The Evolution of Zoos as Conservation Institutions: A Summary of the Transition from Menageries to Zoological Gardens and Parallel Improvement of Mammalian Welfare Management
Abstract
:1. Introduction
- Relevance: Information was included from scholarly articles, books, and reputable online sources that provided insight on the long transformation of the role that zoos fulfill in species conservation. We were particularly interested in the emergence of science-backed approaches to animal welfare management and their contribution to the ex situ components of conservation.
- Credibility: The scientific information described in this review is from studies that utilized sound methodology, were produced by experts in the field, and were available via reputable publishers and associations.
- Timeliness: For discussions of modern components, the most up-to-date information from the latest research was incorporated, along with seminal work and historical information, to capture the evolution of the zoo mission and welfare management.
- Diversity: The sources included represent diverse perspectives and interpretations of the subjects. This includes information produced from widely differing geographical regions, time periods, and cultures, as well as information produced across species and captive environments.
2. Historical Evolution of Zoos
2.1. Pre-Modern Animal Collections
2.2. The Rise of the Modern Zoo
2.3. Contemporary Innovations in Zoo Strategies
3. The Mission of Modern Zoos
3.1. Species Conservation
Not Evaluated | Data Deficient | Least Concern |
Near Threatened | Vulnerable | Endangered |
Critically Endangered | Extinct in the Wild | Extinct |
3.2. Leveraging Recreation to Facilitate Education
3.3. Performing Research to Enable Education
3.4. Research Leading to Better Welfare
4. Advancements in Zoo Animal Welfare
4.1. Accurately Assessing Welfare Status
4.2. The Role of Zoo Staff in Welfare Management
4.3. Environmental Enrichment
4.3.1. The Impact of Enriched Environments on Zoo Animal Welfare
4.3.2. Effective Environmental Enrichment Approaches
5. Opportunities for Continued Improvements in Welfare Management
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Roe, K.; McConney, A.; Mansfield, C.F. The Role of Zoos in Modern Society—A Comparison of Zoos’ Reported Priorities and What Visitors Believe They Should Be. Anthrozoös 2015, 27, 529–541. [Google Scholar] [CrossRef]
- Kisling, V.N.J. Zoo and Aquarium History: Ancient Animal Collections to Zoological Gardens; CRC Press: Boca Raton, FL, USA, 2000. [Google Scholar]
- Barber, J.C. Programmatic approaches to assessing and improving animal welfare in zoos and aquariums. Zoo Biol. 2009, 28, 519–530. [Google Scholar] [CrossRef]
- Bacon, H. Behaviour-Based Husbandry-A Holistic Approach to the Management of Abnormal Repetitive Behaviors. Animals 2018, 8, 103. [Google Scholar] [CrossRef] [PubMed]
- Rose, P.; Riley, L. The use of Qualitative Behavioural Assessment in zoo welfare measurement and animal husbandry change. J. Zoo Aquar. Res. 2018, 7, 150–161. [Google Scholar] [CrossRef]
- Diana, A.; Salas, M.; Pereboom, Z.; Mendl, M.; Norton, T. A Systematic Review of the Use of Technology to Monitor Welfare in Zoo Animals: Is There Space for Improvement? Animals 2021, 11, 3048. [Google Scholar] [CrossRef] [PubMed]
- Miller, L.J.; Vicino, G.A.; Sheftel, J.; Lauderdale, L.K. Behavioral Diversity as a Potential Indicator of Positive Animal Welfare. Animals 2020, 10, 1211. [Google Scholar] [CrossRef]
- Tallo-Parra, O.; Salas, M.; Manteca, X. Zoo Animal Welfare Assessment: Where Do We Stand? Animals 2023, 13, 1966. [Google Scholar] [CrossRef]
- Jordan, B. Science-based assessment of animal welfare: Wild and captive animals. Rev. Sci. Tech. 2005, 24, 515–528. [Google Scholar] [CrossRef]
- Mendl, M.; Burman, O.H.; Paul, E.S. An integrative and functional framework for the study of animal emotion and mood. Proc. Biol. Sci. 2010, 277, 2895–2904. [Google Scholar] [CrossRef]
- Jones, N.; Sherwen, S.L.; Robbins, R.; McLelland, D.J.; Whittaker, A.L. Welfare Assessment Tools in Zoos: From Theory to Practice. Vet. Sci. 2022, 9, 170. [Google Scholar] [CrossRef]
- Melfi, V.A. There are big gaps in our knowledge, and thus approach, to zoo animal welfare: A case for evidence-based zoo animal management. Zoo Biol. 2009, 28, 574–588. [Google Scholar] [CrossRef] [PubMed]
- Quirke, T.; O’Riordan, R.M. The effect of a randomised enrichment treatment schedule on the behaviour of cheetahs (Acinonyx jubatus). Appl. Anim. Behav. Sci. 2011, 135, 103–109. [Google Scholar] [CrossRef]
- Foster, K.P. The earliest zoos and gardens. Sci. Am. 1999, 281, 64–71. [Google Scholar] [CrossRef]
- Bostock, S.S.C. Zoos and Animal Rights: The Ethics of Keeping Animals; Taylor & Francis Group: London, UK, 1993; p. 1789. [Google Scholar]
- Hancocks, D. A Different Nature: The Paradoxical World of Zoos and Their Uncertain Future; University of California Press: Berkeley, CA, USA, 2001. [Google Scholar]
- Baratay, E.; Hardouin-Fugier, E. Zoo: A History of Zoological Gardens in the West; Reaktion Books: London, UK, 2002; p. 400. [Google Scholar]
- Parker, M. The genealogy of the zoo: Collection, park and carnival. Organization 2020, 28, 604–620. [Google Scholar] [CrossRef]
- Kallipoliti, L. Evolution of the Zoo. An Overview of Significant Zoological Developments Spanning from Biblical Times through to Contemporary Proprosals. Wordpress Terra Incogn. 2014, 6, 1–26. [Google Scholar]
- Dölek-Sever, D. Captive wild animals as visual commodities in the Ottoman Empire: A historical review. Middle East. Stud. 2023, 59, 1–17. [Google Scholar] [CrossRef]
- Rabb, G.B. The evolution of zoos from menageries to centers of conservation and caring. Curator Mus. J. 2004, 47, 237–246. [Google Scholar] [CrossRef]
- Coe, J.C. Towards a co-evolution of zoos, aquariums and natural history museums. In Proceedings of the Annual Conference Proceedings, American Association of Zoological Parks and Aquariums, Wheeling, WV, USA, 8–12 September 1985; pp. 366–376. [Google Scholar]
- Ryan, S. The Unorthodox Imagination in Late Medieval Britain; Cambridge University Press: Cambridge, UK, 2011; Volume 62, pp. 818–819. [Google Scholar]
- Graetz, M.J. The Role of Architectural Design in Promoting the Social Objectives of Zoos: A Study of Zoo Exhibit Design with Reference to Selected Exhibits in Singapore Zoological Gardens. Master’s Thesis, National University of Singapore, Singapore, 1996. [Google Scholar]
- Escobar-Ibarra, I.; Mota-Rojas, D.; Gual-Sill, F.; Sánchez, C.R.; Baschetto, F.; Alonso-Spilsbury, M. Conservation, animal behaviour, and human-animal relationship in zoos. Why is animal welfare so important? J. Anim. Behav. Biometeorol. 2021, 9, 2111. [Google Scholar] [CrossRef]
- Powell, D.M.; Watters, J.V. The Evolution of the Animal Welfare Movement in U.S. Zoos and Aquariums. Zool. Gart. 2017, 86, 219–234. [Google Scholar] [CrossRef]
- Hill, S.P.; Broom, D.M. Measuring zoo animal welfare: Theory and practice. Zoo Biol. 2009, 28, 531–544. [Google Scholar] [CrossRef]
- Maulana, R.; Gawi, J.M.; Utomo, S.W. Architectural design assessment of Javan leopard rehabilitation facility regarding the occurrence of stereotypical pacing. IOP Conf. Ser. Earth Environ. Sci. Bristol. 2020, 426, 12075. [Google Scholar] [CrossRef]
- Spooner, S.L.; Farnworth, M.J.; Ward, S.J.; Whitehouse-Tedd, K.M. Conservation education: Are zoo animals effective ambassadors and is there any cost to their welfare? J. Zool. Bot. Gard. 2021, 2, 41–65. [Google Scholar] [CrossRef]
- Hosey, G.; Melfi, V.; Pankhurst, S. Zoo Animals: Behaviour, Management, and Welfare; Oxford University Press: Oxford, UK, 2009; Volume 1, p. 659. [Google Scholar]
- Ito, T. London Zoo and the Victorians, 1828–1859, 2nd ed.; The Boydell Press: Woodbridge, UK, 2020; Volume 2, p. 216. [Google Scholar]
- Taplin, R.H. Competitive importance-performance analysis of an Australian wildlife park. Tour. Manag. 2012, 33, 29–37. [Google Scholar] [CrossRef]
- AZA. Association of Zoos & Aquariums. Available online: https://www.aza.org/ (accessed on 19 July 2022).
- Dick, G. WAZA History at a Glance; World Association of Zoos and Aquariums: Gland, Switzerland, 2015; pp. 2–5. [Google Scholar]
- Rodrigues, A.S.; Pilgrim, J.D.; Lamoreux, J.F.; Hoffmann, M.; Brooks, T.M. The value of the IUCN Red List for conservation. Trends Ecol. Evol. 2006, 21, 71–76. [Google Scholar] [CrossRef]
- Beausoleil, N.J.; Mellor, D.J.; Baker, L.; Baker, S.E.; Bellio, M.; Clarke, A.S.; Dale, A.; Garlick, S.; Jones, B.; Harvey, A.; et al. “Feelings and Fitness” Not “Feelings or Fitness”—The Raison d’etre of Conservation Welfare, Which Aligns Conservation and Animal Welfare Objectives. Front. Vet. Sci. 2018, 5, 296. [Google Scholar] [CrossRef]
- Hediger, H. Studies of the Psychology and Behavior of Captive Animals in Zoos and Circuses; Butterworths Scientific Publications: London, UK, 1955; p. 166. [Google Scholar]
- Rübel, A. Heini Hediger: Tierpsychologe, Tiergartenbiologe, Zoodirektor; Gelehrte Gesellschaft: Zürich, Switzerland, 2009. [Google Scholar]
- Miller, L.J.; Chinnadurai, S.K. Beyond the Five Freedoms: Animal Welfare at Modern Zoological Facilities. Animals 2023, 13, 1818. [Google Scholar] [CrossRef]
- Greenwell, P.J.; Riley, L.M.; Lemos de Figueiredo, R.; Brereton, J.E.; Mooney, A.; Rose, P.E. The Societal Value of the Modern Zoo: A Commentary on How Zoos Can Positively Impact on Human Populations Locally and Globally. J. Zool. Bot. Gard. 2023, 4, 53–69. [Google Scholar] [CrossRef]
- Rose, P.E.; Riley, L.M. Expanding the role of the future zoo: Wellbeing should become the fifth aim for modern zoos. Front. Psychol. 2022, 13, 1018722. [Google Scholar] [CrossRef]
- Buckley, K.A.; Smith, L.D.G.; Crook, D.A.; Pillans, R.D.; Kyne, P.M. Conservation impact scores identify shortfalls in demonstrating the benefits of threatened wildlife displays in zoos and aquaria. J. Sustain. Tour. 2020, 28, 978–1002. [Google Scholar] [CrossRef]
- Mace, G.M.; Collar, N.J.; Gaston, K.J.; Hilton-Taylor, C.; Akcakaya, H.R.; Leader-Williams, N.; Milner-Gulland, E.J.; Stuart, S.N. Quantification of extinction risk: IUCN’s system for classifying threatened species. Conserv. Biol. 2008, 22, 1424–1442. [Google Scholar] [CrossRef]
- Che-Castaldo, J.P.; Grow, S.A.; Faust, L.J. Evaluating the Contribution of North American Zoos and Aquariums to Endangered Species Recovery. Sci. Rep. 2018, 8, 9789. [Google Scholar] [CrossRef]
- Barongi, R.; Fisken, F.; Parker, M.; Gusset, M. Committing to Conservation: The World Zoo and Aquarium Conservation Strategy; WAZA Executive Office: Gland, Switzerland, 2015; Volume 6. [Google Scholar]
- WAZA. Building a Future for Wildlife—The World Zoo and Aquarium Conservation Strategy; WAZA Executive Office: Bern, Switzerland, 2005. [Google Scholar]
- Ballou, J.D.; Foose, T.J. Demographic and genetic management of captive populations. In Wild Mammals in Captivity; DG, K., Ed.; The University of Chicago Press: Chicago, IL, USA, 1996; pp. 263–283. [Google Scholar]
- Keulartz, J. Captivity for Conservation? Zoos at a Crossroads. J. Agric. Environ. Ethics 2015, 28, 335–351. [Google Scholar] [CrossRef]
- Miller, B.; Conway, W.; Reading, R.P.; Wemmer, C.; Wildt, D.; Kleiman, D.; Monfort, S.; Rabinowitz, A.; Armstrong, B.; Hutchins, M. Evaluating the Conservation Mission of Zoos, Aquariums, Botanical Gardens, and Natural History Museums. Conserv. Biol. 2004, 18, 86–93. [Google Scholar] [CrossRef]
- Whitham, J.C.; Wielebnowski, N. New directions for zoo animal welfare science. Appl. Anim. Behav. Sci. 2013, 147, 247–260. [Google Scholar] [CrossRef]
- Flesness, N. International Species Information System (ISIS): Over 25 years of compiling global animal data to facilitate collection and population management. Int. Zoo Yearb. 2003, 38, 53–61. [Google Scholar] [CrossRef]
- Mace, G.; Balmford, A.; Leader-Williams, N.; Manica, A.; Walter, O.; West, C.D.; Zimmerman, A. Measuring conservation success: Assessing zoos’ contributions. In Proceedings of the Catalysts for Conservation: A Direction for Zoos in the 21st Century, London, UK, 19–20 February 2004; pp. 322–342. [Google Scholar]
- Gusset, M.; Dick, G. ‘Building a Future for Wildlife’? Evaluating the contribution of the world zoo and aquarium community to in situ conservation. Int. Zoo Yearb. 2010, 44, 183–191. [Google Scholar] [CrossRef]
- Anderson, U.S.; Kelling, A.S.; Pressley-Keough, R.; Bloomsmith, M.A.; Maple, T.L. Enhancing the Zoo Visitor’s Experience by Public Animal Training and Oral Interpretation at an Otter Exhibit. Environ. Behav. 2016, 35, 826–841. [Google Scholar] [CrossRef]
- Brando, S.; Herrelko, E.S. Wild Animals in the City: Considering and Connecting with Animals in Zoos and Aquariums. In Animals in Our Midst: The Challenges of Co-Existing with Animals in the Anthropocene; The International Library of Environmental, Agricultural and Food Ethics; Springer International Publishing AG: Cham, Switzerland, 2021; Volume 33, pp. 341–360. [Google Scholar]
- Curtin, P.; Papworth, S. Increased information and marketing to specific individuals could shift conservation support to less popular species. Mar. Policy 2018, 88, 101–107. [Google Scholar] [CrossRef]
- Quirke, T.; O’Riordan, R.; Davenport, J. A comparative study of the speeds attained by captive cheetahs during the enrichment practice of the “cheetah run”. Zoo Biol. 2013, 32, 490–496. [Google Scholar] [CrossRef]
- Higgs, S.J.; Van Eck, E.; Heynis, K.; Braodberry, S.H. Humans as Enrichment: Human-Animal Interactions and the Perceived Benefit to the Cheetah (Acinonyx jubatus) Human and Zoological Establishment. Int. J. Biol. Life Agric. Sci. 2018, 11, 97–103. [Google Scholar] [CrossRef]
- Mellor, D.J. Updating Animal Welfare Thinking: Moving beyond the “Five Freedoms” towards “A Life Worth Living”. Animals 2016, 6, 21. [Google Scholar] [CrossRef] [PubMed]
- Carlstead, K.; Brown, J.L. Relationships between patterns of fecal corticoid excretion and behavior, reproduction, and environmental factors in captive black (Diceros bicornis) and white (Ceratotherium simum) rhinoceros. Zoo Biol. Publ. Affil. Am. Zoo Aquar. Assoc. 2005, 24, 215–232. [Google Scholar] [CrossRef]
- Mellor, D.J.; Beausoleil, N.J.; Littlewood, K.E.; McLean, A.N.; McGreevy, P.D.; Jones, B.; Wilkins, C. The 2020 Five Domains Model: Including Human-Animal Interactions in Assessments of Animal Welfare. Animals 2020, 10, 1870. [Google Scholar] [CrossRef] [PubMed]
- Greco, B.J.; Meehan, C.L.; Miller, L.J.; Shepherdson, D.J.; Morfeld, K.A.; Andrews, J.; Baker, A.M.; Carlstead, K.; Mench, J.A. Elephant Management in North American Zoos: Environmental Enrichment, Feeding, Exercise, and Training. PLoS ONE 2016, 11, e0152490. [Google Scholar] [CrossRef]
- Sherwen, S.L.; Hemsworth, L.M.; Beausoleil, N.J.; Embury, A.; Mellor, D.J. An Animal Welfare Risk Assessment Process for Zoos. Animals 2018, 8, 130. [Google Scholar] [CrossRef]
- Mellor, D.J.; Beausoleil, N.J. Extending the ‘Five Domains’ model for animal welfare assessment to incorporate positive welfare states. Anim. Welf. 2023, 24, 241–253. [Google Scholar] [CrossRef]
- Dickens, M.J.; Delehanty, D.J.; Michael Romero, L. Stress: An inevitable component of animal translocation. Biol. Conserv. 2010, 143, 1329–1341. [Google Scholar] [CrossRef]
- Spiezio, C.; Vaglio, S.; Scala, C.; Regaiolli, B. Does positive reinforcement training affect the behaviour and welfare of zoo animals? The case of the ring-tailed lemur (Lemur catta). Appl. Anim. Behav. Sci. 2017, 196, 91–99. [Google Scholar] [CrossRef]
- Edes, A.N.; Wolfe, B.A.; Crews, D.E. Evaluating Allostatic Load: A New Approach to Measuring Long-Term Stress in Wildlife. J. Zoo Wildl. Med. 2018, 49, 272–282. [Google Scholar] [CrossRef]
- McEwen, B.S. Stress, adaptation, and disease. Allostasis and allostatic load. Ann. N. Y. Acad Sci. 1998, 840, 33–44. [Google Scholar] [CrossRef]
- Quirke, T.; O’Riordan, R.M.; Zuur, A. Factors influencing the prevalence of stereotypical behaviour in captive cheetahs (Acinonyx jubatus). Appl. Anim. Behav. Sci. 2012, 142, 189–197. [Google Scholar] [CrossRef]
- Furlong, E.; Gaskill, B.; Erasmus, M. Exotic Feline Enrichment; Purdue University: Purdue, IN, USA, 2021; pp. 1–5. [Google Scholar]
- Skibiel, A.L.; Trevino, H.S.; Naugher, K. Comparison of several types of enrichment for captive felids. Zoo Biol. 2007, 26, 371–381. [Google Scholar] [CrossRef] [PubMed]
- Sena, M.V.d.A.; Santos, G.d.S.; Oliveira, M.A.B.d. Strategies of Environmental Enrichment for ocelot Leopardus pardalis (Carnivora, Felidae) at Parque Estadual Dois Irmãos: A study case in Brazil. Rev. Bras. Zoociências 2018, 19, 35–46. [Google Scholar] [CrossRef]
- Mason, G.; Rushen, J. Stereotypic Animal Behaviour Fundamentals and Applications to Welfare, 2nd ed.; CAB International: Wallingford, UK, 2006. [Google Scholar]
- Coe, J.; Hoy, J. Choice, Control and Computers: Empowering Wildlife in Human Care. Multimodal Technol. Interact. 2020, 4, 92. [Google Scholar] [CrossRef]
- Carlstead, K. A comparative approach to the study of Keeper-Animal Relationships in the zoo. Zoo Biol. 2009, 28, 589–608. [Google Scholar] [CrossRef]
- Fernandez, E.J. Training as Enrichment: A Critical Review. Anim. Welf. 2022, 31, 1–12. [Google Scholar] [CrossRef]
- Skinner, B.F. The Behavior of Organisms; D. Appleton-Century Company: New York, NY, USA, 1938. [Google Scholar]
- Crowell-Davis, S.L. Use of operant conditioning to facilitate examination of zoo animals. Compend. Contin. Educ. Vet. 2008, 30, 218–219. [Google Scholar]
- Daffin, L.W. Principles of Learning and Behavior, 2nd ed.; Washington State University: Pullman, WA, USA, 2021; p. 397. [Google Scholar]
- Lithner, J. On the Hunt for Improvements-Possibilities of Increasing Welfare in Captive Cheetahs through Hunting Enrichment. Ph.D. Thesis, Sveriges lantbruksuniversitet (Swedish University of Agricultural Sciences), Uppsala, Sweden, 2014. [Google Scholar]
- Damasceno, J.; Genaro, G.; Quirke, T.; McCarthy, S.; McKeown, S.; O’Riordan, R. The effects of intrinsic enrichment on captive felids. Zoo Biol. 2017, 36, 186–192. [Google Scholar] [CrossRef]
- Hoy, J.M.; Murray, P.J.; Tribe, A. Thirty years later: Enrichment practices for captive mammals. Zoo Biol. 2010, 29, 303–316. [Google Scholar] [CrossRef]
- Fischer Meinert, R.; Pitlovanciv, A.K.; Marenzi, R.C.; Silva Barreto, A. Behavioral Evaluation of Herpailurus yagouaroundi (E. Geoffroy Saint-Hilaire, 1803) in Response to Environmental Enrichment. J. Appl. Anim. Welf. Sci. 2021, 24, 149–158. [Google Scholar] [CrossRef]
- Ellis, S.L. Environmental enrichment: Practical strategies for improving feline welfare. J. Feline Med. Surg. 2009, 11, 901–912. [Google Scholar] [CrossRef] [PubMed]
- Makecha, R.N.; Highfill, L.E. Environmental Enrichment, Marine Mammals, and Animal Welfare: A Brief Review. Aquat. Mamm. 2018, 44, 221–230. [Google Scholar] [CrossRef]
- Cannon, T.H.; Heistermann, M.; Hankison, S.J.; Hockings, K.J.; McLennan, M.R. Tailored Enrichment Strategies and Stereotypic Behavior in Captive Individually Housed Macaques (Macaca spp.). J. Appl. Anim. Welf. Sci. 2016, 19, 171–182. [Google Scholar] [CrossRef] [PubMed]
- Regaiolli, B.; Rizzo, A.; Ottolini, G.; Miletto Petrazzini, M.E.; Spiezio, C.; Agrillo, C. Motion Illusions as Environmental Enrichment for Zoo Animals: A Preliminary Investigation on Lions (Panthera leo). Front. Psychol. 2019, 10, 2220. [Google Scholar] [CrossRef] [PubMed]
- Machado, J.C.; Genaro, G. Influence of olfactory enrichment on the exploratory behaviour of captive-housed domestic cats. Aust. Vet. J. 2014, 92, 492–498. [Google Scholar] [CrossRef]
- Berman, G.J.; Choi, D.M.; Bialek, W.; Shaevitz, J.W. Mapping the stereotyped behaviour of freely moving fruit flies. J. R. Soc. Interface 2014, 11, 20140672. [Google Scholar] [CrossRef]
- Schmidt, T.B.; Lancaster, J.M.; Psota, E.; Mote, B.E.; Hulbert, L.E.; Holliday, A.; Woiwode, R.; Pérez, L.C. Evaluation of a novel computer vision-based livestock monitoring system to identify and track specific behaviors of individual nursery pigs within a group-housed environment. Transl. Anim. Sci. 2022, 6, txac082. [Google Scholar] [CrossRef]
- Rangel, M.; Júnior, N.D.S. Environmental food and cognitive enrichment: A study of well-being for large captive felids at the Zoo of Goiânia. Sci. Rep. 2021. [Google Scholar] [CrossRef]
- Ogura, T. Contrafreeloading and the value of control over visual stimuli in Japanese macaques (Macaca fuscata). Anim. Cogn. 2011, 14, 427–431. [Google Scholar] [CrossRef]
- Frederick, M.J.; Cocuzzo, S.E. Contrafreeloading in Rats Is Adaptive and Flexible: Support for an Animal Model of Compulsive Checking. Evol. Psychol. 2017, 15, 147470491773593. [Google Scholar] [CrossRef]
- Markowitz, H.; LaForse, S. Artificial prey as behavioral enrichment devices for felines. Appl. Anim. Behav. Sci. 1987, 18, 31–43. [Google Scholar] [CrossRef]
- Markowitz, H.; Aday, C.; Gavazzi, A. Effectiveness of acoustic “prey”: Environmental enrichment for a captive African leopard (Panthera pardus). Zoo Biol. 1995, 14, 371–379. [Google Scholar] [CrossRef]
- Bashaw, M.J.; Bloomsmith, M.A.; Marr, M.; Maple, T.L. To hunt or not to hunt? A feeding enrichment experiment with captive large felids. Zoo Biol. Publ. Affil. Am. Zoo Aquar. Assoc. 2003, 22, 189–198. [Google Scholar] [CrossRef]
- Beer, H.N. Continuous Video Monitoring of Zoo Cheetahs Demonstrates Differential Engagement Patterns for Six Different Types of Environmental Enrichment; Placental Insufficiency Indicators Improve in Intrauterine Growth-Restricted Fetal Sheep Receiving Daily ω-3 Polyunsaturated Fatty Acid Infusions; Investigation of Differentially Expressed Transcripts of the Adipose Tissue in Fetal and Neonatal IUGR Sheep. Ph.D. Thesis, The University of Nebraska-Lincoln, Lincoln, NE, USA, 2022. [Google Scholar]
- Barcellos, H.H.A.; Koakoski, G.; Chaulet, F.; Kirsten, K.S.; Kreutz, L.C.; Kalueff, A.V.; Barcellos, L.J.G. The effects of auditory enrichment on zebrafish behavior and physiology. PeerJ 2018, 6, e5162. [Google Scholar] [CrossRef]
- Maple, T.L.; Segura, V.D. Advancing Behavior Analysis in Zoos and Aquariums. Behav. Anal. 2015, 38, 77–91. [Google Scholar] [CrossRef] [PubMed]
- Cole, J.; Fraser, D. Zoo Animal Welfare: The Human Dimension. J. Appl. Anim. Welf. Sci. 2018, 21, 49–58. [Google Scholar] [CrossRef] [PubMed]
- Rodrigues, S.M.; LeDoux, J.E.; Sapolsky, R.M. The influence of stress hormones on fear circuitry. Annu. Rev. Neurosci. 2009, 32, 289–313. [Google Scholar] [CrossRef]
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Beer, H.N.; Shrader, T.C.; Schmidt, T.B.; Yates, D.T. The Evolution of Zoos as Conservation Institutions: A Summary of the Transition from Menageries to Zoological Gardens and Parallel Improvement of Mammalian Welfare Management. J. Zool. Bot. Gard. 2023, 4, 648-664. https://doi.org/10.3390/jzbg4040046
Beer HN, Shrader TC, Schmidt TB, Yates DT. The Evolution of Zoos as Conservation Institutions: A Summary of the Transition from Menageries to Zoological Gardens and Parallel Improvement of Mammalian Welfare Management. Journal of Zoological and Botanical Gardens. 2023; 4(4):648-664. https://doi.org/10.3390/jzbg4040046
Chicago/Turabian StyleBeer, Haley N., Trenton C. Shrader, Ty B. Schmidt, and Dustin T. Yates. 2023. "The Evolution of Zoos as Conservation Institutions: A Summary of the Transition from Menageries to Zoological Gardens and Parallel Improvement of Mammalian Welfare Management" Journal of Zoological and Botanical Gardens 4, no. 4: 648-664. https://doi.org/10.3390/jzbg4040046