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Cited by 22Animal Behavior and Welfare StudiesWildlife Ecology and ConservationPrimate Behavior and Ecology

Gender, season and management affect fecal glucocorticoid metabolite concentrations in captive goral (Naemorhedus griseus) in Thailand

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Khonmee, Jaruwan, Brown, Janine L., Rojanasthien, Suvichai, Aunsusin, Anurut, Thumasanukul, Dissakul, Kongphoemphun, Adisorn, Siriaroonrat, Boripat, Tipkantha, Wanlaya +2 more·2014·PLoS ONE
DOI 10.1371/journal.pone.0091633PMC PMC3956719
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Abstract

Chinese goral (Naemorhedus griseus) are a threatened species in Thailand and the focus of captive breeding for possible reintroduction. However, little is known of their biology or what factors in the captive environment affect welfare. Our objective was to determine the impact of gender, season, and management on goral adrenal activity. We hypothesized that differences in fecal glucocorticoid concentrations would be related to animal density. Fecal samples were collected 3 days/week for 1 year from 63 individuals (n = 32 males, 31 females) at two facilities that house the majority of goral in Thailand: Omkoi Wildlife Sanctuary (Omkoi), an off-exhibit breeding center that houses goral in individual pens (16 pens; n = 8 males, 8 females) and in small family groups (8 pens; n = 8 males, 8 females); and the Chiang Mai Night Safari (NS), a zoo that maintains 31 goral (n = 17 males, 14 females) in one large pen. Glucocorticoid metabolite concentrations were higher in male than female goral at Omkoi throughout the year, and there was a seasonal effect on adrenal activity (p<0.05). Goral at Omkoi and NS were used to test the effect of animal density on fecal glucocorticoid excretion of goral housed in similar-sized enclosures. Overall, the highest levels were found at NS (n = 31 adults/pen; 27 m2 per animal) compared to Omkoi (n = 2 adults/pen; 400 m2 per animal) (p<0.05). Overall findings support our hypothesis that animal density and aspects of the captive environment impact adrenal steroid activity in captive goral. In addition, gender and season also had significant effects on glucocorticoid metabolite production. Potential stressors pertaining to the welfare of this species were identified, which will guide future efforts to improve management and create self-sustaining and healthy populations of this threatened species.

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  • In gorals, an increase of glucocorticoids was observed during summer months, which could reflect heat stress.

    “In particular, authors observed an increase of glucocorticoids in gorals during the summer months and this result could reflect a form of heat stress in this species (Khonmee et al., 2014).”

    From Effect of weather conditions and presence of visitors on adrenocortical activity in captive African penguins (Spheniscus demersus) (2017) · cites this paper as Khonmee et al., 2014

    The Results (page not provided) report that summer fecal glucocorticoid concentrations were highest at Night Safari but lowest at Omkoi. The Discussion (page not provided) says the higher summer concentrations at Night Safari could reflect heat stress. The claim omits this facility-specific qualification and implies an increase in gorals generally. (LLM, conf=0.90)

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  • Recent studies on captive animals such as African lions, Siberian tigers, and gorals show that high temperature could affect animal welfare.

    “A few recent studies on captive animals, such as African lions (Panthera leo), Siberian tigers (Pantera tigris) (Young et al., 2013) and gorals (Naemorhedus griseus) (Khonmee et al., 2014) show that high temperature could affect animal welfare.”

    From Effect of weather conditions and presence of visitors on adrenocortical activity in captive African penguins (Spheniscus demersus) (2017) · cites this paper as Khonmee et al., 2014

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Research works printed but not linked: 33

  1. [2]Patton ML, Aubrey L, Edwards M, Rieches R, Zuba J, et al (2000) Successful contraception in a herd of Chinese goral (Nemorhaedus goral arnouxianus) with melengestrol acetate. J Zoo Wildl Med 31: 228– 230. 10982138
  2. [5]Hoffmann M, Hilton-Taylor C, Angulo A, Böhm M, Brooks TM, et al (2010) The Impact of conservation on the status of the world's vertebrates. Science 330: 1503– 1509. 20978281
  3. [6]Conde DA, Flesness N, Colchero F, Jones OR, Scheuerlein A (2011) An emerging role of zoos to conserve biodiversity. Science 331: 1390– 1391. 21415339
  4. [11]Saito TR, Motomura N, Taniguchi K, Hokao R, Arkin A, et al (1996) Effect of cage size on sexual behavior pattern in male rats. Contemp Top Lab Anim Sci 35: 80– 82. 16457502
  5. [13]Huber S, Palme R, Arnold W (2003) Effects of season, sex, and sample collection on concentrations of fecal cortisol metabolites in red deer (Cervus elaphus). Gen Comp Endocrinol 130: 48– 54. 12535624
  6. [17]Li C, Jiang Z, Tang S, Zeng Y (2007) Influence of enclosure size and animal density on fecal cortisol concentration and aggression in Pere David's deer stags. Gen Comp Endocrinol 151: 202– 209. 17324429
  7. [19]Liptrap RM (1993) Stress and reproduction in domestic animals. Ann N Y Acad Sci 697: 275– 284. 8257018
  8. [20]Dobson H, Smith RF (1995) Stress and reproduction in farm animals. J Reprod Fertil Suppl 49: 451–461. 7623334
  9. [21]Möstl E, Palme R (2002) Hormones as indicators of stress. Domest Anim Endocrinol 23: 67– 74. 12142227
  10. [23]Touma C, Palme R (2005) Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann N Y Acad Sci 1046: 54– 74. 16055843
  11. [27]Morrow CJ, Kolver ES, Verkerk GA, Matthews LR (2002) Fecal glucocorticoid metabolites as a measure of adrenal activity in dairy cattle. Gen Comp Endocrinol 126: 229– 241. 12030779
  12. [28]Brown JL, Wasser SK, Wildt DE, Graham LH (1994) Comparative aspects of steroid hormone metabolism and ovarian activity in felids, measured noninvasively in feces. Biol Reprod 51: 776– 786. 7819459
  13. [29]Young KM, Walker SL, Lanthier C, Waddell WT, Monfort SL, et al (2004) Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. Gen Comp Endocrinol 137: 148– 165. 15158127
  14. [35]Schatz S, Palme R (2001) Measurement of faecal cortisol metabolites in cats and dogs: a non-invasive method for evaluating adrenocortical function. Vet Res Commun 25: 271– 287. 11432429
  15. [36]Teskey-Gerstl A, Bamberg E, Steineck T, Palme R (2000) Excretion of corticosteroids in urine and faeces of hares (Lepus europaeus). J Comp Physiol B 170: 163– 168. 10791576
  16. [38]Möstl E, Messmann S, Bagu E, Robia C, Palme R (1999) Measurement of glucocorticoid metabolite concentrations in faeces of domestic livestock. Zentralbl Veterinarmed A 46: 621– 631. 10638300
  17. [39]Bahr NI, Palme R, Möhle U, Hodges JK, Heistermann M (2000) Comparative aspects of the metabolism and excretion of cortisol in three individual nonhuman primates. Gen Comp Endocrinol 117: 427– 438. 10764553
  18. [40]Cavigelli SA, Monfort SL, Whitney TK, Mechref YS, Novotny M, et al (2005) Frequent serial fecal corticoid measures from rats reflect circadian and ovarian corticosterone rhythms. J Endocrinol 184: 153– 163. 15642792
  19. [44]van Lier E, Pérez-Clariget R, Forsberg M (2003) Sex differences in cortisol secretion after administration of an ACTH analogue in sheep during the breeding and non-breeding season. Anim Reprod Sci 79: 81– 92. 12853181
  20. [45]Buirski P, Plutchik R, Kellerman H (1978) Sex differences, dominance, and personality in the chimpanzee. Anim Behav 26: 123– 129. 565175
  21. [47]Bubenik GA, Schams D, White RG, Rowell J, Blake J, et al (1998) Seasonal levels of metabolic hormones and substrates in male and female reindeer (Rangifer tarandus). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 120: 307– 315. 9827045
  22. [48]Gray JA (1987) The psychology of fear and stress. Cambridge: Cambridge University Press. 436 p.
  23. [49]Eriksson H, Gustafsson J-Å (1970) Steroids in germfree and conventional rats. Eur J Biochem 15: 132– 139. 5489830
  24. [50]Ottenweller JE, Meier AH, Russo AC, Frenzke ME (1979) Circadian rhythms of plasma corticosterone binding activity in the rat and the mouse. Acta Endocrinol 91: 150– 157. 452825
  25. [51]Woodward CJ, Hervey GR, Oakey RE, Whitaker EM (1991) The effects of fasting on plasma corticosterone kinetics in rats. Br J Nutr 66: 117– 127. 1931899
  26. [52]Harper JM, Austad SN (2001) Effect of capture and season on fecal glucocorticoid levels in deer mice (Peromyscus maniculatus) and red-backed voles (Clethrionomys gapperi). Gen Comp Endocrinol 123: 337– 344. 11589634
  27. [53]Strier KB, Ziegler TE, Wittwer DJ (1999) Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Horm Behav 35: 125– 134. 10202120
  28. [56]Thitaram C, Brown JL, Pongsopawijit P, Chansitthiwet S, Wongkalasin W, et al (2008) Seasonal effects on the endocrine pattern of semi-captive female Asian elephants (Elephas maximus): Timing of the anovulatory luteinizing hormone surge determines the length of the estrous cycle. Theriogenology 69: 237– 244. 17997149
  29. [57]Christison GI, Johnson HD (1972) Cortisol turnover in heat-stressed cows. J Anim Sci 35: 1005– 1010. 5085291
  30. [59]Cyr NE, Romero LM (2008) Fecal glucocorticoid metabolites of experimentally stressed captive and free-living starlings: implications for conservation research. Gen Comp Endocrinol 158: 20– 28. 18554600
  31. [60]Poessel SA, Biggins DE, Santymire RM, Livieri TM, Crooks KR, et al (2011) Environmental enrichment affects adrenocortical stress responses in the endangered black-footed ferret. Gen Comp Endocrinol 172: 526– 533. 21549121
  32. [61]Tan HM, Ong SM, Langat G, Bahaman AR, Sharma RSK, et al (2013) The influence of enclosure design on diurnal activity and stereotypic behaviour in captive Malayan Sun bears (Helarctos malayanus). Res Vet Sci 94: 228– 239. 23141171
  33. [65]Rajagopal T, Archunan G, Sekar M (2011) Impact of zoo visitors on the fecal cortisol levels and behavior of an endangered species: Indian blackbuck (Antelope cervicapra L.). J Appl Anim Welf Sci 14: 18– 32. 21191845

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Authors
Khonmee, J., Brown, J. L., Rojanasthien, S., Aunsusin, A., Thumasanukul, D., Kongphoemphun, A., Siriaroonrat, B., Tipkantha, W., Punyapornwithaya, V., & Thitaram, C.
Affiliations
  • Chiang Mai University (TH)
  • Smithsonian Conservation Biology Institute (US)
  • Department of National Parks Wildlife and Plant Conservation (TH)
  • Zoological Park Organization (TH)
Corresponding author
  • Khonmee, Jaruwan
  • Thitaram, Chatchote
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2014-03-17
Volume
9
Issue
3
Pages
e91633
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0091633
PMC
PMC3956719
OpenAlex
W2046350267
Cited by
22
References
5
Citations by year
2026: 2 · 2024: 1 · 2023: 4 · 2022: 1 · 2021: 3 · 2020: 3 · 2019: 2 · 2018: 1 · 2017: 2 · 2016: 2 · 2015: 1
FWCI
2.44
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, public-domain)
  • Europe PMC (PubMed Central) (publishedVersion, public-domain)
  • PubMed Central (publishedVersion, public-domain)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Smithsonian Digital Repository (Smithsonian Institution) (submittedVersion)
Funders
  • Smithsonian Institution
  • Chiang Mai University
  • National Research Council of Thailand
  • Smithsonian Conservation Biology Institute
  • Faculty of Veterinary Medicine, Chiang Mai University
Topics
  • Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
  • Physical Sciences › Environmental Science › Ecology › Wildlife Ecology and Conservation
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
Keywords
Naemorhedus griseus, fecal glucocorticoid metabolites, captive animal welfare, animal density, seasonal variation, sex differences, adrenal function, zoo management, endangered species conservation, reintroduction
MeSH terms
Animals, Feces, Female, Glucocorticoids, Male, Ruminants, Seasons, Thailand, Metabolomics

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