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Individual variation in chimpanzee (Pan troglodytes) repertoires of abnormal behaviour

Published online by Cambridge University Press:  01 January 2023

Z Goldsborough ,
EHM Sterck ,
FBM de Waal  and
CE Webb
Z Goldsborough*
Affiliation:
Animal Behaviour & Cognition, Department of Biology, Utrecht University, Utrecht, The Netherlands Department for the Ecology of Animal Societies, Max Planck of Animal Behavior, Bücklestraße 5a, Room 519a, 78467, Konstanz, Germany Department of Biology, University of Konstanz, Konstanz, Germany
EHM Sterck
Affiliation:
Animal Behaviour & Cognition, Department of Biology, Utrecht University, Utrecht, The Netherlands Animal Science Department, BPRC, Rijswijk, The Netherlands
FBM de Waal
Affiliation:
Animal Behaviour & Cognition, Department of Biology, Utrecht University, Utrecht, The Netherlands Department of Psychology, Emory University, Atlanta, USA
CE Webb
Affiliation:
Animal Behaviour & Cognition, Department of Biology, Utrecht University, Utrecht, The Netherlands Department of Human Evolutionary Biology, Harvard University, Cambridge, USA
*
* Contact for correspondence: zgoldsborough@outlook.com
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Abstract

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Abnormal behaviour in captive animals is both pervasive and ambiguous. Although individual differences are central to the field of animal welfare, studies on abnormal behaviour predominantly employ quantitative, population-level approaches. For example, whereas previous studies on chimpanzee (Pan troglodytes) abnormal behaviour have reported significant variation between groups or individuals in the quantity (eg frequency and duration) of abnormal behaviour, much less is known about qualitative differences. Individual abnormal behavioural repertoires may be highly idiosyncratic, where certain behaviours are over-represented (ie individually specific abnormal behavioural ‘signatures’). The present study investigated qualitative individual variation in the abnormal behaviour of chimpanzees (n = 15) housed at Royal Burgers’ Zoo in Arnhem, The Netherlands. Substantial variation was found between individuals in the diversity (size and evenness) and overall composition of their abnormal behavioural repertoires. Factors including age, sex, and rank did not significantly account for dissimilarity of individuals’ abnormal behavioural repertoires, but kin dyads showed more similar abnormal behaviour than non-kin dyads. Further exploratory analyses examined whether individual variation in one abnormal behaviour (coprophagy) predicted variation in stress-related behaviour (self-scratching). This allowed us to tentatively conclude that there were also individual differences in the link between a given abnormal behaviour and the behavioural expression of stress. Qualitative individual variation in abnormal behaviour provides a novel angle to a literature traditionally focused on quantifying abnormal behaviour at the group- or species-level and may thus represent an important yet previously overlooked source of variation in the extent to which abnormal behaviour reflects the state of individual welfare.

Keywords

animal welfarechimpanzeescoprophagystereotypical behaviourstresszoo-housed
Type
Research Article
Information
Animal Welfare , Volume 31 , Issue 1 , February 2022 , pp. 125 - 135
Copyright
© 2022 Universities Federation for Animal Welfare

References

Aureli, F, Cords, M and van Schaik, CP 2002 Conflict resolution fol-lowing aggression in gregarious animals: A predictive framework. Animal Behaviour 64: 325–343. https://doi.org/10.1006/anbe.2002.3071CrossRefGoogle Scholar
Baker, KC and Aureli, F 1997 Behavioural indicators of anxiety: an empirical test in chimpanzees. Behaviour 134: 1031–1050. https://doi.org/10.1163/156853997X00386CrossRefGoogle Scholar
Bertolani, P and Pruetz, JD 2011 Seed reingestion in savannah chim-panzees (Pan troglodytes verus) at Fongoli, Senegal. International Journal of Primatology 32: 1123–1132. https://doi.org/10.1007/s10764-011-9528-5CrossRefGoogle Scholar
Birkett, LP and Newton-Fisher, NE 2011 How abnormal is the behaviour of captive, zoo-living chimpanzees? PLoS One 6. https://doi.org/10.1371/journal.pone.0020101Google Scholar
Bloomsmith, MA, Baker, KC, Ross, SR and Lambeth, SP 2006 Early rearing conditions and captive chimpanzee behavior: Some surprising findings. In: Sackett, GP, Ruppentahal, GC and Elias, K (eds) Nursery Rearing of Nonhuman Primates in the 21st Century pp 289–312. Springer US: Boston, MA. USA. https://doi.org/10.1007/978-0-387-25640-5_15CrossRefGoogle Scholar
Bloomsmith, MA, Clay, AW, Lambeth, SP, Lutz, CK, Breaux, SD, Lammey, ML, Franklin, AN, Neu, KA, Perlman, JE, Reamer, LA, Mareno, MC, Schapiro, SJ, Vazquez, M and Bourgeois, SR 2019 Survey of behavioral indices of welfare in research chimpanzees (Pan troglodytes) in the United States. Journal of the American Association for Laboratory Animal Science 58: 160–177. https://doi.org/10.30802/AALAS-JAALAS-18-000034CrossRefGoogle ScholarPubMed
Boesch, C 2012 Wild Cultures: A Comparison between Chimpanzee and Human Cultures. Cambridge University Press: Cambridge, UK. https://doi.org/10.1017/CBO9781139178532CrossRefGoogle Scholar
Bonnie, KE, Horner, V, Whiten, A and de Waal, FB 2007 Spread of arbitrary conventions among chimpanzees: a controlled experiment. Proceedings of the Royal Society B: Biological Sciences 274: 367–372. https://doi.org/10.1098/rspb.2006.3733CrossRefGoogle ScholarPubMed
Brando, S and Buchanan-Smith, HM 2017 The 24/7 approach to promoting optimal welfare for captive wild animals. Behavioural Processes 156: 83–95. https://doi.org/10.1016/j.beproc.2017.09.010CrossRefGoogle ScholarPubMed
Burn, CC 2017 Bestial boredom: a biological perspective on animal boredom and suggestions for its scientific investigation. Animal Behaviour 130: 141–151. https://doi.org/10.1016/j.anbehav.2017.06.006CrossRefGoogle Scholar
Clay, AW, Bard, KA and Bloomsmith, MA 2018 Effects of sex and early rearing condition on adult behavior, health, and well-being in captive chimpanzees (Pan troglodytes). Behavioural Processes 156: 58–76. https://doi.org/10.1016/j.beproc.2017.06.011CrossRefGoogle ScholarPubMed
Crawley, JN, Skolnick, P, Pickar, D, Chrousos, GP, Linnoila, M, Ninan, PT and Paul, SM 1985 Neuropharmacological antago-nism of the B-carboline induced anxiety response in rhesus mon-keys. The Journal of Neuroscience 5: 477–485. https://doi.org/10.1523/JNEUROSCI.05-02-00477.1985CrossRefGoogle Scholar
Dekker, D, Krackhardt, D and Snijders, TAB 2007 Sensitivity of MRQAP tests to collinearity and autocorrelation conditions. Psychometrika 72: 563–581. https://doi.org/10.1007/s11336-007-9016-1CrossRefGoogle ScholarPubMed
DeLongis, A and Holtzman, S 2005 Coping in context: The role of stress, social support, and personality in coping. Journal of Personality 73: 1633–1656. https://doi.org/10.1111/j.1467-6494.2005.00361.xCrossRefGoogle ScholarPubMed
de Vries, H, Netto, WJ and Hanegraaf, PLH 1993 Matman: a program for the analysis of sociometric matrices and behavioural transition matrices. Behaviour 125: 157–175. https://doi.org/10.1163/156853993X00218Google Scholar
Erwin, J and Deni, R 1979 Strangers in a strange land: abnormal behaviors or abnormal environments? In: Maple, TL and Mitchell, G (eds) Captivity and Behavior, Primates in Breeding Colonies, Laboratories, and Zoos pp 1–28. Van Nostrand Reinhold: New York, USAGoogle Scholar
Farine, DR 2013 Animal social network inference and permutations for ecologists in R using asnipe. Methods in Ecology and Evolution 4: 1187–1194. https://doi.org/10.1111/2041-210X.12121CrossRefGoogle Scholar
Fraser, ON, Stahl, D and Aureli, F 2008 Stress reduction through consolation in chimpanzees. Proceedings of the National Academy of Sciences 105: 8557–8562. https://doi.org/10.1073/pnas.0804141105CrossRefGoogle ScholarPubMed
Fritz, J, Maki, S, Nash, LT, Martin, T and Matevia, M 1992 The relationship between forage material and levels of coprophagy in captive chimpanzees (Pan troglodytes). Zoo Biology 11: 313–318. https://doi.org/10.1002/zoo.1430110503CrossRefGoogle Scholar
Goldsborough, Z, Webb, CE, de Waal, FBM and van Leeuwen, EJ 2021 Zoo-housed female chimpanzee adopts local female-specific tradition upon immigrating into a new group. Behaviour 158: 547–564. https://doi.org/10.1163/1568539X-bja10075CrossRefGoogle Scholar
Goldstein, MJ 1973 Individual differences in response to stress. American Journal of Community Psychology 1: 113–137. https://doi.org/10.1007/BF00880131CrossRefGoogle ScholarPubMed
Greening, L 2019 Stereotypies and other abnormal behavior in welfare assessment. In: Choe, J (ed) Encyclopedia of Animal Behavior pp 141–146. Elsevier: Amsterdam, The Netherlands. https://doi.org/10.1016/B978-0-12-809633-8.90023-2CrossRefGoogle Scholar
Hill, CA 1966 Coprophagy in apes. International Zoo Yearbook 6: 251–257. https://doi.org/10.1111/j.1748-1090.1966.tb01784.xCrossRefGoogle Scholar
Holahan, CJ and Moos, RH 1986 Personality, coping, and family resources in stress resistance: A longitudinal analysis Journal of Personality and Social Psychology 51: 389–395. https://doi.org/10.1037/0022-3514.51.2.389CrossRefGoogle ScholarPubMed
Hook, MA, Lambeth, SP, Perlman, JE, Stavisky, R, Bloomsmith, MA and Schapiro, SJ 2002 Inter-group variation in abnormal behavior in chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta). Applied Animal Behaviour Science 76: 165–176. https://doi.org/10.1016/S0168-1591(02)00005-9CrossRefGoogle Scholar
Hopper, LM, Freeman, HD and Ross, SR 2016 Reconsidering coprophagy as an indicator of negative welfare for captive chim-panzees. Applied Animal Behaviour Science 176: 112–119. https://doi.org/10.1016/j.applanim.2016.01.002CrossRefGoogle Scholar
Hopper, LM, Schapiro, SJ, Lambeth, SP and Brosnan, SF 2011 Chimpanzees’ socially maintained food preferences indicate both conservatism and conformity. Animal Behaviour 81: 1195–1202. https://doi.org/10.1016/j.anbehav.2011.03.002CrossRefGoogle ScholarPubMed
Jacobson, SL, Ross, SR and Bloomsmith, MA 2016 Characterising abnormal behaviour in a large population of zoo-housed chimpanzees: prevalence and potential influencing factors. PeerJ 4: e2225. https://doi.org/10.7717/peerj.2225CrossRefGoogle Scholar
Koski, SE and Sterck, EHM 2007 Triadic postconflict affiliation in captive chimpanzees: does consolation console? Animal Behaviour 73: 133–142. https://doi.org/10.1016/j.anbehav.2006.04.009CrossRefGoogle Scholar
Krief, S, Jamart, A and Hladik, CM 2004 On the possible adaptive value of coprophagy in free-ranging chimpanzees. Primates 45: 141–145. https://doi.org/10.1007/s10329-003-0074-4CrossRefGoogle ScholarPubMed
Kutsukake, N 2003 Assessing relationship quality and social anxiety among wild chimpanzees using self-directed behaviour. Behaviour 140: 1153–1171. https://doi.org/10.1163/156853903322589687CrossRefGoogle Scholar
Leavens, DA, Aureli, F and Hopkins, WD 2004 Behavioral evi-dence for the cutaneous expression of emotion in a chimpanzee (Pan troglodytes). Behaviour 141: 979–997. https://doi.org/10.1163/1568539042360189CrossRefGoogle Scholar
Lutz, C 2018 A cross-species comparison of abnormal behaviour in three species of singly housed old world monkeys. Applied Animal Behaviour Science 199: 52–58. https://doi.org/10.1016/j.applanim.2017.10.010CrossRefGoogle Scholar
Lutz, C, Well, A and Novak, M 2003 Stereotypic and self-injuri-ous behavior in rhesus macaques: a survey and retrospective anal-ysis of environment and early experience. American Journal of Primatology 60: 1–15. https://doi.org/10.1002/ajp.10075CrossRefGoogle Scholar
Maestripieri, D, Schino, G, Aureli, F and Troisi, A 1992 A mod-est proposal: displacement activities as an indicator of emotions in primates. Animal Behaviour 44: 967–979. https://doi.org/10.1016/S0003-3472(05)80592-5CrossRefGoogle Scholar
Marchant-Forde, JN 2015 The science of animal behavior and welfare: Challenges, opportunities, and global perspective. Frontiers in Veterinary Science 2: 16. https://doi.org/10.3389/fvets.2015.00016CrossRefGoogle ScholarPubMed
Marriner, LM and Drickamer, LC 1994 Factors influencing stereotyped behavior of primates in a zoo. Zoo Biology 13: 267–275. https://doi.org/10.1002/zoo.1430130308CrossRefGoogle Scholar
Martin, P and Bateson, P 2007 Measuring Behaviour, Measuring Behaviour, Cambridge University Press: Cambridge, UK. https://doi.org/10.1017/CBO9780511810893CrossRefGoogle Scholar
Mason, G 2006 Stereotypic behaviour in captive animals: funda-mentals, and implications for welfare and beyond. In: Mason, G and Rushen, J (eds) Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare pp 325–351. CABI: Wallingford, UK. https://doi.org/10.1079/9780851990040.0325CrossRefGoogle Scholar
Mason, GJ and Latham, NR 2004 Can't stop, won't stop: Is stereotypy a reliable animal welfare indicator? Animal Welfare 13: 57–69Google Scholar
Nash, LT, Fritz, J, Alford, PA, Brent, L and Fritz, J 1999 Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees (Pan troglodytes). American Journal of Primatology 48: 15–29. https://doi.org/10.1002/(SICI)1098-2345(1999)48:1<15::AID-AJP2>3.0.CO;2-R3.0.CO;2-R>CrossRefGoogle Scholar
Neal Webb, SJ, Hau, J and Schapiro, SJ 2019 Does group size matter? Captive chimpanzee (Pan troglodytes) behavior as a function of group size and composition. American Journal of Primatology 81: e22947. https://doi.org/10.1002/ajp.22947CrossRefGoogle ScholarPubMed
Neukadye 2017 Timestamped Field Notes (Version 4.7.0). https://itunes.apple.com/nl/app/timestamped-field-notes/id521505393Google Scholar
Ninan, PT, Insel, TM, Cohen, RM, Cook, JM, Skolnick, P and Paul, SM 1982 Benzodiazepine receptor-mediated experimental ‘anxiety’ in primates. Science 218: 1332–1334. https://doi.org/10.1126/science.6293059CrossRefGoogle ScholarPubMed
Paulk, HH, Dienske, H and Ribbens, LG 1977 Abnormal behav-ior in relation to cage size in rhesus monkeys. Journal of Abnormal Psychology 86: 87–92. https://doi.org/10.1037/0021-843X.86.1.87CrossRefGoogle Scholar
Payne, CLR, Webster, TH and Hunt, KD 2008 Coprophagy by the semi-habituated chimpanzees of Semliki, Uganda. Pan Africa News 15: 29–32. https://doi.org/10.5134/143493CrossRefGoogle Scholar
Pielou, EC 1966 The measurement of diversity in different types of biological collections. Journal of Theoretical Biology 13: 131–144. https://doi.org/10.1016/0022-5193(66)90013-0CrossRefGoogle Scholar
R Development Core Team 2016 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing: Vienna, AustriaGoogle 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
Ross, SR and Bloomsmith, MA 2011 A comment on Birkett and Newton-Fisher. PLoS One 6(6): e20101. https://doi.org/10.1371/journal.pone.0020101Google Scholar
Schino, G, Perretta, G, Taglioni, AM, Monaco, V and Troisi, A 1996 Primate displacement activities as an ethopharmacological model of anxiety. Anxiety 2: 186–191. https://doi.org/10.1002/(SICI)1522-7154(1996)2:4<186::AID-ANXI5>3.0.CO;2-M3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Schino, G, Troisi, A, Perretta, G and Monaco, V 1991 Measuring anxiety in nonhuman primates: Effect of lorazepam on macaque scratching. Pharmacology, Biochemistry and Behavior 28: 889–891. https://doi.org/10.1016/0091-3057(91)90258-4CrossRefGoogle Scholar
Schlingloff, L and Moore, R 2017 Do chimpanzees conform to social norms? The Routledge Handbook of Philosophy of Animal Minds: 381-389. https://doi.org/10.4324/9781315742250-37CrossRefGoogle Scholar
Seery, MD, Holman, EA and Silver, RC 2010 Whatever does not kill us: Cumulative lifetime adversity, vulnerability, and resilience. Journal of Personality and Social Psychology 99: 1025–1041. https://doi.org/10.1037/a0021344CrossRefGoogle Scholar
Spijkerman, RP, Dienske, H, van Hooff, JARAM and Jens, W 1994 Causes of body rocking in chimpanzees (Pan troglodytes). Animal Welfare 3: 193–211Google Scholar
Špinka, M 2019 Animal agency, animal awareness and animal wel-fare. Animal Welfare 28: 11–20. https://doi.org/10.7120/09627286.28.1.011CrossRefGoogle Scholar
Trollope, J 1977 A preliminary survey of behavioural stereotypes in captive primates. Laboratory Animals 11: 195–196. https://doi.org/10.1258/002367777780936666CrossRefGoogle ScholarPubMed
Walsh, S, Bramblett, CA and Alford, PL 1982 A vocabulary of abnormal behaviors in restrictively reared chimpanzees. American Journal of Primatology 3: 315–319. https://doi.org/10.1002/ajp.1350030131CrossRefGoogle ScholarPubMed
Whiten, A, Goodall, J, McGrew, WC, Nishida, T, Reynolds, V, Sugiyama, Y, Tutin, CEG, Wrangham, RW and Boesch, C 1999 Cultures in chimpanzees. Nature 399: 682–685. https://doi.org/10.1038/21415CrossRefGoogle ScholarPubMed
Whitten, PL, Stavisky, R, Aureli, F and Russell, E 1998 Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes). American Journal of Primatology 44: 57–69. https://doi.org/10.1002/(SICI)1098-2345(1998)44:1<57::AID-AJP5>3.0.CO;2-W3.0.CO;2-W>CrossRefGoogle ScholarPubMed
Yamanashi, Y and Matsuzawa, T 2010 Emotional consequences when chimpanzees (Pan troglodytes) face challenges: Individual dif-ferences in self-directed behaviours during cognitive tasks. Animal Welfare 19: 25–30Google Scholar
Yamanashi, Y, Nogami, E, Teramoto, M, Morimura, N and Hirata, S 2018 Adult-adult social play in captive chimpanzees: Is it indicative of positive animal welfare? Applied Animal Behaviour Science 199: 75–83. https://doi.org/10.1016/j.applanim.2017.10.006CrossRefGoogle Scholar
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