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Welfare assessment of captive Asian elephants (Elephas maximus) and Indian rhinoceros (Rhinoceros unicornis) using salivary cortisol measurement

Published online by Cambridge University Press:  11 January 2023

A Menargues ,
V Urios  and
M Mauri
A Menargues*
Affiliation:
Estacion Biologica Terra Natura, Fundacion Terra Natura-CIBIO, Universidad de Alicante, Apdo correos 99, E-03080, Alicante, Spain
V Urios
Affiliation:
Estacion Biologica Terra Natura, Fundacion Terra Natura-CIBIO, Universidad de Alicante, Apdo correos 99, E-03080, Alicante, Spain
M Mauri
Affiliation:
Hospital General Universitario de Alicante, E-03010, Alicante, Spain
*
* Contact for correspondence and requests for reprints: a.menargues@ua.es
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Abstract

The measurement of salivary cortisol allows non-invasive assessment of welfare in captive animals. We utilised this technique to test the effect of zoo opening on six Asian elephants and two Indian rhinoceros at the Terra Natura Zoological Park, Alicante, Spain, during pre-opening, opening and post-opening periods. Salivary cortisol concentrations were found to be significantly higher during the opening period than during pre- and post-opening periods for both species. This method could prove a useful tool in monitoring the success of decisions taken to improve the welfare of captive animals.

Keywords

animal welfareAsian elephantIndian rhinocerosmanagementsalivary cortisolstress
Type
Articles
Information
Animal Welfare , Volume 17 , Issue 3 , August 2008 , pp. 305 - 312
Copyright
© 2008 Universities Federation for Animal Welfare

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References

Beerda, B, Schilder, MBH, Janssen, NSCRM and Mol, JA 1996 The use of saliva cortisol, urinary cortisol, and catecholamine measurements for a non-invasive assessment of stress responses in dogs. Hormones and Behaviour 30: 272–279CrossRefGoogle Scholar
Boyce, WT, Champoux, M, Suomi, SJ and Gunnar, MR 1995 Salivary cortisol in nursery-reared rhesus monkeys: reactivity to peer interactions and altered circadian activity. Developmental Psychobiology 28: 257–267Google ScholarPubMed
Brown, JL, Bellem, AC, Fouraker, M, Wildt, DE and Roth, TL 2001 Comparative analysis of gonadal and adrenal activity in the black and white rhinoceros in North America by non-invasive endocrine monitoring. Zoo Biology 20: 463–486CrossRefGoogle Scholar
Carlstead, K and Shepherdson, D 1994 Effects of environmental enrichment on reproduction. Zoo Biology 13: 447–459CrossRefGoogle Scholar
Carlstead, K, Mellen, J and Kleiman, DG 1999 Black rhinoceros (Diceros bicornis) in US Zoos: I Individual behaviour profiles and their relationship to breeding success. Zoo Biology 18: 17–343.0.CO;2-K>CrossRefGoogle Scholar
Carlstead, K and Shepherdson, D 2000 Alleviating stress in zoo animals with environmental enrichment. In: Moberg, GP and Mench, JA (eds) The Biology of Animal Stress pp 337–354. CABI Publishing: New York, USAGoogle Scholar
Cook, DM, Kendall, JW, Greer, MA and Kramer, RM 1973 The effect of acute or chronic ether stress on plasma ACTH concentration in the rat. Endocrinology 93: 1019–1024CrossRefGoogle ScholarPubMed
Cross, N, Pines, MK and Rogers, LJ 2004 Saliva sampling to assess cortisol levels in unrestrained common marmosets and the effect of behavioural stress. American Journal of Primatology 62: 107–114CrossRefGoogle Scholar
Dantzer, R and Mormede, P 1983 Stress in farm animals: a need for revaluation. Journal of Animal Science 57: 6–18CrossRefGoogle Scholar
Dathe, HH, Kuckelkorn, B and Minnemann, D 1992 Salivary cortisol assessment for stress detection in the Asian Elephant (Elephas maximus): a pilot study. Zoo Biology 11: 285–289CrossRefGoogle Scholar
Dawson, A and Howe, PD 1983 Plasma corticosterone in wild starlings (Sturnus vulgaris) immediately following capture and relation to bodyweight during the annual cycle. General and Comparative Endocrinology 51: 303–308CrossRefGoogle Scholar
de Groot, J, de Jong, IC, Prelle, IT and Colas, JM 2000 Immunity in barren and enriched housed pigs differing in baseline cortisol concentration. Physiology and Behavior 71: 217–223CrossRefGoogle ScholarPubMed
Dehnhard, M, Clauss, M, Lechner-Doll, M, Meyer, HHD and Palme, R 2001 Non-invasive monitoring of adrenocortial activity in roe deer (Caproelus caproelus) by measurement of fecal cortisol metabolites. General and Comparative Endocrinology 123: 111–120CrossRefGoogle Scholar
Dehnhard, M 2007 Characterisation of the sympathetic nervous system of Asian (Elephas maximus) and African (Loxodonta africana) elephants based on urinary catecholamine analysis. General and Comparative Endocrinology 151: 274–284CrossRefGoogle Scholar
Ernst, K, Tuchscherer, M, Kanitz, E, Puppe, B and Manteuffel, G 2006 Effects of attention and rewarded activity on immune parameters and wound healing in pigs. Physiology and Behavior 89: 448–456CrossRefGoogle ScholarPubMed
Fuchs, E, Kirschbaum, C, Benisch, D and Bieser, A 1997 Salivary cortisol: a non-invasive measure of hypothalamo-pituitary-adrenocortical activity in the squirrel monkey, Saimiri sciureus. Laboratory Animals 31: 306–311CrossRefGoogle ScholarPubMed
Glatston, AR, Geilvoet-Soetman, E, Hora-Pecek, E and van Hoff, J 1984 The influence of the zoo environment on social behaviour of groups of cotton-top tamarin, Sanguinus oedipus oedipus. Zoo Biology 3: 241–253CrossRefGoogle 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: 143–153CrossRefGoogle Scholar
Haeckel, R 1989 Application of saliva in laboratory medicine. Report on the workshop conference. Journal of Clinical Chemistry and Clinical Biochemistry 27: 233–252Google Scholar
Haemisch, A 1990 Coping with social conflict, and short term changes of plasma cortisol titers in familiar and unfamiliar environments. Physiology and Behaviour 47: 1265–1270CrossRefGoogle ScholarPubMed
Hamilton, GD and Weeks, HP Jr 1985 Cortisol and aldosterone comparisons of cottontail rabbits collected by shooting, trapping, and falconry. Journal of Wildlife Diseases 31: 40–42CrossRefGoogle Scholar
Harper, JM and Austad, SN 2000 Fecal glucocorticoids: a non-invasive method of measuring adrenal activity in wild and captive rodents. Physiological and Biochemical Zoology 73: 12–22CrossRefGoogle Scholar
Herbert, TB and Cohen, S 1993 Stress and immunity in humans: a meta-analytic review. Psychosomatic Medicine 55: 364–379CrossRefGoogle ScholarPubMed
Kirchbaum, C and Hellhammer, DH 1994 Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 19: 313–333CrossRefGoogle Scholar
Kuckelkorn, B and Dathe, HH 1990 Trächtigkeits-diagnose beim Panzernashorn (Rhinoceros unicornis) anhand von Progrdteronbestimmungen im Speiche. Der Zoologische Garten NF 60: 333–340. [Title translation: Pregnancy diagnosis in the Asian rhino on the basis of progesterone determination in saliva]Google Scholar
Lane 2006 Can non-invasive glucocorticoid measures be used as reliable indicators of stress in animals. Animal Welfare 15: 331–342Google Scholar
López-Mondejar, P, Fuentes, MA, Mauri, M, Mora, A, Pérez Soto, M, Vargas, F and Martín Hidalgo, A 2006 Determinación de cortisol salivar en el diagnóstico de la enfermedad de Cushing pediátrico. Anales de Pediatría 64: 270–272. [Title translation: Salivary cortisol determination in pediatric Cushing illness diagnosis]CrossRefGoogle Scholar
Mallapur, A, Sinha, A and 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: 341–352CrossRefGoogle Scholar
McKenzie, S and Deane, EM 2005 Faecal corticosteroid levels as an indicator of well-being in the tammar wallaby, Macropus eugenii. Comparative Biochemistry and Physiology 140: 81–87CrossRefGoogle ScholarPubMed
Meyer, JM, Walker, SL, Freeman, EW, Steinetz, BG and Brown, JL 2004 Species and fetal gender effects on the endocrinology of pregnancy in elephants. General and Comparative Endocrinology 138: 263–270CrossRefGoogle ScholarPubMed
Millspaugh, JJ, Woods, RJ, Hunt, KE, Raedeke, KJ, Brundige, GC, Washburn, BE and Wasser, SK 2001 Using fecal glucocorticoid assays to study the physiological stress response of elk. Wildlife Society Bulletin 29: 899–907Google Scholar
Moberg, GP 2000 Biological response to stress: implications for animal welfare. In: Moberg, GP and Mench, JA (eds) The Biology of Animal Stress pp 1–22. CABI Publishing: New York, USAGoogle Scholar
Moodie, EM and Chamove, AS 1990 Brief threatening events are beneficial for captive tamarins. Zoo Biology 9: 275–286CrossRefGoogle Scholar
Moore-Ede, MC and Sulzman, FM 1977 The physiological basis of circadian time-keeping in primates. Physiologist 20: 17–25Google Scholar
Morrow, CJ, Kolver, ES, Verkerk, GA and Matthews, L 2002 Fecal glucocorticoid metabolites of adrenal activity in dairy cattle. General and Comparative Endocrinology 126: 229–241CrossRefGoogle ScholarPubMed
Morton, DJ, Anderson, E, Foggin, CM, Kock, MD and Tiran, EP 1995 Plasma cortisol as an indicator of stress due to capture and translocation in wildlife species. Veterinary Record 136: 60–63CrossRefGoogle ScholarPubMed
Munck, A, Guyre, PM and Holbrook, NJ 1984 Physiological functions of glucocorticoids in stress and their relation to pharmacological effects. Endocrine Reviews 5: 25–44CrossRefGoogle Scholar
Norcross, JL and Newman, JD 1999 Effects of separation and novelty on distress vocalizations and cortisol in the common marmoset (Callithrix jacchus). American Journal of Primatology 47: 209–2223.0.CO;2-0>CrossRefGoogle ScholarPubMed
Ohl, F, Kirschbaum, C and Fuchs, E 1999 Evaluation of hypothalamo-pituitary-adrenal activity in the tree shrew (Tupaia belangeri) via salivary cortisol measurement. Laboratory Animals 33: 269–274CrossRefGoogle ScholarPubMed
Palme, R, Robia, C, Messmann, S, Hofer, J and Mostl, E 1999 Measurement of faecal cortisol metabolites in ruminants: a non-invasive parameter of adrenocortical function. Wiener Tierarztliche Monatsschrift 86: 237–241Google Scholar
Palme, R, Robia, C, Baumgartner, W and Mostl, E 2000 Transport stress in cattle as reflected by an increase in faecal cortisol metabolite concentrations. The Veterinary Record 146: 108–109CrossRefGoogle ScholarPubMed
Parrot, RF, Misson, BH and Baldwin, BA 1989 Salivary cortisol in pigs following adrenocorticotrophic hormone stimulation: comparison with plasma levels. British Veterinary Journal 145: 362–366CrossRefGoogle Scholar
Powell, DM, Carlstead, K, Tarou, LR, Brown, JL and Monfort, SL 2006 Effects of construction noise on behaviour and cortisol levels in a pair of captive giant pandas (Ailuropoda melanoleuca). Zoo Biology 25: 391–408CrossRefGoogle Scholar
Queyras, A and Carossi, M 2004 Non-invasive techniques for analysing hormonal indicatorsofstress.Ann Ist Super Sanità 40: 211–221Google Scholar
Romero, LM and Romero, RC 2002 Corticosterone responses in birds: the importance of rapid initial sampling. Condor 104: 129–135CrossRefGoogle Scholar
Sabatino, F, Masoro, EJ, McMahan, A and Kuhn, RW 1991 Assessment of the role of glucocorticoid system in aging process and in the action of food restriction. Journal of Gerontology 46: 171–179CrossRefGoogle ScholarPubMed
Schapiro, S, Bloomsmith, MA, Kessel, AL and Shively, CA 1993 Effects of enrichment and housing on cortisol response in juvenile rhesus monkeys. Applied Animal Behaviour Science 37: 251–263CrossRefGoogle Scholar
Schoech, SJ, Ketterson, ED and Nolan, V Jr 1999 Exogenous testosterone and the adrenocortical response in dark-eyed juncos. Auk 116: 64–72CrossRefGoogle Scholar
Shepherdson, DJ, Carlstead, KC and Wielebnowski, NC 2004 Cross-institutional assessment of stress responses in zoo animals using longitudional monitoring of faecal corticoids. Animal Welfare 13: 105–115Google Scholar
Siegel, RA, Ducker, EM, Pahnke, U and Wuttke, W 1987 Stress-induced changes in cholecystokinin and substance P concentrations in discrete regions of the rat hypothalamus. Neuroendocrinology 46: 75–81CrossRefGoogle ScholarPubMed
Soltis, J, Wegner, FH and Newman, JD 2003 Adult cortisol response to immature offspring play in captive squirrel monkeys. Physiology and Behaviour 80: 217–223CrossRefGoogle ScholarPubMed
Stead, SK, Meltzer, DGA and Palme, R 2000 The measurement of glucocorticoid concentrations in the serum and faeces of captive African elephants (Loxodonta africana) after ACTH stimulation. Journal of the South African Veterinary Medical Association 71: 192–196CrossRefGoogle ScholarPubMed
Stratakin, CA and Chrousos, GP 1995 Neuroendocrinology and pathophysiology of the stress system: In stress, basic mechanism and clinical implications. Annals of the New York Academy of Sciences 771: 1–18CrossRefGoogle Scholar
Swaisgood, R 2007 Current status and future directions of applied behavioural research for animal welfare conservation. Applied Animal Behaviour Science 102: 139–162CrossRefGoogle Scholar
Thompson, VD 1989 Behavioural response of 12 ungulate species in captivity to the presence of humans. Zoo Biology 8: 275–297CrossRefGoogle Scholar
Tiefenbacher, S, Lee, B, Meyer, JS and Spealman, RD 2003 Non-invasive technique for repeated sampling of salivary free cortisol in awake, unrestrained squirrel monkeys. American Journal of Primatology 60: 69–75CrossRefGoogle Scholar
Vincent, IC and Michell, AR 1992 Comparison of cortisol concentrations in saliva and plasma of dogs. Research in Veterinary Science 53: 342–345CrossRefGoogle ScholarPubMed
Von der Ohe, CG and Servheen, C 2002 Measuring stress in mammals using faecal glucocorticoids: opportunities and challenges. Wildlife Society Bulletin 30: 1215–1225Google Scholar
Washburn, BE and Millspaugh, JJ 2002 Effects of simulated environmental conditions on glucocorticoid metabolite measurements in white-tailed deer faeces. General and Comparative Endocrinology 127: 217–222CrossRefGoogle Scholar
Wasser, SK, Hunt, KE, Brown, JL, Cooper, K, Crockett, CM, Bechert, U, Millspaugh, JJ, Larson, S and Monfort, SL 2000 A generalized fecal glucocorticoid assay for use in a diverse array of non domestic mammalian and avian species. General and Comparative Endocrinology 120: 260–275CrossRefGoogle Scholar
Wells, DL and Hepper, PG 2000 The influence of environmental change on the behaviour of sheltered dogs. Applied Animal Behaviour Science 68: 151–162CrossRefGoogle ScholarPubMed
Wells, DL 2004 A review of environmental enrichment for kennelled dogs, Canis familiaris. Applied Animal Behaviour Science 85: 307–317CrossRefGoogle Scholar
Wells, DL 2005 A note on the influence of visitors on the behaviour and welfare of zoo-housed gorillas. Applied Animal Behaviour Science 93: 13–17CrossRefGoogle Scholar
Wells, DL, Hepper, PG, Coleman, D and Challis, MG 2007 A note on the effect of olfactory stimulation on the behaviour and welfare of zoo-housed gorillas. Applied Animal Behaviour Science 106: 155–160CrossRefGoogle Scholar
Whitten, PL, Brockman, DK and Stavisky, RC 1998 Recent advances in non-invasive techniques to monitor hormone-behaviour interactions. Yearbook of Physical Anthropology 41: 1–233.0.CO;2-H>CrossRefGoogle Scholar
Wielebnowski, NC, Fletchall, N, Carlstead, K, Busso, JM and Brown, JL 2002 Non-invasive assessment of adrenal activity associated with husbandry and behavioural factors in the North American clouded leopard population. Zoo Biology 21: 77–98CrossRefGoogle Scholar
Zayan, R 1991 The specificityofsocial stress.Behavioural Process 25: 81–93CrossRefGoogle Scholar
Zoldag, L, Heuwiesser, W, Grunert, E and Stephan, E 1983 Steroid hormone profile in pregnant cows after exposure to noise stress, with particular reference to corticosteroids. Zentrall Veterinärmed 30: 737–748Google Scholar