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

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Abstract

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.

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References

  • Anzenberger G (1985) How stranger encounters of common marmosets (Callithrix jacchus jacchus) are influenced by family members: the quality of behavior. Folia Primatol 45:204–224

    Google Scholar 

  • 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 108:205–211

    Article  PubMed  CAS  Google Scholar 

  • 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 68:255–262

    Article  CAS  Google Scholar 

  • Barros M, Boere V, Mello EL, Tomaz C (2002) Reactions to potential predators in captive-born marmosets (Callithrix penicillata). Int J Primatol 23:443–454

    Article  Google Scholar 

  • Bartecki U, Heymann EW (1987) Field observation of snake-mobbing in a group of saddle-back tamarins, Saguinus fuscicollis nigrifrons. Folia Primatol 48:199–202

    PubMed  CAS  Google Scholar 

  • Blumstein DT (2006) The multipredator hypothesis and the evolutionary persistence of antipredator behavior. Ethology 112:209–217

    Article  Google Scholar 

  • Bovet D, Vauclair J (2000) Picture recognition in animals and humans. Behav Brain Res 109:143–165

    Article  PubMed  CAS  Google Scholar 

  • Campbell MW, Snowdon CT (2007) Vocal response of captive-reared Saguinus oedipus during mobbing. Int J Primatol 28:257–270

    Article  Google Scholar 

  • Cheney DL, Seyfarth RM (1990) How monkeys see the world: inside the mind of another species. University of Chicago Press, Chicago

    Google Scholar 

  • Coe CL, Franklin D, Smith ER, Levine S (1982) Hormonal responses accompanying fear and agitation in the squirrel monkey. Physiol Behav 29:1051–1057

    Article  PubMed  CAS  Google Scholar 

  • Cook M, Mineka S (1990) Selective associations in the observational conditioning of fear in rhesus monkeys. J Exp Psychol Anim B 16:372–389

    Article  CAS  Google Scholar 

  • Corrêa HKM, Coutinho PEG (1997) Fatal attack of a pit viper, Bothrops jararaca, on an infant buffy-tuftef ear marmoset (Callithrix aurita). Primates 38:215–217

    Article  Google Scholar 

  • Cross N, Rogers LJ (2004) Diurnal cycle in salivary cortisol levels in common marmosets. Dev Psychobiol 45(3):134–139

    Article  PubMed  CAS  Google Scholar 

  • Cross N, Rogers LJ (2005) Mobbing vocalisations as a coping response in the common marmoset. Horm Behav 49:237–245

    Article  PubMed  Google Scholar 

  • 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 62:107–114

    Article  PubMed  CAS  Google Scholar 

  • Curio E (1978) The adaptive significance of avian mobbing I: Teleonomic hypotheses and predictions. Z Tierpsychol 48:75–183

    Google Scholar 

  • Dettling A, Feldon J, Price CR (2002) Early deprivation and behavioural and physiological responses to social separation/novelty in the marmoset. Pharmacol Biochem Behav 73:259–269

    Article  PubMed  CAS  Google Scholar 

  • Dugatkin LA, Godin J-GJ (1992) Prey approaching predators: a cost-benefit perspective. Ann Zool Fenn 29:233–252

    Google Scholar 

  • Epple G (1968) Comparative studies on vocalization in marmoset monkeys (Hapalidae). Folia Primatol 8:1–40

    PubMed  CAS  Google Scholar 

  • Epple G (1975) The behavior of marmoset monkeys (Callithricidae). In: Rosenblum L (ed) Primate behavior, vol 4. Academic, New York, pp 195–239

    Google Scholar 

  • Evans S, Poole TB (1984) Long-term changes and maintenance of the pair-bond in common marmosets, Callithrix jacchus jacchus. Folia Primatol 42:33–41

    Google Scholar 

  • Ferrari SF, Ferrari MAL (1990) Predator avoidance behavior in the buffy-headed marmoset, Callithrix flaviceps. Primates 31(3):323–338

    Article  Google Scholar 

  • Galef BG Jr, Allen C (1995) A new model system for studying behavioural traditions in animals. Anim Behav 50:705–717

    Article  Google Scholar 

  • Greene HW (1997) Snakes: the evolution of mystery in nature. University of California Press, Berkley

    Google Scholar 

  • Griffin AS, Evans CR (2003) Social learning of antipredator behaviour in a marsupial. Anim Behav 66:485–492

    Article  Google Scholar 

  • Gursky S (2005) Predator mobbing in Tarsius spectrum. Int J Primatol 26(1):207–221

    Article  Google Scholar 

  • Gursky S (2006) Function of snake mobbing in spectral tarsiers. Am J Phys Anthropol 129:601–608

    Article  PubMed  Google Scholar 

  • Hankerson SJ, Caine NG (2004) Pre-retirement predator encounters alter the morning behavior of captive marmosets (Callithrix geoffroyi). Am J Primatol 63:75–85

    Article  PubMed  Google Scholar 

  • Hayes SL, Snowdon CT (1990) Predator recognition in cotton-top tamarins (Saguinus oedipus). Am J Primatol 20:283–291

    Article  Google Scholar 

  • von Heusser H (1968) Ein frei gehaltener Krallenaffe (Callithrix jacchus) erkennt Bilder. Z Tierpsychol 25:710–718

    PubMed  CAS  Google Scholar 

  • Hook-Costigan MA, Rogers LJ (1998a) Eye preferences in common marmosets (Callithrix jacchus): influence of age, stimulus and hand preference. Laterality 3(2):109–130

    Article  PubMed  CAS  Google Scholar 

  • Hook-Costigan MA, Rogers LJ (1998b) Lateralized use of the mouth in production of vocalizations by marmosets. Neuropsychologia 36(12):1265–1273

    Article  PubMed  CAS  Google Scholar 

  • Isbell LA (2006) Snakes as agents of evolutionary change in primate brains. J Hum Evol 51:1–35

    Article  PubMed  Google Scholar 

  • 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):69

    Google Scholar 

  • Kaplan G, Rogers LJ (1999) Parental care in marmosets (Callithrix jacchus jacchus): development and effect of anogenital licking on exploration. J Comp Psychol 113:269–276

    Article  Google Scholar 

  • Kaplan G, Rogers LJ (2006) Head cocking as a form of exploration in the common marmoset and its development. Dev Psychobiol 48:551–560

    Article  PubMed  Google Scholar 

  • 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):44

    Article  Google Scholar 

  • 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 66:189–226

    Google Scholar 

  • 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 23:925–935

    Article  CAS  Google Scholar 

  • 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 63:403–406

    Article  Google Scholar 

  • Levine S, Mody T (2003) The long-term psychobiological consequences of intermittent postnatal separation in the squirrel monkeey. Neurosci Biobehav R 27:83–89

    Article  Google Scholar 

  • Menzel CR (1980) Head cocking and visual perception in primates. Anim Behav 28:151–159

    Article  PubMed  Google Scholar 

  • 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 51–73

    Google Scholar 

  • 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, 73p

  • Raul J-S, Cirimele V, Ludes B, Kintz P (2004) Detection of physiological concentrations of cortisol and corticosterone in human hair. Clin Biochem 37:1105–1111

    Article  PubMed  CAS  Google Scholar 

  • Rogers LJ, Stafford D, Ward JP (1993) Head cocking in galagos. Anim Behav 45:943–952

    Article  Google Scholar 

  • 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 56:801–810

    Article  PubMed  CAS  Google Scholar 

  • Sihi A, Bell A, Johnson JC (2004) Behavioural syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19(7):372–378

    Article  Google Scholar 

  • 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 62:243–259

    Article  PubMed  Google Scholar 

  • Zuberbühler K, Jenny D, Bshary R (1999) The predator deterrence function of primate alarm calls. Ethology 105:477–490

    Google Scholar 

Download references

Acknowledgments

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.

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Clara, E., Tommasi, L. & Rogers, L.J. Social mobbing calls in common marmosets (Callithrix jacchus): effects of experience and associated cortisol levels. Anim Cogn 11, 349–358 (2008). https://doi.org/10.1007/s10071-007-0125-0

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  • DOI: https://doi.org/10.1007/s10071-007-0125-0

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