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Animal Cognition

, Volume 16, Issue 1, pp 35–43 | Cite as

Ravens (Corvus corax) are indifferent to the gains of conspecific recipients or human partners in experimental tasks

  • Felice Di Lascio
  • François Nyffeler
  • Redouan Bshary
  • Thomas Bugnyar
Original Paper

Abstract

Although cooperative behaviours are common in animals, the cognitive processes underpinning such behaviours are very likely to differ between species. In humans, other-regarding preferences have been proposed to sustain long-term cooperation between individuals. The extent to which such psychological capacities exist in other animals is still under investigation. Five hand-reared ravens were first tested in an experiment where they could provide food to a conspecific at no cost to themselves. We offered them two behavioural options that provided identical amounts of food to the actor and where one of the two options additionally delivered a reward to a recipient. Subsequently, we made the ravens play a no-cost cooperation game with an experimenter. The experimenter had the same options as the animals and matched the ravens’ choices, making the prosocial choice the more profitable option. In both conditions, ravens were indifferent to the effects of their choices and hence failed to help conspecifics and to cooperate with the experimenter. While our negative results should be interpreted with care, overall, our findings suggest that the ravens had no understanding of the consequences of their actions for a potential recipient. This study adds to several others that have used a similar set-up and have reported negative results on other-regarding preferences in animals.

Keywords

Ravens Corvus corax Other-regarding preferences No-cost cooperation 

Notes

Acknowledgments

We thank Kurt Kotrschal, Chris Schloegl and Anna Braun for their great support on site, and three referees for their constructive comments. We thank also Sharon Wismer for having improved our English and Albert Ros for his advices regarding the power analysis. RB is financed by the Swiss Science Foundation. The study has been co-funded by the COCOR project I 105-G11 conducted within the ESF-EUROCORES framework TECT. Permanent support is provided by the ‘Verein d. Förderer KLF’ and the Herzog von Cumberland Stiftung. We are grateful to the zoos Wien and Wuppertal for the donation of raven nestlings and P. Sömmer for help with capturing wild birds. Permission to take nestlings from the wild was derived from the Ministerium für Landwirtschaft, Umweltschutz und Raumordnung des Landes Brandenburg.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Aureli F, de Waal FBM (2000) In: Aureli F, de Waal FBM (eds) Natural conflict resolution. University of California Press, BerkeleyGoogle Scholar
  2. Baumard N, André JB, Sperber D (2012) A mutualistic approach to morality. Behav Brain Sci (submitted)Google Scholar
  3. Boesch C (2007) What makes us human (Homo sapiens)? The challenge of cognitive crossspecies comparison. J Comp Psychol 121:227–240. doi: 10.1037/0735-7036.121.3.227 PubMedCrossRefGoogle Scholar
  4. Boesch C, Boesch H (1989) Hunting behavior of wild chimpanzees in the thai-national-park. Am J Phys Anthropol 78:547–573PubMedCrossRefGoogle Scholar
  5. Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287. doi: 10.1046/j.1461-0248.2001.00218.x CrossRefGoogle Scholar
  6. Brosnan SF, de Waal FBM (2003) Monkeys reject unequal pay. Nature 425:297–299. doi: 10.1038/nature01963 PubMedCrossRefGoogle Scholar
  7. Brosnan SF, Silk JB, Heinrich J, Mareno MC, Lambeth SP, Schapiro SJ (2009) Chimpanzees (Pan troglodytes) do not develop contingent reciprocity in an experimental task. Anim Cogn 12:587–597. doi: 10.1007/s10071-009-0218-z PubMedCrossRefGoogle Scholar
  8. Brosnan SF, Salwiczek L, Bshary R (2010) The interplay of cognition and cooperation. Phil Trans R Soc B 365:2699–2710. doi: 10.1098/rstb.2010.0154 PubMedCrossRefGoogle Scholar
  9. Bshary R, Bergmueller R (2008) Distinguishing four fundamental approaches to the evolution of helping. J Evol Biol 21:405–420. doi: 10.1111/j.1420-9101.2007.01482.x PubMedCrossRefGoogle Scholar
  10. Bshary R, Bronstein JL (2004) Game structures in mutualisms: what can the evidence tell us about the kind of models we need? Adv Study Behav 34:59–101. doi: 10.1016/S0065-3454(04)34002-7 CrossRefGoogle Scholar
  11. Bshary R, Grutter AS, Willener AST, Leimar O (2008) Pairs of cooperating cleaner fish provide better service quality than singletons. Nature 455:964–966. doi: 10.1038/nature07184 PubMedCrossRefGoogle Scholar
  12. Bugnyar T, Kortschal K (2002) Observational learning and the raiding of food caches in ravens, Corvus corax: is it “tactical” deception? Anim Behav 64:185–195. doi: 10.1006/anbe.2002.3056 CrossRefGoogle Scholar
  13. Bugnyar T, Schwab C, Schloegel C, Kotrschal K, Heinrich B (2007) Ravens judge competitors through experience with play caching. Curr Biol 17:1804–1808. doi: 10.1016/j.cub.2007.09.048 PubMedCrossRefGoogle Scholar
  14. Burkart JM, Fehr E, Efferson C, Van Schaik CP (2007) Other-regarding preferences in a non-human primate: common marmosets provision food altruistically. PNAS 104:19762–19766. doi: 10.1073/pnas.0710310104 PubMedCrossRefGoogle Scholar
  15. Burkart JM, Hrdy SB, Van Schaik CP (2009) Cooperative breeding and human cognitive evolution. Evol Anthropol 18:175–186. doi: 10.1002/evan.20222 CrossRefGoogle Scholar
  16. Call J, Tomasello M (1996) The effect of humans on the cognitive development of apes. In: Russon AE, Bard KA, Parker ST (eds) Reaching into thought: the minds of the great apes. Cambridge University Press, Cambridge, UK, pp 371–403Google Scholar
  17. Colman AD, Liebold KE, Boren JJ (1969) A method for studying altruism in monkeys. Psychol Rec 19:401–405Google Scholar
  18. Cronin KA, Schroeder KKE, Rothwell ES, Silk JB, Snowdon CT (2009) Cooperatively breeding cottontop tamarins (Saguinus oedipus) do not donate rewards to their long-term mates. J Comp Psychol 123:231–241. doi: 10.1037/a0015094 PubMedCrossRefGoogle Scholar
  19. Cronin KA, Schroeder KKE, Snowdon CT (2010) Prosocial behaviour emerges independent of reciprocity in cottontop tamarins. Proc R Soc B 277:3845–3851. doi: 10.1098/rspb.2010.0879 PubMedCrossRefGoogle Scholar
  20. Dally JM, Emery NJ, Clayton NS (2006) Food-caching Western scrub-jays keep track of who was watching when. Science 312:1662–1665. doi: 10.1126/science.1126539 PubMedCrossRefGoogle Scholar
  21. de Waal FBM (1982) Chimpanzee politics: power and sex among apes. Jonathan Cape, LondonGoogle Scholar
  22. de Waal FBM (2008) Putting the altruism back into altruism: the evolution of empathy. Annu Rev Psychol 59:279–300. doi: 10.1146/annurev.psych.59.103006.093625 PubMedCrossRefGoogle Scholar
  23. de Waal FBM, Suchak M (2010) Prosocial primates: selfish and unselfish motivations. Phil Trans R Soc B 365:2711–2722. doi: 10.1098/rstb.2010.0119 PubMedCrossRefGoogle Scholar
  24. de Waal FBM, Leimgruber K, Greenberg AR (2008) Giving is self-rewarding for monkeys. PNAS 105:13685–13689. doi: 10.1073/pnas.0807060105 PubMedCrossRefGoogle Scholar
  25. Emery NJ (2006) Cognitive ornithology: the evolution of avian intelligence. Proc R Soc B 361:23–43. doi: 10.1098/rstb.2005.1736 Google Scholar
  26. Emery NJ, Seed AM, von Bayern AMP, Clayton NS (2007) Cognitive adaptations of social bonding in birds. Phil Trans R Soc B 362:489–505. doi: 10.1098/rstb.2006.1991 PubMedCrossRefGoogle Scholar
  27. Fehr E, Fischbacher U (2003) The nature of human altruism. Nature 425:785–791. doi: 10.1038/nature02043 PubMedCrossRefGoogle Scholar
  28. Fehr E, Gächter S (2002) Altruistic punishment in humans. Nature 415:137–140. doi: 10.1038/415137a PubMedCrossRefGoogle Scholar
  29. Fletcher GE (2008) Attending to the outcome of others: disadvantageous inequity aversion in male capuchin monkeys (Cebus apella). Am J Primatol 70:901–905. doi: 10.1002/ajp.20576 PubMedCrossRefGoogle Scholar
  30. Fraser ON, Bugnyar T (2010) Do ravens show consolation? Responses to distressed others. PLoS ONE 5:e10605. doi: 10.1371/journal.pone.0010605 PubMedCrossRefGoogle Scholar
  31. Greenberg JR, Hamann K, Warneken F, Tomasello M (2010) Chimpanzee helping in collaborative and noncollaborative contexts. Anim Behav 80:873–880. doi: 10.1016/j.anbehav.2010.08.008 CrossRefGoogle Scholar
  32. Hare B (2001) Can competitive paradigms increase the validity of experiments on primate social cognition? Anim Cogn 4:269–280. doi: 10.1007/s100710100084 CrossRefGoogle Scholar
  33. Hare B, Kwetuenda S (2010) Bonobos voluntarily share their own food with others. Curr Biol 20:230–231. doi: 10.1016/j.cub.2009.12.038 CrossRefGoogle Scholar
  34. Hare B, Tomasello M (2004) Chimpanzees are more skillful in competitive than in cooperative cognitive tasks. Anim Behav 68:571–581. doi: 10.1016/j.anbehav.2003.11.011 CrossRefGoogle Scholar
  35. Hattori Y, Kano F, Tomonaga M (2010) Differential sensitivity to conspecific and allospecific cues in chimpanzees and humans: a comparative eye-tracking study. Biol Let 6:610–613. doi: 10.1098/rsbl.2010.0120 CrossRefGoogle Scholar
  36. Heinrich B, Marzluff JM (1991) Do common ravens yell because they want to attract others? Behav Ecol Sociobiol 28:13–21. doi: 10.1007/BF00172134 CrossRefGoogle Scholar
  37. Heinrich B, Marzluff JM, Marzluff CS (1993) Common ravens are attracted by appeasement calls of food discoverers when attacked. Auk 110:247–254Google Scholar
  38. Horner V, Carter JD, Suchak M, de Waal FBM (2011) Spontaneous prosocial choice by chimpanzees. PNAS 108:13847–13851. doi: 10.1073/pnas.1111088108 PubMedCrossRefGoogle Scholar
  39. Jaeggi AV, Burkart JM, Van Schaik CP (2010) On the psychology of cooperation in humans and other primates: combining the natural history and experimental evidence of prosociality. Phil Trans R Soc B 365:2723–2735. doi: 10.1098/rstb.2010.0118 PubMedCrossRefGoogle Scholar
  40. Jensen K, Hare B, Call J, Tomasello M (2006) What’s in it for me? Self-regard precludes altruism and spite in chimpanzees. Proc R Soc B 273:1013–1021. doi: 10.1098/rspb.2005.3417 PubMedCrossRefGoogle Scholar
  41. Jensen K, Call J, Tomasello M (2007) Chimpanzees are rational maximizers in an ultimatum game. Science 318:107–109. doi: 10.1126/science.1145850 PubMedCrossRefGoogle Scholar
  42. Krams I, Krama T, Igaune K, Mänd R (2008) Experimental evidence of reciprocal altruism in the pied flycatcher. Behav Ecol Sociobiol 62:599–605. doi: 10.1007/s00265-007-0484-1 CrossRefGoogle Scholar
  43. Kuroshima H, Kuwahata H, Fujita K (2008) Learning from others’ mistakes in capuchin monkeys (Cebus apella). Anim Cogn 11:599–609. doi: 10.1007/s10071-008-0150-7 PubMedCrossRefGoogle Scholar
  44. Lakshminarayanan VR, Santos LR (2008) Capuchin monkeys are sensitive to others’ welfare. Curr Biol 18:999–1000. doi: 10.1016/j.cub.2008.08.057 CrossRefGoogle Scholar
  45. Langergraber KE, Mitani JC, Vigilant L (2007) The limited impact of kinship on cooperation in wild chimpanzees. PNAS 104:7786–7790. doi: 10.1073/pnas.0611449104 PubMedCrossRefGoogle Scholar
  46. Leimar O, Hammerstein P (2010) Cooperation for direct fitness benefits. Phil Trans R Soc B 365:2619–2626. doi: 10.1098/rstb.20100116 PubMedCrossRefGoogle Scholar
  47. Marzluff JMB, Heinrich B, Marzluff CS (1996) Raven roosts are mobile information centers. Anim Behav 51:89–103. doi: 10.1006/anbe.1996.0008 Google Scholar
  48. Melis AP, Warneken F, Jensen K, Schneider A, Call J, Tomasello M (2011) Chimpanzees help conspecifics obtain food and non-food items. Proc R Soc B 278:1405–1413. doi: 10.1098/rspb.2010.1735 PubMedCrossRefGoogle Scholar
  49. Noë R (2006) Cooperation experiments: coordination through communication versus acting apart together. Anim Behav 71:1–18. doi: 10.1016/j.anbehav.2005.03.037 CrossRefGoogle Scholar
  50. Raihani NJ, Bshary R (2011) Resolving the iterated prisoner’s dilemma: theory and reality. J Evol Biol 24:1628–1639. doi: 10.1111/j.1420-9101.2011.02307.x PubMedCrossRefGoogle Scholar
  51. Raihani NJ, Grutter AS, Bshary R (2010) Punishers benefit from third-party punishment in fish. Science 327:171. doi: 10.1126/science.1183068 PubMedCrossRefGoogle Scholar
  52. Rutte C, Taborsky M (2008) The influence of social experience on cooperative behaviour of rats (Rattus norvegicus): direct vs generalised reciprocity. Behav Ecol Sociobiol 62:499–505. doi: 10.1007/s00265-007-0474-3 CrossRefGoogle Scholar
  53. Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Q Rev Biol 79:135–160. doi: 10.1086/383541 PubMedCrossRefGoogle Scholar
  54. Schloegl C, Kotrschal K, Bugnyar T (2007) Gaze following in common ravens, Corvus corax: ontogeny and habituation. Anim Behav 74:769–778. doi: 10.1016/j.anbehav.2006.08.017 CrossRefGoogle Scholar
  55. Schloegl C, Kotrschal K, Bugnyar T (2008) Do common ravens (Corvus corax) rely on human or conspecific gaze cues to detect hidden food? Anim Cogn 11:231–241. doi: 10.1007/s10071-007-0105-4 PubMedCrossRefGoogle Scholar
  56. Schwab C, Swoboda R, Kotrschal K, Bugnyar T (2012) Recipients affects prosocial and altruistic choices in jackdaws, Corvus monedula. PLoS ONE 7:e34922. doi: 10.1371/journal.pone.0034922 PubMedCrossRefGoogle Scholar
  57. Silk JB, Brosnan SF, Vonk J, Heinrich J, Povinelli DJ, Richardson AS, Lambeth SP, Mascaro J, Schapiro SJ (2005) Chimpanzees are indifferent to the welfare of unrelated group members. Nature 437:1357–1359. doi: 10.1038/nature04243 PubMedCrossRefGoogle Scholar
  58. Skerry AE, Sheskin M, Santos LR (2011) Capuchin monkeys are not prosocial in an instrumental helping task. Anim Cogn 14:647–654. doi: 10.1007/s10071-011-0399-0 PubMedCrossRefGoogle Scholar
  59. Stahler D, Heinrich B, Smith D (2002) Common ravens, Corvus corax, preferentially associate with grey wolves, Canis lupus, as a foraging strategy in winter. Anim Behav 64:283–290. doi: 10.1006/anbe.2002.3047 CrossRefGoogle Scholar
  60. Stephens DW, McLinn CM, Stevens JR (2002) Discounting and reciprocity in an iterated prisoner’s dilemma. Science 298:2216–2218. doi: 10.1126/science.1078498 PubMedCrossRefGoogle Scholar
  61. Stevens JR (2010) Donor payoffs and other-regarding preferences in cotton-top tamarins (Saguinus oedipus). Anim Cogn 13:663–670. doi: 10.1007/s10071-010-0309-x PubMedCrossRefGoogle Scholar
  62. Takimoto A, Kuroshima H, Fujita K (2010) Capuchin monkeys (Cebus apella) are sensitive to others’ reward: an experimental analysis of food-choice for conspecifics. Anim Cogn 13:249–261. doi: 10.1007/s10071-009-0262-8 PubMedCrossRefGoogle Scholar
  63. Viana DS, Gordo I, Sucena E, Moita MAP (2010) Cognitive and motivational requirements for the emergence of cooperation in a rat social game. PLoS ONE 5:e8483. doi: 10.1371/journal.pone.0008483 PubMedCrossRefGoogle Scholar
  64. Yamamoto S, Tanaka M (2009) Do chimpanzees (Pan troglodytes) spontaneously take turns in a reciprocal cooperation task? J Comp Psychol 123:242–249. doi: 10.1037/a0015838 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Felice Di Lascio
    • 1
  • François Nyffeler
    • 1
  • Redouan Bshary
    • 1
  • Thomas Bugnyar
    • 2
    • 3
  1. 1.Institute of Biology, University of NeuchâtelNeuchâtelSwitzerland
  2. 2.Department of Cognitive BiologyUniversity of ViennaViennaAustria
  3. 3.Konrad Lorenz ForschungsstelleGrünauAustria

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