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Cross-institutional assessment of stress responses in zoo animals using longitudinal monitoring of faecal corticoids and behaviour

Published online by Cambridge University Press:  11 January 2023

DJ Shepherdson ,
KC Carlstead  and
N Wielebnowski
DJ Shepherdson*
Affiliation:
Oregon Zoo, 4001 SW Canyon Road, Portland, Oregon 97221, USA
KC Carlstead
Affiliation:
Honolulu Zoo, 151 Kapahulu Avenue, Honolulu, Hawaii 96815, USA
N Wielebnowski
Affiliation:
BRookfield Zoo, 3300 Golf Road, BRookfield, Illinois 60513, USA
*
* Contact for correspondence and requests for reprints: shepherdsond@metro.dst.or.us
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Abstract

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Cross-institutional studies that combine non-invasive physiological measures of stress responses and the assessment of individual differences in behaviour and temperament have great potential as tools for assessing the well-being of zoo animals and for identifying key environmental stimuli relevant to well-being. In addition, such studies allow comparison of animals under a wide variety of conditions and enable researchers to obtain sufficiently large samples sizes for statistical data analyses. Faecal corticoid measurements, a method recently developed to monitor adrenal activity in wildlife and domestic species, can be obtained non-invasively as part of the normal husbandry routine. While basic techniques still need improvement, and interpretation of the acquired measures can be challenging, assessment of faecal corticoid concentrations can provide a useful indicator of stress responses under a variety of captive conditions. Here we report on three studies that illustrate this approach and the results that can be obtained. An on-going study reveals significant differences in the pattern of variability of faecal corticoid concentrations between polar bears that are reported by keepers to perform stereotypic behaviour and those that do not. In another study, faecal corticoid measures indicated that stress responses to certain extraneous noises might interfere with the breeding of Hawaiian honeycreepers in captivity. In a study of clouded leopards, higher faecal corticoid concentrations were measured when cats were kept on public display or near potential predators compared to individuals maintained off exhibit or in the absence of visible predators. The findings of an on-going experimental study suggest a causal relationship between the provision of additional hiding spaces and a decline in faecal corticoid concentrations in clouded leopards.

Keywords

animal welfarecorticosteroidhousing and husbandrystereotypiesstresszoo
Type
Research Article
Information
Animal Welfare , Volume 13 , Issue S1: Science in the Service of Animal Welfare: Proceedings of the UFAW International Symposium, Edinburgh, 2-4 April 2003 , February 2004 , pp. S105 - S113
Copyright
© 2004 Universities Federation for Animal Welfare

References

Ames, A 1993 The Behaviour of Captive Polar Bears. Universities Federation for Animal Welfare: Wheathampstead, Herts, UKGoogle Scholar
Boorer, M K 1972 Some aspects of stereotyped pattern of movement exhibited by zoo animals. International Zoo Yearbook 12: 164–168CrossRefGoogle Scholar
Capitanio, J P, Mendoza, S P and Baroncelli, S 1999 The relationship of personality dimensions in adult male rhesus macaques to progression of Simian Immunodeficiency Virus disease. Brain, Behaviour and Immunity 13: 138–154CrossRefGoogle ScholarPubMed
Carlstead, K 1991 Husbandry of the fennec fox Fennecus zerda: environmental conditions influencing stereotypic behaviour. International Zoo Yearbook 30: 202–207Google Scholar
Carlstead, K 1998 Determining the causes of stereotypic behaviors in zoo carnivores: toward appropriate enrichment strategies. In: Shepherdson, D J, Mellen, J D and Hutchins, M (eds) Second Nature: Environmental Enrichment for Captive Animals pp 172–183. Smithsonian Institution Press: Washington, DC, USAGoogle Scholar
Carlstead, K and Seidensticker, J 1991 Seasonal variation in stereotypic pacing in an American black bear (Ursus Americanus). Behavioural Processes 25: 155–161CrossRefGoogle Scholar
Carlstead, K, Brown, J L and Seidensticker, J 1993 Behavioural and adrenocortical responses to environmental changes in leopard cats (Felis bengalensis). Zoo Biology IP: 321–331.CrossRefGoogle Scholar
Carlstead, K, Fraser, J, Bennett, C and Kleiman, D G 1999b Black rhinoceros (Diceros bicornis) in US Zoos: 11. Behaviour, breeding success and mortality in relation to housing facilities. Zoo Biology 15: 35–523.0.CO;2-L>CrossRefGoogle Scholar
Carlstead, K, Mellen, J and Kleiman, D G 1999a Black rhinoceros (Diceros bicornis) in US Zoos: I. Individual behaviour profiles and their relationship to breeding success. Zoo Biology 15: 14–34Google Scholar
Carlstead, K, Shepherdson, D, Sheppard, C, Mellen, J and Bennet, C 2000 Constructing Behavioural Profiles for Zoo Animals: Incorporating Behavioural Information into Captive Population Management. American Zoo and Aquarium Association's Behaviour and Husbandry Advisory Group and Oregon Zoo. Available at: http://www.lpzoo.org/ethograms/MBA_Techniques_Manual.doc.Google Scholar
Dathe, H H, Kuckelhorn, B and Minnemann, D 1992 Salivary cortisol assessment for stress detection in the Asian elephant (Elephas maximus): a pilot study. Zoo Biology 14: 555–564Google Scholar
Dittrich, L 1984 On the necessity to promote activity of Zoo-kept wild animals by artificial stimuli. In: Unshelm, J, van Putten, G and Zeeb, K (eds) Proceedings of the International Congress on Applied Ethology in Farm Animals pp 283–287. KTBL: Darmstadt, GermanyGoogle Scholar
Forthman, D L, Elder, S D, Bakeman, R, Kurkowski, T W, Noble, C C and Winslow, S W 1992 Effects of feeding enrichment on behaviour of three species of captive bears. Zoo Biology 11: 187–195CrossRefGoogle Scholar
Gosling, S D 2001 From mice to men: what we can learn about personality from animal research? Psychological Bulletin 127: 54–86CrossRefGoogle ScholarPubMed
Hediger, H 1955 Studies of the Psychology and Behaviour of Captive Animals in Zoos and Circuses. Butterworths Scientific Publications: London, UKGoogle Scholar
Hennessy, J W and Levine, S 1979 Stress, arousal, and the pititary-adrenal system: a psychoendocrine hypothesis. Progress in Psychobiology and Physiological Psychology S: 133–178.Google Scholar
Hennessy, J W, Heybach, J P, Vernikos, J and Levine, S 1979 Plasma corticosterone concentrations sensitively reflect levels of stimulus intensity in the rat. Physiology and Behavior 22: 821–825CrossRefGoogle ScholarPubMed
Jones, M T 1979 Control of adrenocortical hormone secretion. In: James, V H T (ed) The Adrenal Gland pp 93–103. Raven Press: New York, USAGoogle Scholar
Jurke, M H, Czekala, N M, Lindburg, D G and Millard, S E 1997 Faecal corticoid metabolite measurement in the cheetah (Acynonyxjubatus). Zoo Biology 66: 133–1473.0.CO;2-B>CrossRefGoogle Scholar
Kitchener, A C 1999 Mate killing in clouded leopards: a hypothesis. International Zoo News 46: 221–224Google Scholar
Law, G and Tatner, P 1998 Behaviour of a captive pair of clouded leopards (Neofelis nebulosa): introduction without injury. Animal Welfare 7: 57–76Google Scholar
Manteca, X and Deag, J M 1993 Individual differences in temperament of domestic animals: a review of methodology. Animal Welfare 2: 247–268Google Scholar
Marriner, L M and Drickamer, L C 1994 Factors influencing stereotyped behaviour of primates in zoos. Zoo Biology 13: 267–275CrossRefGoogle Scholar
Mason, G 1991 Stereotypies: a critical review. Animal Behaviour 41: 1015–1037CrossRefGoogle Scholar
Mason, G J 1993 Forms of stereotypic behaviour. In: Lawrence, A B and Rushen, J (eds) Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare pp 7–40. CAB International: Wallingford, UKGoogle Scholar
Mason, G J and Latham, N R 2004 Can't stop, won't stop: is stereotypy a reliable animal welfare indicator? In: KirkWood, J K, Roberts, E A and Vickery, S (eds) Proceedings of the UFAW International Symposium ‘Science in the Service of Animal Welfare’, Edinburgh, 2003. Animal Welfare 13: 557–569 (Suppl)Google Scholar
Mason, J W 1968 A review of psychoendocrine research on the pituitary adrenal cortical system. Psychosomatic Medicine 30: 576–607CrossRefGoogle ScholarPubMed
McGlone, J J, Salak, J L, Lumpkin, E A, Nicholson, R L, Gibson, M and Norman, R L 1993 Shipping stress and social status effects on pig performance, plasma cortisol, natural killer cell activity, and leukocyte numbers. Journal of Animal Science 71: 888–896CrossRefGoogle ScholarPubMed
McLeod, P J, Moger, W H, Ryon, J, Gadbois, S and Fentress, J C 1996 The relation between urinary Cortisol levels and social behaviour in captive timber wolves. Canadian Journal of Zoology 74: 209–216CrossRefGoogle Scholar
Mellen, J 1994 Survey and inter Zoo studies used to address husbandry problems in some Zoo vertebrates. Zoo Biology 13: 459–470CrossRefGoogle Scholar
Mellen, J D 1991 Factors influencing reproductive success in small captive exotic felids (Felis spp): a multiple regression analysis. Zoo Biology 10: 95–110CrossRefGoogle Scholar
Miller-Schroeder, P and Paterson, J D 1989 Environmental influences on reproductive and maternal behaviour in captive gorillas: results of a survey. In: Segal, S (ed) Housing, Care and Psychological Well-Being of Captive and Laboratory Primates pp 389–415. Noyes: Park Ridge, New Jersey, USAGoogle Scholar
Morris, D 1964 The response of animals to a restricted environment. Symposium of the Zoological Society of London 13: 99–118Google Scholar
Möstl, E and Palme, R 2002 Hormones as indicators of stress. Domestic Animal Endocrinology 23: 67–74CrossRefGoogle ScholarPubMed
Pottinger, T G 2000 Genetic selection to reduce stress in animals. In: Moberg, G P and Mench, J A (eds) Biology of Animal Stress pp 291–308. CAB International: Wallingford, UKGoogle Scholar
Pottinger, T G, Pickering, A D and Hurley, M A 1992 Consistency in the stress response of individuals of two strains of rainbow trout (Oncorrhyncus mykiss). Aquaculture 103: 275–289CrossRefGoogle Scholar
Richardson, D M 1987 Polar bear problems or between a rock and an iceberg. International Zoo News 200: 14–19Google Scholar
Roberts, M S 1989 A survey and analysis of management practice in the North American red panda SSP. In: Glatston, A R (ed) Red Panda Biology pp 129–151. SPB Academic Publishing: The Hague, The NetherlandsGoogle Scholar
Rushen, J, Lawrence, A B and Terlouw, E M C 1993 The motivational basis of stereotypies. In: Lawrence, A B and Rushen, J (eds) Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare pp 41–65. CAB International: Wallingford, UKGoogle Scholar
Schouten, W G P and Wiegant, V M 1997 Individual responses to acute and chronic stress in pigs. Acta Physiologica Scandinavica 161 (Suppl 64): 88–91Google Scholar
Selye, H 1956 The Stress of Life. McGraw: New York, USAGoogle Scholar
Silverin, B 1997 The stress response and autumn dispersal behaviour in willow tits. Animal Behaviour 53: 451–459CrossRefGoogle Scholar
Silverin, B 1998 Stress responses in birds. Poultry and Avian Biology Reviews 9: 153–158Google Scholar
Stevenson-Hinde, J 1983 Individual characteristics: a statement of the problem. In: Hinde, R A (ed) Primate Social Relationships. Blackwell Scientific: Oxford, UKGoogle Scholar
Van Keulen-Kromhout, G V 1978 Zoo enclosures for bears: their influence on captive behaviour and reproduction. International Zoo Yearbook 15: 177–186CrossRefGoogle Scholar
Wasser, S K, Hunt, K E, Brown, J L, Cooper, K, Crockett, C M, Bechert, U, Millspaugh, J J, Larson, S, and Monfort, S L 2000 A generalized faecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. General Comparative Endocrinology 120: 260-275.CrossRefGoogle Scholar
Wechsler, B 1991 Stereotypies in polar bears. Zoo Biology 10: 177–188CrossRefGoogle Scholar
Whitten, P L, Brockman, D K and Stavisky, R C 1998 Recent advances in noninvasive techniques to monitor hormone-behaviour interactions. Yearbook of Physical Anthropology 41: 1–233.0.CO;2-H>CrossRefGoogle Scholar
Wielebnowski, N C 1999 Behavioural differences as predictors of breeding status in captive cheetahs. Zoo Biology 15: 335–3493.0.CO;2-X>CrossRefGoogle Scholar
Wielebnowski, N C, Fletchall, N, Carlstead, K, Busso, J M and Brown, J L 2002 Noninvasive assessment of adrenal activity associated with husbandry and behavioural factors in the North American clouded leopard population. Zoo Biology 21: 77–98CrossRefGoogle Scholar
Wingfield, J C 1994 Modulation of the adrenocortical response to stress in birds. In: Tobe, S (ed) Perspectives in Comparative Endocrinology pp 520–528. National Research Council of Canada: Ottawa, CanadaGoogle Scholar
Wingfield, J C, Breuner, C and Jacobs, J 1997 Corticosterone and behavioural responses to unpredictable events. In: Harvey, S and Etches, R J (eds) Perspectives in Avian Endocrinology pp 267–278. Society for Endocrinology: Bristol, UKGoogle Scholar
Wingfield, J C, Maney, D L, Breuner, C W, Honey, P, Jacobs, J D, Lynn, S, Ramenofsky, M and Richardson, R D 1998 Ecological basis of hormone-behavior interactions: the ‘emergency life history stage’. American Zoologist 35: 191–206CrossRefGoogle Scholar
Yamada, J K and Durrant, B S 1989 Reproductive parameters of clouded leopards (Neofelis nebulosa). Zoo Biology 8: 223–231CrossRefGoogle Scholar