Conservation, animal behaviour, and human-animal relationship in zoos. Why is animal welfare so important?
Isabel Escobar-Ibarra, Daniel Mota-Rojas, Fernando Gual-Sill, Carlos R. Sánchez, Fidel Baschetto, María Alonso-Spilsbury
Abstract
Although zoos are committed to wildlife conservation and have a long-term positive impact on visitors’ attitudes towards wildlife, the question of whether maintaining wild animals in human care is justified remains as animal welfare concerns grow and human understanding of animal intelligence and capacities broadens. Zoos have always been the subject of debate, with conflicts between those who argue they save endangered species and educate visitors, and animal rights activists who believe that conditions of wild animals are inadequate and that zoos should not exist. In this review, we do not discuss the moral side of the issue, but the scientific one. This manuscript aims to show the scope of literature available on the strengths and weaknesses of modern zoos regarding wild animal welfare. We provide information useful to argue why zoos are important in modern society and factors that influence welfare are examined. Some potentially stressful stimuli may diminish animal welfare in zoo animals, while some of the benefits zoos offer to conservation and science include the opportunity to study and learn about different aspects necessary to improve management practices; the possibility of breeding wild animals in zoos has been a key factor in the recovery of species that have improved their conservation status. Animal welfare is an essential part of wildlife conservation, so efforts should be directed to ensure the best possible quality of life and optimum conditions of all zoo animals in our care.
Keywords
References
Altman JD (1998) Animal activity and visitor learning at the zoo. Anthrozoos 11:2-21.
Amrein M, Heistermann M, Weingrill T (2014) The effect of fission-fusion zoo housing on hormonal and behavioral indicators of stress in Bornean orangutans (Pongo pygmaeus). International Journal of Primatology 35:509-28.
Arias BF (2011) Animal welfare, a bioethical principle to consider in wildlife conservation in zoos. In: Escobar TJ (ed) Proposals and Reflections to Support Bioethics Education. Colección Bios y Ethos. Editorial del Bosque, Bogota, pp 235-63.
Arlettaz R, Schaub M, Fournier J, Reichlin TS, Sierro A, Watson JEM, Braunisch V (2010) From publications to public actions: When conservation biologists bridge the gap between research and implementation. BioScience 60:835–842.
Baker K (2004) Benefits of positive human interaction for socially housed chimpanzees. Animal Welfare 13:239-45.
Barber J, Lewis D, Agoramoorthy G, Stevenson MF (2010) Setting standards for evaluation of captive facilities. In: Kleiman D, Thompson K, Baer K (eds) Wild Mammals in Captivity: Principles and Techniques for Zoo Management 2nd ed. University of Chicago Press, Chicago, pp 22-34.
Barja I, Silván G, Illera JC (2008) Relationships between sex and stress hormone levels in feces and marking behavior in a wild population of Iberian wolves (Canis lupus signatus). Journal of Chemical Ecology 34:697-701.
Barongi R, Fisken FA, Parker M, Gusset M (2015) Committing to Conservation: The World Zoo and Aquarium Conservation Strategy. Gland: WAZA Executive Office. WAZA, USA.
Baschetto F (2019) Zoos: society and paradigms. In: Fernandez C (ed) Embassies of Nature. Zoos, Aquariums and Oceanariums of Argentina in the 21st Century. Vazquez Mazzini Editores, Buenos Aires, pp 23– 71.
Bechert US, Brown JL, Dierenfeld ES, Ling PD, Molter CM, Schulte BA (2019) Zoo elephant research: contirbutions to conservation of captive and free-ranging species. International Zoo Yearbook 53:1-27.
Bekoff M (2013) Ignoring Nature no More: The Case for Compassionate Conservation. University of Chicago Press, USA.
Bertschinger HJ, Meltzer DGA, van Dyk A (2008) Captive breeding of cheetahs in South Africa: 30 years of data from the de Wildt cheetah and wildlife centre. Reproduction in Domestic Animals 43 (Suppl):66-73.
Bonnie KE, Ang MYL, Ross SR (2016) Effects of crowd size on exhibit use by and behavior of chimpanzees (Pan troglodytes) and Western lowland gorillas (Gorilla gorilla) at a zoo. Applied Animal Behaviour Science 178:102-10.
Boppre M, Vane-Wright RI (2019) Welfare Dilemmas Created by Keeping Insects in Captivity. In: Carere C, Mather J (eds) The Welfare of Invertebrate Animals. Springer Nature, Switzerland, pp 23-67.
Brando S, Broom DM, Acasuso-Rivero C, Clark F (2018) Optimal marine mammal welfare under human care: Current efforts and future directions. Behavioural Processes 156:16-36.
Breton G, Barrot S (2014) Influence of enclosure size on the distances covered and paced by captive tigers (Panthera tigris). Applied Animal Behaviour Science 154:66-75.
Broom DM (1983) Stereotypies as animal welfare indicators. Current Topics in Veterinary Medicine and Animal Science 23:81-87.
Brummer SP, Gese EM, Shivik JA (2010) The effect of enclosure type on the behavior and heart rate of captive coyotes. Applied Animal Behaviour Science 125:171-80.
Byers O, Lees C, Wicken J, Schwitzer C (2013) The One Plan Approach: The Philosophy and Implementation of CBSG’s Approach to Integrated Species Conservation Planning. WAZA Magazine, Towards Integrated Species Conservation 14: 2-5.
Carder G, Semple S (2008) Visitor effects on anxiety in two captive groups of western lowland gorillas. Applied Animal Behaviour Science 115:211-20.
Carlstead K, Brown JL (2005) Relationships between patterns of feacal corticoid excretion and behavior, reproduction, and environmental factors in captive black (Diceros bicornis) and white (Ceratotherium simum) rhinoceros. Zoo Biology 24:215-32.
Carlstead K, Mench JA, Meehan C, Brown JL (2013) An epidemiological approach to welfare research in zoos: The elephant welfare project. Journal of Applied Animal Welfare Science 16:319-37.
Chamove AS, Hosey G, Schaetzel P (1988) Visitors excite primates in zoos. Zoo Biology 7:359-69.
Chelluri GI, Ross SR, Wagner KE (2013) Behavioral correlates and welfare implications of informal interactions between caretakers and zoo-housed chimpanzees and gorillas. Applied Animal Behaviour Science 147:306-15.
Chosy J, Wilson M, Santymire R (2014) Behavioral and physiological responses in felids to exhibit construction. Zoo Biology 33:267-74.
Claxton AM (2011) The potential of the human-animal relationship as an environmental enrichment for the welfare of zoo-housed animals. Applied Animal Behaviour Science 133:1-10.
Clayton S (2016) Learning to care about animal conservation. Center for Humans and Nature, Expanding our Natural & Civic Imagination. https://www.humansandnature.org/learning-to-care-about-animal-conservation. Accessed on: February 15, 2016.
Clubb R, Mason G (2007) Natural behavioural biology as a risk factor in carnivore welfare: how analysing species differences could help zoos improve enclosures. Applied Animal Behaviour Science 102:303-28.
Clubb R, Mason, G (2003) Captivity effects on wide-raging carnivores. Nature 425:473-474.
Coe J, Dykstra G (2010) New and sustainable directions in zoo exhibit design. In: Kleiman D, Thompson K, Baer K (eds) Wild Mammals in Captivity: Principles and Techniques for Zoo Management 2nd ed. University of Chicago Press, Chicago, pp 202-215.
Conde DA, Flesness N, Colchero F, Jones OR, Scheuerlein AA (2011) An emerging role of zoos to conserve biodiversity. Science 331:1390-1391.
Conway WG (1976) The surplus problem. In Wheeling WV (ed) AAZPA National Conference. American Association of Zoological Parks and Aquariums, pp 20–24.
Crockett C (1996) Data collection in the zoo setting, emphasizing behavior. In: Harris H, Kleiman D, Allen M, Thompson K, Lumpkin S (eds) Wild Mammals in Captivity. The University of Chicago Press, Chicago, pp 545-65.
Crockford C, Wittig RM, Whitten PL, Seyfarth RA, Cheney DL (2008) Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Hormones and Behavior 53:254-65.
Davey G (2007) Public perceptions in urban China towards zoos and their animal welfare. Human Dimensions of Wildlife 12:367-74.
Dawkins MS (2003). Behaviour as a tool in the assessment of animal welfare. Zoology 106:383-87.
de Azevedo CS, Lima MF, da Silva VC, Young RJ, Rodrigues M (2012) Visitor influence on the behavior of captive greater rheas (Rhea americana, Rheidae Aves). Journal of Applied Animal Welfare Science 15:113-25.
Descovich KA, Lisle AT, Johnston S, Phillips CJC (2012) Space allowance and the behaviour of captive southern hairy-nosed wombats (Lasiorhinus latifrons). Applied Animal Behaviour Science 140:92-98.
Durant SM (2000) Predator avoidance, breeding experience and reproductive success in endangered cheetahs, Acinonyx jubatus. Animal Behaviour 60:121-30.
Eltorai AEM, Sussman RW (2010) The visitor effect and captive black-tailed prairie dog behavior. Zoologische Garten 79:109-20.
Escobar-Ibarra I, Mayagoitia-Novales L, Alcántara-Barrera A, Cerda-Molina AL, Mondragón-Ceballos R, Ramírez-Necoechea R, Alonso-Spilsbury M (2017) Long-term quantification of faecal glucocorticoid metabolite concentrations reveals that Mexican gray wolves may habituate to captivity. The European Zoological Journal 84:311-20.
Falk JH (2005) Free‐choice environmental learning: framing the discussion. Environmental Education Research 11:265-80.
Fernández-Juricic E, Schulte BA (2016) Conservation behavior: continued application, development and expansion. Animal Behaviour 120:195-96.
Fox MW (1968) Abnormal behavior in animals. Philadelphia, USA
Garner JP (2005) Stereotypies and other abnormal repetitive behaviours: potential impact on viability reliability, and replicability of scientific outcomes. Institute for Laboratory Animal Research Journal 42:106-17.
Gillespie TH (1934) Is it cruel? A study of the condition of captive and performing animals. Herbert Jenkins, London.
Gold KC, Maple TL (1994) Personality assessment in the gorilla and its utility as a management tool. Zoo Biology 13:509-22.
Goswami S, Tyagi PC, Malik PK, Pandit SJ, Kadivar RF, Fitzpatrick M, Mondol S (2020) Effects of personality and rearing-history on the welfare of captive Asiatic lions (Panthera leo persica). PeerJournal 8:e8425.
Grand AP, Kuhar CW, Leighty KA, Bettinger TL, Laudenslager ML (2012) Using personality ratings and cortisol to characterize individual differences in African Elephants (Loxodonta africana). Applied Animal Behaviour Science 142: 69-75.
Gray J (2017) Zoo Ethics. The Challenges of Compassionate Conservation. CSIRO Publishing. Clayton South, Australia.
Gray J (2018) Challenges of compassionate conservation. Journal of Applied Animal Welfare Science 21(Sppl):34-42.
Gross M (2012) Felids fighting for survival. Current Biology 22:R993-R895.
Gusset M, Dick G (2012) Editorial. Fighting extinction. World Association of Zoos and Aquariums Magazine 13:1–2.
Heintz MR, Fuller G, Allard S (2019) Exploratory Investigation of Infrared Thermography for Measuring Gorilla Emotional Responses to Interactions with Familiar Humans. Animals 9:604.
Hoffmann M, Hilton-Taylor C, Angulo A, Böhm M, Brooks TM, Butchart SHM (2010) The Impact of Conservation on the Status of the World’s Vertebrates. Science 330:1503–1509.
Hogan LA, Johnston, SD, Lisle TA, Keeley T, Wong P, Nicolson V, Horsup AB, Janssen T (2011) Behavioural and physiological responses of captive wombats (Lasiorhinus latifrons) to regular handling by humans. Applied Animal Behaviour Science 134:217-28.
Hogan LA, Lisle AT, Johnston SD, Robertson H (2012) Non-invasive assessment of stress in captive numbats, Myrmecobius fasciatus (Mammalia: Marsupialia), using faecal cortisol measurement. General and Comparative Endocrinology 179:376-83.
Hopper L (2017) Cognitive research in zoos. Current Opinion in Behavioral Sciences 16:100-110.
Horback KM, Miller LJ, Andrews J, Kuczaj SA, Anderson M (2012) The effects of GPS collars on African elephant (Loxodonta africana) behavior at the San Diego Zoo Safari Park. Applied Animal Behaviour Science 142:76-81.
Hosey G (2000) Zoo animals and their audiences: what is the visitor effect? Animal Welfare 9:343-57.
Hosey G, Melfi V (2015) Are we ignoring neutral and negative human-animal relationships in zoos?. Zoo Biology 34:1-8.
Hosey GA (2008) Preliminary model of human-animal relationships in the zoo. Applied Animal Behaviour Science 109:105-27.
Hutchins M (2001) Conservation fieldwork. In: Bell CE (Ed) Encyclopedia of the World’s Zoos, Fitzroy Dearborn Publishers, Chicago, pp 299 – 303.
Hutchins M (2007) The animal rights – conservation debate: can zoos and aquariums play a role? In: Zimmermann A, Hatchwell M, Dickie L, West C (eds) Zoos in the 21st Century. Cambridge University Press, Cambridge, pp 92–109.
IUDZG/CBSG (IUCN/SSC) (1993) Executive Summary, The World Zoo Conservation Strategy; The Role of the Zoos and Aquaria of the World in Global Conservation, Chicago Zoological Society, USA.
Jackson DW (1990) Landscaping in hostile environments. International Zoo Yearkbook 29:10-15.
Kagan R, Allard S, Carter S (2018) What is the future for zoos and aquariums? Journal of Applied Animal Welfare Science 21(Suppl): 59-70.
Kagan R, Carter S, Allard S (2015) An universal welfare framework for zoos. Journal of Applied Animal Welfare Science 18:S1-S10.
Kagan R, Veasey J 2010 Challenges of zoo animal welfare. In: Kleiman D, Thompson K, Baer K (eds) Wild Mammals in Captivity: Principles and Techniques for Zoo Management, 2nd ed. University of Chicago Press, Chicago, pp 11-21.
Kalafut K, Kinley R (2020) Using radio frequency identification for behavioral monitoring in little blue penguins. Journal of Applied Animal Welfare Science 23:62-73.
Karanikola P, Tampakis S, Tsantopoulos G, Digbasani C (2014) The public zoo as recreation and environmental education area: Visitor's perceptions and management implications. WSEAS Transactions on Environment and Development 10:81-91.
Kelly KR, Harrison ML, Size DD, MacDonald, SE (2015) Individual effects of seasonal changes, visitor density, and concurrent bear behavior on stereotypical behaviors in captive polar bears (Ursus maritimus). Journal of Applied Animal Welfare Science 18:17-31.
Keulartz J (2015) Captivity for conservation? Zoos at a crossroads. Journal of Agricultural and Environmental Ethic 28:335-51.
Kneidinger N, Nagl A, Kiik K, Schwarzenberger F, Maran T (2018) The individual courtship behaviour of male European mink (Mustela lutreola) is a good indicator for their breeding success. Applied Animal Behaviour Science 205:98-106.
Kuar CW (2008) Group differences in captive gorillas’ reaction to large crowds. Applied Animal Behaviour Science 110:377-385
Kumar V, Reddy VP, Kokkiligadda A, Shivaji S, Umapathy G (2014) Non-invasive assessment of reproductive status and stress in captive Asian elephants in three south Indian zoos. General and Comparative Endocrinology 201:37-44.
Ladeia DLM, Young RJ (2015) Can enrichment make Brazilian tapir spend more time on view to the public?. Journal of Applied Animal Welfare Science 18:74-81.
Larsen MJ, Sherwen SL, Rault JL (2014) Number of nearby visitors and noise level affect vigilance in captive koalas. Applied Animal Behaviour Science 154:76-82.
Lascuráin M, List R, Barraza L, Díaz PE, Gual SF, Maunder M, Dorantes J, Luna VE (2009) Ex situ conservation. In: Capital Natural de México Vol. II. Estado de Conservación y Tendencias de Cambio. CONABIO, México, pp 517-44
Laule G, Desmond T (1998) Positive reinforcement training as an enrichment strategy. In: Shepherdson D, Mellen JD, Hutchins M (eds) Second Nature: Environmental Enrichment for Captive Animals. Smithsonian Institution Press, Washington, pp 302-13.
Lee HS (2015) Measurement of visitors' satisfaction with public zoos in Korea using importance-performance analysis. Tourism Management 47:251-60.
Lee PC, Moss CJ (2012) Wild female African elephants (Loxodonta africana) exhibit personality traits of leadership and social integrations. Journal of Comparative Psychology 126:224-32.
Less EH, Kuhar CW, Dennis PM, Lukas KE (2012) Assessing inactivity in zoo gorillas using keeper ratings and behavioral data. Applied Animal Behaviour Science 137:74-79.
Lewis K, Deskovich K, Jones M (2017) Enclosure utilisation and activity budgets of disabled Malayan sun bears (Helarctos malayanus). Behavioural Processes 145:65-72.
Li C, Juang Z, Tang S. Zeng Y (2007) Evidence of effects of human disturbance on alert response in Pere David´s deer (Elephurus davidaneus). Zoo Biology 26:461-70.
Lindblom E (2014) The effect of visual barriers, outdoor housing and feeding enrichment on the behaviour of drills (Mandrillus leucophaeus) at Parken Zoo. Master’s thesis, Linkőpings Universitet, Linkőping, Sweden.
List R (2005) Canis lupus. In: Ceballos G, Oliva G (eds) The Wild Mammals of Mexico. CONABIO-Fondo de Cultura Económica, México, pp 350-53
Loh TL, Larson ER, David SR, de Souza LS, Gericke R, Gryzbek M, Kough AS, Willink PW, Knapp CR (2018) Quantifying the contribution of zoos and aquariums to peer-reviewed scientific research. FACETS 3:287–299.
Lundin L (2013). Visitor effects on the behavior of drills (Mandrillus leucophaeus) and petting zoo animals at Parken Zoo. Master Thesis, Linkőpings Universitet. Linkőping, Sweden.
Majchrzak YN, Mastromonaco GF, Korver W, Burness G (2015) Use of salivary cortisol to evaluate the influence of rides in dromedary camels. General and Comparative Endocrinology 211:123-30.
Mallapur A, Chellam R (2002) Environmental influences on the activity budget of leopards (Panthera pardus) in four zoos in southern India. Journal of Applied Animal Welfare Science 5:111-24.
Mallapur A, Sinha A, Waran N (2005) Influence of visitor presence on the behaviour of captive lion-tailed macaques (Macaca silenus) housed in Indian zoos. Applied Animal Behaviour Science 94:341-52.
Maple TL, Bashaw MJ (2010) Research trends in zoos. In: Kleiman D, Thompson K, Baer K (eds) Wild Mammals in Captivity: Principles and Techniques for Zoo Management, 2nd ed. University of Chicago Press, Chicago, pp 288-300.
Margulis SW, Hoyos CH, Anderson M (2003) Effect of felid activity on zoo visitor interest. Zoo Biology 22:587-99.
Marzluff JM, Swift KN (2017) Connecting animal and human cognition to conservation. Current Opinion in Behavioral Sciences 16:87-92.
Mason GJ (1991) Stereotypies: a critical review. Animal Behaviour 41:1015-37.
Mason GJ (2010) Species differences in responses to captivity: stress, welfare and the comparative method. Trends Ecology Evolutions 25:718-21.
Mason GJ, Latham N (2004) Can’t stop, won’t stop: is stereotypy a reliable animal welfare indicator? Animal Welfare 13:S57-S69.
Mason GJ, Veasey JS (2010) How should the psychological well-being of zoo elephants be objectively investigated? Zoo Biology 29:237-55.
McGrath N, Walker J, Nilsson D, Phillips C (2013) Public attitudes towards grief in animals. Animal Welfare 22:33-47.
McKenzie S, Deane EM (2005) Faecal corticosteroid levels as an indicator of wellbeing in the tammar wallaby, Macropus eugenii. Comparative Biochemistry and Physiology-Part A 140:81-87.
McLeod KJ, Sheriff MJ, Ensminger DC, Owen DAS, Langkilde T (2018) Survival and reproductive costs of repeated acute glucocorticoid elevations in a captive, wild animal. General and Comparative Endocrinology 268:1-6.
Mcphee ME, Carlstead K (2010) The importance of maintaining natural behaviors in captive mammals. In: Kleiman D, Thompson K, Baer K (eds) Wild Mammals in Captivity: Principles and Techniques for Zoo Management 2nd ed. University of Chicago Press, Chicago, pp 303-13.
Meehan CL, Mench JA, Carlstead K, Hogan JN (2016) Determining connections between the daily lives of zoo elephants and their welfare: An epidemiological approach. PlosOne 11(7):e0158124.
Mellor D, Beausoleil N (2015) Extending the ‘five domains’ model for animal welfare assessment to incorporate positive welfare states. Animal Welfare 24:241-53.
Mellor DJ (2015) Enhancing animal welfare by creating opportunities for positive affective engagement. New Zealand Veterinary Journal 63:3-8.
Mellor DJ, Hunt S, Gusset M (2015) Caring for Wildlife: The World Zoo and Aquarium Animal Welfare Strategy. WAZA Executive Office, Gland.
Miller CS, Hebblewhite M, Petrunenko YK, Seryodkin IV, Goodrich JM, Miquelle DG (2014) Amur tiger (Panthera tigris altaica) energetic requirements: Implications for conserving wild tigers. Biological Conservation 170:120-29.
Miller L, Tobey JR 2012 Regurgitation and reingestion in bonobos (Pan paniscus): Relationships between abnormal and social behavior. Applied Animal Behaviour Science 141:65-70.
Miller LJ (2012) Visitor reaction to pacing behavior: Influence on the perception of animal care and interest in supporting zoological institutions. Zoo Biology 31:242-48.
Mohapatra RK, Panda S, Acharya UR (2014) Study on activity pattern and incidence of stereotypic behavior in captive tigers. Journal of Veterinary Behavior: Clinical Applications and Research 9:172–176.
Montaudouin S, Pape G (2004) Comparison of the behaviour of European brown bears (Ursus arctos arctos) in six different parks, with particular attention to stereotypies. Behavioural Processes 67(2):235-44.
Montenha JC, Silva SL, Boere, V (2009) Comparison of salivary cortisol concentrations in jaguars kept in captivity with differences in exposure to the public. Ciencia Rural 9:1745-51.
Mooney A, Conde DA, Healy K, Buckley YM (2020) A system wide approach to managing zoo collections for visitor attendance and in situ conservation. Nature Communications 11:584.
Moreira N, Brown JL, Moraes W, Swanson WF, Monteiro-Filho ELA (2007) Effect of housing and environmental enrichment on adrenocortical activity, behaviour and reproductive cyclicity in the female tigrina (Leopardus tigrinus) and margay (Leopardus wiedii). Zoo Biology 26:441-60.
Morgan KN, Tromborg CT (2007) Sources of stress in captivity. Applied Animal Behaviour Science 102:262-302.
Nygren NV, Ojalammi S (2018) Conservation education in zoos: A literature review. Finnish Journal for Human-Animal Studies 4:62-76.
O’Donovan D, Hindle JE, McKeown S, O’Donovan S (1993) Effect of visitors on the behaviour of female cheetahs. International Zoo Yearbook 32:238-44.
Owen C. (2004). Do visitors affect Asian short-clawed otter (Ambionyx cinerea) in a captive environment?. Proceedings 6th Annual Symposium on Zoo Research. UK, Edinburgh, pp 202-211.
Palmer C, Sandøe P (2016) How to care while conserving zoo animals. Center for Humans and Nature, Expanding our Natural & Civic Imagination. July 2016. https://www.humansandnature.org/how-to-care-while-conserving-zoo-animals. Accessed on: October 2, 2018.
Paquet PC, Darimont CT (2010) Wildlife conservation and animal welfare: two sides of the same coin? Animal Welfare 19:177-190.
Patel F, Wemelsfelder F, Ward SJ (2019) Using qualitative behaviour assessment to investigate human-animal relationships in zoo-housed giraffes (Giraffa camelopardalis). Animals 9:381.
Patel F, Whitehouse-Tedd K, Ward SJ (2019) Redefining human-animal relationships: An evaluation of methods to allow their empirical measurement in zoos. Animal Welfare 28:247-59.
Pearson EL, Lowry L, Dorrian J, Litchfield CA (2014) Evaluating the conservation impact of an innovative zoo‐based educational campaign: ‘Don't palm us off’ for orang‐utan conservation. Zoo Biology 33:184-96.
Phillips CJC, Tribe A, Lisle A, Galloway TK, Hansen K (2017) Keepers’ rating of emotions in captive big cats, and their use in determining responses to different types of enrichment. Journal of Veterinary Behavior 20:22-30.
Pifarre M, Valdez R, González-Rebeles C, Vázquez C, Romano M, Galindo F (2012) The effect of zoo visitors on the behaviour and faecal cortisol of the Mexican Wolf (Canis lupus baileyi). Applied Animal Behaviour Science 136:57-62.
Polanco A, Díez-León M, Mason G (2018) Stereotypic behaviours are heterogeneous in their triggers and treatments in the American mink, Neovison vison, a model carnivore. Animal Behaviour 141:105-14.
Pomerantz O, Meiri S, Terkel J (2013) Socio-ecological factors correlate with levels of stereotypic behavior in zoo-housed primates. Behavioural Processes 98:85-91.
Pomerantz O, Paukner A, Terkel J (2012) Some stereotypic behaviours in rhesus macaques (Macaca mulatta) are correlated with both perseveration and the ability to cope with acute stressors. Behavioural Brain Research 230:274-80.
Puan CL, Zakariz M (2007) Perception of visitors towards the role of zoos: a Malasyan perspective. International Zoo Yearbook 41:226-32.
Quadros S, Goulart VDL, Passos L, Vecci MAM, Young RJ (2014) Zoo visitor effect on mammal behaviour: Does noise matter? Applied Animal Behaviour Science 156:78-84.
Quirke T, O’Riordan RM, Zuur A (2012) Factors influencing the prevalence of stereotypical behaviour in captive cheetahs (Acinonyx jubatus). Applied Animal Behaviour Science 143:189-97.
Reade RS, Waran NK (1996) The modern zoo: How do people perceive zoo animals? Animal Welfare 47:109-18.
Riva HG, Zordan MA, Sanchez CR (2019) The Current State of Zoological Medicine in Zoos and Aquariums in Latin America. International Zoo Yearbook 54:1-17.
Robinson LM, Altschul DM, Wallace EK, Úbeda Y, Llorente M, Machanda Z, Slocombe KE, Leach MC, Waran NK Weiss A (2017) Chimpanzees with positive welfare are happier, extraverted, and emotionally stable. Applied Animal Behaviour Science 191:90-97.
Robson, C (2004) Do visitors and weather affect captive Asian elephant (Elephas maximus) behaviour?. Proceedings 6th Annual Symposium on Zoo Research. UK, Edinburgh.
Roe K, McConney A (2015) Do zoo visitors come to learn? An internationally comparative, mixed-methods study. Environmental Education Research 1:865-84.
Safina C (2018) Where are zoos going, or are they gone? Journal of Applied Animal Welfare Science 21:4-11.
Saunders SP, Harris T, Traylor-Holzer K, Beck KG (2014) Factors influencing breeding success, ovarian cyclicity, and cub survival in zoo-managed tigers (Panthera tigris). Animal Reproduction Science 144:38-47.
Schultz JT, Young JK (2018) Behavioral and spatial responses of captive coyotes to human activity. Applied Animal Behaviour Science 205:83-88.
Scientific American (2009) How do zoos help endangered animals?. April 2009. https://www.scientificamerican.com/article/how-do-zoos-help-endangered-animals/. Accessed on: February 10, 2019.
Scott K (2014) Behaviour and endocrinology of meerkats in zoos. Doctoral Thesis, University of Exeter, England.
Sellinger RL, Ha JC 2005 The effects of visitor density and intensity on the behaviour of two captive jaguars (Panthera onca). Journal of Applied Animal Welfare Science 8:233-44.
Shepherdson D (1998) Tracing the path of environmental enrichment in zoos. In: Shepherdson D, Mellen JD, Hutchins M (eds) Environmental Enrichment for Captive Animals. Smithsonian Institution Press,Washington, pp 1-12.
Shepherdson D (2010) Principles of and research on environmental enrichment for mammals. In: Kleiman D, Thompson K, Baer K (eds) Wild Mammals in Captivity: Principles and Techniques for Zoo Management 2nd ed. University of Chicago Press, Chicago, pp 62-67.
Shepherdson D, Lewis KD, Carlstead K, Bauman J, Perrin N (2013) Individual and environmental factors associated with stereotypic behavior and fecal glucocorticoid metabolite levels in zoo housed polar bears. Applied Animal Behaviour Science 147:268-77.
Sherwen S.L, Harvey TJ, Magrath MJ.L, Butler KL, Fanson KV, Hemsworth PH (2015) Effects of visual contact with zoo visitors on black-capped capuchin welfare Applied Animal Behaviour Science 167:65-73.
Sherwen SL, Hemsworth PH, Butler KL, Fanson KV, Magrath MJL (2015) Impacts of visitor number on kangaroos housed in free-range exhibits. Zoo Biology 34:287-95.
Sherwen SL, Magrath MJL, Butler KL. Hemsworth PH (2015b) Little penguins, Eudyptula minor, show increased avoidance aggression and vigilance in response to zoo visitors. Applied Animal Behaviour Science168:71-76.
Sherwen SL, Magrath, MJL, Butler KL, Phillips, CJ, Hemsworth PH (2014) A multi-enclosure study investigating the behavioural response of meerkats to zoo visitors. Applied Animal Behaviour Science 156:70-77.
Soriano AI, Vinyoles D, Maté C (2013) The influence of visitors on behavior and on the use of space in two species of ursids: a management question? International Zoo News 60:341-56.
Soriano AI, Vinyoles D, Maté C (2017) Abnormal behaviours in two captive brown bear (Ursus arctos Linnaeus, 1758) females: Individual differences and seasonal variations. Zoologische Garten 86:88-101.
Stevens JMG, Thyssen A, Laevens H, Vervaecke H (2013) The influence of zoo visitor numbers on the behaviour of harbour seals (Phoca vitulina). Journal Zoo and Aquarium Research 1:31-34.
Sutherland WJ, Pullin AS, Dolman PM, Knight TM (2004) The need for evidence-based conservation. Trends in Ecology & Evolution 19:305–308.
Tennant KS, Segura VD, Morris MC, Snyder KD, Bocian D, Maloney D, Maple TL (2018) Achieving optimal welfare for the Nile hippopotamus (Hippopotamus amphibius) in North American zoos and aquariums. Behavioural Processes 156:83-95.
Tetley CL. O’Hara SJ (2012) Ratings of animal personality as a tool for improving the breeding, management and welfare of zoo mammals. Animal Welfare 21:463-76.
Tribe A, Booth R (2003) Assessing the role of zoos in wildlife conservation. Human Dimensions of Wildlife 8:65-74.
van der Weyde LK, Martin GB, Paris MCJ (2016) Monitoring stress in captive and free-ranging African wild dogs (Lycaon pictus) using faecal glucocorticoid metabolites. General and Comparative Endocrinology 226:50-55.
Vaz J, Narayan EJ, Kumar RD, Thenmozh K, Thiyagesai K, Baskaran N (2017) Prevalence and determinants of stereotypic behaviours and physiological stress among tigers and leopards in Indian zoos. PlosOne 12(4):e0174711.
Wallace MP, Clark M, Vargas J, Porras MC (2007) Release of puppet-reared California condors in Baja California, Mexico: evaluation of a modified rearing technique. In: Mee A, Hall LS (eds) California Condors in the 21st Century, Series in Ornithology, No. 2. American Ornithologists Union Fayettevile Ark, USA, pp 227-242.
Warwick C, Frye FL, Murphy JB (2013) Health and Welfare of Captive Reptiles. Chapman & Hall, UK.
Weiss A, Adams MJ, King JE (2011) Happy orang-utans live longer lives. Biology Letters 7:872-74.
Weiss A, King JE, Perkins L (2006) Personality and subjective well-being in orangutans (Pongo pygmaeus and Pongo abelii). Journal of Personality and Social Psychology 90:501-11.
Wells DL (2005) A note on the influence of visitors on the behaviour and welfare of zoo-housed gorillas. Applied Animal Behaviour Science 93:13-17.
Whitham JC, Wielebnowski N (2009) Animal-based welfare monitoring: using keeper ratings as an assessment tool. Zoo Biology 28:545-60.
Whitham JC, Wielebnowski N (2013) New directions for zoo animal welfare science. Applied Animal Behaviour Science 147:247-60.
Wielebnowski N (2003) Stress and distress: evaluating their impact for the well-being of zoo animals. Journal of the American Veterinary Medical Association 223:973-77.
Wielebnowski NC, Fletchall N, Carlstead K, Busso JM, Brown JL (2002) Noninvasive assessment of adrenal activity associates with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biology 21:77-98.
Wolfe BA, Aguilar RF, Aguirre AA, Olsen GH, Blumer ES (2012) Sorta situ. The New Reality of Management Conditions for Wildlife Populations in the Absence of “Wild” Spaces. In: Aguirre AA, Ostfeld RS, Daszak P (eds) New Directions in Conservation Medicine. Applied Cases of Ecological Health. Oxford University Press, USA, pp 576-589.
Wolfensohn S, Shotton J, Bowley H, David S, Thompson S, Justice WSM (2018) Assessment of welfare in zoo animals: Towards optimum quality of life. Animals 8(110):doi:10.3390.
Wood W (1998) Interactions among environmental enrichment, viewing crowds, and zoo chimpanzees (Pan troglodytes). Zoo Biology 17:211-30.
World Association of Zoos and Aquariums (WAZA) (2005) Building a Future for Wildlife. The World zoo Conservation Strategy. World Aquaria and Zoos Association Executive Office, Switzerland.
World Association of Zoos and Aquariums (WAZA) (2016) Guidelines for the Use of Animals in Visitor Interactions. Switzerland WAZA: Executive Office. 2016. http://www.zoosafrica.com/about/projects.html. Accessed on June 28, 2018.
Yasuda H (2013) Negotiating entertainment and education: A zoo in Japan. International Journal of Culture, Tourism and Hospitality Research 7:105-12.
Yeates JW, Main DCJ (2008) Assessment of positive welfare: a review. The Veterinary Journal 175:293-300.
Yon L, Williams E, Harvey ND, Asher L (2019) Development of a behavioural welfare assessment tool for routine use with captive elephants. PLoS ONE 14(2):e0210783.
Young KM, Walker SL, Lanthier C, Waddell WJ, Monfort SL, Brown JL (2004) Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. General and Comparative Endocrinology 137:148-65.
Young RJ (2003) Environmental Enrichment for Captive Animals. Blackwell Science, Oxford.
Zimmermann A (2010) The role of zoos in contributing to in situ conservation. In: Kleiman D, Thompson K, Baer K (ed) Wild Mammals in Captivity: Principles and Techniques for Zoo Management, 2nd ed. University of Chicago Press, Chicago, pp 268-287.
Zoo and Aquarium Association Animal Welfare (2020) Assessment Tool; Zoo and Aquarium Association Australasia Accreditation 2020. https://www.zooaquarium.org.au/index.php/accreditation-2020/. Accessed on: April 27, 2020.
Zwijacz-Kozica T, Selva N, Barja I, Silván G, Martínez-Fernández L, Illers JC, Jodlowski M (2013) Concentration of fecal cortisol metabolites in chamois in relation to tourist pressure in Tartra National Park (South Poland). Acta Theriologica 58:215-22.
Submitted date:
10/02/2020
Accepted date:
10/26/2020
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