Animal Cognition

, Volume 11, Issue 2, pp 349–358 | Cite as

Social mobbing calls in common marmosets (Callithrix jacchus): effects of experience and associated cortisol levels

  • Elena Clara
  • Luca Tommasi
  • Lesley J. Rogers
Original Paper


We compared the mobbing response to model snakes of two groups of captive-born common marmosets (Callithrix jacchus) differing in genetic relatedness, age and past experience. Mobbing vocalisations (tsik calls), other mobbing behaviour and attention to the stimulus were recorded for 2 min. intervals pre-exposure, during exposure to various stimuli and post-exposure. Marmosets in one group were vocally reactive to all stimuli, although more so to one particular stimulus resembling rearing snakes and modified images of it, whereas the marmosets in a younger and genetically unrelated group attended to the stimuli but made very few mobbing calls. The parent stock of the first group had suffered stress in early life and had developed a phobic response to a specific stimulus, which they had transmitted to their offspring. A third group, matching the older group in age range but genetically unrelated, was also found to be unresponsive to the stimulus that elicited the strongest response in the first group. Cortisol levels in samples of hair were assayed and a significant negative correlation was found between the number of tsik calls made during presentation of the stimuli and the cortisol level, showing that mobbing behaviour/behavioural reactivity is associated with low levels of physiological stress.


Common marmoset Vocalisations Mobbing snakes Cultural transmission Age Cortisol in hair 



E.C. is grateful for funding from the Australian Department of Education Science and Training (DEST) for an Endeavour Scholarship to visit the Centre for Neuroscience and Animal Behaviour at UNE. The research costs were funded, in part, by an Australian Research Council grant to L.J.R.. We are grateful to Dr. S. Cairns and Dr. R. Freire for advice on statistical procedures, and to Dr. J. McFarland and Dr. N.J. Branson for assistance in assaying for cortisol. E.C. would like to thank Giuseppe Clara for technical advice.


  1. Anzenberger G (1985) How stranger encounters of common marmosets (Callithrix jacchus jacchus) are influenced by family members: the quality of behavior. Folia Primatol 45:204–224Google Scholar
  2. Barros M, Boere V, Huston JP, Tomaz C (2000) Measuring fear and anxiety in the marmoset (Callithrix penicillata) with a novel predator confrontation model: effects of diazepam. Behav Brain Res 108:205–211PubMedCrossRefGoogle Scholar
  3. Barros M, Mello EL, Huston JP, Tomaz C (2001) Behavioral effects of buspirone in the marmoset employing a predator confrontation test of fear and anxiety. Pharmacol, Biochem Beh 68:255–262CrossRefGoogle Scholar
  4. Barros M, Boere V, Mello EL, Tomaz C (2002) Reactions to potential predators in captive-born marmosets (Callithrix penicillata). Int J Primatol 23:443–454CrossRefGoogle Scholar
  5. Bartecki U, Heymann EW (1987) Field observation of snake-mobbing in a group of saddle-back tamarins, Saguinus fuscicollis nigrifrons. Folia Primatol 48:199–202PubMedGoogle Scholar
  6. Blumstein DT (2006) The multipredator hypothesis and the evolutionary persistence of antipredator behavior. Ethology 112:209–217CrossRefGoogle Scholar
  7. Bovet D, Vauclair J (2000) Picture recognition in animals and humans. Behav Brain Res 109:143–165PubMedCrossRefGoogle Scholar
  8. Campbell MW, Snowdon CT (2007) Vocal response of captive-reared Saguinus oedipus during mobbing. Int J Primatol 28:257–270CrossRefGoogle Scholar
  9. Cheney DL, Seyfarth RM (1990) How monkeys see the world: inside the mind of another species. University of Chicago Press, ChicagoGoogle Scholar
  10. Coe CL, Franklin D, Smith ER, Levine S (1982) Hormonal responses accompanying fear and agitation in the squirrel monkey. Physiol Behav 29:1051–1057PubMedCrossRefGoogle Scholar
  11. Cook M, Mineka S (1990) Selective associations in the observational conditioning of fear in rhesus monkeys. J Exp Psychol Anim B 16:372–389CrossRefGoogle Scholar
  12. Corrêa HKM, Coutinho PEG (1997) Fatal attack of a pit viper, Bothrops jararaca, on an infant buffy-tuftef ear marmoset (Callithrix aurita). Primates 38:215–217CrossRefGoogle Scholar
  13. Cross N, Rogers LJ (2004) Diurnal cycle in salivary cortisol levels in common marmosets. Dev Psychobiol 45(3):134–139PubMedCrossRefGoogle Scholar
  14. Cross N, Rogers LJ (2005) Mobbing vocalisations as a coping response in the common marmoset. Horm Behav 49:237–245PubMedCrossRefGoogle Scholar
  15. Cross N, Pines MK, Rogers LJ (2004) Saliva sampling to assess cortisol levels in unrestrained common marmosets and the effect of behavioral stress. Am J Primatol 62:107–114PubMedCrossRefGoogle Scholar
  16. Curio E (1978) The adaptive significance of avian mobbing I: Teleonomic hypotheses and predictions. Z Tierpsychol 48:75–183Google Scholar
  17. Dettling A, Feldon J, Price CR (2002) Early deprivation and behavioural and physiological responses to social separation/novelty in the marmoset. Pharmacol Biochem Behav 73:259–269PubMedCrossRefGoogle Scholar
  18. Dugatkin LA, Godin J-GJ (1992) Prey approaching predators: a cost-benefit perspective. Ann Zool Fenn 29:233–252Google Scholar
  19. Epple G (1968) Comparative studies on vocalization in marmoset monkeys (Hapalidae). Folia Primatol 8:1–40PubMedGoogle Scholar
  20. Epple G (1975) The behavior of marmoset monkeys (Callithricidae). In: Rosenblum L (ed) Primate behavior, vol 4. Academic, New York, pp 195–239Google Scholar
  21. Evans S, Poole TB (1984) Long-term changes and maintenance of the pair-bond in common marmosets, Callithrix jacchus jacchus. Folia Primatol 42:33–41Google Scholar
  22. Ferrari SF, Ferrari MAL (1990) Predator avoidance behavior in the buffy-headed marmoset, Callithrix flaviceps. Primates 31(3):323–338CrossRefGoogle Scholar
  23. Galef BG Jr, Allen C (1995) A new model system for studying behavioural traditions in animals. Anim Behav 50:705–717CrossRefGoogle Scholar
  24. Greene HW (1997) Snakes: the evolution of mystery in nature. University of California Press, BerkleyGoogle Scholar
  25. Griffin AS, Evans CR (2003) Social learning of antipredator behaviour in a marsupial. Anim Behav 66:485–492CrossRefGoogle Scholar
  26. Gursky S (2005) Predator mobbing in Tarsius spectrum. Int J Primatol 26(1):207–221CrossRefGoogle Scholar
  27. Gursky S (2006) Function of snake mobbing in spectral tarsiers. Am J Phys Anthropol 129:601–608PubMedCrossRefGoogle Scholar
  28. Hankerson SJ, Caine NG (2004) Pre-retirement predator encounters alter the morning behavior of captive marmosets (Callithrix geoffroyi). Am J Primatol 63:75–85PubMedCrossRefGoogle Scholar
  29. Hayes SL, Snowdon CT (1990) Predator recognition in cotton-top tamarins (Saguinus oedipus). Am J Primatol 20:283–291CrossRefGoogle Scholar
  30. von Heusser H (1968) Ein frei gehaltener Krallenaffe (Callithrix jacchus) erkennt Bilder. Z Tierpsychol 25:710–718PubMedGoogle Scholar
  31. Hook-Costigan MA, Rogers LJ (1998a) Eye preferences in common marmosets (Callithrix jacchus): influence of age, stimulus and hand preference. Laterality 3(2):109–130PubMedCrossRefGoogle Scholar
  32. Hook-Costigan MA, Rogers LJ (1998b) Lateralized use of the mouth in production of vocalizations by marmosets. Neuropsychologia 36(12):1265–1273PubMedCrossRefGoogle Scholar
  33. Isbell LA (2006) Snakes as agents of evolutionary change in primate brains. J Hum Evol 51:1–35PubMedCrossRefGoogle Scholar
  34. Kalra S, Klein J, Karaskov T, Woodland C, Einarson A, Koren G (2004) Use of hair cortisol as a biomarker for chronic stress in pregnancy. Clin Pharmacol Ther 77(2):69Google Scholar
  35. Kaplan G, Rogers LJ (1999) Parental care in marmosets (Callithrix jacchus jacchus): development and effect of anogenital licking on exploration. J Comp Psychol 113:269–276CrossRefGoogle Scholar
  36. Kaplan G, Rogers LJ (2006) Head cocking as a form of exploration in the common marmoset and its development. Dev Psychobiol 48:551–560PubMedCrossRefGoogle Scholar
  37. Klein J, Karaskov T, Stevens B, Yamada J, Koren G (2004) Hair cortisol—a potential biological marker for chronic stress. Clin Pharmacol Ther 75(2):44CrossRefGoogle Scholar
  38. Klump GM, Shalter MD (1984) Acoustic behaviour of birds and mammals in the predator context. I. Factors affecting the structure of alarm signals. II. The functional significance and evolution of alarm signals. Z Tierpsychol 66:189–226Google Scholar
  39. 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 stressphysiology. Neurosci Biobehav R 23:925–935CrossRefGoogle Scholar
  40. Koren L, Mokady O, Karaskov T, Klein J, Koren G, Geffen E (2002) A novel method using hair for determining hormonal levels in wildlife. Anim Behav 63:403–406CrossRefGoogle Scholar
  41. Levine S, Mody T (2003) The long-term psychobiological consequences of intermittent postnatal separation in the squirrel monkeey. Neurosci Biobehav R 27:83–89CrossRefGoogle Scholar
  42. Menzel CR (1980) Head cocking and visual perception in primates. Anim Behav 28:151–159PubMedCrossRefGoogle Scholar
  43. Mineka S, Cook M (1988) Social learning and the acquisition of snake fear in monkeys. In: Zentall T, Galef B (eds) Social learning: psychological and biological perspectives. Hillsdale, Erlbaum, pp 51–73Google Scholar
  44. National Health and Medical Research Council (1997) Australian code of practice for the care and use of animals for scientific purposes, 6th edn. Commonwealth of Australia, Canberra, 73pGoogle Scholar
  45. Raul J-S, Cirimele V, Ludes B, Kintz P (2004) Detection of physiological concentrations of cortisol and corticosterone in human hair. Clin Biochem 37:1105–1111PubMedCrossRefGoogle Scholar
  46. Rogers LJ, Stafford D, Ward JP (1993) Head cocking in galagos. Anim Behav 45:943–952CrossRefGoogle Scholar
  47. Saltzman W, Schultz-Darken NJ, Scheffler G, Wegner FH, Abbott DH (1994) Social and reproductive influences on plasma cortisol in female marmoset monkeys. Physiol Behav 56:801–810PubMedCrossRefGoogle Scholar
  48. Sihi A, Bell A, Johnson JC (2004) Behavioural syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19(7):372–378CrossRefGoogle Scholar
  49. Weaver A, Richardson R, Worlein J, de Waal F, Laudenslager M (2004) Response to social challenge in young bonnet (Macaca radiata) and pigtail (Macaca nemestrina) macaques is related to early maternal experience. Am J Primatol 62:243–259PubMedCrossRefGoogle Scholar
  50. Zuberbühler K, Jenny D, Bshary R (1999) The predator deterrence function of primate alarm calls. Ethology 105:477–490Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Elena Clara
    • 1
    • 4
  • Luca Tommasi
    • 2
    • 3
  • Lesley J. Rogers
    • 1
  1. 1.Centre for Neuroscience and Animal BehaviourUniversity of New EnglandArmidaleAustralia
  2. 2.Department of Biomedical SciencesUniversity of ChietiChietiItaly
  3. 3.Konrad Lorenz Institute for Evolution and Cognition ResearchAltenbergAustria
  4. 4.Department of General PsychologyUniversity of PadovaPadovaItaly

Personalised recommendations