Animal Cognition

, Volume 13, Issue 3, pp 545–553 | Cite as

The performance of rooks in a cooperative task depends on their temperament

  • Christelle Scheid
  • Ronald NoëEmail author
Original Paper


In recent years, an increasing number of studies demonstrated the existence of consistent individual differences in behaviour, often referred to as differences in temperament or personality, in a wide range of animal species. There notably is a growing body of evidence showing that individuals differ in their propensity for risk taking or reacting to stressful situations. This variation has been related to differences in learning abilities or performance in cognitive tasks. In the present study, we examined the consequences of inter-individual variation in boldness on performance in a cooperative task in rooks (Corvus frugilegus). Birds were tested individually to measure a number of behavioural parameters related to boldness. The level of a stress-related hormone, corticosterone, in the faeces of each bird was measured under control conditions and after a stress-provoking event. In parallel, we conducted a cooperative string pulling task in which birds were tested in dyads. Successful cooperation depended to a large extent on the temperament of the two partners involved. Temperament, in turn, correlated well with corticosterone levels under stress. Bolder individuals appeared to be more willing to participate in the task, whereas shyer individuals were more influenced by the behaviour of their partner. These findings suggest that a rook’s temperament can limit its options of forming successfully cooperating partnerships under stressful conditions.


Cooperation Boldness Temperament Personality Corvus frugilegus Rook Stress Corticosterone 



This work received funding under the GEBACO contract n. 28696 (EC-Framework 6 programme 2002–2006). C. Scheid was supported by a studentship of the French Ministry of Research. We are grateful to G. Gaudiot for the conception of the experimental apparatus, to H. Gachot and S. Zahn for the DNA sexing, to E. Möstl and his team at the University of Veterinary Medicine, Vienna for the hormone analyses, to N. Poulin for advises concerning statistics and to J. Schmidt, T. Hindelang, L. Durand, J. P. Robin and S. Calibre for their help.


  1. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188CrossRefGoogle Scholar
  2. Bergmüller R, Johnstone RA, Russel AF, Bshary R (2007) Integrating cooperative breeding into theoretical concepts of cooperation. Behav Proc 76:61–72CrossRefGoogle Scholar
  3. Boesch C (1994) Cooperative hunting in wild chimpanzees. Anim Behav 48:653–667CrossRefGoogle Scholar
  4. Boesch C, Boesch H (1989) Hunting behavior of wild chimpanzees in the Tai National Park. Am J Phys Anthrop 78:547–573CrossRefPubMedGoogle Scholar
  5. Brick O, Jakobsson S (2002) Individual variation in risk taking: the effect of a predatory threat on fighting behavior in Nannacara anomal. Behav Ecol 13:439–442CrossRefGoogle Scholar
  6. Carere C, Eens M (2005) Unravelling animal personalities: how and why individuals consistently differ. Behaviour 142:1149–1157CrossRefGoogle Scholar
  7. Carere C, Groothuis TGG, Mostl E, Daan S, Koolhaas JM (2003) Fecal corticosteroids in a territorial bird selected for different personalities: daily rhythm and the response to social stress. Horm Behav 43:540–548CrossRefPubMedGoogle Scholar
  8. Chalmeau R, Visalberghi E, Gallo A (1997) Capuchin monkeys, Cebus apella fail to understand a cooperative task. Anim Behav 54:1215–1225CrossRefPubMedGoogle Scholar
  9. Cockrem JF (2007) Stress, corticosterone responses and avian personalities. J Ornith 148:169–178CrossRefGoogle Scholar
  10. Cronin KA, Kurian AV, Snowdon CT (2005) Cooperative problem solving in a cooperatively breeding primate (Saguinus oedipus). Anim Behav 69:133–142CrossRefPubMedGoogle Scholar
  11. Dugatkin LA (1988) Do guppies play TIT FOR TAT during predator inspection visits? Behav Ecol Sociobiol 23:395–399CrossRefGoogle Scholar
  12. Dugatkin LA (1997) Cooperation among animals: An evolutionary perspective. Oxford University Press, New YorkGoogle Scholar
  13. Emery NJ, Clayton NS (2004) The mentality of crows: Convergent evolution of intelligence in corvids and apes. Science 306:1903–1907CrossRefPubMedGoogle Scholar
  14. Emery NJ, Seed AM, von Bayern AMP, Clayton NS (2007) Cognitive adaptations of social bonding in birds. Phil Trans R Soc B 362:489–505CrossRefPubMedGoogle Scholar
  15. Fishman MA (2003) Indirect reciprocity among imperfect individuals. J Theor Biol 225:285–292CrossRefPubMedGoogle Scholar
  16. Fishman MA, Lotem A, Stone L (2001) Heterogeneity stabilizes reciprocal altruism interactions. J Theor Biol 209:87–95CrossRefPubMedGoogle Scholar
  17. Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121CrossRefGoogle Scholar
  18. Frigerio D, Dittami J, Möstl E, Kotrschal K (2004) Excreted corticosterone metabolites co-vary with ambient temperature and air pressure in male Greylag geese (Anser anser). Gen Comp Endocr 137:29–36CrossRefPubMedGoogle Scholar
  19. Gilby IC, Eberly LE, Wrangham RW (2008) Economic profitability of social predation among wild chimpanzees: individual variation promotes cooperation. Anim Behav 75:351–360CrossRefGoogle Scholar
  20. Godin JGG, Davis SA (1995) Who dares, benefits: predator approach behaviour in the guppy (Poecilia reticulata) deters predator pursuit. Proc R Soc B 259:193–200CrossRefGoogle Scholar
  21. Groothuis TGG, Carere C (2005) Avian personalities: characterization and epigenesis. Neurosci Biobehav Rev 29:137–150CrossRefPubMedGoogle Scholar
  22. Hare B, Melis AP, Woods V, Hastings S, Wrangham R (2007) Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17:619–623CrossRefPubMedGoogle Scholar
  23. Hauser MD, Chen MK, Chen F, Chuang E (2003) Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back. Proc R Soc B 270:2363–2370CrossRefPubMedGoogle Scholar
  24. Heinsohn R, Packer C (1995) Complex cooperative strategies in group-territorial African lions. Science 269:1260–1262CrossRefPubMedGoogle Scholar
  25. Helme AE, Clayton NS, Emery NJ (2006) What do rooks (Corvus frugilegus) understand about physical contact? J Comp Psychol 120:288–293CrossRefPubMedGoogle Scholar
  26. Hirata S (2003) Cooperation in chimpanzees. Hattatsu 95:103–111Google Scholar
  27. Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ (1999) Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev 23:925–935CrossRefPubMedGoogle Scholar
  28. Kotrschal K, Hirschenhauser K, Möstl E (1998) The relationship between social stress and dominance is seasonal in greylag geese. Anim Behav 55:171–176CrossRefPubMedGoogle Scholar
  29. Legge S (1996) Cooperative lions escape the prisoner’s dilemma. Trends Ecol Evol 11:2–3CrossRefGoogle Scholar
  30. Lotem A, Fishman MA, Stone L (1999) Evolution of cooperation between individuals. Nature 400:226–227CrossRefPubMedGoogle Scholar
  31. Madge S, Burn H (1994) Crows and Jays. C Helme, LondonGoogle Scholar
  32. McNamara JM, Barta Z, Houston AI (2004) Variation in behaviour promotes cooperation in the Prisoner’s Dilemma game. Nature 428:745–748CrossRefPubMedGoogle Scholar
  33. Melis AP, Hare B, Tomasello M (2006) Engineering cooperation in chimpanzees: tolerance constraints on cooperation. Anim Behav 72:275–286CrossRefGoogle Scholar
  34. Mendres KA, de Waal FBM (2000) Capuchins do cooperate: the advantage of an intuitive task. Anim Behav 60:523–529CrossRefPubMedGoogle Scholar
  35. Milinski M (1987) TIT FOR TAT in sticklebacks and the evolution of cooperation. Nature 325:433–435CrossRefPubMedGoogle Scholar
  36. Möstl E, Maggs JL, Schrötter G, Besenfelder U, Palme R (2002) Measurement of cortisol metabolites in faeces of ruminants. Vet Res Commun 26:127–139CrossRefPubMedGoogle Scholar
  37. Nakagawa S, Möstl E, Waas JR (2003) Validation of an enzyme immunoassay to measure faecal glucocorticoid metabolites from Adelie penguins (Pygoscelis adeliae): a non-invasive tool for estimating stress? Polar Biol 26:491–493Google Scholar
  38. Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet V7:783–787CrossRefGoogle Scholar
  39. Noë R (2006) Cooperation experiments: coordination through communication versus acting apart together. Anim Behav 71:1–18CrossRefGoogle Scholar
  40. Noë R, Sluijter AA (1995) Which adult male savanna baboons form coalitions? Int J Primatol 16:77–105CrossRefGoogle Scholar
  41. Nowak MA (2006) Five rules for the evolution of cooperation. Science 314:1560–1563CrossRefPubMedGoogle Scholar
  42. Nowak AM, Sasaki A, Taylor C, Fudenberg D (2004) Emergence of cooperation and evolutionary stability in finite population. Nature 428:646–650CrossRefPubMedGoogle Scholar
  43. Nunn CL, Deaner RO (2004) Patterns of participation and free riding in territorial conflicts among ringtailed lemurs (Lemur catta). Behav Ecol Sociobiol 57:50–61CrossRefGoogle Scholar
  44. Parsons KM, Durban JW, Claridge DE, Balcomb KC, Noble LR, Thompson PM (2003) Kinship as a basis for alliance formation between male bottlenose dolphins, Tursiops truncatus, in the Bahamas. Anim Behav 66:185–194CrossRefGoogle Scholar
  45. Petit O, Desportes C, Thierry B (1992) Differential probability of coproduction in two species of macaque (Macaca tonkeana, M. mulatta). Ethology 90:107–120CrossRefGoogle Scholar
  46. Range F, Bugnyar T, Schloegl C, Kotrschal K (2006) Individual and sex differences in learning abilities of ravens. Behav Proc 73:100–106CrossRefGoogle Scholar
  47. Rettenbacher S, Möstl E, Hackl R, Ghareeb K, Palme R (2004) Measurement of corticosterone metabolites in chicken droppings. Brit Poultry Sci 45:704–711CrossRefGoogle Scholar
  48. Riolo RL, Cohen MD, Axelrod R (2001) Evolution of cooperation without reciprocity. Nature 414:441–443CrossRefPubMedGoogle Scholar
  49. Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Quart Rev Biol 79:135–160CrossRefPubMedGoogle Scholar
  50. Scheel D, Packer C (1991) Group hunting behaviour of lions: a search for cooperation. Anim Behav 41:697–709CrossRefGoogle Scholar
  51. Scheid C, Schmidt J, Noë R (2008) Distinct patterns of food offering and cofeeding in rooks. Anim Behav 76:1701–1707CrossRefGoogle Scholar
  52. Seed AM, Clayton NS, Emery NJ (2008) Cooperative problem solving in rooks (Corvus frugilegus). Proc R Soc B 275:1421–1429CrossRefPubMedGoogle Scholar
  53. Sherratt TN, Roberts G (1998) The evolution of generosity and choosiness in cooperative exchanges. J Theor Biol 193:167–177CrossRefPubMedGoogle Scholar
  54. Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill, BostonGoogle Scholar
  55. Silk JB, Alberts SC, Altmann J (2004) Patterns of coalition formation by adult female baboons in Amboseli, Kenya. Anim Behav 67:573–582CrossRefGoogle Scholar
  56. Stephens DW, McLinn CM, Stevens JR (2002) Discounting and reciprocity in an Iterated Prisoner’s Dilemma. Science 298:2216–2218CrossRefPubMedGoogle Scholar
  57. Stöwe M, Bugnyar T, Schloegl C, Heinrich B, Kotrschal K, Möstl E (2008) Corticosterone excretion patterns and affiliative behavior over development in ravens (Corvus corax). Horm Behav 53:208–216CrossRefPubMedGoogle Scholar
  58. Svartberg K (2002) Shyness-boldness predicts performance in working dogs. Appl Anim Behav Sci 79:157–174CrossRefGoogle Scholar
  59. Touma C, Palme R (2004) Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann NY Acad Sci 1046:54–74CrossRefGoogle Scholar
  60. Toxopeus IB, Sterck EHM, van Hooff JARAM, Spruijt BM, Heeren TJ (2005) Effects of trait anxiety on performance of socially housed monkeys in a learning test. Behaviour 142:1269–1287CrossRefGoogle Scholar
  61. West SA, Griffin AS, Gardner A (2007) Evolutionary explanations for cooperation. Curr Biol 17:661–672CrossRefGoogle Scholar
  62. Wilson DS, Coleman K, Clark AB, Biederman L (1993) The shy–bold continuum in pumpkinseed sunfish (Lepomis gibbosus). J Comp Psychol 107:250–260CrossRefGoogle Scholar
  63. Wilson DS, Clark AB, Coleman K, Dearstyne T (1994) Shyness and boldness in humans and other animals. Trends Ecol Evol 9:442–446Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Ethologie des Primates, DEPE-IPHC-CNRS UMR 7178Université de StrasbourgStrasbourgFrance

Personalised recommendations