Motor Stereotypic Behaviors in Zoo Rhesus Monkeys: a Case Study of the Central Zoo, Kathmandu, Nepal
Abstract
Motor stereotypic behaviors (MSBs) are a kind of repetitive behaviors performed by stressed animals and are more common in captivity. This study aimed to assess whether the MSB in captive rhesus monkeys varies between males and females, and with the extent of visitor-monkey interactions. A group of six rhesus monkeys (two adult males and four adult females; among females, two were rescued from the wild and two were captive-born) housed in the Central Zoo, Kathmandu Nepal were sampled in the study. Behavioral observations were done by focal animal sampling for 30 minutes in each session from 8:00 AM till 10:00 AM in the absence of visitors and 10:00 AM–12:00 PM in the presence of visitors. At every 10 minutes interval, the number of visitors around the cage and the level of visitor-monkey interactions were scanned. Pacing and bounce were the MSBs performed by the zoo rhesus monkeys. Females, especially the rescued ones, performed significantly more MSBs than the males. An increase in visitor-monkey interaction involved the monkeys into more begging and feeding, which in turn lowered the MSBs. The findings of this study indicate that interactive enrichment such as feeding and visitor-monkey interactions help to reduce MSBs in zoo monkeys.
References
Altmann, J. 1974. Observational sampling study of behavior: Sampling methods. Behavior, 49, 227-265.
https://doi.org/10.1163/156853974X00534
Barongi, R., Fisken, F. A., Parker, M. & Gusset, M. (eds.). 2015. Committing to conservation: The world zoo and aquarium conservation strategy: World Association of Zoos and Aquariums (WAZA) Executive Office, Gland, Switzerland, 1-70.
Bartlett, M. S. & Fowler, R. H. 1937. Properties of sufficiency and statistical tests. Proceedings of the Royal Society of London. Series A - Mathematical and Physical Sciences, 160, 268-282.
https://doi.org/10.1098/rspa.1937.0109
Bashaw, M. J., Tarou, L. R., Maki, T. S. & Maple, T. L. 2001. A survey assessment of variable related to stereotypic in captive giraffe and okapi. Applied Animal Behaviour Science, 73, 235-247.
https://doi.org/10.1016/S0168-1591(01)00137-X
Ben-Shachar, M., Lüdecke, D. & Makowski, D. 2020. effectsize: Estimation of Effect Size Indices and Standardized Parameters. Journal of Open Source Software, 5, 2815.
https://doi.org/10.21105/joss.02815
Capitanio, J. P. 1986. Behavioral pathology. In: Mitchell, G., Erwin, J. & Swindler, D. (eds.) Comparative primate biology. Behavior, Conservation and Ecology. A.R. Liss, New York: 411-454.
Carr, N. & Cohen, S. 2015. The public face of zoos: Images of entertainment, education and conservation. Anthrozoös, 24, 175-189.
https://doi.org/10.2752/175303711X12998632257620
Conde, D. A., Flesness, N., Colchero, F., Jones, O. R. & Scheuerlein, A. 2011. Conservation: An emerging role of zoos to conserve biodiversity. Science, 331, 1390-1.
https://doi.org/10.1126/science.1200674
Crast, J., Bloomsmith, M. A., Perlman, J. E., Meeker, T. L. & Remillard, C. M. 2014. Abnormal behaviour in captive sooty mangabeys. Animal Welfare, 23, 167-177.
https://doi.org/10.7120/09627286.23.2.167
Cuarón, A. D. 2005. Further role of zoos in conservation: Monitoring wildlife use and the dilemma of receiving donated and confiscated animals. Zoo Biology, 24, 115-124.
https://doi.org/10.1002/zoo.20040
de la Barrera Cardozo, M., Chiba de Castro, W. A. & Aguiar, L. M. 2021. Stress behaviors in captive robust capuchins: Effects of humidity, visitors, management and sex. American Journal of Primatology, 83, e23265.
https://doi.org/10.1002/ajp.23265
Goodenough, A. E., McDonald, K., Moody, K. & Wheeler, C. 2019. Are "visitor effects" overestimated? Behaviour in captive lemurs is mainly driven by co-variation with time and weather. Journal of Zoo and Aquarium Research, 7, 59-66.
Gottlieb, D. H., Capitanio, J. P. & McCowan, B. 2013 a. Risk factors for stereotypic behavior and self-biting in rhesus macaques (Macaca mulatta): animal's history, current environment, and personality. American Journal of Primatology, 75, 995-1008.
https://doi.org/10.1002/ajp.22161
Gottlieb, D. H., Coleman, K. & McCowan, B. 2013 b. The effects of predictability in daily husbandry routines on captive rhesus macaques (Macaca mulatta). Applied Animal Behaviour Science, 143, 117-127.
https://doi.org/10.1016/j.applanim.2012.10.010
Gottlieb, D. H., Maier, A. & Coleman, K. 2015. Evaluation of environmental and intrinsic factors that contribute to stereotypic behavior in captive rhesus macaques (Macaca mulatta). Applied Animal Behaviour Science, 171, 184-191.
https://doi.org/10.1016/j.applanim.2015.08.005
Hashmi, A. & Sullivan, M. 2020. The visitor effect in zoo-housed apes: The variable effect on behaviour of visitor number and noise. Journal of Zoo and Aquarium Research, 8, 268-282.
Honess, P. E. & Marin, C. M. 2006. Enrichment and aggression in primates. Neuroscience and Biobehavioral Reviews, 30, 413-436.
https://doi.org/10.1016/j.neubiorev.2005.05.002
Hook, M. A., Lambeth, S. P., Perlman, J. E., Stavisky, R., Bloomsmith, M. A. & Schapiro, S. J. 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)00005-9
Hosey, G. 2008. A preliminary model of human-animal relationships in the zoo. Applied Animal Behaviour Science, 109, 105-127.
https://doi.org/10.1016/j.applanim.2007.04.013
Hosey, G. 2013. Hediger revisited: How do zoo animals see us? Journal of Applied Animal Welfare Science, 16, 338-359.
https://doi.org/10.1080/10888705.2013.827916
Hosey, G. R. & Druck, P. L. 1987. The influence of zoo visitors on the behaviour of captive primates. Applied Animal Behaviour Science, 18, 19-29.
https://doi.org/10.1016/0168-1591(87)90251-6
Jacobson, S. L., Ross, S. R. & Bloomsmith, M. A. 2016. Characterizing abnormal behavior in a large population of zoo-housed chimpanzees: prevalence and potential influencing factors. PeerJ, 4, e2225.
https://doi.org/10.7717/peerj.2225
Jakob-Hoff, R., Kingan, M., Fenemore, C., Schmid, G., Cockrem, J. F., Crackle, A., Bemmel, E. V., Connor, R. & Descovich, K. 2019. Potential impact of construction noise on selected zoo animals. Animals, 9, 1-25.
https://doi.org/10.3390/ani9080504
Jones, H., McGregor, P. K., Farmer, H. L. & Baker, K. R. 2016. The influence of visitor interaction on the behavior of captive crowned lemurs (Eulemur coronatus) and implications for welfare. Zoo Biology, 35, 222-227.
https://doi.org/10.1002/zoo.21291
Lewis, M. & Kim, S. J. 2009. The pathophysiology of restricted repetitive behavior. Journal of Neurodevelopmental Disorders, 1, 114-32.
https://doi.org/10.1007/s11689-009-9019-6
Line, S. W., Morgan, K. N. & Markowitz, H. 1991. Simple toys do not alter the behavior of aged rhesus monkeys. Zoo Biology, 10, 473-484.
https://doi.org/10.1002/zoo.1430100606
Lutz, C., Well, A. & Novak, M. 2003. Stereotypic and self-injurious behavior in rhesus macaques: a survey and retrospective analysis of environment and early experience. American Journal of Primatology, 60, 1-15.
https://doi.org/10.1002/ajp.10075
Lutz, C. K. 2018. A cross-species comparison of abnormal behavior in three species of singly-housed Old world monkeys. Applied Animal Behaviour Science, 199, 52-58.
https://doi.org/10.1016/j.applanim.2017.10.010
Lutz, C. K., Coleman, K., Hopper, L. M., Novak, M. A., Perlman, J. E. & Pomerantz, O. 2022. Nonhuman primate abnormal behavior: Etiology, assessment, and treatment. American Journal of Primatology, 84, e23380.
https://doi.org/10.1002/ajp.23380
Lutz, C. K., Williams, P. C. & Sharp, R. M. 2014. Abnormal behavior and associated risk factors in captive baboons (Papio hamadryas spp.). American Journal of Primatology, 76, 355-61.
https://doi.org/10.1002/ajp.22239
Mallapur, A. & Choudhury, B. C. 2003. Behavioral abnormalities in captive nonhuman primates. Journal of Applied Animal Welfare Science, 6, 275-84.
https://doi.org/10.1207/s15327604jaws0604_2
Mallapur, A., Sinha, A. & Waran, N. 2005. Influence of visitor presence on the behaviour of captive lion-tailed macaques (Macaca silenus) housed in Indian zoos. Applied Animal Behaviour Science, 94, 341-352.
https://doi.org/10.1016/j.applanim.2005.02.012
Mangiafico, S. 2022. rcompanion: Functions to Support Extension Education Program Evaluation. [Online]. Available: https://CRAN.R-project.org/package=rcompanion.
Marriner, L. M. & Drickamer, L. C. 1994. Factors influencing stereotyped behavior of primates in a zoo. Zoo Biology, 13, 267-275.
https://doi.org/10.1002/zoo.1430130308
Mason, G. J. 1991. Stereotypies an suffering. Behavioral Processes, 25, 103-115.
https://doi.org/10.1016/0376-6357(91)90013-P
Mason, G. J. & Latham, N. 2004. Can't stop, won't stop: is stereotypy a reliable animal welfare indicator? Animal Welfare, 13 (Suppl.), S57-S69.
https://doi.org/10.1017/S096272860001438X
Morgan, K. N. & Tromborg, C. T. 2007. Sources of stress in captivity. Applied Animal Behaviour Science, 102, 262-302.
https://doi.org/10.1016/j.applanim.2006.05.032
Pan, X., Liu, F., Song, Y., Wang, H., Wang, L., Qiu, H., Price, M. & Li, J. 2021. Motor stereotypic behavior was associated with immune response in macaques: Insight from transcriptome and gut microbiota analysis. Frontiers in Microbiology, 12, 644540.
https://doi.org/10.3389/fmicb.2021.644540
Patrick, P. G. & Caplow, S. 2018. Identifying the foci of mission statements of the zoo and aquarium community. Museum Management and Curatorship, 33, 120-135.
https://doi.org/10.1080/09647775.2018.1438205
Poirier, C. & Bateson, M. 2017. Pacing stereotypies in laboratory rhesus macaques: Implications for animal welfare and the validity of neuroscientific findings. Neuroscience and Biobehavioral Reviews, 83, 508-515.
https://doi.org/10.1016/j.neubiorev.2017.09.010
Polanco, A., McCowan, B., Niel, L., Pearl, D. L. & Mason, G. 2021. Recommendations for abnormal behaviour Ethograms in monkey research. Animals, 11, 1461.
https://doi.org/10.3390/ani11051461
Pomerantz, O., Paukner, A. & Terkel, J. 2012. Some stereotypic behaviors in rhesus macaques (Macaca mulatta) are correlated with both perseveration and the ability to cope with acute stressors. Behavioural Brain Research, 230, 274-80.
https://doi.org/10.1016/j.bbr.2012.02.019
Rommeck, I., Anderson, K., Heagerty, A., Cameron, A. & McCowan, B. 2009. Risk factors and remediation of self-injurious and self-abuse behavior in rhesus macaques. Journal of Applied Animal Welfare Science, 12, 61-72.
https://doi.org/10.1080/10888700802536798
Schapiro, S. J., Porter, P. M. & Suarez, S. A. 1995. The behavior of singly-caged, yearling rhesus monkeys is affected by the environment outside of the cage. Applied Animal Behaviour Science, 45, 151-163.
https://doi.org/10.1016/0168-1591(95)00597-L
Shapiro, S. S., Wilk, M. B. 1965. An analysis of variance test for normality (complete samples). Biometrika, 52, 591-611.
https://doi.org/10.1093/biomet/52.3-4.591
Sharma, S., Khanal, L., Shrestha, S., Pandey, N., Bellanca, R. U. & Kyes, R. C. 2023. Zoo visitors as a source of enrichment to reduce abnormal behavior in captive rhesus macaques (Macaca mulatta) in the Central Zoo, Kathmandu, Nepal. Journal of Animal Behaviour and Biometeorology, 11, e2023005.
https://doi.org/10.31893/jabb.23005
Sherwen, S. L. & Hemsworth, P. H. 2019. The visitor effect on zoo animals: Implications and opportunities for zoo animal welfare. Animals, 9,
https://doi.org/10.3390/ani9060366
Shih, H.-Y., Yu, J.-F. & Wang, L.-C. 2016. Stereotypic behaviors in bears. Taiwan Veterinary Journal, 42, 11-17.
https://doi.org/10.1142/S168264851530004X
Shyne, A. 2006. Meta-analytic review of the effects of enrichment on stereotypic behavior in zoo mammals. Zoo Biology, 25, 317-337.
https://doi.org/10.1002/zoo.20091
Todd, P. A., Macdonald, C. & Coleman, D. 2007. Visitor-associated variation in captive Diana monkey (Cercopithecus diana diana) behaviour. Applied Animal Behaviour Science, 107, 162-165.
https://doi.org/10.1016/j.applanim.2006.09.010
Vandeleest, J. J., McCowan, B. & Capitanio, J. P. 2011. Early rearing interacts with temperament and housing to influence the risk for motor stereotypy in rhesus monkeys (Macaca mulatta). Applied Animal Behaviour Science, 132, 81-89.
https://doi.org/10.1016/j.applanim.2011.02.010
Vanlangendonck, N., Nuñez, G., Chaves, A. & Gutiérrez-Espeleta, G. A. 2015. New route of investigation for understanding the impact of human activities on the physiology of non-human primates. Journal of Primatology, 04, 123-129.
https://doi.org/10.4172/2167-6801.1000123
Wells, D. L. 2005. A note on the influence of visitors on the behaviour and welfare of zoo-housed gorillas. Applied Animal Behaviour Science, 93, 13-17.