Non-invasive evaluation of stress hormone responses in a captive population of sugar gliders (Petaurus breviceps)
Juan Scheun A B F , Fritz Geiser C , Andre Ganswindt A B D and Julia Nowack C E
+ Author Affiliations
- Author Affiliations
A National Zoological Garden, South African National Biodiversity Institute, P.O. Box 754, Pretoria, 0001, South Africa.
B Mammal Research Institute, University of Pretoria, Pretoria 0028, Republic of South Africa.
C Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, NSW 2351, Australia.
D Endocrine Research Laboratory, Department of Anatomy and Physiology, University of Pretoria, Onderstepoort 0110, South Africa.
E School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK.
F Corresponding author. Email: J.Scheun@sanbi.org.za
Australian Mammalogy 42(2) 176-184 https://doi.org/10.1071/AM18044
Submitted: 17 October 2018 Accepted: 17 July 2019 Published: 6 September 2019
Abstract
Faecal hormone monitoring offers a robust tool to non-invasively determine the physiological stress experienced by an individual when faced with natural or human-driven stressors. Although already quantified for several species, the method needs to be validated for each new species to ensure reliable quantification of the respective glucocorticoids. Here we investigated whether measurement of faecal glucocorticoid metabolite (fGCM) provides a feasible and non-invasive way to assess the physiological state of sugar gliders (Petaurus breviceps), an arboreal marsupial native to Australia, by using both a biological and physiological validation. Our analysis confirmed that the cortisol enzyme immunoassay (EIA) was the most appropriate assay for monitoring fGCM concentrations in sugar gliders. Comparing the fGCM response to the physiological and the biological validation, we found that while the administration of ACTH led to a significant increase in fGCM concentration in all individuals, only six of eight individuals showed a considerable fGCM response following the biological validation. Our study identified the most appropriate immunoassay for monitoring fGCM concentrations as an indicator of physiological stress in sugar gliders, but also supports recent suggestions that, if possible, both biological and physiological stressors should be used when testing the suitability of an EIA for a species.
Additional keywords: ACTH challenge, faecal glucocorticoid metabolites, individual variation, physiological stress, separation.
References
Behringer, V., and Deschner, T. (2017). Non-invasive monitoring of physiological markers in primates. Hormones and Behavior 91, 3–18.| Non-invasive monitoring of physiological markers in primates.Crossref | GoogleScholarGoogle Scholar | 28202354PubMed |
Bosson, C. O., Palme, R., and Boonstra, R. (2009). Assessment of the stress response in Columbian ground squirrels: laboratory and field validation of an enzyme immunoassay for fecal cortisol metabolites. Physiological and Biochemical Zoology 82, 291–301.
| Assessment of the stress response in Columbian ground squirrels: laboratory and field validation of an enzyme immunoassay for fecal cortisol metabolites.Crossref | GoogleScholarGoogle Scholar | 19335228PubMed |
Brearley, G., McAlpine, C., Bell, S., and Bradley, A. (2012). Influence of urban edges on stress in an arboreal mammal: a case study of squirrel gliders in southeast Queensland, Australia. Landscape Ecology 27, 1407–1419.
| Influence of urban edges on stress in an arboreal mammal: a case study of squirrel gliders in southeast Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |
Brown, J. L., Wasser, S. K., Wildt, D. E., and Graham, L. H. (1994). Comparative aspects of steriod-hormone metabolism and ovarian activity in felids, measured noninvasively in feces. Biology of Reproduction 51, 776–786.
| Comparative aspects of steriod-hormone metabolism and ovarian activity in felids, measured noninvasively in feces.Crossref | GoogleScholarGoogle Scholar | 7819459PubMed |
Burbidge, A. A., and McKenzie, N. L. (1989). Patterns in the modern decline of western Australia’s vertebrate fauna: causes and conservation implications. Biological Conservation 50, 143–198.
| Patterns in the modern decline of western Australia’s vertebrate fauna: causes and conservation implications.Crossref | GoogleScholarGoogle Scholar |
Charmandari, E., Tsigos, C., and Chrousos, G. (2005). Endocrinology of the stress response. Annual Review of Physiology 67, 259–284.
| Endocrinology of the stress response.Crossref | GoogleScholarGoogle Scholar | 15709959PubMed |
Christian, N., and Geiser, F. (2007). To use or not to use torpor? Activity and body temperature as predictors. Naturwissenschaften 94, 483–487.
| To use or not to use torpor? Activity and body temperature as predictors.Crossref | GoogleScholarGoogle Scholar | 17252241PubMed |
Cockrem, J. F. (2013). Individual variation in glucocorticoid stress responses in animals. General and Comparative Endocrinology 181, 45–58.
| Individual variation in glucocorticoid stress responses in animals.Crossref | GoogleScholarGoogle Scholar | 23298571PubMed |
Cohen, S., Janicki-Deverts, D., and Miller, G. E. (2007). Psychological stress and disease. Journal of the American Medical Association 298, 1685–1687.
| Psychological stress and disease.Crossref | GoogleScholarGoogle Scholar | 17925521PubMed |
Creel, S., Dantzer, B., Goymann, W., and Rubenstein, D. R. (2013). The ecology of stress: effects of the social environment. Functional Ecology 27, 66–80.
| The ecology of stress: effects of the social environment.Crossref | GoogleScholarGoogle Scholar |
Fichtel, C., Kraus, C., Ganswindt, A., and Heistermann, M. (2007). Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux’s sifakas (Propithecus verreauxi). Hormones and Behavior 51, 640–648.
| Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux’s sifakas (Propithecus verreauxi).Crossref | GoogleScholarGoogle Scholar | 17448474PubMed |
Fieß, M., Heistermann, M., and Hodges, J. K. (1999). Patterns of urinary and fecal steroid excretion during the ovarian cycle and pregnancy in the African elephant (Loxodonta africana). General and Comparative Endocrinology 115, 76–89.
| Patterns of urinary and fecal steroid excretion during the ovarian cycle and pregnancy in the African elephant (Loxodonta africana).Crossref | GoogleScholarGoogle Scholar | 10375466PubMed |
Ganswindt, A., Tordiffe, A. S. W., Stam, E., Howitt, M. J., and Jori, F. (2012). Determining adrenocortical activity as a measure of stress in African buffalo (Syncerus caffer) based on faecal analysis. African Zoology 47, 261–269.
| Determining adrenocortical activity as a measure of stress in African buffalo (Syncerus caffer) based on faecal analysis.Crossref | GoogleScholarGoogle Scholar |
Goymann, W., Möstl, E., Van’t Hof, T., East, M. L., and Hofer, H. (1999). Noninvasive fecal monitoring of glucocorticoids in spotted hyenas, Crocuta crocuta. General and Comparative Endocrinology 114, 340–348.
| Noninvasive fecal monitoring of glucocorticoids in spotted hyenas, Crocuta crocuta.Crossref | GoogleScholarGoogle Scholar | 10336822PubMed |
Guimont, F. S., and Wynne-Edwards, K. E. (2006). Individual variation in cortisol responses to acute ‘on-back’ restraint in an outbred hamster. Hormones and Behavior 50, 252–260.
| Individual variation in cortisol responses to acute ‘on-back’ restraint in an outbred hamster.Crossref | GoogleScholarGoogle Scholar | 16697381PubMed |
Heistermann, M. (2010). Non-invasive monitoring of endocrine status in laboratory primates: methods, guidelines and applications. Advances in Science and Research 5, 1–9.
| Non-invasive monitoring of endocrine status in laboratory primates: methods, guidelines and applications.Crossref | GoogleScholarGoogle Scholar |
Hennessy, M. B., Mendoza, S. P., and Kaplan, J. N. (1982). Behavior and plasma cortisol following brief peer separation in juvenile squirrel monkeys. American Journal of Primatology 3, 143–151.
| Behavior and plasma cortisol following brief peer separation in juvenile squirrel monkeys.Crossref | GoogleScholarGoogle Scholar |
Hennessy, M. B., Zate, R., and Maken, D. S. (2008). Social buffering of the cortisol response of adult female guinea pigs. Physiology & Behavior 93, 883–888.
| Social buffering of the cortisol response of adult female guinea pigs.Crossref | GoogleScholarGoogle Scholar |
Henry, S., and Suckling, G. (1984). A review of the ecology of the sugar glider. In ‘Possums and gliders’. (Eds A. Smith and I. Hume.) pp. 355–358. (Australian Mammal Society: Sydney, NSW.)
Hing, S., Narayan, E., Thompson, R. C. A., and Godfrey, S. (2014). A review of factors influencing the stress response in Australian marsupials. Conservation Physiology 2, cou027.
| A review of factors influencing the stress response in Australian marsupials.Crossref | GoogleScholarGoogle Scholar | 27293648PubMed |
Hodges, K., Brown, J., and Heistermann, M. (2010). Endocrine monitoring of reproduction and stress. In ‘Wild mammals in captivity: principles and techniques for zoo management’. (Eds D.G. Kleiman, K.V. Thompson and C.K. Baer.) pp. 447–468. (University of Chicago: Chicago, IL, USA.)
Jepsen, E. M., Ganswindt, A., Ngcamphalala, C. A., Bourne, A. R., Ridley, A. R., and McKechnie, A. E. (2019). Non-invasive monitoring of physiological stress in an afrotropical arid-zone passerine bird, the southern pied babbler. General and Comparative Endocrinology 276, 60–68.
| Non-invasive monitoring of physiological stress in an afrotropical arid-zone passerine bird, the southern pied babbler.Crossref | GoogleScholarGoogle Scholar | 30836104PubMed |
Koolhaas, J. M., de Boer, S. F., Buwalda, B., and van Reenen, K. (2007). Individual variation in coping with stress: a multidimensional approach of ultimate and proximate mechanisms. Brain, Behavior and Evolution 70, 218–226.
| Individual variation in coping with stress: a multidimensional approach of ultimate and proximate mechanisms.Crossref | GoogleScholarGoogle Scholar | 17914253PubMed |
Koolhaas, J., De Boer, S., Coppens, C., and Buwalda, B. (2010). Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Frontiers in Neuroendocrinology 31, 307–321.
| Neuroendocrinology of coping styles: towards understanding the biology of individual variation.Crossref | GoogleScholarGoogle Scholar | 20382177PubMed |
Körtner, G., and Geiser, F. (2000). Torpor and activity patterns in free-ranging sugar gliders Petaurus breviceps (Marsupialia). Oecologia 123, 350–357.
| Torpor and activity patterns in free-ranging sugar gliders Petaurus breviceps (Marsupialia).Crossref | GoogleScholarGoogle Scholar | 28308589PubMed |
Kudielka, B. M., and Kirschbaum, C. (2005). Sex differences in HPA axis responses to stress: a review. Biological Psychology 69, 113–132.
| Sex differences in HPA axis responses to stress: a review.Crossref | GoogleScholarGoogle Scholar | 15740829PubMed |
Laver, P. N., Ganswindt, A., Ganswindt, S. B., and Alexander, K. A. (2012). Non-invasive monitoring of glucocorticoid metabolites in banded mongooses (Mungos mungo) in response to physiological and biological challenges. General and Comparative Endocrinology 179, 178–183.
| Non-invasive monitoring of glucocorticoid metabolites in banded mongooses (Mungos mungo) in response to physiological and biological challenges.Crossref | GoogleScholarGoogle Scholar | 22926328PubMed |
Lincoln, G. A., Almeida, O. F. X., Klandorf, H., and Cunningham, R. A. (1982). Hourly fluctuations in the blood levels of melatonin, prolactin, luteinizing hormone, follicle-stimulating hormone, testosterone, tri-iodothyronine, thyroxine and cortisol in rams under artificial photoperiods, and the effects of cranial sympathectomy. The Journal of Endocrinology 92, 237–250.
| Hourly fluctuations in the blood levels of melatonin, prolactin, luteinizing hormone, follicle-stimulating hormone, testosterone, tri-iodothyronine, thyroxine and cortisol in rams under artificial photoperiods, and the effects of cranial sympathectomy.Crossref | GoogleScholarGoogle Scholar | 7199556PubMed |
Ludwig, C., Wachter, B., Silinski-Mehr, S., Ganswindt, A., Bertschinger, H., Hofer, H., and Dehnhard, M. (2013). Characterisation and validation of an enzyme-immunoassay for the non-invasive assessment of faecal glucocorticoid metabolites in cheetahs (Acinonyx jubatus). General and Comparative Endocrinology 180, 15–23.
| Characterisation and validation of an enzyme-immunoassay for the non-invasive assessment of faecal glucocorticoid metabolites in cheetahs (Acinonyx jubatus).Crossref | GoogleScholarGoogle Scholar | 23108105PubMed |
McKenzie, N. L., Burbidge, A. A., Baynes, A., Brereton, R. N., Dickman, C. R., Gordon, G., Gibson, L. A., Menkhorst, P. W., Robinson, A. C., Williams, M. R., and Woinarski, J. C. Z. (2007). Analysis of factors implicated in the recent decline of Australia’s mammal fauna. Journal of Biogeography 34, 597–611.
| Analysis of factors implicated in the recent decline of Australia’s mammal fauna.Crossref | GoogleScholarGoogle Scholar |
Moberg, G. (2000). Biological response to stress: implications for animal welfare. In ‘The biology of animal stress: basic principles and implications for animal welfare’. (Eds G.P. Moberg and J.A. Mench.) pp. 1–21. (CABI Publishing: Oxon, UK.)
Montiglio, P. O., Pelletier, F., Palme, R., Garant, D., Réale, D., and Boonstra, R. (2012). Noninvasive monitoring of fecal cortisol metabolites in the eastern chipmunk (Tamias striatus): validation and comparison of two enzyme immunoassays. Physiological and Biochemical Zoology 85, 183–193.
| Noninvasive monitoring of fecal cortisol metabolites in the eastern chipmunk (Tamias striatus): validation and comparison of two enzyme immunoassays.Crossref | GoogleScholarGoogle Scholar | 22418710PubMed |
Möstl, E., Maggs, J. L., Schrötter, G., Besenfelder, U., and Palme, R. (2002). Measurement of cortisol metabolites in faeces of ruminants. Veterinary Research Communications 26, 127–139.
| Measurement of cortisol metabolites in faeces of ruminants.Crossref | GoogleScholarGoogle Scholar | 11922482PubMed |
Narayan, E. J., Molinia, F. C., Cockrem, J. F., and Hero, J.-M. (2012). Individual variation and repeatability in urinary corticosterone metabolite responses to capture in the cane toad (Rhinella marina). General and Comparative Endocrinology 175, 284–289.
| Individual variation and repeatability in urinary corticosterone metabolite responses to capture in the cane toad (Rhinella marina).Crossref | GoogleScholarGoogle Scholar | 22137908PubMed |
Nowack, J., and Geiser, F. (2016). Friends with benefits: the role of huddling in mixed groups of torpid and normothermic animals. The Journal of Experimental Biology 219, 590–596.
| Friends with benefits: the role of huddling in mixed groups of torpid and normothermic animals.Crossref | GoogleScholarGoogle Scholar | 26685170PubMed |
Palme, R. (2005). Measuring fecal steroids: guidelines for practical application. Annals of the New York Academy of Sciences 1046, 75–80.
| Measuring fecal steroids: guidelines for practical application.Crossref | GoogleScholarGoogle Scholar | 16055844PubMed |
Palme, R. (2019). Non-invasive measurement of glucocorticoids: advances and problems. Physiology & Behavior 199, 229–243.
| Non-invasive measurement of glucocorticoids: advances and problems.Crossref | GoogleScholarGoogle Scholar |
Palme, R., and Möstl, E. (1997). Measurement of cortisol metabolites in faeces of sheep as a parameter of cortisol concentration in blood. International Journal of Mammalian Biology 62, 192–197.
Palme, R., Rettenbacher, S., Touma, C., El-Bahr, S. M., and Möstl, E. (2005). Stress hormones in mammals and birds: comparative aspects regarding metabolism, excretion, and noninvasive measurement in fecal samples. Annals of the New York Academy of Sciences 1040, 162–171.
| Stress hormones in mammals and birds: comparative aspects regarding metabolism, excretion, and noninvasive measurement in fecal samples.Crossref | GoogleScholarGoogle Scholar | 15891021PubMed |
Parmesan, C., Root, T. L., and Willig, M. R. (2000). Impacts of extreme weather and climate on terrestrial biota. Bulletin of the American Meteorological Society 81, 443–450.
| Impacts of extreme weather and climate on terrestrial biota.Crossref | GoogleScholarGoogle Scholar |
Peter, R. E., Hontela, A., Cook, A. F., and Paulencu, C. R. (1978). Daily cycles in serum cortisol levels in the goldfish: effects of photoperiod, temperature, and sexual condition. Canadian Journal of Zoology 56, 2443–2448.
| Daily cycles in serum cortisol levels in the goldfish: effects of photoperiod, temperature, and sexual condition.Crossref | GoogleScholarGoogle Scholar |
Reeder, D. M., and Kramer, K. M. (2005). Stress in free-ranging mammals: integrating physiology, ecology, and natural history. Journal of Mammalogy 86, 225–235.
| Stress in free-ranging mammals: integrating physiology, ecology, and natural history.Crossref | GoogleScholarGoogle Scholar |
Rimbach, R., Heymann, E. W., Link, A., and Heistermann, M. (2013). Validation of an enzyme immunoassay for assessing adrenocortical activity and evaluation of factors that affect levels of fecal glucocorticoid metabolites in two New World primates. General and Comparative Endocrinology 191, 13–23.
| Validation of an enzyme immunoassay for assessing adrenocortical activity and evaluation of factors that affect levels of fecal glucocorticoid metabolites in two New World primates.Crossref | GoogleScholarGoogle Scholar | 23707497PubMed |
Romano, M. C., Rodas, A. Z., Valdez, R. A., Hernández, S. E., Galindo, F., Canales, D., and Brousset, D. M. (2010). Stress in wildlife species: noninvasive monitoring of glucocorticoids. Neuroimmunomodulation 17, 209–212.
| Stress in wildlife species: noninvasive monitoring of glucocorticoids.Crossref | GoogleScholarGoogle Scholar | 20134205PubMed |
Romero, L. M. (2002). Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. General and Comparative Endocrinology 128, 1–24.
| Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates.Crossref | GoogleScholarGoogle Scholar | 12270784PubMed |
Romero, L. M., Dickens, M. J., and Cyr, N. E. (2009). The reactive scope model – a new model integrating homeostasis, allostasis, and stress. Hormones and Behavior 55, 375–389.
| The reactive scope model – a new model integrating homeostasis, allostasis, and stress.Crossref | GoogleScholarGoogle Scholar | 19470371PubMed |
Ruscio, M. G., Sweeny, T., Hazelton, J., Suppatkul, P., and Carter, C. S. (2007). Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles. Hormones and Behavior 51, 54–61.
| Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles.Crossref | GoogleScholarGoogle Scholar | 17007856PubMed |
Salas, L., Dickman, C., Helgen, K., Winter, J., Ellis, M., Denny, M., Woinarski, J., Lunney, D., Oakwood, M., Menkhorst, P., and Strahan, R. (2016). Petaurus breviceps. The IUCN Red List of Threatened Species 2016: e.T16731A21959798
Sapolsky, R. M. (2002). Endocrinology of the stress-response. In ‘Behavioral endocrinology’. (Eds J.B. Becker, S.M. Breedlove, D. Crews and M.M. McCarthy.) pp. 409–450. (MIT Press: Cambridge, MA, USA.)
Sapolsky, R. M., Romero, L. M., and Munck, A. U. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21, 55–89.
| 10696570PubMed |
Scheun, J., Bennett, N., Ganswindt, A., and Nowack, J. (2015). The hustle and bustle of city life: monitoring the effects of urbanisation in the African lesser bushbaby. Naturwissenschaften 102, 1–11.
Scheun, J., Nowack, J., Bennett, N., and Ganswindt, A. (2016). Female reproductive activity and its endocrine correlates in the African lesser bushbaby, Galago moholi. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 186, 255–264.
| Female reproductive activity and its endocrine correlates in the African lesser bushbaby, Galago moholi.Crossref | GoogleScholarGoogle Scholar | 26649553PubMed |
Scheun, J., Greeff, D., and Ganswindt, A. (2018). Non-invasive monitoring of glucocorticoid metabolite concentrations in urine and faeces of the sungazer (Smaug giganteus). PeerJ 6, e6132.
| Non-invasive monitoring of glucocorticoid metabolite concentrations in urine and faeces of the sungazer (Smaug giganteus).Crossref | GoogleScholarGoogle Scholar | 30595985PubMed |
Sheriff, M., Dantzer, B., Delehanty, B., Palme, R., and Boonstra, R. (2011). Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166, 869–887.
| Measuring stress in wildlife: techniques for quantifying glucocorticoids.Crossref | GoogleScholarGoogle Scholar | 21344254PubMed |
Smith, T. E., and French, J. A. (1997). Psychosocial stress and urinary cortisol excretion in marmoset monkeys. Physiology & Behavior 62, 225–232.
| Psychosocial stress and urinary cortisol excretion in marmoset monkeys.Crossref | GoogleScholarGoogle Scholar |
Smith, J. E., Monclús, R., Wantuck, D., Florant, G. L., and Blumstein, D. T. (2012). Fecal glucocorticoid metabolites in wild yellow-bellied marmots: experimental validation, individual differences and ecological correlates. General and Comparative Endocrinology 178, 417–426.
| Fecal glucocorticoid metabolites in wild yellow-bellied marmots: experimental validation, individual differences and ecological correlates.Crossref | GoogleScholarGoogle Scholar | 22732084PubMed |
Soto‐Gamboa, M., Gonzalez, S., Hayes, L. D., and Ebensperger, L. A. (2009). Validation of a radioimmunoassay for measuring fecal cortisol metabolites in the hystricomorph rodent, Octodon degus. Journal of Experimental Zoology. Part A, Ecological Genetics and Physiology 311A, 496–503.
| Validation of a radioimmunoassay for measuring fecal cortisol metabolites in the hystricomorph rodent, Octodon degus.Crossref | GoogleScholarGoogle Scholar |
Suckling, G. C. (1984). Population ecology of the sugar glider, Petaurus breviceps, in a system of fragmented habitats. Wildlife Research 11, 49–75.
| Population ecology of the sugar glider, Petaurus breviceps, in a system of fragmented habitats.Crossref | GoogleScholarGoogle Scholar |
Tilbrook, A., Turner, A., and Clarke, I. (2000). Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences. Reviews of Reproduction 5, 105–113.
| Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences.Crossref | GoogleScholarGoogle Scholar | 10864855PubMed |
Touma, C., and Palme, R. (2005). Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Annals of the New York Academy of Sciences 1046, 54–74.
| Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation.Crossref | GoogleScholarGoogle Scholar | 16055843PubMed |
Touma, C., Sachser, N., Möstl, E., and Palme, R. (2003). Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. General and Comparative Endocrinology 130, 267–278.
| Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice.Crossref | GoogleScholarGoogle Scholar | 12606269PubMed |
Touma, C., Palme, R., and Sachser, N. (2004). Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Hormones and Behavior 45, 10–22.
| Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones.Crossref | GoogleScholarGoogle Scholar | 14733887PubMed |
Wasser, S. K., Hunt, K. E., Brown, J. L., Cooper, K., Crockett, C. M., Bechert, U., Millspaugh, J. J., Larson, S., and Monfort, S. L. (2000). A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. General and Comparative Endocrinology 120, 260–275.
| A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species.Crossref | GoogleScholarGoogle Scholar | 11121291PubMed |
Wielebnowski, N. C., Fletchall, N., Carlstead, K., Busso, J. M., and Brown, J. L. (2002). Noninvasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biology 21, 77–98.
| Noninvasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population.Crossref | GoogleScholarGoogle Scholar |
Yoshimura, S., Sakamoto, S., Kudo, H., Sassa, S., Kumai, A., and Okamoto, R. (2003). Sex-differences in adrenocortical responsiveness during development in rats. Steroids 68, 439–445.
| Sex-differences in adrenocortical responsiveness during development in rats.Crossref | GoogleScholarGoogle Scholar | 12798494PubMed |
Young, K., Brown, J., and Goodrowe, K. (2001). Characterization of reproductive cycles and adrenal activity in the black‐footed ferret (Mustela nigripes) by fecal hormone analysis. Zoo Biology 20, 517–536.
| Characterization of reproductive cycles and adrenal activity in the black‐footed ferret (Mustela nigripes) by fecal hormone analysis.Crossref | GoogleScholarGoogle Scholar |
Young, C., Ganswindt, A., McFarland, R., de Villiers, C., van Heerden, J., Ganswindt, S., Barrett, L., and Henzi, S. P. (2017). Faecal glucocorticoid metabolite monitoring as a measure of physiological stress in captive and wild vervet monkeys. General and Comparative Endocrinology 253, 53–59.
| Faecal glucocorticoid metabolite monitoring as a measure of physiological stress in captive and wild vervet monkeys.Crossref | GoogleScholarGoogle Scholar | 28843615PubMed |
