Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-04-30T15:34:18.769Z Has data issue: false hasContentIssue false
  • English
  • Français

Seasonal pattern of salivary cortisol secretion in the greater one-horned rhino (Rhinoceros unicornis)

Published online by Cambridge University Press:  01 January 2023

A Menargues ,
V Urios  and
R Limiñana
A Menargues*
Affiliation:
Universidad de Alicante, Campus San Vicente del Raspeig, Facultad de Educación I, E-03080 Alicante, Spain Estación Biológica Terra Natura, Instituto Universitario de Investigación CIBIO, Universidad de Alicante, Apdo correos 99, E-03080, Alicante, Spain Didáctica de las Ciencias Experimentales, Facultad de Educación, Universidad de Alicante, Apdo correos 99, E-03080, Alicante, Spain
V Urios
Affiliation:
Estación Biológica Terra Natura, Instituto Universitario de Investigación CIBIO, Universidad de Alicante, Apdo correos 99, E-03080, Alicante, Spain
R Limiñana
Affiliation:
Estación Biológica Terra Natura, Instituto Universitario de Investigación CIBIO, Universidad de Alicante, Apdo correos 99, E-03080, Alicante, Spain Didáctica de las Ciencias Experimentales, Facultad de Educación, Universidad de Alicante, Apdo correos 99, E-03080, Alicante, Spain Instituto de Investigación en Recursos Cinegéticos (IREC), CSIC-UCLM-JCCM, Ronda de Toledo, s/n E-13071, Ciudad Real, Spain
*
* Contact for correspondence and requests for reprints: a.menargues@ua.es
Get access Rights & Permissions [Opens in a new window]

Abstract

The Indian rhinoceros or greater one-horned rhino (Rhinoceros unicornis) is listed as vulnerable by the IUCN Red List of Threatened Species and, therefore, captive individuals have been subject to the European Endangered Species Programme since 1990. Enhancement of welfare is key in ensuring the breeding success of this species in captivity. Salivary cortisol has been recently used to assess welfare of captive and free-ranging animals. Nevertheless, rhythms of cortisol secretion may fluctuate throughout the year and therefore, knowledge of the circannual pattern of cortisol secretion is essential to evaluate the physiological significance of seasonal variations of cortisol levels as an indicator of stress in animals. Here, we analyse monthly differences in cortisol secretion in two Indian rhinoceros. Saliva samples of two rhinoceros were collected and analysed by radioimmunoassay for the period of one year to determine cortisol concentrations. We found a seasonal pattern of salivary cortisol secretion. The highest cortisol concentrations were found in August and decreased until reaching a nadir in January. Cortisol concentrations in these two animals showed a correlation with temperature and visitor numbers but it is not possible to draw conclusions from this study as to whether the variation in cortisol was due to these or other factors.

Keywords

animal welfareIndian rhinocerossalivary cortisolseasonalitystresszoo visitors
Type
Research Article
Information
Animal Welfare , Volume 22 , Issue 4 , November 2013 , pp. 467 - 472
Copyright
© 2013 Universities Federation for Animal Welfare

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, US, Benne, M, Bloomsmith, MA and Maple, TL 2002 Retreat space and human visitor density moderate undesirable behavior in petting zoo animals. Journal of Applied Animal Welfare Science 5: 125–137. http://dx.doi.org/10.1207/S15327604JAWS0502_03CrossRefGoogle ScholarPubMed
Brown, JL, Kersey, DC, Freeman, EW and Wagener, T 2010 Assessment of diurnal urinary cortisol excretion in Asian and African elephants using different endocrine methods. Zoo Biology 29: 274–283. http://dx.doi.org/10.1002/zoo.20268CrossRefGoogle ScholarPubMed
Carlstead, K and Brown, JL 2005 Relationships between patterns of fecal corticoid excretion and behavior, reproduction, and environmental factors in captive black (Diceros bicornis) and white (Ceratotherium simum) rhinoceros. Zoo Biology 24: 215–232. http://dx.doi.org/10.1002/zoo.20050CrossRefGoogle Scholar
Carragher, JF, Sumpter, JP, Pottinger, TG and Pickering, AD 1989 The deleterious effects of cortisol implantation on reproductive function in two species of trout, Salmo trutta L. and Salmo gairdneri Richardson. General and Comparative Endocrinology 76: 310–321. http://dx.doi.org/10.1016/0016-6480(89)90163-9CrossRefGoogle ScholarPubMed
Creel, S, Fox, JE, Hardy, A, Sands, J, Garrot, B and Petterson, RO 2002 Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conservation Biology 16: 809–814. http://dx.doi.org/10.1046/j.1523-1739.2002.00554.xGoogle Scholar
de Jong, IC, Prelle, IT, van de Burgwal, JA, Lambooij, E, Korte, SM, Blokhuis, HJ and Koolhaas, JM 2000 Effects of environmental enrichment on behavioral responses to novelty, learning, and memory, and the circadian rhythm in cortisol in growing pigs. Physiology & Behavior 68: 571–578. http://dx.doi.org/10.1016/S0031-9384(99)00212-7CrossRefGoogle ScholarPubMed
Dhabhar, FS 2009 Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology. Neuroimmunomodulation 16: 300–317. http://dx.doi.org/10.1159/000216188Google ScholarPubMed
Duncko, R, Brian, C, Cui, L, Merikangas, KR and Grillon, C 2007 Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men. Learning Memory 14: 329–335. http://dx.doi.org/10.110 1/lm.483807CrossRefGoogle ScholarPubMed
Ekkel, ED, Dieleman, SJ, Shouten, WGP, Portela, A, Cornelissen, G, Tielen, MJM and Halberg, F 1996 The circadian rhythm of cortisol in the saliva of young pigs. Physiology & Behavior 60: 985–989Google ScholarPubMed
Fernandez, EJ, Tamborski, MA, Pickens, SR and Timberlake, W 2009 Animal-visitor interactions in the modern zoo: conflicts and interventions. Applied Animal Behavior Science 120: 1–8. http://dx.doi.org/10.1016/j.applanim.2009.06.002Google Scholar
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: 306–311. http://dx.doi.org/10.1258/002367797780596077Google ScholarPubMed
Gómez, A, Jewell, E, Walker, SL and Brown, JL 2004 Use of salivary steroid analyses to assess ovarian cycles in an Indian rhinoceros at the National Zoological Park. Zoo Biology 23: 501–512. http://dx.doi.org/10.1002/zoo.20028CrossRefGoogle Scholar
Goyman, W 2012 On the use of non-invasive hormone research in uncontrolled, natural environments: the problem with sex, diet, metabolic rate and the individual. Methods in Ecology and Evolution 3: 757–765. http://dx.doi.org/10.1111/j.2 041-210X.2012.00203.xGoogle Scholar
Gröschl, M 2007 Current status of salivary hormone analysis. Clinical Chemistry 54: 1759–1769. http://dx.doi.org/10.1373/clinchem.2008.108910CrossRefGoogle Scholar
Hardy, MP, Gao, HB, Dong, Q, Ge, R, Wang, Q, Chai, WR, Feng, X and Sottas, C 2005 Stress hormone and male reproductive function. Cell and Tissue Research 322: 147–153. http://dx.doi.org/10.1007/s00441-005-0006-2Google ScholarPubMed
Hosey, GR 2000 Zoo animals and their human audiences: what is the visitor effect? Animal Welfare 9: 343–357Google Scholar
Huber, S, Palme, R and Arnold, W 2003 Effects of season, sex, and sample collection on concentrations of fecal cortisol metabolites in red deer (Cervus elaphus). General and Comparative Endocrinology 130: 48–54. http://dx.doi.org/10.1016/S0016-6480(02)00535-XCrossRefGoogle Scholar
Ingram, JR, Crockford, JN and Matthews, LR 1999 Ultradian, circadian and seasonal rhythms in cortisol secretion and adrenal responsiveness to ACTH and yarding in unrestrained red deer (Cervus elaphus) stags. Journal of Endocrinology 163: 289–300. http://dx.doi.org/10.1677/joe.0.1620289Google Scholar
Kirchbaum, C and Hellhammer, DH 1994 Salivary cortisol in psychoneuroendocrine research: recent developments and applications. Psychoneuroendocrinology 19: 313–333. http://dx.doi.org/10.1016/0306-4530(94)90013-2CrossRefGoogle Scholar
López-Mondéjar, 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 Pediatria 64: 270–272. [Title translation: Salivary cortisol determination in diagnosis of paediatric Cushings disease]. http://dx.doi.org/10.1157/13085516CrossRefGoogle Scholar
Mallapur, A, Sinha, A and Waran, N 2005 Influence of visitor presence on the behavior of captive lion-tailed macaques (Macaca silenus) housed in Indian zoos. Applied Animal Behavior Science 94: 341–352. http://dx.doi.org/10.1016/j.applanim.2005.02.012Google Scholar
McEwen, B 2006 Stress, adaptation and disease: allostasis and allostatic load. Annals of the New York Academy of Sciences 840: 33–44. http://dx.doi.org/10.1111/j.1749-6632.1998.tb09546.xCrossRefGoogle Scholar
Menargues, A, Urios, V and Limiñana, R 2012a Seasonal rhythms of salivary cortisol secretion in captive Asian elephants (Elephas maximus). General and Comparative Endocrinology 176: 259–264. http://dx.doi.org/10.1016/j.ygcen.2012.02.001Google Scholar
Menargues, A, Urios, V, Limiñana, R and Mauri, M 2012b Circadian rhythm of salivary cortisol in Asian elephants (Elephas maximus): a factor to consider during welfare assessment. Journal of Applied Animal Welfare Science 15: 383–390. http://dx.doi.org/10.1080/10888705.2012.709157CrossRefGoogle Scholar
Menargues, A, Urios, V and Mauri, M 2008 Welfare assessment of captive Asian elephants (Elephas maximus) and Indian rhinoceros (Rhinoceros unicornis) using salivary cortisol measurement. Animal Welfare 17: 305–312Google Scholar
Milliken, T, Emslie, RH and Talukdar, B 2009 African and Asian rhinoceroses: A report from the IUCN Species Survival Commission (IUCN/SSC) African and Asian Rhino Specialist Groups and TRAFFIC to the CITES Secretariat pursuant to Resolution Conference 9.14 (Rev CoP14) and Decision 14.89. Report to CITES 15th meeting. CoP15 Doc.45.1A annex pp 1–18. March 2010, Doha, QatarGoogle Scholar
Millspaugh, JJ, Woods, RJ, Hunt, KE, Raedeke, KJ, Brundige, GC, Washburn, BE and Wasser, SK 2001 Fecal glucocorticoid assays and the physiological stress response in elk. Wildlife Society Bulletin 29: 899–907Google Scholar
Moberg, GP 1990 How behavioral stress disrupts the endocrine control of reproduction in domestic animals. Journal of Dairy Science 74: 304–311. http://dx.doi.org/10.3168/jds.S0022-0302(91)78174-5Google Scholar
Monfort, SL, Brown, JL and Wildt, DE 1993 Episodic and seasonal rhythms of cortisol secretion in male Eld's deer (Cervus eldi thamin). Journal of Endocrinology 138: 41–49. http://dx.doi.org/10.1677/joe.0.1380041CrossRefGoogle Scholar
Munck, A, Guyre, PM and Holbrook, NI 1984 Physiological functions of glucocorticoids in stress and their relationship to pharmacological actions. Endocrine Reviews 5: 25–44. http://dx.doi.org/10.1210/edrv-5-1-25CrossRefGoogle Scholar
Pedernera-Romano, C, Valdez, RA, Singh, S, Chiappa, X, Romano, MC and Galindo, F 2006 Salivary cortisol in captive dolphins (Tursiops truncatus): a non-invasive technique. Animal Welfare 15: 359–362Google 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: 391–408. http://dx.doi.org/10.1002/zoo.20098Google Scholar
Rajagopal, T, Archunan, G and Sekar, M 2011 Impact of zoo visitors on the fecal cortisol levels and behaviour of an endangered species: Indian blackbuck (Antelope cervicapra L). Journal of Applied Animal Welfare Science 14: 18–32. http://dx.doi.org/10.1080/10888705.2011.527598CrossRefGoogle Scholar
Romero, LM 2002 Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. General and Comparative Endocrinology 128: 1–24. http://dx.doi.org/10.1016/S0016-6480(02)00064-3CrossRefGoogle ScholarPubMed
Ruis, MA, Te Brake, JH, Engel, B, Ekkel, ED, Buist, WG, Blokhuis, HJ and Koolhaas, JM 1997 The circadian rhythm of salivary cortisol in growing pigs: effects of age, gender and stress. Physiology & Behavior 62: 623–630. http://dx.doi.org/10.1016/S0031-9384(97)00177-7Google ScholarPubMed
Sheriff, MJ, Dantzer, B, Delehantym, B, Palme, R and Boonstra, R 2011 Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166: 869–887. http://dx.doi.org/10.1007/s00442-011-1943-yGoogle ScholarPubMed
Sheriff, MJ, Wheeler, H, Donker, SA, Krens, CJ, Palme, R, Hik, DS and Boonostra, R 2012 Mountain-top and valley bottom experiences: the stress axis as an integrator of environmental variability in arctic ground squirrel populations. Journal of Zoology 287: 65–75. http://dx.doi.org/10.1111/j.1469-7998.2011.00888.xCrossRefGoogle Scholar
Suzuki, M, Uchida, S, Ueda, K, Tobayama, T, Katsumata, E, Yoshioka, M and Aida, K 2003 Diurnal and annual changes in serum cortisol concentrations in Indo-Pacific bottlenose dolphins Tursiops aduncus and killer whales Orcinus orca. General and Comparative Endocrinology 132: 427–433. http://dx.doi.org/10.1016/S0016-6480(03)00100-XCrossRefGoogle ScholarPubMed
Talukdar, BK, Emslie, R, Bist, SS, Choudhury, A, Ellis, S, Bonal, BS, Malakar, MC, Talukdar, BN and Barua, M 2008 Rhinoceros unicornis. IUCN Red List of Threatened Species. Version 2011.1. www.iucnredlist.orgGoogle Scholar
Vera, F, Antenucci, CD and Zenuto, RR 2011 Cortisol and corticosterone exhibit different seasonal variation and responses to acute stress and captivity in tuco tucos (Ctenomys talarum). General and Comparative Endocrinology 170: 550–557. http://dx.doi.org/10.1016/j.ygcen.2010.11.012CrossRefGoogle Scholar
Wingfield, JC, Moore, MC and Farner, DS 1983 Endocrine responses to inclement weather in naturally breeding populations of white-crowned sparrows (Zonotrichia leucophrys pugetensis). The Auk 100: 56–62CrossRefGoogle Scholar
Wood, P 2009 Salivary steroid assays-research or routine? Annals Of Clinical Biochemistry 46: 183–196. http://dx.doi.org/10.1258/acb.2008.008208Google ScholarPubMed