Animal Cognition

, Volume 16, Issue 4, pp 583–597 | Cite as

Tests of inferential reasoning by exclusion in Clark’s nutcrackers (Nucifraga columbiana)

  • Jan K. TornickEmail author
  • Brett M. Gibson
Original Paper


We examined inferential reasoning by exclusion in the Clark’s nutcracker (Nucifraga columbiana) using two-way object-choice procedures. While other social scatter-hoarding corvids appear capable of engaging in inferential reasoning, it remains unclear if the relatively less social nutcracker is able to do so. In an initial experiment, food was hidden in one of two opaque containers. All of the birds immediately selected the baited container when shown only the empty container during testing. We subsequently examined the nutcrackers in two follow-up experiments using a task that may have been less likely to be solved by associative processes. The birds were trained that two distinctive objects were always found hidden in opaque containers that were always positioned at the same two locations. During testing, one of the two objects was found in a transparent “trash bin” and was unavailable. The birds were required to infer that if one of the objects was in the “trash,” then the other object should still be available in its hidden location. Five out of six birds were unable to make this inference, suggesting that associative mechanisms likely accounted for our earlier results. However, one bird consistently chose the object that was not seen in the “trash,” demonstrating that nutcrackers may have the ability to use inferential reasoning by exclusion to solve inference tasks. The role of scatter hoarding and social organization is discussed as factors in the ability of corvid birds to reason.


Clark’s nutcracker Inference Reasoning Exclusion performance Adaptive specialization Social intelligence hypothesis 



We thank Robert Drugan, Winsor Watson, Michelle Pellissier Scott, and Robert Mair for their advice and support; Daniel Landry, Lindsey MacMillan, Alex Politis, and Erin Cuneo for testing and animal care. Funding was provided by Summer Teaching Assistant Fellowships and a Dissertation Year Fellowship though Graduate School at the University of New Hampshire.

Supplementary material

Supplementary material 1 (WMV 7310 kb)

Supplementary material 2 (WMV 4396 kb)


  1. Aust U, Range F, Steurer M, Huber L (2008) Inferential reasoning by exclusion in pigeons, dogs and humans. Anim Cogn 11(4):587–597PubMedCrossRefGoogle Scholar
  2. Balda RP, Kamil AC, Bednekoff PA (1996) Predicting cognitive capacity from natural history: examples from four species of corvids. In: Nolan V, Ketterson JR (eds) Current ornithology, vol 13. Plenum Press, New York, pp 33–66CrossRefGoogle Scholar
  3. Bednekoff PA, Balda RP (1996) Observational spatial memory in Clark’s nutcrackers and Mexican jays. Anim Behav 52:833–839CrossRefGoogle Scholar
  4. Beran MJ, Washburn DA (2002) Chimpanzee responding during matching to sample: control by exclusion. J Exp Anal Behav 78:497–508PubMedCrossRefGoogle Scholar
  5. Bond AB, Kamil AC, Balda RP (2003) Social complexity and transitive inference in corvids. Anim Behav 65:479–487CrossRefGoogle Scholar
  6. Bossema L (1979) Jays and oaks: an eco-ethological study of a symbiosis. Behaviour 70:1–117CrossRefGoogle Scholar
  7. Boysen ST, Berntson GG (1995) Responses to quantity: perceptual vs. cognitive mechanisms in chimpanzees (Pan troglodytes). J Exp Psychol Anim Behav Process 21:83–86CrossRefGoogle Scholar
  8. Bräuer J, Kaminski J, Riedel J, Call J, Tomasello M (2006) Making inference about the location of hidden food: social dog, causal ape. J Comp Psychol 120(1):38–47PubMedCrossRefGoogle Scholar
  9. Bugnyar T, Heinrich B (2005) Ravens, Corvus corax, differentiate between knowledgeable and ignorant conspecifics. Proc R Soc Lond B Biol Sci 272:1641–1646CrossRefGoogle Scholar
  10. Bugnyar T, Kotrschal K (2002) Leading a conspecific away from food in ravens, Corvus corax? Anim Cogn 7:69–76CrossRefGoogle Scholar
  11. Burnell KL, Tomback DF (1985) Stellar’s jays steal gray jay caches: field and laboratory observations. The Auk 102:417–419CrossRefGoogle Scholar
  12. Byrne RW, Whiten A (eds) (1988) Machiavellian intelligence: social expertise and the evolution of intellect in monkeys. Apes and Humans, Clarendon, pp 1–23Google Scholar
  13. Call J (2004) Inferences about the location of food in the great apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, and Pongo pygmaeus). J Comp Psychol 118(2):232–241PubMedCrossRefGoogle Scholar
  14. Clarkson K, Eden SF, Sutherland WJ, Houston AI (1986) Density dependence and magpie food hoarding. J Anim Ecol 55:11–121CrossRefGoogle Scholar
  15. Clayton NS, Dickinson A (1998) Episodic-like memory during cache recovery by scrub jays. Nature 395:272–278PubMedCrossRefGoogle Scholar
  16. Correia SP, Dickinson A, Clayton NS (2007) Western scrub-jays anticipate future needs independently of their current motivational state. Curr Biol 17(10):856–861PubMedCrossRefGoogle Scholar
  17. Cramp S, Perrins C (1994) Handbook of the birds of Europe, the Middle East and North Africa: the birds of the Western Palearctic. Vol VIII crows to finches. Oxford University Press, Oxford, pp 12–19Google Scholar
  18. Dally JM, Emery NJ, Clayton NS (2004) Cache protection strategies by western scrub-jays (Aphelocoma californica): hiding food in the shade. Proc Roy Soc Lond B 271:S387–S390CrossRefGoogle Scholar
  19. Dally JM, Emery NJ, Clayton NS (2005a) Cache protection strategies by western scrub-jays, Aphelocoma californica: implications for social cognition. Anim Behav 70:1251–1263CrossRefGoogle Scholar
  20. Dally JM, Emery NJ, Clayton NS (2005b) The social suppression of caching in western scrub-jays (Aphelocoma californica). Behaviour 142:961–977CrossRefGoogle Scholar
  21. de Kort SR, Clayton NS (2006) An evolutionary perspective on caching by corvids. Proc R Soc Lond B 273:417–423CrossRefGoogle Scholar
  22. Ekman J, Ericson GP (2006) Out of Gondwanaland; the evolutionary history of cooperative breeding and social behavior among crows, magpies, jays and allies. Proc Royal Soc Lond B 273:1117–1125CrossRefGoogle Scholar
  23. Emery NJ (2006) Cognitive ornithology: the evolution of avian intelligence. Philos Tran Roy Soc B 361:23–43CrossRefGoogle Scholar
  24. Emery NJ, Clayton NS (2001) Effects of experience and social context on prospective caching strategies by scrub jays. Nature 414:443–446PubMedCrossRefGoogle Scholar
  25. Emery NJ, Clayton NS (2004) The mentality of crows: convergent evolution of intelligence in corvids and apes. Science 306(5703):59–84CrossRefGoogle Scholar
  26. Erdöhegyi A, Topál J, Virányi Z, Miklósi A (2007) Dog-logic: inferential reasoning in a two-way choice task and its restricted use. Anim Behav 74(4):725–737CrossRefGoogle Scholar
  27. Ericson GP, Jansen A, Johansson US, Ekman J (2005) Inter-generic relationships of the crows, jays, magpies and allied groups (Aves: Corvidae) based on nucleotide sequence data. J Avian Biol 36:222–234CrossRefGoogle Scholar
  28. Gibson BM, Kamil AC (2001) Search for a hidden goal by Clark’s nutcrackers (Nucifraga columbiana) is more accurate inside than outside a landmark array. Anim Learn Behav 29:234–249CrossRefGoogle Scholar
  29. Gibson BM, Kamil AC (2005) The fine-grained spatial abilities of three seed-caching corvids. Learn Behav 33:59–66PubMedCrossRefGoogle Scholar
  30. Goodwin D (1955) Jays and crows recovering hidden food. Br Bird 48:181–183Google Scholar
  31. Gould-Beierle K (2000) A comparison of four corvid species in a working and reference memory task using a radial maze. J Comp Psychol 114(4):347–356PubMedCrossRefGoogle Scholar
  32. Heinrich B, Pepper J (1998) Influence of competitors on caching behaviour in the common raven, Corvus corax. Anim Behav 56:1083–1090PubMedCrossRefGoogle Scholar
  33. Hermann LM, Richards DG, Wolz JP (1984) Comprehension of sentences by bottlenose dolphins. Cognition 16:129–219CrossRefGoogle Scholar
  34. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  35. Holyoak KJ, Morrison RG (eds) (2005) Cambridge handbook of thinking and reasoning. Cambridge University Press, Cambridge, MA, p 763Google Scholar
  36. Hunt GR, Gary RD (2004) Direct observations of pandanus-tool manufacture and use by a New Caledonian crow (Corvus moneduloides). Anim Cogn 7(2):114–120PubMedCrossRefGoogle Scholar
  37. Hunt GR, Rutledge RB, Gary RD (2006) The right tool for the job: what strategies do wild New Caledonian crows use? Anim Cogn 9:307–316PubMedCrossRefGoogle Scholar
  38. James PC, Verbeek NAM (1984) Temporal and energetic aspects of food storage in northwestern crows. Ardea 72:207–216Google Scholar
  39. Kamil AC (1988) A synthetic approach to the study of animal intelligence. In: Ledger DW (ed) Comparative perspectives in modern psychology, Nebraska symposium on motivation, vol 35, pp 230–257Google Scholar
  40. Kaminski J, Call J, Fischer J (2004) Word learning in a domestic dog: evidence for ‘‘fast mapping’’. Science 304:1682–1683PubMedCrossRefGoogle Scholar
  41. Kastak CR, Schustermann RJ (2002) Sea lions and equivalence: expanding classes by exclusion. J Exp Anal Behav 78:449–465PubMedCrossRefGoogle Scholar
  42. Köhler W (1951) The mentality of apes. Translated from the second revised edition by Ella Winter Routledge, Kegan (eds), Humanities Press Inc., Imprint New York, London, p 190Google Scholar
  43. Lanner RM (1996) Made for each other a symbiosis of birds and pines. Oxford University Press, New York NY, pp 38–48Google Scholar
  44. Ludbrook J (1998) Multiple comparison procedures updated. Clin Exp Pharmacol Physiol 25:1032–1037PubMedCrossRefGoogle Scholar
  45. Mikolasch S, Kotrschal K, Schloegl C (2011) African grey parrots (Psittacus erithacus) use inference by exclusion to find hidden food. Biol Lett 7(6):875–877. doi: 10.1098/rsbl.2011.0500 PubMedCrossRefGoogle Scholar
  46. Mikolasch S, Kotrschal K, Schloegl C (2012) Is caching the key to exclusion in corvids? The case of carrion crows (Corvus corone corone). Anim Cogn 15:73–82. doi: 101007/s10071-011-0434-1 PubMedCrossRefGoogle Scholar
  47. Mischel W, Shoda Y, Rodriguez ML (1989) Delay of gratification in children. Sci 244:933–937Google Scholar
  48. Paukner A, Anderson JR, Fujita K (2006) Redundant food searches by capuchin monkeys (Cebus apella): a failure of metacognition? Anim Cogn 9:110–117PubMedCrossRefGoogle Scholar
  49. Paz-y-Mino GC, Bond AB, Kamil AC, Balda RP (2004) Pinyon jays use transitive inference to predict social dominance. Nature 430:778–781CrossRefGoogle Scholar
  50. Petit O, Call J, Thierry B (2005) Inference about food location in Tonkean macaques. Primate Rep 72:76Google Scholar
  51. Pilley JW, Reid AK (2011) Border collie comprehends object names as verbal referents. Behav Process 86(2):184–195CrossRefGoogle Scholar
  52. Pollok B, Prior H, Gtinttirktin O (2000) Development of object permanence in food-storing magpies (Pica pica). J Comp Psychol 114(2):148–157PubMedCrossRefGoogle Scholar
  53. Premack D, Premack AJ (1994) Levels of causal understanding in chimpanzees and children. Cognition 50:347–362PubMedCrossRefGoogle Scholar
  54. Rifkin S (2007) The evolution of primate intelligence. In volume 2 of the Harvard Undergraduate Society for Neuroscience’s BRAIN magazine. http://wwwhcsharvardedu/~husn/BRAIN/vol2/Primatehtml. That site (and presumably the society) is now defunct
  55. Sabbatini G, Visalberghi E (2008) Inferences about the location of food in Capuchin monkeys (Cebus apella) in two sensory modalities. Anim Behav 122(2):156–166Google Scholar
  56. Salwiczek LH, Emery NJ, Schlinger B, Clayton NS (2009) The development of caching and object permanence in Western scrub-jays (Aphelocoma californica): which emerges first? J Comp Psychol 123(3):295–303PubMedCrossRefGoogle Scholar
  57. Schloegl C (2011) What you see is what you get–reloaded: can jackdaws (Corvus monedula) find hidden food through exclusion? J Comp Psychol 125(2):162–174PubMedCrossRefGoogle Scholar
  58. Schloegl C, Dierks A, Gajdon GK, Huber L, Kotrschal K, Bugnyar T (2009) What you see is what you get? Exclusion performances in ravens and keas. PLoS ONE 4(8):1–12CrossRefGoogle Scholar
  59. Schloegl C, Kortschal K, Bugnyar T (2007) Gaze following in common ravens, Corvus corax: ontogeny and habituation. Anim Behav 74:769–778CrossRefGoogle Scholar
  60. Schloegl C, Kortschal K, Bugnyar T (2008) Do common ravens (Corvus corax) rely on human or conspecific gaze cues to detect hidden food? Anim Cogn 11:231–241PubMedCrossRefGoogle Scholar
  61. Schmitt V, Fischer J (2009) Inferential reasoning and modality dependent discrimination learning in olive baboons (Papio hamadryas anubis). J Comp Psychol 123(3):316–325PubMedCrossRefGoogle Scholar
  62. Schustermann RJ, Krieger K (1984) California sea lions are capable of semantic comprehension. Psychol Rec 34:3–23Google Scholar
  63. Shettleworth SJ (2010) Cognition, evolution, and behavior. Oxford University Press, New York, pp 51–53Google Scholar
  64. Shettleworth SJ, Hampton RR (1998) Adaptive specializations of spatial cognition in food-storing birds? Approaches to testing a comparative hypothesis. In: Balda RP, Pepperberg IM, Kamil AC (eds) Animal cognition in nature. RP Academic Press, San Diego, pp 65–98CrossRefGoogle Scholar
  65. Simmons KEL (1968) Food-hiding by rooks and other crows. Brit Birds 61:228–229Google Scholar
  66. Simonton DK (1995) Foresight in insight? A Darwinian answer. In: Sternberg RJ, Davidson JE (eds) The nature of insight. MIT Press, Cambridge, MA, pp 465–494Google Scholar
  67. Tobin H, Logue AW (1994) Self-control across species (Columba livia, Homo sapiens, and Rattus norvegicus). J Comp Psychol 108:126–133PubMedCrossRefGoogle Scholar
  68. Tomonaga M (1993) Test for control by exclusion and negative stimulus relations of arbitrary matching to sample in a ‘‘symmetry-emergent’’ chimpanzee. J Exp Anal Behav 59:215–229PubMedCrossRefGoogle Scholar
  69. Tornick JK, Gibson BM, Kispert D, Wilkinson M (2011) Clark’s nutcrackers (Nucifraga columbiana) use gestures to locate hidden food. Anim Cogn 14:117–125PubMedCrossRefGoogle Scholar
  70. Waite TA, Reeve JD (1995) Source-use decisions by hoarding gray jays: effects of local cache density and food value. J Avian Biol 26:59–66Google Scholar
  71. Zucca P, Milos N, Vallortigara G (2007) Piagetian object permanence and its development in Eurasian jays (Garrulus glandarius). Anim Cogn 10(2):243–258PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of New HampshireDurhamUSA

Personalised recommendations