Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T10:09:33.008Z Has data issue: false hasContentIssue false
  • English
  • Français

Do social factors related to allostatic load affect stereotypy susceptibility? Management implications for captive social animals

Published online by Cambridge University Press:  01 January 2023

MB Nagy-Reis ,
O Mendonça-Furtado  and
B Resende
MB Nagy-Reis*
Affiliation:
Department of Biological Sciences, University of Alberta, 116 St and 85 Ave, Edmonton, Canada, T6G 2R3
O Mendonça-Furtado*
Affiliation:
Institute of Psychology, University of São Paulo, Av Prof Mello Moraes, 1721, São Paulo, Brazil, 05508-030
B Resende
Affiliation:
Institute of Psychology, University of São Paulo, Av Prof Mello Moraes, 1721, São Paulo, Brazil, 05508-030
*
* Contact for correspondence and requests for reprints: nagy.reis@ualberta.com/olimendonca@gmail.com
* Contact for correspondence and requests for reprints: nagy.reis@ualberta.com/olimendonca@gmail.com
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Stereotypies are frequently associated with sub-optimal captive environments and are used as welfare indicators. However, susceptibility to stereotypy can vary across individuals of the same group. As such, identifying which individuals are more susceptible to this behaviour may be helpful in managing this issue. We have investigated which sex-age class of semi-captive capuchin monkeys (Sapajus spp) is more susceptible to stereotypic behaviours and evaluated whether or not they are also more affected by the social factors that typically influence and increase allostatic load. To accomplish this, we used instantaneous sampling to collect data on a group of capuchins kept on an island in an urban park in São Paulo, Brazil. We found that sub-adult males were the only sex-age class to display stereotypic behaviours and they all displayed pacing. Furthermore, 33% of sub-adult males also exhibited a second stereotypic behaviour associated with their pacing. Compared to the other sex-age classes, sub-adult males had a higher participation in social conflicts and experienced higher social isolation. Sub-adult males also demonstrated a lower level of positive social interactions. All of these factors typically increase allostatic load. We suggest that distal causation of the observed pacing behaviour would be the ecological/evolutionary need of sub-adult males to disperse from their natal group and that the proximal causation would relate to the high allostatic load from social sources. We recommend that managers of zoos and other facilities monitor changes in the social composition of captive groups and evaluate individuals’ age so that necessary alterations may be made, where appropriate, to reduce allostatic load and generate better welfare at individual and group levels.

Keywords

allostatic loadanimal welfarecapuchin monkeyspacingsocial animalsstereotypy
Type
Articles
Information
Animal Welfare , Volume 28 , Issue 2 , May 2019 , pp. 183 - 190
Copyright
© 2019 Universities Federation for Animal Welfare

References

Abbott, DH, Keverne, EB, Bercovitch, FB, Shively, CA, Mendonza, SP, Saltsman, W, Snowdon, CT, Ziegler, TE, Banjevic, M, Garland, T and Sapolsky, RM 2003 Are subordi-nates always stressed? A comparative analysis of rank differences in cortisol levels among primates Hormones and Behavior 43: 67–82. https://doi.org/10.1016/S0018-506X(02)00037-5CrossRefGoogle ScholarPubMed
Altmann, J 1974 Observational study of behavior sampling meth-ods. Behaviour 49: 227–267. https://doi.org/10.1163/156853974X00534CrossRefGoogle Scholar
Bekoff, M 1977 Mammalian dispersal and the ontogeny of individ-ual behavioral phenotypes. The American Naturalist 111(980): 715–732. https://doi.org/10.1086/283201CrossRefGoogle Scholar
Broom, DM 1991 Animal welfare: concepts and measurement. Journal of Animal Science 69: 4167–4175. https://doi.org/10.2527/1991.69104167xCrossRefGoogle Scholar
Cacioppo, JT and Hawkley, LC 2009 Perceived social isolation and cognition. Trends in Cognitive Sciences 13(10): 447–454. https://doi.org/10.1016/j.tics.2009.06.005CrossRefGoogle ScholarPubMed
Carosi, M, Linn, GS and Visalbergui, E 2005 The sexual behav-ior and breeding system of tufted capuchin monkeys (Cebus apel-la). Advances in the Study of Behavior 35: 105–149. https://doi.org/10.1016/S0065-3454(05)35003-0CrossRefGoogle Scholar
Christofides, N 1975 Graph Theory: An Algorithmic Approach. Academic Press: New York, USAGoogle Scholar
Clubb, R and Mason, G 2003 Captivity effects on wide-ranging carnivores. Nature 425: 473–474. https://doi.org/10.1038/425473aCrossRefGoogle ScholarPubMed
Clubb, R and Mason, G 2007 Natural behavioural biology as risk factor in carnivore welfare: How analyzing species differences could help zoos improve enclosures. Applied Animal Behaviour Science 102: 303–328. https://doi.org/10.1016/j.applan-im.2006.05.033CrossRefGoogle Scholar
Clubb, R and Vickery, S 2006 Locomotory stereotypies in car-nivores: does pacing stem from hunting, ranging, or frustrated escape? In: Mason, G and Rushen, J (eds) Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare, Second Edition pp 58–79. Cromwell Press: Trowbridge, UK. https://doi.org/10.1079/9780851990040.0058CrossRefGoogle Scholar
Dantzer, R 1986 Behavioral, physiological and functional aspects of stereotyped behavior: a review and a re-interpretation. Journal of Animal Science 62: 1776–1786. https://doi.org/10.2527/jas1986.6261776xCrossRefGoogle Scholar
Ferreira, RG, Izar, P and Lee, PC 2006 Exchange, affiliation, and protective interventions in semifree-ranging brown capuchin monkeys (Cebus apella). American Journal of Primatology 68: 765–776. https://doi.org/10.1002/ajp.20277Google Scholar
Ferreira, RG, Mendl, M, Wagner, PGC, Araujo, T, Nunes, D and Mafra, AL 2016 Coping strategies in captive capuchin mon-keys (Sapajus spp). Applied Animal Behaviour Science 176: 120–127. https://doi.org/10.1016/j.applanim.2015.12.007CrossRefGoogle Scholar
Fragaszy, DM, Visalberghi, E and Fedigan, LM 2004 The Complete Capuchin – The Biology of the Genus Cebus. Cambridge University Press: Cambridge, UKGoogle Scholar
Gottlieb, DH, Capitanio, JP and McCowan, B 2013 Risk fac-tors for stereotypic behavior and self-biting in rhesus macaques (Macaca mulatta): Animal's history, current environment, and per-sonality. American Journal of Primatology 75(10): 995–1008. https://doi.org/10.1002/ajp.22161CrossRefGoogle Scholar
Goymann, W and Wingfield, JC 2004 Allostatic load, social status and stress hormones: the costs of social status matter. Animal Behaviour 67: 591–602. https://doi.org/10.1016/j.anbe-hav.2003.08.007CrossRefGoogle Scholar
Harrison, DJ 1992 Dispersal characteristics of juvenile coyotes in Maine. The Journal of Wildlife Management 56(1): 128–138. https://doi.org/10.2307/3808800CrossRefGoogle Scholar
Ijichi, CL, Collins, LM and Elwood, RW 2013 Evidence for the role of personality in stereotypy predisposition. Animal Behaviour 85(6): 1145–1151. https://doi.org/10.1016/j.anbe-hav.2013.03.033CrossRefGoogle Scholar
Izar, P, Verderane, MP, Peternelli-dos-Santos, L, Mendonça-Furtado, O, Presotto, A, Tokuda, M, Visalberghi, E and Fragaszy, D 2012 Flexible and conservative features of social systems in tufted capuchin monkeys: comparing the socioe-cology of Sapajus libidinosus and Sapajus nigritus. American Journal of Primatology 74: 315–331. https://doi.org/10.1002/ajp.20968CrossRefGoogle ScholarPubMed
Lutz, CK 2014 Stereotypic behavior in nonhuman primates as a model for the human condition. ILAR Journal 55(2): 284–296. https://doi.org/10.1093/ilar/ilu016CrossRefGoogle ScholarPubMed
Martin, AL 2017 The primatologist as a behavioral engineer. American Journal of Primatology 79: e22500. https://doi.org/10.1002/ajp.22500CrossRefGoogle ScholarPubMed
Mason, G, Clubb, R, Latham, N and Vickery, S 2007 Why and how should we use environmental enrichment to tackle stereo-typic behaviour? Applied Animal Behaviour Science 102: 163–188. https://doi.org/10.1016/j.applanim.2006.05.041CrossRefGoogle Scholar
Mason, GJ and Latham, NR 2004 Can't stop, won't stop: is stereo-typy a reliable animal welfare indicator? Animal Welfare 13: S57–S69Google Scholar
McBride, SB and Parker, MO 2015 The disrupted basal ganglia and behavioural control: an integrative cross-domain perspective of spontaneous stereotypy. Behavioural Brain Research 276: 45–58. https://doi.org/10.1016/j.bbr.2014.05.057CrossRefGoogle ScholarPubMed
McEwen, BS and Wingfield, JC 2003 The concept of allostasis in biology and biomedicine. Hormones and Behavior 43: 2–15. https://doi.org/10.1016/S0018-506X(02)00024-7Google ScholarPubMed
Ottoni, EB and Mannu, M 2001 Semifree-ranging tufted capuchins (Cebus apella) spontaneously use tools to crack open nuts. International Journal of Primatology 22(3): 347–358. https://doi.org/10.1023/A:1010747426841CrossRefGoogle Scholar
Poirier, C and Bateson, M 2017 Pacing stereotypies in labora-tory rhesus macaques: Implications for animal welfare and the validity of neuroscientific findings. Neuroscience and Behavioral Reviews 83: 508–515. https://doi.org/10.1016/j.neu-biorev.2017.09.010CrossRefGoogle Scholar
Pomerantz, O, Meiri, S and Terkel, J 2013 Socio-ecological factors correlate with levels of stereotypic behavior in zoo-housed primates. Behavioural Processes 98: 85–91. https://doi.org/10.1016/j.beproc.2013.05.005CrossRefGoogle ScholarPubMed
Pomerantz, O, Terkel, J, Suomi, SJ and Paukner, A 2012 Stereotypic head twirls, but not pacing, are related to a ‘pes-simistic’-like judgment bias among captive tufted capuchins (Cebus apella). Animal Cognition 15: 689–698. https://doi.org/10.1007/s 10071-012-0497-7Google Scholar
Powell, DM and Watters, JV 2017 The evolution of the ani-mal welfare movement in U.S. zoos and aquariums. Der Zoologische Garten 86: 219–234. https://doi.org/10.1016/j.zool-gart.2017.04.007CrossRefGoogle Scholar
Resende, BD 2004 Ontogenia de comportamentos manipulativos em um grupo de macacos-prego (Cebus apella) em situac?a?o de semili-berdade. PhD Thesis, Universidade de São Paulo, Brazil. [Title translation: Ontogeny of manipulative behaviour in a semifree-ranging group of tufted capuchin monkeys (Cebus apella)]Google Scholar
Rodrigues, B 2014 Etologia aplicada ao enriquecimento ambiental para macacos-prego (Sapajus spp) semi-cativos. Dissertation, Universidade de São Paulo, Brazil. [Title translation: Ethology applied to environmental enrichment for semi-captive capuchin monkeys (Sapajus spp)]Google Scholar
Rose, PE, Nash, SM and Riley, LM 2017 To pace or not to pace? A review of what abnormal repetitive behavior tells us about zoo animal management. Journal of Veterinary Behavior: Clinical Applications and Research 20: 11–21. https://doi.org/10.1016/j.jveb.2017.02.007CrossRefGoogle Scholar
Rushen, J 1993 The ‘coping’ hypothesis of stereotypic behavior. Animal Behaviour 45: 613–615. https://doi.org/10.1006/anbe.1993.1071CrossRefGoogle Scholar
Sapolsky, RM 2005 The influence of social hierarchy on primate health. Science 308: 648–652. https://doi.org/10.1126/sci-ence.1106477CrossRefGoogle ScholarPubMed
Seeman, TE, McEwen, BS, Rowe, JW and Singer, BH 2001 Allostatic load as a marker of cumulative biological risk: MacArthur studies of successful aging. Proceedings of the National Academy of Science 98(8): 4770–4775. https://doi.org/10.1073/pnas.081072698CrossRefGoogle ScholarPubMed
Verderane, MP, Falótico, T, Resende, BD, Labruna, MB, Izar, P and Ottoni, EB 2007 Anting in a semifree-ranging group of Cebus apella. International Journal of Primatology 28(1): 47. https://doi.org/10.1007/s10764-006-9102-8CrossRefGoogle Scholar