Hostname: page-component-7b7567c8c-2n9c9 Total loading time: 0 Render date: 2026-11-15T16:17:49.618Z Has data issue: false hasContentIssue false
  • English
  • Français

Training as enrichment: A critical review

Part of:Zoo Animals Collection

Published online by Cambridge University Press:  01 January 2023

EJ FernandezOpen the ORCID record for EJ Fernandez[Opens in a new window]
EJ Fernandez*
Affiliation:
School of Animal and Veterinary Sciences, University of Adelaide, Adelaide, SA 5005, Australia
*
email; edjfern@gmail.com
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.

Husbandry training and environmental enrichment are both important advancements associated with current behavioural welfare practices. Additionally, the use of training procedures has been proposed as a form of enrichment, with the implication that training can produce beneficial behavioural welfare results. This paper examines the concept of training as enrichment through three distinct ways training procedures could enrich: (i) training facilitates enrichment usage; (ii) training modifies interactions, conspecific or otherwise; and (iii) training expands behavioural repertoires. Within each category, the paper focuses on past research that provides empirical support for training functioning as enrichment, as well as related areas of research that provide additional evidence. Previous studies support the claim that training is enriching, with additional research necessary to better understand how prevalent and under what conditions training procedures function as enrichment. Future training research should examine these potential enrichment effects, including methodology that allows for comparisons to traditional enrichment, the use of welfare diversity/variability indices, and the effects of learning on trainers and trainees alike.

Keywords

animal welfareenrichmenthusbandrylearningpositive reinforcementtraining

Information

Type
Research Article
Information
Animal Welfare , Volume 31 , Issue 1 , February 2022, pp. 1 - 12
Copyright
© 2022 Universities Federation for Animal Welfare

References

Alligood, CA, Dorey, NR, Mehrkam, LR and Leighty, KA 2017 Applying behavior-analytic methodology to the science and practice of environmental enrichment in zoos and aquariums. Zoo Biology 36: 175–185. https://doi.org/10.1002/zoo.21368CrossRefGoogle Scholar
Anderson, US, Kelling, AS, Pressley-Keough, R, Bloomsmith, MA and Maple, TL 2003 Enhancing the zoo visitor's experience by public animal training and oral interpretation at an otter exhib-it. Environment and Behavior 35: 826–841. https://doi.org/10.1177/0013916503254746CrossRefGoogle Scholar
Andrews, NL and Ha, JC 2014 The effects of automated scatter feeders on captive grizzly bear activity budgets. Journal of Applied Animal Welfare Science 17: 148–156. https://doi.org/10.1080/10888705.2013.856767Google ScholarPubMed
Association of Zoos and Aquariums 2020 Animal care manu-als. https://www.aza.org/animal-care-manualsGoogle Scholar
Bailey, JS and Burch, MR 2017 Research Methods in Applied Behavior Analysis. Routledge: Oxon, UK. https://doi.org/10.4324/9781315543369CrossRefGoogle Scholar
Bailey, RE and Gillaspy, JA 2005 Operant psychology goes to the fair: Marian and Keller Breland in the popular press, 1947–1966. The Behavior Analyst 28: 143–159. https://doi.org/10.1007/BF03392110CrossRefGoogle Scholar
Baker, KC, Bloomsmith, M, Neu, K, Griffis, C, Maloney, M, Oettinger, B, Schoof, VAM and 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. https://doi.org/10.1080/10888700902956011CrossRefGoogle ScholarPubMed
Bashaw, MJ, Gibson, MD, Schowe, DM and Kucher, AS 2016 Does enrichment improve reptile welfare? Leopard geckos (Eublepharis macularius) respond to five types of environmental enrichment. Applied Animal Behaviour Science 184: 150–160. https://doi.org/10.1016/j.applanim.2016.08.003CrossRefGoogle Scholar
Bassett, L, Buchanan-Smith, HM, McKinley, J and Smith, TE 2003 Effects of training on stress-related behavior of the common marmoset (Callithrix jacchus) in relation to coping with routine husbandry procedures. Journal of Applied Animal Welfare Science 6: 221–233. https://doi.org/10.1207/S15327604JAWS0603_07CrossRefGoogle ScholarPubMed
Batt, L, Batt, M, Baguley, J and McGreevy, P 2008 The effects of structured sessions for juvenile training and socialization on guide dog success and puppy-raiser participation. Journal of Veterinary Behavior 3: 199–206. https://doi.org/10.1016/j.jveb.2008.05.001CrossRefGoogle Scholar
Bender, A and Strong, E 2019 Canine Enrichment for the Real World. Dogwise Publishing: Wenatchee, WA, USAGoogle Scholar
Bihm, EM, Gillaspy, JA, Lammers, WJ and Huffman, SP 2010 IQ Zoo and teaching operant concepts. The Psychological Record 60: 523–526. https://doi.org/10.1007/BF03395725CrossRefGoogle Scholar
Bitgood, S and Patterson, D 1987 Principles of exhibit design. Visitor Behavior 2: 4–6. https://doi.org/10.1177/0013916588204006Google Scholar
Blackwell, EJ, Twells, C, Seawright, A and Casey, RA 2008 The relationship between training methods and the occurrence of behavior problems, as reported by owners, in a population of domestic dogs. Journal of Veterinary Behavior 3: 207–217. https://doi.org/10.1016/j.jveb.2007.10.008CrossRefGoogle Scholar
Bloomsmith, MA, Laule, GE, Alford, PL and Thurston, RH 1994 Using training to moderate chimpanzee aggression during feeding. Zoo Biology 13: 557–566. https://doi.org/10.1002/zoo.1430130605CrossRefGoogle Scholar
Bloomsmith, MA, Marr, MJ and 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. https://doi.org/10.1016/j.applanim.2006.05.028CrossRefGoogle Scholar
Bloomsmith, MA, Stone, AM and Laule, GE 1998 Positive reinforcement training to enhance the voluntary movement of group-housed chimpanzees within their enclosures. Zoo Biology 17: 333–341. https://doi.org/10.1002/(SICI)1098-2361(1998)17:4<333::AID-ZOO6>3.0.CO;2-A3.0.CO;2-A>CrossRefGoogle Scholar
Brando, SI 2012 Animal learning and training: implications for ani-mal welfare. Veterinary Clinics: Exotic Animal Practice 15: 387–398. https://doi.org/10.1016/j.cvex.2012.06.008Google Scholar
Breland, K 1962 New strides in animal psychology bring about naturalistic behavior exhibits. Parks and Recreation 45: 80Google Scholar
Breland, K and Breland, M 1951 A field of applied animal psy-chology. American Psychologist 6: 202. https://doi.org/10.1037/h0063451CrossRefGoogle Scholar
Brereton, JE 2020 Directions in animal enclosure use studies. Journal of Zoo and Aquarium Research 8: 1–9. https://doi.org/10.3390/jzbg1010002Google Scholar
Brown, PL and Jenkins, HM 1968 Auto-shaping of the pigeon's key-peck. Journal of the Experimental Analysis of Behavior 11: 1–8. https://doi.org/10.1901/jeab.1968.11-1CrossRefGoogle ScholarPubMed
Capshew, JH 1993 Engineering behavior: project pigeon, World War II, and the conditioning of BF Skinner. Technology and Culture 34: 835–857. https://doi.org/10.2307/3106417CrossRefGoogle ScholarPubMed
Carlstead, K, Brown, JL and Seidensticker, J 1993 Behavioral and adrenocortical responses to environmental changes in leop-ard cats (Felis bengalensis). Zoo Biology 12: 321–331. https://doi.org/10.1002/zoo.1430120403Google Scholar
Carlstead, K and Seidensticker, J 1991 Seasonal variation in stereotypic pacing in an American black bear (Ursus americanus). Behavioural Processes 25: 155–161. https://doi.org/10.1016/0376-6357(91)90017-TCrossRefGoogle Scholar
Carlstead, K, Seidensticker, J and Baldwin, R 1991 Environmental enrichment for zoo bears. Zoo Biology 10: 3–16. https://doi.org/10.1002/zoo.1430100103CrossRefGoogle Scholar
Carrasco, L, Colell, M, Calvo, M, Abello, MT, Velasco, M and Posada, S 2009 Benefits of training/playing therapy in a group of captive lowland gorillas (Gorilla gorilla gorilla). Animal Welfare 18: 9–19Google Scholar
Carter, M, Sherwen, S and Webber, S 2021 An evaluation of interactive projections as digital enrichment for orangutans. Zoo Biology 40: 107–114. https://doi.org/10.1002/zoo.21587CrossRefGoogle ScholarPubMed
China, L, Mills, DS and Cooper, JJ 2020 Efficacy of dog training with and without remote electronic collars vs a focus on positive reinforcement. Frontiers in Veterinary Science 7: 508. https://doi.org/10.3389/fvets.2020.00508CrossRefGoogle Scholar
Claxton, AM 2011 The potential of the human-animal relation-ship as an environmental enrichment for the welfare of zoo-housed animals. Applied Animal Behaviour Science 133: 1–10. https://doi.org/10.1016/j.applanim.2011.03.002CrossRefGoogle Scholar
Clayton, M and Shrock, T 2020 Making a tiger's day: Free-oper-ant assessment and environmental enrichment to improve the daily lives of captive Bengal tigers (Panthera tigris tigris). Behavior Analysis in Practice 13: 883–893. https://doi.org/10.1007/s40617-020-00478-zCrossRefGoogle ScholarPubMed
Coe, J 2004 Mixed species rotation exhibits. joncoedesign.comGoogle Scholar
Coe, J and Hoy, J 2020 Choice, control and computers: Empowering wildlife in human care. Multimodal Technologies and Interaction 4: 92. https://doi.org/10.3390/mti4040092CrossRefGoogle Scholar
Coe, JC 1985 Design and perception: Making the zoo experience real. Zoo Biology 4: 197–208. https://doi.org/10.1002/zoo.1430040211CrossRefGoogle Scholar
Coleman, K and Maier, A 2010 The use of positive reinforce-ment training to reduce stereotypic behavior in rhesus macaques. Applied Animal Behaviour Science 124: 142–148. https://doi.org/10.1016/j.applanim.2010.02.008CrossRefGoogle Scholar
Curtis, L 1957 Coin-operated animal acts. Parks and Recreation 40: 18Google Scholar
Dadone, LI, Schilz, A, Friedman, SG, Bredahl, J, Foxworth, S and Chastain, B 2016 Training giraffe (Giraffa camelopardalis retic-ulata) for front foot radiographs and hoof care. Zoo Biology 35: 228–236. https://doi.org/10.1002/zoo.21279CrossRefGoogle ScholarPubMed
Davey, G 2007 Visitors’ effects on the welfare of animals in the zoo: A review. Journal of Applied Animal Welfare Science 10: 169–183. https://doi.org/10.1080/10888700701313595CrossRefGoogle ScholarPubMed
De Jonge, FH, Tilly, SL, Baars, AM and Spruijt, BM 2008 On the rewarding nature of appetitive feeding behaviour in pigs (Sus scrofa): do domesticated pigs contrafreeload? Applied Animal Behaviour Science 114: 359–372. https://doi.org/10.1016/j.applanim.2008.03.006CrossRefGoogle Scholar
Delfour, F, Monreal-Pawlowsky, T, Vaicekauskaite, R, Pilenga, C, Garcia-Parraga, D, Rödel, HG, Caro, NG, Campos, EP and Mercera, B 2020 Dolphin welfare assessment under professional care:‘willingness to participate’, an indicator significantly associat-ed with six potential ‘alerting factors.’ Journal of Zoological and Botanical Gardens 1: 42–60. https://doi.org/10.3390/jzbg1010004CrossRefGoogle Scholar
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
Domjan, MP 2014 The Principles of Learning and Behavior. Cengage Learning: Boston, MA, USAGoogle Scholar
Dorey, NR and Cox, DJ 2018 Function matters: a review of ter-minological differences in applied and basic clicker training research. PeerJ 6: e5621. https://doi.org/10.7717/peerj.5621CrossRefGoogle ScholarPubMed
Dorey, NR, Mehrkam, LR and Tacey, J 2015 A method to assess relative preference for training and environmental enrichment in captive wolves (Canis lupus and Canis lupus arctos). Zoo Biology 34: 513–517. https://doi.org/10.1002/zoo.21239CrossRefGoogle ScholarPubMed
Eskelinen, HC, Winship, KA and Borger-Turner, JL 2015 Sex, age, and individual differences in bottlenose dolphins (Tursiops trun-catus) in response to environmental enrichment. Animal Behavior and Cognition 2: 241–253. https://doi.org/10.12966/abc.08.04.2015CrossRefGoogle Scholar
European Association of Zoos and Aquaria 2019 Standards for the accommodation and care of animals in zoos and aquaria. https://www.eaza.net/assets/Uploads/Standards-and-policies/2019-04-EAZA-Standards-for-Accomodation-and-Care.pdfGoogle Scholar
Fernandez, EJ 2001 Click or treat: A trick or two in the zoo. American Animal Trainer Magazine 2: 41–44Google Scholar
Fernandez, EJ 2010 Stereotypies and Foraging: Appetitive Search Behaviors and Stereotypies in Captive Animals. VDM Publishing: Saarbrucken, GermanyGoogle Scholar
Fernandez, EJ 2020 Training petting zoo sheep to act like petting zoo sheep: An empirical evaluation of response-independent schedules and shaping with negative reinforcement. Animals 10(7): 1122. https://doi.org/10.3390/ani10071122CrossRefGoogle ScholarPubMed
Fernandez, EJ 2021 Appetitive search behaviors and stereotypies in polar bears (Ursus maritimus). Behavioural Processes 182: 104299. https://doi.org/10.1016/j.beproc.2020.104299CrossRefGoogle ScholarPubMed
Fernandez, EJ and Dorey, NR 2020 An examination of shaping with an African crested porcupine (Hystrix cristata). Journal of Applied Animal Welfare Science 1-7. https://doi.org/10.1080/10888705.2020.1753191CrossRefGoogle Scholar
Fernandez, EJ, Dorey, N and Rosales-Ruiz, J 2004 A two-choice preference assessment with five cotton-top tamarins (Saguinus oedipus). Journal of Applied Animal Welfare Science 7: 163–169. https://doi.org/10.1207/s15327604jaws0703_2CrossRefGoogle ScholarPubMed
Fernandez, EJ, Kinley, RC and Timberlake, W 2019 Training penguins to interact with enrichment devices for lasting effects. Zoo Biology 38: 481–489. https://doi.org/10.1002/zoo.21510CrossRefGoogle ScholarPubMed
Fernandez, EJ, Myers, M and Hawkes, NC 2021a The effects of live feeding on swimming activity and exhibit use in zoo Humboldt penguins (Spheniscus humboldti). Journal of Zoological and Botanical Gardens 2: 88–100. https://doi.org/10.3390/jzbg2010007CrossRefGoogle Scholar
Fernandez, EJ and Rosales-Ruiz, J 2020 A comparison of fixed-time food schedules and shaping involving a clicker for halter behavior in a petting zoo goat. The Psychological Record 1-5. https://doi.org/10.1007/s40732-020-00420-3CrossRefGoogle Scholar
Fernandez, EJ, Tamborski, MA, Pickens, SR and Timberlake, W 2009 Animal-visitor interactions in the modern zoo: Conflicts and interventions. Applied Animal Behaviour Science 120: 1–8. https://doi.org/10.1016/j.applanim.2009.06.002CrossRefGoogle Scholar
Fernandez, EJ and Timberlake, W 2005 The functional value of enrichment: determining environmental enrichment effects in lemurs through the use of paired-choice preference assessments. Association for Behavior Analysis Conference. 27-31 May 2005, Chicago, IL, USAGoogle Scholar
Fernandez, EJ and Timberlake, W 2008 Mutual benefits of research collaborations between zoos and academic institutions. Zoo Biology 27: 470–487. https://doi.org/10.1002/zoo.20215CrossRefGoogle ScholarPubMed
Fernandez, EJ and Timberlake, W 2019a Foraging devices as enrichment in captive walruses (Odobenus rosmarus). Behavioural Processes 168: 103943. https://doi.org/10.1016/j.beproc.2019.103943CrossRefGoogle ScholarPubMed
Fernandez, EJ and Timberlake, W 2019b Selecting and testing environmental enrichment in lemurs. Frontiers in Psychology 10: 2119. https://doi.org/10.3389/fpsyg.2019.02119CrossRefGoogle ScholarPubMed
Fernandez, EJ, Upchurch, B and Hawkes, NC 2021b Public feeding interactions as enrichment for three zoo-housed ele-phants. Animals 11(6): 1689. https://doi.org/10.3390/ani11061689CrossRefGoogle Scholar
Finlay, T, James, LR and Maple, TL 1988 People's perceptions of animals: the influence of zoo environment. Environment and Behavior 20: 508–528. https://doi.org/10.1177/0013916588204008CrossRefGoogle Scholar
Forthman, DL and Ogden, JJ 1992 The role of applied behavior analysis in zoo management: today and tomorrow. Journal of Applied Behavior Analysis 25: 647. https://doi.org/10.1901/jaba.1992.25-647CrossRefGoogle ScholarPubMed
Forthman-Quick, DL 1984 An integrative approach to environ-mental engineering in zoos. Zoo Biology 3: 65–77. https://doi.org/10.1002/zoo.1430030107CrossRefGoogle Scholar
Gillaspy, JA Jr, Brinegar, JL and Bailey, RE 2014 Operant psy-chology makes a splash: in marine mammal training (1955–1965). Journal of the History of the Behavioral Sciences 50: 231–248. https://doi.org/10.1002/jhbs.21664CrossRefGoogle Scholar
Godinez, AM and Fernandez, EJ 2019 What is the zoo experi-ence? How zoos impact a visitor's behaviors, perceptions, and con-servation efforts. Frontiers in Psychology 10: 1746. https://doi.org/10.3389/fpsyg.2019.01746CrossRefGoogle Scholar
Graham, L, Wells, DL and Hepper, PG 2005 The influence of olfactory stimulation on the behaviour of dogs housed in a rescue shelter. Applied Animal Behaviour Science 91: 143–153. https://doi.org/10.1016/j.applanim.2004.08.024CrossRefGoogle Scholar
Grandin, T, Rooney, MB, Phillips, M, Cambre, RC, Irlbeck, NA and Graffam, W 1995 Conditioning of nyala (Tragelaphus angasi) to blood sampling in a crate with positive reinforcement. Zoo Biology 14: 261–273. https://doi.org/10.1002/zoo.1430140307CrossRefGoogle Scholar
Grant, RA and Warrior, JR 2019 Clicker training increases exploratory behaviour and time spent at the front of the enclo-sure in shelter cats: Implications for welfare and adoption rates. Applied Animal Behaviour Science 211: 77–83. https://doi.org/10.1016/j.applanim.2018.12.002CrossRefGoogle Scholar
Hancocks, D 1980 Bringing nature into the zoo: inexpensive solutions for zoo environments. International Journal for the Study of Animal Behavior Problems 1: 170–177Google Scholar
Hare, VJ and Sevenich, M 2001 Is it training or is it enriching? Proceedings of the Fourth International Conference on Environmental Enrichment. Edinburgh, UKGoogle Scholar
Haug, LI 2008 Canine aggression toward unfamiliar people and dogs. Veterinary Clinics of North America: Small Animal Practice 38: 1023–1041. https://doi.org/10.1016/j.cvsm.2008.04.005CrossRefGoogle ScholarPubMed
Hazel, SJ, O’Dwyer, L and Ryan, T 2015 ‘Chickens are a lot smarter than I originally thought’: changes in student attitudes to chickens following a chicken training class. Animals 5: 821–837. https://doi.org/10.3390/ani5030386CrossRefGoogle ScholarPubMed
Hediger, H 1950 Wild Animals in Captivity. Butterworth-Heinemann: Oxford, UKGoogle Scholar
Homme, L, C'de Baca, P, Cottingham, L and Homme, A 1968 What behavioral engineering is. The Psychological Record 18: 425–434. https://doi.org/10.1007/BF03393790CrossRefGoogle Scholar
Hosey, GR 2000 Zoo animals and their human audiences: what is the visitor effect? Animal Welfare 9: 343–357Google Scholar
Hoy, JM, Murray, PJ and Tribe, A 2010 Thirty years later: Enrichment practices for captive mammals. Zoo Biology 29: 303–316. https://doi.org/10.1002/zoo.20254CrossRefGoogle ScholarPubMed
Hutchins, M, Hancocks, D and Crockett, C 1984 Natural solutions to the behavioral problems of captive animals. Zoologische Garten 54: 28–42Google Scholar
Inglis, IR, Forkman, B and Lazarus, J 1997 Free food or earned food? A review and fuzzy model of contrafreeloading. Animal Behaviour 53: 1171–1191. https://doi.org/10.1006/anbe.1996.0320CrossRefGoogle ScholarPubMed
Jensen, GD 1963 Preference for bar pressing over ‘freeloading’ as a function of number of rewarded presses. Journal of Experimental Psychology 65: 451. https://doi.org/10.1037/h0049174CrossRefGoogle ScholarPubMed
Jensen, P, Schütz, K and Lindqvist, C 2002 Red jungle fowl have more contrafreeloading than white leghorn layers: effect of food deprivation and consequences for information gain. Behaviour 139: 1195–1209. https://doi.org/10.1163/15685390260437335CrossRefGoogle Scholar
Johnston, JM and Pennypacker, HS 2010 Strategies and Tactics of Behavioral Research. Routledge: Oxon, UK. https://doi.org/10.4324/9780203837900CrossRefGoogle Scholar
Kyngdon, DJ, Minot, EO and Stafford, KJ 2003 Behavioural responses of captive common dolphins (Delphinus delphis) to a ‘Swim-with-Dolphin’ programme. Applied Animal Behaviour Science 81: 163–170. https://doi.org/10.1016/S0168-1591(02)00255-1CrossRefGoogle Scholar
Laule, GE 2003 Positive reinforcement training and environmen-tal enrichment: enhancing animal well-being. Journal of the American Veterinary Medical Association 223: 969–973. https://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. https://doi.org/10.1207/S15327604JAWS0603_02CrossRefGoogle ScholarPubMed
Laule, G 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
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: 31–38. https://doi.org/10.1080/10888700701277311CrossRefGoogle ScholarPubMed
Lawrence, AB, Vigors, B and Sandøe, P 2019 What is so positive about positive animal welfare? A critical review of the literature. Animals 9: 783. https://doi.org/10.3390/ani9100783CrossRefGoogle ScholarPubMed
Leeds, A, Elsner, R and Lukas, KE 2016 The effect of positive reinforcement training on an adult female western lowland goril-la's (Gorilla gorilla gorilla) rate of abnormal and aggressive behav-ior. Animal Behavior and Cognition 3: 78–87. https://doi.org/10.12966/abc.02.05.2016CrossRefGoogle Scholar
Lindqvist, C and Jensen, P 2009 Domestication and stress effects on contrafreeloading and spatial learning performance in red jungle fowl (Gallus gallus) and White Leghorn layers. Behavioural Processes 81: 80–84. https://doi.org/10.1016/j.beproc.2009.02.005Google ScholarPubMed
Luescher, AU and Medlock, RT 2009 The effects of training and environmental alterations on adoption success of shelter dogs. Applied Animal Behaviour Science 117: 63–68. https://doi.org/10.1016/j.applanim.2008.11.001CrossRefGoogle Scholar
Lukas, KE, Marr, MJ and Maple, TL 1998 Teaching operant con-ditioning at the zoo. Teaching of Psychology 25: 112–116. https://doi.org/10.1207/s15328023top2502_7CrossRefGoogle Scholar
Mackie, J 2020 The application of positive reinforcement training to enhance welfare of primates in zoological collections. Zoo Animal Learning and Training: 211-215. https://doi.org/10.1002/9781118968543.oth9CrossRefGoogle Scholar
Maple, TL and Finlay, TW 1986 Evaluating the environments of captive nonhuman primates. In: Benirschke, K (ed) Primates: The Road to Self-Sustaining Populations pp 479–488. Springer-Verlag: New York, NY, USA. https://doi.org/10.1007/978-1-4612-4918-4_38CrossRefGoogle Scholar
Maple, TL and Finlay, TW 1987 Post-occupancy evaluation in the zoo. Applied Animal Behaviour Science 18: 5–18. https://doi.org/10.1016/0168-1591(87)90250-4CrossRefGoogle Scholar
Maple, TL and Perdue, BM 2013 Zoo Animal Welfare. Springer: Berlin, Germany. https://doi.org/10.1007/978-3-642-35955-2CrossRefGoogle Scholar
Maple, TL and Segura, VD 2015 Advancing behavior analysis in zoos and aquariums. The Behavior Analyst 38: 77–91. https://doi.org/10.1007/s40614-014-0018-xCrossRefGoogle ScholarPubMed
Markowitz, H 1978 Engineering environments for behavioral opportunities in the zoo. The Behavior Analyst 1: 34–47. https://doi.org/10.1007/BF03392371CrossRefGoogle ScholarPubMed
Markowitz, H 1982 Behavioral Enrichment in the Zoo. Van Nostrand Reinhold: New York, NY, USAGoogle Scholar
Markowitz, H 2011 Enriching Animal Lives. Mauka Press: Pacifica, CA, USAGoogle Scholar
Markowitz, H, Aday, C and Gavazzi, A 1995 Effectiveness of acoustic ‘prey’: Environmental enrichment for a captive African leopard (Panthera pardus). Zoo Biology 14: 371–379. https://doi.org/10.1002/zoo.1430140408CrossRefGoogle Scholar
Markowitz, H and LaForse, S 1987 Artificial prey as behavioral enrichment devices for felines. Applied Animal Behaviour Science 18: 31–43. https://doi.org/10.1016/0168-1591(87)90252-8CrossRefGoogle Scholar
Markowitz, H, Schmidt, MJ and Moody, A 1978 Behavioural engineering and animal health in the zoo. International Zoo Yearbook 18: 190–194. https://doi.org/10.1111/j.1748-1090.1978.tb00256.xCrossRefGoogle Scholar
Markowitz, H and Spinelli, JS 1986 Environmental engineering for primates. In: Benirschke, K (ed) Primates: The Road to Self-Sustaining Populations pp 489–498. Springer-Verlag: New York, NY, USA. https://doi.org/10.1007/978-1-4612-4918-4_39CrossRefGoogle Scholar
Markowitz, H and Stevens, VJ 1978 Behavior of Captive Wild Animals. Nelson-Hall: Chicago, IL, USAGoogle Scholar
Martin, AL 2017 The primatologist as a behavioral engineer. American Journal of Primatology 79(1): e22500. https://doi.org/10.1002/ajp.22500CrossRefGoogle ScholarPubMed
McCormick, W and Melfi, VA 2003 How enriching is training? Proceedings of the Sixth International Conference on Environmental Enrichment. Johannesburg, South AfricaGoogle Scholar
McGowan, RT, Robbins, CT, Alldredge, JR and Newberry, RC 2010 Contrafreeloading in grizzly bears: implications for captive foraging enrichment. Zoo Biology 29: 484–502. https://doi.org/10.1002/zoo.20282Google ScholarPubMed
Mehrkam, LR and Dorey, NR 2014 Is preference a predictor of enrichment efficacy in Galapagos tortoises (Chelonoidis nigra)? Zoo Biology 33: 275–284. https://doi.org/10.1002/zoo.21151CrossRefGoogle ScholarPubMed
Melfi, V 2013 Is training zoo animals enriching? Applied Animal Behaviour Science 147: 299–305. https://doi.org/10.1016/j.applanim.2013.04.011CrossRefGoogle Scholar
Melfi, V 2014 In response to the letter to the editor regarding the article: ‘Is training zoo animals enriching?’ Applied Animal Behaviour Science 152: 103–105. https://doi.org/10.1016/j.applanim.2013.12.012CrossRefGoogle Scholar
Melfi, VA, Dorey, NR and Ward, SJ 2020 Zoo Animal Learning and Training. Wiley Blackwell: Hoboken, NJ, USA. https://doi.org/10.1002/9781118968543CrossRefGoogle Scholar
Melfi, VA and Ward, SJ 2020 Welfare implications of zoo animal training. In: Melfi VA Dorey, NR and Ward, SJ (eds) Zoo Animal Learning and Training pp 271–288. Wiley Blackwell: Hoboken, NJ, USA. https://doi.org/10.1002/9781118968543.ch11CrossRefGoogle Scholar
Mellen, J and Sevenich MacPhee, M 2001 Philosophy of envi-ronmental enrichment: past, present, and future. Zoo Biology 20: 211–226. https://doi.org/10.1002/zoo.1021CrossRefGoogle Scholar
Mellor, DJ 2016 Updating animal welfare thinking: Moving beyond the ‘Five Freedoms’ towards ‘a Life Worth Living.’ Animals 6: 21. https://doi.org/10.3390/ani6030021CrossRefGoogle ScholarPubMed
Mellor, DJ and Beausoleil, NJ 2019 Moving beyond a problem-based focus on poor animal welfare toward creating opportunities to have positive welfare experiences. Mental Health and Well-being in Animals, Second Edition pp 50–66. Blackwell Publishing: UK. https://doi.org/10.1079/9781786393401.0050CrossRefGoogle Scholar
Mellor, DJ, Beausoleil, NJ, Littlewood, KE, McLean, AN, McGreevy, PD, Jones, B and Wilkins, C 2020 The 2020 Five Domains Model: Including human-animal interactions in assess-ments of animal welfare. Animals 10: 1870. https://doi.org/10.3390/ani10101870CrossRefGoogle Scholar
Mench, JA 1998 Environmental enrichment and the importance of exploratory behavior. In: Shepherdson, DJ, Mellen, JD and Hutchins, M (eds) Second Nature: Environmental Enrichment for Captive Animals pp 30–46. Smithsonian Institution Press: Washington, DC, USAGoogle Scholar
Miller, LJ, Vicino, GA, Sheftel, J and Lauderdale, LK 2020 Behavioral diversity as a potential indicator of positive animal wel-fare. Animals 10: 1211. https://doi.org/10.3390/ani10071211Google Scholar
Neuringer, AJ 1969 Animals respond for food in the presence of free food. Science 166: 399–401. https://doi.org/10.1126/science.166.3903.399CrossRefGoogle ScholarPubMed
Newberry, RC 1995 Environmental enrichment: increasing the biological relevance of captive environments. Applied Animal Behaviour Science 44: 229–243. https://doi.org/10.1016/0168-1591(95)00616-ZCrossRefGoogle Scholar
Ogura, T 2011 Contrafreeloading and the value of control over visual stimuli in Japanese macaques (Macaca fuscata). Animal Cognition 14: 427–431. https://doi.org/10.1007/s10071-010-0377-yCrossRefGoogle ScholarPubMed
Peterson, GB 2004 A day of great illumination: BF Skinner's dis-covery of shaping. Journal of the Experimental Analysis of Behavior 82: 317–328. https://doi.org/10.1901/jeab.2004.82-317CrossRefGoogle Scholar
Pfaller-Sadovsky, N, Hurtado-Parrado, C, Cardillo, D, Medina, LG and Friedman, SG 2020 What's in a Click? The effi-cacy of conditioned reinforcement in applied animal training: A systematic review and meta-analysis. Animals 10(10): 1757. https://doi.org/10.3390/ani10101757CrossRefGoogle Scholar
Phillips, M, Grandin, T, Graffam, W, Irlbeck, NA and Cambre, RC 1998 Crate conditioning of bongo (Tragelaphus eurycerus) for veterinary and husbandry procedures at the Denver Zoological Gardens. Zoo Biology 17: 25–32. https://doi.org/10.1002/(SICI)1098-2361(1998)17:1<25::AID-ZOO3>3.0.CO;2-C3.0.CO;2-C>CrossRefGoogle Scholar
Pierce, WD and Cheney, CD 2013 Behavior Analysis and Learning. Psychology Press: Hove, East Sussex, UK. https://doi.org/10.4324/9780203726624Google Scholar
Platt, DM and Novak, MA 1997 Videostimulation as enrichment for captive rhesus monkeys (Macaca mulatta). Applied Animal Behaviour Science 52: 139–155. https://doi.org/10.1016/S0168-1591(96)01093-3CrossRefGoogle Scholar
Pomerantz, O and Terkel, J 2009 Effects of positive reinforce-ment training techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). American Journal of Primatology 71: 687–695. https://doi.org/10.1002/ajp.20703CrossRefGoogle Scholar
Priest, G 1991 Training a diabetic drill (Mandrillus leucophaeus) to accept insulin injections and venipuncture. Laboratory Primate Newsletter 30: 1–4Google Scholar
Pryor, K 1999 Don't shoot the dog! The new art of teaching and training, Revised Edition. Bantam Books: New York, NY, USAGoogle Scholar
Pryor, K and Ramirez, KR 2014 A Handbook of Operant and Classical Conditioning. Wiley-Blackwell: Hoboken, NJ, USAGoogle Scholar
Pryor, KW and Chase, S 2014 Training for variability and inno-vative behavior. International Journal of Comparative Psychology 27: 361–368. https://doi.org/10.46867/ijcp.2014.27.02.01CrossRefGoogle Scholar
Pryor, KW, Haag, R and O’Reilly, J 1969 The creative por-poise: Training for novel behavior. Journal of the Experimental Analysis of Behavior 12: 653–661. https://doi.org/10.1901/jeab.1969.12-653CrossRefGoogle ScholarPubMed
Ramirez, K 1999 Animal Training: Successful Animal Management through Positive Reinforcement. Shedd Aquarium Press: Chicago, IL, USAGoogle Scholar
Ramirez, K 2020 The Eye of the Trainer: Animal Training, Transformation, and Trust. First Stone Publishing: Gloucestershire, UKGoogle Scholar
Rooney, NJ and Cowan, S 2011 Training methods and owner-dog interactions: Links with dog behaviour and learning ability. Applied Animal Behaviour Science 132: 169–177. https://doi.org/10.1016/j.applanim.2011.03.007CrossRefGoogle Scholar
Rose, NA and Parsons, ECM 2019 The Case Against Marine Mammals in Captivity, Fifth Edition. Animal Welfare Institute and World Animal Protection: Washington, DC, USAGoogle Scholar
Sasson-Yenor, J and Powell, DM 2019 Assessment of con-trafreeloading preferences in giraffe (Giraffa camelopardalis). Zoo Biology 38: 414–423. https://doi.org/10.1002/zoo.21513CrossRefGoogle ScholarPubMed
Savastano, G, Hanson, A and McCann, C 2003 The develop-ment of an operant conditioning training program for New World primates at the Bronx Zoo. Journal of Applied Animal Welfare Science 6: 247–261. https://doi.org/10.1207/S15327604JAWS0603_09CrossRefGoogle Scholar
Schapiro, SJ, Perlman, JE and Boudreau, BA 2001 Manipulating the affiliative interactions of group-housed rhesus macaques using positive reinforcement training techniques. American Journal of Primatology 55: 137–149. https://doi.org/10.1002/ajp.1047CrossRefGoogle ScholarPubMed
Schmidt, MJ and Markowitz, H 1977 Behavioral engineering as an aid in the maintenance of healthy zoo animals. Journal of the American Veterinary Medical Association 171: 966–969Google ScholarPubMed
Shepherdson, DJ 1998 Tracing the path of environmental enrich-ment in zoos. In: Shepherdson, DJ, Mellen, JD and Hutchins, M (eds) Second Nature: Environmental Enrichment for Captive Animals pp 1–12. Smithsonian Institution Press: Washington, DC, USAGoogle Scholar
Shepherdson, DJ, Carlstead, K, Mellen, JD and Seidensticker, J 1993 The influence of food presentation on the behavior of small cats in confined environments. Zoo Biology 12: 203–216. https://doi.org/10.1002/zoo.1430120206CrossRefGoogle Scholar
Shepherdson, DJ, Mellen, JD and Hutchins, M 1998 Second Nature: Environmental Enrichment for Captive Animals. Smithsonian Institutional Press: Washington, DC, USAGoogle Scholar
Sherwen, SL and Hemsworth, PH 2019 The visitor effect on zoo animals: Implications and opportunities for zoo animal wel-fare. Animals 9: 366. https://doi.org/10.3390/ani9060366CrossRefGoogle Scholar
Sherwin, CM, Lewis, PD and Perry, GC 1999 The effects of environmental enrichment and intermittent lighting on the behav-iour and welfare of male domestic turkeys. Applied Animal Behaviour Science 62: 319–333. https://doi.org/10.1016/S0168-1591(98)00215-9CrossRefGoogle Scholar
Shyne, A and Block, M 2010 The effects of husbandry training on stereotypic pacing in captive African wild dogs (Lycaon pictus). Journal of Applied Animal Welfare Science 13: 56–65. https://doi.org/10.1080/10888700903372069CrossRefGoogle ScholarPubMed
Skinner, BF 1951 How to teach animals. Scientific American 185: 26–29. https://doi.org/10.1038/scientificamerican1251-26CrossRefGoogle Scholar
Spiezio, C, Piva, F, Regaiolli, B and Vaglio, S 2016 Positive rein-forcement training: a tool for care and management of captive vervet monkeys (Chlorocebus aethiops). Animal Welfare 24: 283–290. https://doi.org/10.7120/09627286.24.3.283Google Scholar
Spiezio, C, Vaglio, S, Scala, C and Regaiolli, B 2017 Does pos-itive 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. https://doi.org/10.1016/j.applanim.2017.07.007CrossRefGoogle Scholar
Trone, M, Kuczaj, S and Solangi, M 2005 Does participation in dolphin-human interaction programs affect bottlenose dolphin behaviour? Applied Animal Behaviour Science 93: 363–374. https://doi.org/10.1016/j.applanim.2005.01.003CrossRefGoogle Scholar
Vasconcellos, AS, Adania, CH and Ades, C 2012 Contrafreeloading in maned wolves: Implications for their man-agement and welfare. Applied Animal Behaviour Science 140: 85–91. https://doi.org/10.1016/j.applanim.2012.04.012CrossRefGoogle Scholar
Ward, SJ and Melfi, V 2013 The implications of husbandry training on zoo animal response rates. Applied Animal Behaviour Science 147: 179–185. https://doi.org/10.1016/j.applanim.2013.05.008CrossRefGoogle Scholar
Wells, DL and Irwin, RM 2008 Auditory stimulation as enrich-ment for zoo-housed Asian elephants (Elephas maximus). Animal Welfare 17: 335–340Google Scholar
Westlund, K 2014 Training is enrichment and beyond. Applied Animal Behaviour Science 152: 1–6. https://doi.org/10.1016/j.applan-im.2013.12.009CrossRefGoogle Scholar
Woods, JM, Lane, EK and Miller, LJ 2020 Preference assess-ments as a tool to evaluate environmental enrichment. Zoo Biology 39: 382–390. https://doi.org/10.1002/zoo.21566CrossRefGoogle Scholar
Yanofsky, R and Markowitz, H 1978 Changes in general behav-ior of two mandrills (Papio sphinx) concomitant with behavioral testing in the zoo. The Psychological Record 28: 369–373. https://doi.org/10.1007/BF03394548CrossRefGoogle Scholar
Yerkes, RM 1925 Almost Human. Century: New York, NY, USAGoogle Scholar
Yin, S 2012 Bells and whistles: When operant conditioning clicked (and clucked). Barks Magazine 69: 74–78Google Scholar
Young, RJ 2003 Environmental Enrichment for Captive Animals. Blackwell Publishing: Hoboken, NJ, USA. https://doi.org/10.1002/9780470751046CrossRefGoogle Scholar
Young, RJ, de Azevedo, CS and Cipreste, CF 2020 Environmental enrichment: the creation of opportunities for infor-mal learning. In: Melfi, VA, Dorey, NR and Ward, SJ (eds) Zoo Animal Learning and Training pp 101–118. Wiley Blackwell: Hoboken, NJ, USA. https://doi.org/10.1002/9781118968543.ch6CrossRefGoogle Scholar
Young, RJ and Cipreste, CF 2004 Applying animal learning the-ory: training captive animals to comply with veterinary and hus-bandry procedures. Animal Welfare 13: 225–232Google Scholar
Young, RJ and Lawrence, AB 2003 Do domestic pigs in controlled environments contrafreeload? Journal of Applied Animal Welfare Science 6: 309–318. https://doi.org/10.1207/s15327604jaws0604_5Google ScholarPubMed