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An evaluation of the role of ‘biological evidence’ in zoo and aquarium enrichment practices

Published online by Cambridge University Press:  01 January 2023

J Brereton  and
P Rose
J Brereton*
Affiliation:
University Centre Sparsholt, Westley Lane, Sparsholt, Winchester SO21 2NF, UK
P Rose
Affiliation:
College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4SB, UK
*
* Contact for correspondence: James.Brereton@sparsholt.ac.uk
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Abstract

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Evidence-based approaches are key to advancing all areas of zoo and aquarium practice. Output from empirical study must be disseminated to those within the industry so that results can support changes to husbandry and management for individual species. Information on enrichment techniques is published in a range of sources, including papers in the peer-reviewed and ‘grey literature’ (ie professional but non-reviewed publications). To investigate how evidence is implemented into enrichment practices, we sampled all enrichment studies identified in one online repository of peer-reviewed papers and two grey literature publications across an eleven-year period. We recorded whether the enrichment was supported with biological evidence (whether it was developed using published enrichment-focused research for that species and/or with the species’ ecology and behaviour information) alongside analysis of the type of enrichment used and the chosen study species. Enrichment articles were more likely to be supported by biological evidence in peer-reviewed than grey literature. Taxonomic differences in the use of evidence were noted; for example, enrichment provided to carnivores and parrots was more likely to be supported with biological evidence compared to that used for penguins. Of the five enrichment types, nutritional enrichment was most often based on biological evidence. Multi-category and physical enrichment types were more common across all literature sources whereas social enrichment was less common, suggesting barriers to implementation of all enrichment types in zoological facilities. Our research suggests that zoo and aquarium professionals are considering species-specific welfare needs by ensuring that enrichment protocols are supported by biological evidence. However, opportunities to diversify the enrichment types being offered and species being researched are identified.

Keywords

animal traininganimal welfareenvironmental enrichmentevidence-based approacheszoo animal managementzoo research
Type
Research Article
Information
Animal Welfare , Volume 31 , Issue 1 , February 2022 , pp. 13 - 26
Copyright
© 2022 Universities Federation for Animal Welfare

References

AAZK 2020 Animal Keepers’ Forum. https://aazk.org/animal-keepers-forum/Google Scholar
ABWAK 2020 Ratel archives. https://abwak.org/Google Scholar
Altman, JD, Gross, KL and Lowry, SR 2005 Nutritional and behavioral effects of gorge and fast feeding in captive lions. Journal of Applied Animal Welfare Science 8: 47–57. https://doi.org/10.1207/s15327604jaws0801_4CrossRefGoogle ScholarPubMed
Barber, JC 2009 Programmatic approaches to assessing and improving animal welfare in zoos and aquariums. Zoo Biology 28: 519–530. https://doi.org/10.1002/zoo.20260Google ScholarPubMed
Bashaw, MJ, Gibson, MD, Schowe, DM and Kucher, AS 2016 Does enrichment improve reptile welfare? Leopard geckos (Eublepharis maculariu s) 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
Bautista, LM and Pantoja, JC 2005 What animal species should we study next? Bulletin of the British Ecological Society 36: 27–31. http://hdl.handle.net/10261/43928Google Scholar
Benjamini, Y and Hochberg, Y 1995 Controlling the false dis-covery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57: 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.xCrossRefGoogle Scholar
Bloomsmith, MA, Brent, LY and Schapiro, SJ 1991 Guidelines for developing and managing an environmental enrichment pro-gram for nonhuman primates. Laboratory Animal Science 41: 372–377. https://doi.org/10.1111/j.2517-6161.1995.tb03450321.Google Scholar
Brereton, SR and Brereton, JE 2020 Sixty years of collection planning: what species do zoos and aquariums keep? International Zoo Yearbook 52: 131–145. https://doi.org/10.1111/izy.12264CrossRefGoogle Scholar
Britt, S, Cowlard, K, Baker, K and Plowman, A 2015 Aggression and self-directed behaviour of captive lemurs (Lemur catta, Varecia variegata, V. rubra and Eulemur coronatus) is reduced by feeding fruit-free diets. Journal of Zoo and Aquarium Research 3: 52–58. https://doi.org/10.19227/jzar.v3i2.119Google Scholar
Browning, H 2020 The natural behavior debate: Two conceptions of animal welfare. Journal of Applied Animal Welfare Science 23: 325–337. https://doi.org/10.1080/10888705.2019.1672552CrossRefGoogle ScholarPubMed
Burghardt, GM 2013 Environmental enrichment and cognitive complexity in reptiles and amphibians: concepts, review, and impli-cations for captive populations. Applied Animal Behaviour Science 147: 286–298. https://doi.org/10.1016/j.applanim.2013.04.013CrossRefGoogle 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
Clubb, R and Mason, G 2003 Captivity effects on wide-ranging carnivores. Nature 425: 473–474. https://doi.org/10.1038/425473aCrossRefGoogle ScholarPubMed
Courchamp, F, Jaric, I, Albert, C, Meinard, Y, Ripple, WJ and Chapron, G 2018 The paradoxical extinction of the most charis-matic animals. PLoS Biology 16: 1–15. https://doi.org/10.1371/jour-nal.pbio.2003997CrossRefGoogle ScholarPubMed
CPSG 2020 The One Plan Approach. https://www.cpsg.org/our-approach/one-plan-approach-conservationGoogle Scholar
dos Santos, JW, Correia, RA, Malhado, AC, Campos-Silva, JV, Teles, D, Jepson, P and Ladle, RJ 2020 Drivers of taxonomic bias in conservation research: a global analysis of terrestrial mam-mals. Animal Conservation 23: 679–688. https://doi.org/10.1111/acv.12586CrossRefGoogle Scholar
EAZA 2020 EAZA Best Practice Guidelines. https://www.eaza.net/about-us/eazadocuments/Google Scholar
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 and Timberlake, W 2019 Selecting and testing environmental enrichment in Lemurs. Frontiers in Psychology 10: 1–12. https://doi.org/10.3389/fpsyg.2019.02119CrossRefGoogle ScholarPubMed
Field, DA and Thomas, R 2000 Environmental enrichment for psittacines at Edinburgh Zoo. International Zoo Yearbook 37: 232–237. https://doi.org/10.1111/j.1748-1090.2000.tb00728.xCrossRefGoogle Scholar
Graham, C, von Keyserlingk, MA and Franks, B 2018 Zebrafish welfare: Natural history, social motivation and behav-iour. Applied Animal Behaviour Science 200: 13–22. https://doi.org/10.1016/j.applanim.2017.11.005CrossRefGoogle Scholar
Greenway, E, Jones, KS and Cooke, GM 2016 Environmental enrichment in captive juvenile thornback rays, Raja clavata (Linnaeus 1758). Applied Animal Behaviour Science 182: 86–93. https://doi.org/10.1016/j.applanim.2016.06.008CrossRefGoogle Scholar
Greggor, AL, Vicino, GA, Swaisgood, RR, Fidgett, A, Brenner, D, Kinney, ME, Farabaugh, S, Masuda, B and Lamberski, N 2018 Animal welfare in conservation breeding: applications and challenges. Frontiers in Veterinary Science 5: 323. https://doi.org/10.3389/fvets.2018.00323CrossRefGoogle ScholarPubMed
Hopper, LM, Shender, MA and Ross, SR 2016 Behavioral research as physical enrichment for captive chimpanzees. Zoo Biology 35: 293–297. https://doi.org/10.1002/zoo.21297CrossRefGoogle ScholarPubMed
Hosey, G, Harley, J and Ward, S 2019 Research and research training in BIAZA zoos and aquariums. Journal of Zoo and Aquarium Research 7: 210–217. https://doi.org/10.19227/jzar.v7i4.458Google 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
Huskisson, SM, Jacobson, SL, Egelkamp, CL, Ross, SR and Hopper, LM 2020 Using a Touchscreen paradigm to evaluate food preferences and response to novel photographic stimuli of food in three primate species (Gorilla gorilla gorilla, Pan troglodytes, and Macaca fuscata). International Journal of Primatology 41: 5–23. https://doi.org/10.1007/s10764-020-00162-7CrossRefGoogle Scholar
Joly, M, Ammersdörfer, S, Schmidtke, D and Zimmermann, E 2014 Touchscreen-based cognitive tasks reveal age-related impairment in a primate aging model, the grey mouse lemur (Microcebus murinus). PLoS One 9: 1–12. https://doi.org/10.1371/journal.pone.0109393CrossRefGoogle Scholar
Kaufman, AB, Bashaw, MJ and Maple, TL 2019 Scientific Foundations of Zoos and Aquariums: Their Role in Conservation and Research. Cambridge University Press: Cambridge, UK. https://doi.org/10.1017/9781108183147CrossRefGoogle Scholar
Kim-McCormack, NN, Smith, CL and Behie, AM 2016 Is interactive technology a relevant and effective enrichment for captive great apes? Applied Animal Behaviour Science 185: 1–8. https://doi.org/10.1016/j.applanim.2016.09.012CrossRefGoogle Scholar
Kirkey, TL 2005 Differentiated instruction and enrichment opportunities: An action research report. The Ontario Action Researcher 8: 1–5. https://doi.org/10.10169061p2dfGoogle 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
Less, EH, Lukas, KE, Bergl, R, Ball, R, Kuhar, CW, Lavin, SR, Raghanti, MA, Wensvoort, J, Willis, MA and Dennis, PM 2014 Implementing a low-starch biscuit-free diet in zoo gorillas: the impact on health. Zoo Biology 33: 74–80. https://doi.org/10.1002/zoo.21115CrossRefGoogle ScholarPubMed
Loh, TL, Larson, ER, David, SR, de Souza, LS, Gericke, R, Gryzbek, M, Kough, AS, Willink, PW and Knapp, CR 2018 Quantifying the contribution of zoos and aquariums to peer-reviewed scientific research. Facets 3: 287–299 https://doi.org/10.1139/facets-2017-0083CrossRefGoogle Scholar
Lutz, CK and Novak, MA 2005 Environmental enrichment for nonhuman primates: theory and application. Ilar Journal 46: 178–191. https://doi.org/10.1093/ilar.46.2.178CrossRefGoogle ScholarPubMed
Mason, G, Clubb, R, Latham, N and Vickery, S 2007 Why and how should we use environmental enrichment to tackle stereo-typic behaviour? Applied Animal Behaviour Science 102: 163–188. https://doi.org/10.1016/j.applanim.2006.05.041CrossRefGoogle Scholar
Mather, JA 2019 Ethics and care: For animals, not just mammals. Animals 9: 1018. https://doi.org/10.3390/ani9121018CrossRefGoogle Scholar
MDPI 2020 Special issue ‘Evidence-based practice in zoo animal man-agement.’ Animals Journal. https://www.mdpi.com/journal/animals/spe-cial_issues/Evidence-Based_Practice_Zoo_Animal_ManagementGoogle Scholar
Meehan, CL and Mench, JA 2007 The challenge of challenge: Can problem solving opportunities enhance animal welfare? Applied Animal Behaviour Science 102: 246–261. https://doi.org/10.1016/j.applanim.2006.05.031CrossRefGoogle Scholar
Melfi, VA 2009 There are big gaps in our knowledge, and thus approach, to zoo animal welfare: a case for evidence-based zoo animal management. Zoo Biology 28: 574–588. https://doi.org/10.1002/zoo.20288Google ScholarPubMed
Melfi, VA 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 and Hosey, G 2011 Capacity building for better animal welfare. International Zoo Yearbook 45: 274–281. https://doi.org/10.1111/j.1748-1090.2011.00136.xCrossRefGoogle Scholar
Michaels, CJ, Downie, JR and Campbell-Palmer, R 2014 The importance of enrichment for advancing amphibian welfare and conservation goals. Amphibian Reptile Conservation 8: 7–23Google Scholar
Mooney, A, Conde, DA, Healy, K and Buckley, YM 2020 A sys-tem wide approach to managing zoo collections for visitor atten-dance and in situ conservation. Nature Communications 11: 1–8. https://doi.org/10.1038/s41467-020-14303-2CrossRefGoogle Scholar
Pich, JM, Belden, AJ and Carlson, BE 2019 Individual variation in boldness in turtles is consistent across assay conditions and behavioural measures. Behaviour 156: 1039–1056. https://doi.org/10.1163/1568539X-00003555CrossRefGoogle Scholar
Regaiolli, B, Rizzo, A, Ottolini, G, Miletto Petrazzini, ME, Spiezio, C and Agrillo, C 2019 Motion illusions as environmen-tal enrichment for zoo animals: a preliminary investigation on lions (Panthera leo). Frontiers in Psychology 10: 2220. https://doi.org/10.3389/fpsyg.2019.02220CrossRefGoogle Scholar
Reinhardt, V, Dan Houser, W, Eisele, SG and Champoux, M 1987 Social enrichment of the environment with infants for singly caged adult rhesus monkeys. Zoo Biology 6: 365–371. https://doi.org/10.1002/zoo.1430060410CrossRefGoogle Scholar
Resende, LDS, Pedretti Gomes, KC, Andriolo, A, Genaro, G, Remy, GL and Almeida Ramos, VD 2011 Influence of cinnamon and catnip on the stereotypical pacing of oncilla cats (Leopardus tigri-nus) in captivity. Journal of Applied Animal Welfare Science 14: 247–254. https://doi.org/10.1080/10888705.2011.576981CrossRefGoogle ScholarPubMed
Riley, LM and Rose, PE 2020 Concepts, applications, uses and evaluation of environmental enrichment. Journal of Zoo and Aquarium Research 8: 18–28. https://doi.org/10.19227/jzar.v8i1.384Google Scholar
Ritvo, SE and Allison, RS 2017 Designing for the exceptional user: Nonhuman animal-computer interaction (ACI). Computers in Human Behavior 70: 222–233. https://doi.org/10.1016/j.chb.2016.12.062CrossRefGoogle Scholar
Ritvo, SE and MacDonald, SE 2016 Music as enrichment for Sumatran orangutans (Pongo abelii). Journal of Zoo and Aquarium Research 4: 156–163. https://doi.org/10.19227/jzar.v4i3.231Google Scholar
Rose, P, Brereton, JE and Gardner, L 2016 Developing flamingo husbandry practices through workshop communication. Journal of Zoo and Aquarium Research 4: 115–121. https://doi.org/10.19227/jzar.v4i2.109Google Scholar
Rose, PE, Brereton, JE, Rowden, LJ, de Figueiredo, RL and Riley, LM 2019a What's new from the zoo? An analysis of ten years of zoo-themed research output. Palgrave Communications 5: 1–10. https://doi.org/10.1057/s41599-019-0345-3CrossRefGoogle Scholar
Rose, PE, Brereton, JE, Rowden, LJ, de Figueiredo, RL and Riley, LM 2019b Zoo research output dataset. University of Exeter, Exeter, Devon, UK. https://doi.org/10.24378/exe.1903CrossRefGoogle Scholar
Rose, PE, Nash, SM and Riley, LM 2017a Moving forward with zoo welfare assessment: A response to Cooke (2017). Journal of Veterinary Behavior: Clinical Applications and Research 22: 75–77. https://doi.org/10.1016/j.jveb.2017.11.001CrossRefGoogle Scholar
Rose, PE, Nash, SM and Riley, LM 2017b To pace or not to pace? A review of what abnormal repetitive behavior tells us about zoo animal management. Journal of Veterinary Behavior: Clinical Applications and Research 20: 11–21. https://doi.org/10.1016/j.jveb.2017.02.007CrossRefGoogle Scholar
Rose, P and O’Brien, M 2020 Welfare assessment for captive Anseriformes: A guide for practitioners and animal keepers. Animals 10: 1132–1139. https://doi.org/10.3390/ani10071132CrossRefGoogle ScholarPubMed
Rosenthal, MF, Gertler, M, Hamilton, AD, Prasad, S and Andrade, MC 2017 Taxonomic bias in animal behaviour publications. Animal Behaviour 127: 83–89. https://doi.org/10.1016/j.anbe-hav.2017.02.017CrossRefGoogle Scholar
Schmitt, V 2018 Implementing new portable touchscreen-setups to enhance cognitive research and enrich zoo-housed animals. BioRxiv 31: 1–21. https://doi.org/10.1101/316042Google Scholar
Shape of Enrichment, Inc 2020 The Shape of Enrichment. https://theshapeofenrichmentinc.wildapricot.org/Google Scholar
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.20091CrossRefGoogle Scholar
Stanton, LA, Sullivan, MS and Fazio, JM 2015 A standardized ethogram for the felidae: A tool for behavioral researchers. Applied Animal Behaviour Science 173: 3–16. https://doi.org/10.1016/j.applanim.2015.04.001CrossRefGoogle Scholar
Stoinski, TS, Daniel, E and Maple, TL 2000 A preliminary study of the behavioral effects of feeding enrichment on African ele-phants. Zoo Biology 19: 485–493. https://doi.org/10.1002/1098-2361(2000)19:6<485::AID-ZOO1>3.0.CO;2-53.0.CO;2-5>CrossRefGoogle Scholar
Swaisgood, RR and Shepherdson, DJ 2005 Scientific approach-es to enrichment and stereotypies in zoo animals: what's been done and where should we go next? Zoo Biology 24: 499–518. https://doi.org/10.1002/zoo.20066CrossRefGoogle Scholar
Tahamtan, I, Afshar, AS and Ahamdzadeh, K 2016 Factors affecting number of citations: a comprehensive review of the liter-ature. Scientometrics 107: 1195–1225. https://doi.org/10.1007/s11192-016-1889-2CrossRefGoogle Scholar
Therrien, CL, Gaster, L, Cunningham-Smith, P and Manire, CA 2007 Experimental evaluation of environmental enrichment of sea turtles. Zoo Biology 26: 407–416. https://doi.org/10.1002/zoo.20145CrossRefGoogle Scholar
Traylor-Holzer, K, Leus, K and Bauman, K 2019 Integrated collection assessment and planning (ICAP) workshop: helping zoos move toward the One Plan Approach. Zoo Biology 38: 95–105. https://doi.org/10.1002/zoo.21478CrossRefGoogle ScholarPubMed
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
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
Wild Welfare 2020 Wild Welfare. https://wildwelfare.org/Google Scholar
Williams, I, Hoppitt, W and Grant, R 2017 The effect of audi-tory enrichment, rearing method and social environment on the behavior of zoo-housed psittacines (Aves: Psittaciformes); implications for welfare. Applied Animal Behaviour Science 186: 85–92. https://doi.org/10.1016/j.applanim.2016.10.013CrossRefGoogle Scholar
Wooddell, LJ, Beisner, B, Hannibal, DL, Nathman, AC and McCowan, B 2019 Increased produce enrichment reduces trau-ma in socially housed captive rhesus macaques (Macaca mulatta). American Journal of Primatology 81: e23073. https://doi.org/10.1002/ajp.23073CrossRefGoogle 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
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