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Clark’s nutcrackers (Nucifraga columbiana) use gestures to identify the location of hidden food

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Abstract

Heterospecific cues, such as gaze direction and body position, may be an important source of information that an animal can use to infer the location of resources like food. The use of heterospecific cues has been largely investigated using primates, dogs, and other mammals; less is known about whether birds can also use heterospecific gestures. We tested six Clark’s nutcrackers in a two-way object-choice task using touch, point, and gaze cues to investigate whether these birds can use human gestures to find food. Most of the birds were able to use a touch gesture during the first trial of testing and were able to learn to use point and gaze (eyes and head alternation) cues after a limited number of trials. This study is the first to test a non-social corvid on the object-choice task. The performance of non-social nutcrackers is similar to that of more social and related corvids, suggesting that species with different evolutionary histories can utilize gestural information.

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References

  • Anderson JR, Sallaberry P, Barbier H (1995) Use of experimenter-given cues during object-choice tasks by capuchin monkeys. Anim Behav 49:201–208

    Google Scholar 

  • Anderson JR, Montant M, Schmitt D (1996) Rhesus monkeys fail to use gaze direction as an experimenter-given cue in an object-choice task. Behav Process 37:47–55

    Article  Google Scholar 

  • Balda RP, Kamil AC (1988) The spatial memory of Clark’s nutcrackers (Nucifraga columbiana) in an analogue of the radial arm maze. Anim Learn Behav 16:116–122

    Google Scholar 

  • Barth J, Reaux JE, Povinelli DJ (2005) Chimpanzees’ (Pan troglodytes) use of gaze cues in object- choice tasks: Different methods yield different results. Anim Cogn 8:84–92

    Article  PubMed  Google Scholar 

  • Brauer J, Call J, Tomasello M (2005) All great ape species follow gaze to distant locations and around barriers. J Comp Psychol 119:145–154

    Article  PubMed  Google Scholar 

  • Bugnyar T, Stöwe M, Bernd H (2004) Ravens, Corvus corax, follow gaze direction of humans around obstacles. Proc Biol Sci 271:1331–1336

    Article  PubMed  Google Scholar 

  • Byrnit JT (2004) Nonenculturated orangutans (Pongo Pygmaeus) use of experimenter-given manual and facial cues in an object-choice task. J Comp Psychol 118:309–315

    Article  PubMed  Google Scholar 

  • Call J, Tomasello M (1994) Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). J Comp Psych 108:307–317

    Article  CAS  Google Scholar 

  • Call J, Hare B, Tomasello M (1998) Chimpanzee gaze following in an object-choice task. Anim Cogn 1:89–99

    Article  Google Scholar 

  • Carter J, Lyons NJ, Cole HL, Goldsmith AR (2008) Subtle cues of predation risk: starlings respond to a predator’s direction of eye gaze. Proc R Soc Lond B Biol Sci 275:1709–1715

    Article  Google Scholar 

  • Clayton NS, Emery NJ (2007) The social life of corvids. Curr Biol 17:R652–R656

    Article  CAS  PubMed  Google Scholar 

  • Emery NJ (2000) The eyes have it: the neuroethology, function, and evolution of social gaze. Neurosci Biobehav Rev 2000:581–604

    Article  Google Scholar 

  • Emery NJ, Clayton NS (2009) Comparative social cognition. Annu Rev Psychol 60:87–113

    Article  PubMed  Google Scholar 

  • 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 36:222–234

    Article  Google Scholar 

  • Flombaum JI, Santos LR (2005) Rhesus monkeys attribute perceptions to others. Curr Biol 15:447–452

    Article  CAS  PubMed  Google Scholar 

  • Fritz J, Kotrschal K (1999) Social learning in common ravens, Corvus corax. Anim Behav 57:785–793

    Article  PubMed  Google Scholar 

  • 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 29:234–249

    Google Scholar 

  • Gibson BM, Kamil AC (2005) The fine-grained spatial abilities of three seed-caching corvids. Learn Behav 33:59–66

    PubMed  Google Scholar 

  • Gibson BM, Kamil AC (2009) The synthetic approach to the study of spatial memory: have we properly addressed Tinbergen’s “four questions?”. Behav Process 80:278–287

    Article  Google Scholar 

  • Gibson BM, Wilks T (2008) The use of self-motion cues and landmarks by Clark's nutcrackers (Nucifraga columbiana) during a small-scale search task. Anim Behav 76(4):1305–1317

    Google Scholar 

  • Giret N, Miklósi Á, Kreutzer M, Bovet D (2009) Use of experimenter-given cues by African gray parrots (Psittacus erithacus). Anim Cogn 12:1–10

    Article  PubMed  Google Scholar 

  • Hampton RR (1994) Sensitivity to information specifying the line of gaze of humans in sparrows (Passer domesticus). Behav 130:41–51

    Article  Google Scholar 

  • Hare B (2001) Can competitive paradigms increase the validity of experiments on primate social cognition? Anim Cogn 4:269–280

    Article  Google Scholar 

  • Hare B, Tomasello M (1999) Domestic dogs (Canis familiaris) use human and conspecific social cues to locate hidden food. J Comp Psych 113:173177

    Google Scholar 

  • Hare B, Call J, Agnetta B, Tomasello M (2000) Chimpanzees know what conspecifics do and do not see. Anim Behav 59:771–785

    Article  PubMed  Google Scholar 

  • Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636

    Article  CAS  PubMed  Google Scholar 

  • Hauser M, Glynn D, Wood J (2007) Rhesus monkeys correctly read the goal-relevant gestures of a human agent. Proc R Acad B 274:1913–1918

    Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Statist 6:65–70

    Google Scholar 

  • Itakura S, Anderson JR (1996) Learning to use experimenter-given cues during an object-choice task by a capuchin monkey. Curr Psych Cogn 15:103–112

    Google Scholar 

  • Itakura S, Tanaka M (1998) Use of experimenter given cues during object-choice tasks by chimpanzees (Pan troglodytes), an orangutan (Pongo pygmaeus), and human infants (Homo sapiens). J Comp Psych 112:119–126

    Article  CAS  Google Scholar 

  • Jaime M, Lopez JP, Lickliter R (2009) Bobwhite quail (Colinus virginianus) hatchlings track the direction of human gaze. Anim Cogn 12:559–565

    Article  PubMed  Google Scholar 

  • Kaminski J, Riedel J, Call J, Tomasello M (2005) Domestic goats (Capra hircus) follow gaze direction and use some social cues in an object choice task. Anim Behav 69:11–18

    Article  Google Scholar 

  • Kelly DM (2010) Features enhance the encoding of geometry. Anim Cogn 13:453–462

    Article  PubMed  Google Scholar 

  • LaDage LD, Roth TC II, Fox AF, Pravosudov VV (2009) Flexible cue use in food-caching birds. Anim Cogn 12:419–426

    Article  PubMed  Google Scholar 

  • Ludbrook J (1998) Multiple comparison procedures updated. Clin Exp Pharmacol Physiol 25:1032–1037

    Article  CAS  PubMed  Google Scholar 

  • MacDonald SE (1994) Gorilla’s (Gorilla gorilla gorilla) spatial memory in a foraging task. J Comp Psych 108:107–113

    Article  CAS  Google Scholar 

  • McKinley J, Shambrook TD (2000) Use of human-given cues by domestic dogs (Canis familiaris) and horses (Equus caballus). Anim Cogn 3:13–22

    Article  Google Scholar 

  • Menzel CR (1999) Unprompted recall and reporting of hidden objects by a chimpanzee (Pan troglodytes) after extended delays. J Comp Psych 113:426–434

    Article  CAS  Google Scholar 

  • Mewaldt JM (1956) Nesting behavior of the Clark’s nutcracker. Condor 58:3–23

    Article  Google Scholar 

  • Miklósi Á, Soproni K (2006) A comparative analysis of animals’ understanding of the human pointing gesture. Anim Cogn 9:81–93

    Article  PubMed  Google Scholar 

  • Miklósi Á, Polgárdi R, Topál J, Csányi V (1998) Use of experimenter given cues in dogs. Anim Cogn 1:113–121

    Article  Google Scholar 

  • Miklósi Á, Kubinyi E, Topál J, Gácsi M, Virányi Z, Csányi V (2003) A simple reason for a big difference: Wolves do not look back at humans but dogs do. Curr Biol 13:763–766

    Article  PubMed  Google Scholar 

  • Nieworth JJ, Burman MA, Basile BM, Lickteig MT (2002) Use of experimenter-given cues in visual co-orienting and in an object-choice task by a new world monkey species, cotton-top tamarins (Saguinus oedipus). J Comp Psych 116(1):1–3

    Google Scholar 

  • Peignot P, Anderson JR (1999) Use of experimenter given manual and facial cues by gorillas (Gorilla gorilla) in an object-choice task. J Comp Psychol 113:253–260

    Article  Google Scholar 

  • Povinelli DJ, Eddy TJ (1996) Chimpanzees: joint visual attention. Psychol Sci 7:129–135

    Article  Google Scholar 

  • Povinelli DJ, Reaux JE, Bierschwale DT, Allain AD, Simon BB (1997) Exploitation of pointing as a referential gesture in young children, but not adolescent chimpanzees. Cogn Dev 12:423–461

    Article  Google Scholar 

  • Pravosudov VV, Clayton NS (2001) Effects of demanding foraging conditions on cache retrieval accuracy in food-caching mountain chickadees (Poecile gambeli). Proc Biol Sci 268:363–368

    Google Scholar 

  • Premack D (1988) “Does the chimpanzee have a theory of mind?” revisited. In: Byrne RW, Whiten A (eds) Machiavellian Intelligence. Oxford University Press, New York, pp 160–178

    Google Scholar 

  • Proops L, McComb K (2010) Attributing attention: the use of human-given cues by domestic horses (Equus caballus). Anim Cogn 13:197–205

    Article  PubMed  Google Scholar 

  • Schloegl C, Kotrschal K, Bugnyar T (2008a) Do common ravens (Corvus corax) rely on human or conspecific gaze cues to detect hidden food? Anim Cogn 11:231–241

    Article  PubMed  Google Scholar 

  • Schloegl C, Kotrschal K, Bugnyar T (2008b) Modifying the object-choice task: is the way you look important for ravens? Behav Process 77:61–65

    Article  Google Scholar 

  • Schwartz BL, Colon MR, Sanchez IC, Rodriguez IA, Evans S (2002) Single-trial learning of “what” and “who” information in a gorilla (Gorilla gorilla gorilla): implications for episodic memory. Anim Cogn 5(2):85–90

    Article  PubMed  Google Scholar 

  • Smith BP, Litchfield CA (2010) Dingoes (Canis dingo) can use human social cues to locate hidden food. Anim Cogn 13:367–376

    Article  PubMed  Google Scholar 

  • Sokolov EN (1963) Higher nervous functions—orienting reflex. Ann Rev Physiol 25:545–562

    Article  CAS  Google Scholar 

  • Soproni K, Miklósi Á, Topál J, Csányi V (2002) Dogs’ (Canis familiaris) responsiveness to human pointing gestures. J Comp Psychol 116:27–34

    Article  PubMed  Google Scholar 

  • Tomasello M, Call J, Gluckman A (1997) Comprehension of novel communicative signs by apes and human children. Child Dev 68:1067–1080

    Article  CAS  PubMed  Google Scholar 

  • Tomasello M, Hare B, Agnetta B (1999) Chimpanzees, Pan troglodytes, follow gaze direction geometrically. Anim Behav 58:769–777

    Article  PubMed  Google Scholar 

  • Virányi Z, Gácsi M, Kubinyi E, Topál J, Belényi B, Ujfalussy D, Miklósi Á (2008) Comprehension of human pointing in young human-reared wolves (Canis lupus) and dogs (Canis familiaris). Anim Cogn 11:373–387

    Article  PubMed  Google Scholar 

  • von Bayern AMP, Emery NJ (2009) Jackdaws respond to human attentional states and communicative cues in different contexts. Curr Biol 19:1–5

    Article  Google Scholar 

  • Wood JN, Glynn DD, Phillips BC, Hauser MD (2007) The perception of rational, goal-directed action in nonhuman primates. Science 317:1402–1405

    Article  CAS  PubMed  Google Scholar 

  • Zuberbühler K (2008) Gaze following. Curr Biol 18:R453–R455

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Robert Drugan and William Stine for their advice and support; Kasandra Babineau for testing and animal care; and Erika Wells for photography. The experiment complies with the US laws concerning animal care, and was reviewed and approved by the University of New Hampshire (UNH) Institutional Animal Care and Use Committee (IACUC). The authors declare that they have no conflict of interest.

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Correspondence to Jan K. Tornick.

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Tornick, J.K., Gibson, B.M., Kispert, D. et al. Clark’s nutcrackers (Nucifraga columbiana) use gestures to identify the location of hidden food. Anim Cogn 14, 117–125 (2011). https://doi.org/10.1007/s10071-010-0349-2

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  • DOI: https://doi.org/10.1007/s10071-010-0349-2

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