Abstract
The level of glucocorticoids, especially if obtained from noninvasive sampling, can be used as an index of animal well-being, allowing evaluation of the animal’s response to environmental modifications. Despite evidence that these hormones play a relevant role in energy metabolism regulation in perceived or real stress events, little is known regarding the factors that could modify the capability of animals to cope with relocation events. The aim of this research was to assess fecal cortisol metabolite concentrations before, during and after acute stress (transfer and relocation event) in two well-established social groups of Tonkean macaques (Macaca tonkeana). The results showed that the fecal levels of cortisol increased in individuals of both groups in response to the stress event, with a similar trend in males and females. Hormone levels were back to baseline values in both groups a few days after transfer and relocation. The presence of known social partners could be one of the factors that possibly facilitated the adaptation process.
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References
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
Bardi M, Shimizu K, Barrett GM, Borgognini-Tarli SM, Huffman MA (2003) Peripartum cortisol levels and mother-infant interactions in Japanese macaques. Am J Phys Anthropol 120:298–304
Brown JL, Bellem AC, Fouraker M, Wildt DE, Roth TL (2001) Comparative analysis of gonadal and adrenal activity in the black and white rhinoceros in North America by noninvasive endocrine monitoring. Zoo Biol 20:463–486
Carr BR, Parker CR Jr, Madden JD, MacDonald PC, Porter JC (1981) Maternal plasma adrenocorticotropin and cortisol relationships throughout human pregnancy. Am J Obstet Gynecol 139:416–422
Cavigelli SA, Monfort SL, Whitney TK, Mechref YS, Novotny M, McClintock MK (2005) Frequent serial fecal corticoid measures from rats reflect circadian and ovarian corticosterone rhythms. J Endocrinol 184:153–163
Chelini MO, Otta E, Yamakita C, Palme R (2010) Sex differences in the excretion of fecal glucocorticoid metabolites in the Syrian hamster. J Comp Physiol B 180:919–925
Creel S, Christianson D, Schuette P (2013) Glucocorticoid stress responses of lions in relationship to group composition, human land use, and proximity to people. Conserv Physiol 1:cot021. doi:10.1093/conphys/cot021
Davenport MD, Tiefenbacher S, Lutz CK, Novak MA, Meyer JS (2006) Analysis of endogenous cortisol concentrations in the hair of rhesus macaques. Gen Comp Endocrinol 147:255–261
Davenport MD, Lutz CK, Tiefenbacher S, Novak MA, Meyer JS (2008) A rhesus monkey model of self-injury: effects of relocation stress on behavior and neuroendocrine function. Biol Psychiatry 63:990–996
Dufour V, Sueur C, Whiten A, Buchanan-Smith HM (2011) The impact of moving to a novel environment on social networks, activity and wellbeing in two New World primates. Am J Primatol 73:802–811
Ezenwa VO, Ekernas LS, Creel S (2012) Unravelling complex associations between testosterone and parasite infection in the wild. Funct Ecol 26:123–133
Fernström AL, Sutian W, Royo F, Westlund K, Nilsson T, Carlsson HE, Paramastri Y, Pamungkas J, Sajuthi D, Schapiro SJ, Hau J (2008) Stress in cynomolgus monkeys (Macaca fascicularis) subjected to long-distance transport and simulated transport housing conditions. Stress 11:467–476
Goymann 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 Ecol Evol 3:757–765
Heinsbroek RP, VanHaaren F, Feenstra MG, Endert E, Van de Poll NE (1991) Sex- and time-dependent changes in neurochemical and hormonal variables induced by predictable and unpredictable footshock. Physiol Behav 49:1251–1256
Honess PE, Johnson PJ, Wolfensohn SE (2004) A study of behavioural responses of non-human primates to air transport and re-housing. Lab Anim 38:119–132
Landi MS, Kreider JW, Lang CM, Bullock LP (1982) Effects of shipping on the immune function in mice. Am J Vet Res 43:1654–1657
Maestripieri D, Hoffman CL, Fulks R, Gerald MS (2008) Plasma cortisol responses to stress in lactating and nonlactating female rhesus macaques. Horm Behav 53:170–176
McGlone JJ, Salak JL, Lumpkin EA, Nicholson RI, Gibson M, Norman RL (1993) Shipping stress and social status effects on pig performance, plasma cortisol, natural killer cell activity, and leukocyte numbers. J Anim Sci 71:888–896
Möhle U, Heistermann M, Palme R, Hodges JK (2002) Characterization of urinary and fecal metabolites of testosterone and their measurement for assessing gonadal endocrine function in male nonhuman primates. Gen Comp Endocrinol 129:135–145
Norcross JL, Newman JD (1999) Effects of separation and novelty on distress vocalizations and cortisol in the common marmoset (Callithrix jacchus). Am J Primatol 47:209–222
O’Connor KA, Brindle E, Shofer J, Trumble BC, Aranda JD, Rice K, Tatar M (2011) The effects of a long-term psychosocial stress on reproductive indicators in the baboon. Am J Phys Anthropol 145:629–638
Palme R, Fischer P, Schildorfer H, Ismail MN (1996) Excretion of infused 14C-steroid hormones via faeces and urine in domestic livestock. Anim Reprod Sci 43:43–63
Raminelli JLF, Corderio de Sousa MB, Cunha MS, Barbosa FV (2001) Morning and afternoon patterns of fecal cortisol excretion among reproductive and non-reproductive male and female common marmosets, Callithrix jacchus. Biol Rhythm Res 32:159–167
Reimers M, Schwarzenberger F, Preuschoft S (2007) Rehabilitation of research chimpanzees: stress and coping after long-term isolation. Horm Beh 51:428–435
Running A (2015) Decreased cortisol and pain in breast cancer: biofield therapy potential. Evid Based Complement Altern Med. doi:10.1155/2015/870640 (article ID 870640)
Schaffner CM, Smith TE (2005) Familiarity may buffer the adverse effects of relocation on marmosets (Callithrix kuhlii): Preliminary evidence. Zoo Biol 24:93–100
Schapiro SJ, Lambeth SP, Rosenmaj JK, Williams LE, Nehete BN, Nehete PN (2012) Physiological and welfare consequences of transport, relocation, and acclimatization of chimpanzees (Pan troglodytes). Appl Anim Behav Sci 137:183–193
Schatz S, Palme R (2001) Measurement of faecal cortisol metabolites in cats and dogs: a noninvasive method for evaluating adrenocortical function. Vet Res Commun 25:271–287
Shamim W, Yousufuddin M, Bakhai A, Coats AJS, Honour JW (2000) Gender differences in the urinary excretion rates of cortisol and androgen metabolites. Ann Clin Biochem 37:770–774
Stavisky RC, Watson SL, Anthony MS, Manuck SB, Adams MR, Kaplan JR (2003) Influence of estradiol on cortisol secretion in ovariectomized cynomolgus macaques (Macaca fascicularis). Am J Primatol 60:17–22
Suomi SJ, Eisele CD, Grady SA, Harlow HF (1975) Depressive behavior in adult monkeys following separation from family environment. J Abnorm Psychol 84:576–578
Thierry B (2007) Unity in diversity: lessons from macaque societies. Evolut Anthropol 16:224–238
Thierry B (2010) The macaques: a double-layered social organization. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (eds) Primates in perspective. Oxford University Press, Oxford, pp 229–241
Thierry B, Heistermann M, Aujard F, Hodges JK (1996) Long-term data on basic reproductive parameters and evaluation of endocrine, morphological, and behavioral measures for monitoring reproductive status in a group of semifree-ranging Tonkean macaques (Macaca tonkeana). Am J Primatol 39:47–62
Touma C, Möstl E, Sachser N, Palme R (2003) Effect of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen Comp Endocrinol 130:267–278
van Ruiven R, Meijer GW, Wiersma A, Baumans V, van Zutphen LFM, Ritskes-Hoitinga J (1998) The influence of transportation stress on selected nutritional parameters to establish the necessary minimum period for adaptation in rat feeding studies. Lab Anim 32:446–456
Watson SL, McCoy JG, Stavisky RC, Greer TF, Hanbury D (2005) Cortisol response to relocation stress in Garnett’s bushbaby (Otolemur garnettii). Contemp Top Lab Anim Sci 44:22–24
Wolfensohn SE (1997) Brief review of scientific studies of the welfare implications of transporting primates. Lab Anim 31:303–305
Yamanashi Y, Teramoto M, Morimura N, Hirata S, Inoue-Murayama M, Idani G (2016) Effects of relocation and individual and environmental factors on the long-term stress levels in captive chimpanzees (Pan troglodytes): monitoring hair cortisol and behaviors. PLoS One 11:e0160029. doi:10.1371/journal.pone.0160029
Ziegler TE, Scheffler G, Snowdon CT (1995) The relationship of cortisol levels to social environment and reproductive functioning in female cotton-top tamarins, Saguinus oedipus. Horm Behav 29:407–424
Acknowledgements
The authors are grateful to Faye Abbiate, Emiliano Manzo, Melissa Messinese, Cristina Sagnotti and Elena Vero for the collection, and to Antonella Tramutola, Maria Libera Sparago and Manuela Zinni for the processing of fecal samples; our thanks also go to Alessandro Giuliani for help in statistical analysis, and to Monica Carosi for contribution to early development of the project. Sasha Gelpke is kindly acknowledged for her encouragement to investigate the effects of relocation of the Tonkean macaques. We are grateful to the two anonymous reviewers for their help in improving the manuscript. Finally we thank Ludovica Cervi for language revision. Fondazione Ethoikos supported this work. Carlo Cinque and Anna Rita Zuena were supported by Fondazione Ethoikos training grants.
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Our research complied with the ethical standards and guidelines laid down by the EC Guide for Animal Experiments and with Italian national laws (D.L. 116/92, D.L. 26/2014).
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Cinque, C., De Marco, A., Mairesse, J. et al. Relocation stress induces short-term fecal cortisol increase in Tonkean macaques (Macaca tonkeana). Primates 58, 315–321 (2017). https://doi.org/10.1007/s10329-016-0590-7
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DOI: https://doi.org/10.1007/s10329-016-0590-7