolution , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[102]  M. Tomasello,et al.  Apes' use of iconic cues in the object-choice task , 2006, Animal Cognition.

[103]  P. Richerson,et al.  Culture and the Evolutionary Process , 1988 .

[104]  Candy Rowe,et al.  A critique of comparative studies of brain size , 2007, Proceedings of the Royal Society B: Biological Sciences.

[105]  R. Byrne,et al.  Hand Preferences in the Skilled Gathering Tasks of Mountain Gorillas (Gorilla g. berengei) , 1991, Cortex.

[106]  S. Hirata,et al.  Chimpanzees (Pan troglodytes) learn to act with other individuals in a cooperative task , 2006, Primates.

[107]  Lowen,et al.  Neocortex Size, Social Skills and Mating Success in Primates , 1998 .

[108]  N. Emery,et al.  Postconflict Third-Party Affiliation in Rooks, Corvus frugilegus , 2007, Current Biology.

[109]  Michael Tomasello,et al.  Chimpanzees deceive a human competitor by hiding , 2006, Cognition.

[110]  Robin I. M. Dunbar Neocortex size and group size in primates: a test of the hypothesis , 1995 .

[111]  A. Dickinson,et al.  Retrospective cognition by food-caching western scrub-jays☆ , 2005 .

[112]  Richard W. Byrne,et al.  Sociality, Evolution and Cognition , 2007, Current Biology.

[113]  D. Povinelli,et al.  Chimpanzees’ (Pan troglodytes) use of gaze cues in object-choice tasks: different methods yield different results , 2004, Animal Cognition.

[114]  Carol Barner-Barry,et al.  Chimpanzee Politics: Power and Sex Among Apes. Frans de Waal. New York: Harper & Row, 1982 , 1984 .

[115]  Joanna M. Dally,et al.  Social cognition by food-caching corvids. The western scrub-jay as a natural psychologist , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[116]  M. Tomasello,et al.  Do chimpanzees know what conspecifics know? , 2001, Animal Behaviour.

[117]  M. Bitterman Toward a comparative psychology of learning. , 1960 .

[118]  Ron McClamrock,et al.  Marr's three levels: A re-evaluation , 1991, Minds and Machines.

[119]  J. Call,et al.  Raising the level: orangutans use water as a tool , 2007, Biology Letters.

[120]  Josep Call,et al.  What do bonobos (Pan paniscus) understand about physical contact? , 2006, Journal of comparative psychology.

[121]  E. Visalberghi,et al.  Lack of comprehension of cause-effect relations in tool-using capuchin monkeys (Cebus apella). , 1994, Journal of comparative psychology.

[122]  Michael Tomasello,et al.  Human-like social skills in dogs? , 2005, Trends in Cognitive Sciences.

[123]  P. Bednekoff,et al.  Observational spatial memory in Clark's nutcrackers and Mexican jays , 1996, Animal Behaviour.

[124]  S. T. Sakai,et al.  The Spotted Hyena (Crocuta crocuta) as a Model System for Study of the Evolution of Intelligence , 2007 .

[125]  A. Dickinson,et al.  Scrub jays (Aphelocoma coerulescens) form integrated memories of the multiple features of caching episodes. , 2001 .

[126]  Wolfgang Köhler,et al.  The mentality of apes, 2nd rev. ed. , 1927 .

[127]  S. Shettleworth Cognition, evolution, and behavior , 1998 .

[128]  Joanna M. Dally,et al.  Cache protection strategies by western scrub-jays, Aphelocoma californica: implications for social cognition , 2005, Animal Behaviour.

[129]  Jackie Chappell,et al.  Tool selectivity in a non-primate, the New Caledonian crow (Corvus moneduloides) , 2002, Animal Cognition.

[130]  T. Bugnyar,et al.  Gaze following in common ravens, Corvus corax: ontogeny and habituation , 2007, Animal Behaviour.

[131]  D. Mock,et al.  Monogamy and long-term pair bonding in vertebrates. , 1990, Trends in ecology & evolution.

[132]  R. Byrne The Evolution of Thought: The manual skills and cognition that lie behind hominid tool use , 2004 .

[133]  A. Iwaniuk,et al.  Is Cooperative Breeding Associated With Bigger Brains? A Comparative Test in the Corvida (Passeriformes) , 2004 .

[134]  Russell D Gray,et al.  The crafting of hook tools by wild New Caledonian crows , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[135]  A. Dickinson,et al.  Episodic-like memory during cache recovery by scrub jays , 1998, Nature.

[136]  Nicola S Clayton,et al.  Interacting Cache memories: evidence for flexible memory use by Western Scrub-Jays (Aphelocoma californica). , 2003, Journal of experimental psychology. Animal behavior processes.

[137]  T. Deacon Fallacies of progression in theories of brain-size evolution , 1990, International Journal of Primatology.