How to Build a Scrub-Jay that Reads Minds

  • Nathan J. Emery
  • Nicola S. Clayton


Although the search for human-like theory of mind (ToM) in non-human animals has continued unabated for almost 30 years, we have made very little progress in determining the psychological processes involved in non-human social cognition compared to the significant progress made in human infants. The underlying assumption that forms the basis for this research, is that ToM did not appear de novo in the evolutionary record of humans. Therefore, other animals, and most notably monkeys and apes, should at least demonstrate some of the precursors of socio-cognitive processing demonstrated by Homo sapiens. For example, there is good evidence that many animals follow another’s line of sight to external objects (e.g. monkeys; apes; dolphins; domestic dogs; goats; seals; ravens; Grey parrots, see Emery 2000 for review). However, this ability need not be explained in mentalistic terms, as in many cases it may be purely reflexive (Povinelli and Eddy 1996). Indeed, this simpler explanation seems likely based on the generality of the behaviour, and the number of species in which it has been demonstrated.


Social Cognition Knowledge Attribution Transitive Inference Grey Parrot Cache Site 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Avian Brain Nomenclature Consortium (2005) Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6:151–159Google Scholar
  2. Balda RP (2002) Pinyon jay (Gymnorhinus cuanocephalus). In: Poole A, Gill F (eds) The birds of North America, No. 605. The Birds of North America, Inc, Philadelphia, PAGoogle Scholar
  3. Balda RP, Kamil AC, Bednekoff PA (1996) Predicting cognitive capacity from natural history: examples from four species of corvids. In: Nolan V, Ketterson ED (eds) Current ornithology. Plenum Press, New York, pp 33–66Google Scholar
  4. Bednekoff PA, Balda RP (1996a) Observational spatial memory in Clark’s nuterackers and Mexican jays. Anim Behav 52:833–839CrossRefGoogle Scholar
  5. Bednekoff PA, Balda RP (1996b) Social caching and observational spatial memory in pinyon jays. Behaviour 133:807–826CrossRefGoogle Scholar
  6. Bennett ATD (1993) Spatial memory in a food storing corvid: I near tall landmarks are primarily used. J Comp Physiol A 173:193–207CrossRefGoogle Scholar
  7. Bitterman ME (1975) The comparative analysis of learning. Science 188:699–709PubMedCrossRefGoogle Scholar
  8. Bond AB, Kamil AC, Balda RP (2003) Social complexity and transitive inference in corvids. Anim Behav 65:479–487CrossRefGoogle Scholar
  9. Bugnyar T, Heinrich B (2004) Ravens, Corvus corax, differentiate between knowledgeable and ignorant conspecifies. Proc Roy Soc B 272:1641–1646CrossRefGoogle Scholar
  10. Bugnyar T, Kotrschal K (2002) Observational learning and the raiding of food caches in ravens, Corvus corax: is it “tactical” deception? Anim Behav 64:185–195CrossRefGoogle Scholar
  11. Bugnyar T, Stöwe M, Heinrich B (2007) The ontogeny of caching in ravens, Corvus corax. Anim Behav (in press)Google Scholar
  12. Clayton NS, Dickinson A (1998) Episodie-memory during cache recovery by scrub-jays. Nature 395:272–274PubMedCrossRefGoogle Scholar
  13. Clayton NS, Emery NJ (2004) Cache robbing. In: Bekoff M (ed) Encyclopaedia of animal behaviour. Greenwood Publishing Group, Westport, CT, pp 251–252Google Scholar
  14. Clayton NS, Griffiths DP, Emery NJ, Dickinson A (2001) Elements of episodie-like memory in animals, Phil Trans R Soc B 356:1483–1491PubMedCrossRefGoogle Scholar
  15. Clayton NS, Emery NJ, Dickinson A (2006) The rationality of animal memory: the cognition of caching. In: Nudds M, Hurley S (eds) Rational animals? Oxford University Press, Oxford, pp 197–216Google Scholar
  16. Clayton NS, Dally JM, Emery NJ (2007) Social cognition in food-caching corvids: the western serub-jay as a natural psychologist. Phil Trans R Soc B 362:507–522PubMedCrossRefGoogle Scholar
  17. Dally JM, Emery NJ, Clayton NS (2004) Cache protection strategies by western scrubjays (Aphelocoma californica): hiding food in the shade. Proc R Soc Biol Lett 271: S387–S390CrossRefGoogle Scholar
  18. Dally JM, Emery NJ, Clayton NS (2005a) Cache protection strategies by western scrub-jays: implications for social cognition. Anim Behav 70:1251–1263CrossRefGoogle Scholar
  19. Dally JM, Emery NJ, Clayton NS (2005b) The social suppression of caching by western scrub-jays (Aphelocoma californica). Behaviour 142:961–977CrossRefGoogle Scholar
  20. Dally JM, Emery NJ, Clayton NS (2006a) Food-caching scrub-jays keep track of who was watching when. Science 312:1662–1665PubMedCrossRefGoogle Scholar
  21. Dally JM, Clayton NS, Emery NJ (2006b) The behaviour and evolution of cache protection and pilferage. Anim Behav 72:13–23CrossRefGoogle Scholar
  22. Emery NJ (2000) The eyes have it: the neuroethology, evolution and function of social gaze. Neurosci Biobehav Rev 24:581–604PubMedCrossRefGoogle Scholar
  23. Emery NJ (2005) The evolution of social cognition. In: Easton A, Emery NJ (eds) Cognitive neuroscience of social behaviour. Psychology Press, Hove, pp 115–156Google Scholar
  24. Emery NJ (2006) Cognitive ornithology: the evolution of avian intelligence. Phil Trans R Soc B 361:23–43PubMedCrossRefGoogle Scholar
  25. Emery NJ, Clayton NS (2001) Effects of experience and social context on prospective caching strategies in serub jays. Nature 414:443–446PubMedCrossRefGoogle Scholar
  26. Emery NJ, Clayton NS (2004a) The mentality of crows: convergent evolution of intelligence in corvids and apes. Science 306:1903–1907PubMedCrossRefGoogle Scholar
  27. Emery NJ, Clayton NS (2004b) Comparing the complex cognitive abilities of birds and primates. In: Rogers LJ, Kaplan G (eds) Comparative vertebrate cognition: are primates superior to non-primates? Kluwer Academic/Plenum Publishers, New York, pp 3–55Google Scholar
  28. Emery NJ, Dally J, Clayton NS (2004) Western scrub-jays (Aphelocoma california) use cognitive strategies to protect their caches from thieving conspecifics. Anim Cogn 7:37–43PubMedCrossRefGoogle Scholar
  29. Emery NJ, Seed AM, von Bayern AMP, Clayton NS (2007) Cognitive adaptations of social bonding in birds. Phil Trans R Soc B 362:489–505PubMedCrossRefGoogle Scholar
  30. Gallup GG (1982) Self-awareness and the emergence of mind in primates. Am J Primatol 2:237–248CrossRefGoogle Scholar
  31. Gould-Beierle K (2000) A comparison of four corvid species in a working and refence memory task using a radial maze. J Comp Psychol 114:347–356PubMedCrossRefGoogle Scholar
  32. Hampton RR (1994) Sensitivity to information specifying the line of gaze of humans in sparrows (Passer domesticus). Behaviour 130:41–52CrossRefGoogle Scholar
  33. Hare B, Tomasello M (2005) Human-like social skills in dogs? Trends Cogn Sci 9:439–444PubMedCrossRefGoogle Scholar
  34. Hare B, Call J, Agnetta B, Tomasello M (2000) Chimpanzees know what conspecifics do and do not see. Anim Behav 59:771–785PubMedCrossRefGoogle Scholar
  35. Hare B, Call J, Tomasello M (2001) Do chimpanzees know what conspecifics know? Anim Behav 61:139–151PubMedCrossRefGoogle Scholar
  36. Hare B, Plyusnina I, Ignacio N, Schepina A, Wrangham R, Trut L (2005) Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Curr Biol 15:226–230PubMedCrossRefGoogle Scholar
  37. Heinrich B (1999) The mind of the raven: investigations and adventures with wolf-birds. Harper Collins, New YorkGoogle Scholar
  38. Heinrich B, Pepper JW (1998) Influence of competitors on caching behaviour in the common raven. Anim Behav 56:1083–1090PubMedCrossRefGoogle Scholar
  39. Heyes CM (1994) Anecdotes, training, trapping and triangulating: do animals attribute mental states? Anim Behav 46:177–188CrossRefGoogle Scholar
  40. Heyes CM (1998) Theory of mind in nonhuman primates. Behav Brain Sci 21:101–148PubMedGoogle Scholar
  41. Humphrey NK (1980) Nature’s psychologists. In: Josephson B, Ramachandran V (eds) Consciousness and the physical world. Pergam on Press, Oxford, pp 57–75Google Scholar
  42. Jones RB (1980) Reactions of male domestic chicks to two-dimensional eye-like shapes. Anim Behav 28:212–218CrossRefGoogle Scholar
  43. Kallander H (1978) Hoarding in the rook (Corvus frugilegus). Anser Supp 3:124–128Google Scholar
  44. Kamil A, Maudlin JE (1988) A comparative ecological approach to the study of learning. In: Bolles RC, Beecher MD (eds) Evolution and learning. Lawrence Erlbaum Associates, London, pp 117–134Google Scholar
  45. Kaminski J, Riedel J, Call J, Tomasello M (2005) Domestic goats (Capra hircus) follow gaze direction and use social cues in an object choice task. Anim Behav 69:11–18CrossRefGoogle Scholar
  46. de Kort SR, Clayton NS (2006) An evolutionary perspective on caching by corvids. Proc Roy Soc 273:417–423CrossRefGoogle Scholar
  47. de Kort SR, Tebbich S, Dally JM, Emery NJ, Clayton NS (2006) The comparative cognition of caching. In: Wasserman EA, Zentall TR (eds) Comparative cognition: experimental explanations of animal intelligence. Oxford University Press, New York, pp 602–618Google Scholar
  48. Lefebvre L, Bouchard J (2003) Social learning about food in birds. In: Fragaszy DM, Perry S (eds) The biology of traditions. Cambridge University Press, Cambridge, pp 94–126Google Scholar
  49. Lefebvre L, Nicolakakis N, Boire D (2002) Tools and brains in birds. Behaviour 139: 939–973CrossRefGoogle Scholar
  50. Lefebvre L, Whittle P, Lascaris E, Finkelstein A (1997) Feeding innovations and forebrain size in birds. Anim Behav 53:549–560CrossRefGoogle Scholar
  51. MacPhail EM (1987) The comparative psychology of intelligence. Behav Brain Sci 10: 645–696Google Scholar
  52. Nichols S, Stich SP (2003) Mindreading: an integrated account of pretence, self-awareness and understanding other minds. Oxford University Press, OxfordGoogle Scholar
  53. Olson DJ, Kamil AC, Balda RP, Nims PJ (1995) Performance of four seed-caching corvid species in operant tests of non-spatial and spatial memory. J Comp Psychol 109: 173–181PubMedCrossRefGoogle Scholar
  54. Paz-y-Mino CG, Bond AB, Kamil AC, Balda RP (2004) Pinyon jays use transitive inference to predict social dominance. Nature 430:778–781CrossRefGoogle Scholar
  55. Pepperberg IM, McLaughlin MA (1996) Effect of avian-human joint attention on allospecific vocal learning by Grey parrots (Psittacus erithacus). J Comp Psych 110:286–297CrossRefGoogle Scholar
  56. Pollock B, Prior H, Gunturkun O (2000) Development of object permanence in food-storing magpies (Pica pica). J Comp Psychol 114:148–157CrossRefGoogle Scholar
  57. Povinelli DJ (2000) Folk physics for apes. Oxford University Press, New YorkGoogle Scholar
  58. Povinelli DJ, Eddy TJ (1996) What young chimpanzees know about seeing. Monogr Soc Res Child Dev 61, Serial No. 247Google Scholar
  59. Povinelli DJ, Vonk J (2003) Chimpanzee minds: suspiciously human? Trends Cogn Sci 7:157–160PubMedCrossRefGoogle Scholar
  60. Povinelli DJ, Vonk J (2006) We don’t need a microscope to explore the chimpanzee’s mind. In: Hurley S, Nudds M (eds) Rational animals? Oxford University Press, Oxford, pp 385–412Google Scholar
  61. Povinelli DJ, Nelson K, Boysen S (1990) Inferences about guessing and knowing by chimpanzees. J Comp Psychol 104:203–210PubMedCrossRefGoogle Scholar
  62. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxino G, Shimizu T, Stiedter G, Wild M, Ball GF, Durand S, Gunturkun O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377–414PubMedCrossRefGoogle Scholar
  63. Scaife M (1976a) The response to eye-like shapes by birds I: the effect of context: a predator and a strange bird. Anim Behav 24:195–199CrossRefGoogle Scholar
  64. Scaife M (1976b) The response to eye-like shapes by birds II: the importance of staring, pairedness and shape. Anim Behav 24:200–206CrossRefGoogle Scholar
  65. Shettleworth SJ (1998) Cognition, evolution and behavior. Oxford University Press, New YorkGoogle Scholar
  66. Smith PK (1996) Language and the evolution of mind-reading. In: Carruthers P, Smith PK (eds) Theories of theories of mind. Cambridge University Press, Cambridge, pp 344–354Google Scholar
  67. Striedter GF (2005) Principles of brain evolution. Sinauer Associates Inc, Sunderland, MAGoogle Scholar
  68. Tomasello M, Call J (1997) Primate cognition. Oxford University Press, New YorkGoogle Scholar
  69. Tomonaga M (2006) Development of chimpanzee social cognition in the first 2 years of life. In: Matsuzawa T, Tomonaga M, Tanaka M (eds) Cognitive development in chimpanzees. Springer-Verlag, Tokyo, pp 182–197CrossRefGoogle Scholar
  70. Tschudin AJ-PC (2006) Belief attribution tasks with dolphins: what social minds can reveal about animal rationality. In: Hurley S, Nudds M (eds) Rational animals? Oxford University Press, Oxford, pp 413–436Google Scholar
  71. Vander Wall SB (1990) Food hoarding in animals. University of Chicago Press, Chicago, ILGoogle Scholar
  72. Watve M, Thakar J, Kale A, Putambekar S, Shaikh I, Vaze K, Jog M, Paraniape S (2002) Bee-eaters (Merops orientalis) respond to what a predator can see. Anim Cogn 5:253–259PubMedCrossRefGoogle Scholar
  73. Whiten A, Byrne RW (1988) Tactical deception in primates. Behav Brain Sci 11:233–277CrossRefGoogle Scholar
  74. Zentall TR (2004) Action imitation in birds. Learn Behav 32:15–23PubMedGoogle Scholar

Copyright information

© Springer 2008

Authors and Affiliations

  • Nathan J. Emery
    • 1
  • Nicola S. Clayton
    • 2
  1. 1.School of Biological and Chemical SciencesQueen Mary University of LondonLondonUK
  2. 2.Department of Experimental PsychologyUniversity of CambridgeCambridgeUK

Personalised recommendations