Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-16T11:16:50.808Z Has data issue: false hasContentIssue false
  • English
  • Français

The utility of voluntary weighing in captive group-living rhesus macaques (Macaca mulatta)

Published online by Cambridge University Press:  01 January 2023

DGM Zijlmans ,
MK Vernes ,
EHM Sterck  and
JAM Langermans
DGM Zijlmans*
Affiliation:
Animal Science Department, Biomedical Primate Research Centre, Postbus 3306, 2280 GH Rijswijk, The Netherlands Animal Behaviour and Cognition (formerly Animal Ecology), Department of Biology, Utrecht University, Utrecht, The Netherlands
MK Vernes
Affiliation:
Animal Science Department, Biomedical Primate Research Centre, Postbus 3306, 2280 GH Rijswijk, The Netherlands
EHM Sterck
Affiliation:
Animal Science Department, Biomedical Primate Research Centre, Postbus 3306, 2280 GH Rijswijk, The Netherlands Animal Behaviour and Cognition (formerly Animal Ecology), Department of Biology, Utrecht University, Utrecht, The Netherlands Joint senior authors
JAM Langermans
Affiliation:
Animal Science Department, Biomedical Primate Research Centre, Postbus 3306, 2280 GH Rijswijk, The Netherlands Department Population Health Sciences, Unit Animals in Science & Society, Faculty of Veterinary Medicine, Utrecht University, Utrecht, The Netherlands Joint senior authors
*
* Contact for correspondence: [email protected]/[email protected]
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.

Bodyweight is an important health and welfare indicator for captive non-human primates (NHPs). Bodyweight can be measured during routine handling procedures, which cause stress. Alternatively, animals can be trained to step onto a scale, but training success varies greatly between individuals. Being able to weigh animals regularly without having to handle or train them is thus desirable for monitoring animal health and welfare. This study investigates the utility, ie the participation, reliability and time investment, of voluntary weighing in captive NHPs living in large social groups. Subjects of the study were 92 rhesus macaques (Macaca mulatta) housed in four social groups at the Biomedical Primate Research Centre in Rijswijk, The Netherlands. A scale was placed in their home enclosure during several sessions. Individuals were unwilling to step onto an unbaited scale. When likeable food items were used to attract individuals to the scale, 68% of them stepped onto the scale. Age and dominance rank did not affect stepping onto the scale, whereas exploratory tendency and social group did. The level of agreement between bodyweight by voluntary weighing and bodyweight measured during sedation was very high. These results show that the majority of rhesus macaques in social groups can be weighed voluntarily and that voluntary weighing is reliable. When optimising and further developing the method, voluntary weighing can form a valuable tool in the captive management of NHPs.

Keywords

animal welfarebodyweightcaptive managementmacaquesocial housingvoluntary weighing
Type
Research Article
Information
Animal Welfare , Volume 30 , Issue 3 , August 2021 , pp. 249 - 258
Creative Commons
Creative Common License - CCCreative Common License - BYCreative Common License - NCCreative Common License - SA
This is an Open Access article, distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike licence (https://creativecommons.org/licenses/by-nc-sa/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the same Creative Commons licence is included and the original work is properly cited. The written permission of Cambridge University Press must be obtained for commercial re-use.
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Universities Federation for Animal Welfare

References

Altmann, J and Alberts, S 1987 Body mass and growth rates in a wild primate population. Oecologia, 72: 15–20. https://doi.org/10.1007/BF00385038CrossRefGoogle Scholar
Balcombe, JP, Barnard, ND and Sandusky, C 2004 Laboratory routines cause animal stress. Journal of the American Association for Laboratory Animal Science 43: 42–51Google ScholarPubMed
Bassano, B, von Hardenberg, A, Pelletier, F and Gobbi, G 2003 A method to weigh free-ranging ungulates without han-dling. Wildlife Society Bulletin 31: 1205–1209Google Scholar
Bauer, SA, Leslie, KE, Pearl, DL, Fournier, J and Turner, PV 2010 Survey of prevalence of overweight body condition in labo-ratory-housed cynomolgus macaques (Macaca fascicularis). Journal of the American Association for Laboratory Animal Science 49: 407–414Google ScholarPubMed
Boccia, ML, Laudenslager, M and Reite, M 1988 Food distri-bution, dominance, and aggressive behaviors in bonnet macaques. American Journal of Primatology 16: 123–130. https://doi.org/10.1002/ajp.1350160203CrossRefGoogle Scholar
Brennan, J and Anderson, JR 1988 Varying responses to feeding competition in a group of rhesus monkeys (Macaca mulatta). Primates 29: 353–360. https://doi.org/10.1007/BF02380958CrossRefGoogle Scholar
Bronson, RT, O’Connell, M, Klepper-Kilgore, N, Chalifoux, LV and Sehgal, P 1982 Fatal fasting syndrome of obese macaques. Laboratory Animal Science 32: 187–192Google ScholarPubMed
Caine, NG 1990 Unrecognized anti-predator behaviour can bias observational data. Animal Behaviour 39: 195–197. https://doi.org/10.1016/S0003-3472(05)80741-9CrossRefGoogle Scholar
Carter, AJ, Marshall, HH, Heinsohn, R and Cowlishaw, G 2012 How not to measure boldness: novel object and antipredator responses are not the same in wild baboons. Animal Behaviour 84: 603–609. https://doi.org/10.1016/j.anbehav.2012.06.015CrossRefGoogle ScholarPubMed
Coleman, K, Tully, LA and McMillan, JL 2005 Temperament correlates with training success in adult rhesus macaques. American Journal of Primatology 65: 63–71. https://doi.org/10.1002/ajp.20097CrossRefGoogle ScholarPubMed
Desmond, T and Laule, G 1994 Use of positive reinforcement training in the management of species for reproduction. Zoo Biology 13: 471–477. https://doi.org/10.1002/zoo.1430130509CrossRefGoogle Scholar
Dittus, WP 1998 Birth sex ratios in toque macaques and other mammals: integrating the effects of maternal condition and com-petition. Behavioral Ecology and Sociobiology 44: 149–160. https://doi.org/10.1007/s002650050527CrossRefGoogle Scholar
Drea, CM and Wallen, K 1999 Low-status monkeys “play dumb” when learning in mixed social groups. Proceedings of the National Academy of Sciences 96: 12965–12969. https://doi.org/10.1073/pnas.96.22.12965CrossRefGoogle ScholarPubMed
Fernström, AL, Fredlund, H, Spångberg, M and Westlund, K 2009 Positive reinforcement training in rhesus macaques — training progress as a result of training frequency. American Journal of Primatology 71: 373–379. https://doi.org/10.1002/ajp.20659CrossRefGoogle ScholarPubMed
Freeman, HD and Gosling, SD 2010 Personality in nonhuman pri-mates: a review and evaluation of past research. American Journal of Primatology 72: 653–671. https://doi.org/10.1002/ajp.20833CrossRefGoogle Scholar
Gendreau, Y, Côté, SD and Festa-Bianchet, M 2005 Maternal effects on post-weaning physical and social development in juvenile mountain goats (Oreamnos americanus). Behavioral Ecology and Sociobiology 58: 237–246. https://doi.org/10.1007/s00265-005-0938-2CrossRefGoogle Scholar
Hazama, N 1964 Weighing wild Japanese monkeys in Arashiyama. Primates 5: 81–104. https://doi.org/10.1007/BF01791646CrossRefGoogle Scholar
Horne, WA 2001 Primate anesthesia. Veterinary Clinics of North America: Exotic Animal Practice 4: 239–266. https://doi.org/10.1016/S1094-9194(17)30059-2Google ScholarPubMed
Insel, N, Ruiz-Luna, ML, Permenter, M, Vogt, J, Erickson, CA and Barnes, CA 2008 Aging in rhesus macaques is associated with changes in novelty preference and altered saccade dynam-ics. Behavioral Neuroscience 122: 1328. https://doi.org/10.1037/a0012928CrossRefGoogle Scholar
Jennings M, Prescott MJ and Joint Working Group on Refinement (Primates) 2009 Refinements in husbandry, care and common procedures for non-human primates: Ninth report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement. Laboratory Animals 43: 1–47. https://doi.org/10.1258/la.2008.007143CrossRefGoogle Scholar
Kemp, C, Thatcher, H, Farningham, D, Witham, C, MacLarnon, A, Holmes, A, Semple, S and Bethell, EJ 2017 A protocol for training group-housed rhesus macaques (Macaca mulatta) to cooperate with husbandry and research procedures using positive reinforcement. Applied Animal Behaviour Science 197: 90–100. https://doi.org/10.1016/j.applanim.2017.08.006CrossRefGoogle ScholarPubMed
Kurita, H 1999 Hourly changes in body weight in provisioned free-ranging Japanese macaques (Macaca fuscata). Folia Primatologica 70: 286. https://doi.org/10.1159/000021710CrossRefGoogle ScholarPubMed
Lacreuse, A, Kim, CB, Rosene, DL, Killiany, RJ, Moss, MB, Moore, TL, Chennareddi, L and Herndon, JG 2005 Sex, age, and training modulate spatial memory in the rhesus monkey (Macaca mulatta). Behavioral Neuroscience 119: 118–126. https://doi.org/10.1037/0735-7044.119.1.118CrossRefGoogle ScholarPubMed
Layne, DG and Power, RA 2003 Husbandry, handling, and nutrition for marmosets. Comparative Medicine 53: 351–359Google ScholarPubMed
Le Maho, Y, Gendner, JP, Challet, E, Bost, CA, Gilles, J, Verdon, C, Plumere, C, Robin, JP and Handrich, Y 1993 Undisturbed breeding penguins as indicators of changes in marine resources. Marine Ecology Progress Series 95: 1–6. https://doi.org/10.3354/meps095001CrossRefGoogle Scholar
Massen, JJ, Antonides, A, Arnold, AMK, Bionda, T and Koski, SE 2013 A behavioral view on chimpanzee personality: Exploration tendency, persistence, boldness, and tool-orientation measured with group experiments. American Journal of Primatology 75: 947–958. https://doi.org/10.1002/ajp.22159CrossRefGoogle ScholarPubMed
McGuire, MT, Raleigh, MJ and Pollack, DB 1994 Personality features in vervet monkeys: the effects of sex, age, social status, and group composition. American Journal of Primatology 33: 1–13. https://doi.org/10.1002/ajp.1350330102CrossRefGoogle ScholarPubMed
McKinley, J, Buchanan-Smith, HM, Bassett, L and Morris, K 2003 Training common marmosets (Callithrix jacchus) to co-oper-ate during routine laboratory procedures: Ease of training and time investment. Journal of Applied Animal Welfare Science 6: 209–220. https://doi.org/10.1207/S15327604JAWS0603_06CrossRefGoogle ScholarPubMed
Mori, A 1979 Analysis of population changes by measurement of body weight in the Koshima troop of Japanese monkeys. Primates 20: 371–397. https://doi.org/10.1007/BF02373390CrossRefGoogle Scholar
Netto, WJ, Hanegraaf, PL and de Vries, H 1993 Matman: a pro-gram for the analysis of sociometric matrices and behavioural transition matrices. Behaviour 125: 157–175. https://doi.org/10.1163/156853993X00218Google Scholar
Peiper, UM, Edan, Y, Devir, S, Barak, M and Maltz, E 1993 Automatic weighing of dairy cows. Journal of Agricultural Engineering Research 56: 13–24. https://doi.org/10.1006/jaer.1993.1057CrossRefGoogle Scholar
Prescott, MJ, Bowell, VA and Buchanan-Smith, HM 2005 Training laboratory-housed non-human primates, part 2: Resources for developing and implementing training pro-grammes. Animal Technology and Welfare 4: 133. https://doi.org/10.2752/089279305785594153Google Scholar
Réale, D, Reader, SM, Sol, D, McDougall, PT and Dingemanse, NJ 2007 Integrating animal temperament within ecology and evolution. Biological Reviews 82: 291–318. https://doi.org/10.1111/j.1469-185X.2007.00010.xCrossRefGoogle ScholarPubMed
Reinhardt, V 1990 Avoiding undue stress: Catching individual ani-mals in groups of laboratory rhesus monkeys. Lab Animal 19: 52–53Google Scholar
Sánchez, S, Peláez, F, Gil-Bürmann, C and Kaumanns, W 1999 Costs of infant-carrying in the cotton-top tamarin (Saguinus oedipus). American Journal of Primatology 48: 99–111. https://doi.org/10.1002/(SICI)1098-2345(1999)48:2<99::AID-AJP2>3.0.CO;2-63.0.CO;2-6>CrossRefGoogle ScholarPubMed
Schapiro, SJ, Bloomsmith, MA and Laule, GE 2003 Positive reinforcement training as a technique to alter nonhuman primate behavior: quantitative assessments of effectiveness. Journal of Applied Animal Welfare Science 6: 175–187. https://doi.org/10.1207/S15327604JAWS0603_03CrossRefGoogle ScholarPubMed
Schapiro, SJ, Lambeth, SP, Jacobsen, KR, Williams, LE, Nehete, BN and Nehete, PN 2012 Physiological and welfare consequences of transport, relocation, and acclimatization of chimpanzees (P an troglodytes). Applied Animal Behaviour Science 137: 183–193. https://doi.org/10.1016/j.applanim.2011.11.004CrossRefGoogle Scholar
Schwartz, SM and Kemnitz, JW 1992 Age and gender related changes in body size, adiposity, and endocrine and metabolic parameters in free ranging rhesus macaques. American Journal of Physical Anthropology 89: 109–121. https://doi.org/10.1002/ajpa.1330890110CrossRefGoogle ScholarPubMed
Sherwin, CM, Christiansen, SB, Duncan, IJ, Erhard, HW, Lay, DC Jr, Mench, JA, O’Connor, CE and Petherick, JC 2003 Guidelines for the ethical use of animals in applied ethology studies. Applied Animal Behaviour Science 81: 291–305. https://doi.org/10.1016/S0168-1591(02)00288-5CrossRefGoogle Scholar
Suleman, MA, Wango, E, Sapolsky, RM, Odongo, H and Hau, J 2004 Physiologic manifestations of stress from capture and restraint of free-ranging male African green monkeys (Cercopithecus aethiops). Journal of Zoo and Wildlife Medicine 35: 20–24. https://doi.org/10.1638/01-025CrossRefGoogle ScholarPubMed
Terranova, CJ and Coffman, BS 1997 Body weights of wild and captive lemurs. Zoo Biology 16: 17–30. https://doi.org/10.1002/(SICI)1098-2361(1997)16:1<17::AID-ZOO4>3.0.CO;2-E3.0.CO;2-E>CrossRefGoogle Scholar
Turner, MJB, Gurney, P, Crowther, JSW and Sharp, JR 1984 An automatic weighing system for poultry. Journal of Agricultural Engineering Research 29: 17–24. https://doi.org/10.1016/0021-8634(84)90056-8CrossRefGoogle Scholar
Vernes, MK and Louwerse, AL 2010 BPRC's enrichment manual for macaques & marmosets. Biomedical Primate Research Center: Rijswijk, The NetherlandsGoogle Scholar
Vézina, F, Charlebois, D and Thomas, DW 2001 An automated system for the measurement of mass and identification of birds at perches. Journal of Field Ornithology 72: 211–220. https://doi.org/10.1648/0273-8570-72.2.211CrossRefGoogle Scholar
Wergård, EM, Westlund, K, Spångberg, M, Fredlund, H and Forkman, B 2016 Training success in group-housed long-tailed macaques (Macaca fascicularis) is better explained by personality than by social rank. Applied Animal Behaviour Science 177: 52–58. https://doi.org/10.1016/j.applanim.2016.01.017CrossRefGoogle Scholar
Zhang, P, Lyu, MY, Wu, CF, Chu, YMR, Han, N, Yang, D and Hu, K 2016 Variation in body mass and morphological charac-ters in Macaca mulatta brevicaudus from Hainan, China. American Journal of Primatology 78: 679–698. https://doi.org/10.1002/ajp.22534CrossRefGoogle ScholarPubMed
Supplementary material: File

Zijlmans et al. supplementary material
Download undefined(File)
File 64.3 KB