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Positive reinforcement training: a tool for care and management of captive vervet monkeys (Chlorocebus aethiops)

Published online by Cambridge University Press:  03 January 2023

C Spiezio ,
F Piva ,
B Regaiolli  and
S Vaglio
C Spiezio
Affiliation:
Settore Ricerca & Conservazione, Parco Natura Viva-Garda Zoological Park, Località Figara 40, 37012 Bussolengo (VR), Italy
F Piva
Affiliation:
Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università degli Studi di Torino, Via Accademia Albertina 13, 10123 Torino, Italy
B Regaiolli
Affiliation:
Settore Ricerca & Conservazione, Parco Natura Viva-Garda Zoological Park, Località Figara 40, 37012 Bussolengo (VR), Italy
S Vaglio*
Affiliation:
Settore Ricerca & Conservazione, Parco Natura Viva-Garda Zoological Park, Località Figara 40, 37012 Bussolengo (VR), Italy Department of Anthropology & Behaviour, Ecology and Evolution Research Centre, Durham University, South Road, Durham DH1 3LE, UK
*
* Contact for correspondence and requests for reprints: stefano.vaglio@durham.ac.uk
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Abstract

In modern zoos, training should be an integral component of the animal care and management. The benefits of training include the opportunity for positive interactions with caretakers. This study was carried out with a group of vervet monkeys (Chlorocebus aethiops) housed at the Garda Zoological Park, Italy. Using focal animal sampling, we observed the behaviour performed by all group members from December 2007 to August 2008. The group took part in a training programme to be isolated in a familiar area before the subjects were included in a cognitive study. We collected behavioural data during a pre-training period to assess the social behaviour of the colony and during the training period to investigate the effects of the training programme on the behaviour of individuals. Additionally, a second phase of the study was conducted and training sessions with individual monkeys were video-recorded to determine the behaviour of animals during each training session and to thus confirm that they were suitable for participating in the procedure. Our results suggest that the training programme enriched the daily routine of these captive primates by increasing affiliative behaviours while decreasing agonistic behaviours. Furthermore, there was behavioural response variability among the individuals under the training procedure. However, all the individuals were trained to calmly enter a familiar area and be isolated from other members of the group. In conclusion, our findings highlight the importance of using positive reinforcement training to reduce the tension directly associated with potentially stressful procedures by allowing primates to participate voluntarily in these procedures. In addition, the training was found to be an enrichment tool for vervet monkeys.

Keywords

animal welfarecaptivityenrichment toolhusbandry refinementoperational conditioningstress
Type
Research Article
Information
Animal Welfare , Volume 24 , Issue 3 , August 2015 , pp. 283 - 290
Copyright
© 2015 Universities Federation for Animal Welfare

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References

Adeyemo, AI 1997 Diurnal activities of green monkeys Cercopithecus aethiops in Old Oyo National Park, Nigeria. South African Journal of Wildlife Research 27: 24–26Google Scholar
Altmann, J 1974 Observational study of behavior: Sampling methods. Behaviour 49: 227–266. http://dx.doi.org/10.1163/156853974X00534CrossRefGoogle ScholarPubMed
Barros, M, de Souza-Silva, MA, Huston, J and Tomaz, C 2004 Multibehavioural analysis of fear and anxiety before, during, and after experimentally induced predatory stress in Callithrix peni-cillata. Pharmacology, Biochemistry and Behavior 78: 357–367. http://dx.doi.org/10.1016/j.pbb.2004.04.008CrossRefGoogle Scholar
Bassett, L, Buchanan-Smith, HM, McKinley, J and Smith, TE 2003 Effects of training on stress-related behaviour of the common marmoset (Callithrix jacchus) in relation to coping with routine husbandry procedures. Journal of Applied Animal Welfare Science 6:221–223. http://dx.doi.org/10.1207/S15327604JAWS0603_07CrossRefGoogle ScholarPubMed
Box, HO and Rohrhuber, B 1993 Differences in behaviour among adult male, female pairs of cotton-top tamarins (Saguinus oedipus) in different conditions of housing. Animal Technology 44: 19 -30Google Scholar
Carlstead, K 2009 A comparative approach to the study of keeper-animal relationships in the zoo. Zoo Biology 28: 589–608. http://dx.doi.org/10.1002/zoo.20289Google Scholar
Chamove, AS, Hosey, J and Schaetzel, P 1988 Visitors excite primates in zoos. Zoo Biology 7: 359–369. http://dx.doi.org/10.1002/zoo.1430070407CrossRefGoogle Scholar
Cheney, DL and Seyfarth, RM 1990 How monkeys see the world: Inside the mind of another species. University of Chicago Press: Chicago, USA10.7208/chicago/9780226218526.001.0001CrossRefGoogle Scholar
Colahan, H and Breder, C 2003 Primate training at Disney's Animal Kingdom. Journal of Applied Animal Welfare Science 6: 235–246. http://dx.doi.org/10.1207/S15327604JAWS0603_08CrossRefGoogle ScholarPubMed
Crowell-Davis, SL 2008 Use of operant conditioning to facilitate examination of zoo animals. Compendium, Continuing Education for Veterinarians 30: 218–236Google ScholarPubMed
Desmond, T and Laule, G 1994 Use of positive reinforcement training in the management of species for reproduction. Zoo Biology 13: 471–477. http://dx.doi.org/10.1002/zoo.1430130509CrossRefGoogle Scholar
Fedigan, L 1972 Social and solitary play in a colony of vervet monkeys Cercopithecus aethiops. Primates 13: 347–364. http://dx.doi.org/10.1007/BF01793655CrossRefGoogle Scholar
Fedigan, L and Fedigan, LM 1988 Cercopithecus aethiops: A review of field studies. In: Gautier-Hion, A, Bourlière, F, Gautier, JP and Kingdon, J (eds) A Primate Radiation: Evolutionary Biology of the African Guenons pp 389–411. Cambridge University Press: Cambridge, UKGoogle Scholar
Fontani, S, Vaglio, S, Beghelli, V, Mattioli, M, Bacci, S and Accorsi, PA 2014 Fecal concentrations of cortisol, testosterone, and progesterone in cotton-top tamarins housed in different zoological parks: relationships among physiological data, environ-mental conditions, and behavioral patterns. Journal of Applied Animal Welfare Science 17: 228–252. http://dx.doi.org/10.1080/10888705.2014.916173CrossRefGoogle Scholar
Fuller, G, Kuhar, CW, Dennis, PM and Lukas, KE 2013 A survey of husbandry practices for Lorisid primates in North American zoos and related facilities. Zoo Biology 32: 88–100. http://dx.doi.org/10.1002/zoo.21049CrossRefGoogle ScholarPubMed
Hosey, GR and Druck, PL 1987 The influence of zoo visitors on the behaviour of captive primates. Applied Animal Behaviour Science 18: 19–29. http://dx.doi.org/10.1016/0168-1591(87)90251-6CrossRefGoogle Scholar
Kessel, A and Brent, L 2001 The rehabilitation of captive baboons. Journal of Medical Primatology 30: 71–80. http://dx.doi.org/10.1034/j.1600-0684.2001.300201.xCrossRefGoogle ScholarPubMed
Laule, G and Whittaker, M 2007 Enhancing nonhuman primate care and welfare through the use of positive reinforcement training. Journal of Applied Animal Welfare Science 10: 163–173. http://dx.doi.org/10.1080/10888700701277311CrossRefGoogle ScholarPubMed
Laule, GE 1993 The use of behavioural management techniques to reduce or eliminate abnormal behaviour. Animal Welfare Information Center Bulletin 4: 1–11Google Scholar
Laule, GE 2003 Positive reinforcement training and environ-mental enrichment: Enhancing animal well-being. Journal of the American Veterinary Medical Association 223: 969–973. http://dx.doi.org/10.2460/javma.2003.223.969CrossRefGoogle Scholar
Laule, GE, Bloomsmith, MA and Schapiro, SJ 2003 The use of positive reinforcement training techniques to enhance the care, management, and welfare of primates in the laboratory. Journal of Applied Animal Welfare Science 6: 163–173. http://dx.doi.org/10.1207/S15327604JAWS0603_02CrossRefGoogle ScholarPubMed
Laule, GE and Desmond, T 1998 Positive reinforcement training as an enrichment strategy. In: Shepherdson, DJ, Mellen, JD and Hutchins, M (eds) Second Nature: Environmental Enrichment for Captive Animals pp 302–313. Smithsonian Institution Press: Washington DC, USAGoogle Scholar
Luttrell, L, Acker, L, Urben, M and Reinhardt, V 1994 Training a large troop of rhesus macaques to co-operate during catching: analysis of the time investment. Animal Welfare 3: 135–140Google Scholar
Maestripieri, D, Martel, FL, Nevison, CM, Simpson, MJ and Keverne, EB 1991 Anxiety in rhesus monkey infants in relation to interactions with their mother and other social companions. Developmental Psychobiology 24: 571–581. http://dx.doi.org/10.1002/dev.420240805CrossRefGoogle ScholarPubMed
Mattison, S 2012 Training birds and small mammals for medical behaviors. The Veterinary Clinics of North America. Exotic Animal Practice 15: 487–499. http://dx.doi.org/10.1016/j.cvex.2012.06.012CrossRefGoogle ScholarPubMed
Melfi, V 2013 Is training zoo animals enriching? Applied Animal Behaviour Science 147: 299–305. http://dx.doi.org/10.1016/j.applanim.2013.04.011CrossRefGoogle Scholar
Melfi, V and Thomas, S 2012 Can training zoo-housed primates compromise their conservation? A case study using Abyssinian colobus monkeys (Colobus guereza). Anthrozoös: A Multidisciplinary Journal of The Interactions of People & Animals 18: 304–31710.2752/089279305785594063CrossRefGoogle Scholar
Mellen, JD and MacPhee, MS 2001 Philosophy of environ-mental enrichment: past, present, and future. Zoo Biology 20: 211–226. http://dx.doi.org/10.1002/zoo.1021CrossRefGoogle Scholar
Mitchell, G, Tromborg, C, Kaufman, J, Bargabus, S, Simoni, R and Geissler, V 1992 More on the ‘influence’ of zoo visitors on the behaviour of captive primates. Applied Animal Behaviour Science 35: 189–198. http://dx.doi.org/10.1016/0168-1591(92)90009-ZCrossRefGoogle Scholar
Owen, Y and Amory, JR 2011 A case study employing operant conditioning to reduce stress of capture for red-bellied tamarins (Saguinus labiatus). Journal of Applied Animal Welfare Science 14:124–137. http://dx.doi.org/10.1080/10888705.2011.551625CrossRefGoogle ScholarPubMed
Peel, AJ, Vogelnest, L, Finnigan, M, Grossfeldt, L and O’Brien, JK 2005 Non-invasive fecal hormone analysis and behavioural observations for monitoring stress responses in captive Western lowland gorillas (Gorilla gorilla gorilla). Zoo Biology 24: 431–445. http://dx.doi.org/10.1002/zoo.20055CrossRefGoogle Scholar
Pomerantz, O and Terkel, J 2009 Effects of positive reinforce-ment training techniques on the psychological welfare of zoo-housed chimapanzees (Pan troglodytes). American Journal of Primatology 71: 687–695. http://dx.doi.org/10.1002/ajp.20703CrossRefGoogle Scholar
Prescott, MJ and Buchanan-Smith, HM 2003 Training nonhuman primates using positive reinforcement techniques. Journal of Applied Animal Welfare Science 6: 157–161. http://dx.doi.org/10.1207/S15327604JAWS0603_01CrossRefGoogle ScholarPubMed
Schmidt, M 2010 Locomotion and postural behavior. Advances in Science & Research 5: 23–39. http://dx.doi.org/10.5194/asr-5-23-2010CrossRefGoogle Scholar
Schoenfeld, D 1989 Effects of environmental impoverishment on the social behavior of marmosets (Callithrix jacchus). American Journal of Primatology (S1): 45-51Google Scholar
Shapiro, SJ, Bloomsmith, MA and Laule, GE 2003 Positive reinforcement training as a technique to alter non-human primate behaviour: Quantitative assessments of effectiveness. Journal of Applied Animal Welfare Science 6: 175–189. http://dx.doi.org/10.1207/S15327604JAWS0603_03CrossRefGoogle Scholar
Siegel, S and Castellan, NJ 1988 Non Parametric Statistics for the Behavioural Sciences, Second Edition. MacGraw-Hill: London, UKGoogle Scholar
Skinner, BF 1981 Selection by consequence. Science 213: 501–504. http://dx.doi.org/10.1126/science.7244649CrossRefGoogle Scholar
Thorndike, EL 1911 Animal Intelligence. Macmillan: New York, USAGoogle Scholar
Whitehouse, J, Micheletta, J, Powell, LE, Bordier, C and Waller, BM 2013 The impact of cognitive testing on the welfare of group housed primates. PLoS One 8: e78308. http://dx.doi.org/10.1371/journal.pone.0078308CrossRefGoogle ScholarPubMed
Veeder, CL, Bloomsmith, MA, McMillan, JL, Perlman, JE and Martin, AL 2009 Positive reinforcement training to enhance the voluntary movement of group-housed sooty mangabeys (Cercocebus atys atys). Journal of the American Association for Laboratory Animal Science 48: 192–195Google ScholarPubMed