Seasonal variations in immunoreactive cortisol and fecal immunoglobulin levels in Sichuan golden monkey (Rhinopithecus roxellana)

The Sichuan golden monkey is deserving of conservation and the welfare of this species is receiving increasing attention. However, it is difficult to identify physiological parameters for assessing its conservation status. In the present study, we employed noninvasive sampling methods and immunochemical assays to determine if measurements of cortisol and immunoglobulin in feces allowed monitoring of physiological status. The results indicated that the cortisol and immunoglobulin concentrations in feces could serve as biomarkers for monitoring stress and immune status, and that there was a relationship between stress and the immune response. A tendency toward seasonal fluctuation in immunoreactive cortisol and fecal immunoglobulin concentrations emerged, indicating that these indices could be useful tools for monitoring the welfare of the monkey and could be used in the field of wildlife research.

Seasonal variations in immunoreactive cortisol and fecal immunoglobulin levels in Sichuan golden monkey (Rhinopithecus roxellana)

The Sichuan golden monkey is deserving of conservation and the welfare of this species is receiving increasing attention. However, it is difficult to identify physiological parameters for assessing its conservation status. In the present study, we employed noninvasive sampling methods and immunochemical assays to determine if measurements of cortisol and immunoglobulin in feces allowed monitoring of physiological status. The results indicated that the cortisol and immunoglobulin concentrations in feces could serve as biomarkers for monitoring stress and immune status, and that there was a relationship between stress and the immune response. A tendency toward seasonal fluctuation in immunoreactive cortisol and fecal immunoglobulin concentrations emerged, indicating that these indices could be useful tools for monitoring the welfare of the monkey and could be used in the field of wildlife research.

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  • Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T et al. (2003). Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43: 67–82.
  • Aggarwal A, Upadhyay R (2013). Heat stress and immune function. In: Aggarwal A, Upadhyay R, editors. Heat Stress and Animal Productivity. New Delhi, India: Springer India, pp. 113–136.
  • Axelrod J, Reisine TD (1984). Stress hormones: their interaction and regulation. Science 224: 452–459.
  • Bubenik GA, Bubenik AB, Schams D, Leatherland JF (1983). Circadian and circannual rhythms of LH, FSH, testosterone (T), prolactin, cortisol, T3 and T4 in plasma of mature, white- tailed deer. Com Biochem Phys A 76: 37–45.
  • Cavigelli SA (1999). Behavioural patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs (Lemur catta). Anim Behav 57: 935–944.
  • Clark JD, Rager DR, Calpin JP (1997). Animal well-being IV. Specific assessment criteria. Comparative Med 47: 586–597.
  • Fan SG, Shao L, Ding GF (1996). A suppressive protein generated in peripheral lymph tissue induced by restraint stress. J Neuroimmunol 6: 279–288.
  • Ganswindt A, Palme R, Heistermann M, Borraganc S, Hodges JK (2003). Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. Gen Comp Endocr 134: 156–166.
  • Heistermann M (2010). Non-invasive monitoring of endocrine status in laboratory primates: methods, guidelines and applications. Advances in Science and Research 5: 1–9.
  • Hofer H, East ML (1998). Biological conservation and stress. Adv Stud Behav 27: 405–525.
  • Kirkpatrick RC (1995). The natural history and conservation of the snub-nosed monkeys (genus Rhinopithecus). Biol Conserv 72: 363–369.
  • Kirkpatrick RC (1998). Ecology and behavior of the doucs and snub- nosed monkeys. In: Jablonksi NG, editor. The Natural History of the Doucs and Snub-nosed Monkeys. Singapore: World ScientiŞc Press, pp. 155–190.
  • Kirkpatrick RC, Grueter CC (2010). Snub-nosed monkeys: multilevel societies across varied environments. Evol Anthropol 19: 98– 113.
  • Möstl E, Palme R (2002). Hormones as indicators of stress. Domest Anim Endocrin 23: 67–74.
  • Muehlenbein MP (2009). The application of endocrine measures in primate parasite ecology. In: Huffman MA, Chapman CA, editors. Primate Parasite Ecology: The Dynamics and Study of Host–Parasite Relationships. Cambridge, UK: Cambridge University Press, pp. 63–81.
  • Nigel JC (2012). Review: minimally invasive sampling media and the measurement of corticosteroids as biomarkers of stress in animals. Can J Anim Sci 92: 227–259.
  • Paramastri Y, Royo F, Eberova J, Carlsson HE, Sajuthi D, Fernstrom AL, Pamungkas J, Hau J (2007). Urinary and fecal immunoglobulin A, cortisol and 11-17 dioxoandrostanes, and serum cortisol in metabolic cage housed female cynomolgus monkeys (Macaca fascicularis). J Med Primatol 36: 355–364.
  • Peters IR, Calvert EL, Hall EJ, Day MJ (2004). Measurement of immunoglobulin concentrations in the feces of healthy dogs. Clin Vaccine Immunol 11: 841–848.
  • Quillfeldt P, Poisbleau M, Parenteau C, Trouvé C, Demongin L, van Noordwijk HJ, Möstl E (2011). Measuring corticosterone in seabird egg yolk and the presence of high yolk gestagen concentrations. Gen Comp Endocr 173: 11–14.
  • Rehbinder C, Hau J (2006). Quantification of cortisol, cortisol immunoreactive metabolites, and immunoglobulin A in serum, saliva, urine, and feces for noninvasive assessment of stress in reindeer. Can J Vet Res 70: 151–154.
  • Ren BP, Zhang SY, Xia SZ, Li QF, Liang B, Lu MQ (2003). Annual reproductive behavior of Rhinopithecus roxellana. Int J Primatol 24: 575–589.
  • Ren RM, Yan KH, Su YJ, Zhou Y, Li JJ, Zhu ZQ, Hu ZL, Hu YF (2000). A Field Study of the Society of Rhinopithecus roxellana. Beijing, China: Beijing University Press.
  • Royo F, Björk N, Carlsson HE, Mayo S, Hau J (2004). Impact of chronic catheterization and automated blood sampling (Accusampler) on serum corticosterone and fecal corticosterone and immunoglobulin A in male rats. J Endocrinol 180: 145–153.
  • Sapolsky RM, Romero LM, Munck AU (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21: 55–89.
  • Schiml PA, Mendoza SP, Saltzman W, Lyons DM, Mason WA (1996). Seasonality in squirrel monkeys (Saimiri sciureus): social facilitation by females. Physiol Behav 60: 1105–1113.
  • Shutt K, Setchell JM, Heistermann M (2012). Non-invasive monitoring of physiological stress in the western lowland gorilla (Gorilla gorilla gorilla): validation of a fecal glucocorticoid assay and methods for practical application in the field. Gen Comp Endocr 179: 167–177.
  • Smith RS, Sherman NA, Middleton JRE (1972). Effect of hydrocortisone on immunoglobulin synthesis and secretion by human peripheral lymphocytes in vitro. Int Arch Allergy Imm 43: 859–870.
  • Sterck EHM (2012). The behavioral ecology of colobine monkeys. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB, editors. The Evolution of Primate Societies. Chicago, IL, USA: University of Chicago Press, pp. 65–90.
  • Tan CL, Guo ST, Li BG (2007). Population structure and ranging patterns of Rhinopithecus roxellana in Zhouzhi National Nature Reserve, Shaanxi, China. Int J Primatol 28: 577–591.
  • Taylor BC, Brotheridge RM, Jessup DA, Stott JL (2002). Measurement of serum immunoglobulin concentration in killer whales and sea otters by radial immunodiffusion. Vet Immunol Immunop 89: 187–195.
  • Turton JA, Ladds PW, Manolis SC, Webb GJW (1997). Relationship of blood corticosterone, immunoglobulin and haematological values in young crocodiles (Crocodylus porosus) to water temperature, clutch of origin and body weight. Aust Vet J 75: 114–119.
  • Wang YX, Jiang XL, Li DW (1998). Classification and distribution of the extant subspecies of golden snub-nosed monkey (Rhinopithecus [Rhinopithecus] roxellana). In: Oxnard CE, editor. The Natural History of the Doucs and Snub-nosed Monkeys. Singapore: World Scientific Publishing Company, pp. 53–64.
  • Wingfield JC, Sapolsky RM (2003). Reproduction and resistance to stress: when and how. J Neuroendocrinol 15: 711–724.
  • Young AM, Hallford DM (2013). Validation of a fecal glucocorticoid metabolite assay to assess stress in the Budgerigar (Melopsittacus undulatus). Zoo Biol 32: 112–116.
  • Yu XJ, Hu DF, Jin XL, Ge XF, Yang LL, Zhao PP, Zhang Q (2011). Non- invasive determination of fecal steroid hormones relating to conservation practice in giant panda (Ailuropoda melanoleuca). Anim Biol 61: 335–347.
  • Zhang S, Liang B, Wang L (2000). Seasonality of matings and births in captive Sichuan golden monkeys (Rhinopithecus roxellana). Am J Primatol 51: 265–269.
Turkish Journal of Zoology-Cover
  • ISSN: 1300-0179
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
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