Introduction to animal training techniques

One of the major improvements in how we care for captive primates has been refining animal training methods used to manage and care for the primates. Positive reinforcement training techniques have been developed to promote animal welfare, to assist in animal husbandry and veterinary care, and in some cases, to improve the quality of research conducted with the primates. When positive reinforcement methods are used, animals are taught to voluntarily cooperate with procedures rather than relying on coercion to get their participation.

Captive primates have been trained to perform a wide variety of behaviors including: moving when asked into transfer boxes or from one enclosure to another; allowing careful examination of parts of their bodies such as opening their mouths or positioning hands, feet, chest, back, etc. for visual inspection; positioning ears for examination or for using a tympanic thermometer; tolerating the use of a stethoscope to listen to the heart or lungs; having their wounds closely examined and treated with topical medications; receiving injections for anesthesia, antibiotics, or vaccinations; and cooperating with veterinary procedures such as x-rays or blood pressure measurement. Many different biological samples can be collected from cooperating primates, and they can be used either for veterinary care of the primates, or for research studies. Samples that have been collected include: urine, feces, blood, semen, vaginal fluid, and nasal samples. Positive reinforcement training can also be used to reduce aggression and competition within groups of primates, and it can decrease fear or decrease abnormal behavior in some situations. Clearly, primates can be taught a huge range of very useful behaviors that can improve their lives.

There is a growing body of scientific literature that assesses various aspects of animal training including training technique, required training time to achieve certain behaviors, behavioral impacts of the training, and physiological consequences of the training. This literature offers objective information about the value and the limitations of training. These studies should be carefully reviewed by those who are trying to discern the value of positive reinforcement training for their own primate management programs. This list of science-based references and articles about a variety of animal training topics may help you begin that process.

There are a variety of workshops and certification courses that focus on animal training techniques. These workshops and courses are not endorsed by the American Society of Primatologists, but they may be useful to those trying to learn more about training.

Desensitization/Habituation

Clay A, Bloomsmith MA, Marr MJ, Maple TJ. 2009. Habituation and desensitization as methods for reducing fearful behavior in singly housed rhesus macaques. American Journal of Primatology 71:30-39.

Wilson GT, Davison GC. 1971. Processes of fear reduction in systematic desensitization: Animal studies. Psychology Bulletin 76:1-14.

Training and Abnormal Behavior

Baker K, Bloomsmith MA, Neu K, Griffis C, Maloney M, Oettinger B, Schoof V, Martinez M. 2009. Positive reinforcement training moderates only high levels of abnormal behavior in singly-housed rhesus macaques. Journal of Applied Animal Welfare Science 12:236-252.

Bloomsmith MA, Marr MJ, Maple TL. 2007. Addressing nonhuman primate behavioral problems through the application of operant conditioning: Is the human treatment approach a useful model? Applied Animal Behaviour Science 102:205-222.

Bourgeois SR, Vazquez M, Brasky K. 2007. Combination therapy reduces self-injurious behavior in a chimpanzee (Pan troglodytes troglodytes): A case report. Journal of Applied Animal Welfare Science 10:123-140.

Dorey NR, Rosales-Ruiz J, Smith R, Lovelace B. 2009. Functional analysis and treatment of self-injury in a captive olive baboon. Journal of Applied Behaviour Analysis 42:785-794.

Leeds A, Elsner R, Lukas KE, 2016. The effect of positive reinforcement training on an adult female western lowland gorilla’s (Gorilla gorilla gorilla) rate of abnormal and aggressive behavior. Animal Behavior and Cognition 3:78-87.

Martin AL, Bloomsmith MA, Keeley ME, Marr MJ, Maple TL. 2011. Functional analysis and treatment of human-directed undesirable behavior exhibited by a captive chimpanzee. Journal of Applied Behaviour Analysis 44:139-143.

Mason G. 1999. Stereotypies: a critical review. Animal Behaviour. 41:1015-1037.

Morgan L, Howell SM, Fritz J. 1993. Regurgitation and reingestion in a captive chimpanzee (Pan troglodytes). Lab Animal 22:42-45.Whittaker M. 2005. Applied problem solving to diminish abnormal behavior. In: Proceedings of the Seventh International Conference on Environmental Enrichment. New York, pp. 126-131.

Whittaker M. 2005. Applied problem solving to diminish abnormal behavior. In: Proceedings of the Seventh International Conference on Environmental Enrichment. New York, pp. 126-131.

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Training for Medical Care

Gresswell C, Goodman G. 2011. Case study: Training a chimpanzee (Pan troglodytes) to use a nebulizer to aid the treatment of air sacculitis. Zoo Biology 30:570-578.

Magden ER. 2017. Positive reinforcement training and health care. In: Schapiro, SJ (ed) Handbook of Primate Behavioral Management. CRC Press, Boca Raton, pp. 201-213.

Magden, ER, Haller, RL, Thiele, EJ, Buchl, SJ, Lambeth, SP, Schapiro SJ. 2013. Acupuncture as an adjunct therapy for osteoarthritis in chimpanzees. Journal of the American Association for Laboratory Animal Science 52:475-480.

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Training for Present for Injection

Schapiro SJ, Perlman JE, Thiele E, Lambeth SP. 2005. Training nonhuman primates to perform behaviors useful in biomedical research. Lab Animal 34:37-42.

Vertein R, Reinhardt V. 1989. Training female rhesus monkeys to cooperate during in-homecage venipuncture. Laboratory Primate Newsletter 28:1-3.

Videan EN, Fritz J, Murphy J, Borman R, Smith HF, Howell S. 2005. Training captive chimpanzees to cooperate for an anesthetic injection. Lab Animal 34:43-48.

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Training for Sample Collection

Bloomsmith MA, Neu K, Franklin A, Griffis C, McMillan J. 2015. Positive reinforcement methods to train chimpanzees to cooperate with urine collection. Journal of the American Association for Laboratory Animal Science 54:66-69.

Coleman KL, Pranger L, Maier A, Lambeth SP, Perlman JE, Thiele E, Schapiro SJ. 2008. Training rhesus macaques for venipuncture using positive reinforcement training techniques: A comparison with chimpanzees. Journal of the American Association of Laboratory Animal Science 47:37-41.

Houser LA, Ramsey C, de Carvalho FM, Kolwitz B, Naito C, Coleman K, Hanna CB. 2021. Improved training and semen collection outcomes using the closed box chair for macaques. Animals 11:2384. 

Kelley TM, Bramblett CA. 1981. Urine collection from vervet monkeys by instrumental conditioning. American Journal of Primatology 1:95-97.

Laule GE, Thurston RH, Alford PL, Bloomsmith MA. 1996. Training to reliably obtain blood and urine samples from a young diabetic chimpanzee (Pan troglodytes). Zoo Biology 15:587-591.

Reinhardt V. 2003. Working with rather than against macaques during blood collection. Journal of Applied Animal Welfare Science 6:189-197.

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Physiological Impacts of Training

Hanson JD, Larson ME, Snowdon CT. 1976. The effects of control over high intensity noise on plasma cortisol levels in rhesus monkeys. Behavioral Biology 16:333-340.

Lambeth SP, Hau J, Perlman JE, Martino M, Schapiro SJ. 2006. Positive reinforcement training affects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes). American Journal of Primatology 68:245-256.

Reinhardt V, Cowley D, Scheffler J, Vertein R, Wegner F. 1990. Cortisol response of female rhesus monkeys to venipuncture in homecage versus venipuncture in restraint apparatus. Journal of Medical Primatology 19:601-606.

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Training and Socialization

Cox C. 1987. Increase in the frequency of social interactions and the likelihood of reproduction among drills. In: Proceedings of the American Association of Zoological Parks and Aquariums [AAZPA] Western Regional Conference. Wheeling, WV, pp. 321-328.

Desmond T, Laule G, McNary J. 1987. Training to enhance socialization and reproduction in drills. In: Proceedings of the American Association of Zoological Parks and Aquariums [AAZPA] Western Regional Conference. Wheeling, WV, pp. 435-441.

Schapiro SJ, Perlman JE, Boudreau B. 2001. Manipulating the affiliative interactions of group-housed rhesus macaques using positive reinforcement training techniques. American Journal of Primatology 55:137-149.

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Training for Enrichment

Baker KC, Bloomsmith MA, Neu K, Griffis C, Maloney M. 2010. Positive reinforcement training as enrichment for singly housed rhesus macaques (Macaca mulatta). Animal Welfare 19:307-313.

Bourgeois SR, Brent L. 2005. Modifying the behaviour of singly caged baboons: evaluating the effectiveness of four enrichment techniques. Animal Welfare 14:71-81.

Laule G, Desmond T. 1998. Positive reinforcement training as an enrichment strategy, in: Sheperdson, D.J., Mellen, J.D., Hutchins, M. (Eds.), Second Nature: Environmental Enrichment for Captive Animals. Smithsonian Inst. Press, Washington, D.C., pp. 302-313.

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Training to Reduce Aggression

Bloomsmith MA, Laule GE, Alford PL, Thurston RH. 1994. Using training to moderate chimpanzee aggression during feeding. Zoo Biology 13:557-566.

Minier DE, Tatum L, Gottlieb DH, Cameron A, McCowan B. 2011. Human-directed contra-aggression training using positive reinforcement with single and multiple trainers for indoor-housed rhesus macaques. Journal of Applied Animal Behaviour Science 132:178-186.

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Training for Movement

Bloomsmith MA, Stone AM, Laule GE. 1998. Positive reinforcement training to enhance the voluntary movement of group-housed chimpanzees. Zoo Biology 17:333-341.

Veeder CL, Bloomsmith MA, McMillan JL, Perlman JE, Martin AL. 2009. Positive reinforcement training to enhance the voluntary movement of group-housed sooty mangabeys (Cercocebus atys atys). Journal of the American Association of Laboratory Animal Science 48:192-195.

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Training for Restraint

Bliss-Moreau E, Moadab G. 2016. Variation in behavioral reactivity is associated with cooperative restraint training efficiency. Journal of the American Association for Laboratory Animal Science 55:41-49.

McMillan JL, Bloomsmith MA, Prescott MJ. 2017. An international survey of approaches to chair restraint of nonhuman primates. Comparative Medicine 67:442–451.

McMillan JL, Perlman JE, Galvan A, Wichmann T, Bloomsmith MA. 2014. Method of restraint: Emphasizing the use of positive training techniques with rhesus macaques (Macaca mulatta). Journal of the American Association for Laboratory Animal Science 53:61-68.

Moseley JR, Davis JA. 1989. Psychological enrichment techniques and New World monkey restraint device reduce colony management time. Lab Animal 18:31-33.

Reinhardt V. 1997. Training nonhuman primates to cooperate during handling procedures: A review. Animal Technology 48:55-73.

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Training and Welfare

Chelluri GI, Ross SR, Wagner KE. 2013. Behavioral correlates and welfare implications of informal interactions between caretakers and zoo-housed chimpanzees and gorillas. Journal of Applied Animal Welfare Science 147:306-315.

Fernandez EJ, Martin AL. 2021. Animal training, environmental enrichment, and animal welfare: A history of behavior analysis in zoos. Journal of Zoological and Botanical Gardens 2:531-543.

Franklin AN, Martin AL, Perlman JE, Bloomsmith MA. 2021. Functional analysis and successful treatment of a captive rhesus macaque’s disruptive behavior. Journal of Applied Animal Welfare Science 1-10.

Laule GE, Whittaker MA. 2001. The use of positive reinforcement techniques with chimpanzees for enhanced care and welfare. In: Brent L. (ed) Care and management of captive chimpanzees. American Society of Primatologists, Texas, pp. 243-265.

Laule GE, Whittaker MA. 2007. Enhancing nonhuman primate care and welfare through the use of positive reinforcement training. Journal of Applied Animal Welfare Science 10 (1):31-38.

Pomerantz O, Terkel J. 2009. Effects of positive reinforcement techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). American Journal of Primatology 71:687-695.

Spiezio C, Vaglio S, Scala C, Regaiolli B. 2017. Does positive reinforcement training affect the behaviour and welfare of zoo animals? The case of the ring-tailed lemur (Lemur catta). Applied Animal Behaviour Science 196:91–99.

Westlund K. 2015. Training laboratory primates – benefits and techniques. Primate Biology 2:119-132.

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Improving Training Efficiency and Safety

Clay AW, Bloomsmith MA, Marr MJ, Maple TL. 2009. Systematic investigation of the stability of food preferences in captive orangutans: implication for positive reinforcement training. Journal Applied Animal Welfare Science 12:306-313.

Coleman K, Tully LA, McMillan JL. 2005. Temperament correlates with training success in adult rhesus macaques. American Journal of Primatology 65:63-71.

Fernstrom AL, Fredlund H, Spangberg M, Westlund K. 2009. Positive reinforcement training in rhesus macaques – training progress as a result of training frequency. American Journal of Primatology 71:373-379.

Hotchkiss CE, Young MA. 2020. Comparative risk of human injury/exposure while collecting blood from sedated and unsedated nonhuman primates. Journal for the American Association for Laboratory Animal Science 59:371-376.

Martin, AL, Franklin, AN, Perlman, JE, Bloomsmith MA. 2018. Systematic assessment of food item preference and reinforcer effectiveness: Enhancements in training laboratory-housed rhesus macaques. Behavioural Processes 157:445-452.

Rogge J, Sherenco K, Malling R, Thiele E, Lambeth S, Schapiro S, Williams L. 2013. A comparison of positive reinforcement training techniques in owl and squirrel monkeys: Time required to train to reliability. Journal of Applied Animal Welfare Science 16:211-220.

Wergard EM, Temrin H, Forkman B, Spanberg M, Fredlund H, Westlund K. 2016. Training pair-housed rhesus macaques (Macaca mulatta) using a combination of negative and positive reinforcement. Behavioural Processes 113:51-59.

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Training Program Information

Colahan H, Breder C. 2003. Primate Training at Disney’s Animal Kingdom. Journal of Applied Animal Welfare Science 6:235-246.

Mackie, J. 2020. The application of positive reinforcement training to enhance welfare of primates in zoological collections. In Melfi, VA, Dorey, NR & Ward, SJ. (eds) Zoo Animal Learning and Training pp. 211-215.

Perlman JE, Bloomsmith MA, Whittaker MA, McMillan JL, Minier DE, McCowan B. 2012. Implementing positive reinforcement animal training programs at primate laboratories. Applied Animal Behaviour Science 137:114-126.

Prescott MJ, Bowell VA, Buchanan-Smith HM. 2005. Training of laboratory-housed non-human primates, part 2: Resources for developing and implementing training programmes. Animal Technology and Welfare 4:133-148.

Prescott MJ, Buchanan-Smith HM. 2007. Training laboratory-housed non-human primates, part I: a UK survey. Animal Welfare 16:21-36.

Ramirez K. 1999. Animal Training: Successful Animal Management through Positive Reinforcement. Shedd Aquarium, Illinois.

Whittaker M, Perlman J, Laule G. 2008. Facing real world challenges: Keeping behavioral management programs alive and well. In Hare, HJ, Kroshko JE (eds), Proceedings of the Eighth International Conference on Environmental Enrichment, Vienna, Austria. The Shape of Enrichment. San Diego, USA, pp. 87-89.

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Training and Husbandry

Joint Working Group on Refinement. 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 (M Jennings & MJ Prescott, eds). Lab Animal 43 S1:1-S1:47

Laule G, Desmond T. 1990. Use of positive behavioral techniques in primates for husbandry and handling. Proceedings, American Association of Zoo Veterinarians Annual Conference, pp. 269-273.

McKinley J, Buchanan-Smith HM, Bassett L, Morris K. 2003. Training common marmosets (Callithrix jacchus) to cooperate during routine laboratory procedures: Ease of training and time investment. Journal of Applied Animal Welfare Science 6:209-220.

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Regulations

National Research Council, 2011. Guide for the Care and Use of Laboratory Animals, Eighth ed. National Academies Press, Washington, D.C.

OLAW Report on Site Visits to Chimpanzee Facilities and Associated Resources to Aid Grantee Institutions, July 2010. NOT-OD-10-121. National Institutes of Health, Maryland.

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Social Learning

Perlman JE, Horner V, Bloomsmith MA, Lambeth SP, Schapiro SJ. 2010. Positive reinforcement training, social learning, and chimpanzee welfare, in: Lonsdorf EV, Ross SR, Matsuzawa, T. (eds.), The Mind of the Chimpanzee: Ecological and Experimental Perspectives. University of Chicago Press, Chicago, IL. pp. 320-331.

Young RJ, Cipreste CF. 2004. Applying animal learning theory: training captive animals to comply with veterinary and husbandry procedures. Animal Welfare 13:225-232.

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Training for Testing and Research

Bloomsmith MA, Perlman JE, Franklin AF, Martin MA. In press. Training Research Primates. In Robinson LM, Weiss A. (eds) Nonhuman Primate Welfare: From History, Science, and Ethics to Practice. Springer.

Brando S, Basom L, Bashaw M, Druyor C, Fonte E, Thompson R. 2021. Individualized target training facilitated transfer of group housed capuchin monkeys (Sapajus apella) to test cubicles and discrimination of targets on computer touch screens. Animals 11: 2070.

Gillis TE, Janes AC, Kaufman MJ. 2012. Positive reinforcement training in squirrel monkeys using clicker training. American Journal of Primatology 74:712-720.

Graham ML. 2017. Positive reinforcement training and research. In: Schapiro SJ. (ed) Handbook of Primate Behavioral Management. CRC Press, Boca Raton, pp 189-197.

Graham ML, Rieke EF, Mutch LA, Zolondek EK, Faig AW, DuFour TA, Munson JW, Kittredge JA, Schuurman HJ. 2012. Successful implementation of cooperative handling eliminates the need for restraint in a complex non-human primate disease model. Journal of Medical Primatology 41:89-106.

Kemp C, Thatcher H, Farningham D, Whitham C, MacLarnon A, Holmes A, Semple S, Bethell, EJ. 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.

Tulip J, Zimmerman JB, Farningham D, Jackson A. 2017. An automated system for positive reinforcement training of group-housed macaque monkeys at breeding and research facilities. Journal of Neuroscience Methods 285:6-18.

Westlund K. 2012. Can conditioned reinforcers and variable-ratio schedules make food and fluid control redundant? A comment on the NC3Rs working group’s report. Journal of Neuroscience Methods 204:202-205.

Washburn DA, Hopkins WD, Rumbaugh DM. 1991. Perceived control in rhesus monkeys (Macaca mulatta): Enhanced video-task performance. Journal of Experimental Psychology: Animal Behavior Processes 17:123-129.

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Other Training Resources

Kazdin AE. 2001. Behavior Modification in Applied Settings, Sixth Ed. Wadsworth, California.

Pryor K. 2002. Don’t shoot the dog! The new art of teaching and training. Ringpress Books Ltd. Great Britain.