Effects of natural weathering conditions on faecal cortisol metabolite measurements in the greater bilby (Macrotis lagotis)
Nicole Evans A , Edward J. Narayan A B and Jean-Marc Hero AA Environmental Futures Research Institute (EFRI), School of Environment, Griffith University, Gold Coast campus, Qld 4222, Australia.
B Corresponding author. Email: e.narayan@ga.griffith.edu.au
Australian Journal of Zoology 61(5) 351-356 https://doi.org/10.1071/ZO13032
Submitted: 26 April 2013 Accepted: 2 October 2013 Published: 29 October 2013
Abstract
Natural weathering conditions can influence faecal cortisol metabolite (FCM) measurements in wildlife if fresh faeces cannot be collected immediately following defaecation. In this study, we evaluated this issue in a threatened Australian marsupial, the greater bilby (Macrotis lagotis). Fresh (<12 h since defaecation) faecal samples (n = 19 pellets per bilby) were collected one morning from seven adult bilbies kept in captivity. One control faecal sample (Day 1) from each bilby was immediately frozen. The remaining faecal pellets were randomly positioned outdoors. Subsequently, we froze one faecal pellet every 24 h for 19 days. FCM levels in bilby faeces were quantified using an enzyme-immunoassay. Mean FCM levels showed variation (daily mean coefficients of variation [CV %]) of 56.83–171.65% over 19 days. Overall, FCM levels were affected by exposure time; however, multiple comparisons showed that no significant change in FCM occurred after environmental exposure (no significant difference in mean FCM between control (Day 1) with any of the exposure days (Days 2–19). Individuals and sex also affected FCM levels. We found no correlation between mean daily CVs with daily minimum–maximum temperatures or rainfall. Our results indicate that FCM in bilby faeces is fairly stable to long-term environmental exposure (19 days). In future, freshly excreted bilby faeces (where the sample maintains a distinct odour for 9–13 days) should be used to study FCM levels in wild bilbies.
Additional keywords: Australia, conservation physiology, decay, stress.
References
Accorsi, P. A., Carloni, E., Valsecchi, P., Viggiani, R., Garnberoni, M., Tarnanini, C., and Seren, E. (2008). Cortisol determination in hair and faeces from domestic cats and dogs. General and Comparative Endocrinology 155, 398–402.| Cortisol determination in hair and faeces from domestic cats and dogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXislCktA%3D%3D&md5=3a5378e9bfdfe6001d547d6b230c65a1CAS | 17727851PubMed |
Baker, M. L., Gemmell, E., and Gemmell, R. T. (1998). Physiological changes in brushtail possums, Trichosurus vulpecula, transferred from the wild to captivity. The Journal of Experimental Zoology 280, 203–212.
| Physiological changes in brushtail possums, Trichosurus vulpecula, transferred from the wild to captivity.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7jtlSrsA%3D%3D&md5=b7775af0165f69dcde364f48489968bdCAS | 9472479PubMed |
Barja, I., Silván, G., and Illera, J. C. (2008). Relationships between sex and stress hormone levels in feces and marking behavior in a wild population of Iberian wolves (Canis lupus signatus). Journal of Chemical Ecology 34, 697–701.
| Relationships between sex and stress hormone levels in feces and marking behavior in a wild population of Iberian wolves (Canis lupus signatus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1aksLY%3D&md5=bb13e106445ca1e334aa14acc2c6fb62CAS | 18392658PubMed |
Beehner, J. C., and Whitten, P. L. (2004). Modifications of a field method for fecal steroid analysis in baboons. Physiology & Behavior 82, 269–277.
| Modifications of a field method for fecal steroid analysis in baboons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtVagtbg%3D&md5=06b26e689ee7bf7426aeff2b3c62e766CAS |
Bosacker, A. (2008). Stress, evolution, and sociality in wild female baboons. Ph.D. Thesis, University of Minnesota.
Chapman, C. A., Saj, T. L., and Snaith, T. V. (2007). Temporal dynamics of nutrition, parasitism, and stress in Colobus monkeys: implications for population regulation and conservation. American Journal of Physical Anthropology 134, 240–250.
| Temporal dynamics of nutrition, parasitism, and stress in Colobus monkeys: implications for population regulation and conservation.Crossref | GoogleScholarGoogle Scholar | 17596853PubMed |
Dantzer, B., McAdam, A. G., Palme, R., Fletcher, Q. E., Boutin, S., Humphries, M. M., and Boonstra, R. (2010). Fecal cortisol metabolite levels in free-ranging North American red squirrels: assay validation and the effects of reproductive condition. General and Comparative Endocrinology 167, 279–286.
| Fecal cortisol metabolite levels in free-ranging North American red squirrels: assay validation and the effects of reproductive condition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFeqsL0%3D&md5=77473e01a0330324fa605b73e8a7366aCAS | 20346362PubMed |
Dehnhard, M., Clauss, M., Lechner-Doll, M., Meyer, H. H. D., and Palme, R. (2001). Noninvasive monitoring of adrenocortical activity in roe deer (Capreolus capreolus) by measurement of fecal cortisol metabolites. General and Comparative Endocrinology 123, 111–120.
| Noninvasive monitoring of adrenocortical activity in roe deer (Capreolus capreolus) by measurement of fecal cortisol metabolites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFSitrs%3D&md5=a64d6bf340f54d2c41441004a8f224faCAS | 11551112PubMed |
Descovich, K. A., Lisle, A. T., Johnston, S., Keeley, T., and Phillips, C. J. C. (2012). Intrasample variation and the effect of storage delay on faecal metabolite concentrations in the southern hairy-nosed wombat (Lasiorhinus latifrons). Australian Mammalogy 34, 217–222.
| Intrasample variation and the effect of storage delay on faecal metabolite concentrations in the southern hairy-nosed wombat (Lasiorhinus latifrons).Crossref | GoogleScholarGoogle Scholar |
Dunwoody, E., Liu, X., and McDougall, K. (2009). A spatial analysis of greater bilby (Macrotis lagotis) habitat in south-west queensland. In ‘Surveying & Spatial Sciences Institute Biennial International Conference, 2009, Adelaide’. (Eds B. Ostendorf, P. Baldock, D. Bruce, M. Burdett and P. Corcoran.) pp. 977–986.
Ellenberg, U., Setiawan, A. N., Cree, A., Houston, D. M., and Seddon, P. J. (2007). Elevated hormonal stress response and reduced reproductive output in yellow-eyed penguins exposed to unregulated tourism. General and Comparative Endocrinology 152, 54–63.
| Elevated hormonal stress response and reduced reproductive output in yellow-eyed penguins exposed to unregulated tourism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFOitrg%3D&md5=013c2d5f83361b2b360bf057e9498938CAS | 17400221PubMed |
Ellis, T., James, J. D., Stewart, C., and Scott, A. P. (2004). A non-invasive stress assay based upon measurement of free cortisol released into the water by rainbow trout. Journal of Fish Biology 65, 1233–1252.
| A non-invasive stress assay based upon measurement of free cortisol released into the water by rainbow trout.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFakurrJ&md5=a621454cb5e2942685c9be1b755c9572CAS |
Fanson, K. V., Wielebnowski, N. C., Shenk, T. M., and Lucas, J. R. (2012). Comparative patterns of adrenal activity in captive and wild Canada lynx (Lynx canadensis). Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 182, 157–165.
| Comparative patterns of adrenal activity in captive and wild Canada lynx (Lynx canadensis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xks1ynsg%3D%3D&md5=f686b318fe593d0a121d48296f6ae258CAS |
Friend, T., Morris, K., and van Weenen, J. (2008). Macrotis lagotis. In ‘IUCN 2011’. IUCN Red List of Threatened Species.
Gibson, L. A. (2001). Seasonal changes in the diet, food availability and food preference of the greater bilby (Macrotis lagotis) in south-western Queensland. Wildlife Research 28, 121–134.
| Seasonal changes in the diet, food availability and food preference of the greater bilby (Macrotis lagotis) in south-western Queensland.Crossref | GoogleScholarGoogle Scholar |
Graham, C., Narayan, E., McCallum, H., and Hero, J.-M. (2013). Non-invasive monitoring of stress physiology within free-living highland and lowland populations of native Australian great barred frogs (Mixophyes fasciolatus). General and Comparative Endocrinology 191, 24–30.
| Non-invasive monitoring of stress physiology within free-living highland and lowland populations of native Australian great barred frogs (Mixophyes fasciolatus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlWjsb%2FM&md5=24355341fb6b1cc23dea6231e417c8dcCAS | 23727276PubMed |
Hesterman, H., Jones, S. M., and Schwarzenberger, F. (2008). Reproductive endocrinology of the largest dasyurids: characterization of ovarian cycles by plasma and fecal steroid monitoring. Part I. The Tasmanian devil (Sarcophilus harrisii). General and Comparative Endocrinology 155, 234–244.
| Reproductive endocrinology of the largest dasyurids: characterization of ovarian cycles by plasma and fecal steroid monitoring. Part I. The Tasmanian devil (Sarcophilus harrisii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlGiu77M&md5=0492f5528078c6768f51dcb0f7cc944aCAS | 17592734PubMed |
Hogan, L. A., Johnston, S. D., Lisle, A. T., Keeley, T., Wong, P., Nicolson, V., Horsup, A. B., Janssen, T., and Phillips, C. J. C. (2011). Behavioural and physiological responses of captive wombats (Lasiorhinus latifrons) to regular handling by humans. Applied Animal Behaviour Science 134, 217–228.
| Behavioural and physiological responses of captive wombats (Lasiorhinus latifrons) to regular handling by humans.Crossref | GoogleScholarGoogle Scholar |
Kalz, B., Jewgenow, K., and Fickel, J. (2006). Structure of an otter (Lutra lutra) population in Germany – results of DNA and hormone analyses from faecal samples. Mammalian Biology 71, 321–335.
| Structure of an otter (Lutra lutra) population in Germany – results of DNA and hormone analyses from faecal samples.Crossref | GoogleScholarGoogle Scholar |
Khan, M. Z., Altmann, J., Isani, S. S., and Yu, J. (2002). A matter of time: evaluating the storage of fecal samples for steroid analysis. General and Comparative Endocrinology 128, 57–64.
| A matter of time: evaluating the storage of fecal samples for steroid analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVGqsL0%3D&md5=737cddfbd8048adcc4433c3837b064dfCAS | 12270788PubMed |
Kindermann, C., Narayan, E., and Hero, J.-M. (2012). Urinary corticosterone metabolites and chytridiomycosis disease prevalence in a free-living population of male Stony Creek frogs (Litoria wilcoxii). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 162, 171–176.
| Urinary corticosterone metabolites and chytridiomycosis disease prevalence in a free-living population of male Stony Creek frogs (Litoria wilcoxii).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsFOnsbg%3D&md5=9e470abb10a980bc55eb851e3695e5f0CAS |
Lynch, J. W., Ziegler, T. E., and Strier, K. B. (2002). Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus. Hormones and Behavior 41, 275–287.
| Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktVGhs7k%3D&md5=06af22129a3075056927024ed5566403CAS | 11971661PubMed |
McDonald, I. R., Lee, A. K., Bradley, A. J., and Than, K. A. (1981). Endocrine changes in dasyurid marsupials with differing mortality patterns. General and Comparative Endocrinology 44, 292–301.
| Endocrine changes in dasyurid marsupials with differing mortality patterns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXkt1ahsrs%3D&md5=f0f11439263188c18d3cd1d3aa919d36CAS | 7286612PubMed |
Millspaugh, J., and Washburn, B. (2003). Within-sample variation of fecal glucocorticoid measurements. General and Comparative Endocrinology 132, 21–26.
| Within-sample variation of fecal glucocorticoid measurements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFWms7k%3D&md5=b2b1ad3d5d6ca11080bbf27a04e56e98CAS | 12765640PubMed |
Millspaugh, J. J., and Washburn, B. E. (2004). Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. General and Comparative Endocrinology 138, 189–199.
| Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsFSjtr8%3D&md5=33b4e9ce5d526bc1e9fff9d1b7b86877CAS | 15364201PubMed |
Muller, M. N., and Wrangham, R. W. (2004). Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behavioral Ecology and Sociobiology 55, 332–340.
| Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii).Crossref | GoogleScholarGoogle Scholar |
Narayan, E. (2013). Non-invasive reproductive and stress endocrinology in amphibian conservation physiology. Conservation Physiology 1, 1–16.
| Non-invasive reproductive and stress endocrinology in amphibian conservation physiology.Crossref | GoogleScholarGoogle Scholar |
Narayan, E., Molinia, F., Christi, K., Morley, C., and Cockrem, J. (2010a). Annual cycles of urinary reproductive steroid concentrations in wild and captive endangered Fijian ground frogs (Platymantis vitiana). General and Comparative Endocrinology 166, 172–179.
| Annual cycles of urinary reproductive steroid concentrations in wild and captive endangered Fijian ground frogs (Platymantis vitiana).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslSrtbY%3D&md5=0dd4326b355cc6f5864e9f6f844ae7e3CAS | 19840803PubMed |
Narayan, E., Molinia, F., Christi, K., Morley, C., and Cockrem, J. (2010b). Urinary corticosterone metabolite responses to capture, and annual patterns of urinary corticosterone in wild and captive endangered Fijian ground frogs (Platymantis vitiana). Australian Journal of Zoology 58, 189–197.
| Urinary corticosterone metabolite responses to capture, and annual patterns of urinary corticosterone in wild and captive endangered Fijian ground frogs (Platymantis vitiana).Crossref | GoogleScholarGoogle Scholar |
Narayan, E., Hero, J.-M., Evans, N., Nicolson, V., and Mucci, A. (2012). Non-invasive monitoring of physiological stress hormone responses in a captive population of the greater bilby (Macrotis lagotis). Endangered Species Research 18, 279–289.
| Non-invasive monitoring of physiological stress hormone responses in a captive population of the greater bilby (Macrotis lagotis).Crossref | GoogleScholarGoogle Scholar |
Narayan, E., Cockrem, J. F., and Hero, J.-M. (2013a). Sight of a predator induces a corticosterone stress response and generates fear in an amphibian. PLoS ONE 8, e73564.
| Sight of a predator induces a corticosterone stress response and generates fear in an amphibian.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVWht7rO&md5=9be0aef75580856b9f56d36bd13d3477CAS | 24009756PubMed |
Narayan, E., Webster, K., Nicolson, V., Mucci, A., and Hero, J.-M. (2013b). Non-invasive evaluation of physiological stress in an iconic Australian marsupial: the koala (Phascolarctos cinereus). General and Comparative Endocrinology 187, 39–47.
| Non-invasive evaluation of physiological stress in an iconic Australian marsupial: the koala (Phascolarctos cinereus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXot1Oiu7g%3D&md5=bfc9b13f2522e7983ce8f16e68fafbc2CAS | 23583768PubMed |
Owen, M. A., Swaisgood, R. R., Czekala, N. M., Steinman, K., and Lindburg, D. G. (2004). Monitoring stress in captive giant pandas (Ailuropoda melanoleuca): behavioral and hormonal responses to ambient noise. Zoo Biology 23, 147–164.
| Monitoring stress in captive giant pandas (Ailuropoda melanoleuca): behavioral and hormonal responses to ambient noise.Crossref | GoogleScholarGoogle Scholar |
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 | 1:CAS:528:DC%2BD2MXos1eht7Y%3D&md5=cf1e87f83ac408fb9903ceb388520696CAS | 15891021PubMed |
Park, H. C., Han, T. Y., Kim, D. C., Min, M. S., Han, S. Y., Kim, K. S., and Lee, H. (2011). Individual identification and sex determination of Eurasian otters (Lutra lutra) in Daegu city based on genetic analysis of otter spraint. Genes & Genomics 33, 653–657.
| Individual identification and sex determination of Eurasian otters (Lutra lutra) in Daegu city based on genetic analysis of otter spraint.Crossref | GoogleScholarGoogle Scholar |
Rehnus, M., Hackländer, K., and Palme, R. (2009). A non-invasive method for measuring glucocorticoid metabolites (GCM) in mountain hares (Lepus timidus). European Journal of Wildlife Research 55, 615–620.
| A non-invasive method for measuring glucocorticoid metabolites (GCM) in mountain hares (Lepus timidus).Crossref | GoogleScholarGoogle Scholar |
Romero, L. M., and Wikelski, M. (2001). Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proceedings of the National Academy of Sciences of the United States of America 98, 7366–7370.
| Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWmurs%3D&md5=2b6495ecec25493549a59143f1630c70CAS | 11416210PubMed |
Sheriff, M. J., Krebs, C. J., and Boonstra, R. (2009). The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. Journal of Animal Ecology 78, 1249–1258.
| The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares.Crossref | GoogleScholarGoogle Scholar | 19426257PubMed |
Sheriff, M. J., 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, S., McRae, P., and Hughes, J. (2009). Faecal DNA analysis enables genetic monitoring of the species recovery program for an arid-dwelling marsupial. Australian Journal of Zoology 57, 139–148.
| Faecal DNA analysis enables genetic monitoring of the species recovery program for an arid-dwelling marsupial.Crossref | GoogleScholarGoogle Scholar |
Sousa, M. C., and Ziegler, T. E. (1998). Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females. American Journal of Primatology 46, 105–117.
| Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsVektbk%3D&md5=ec36b0cf9685c323e5be289bb11dde04CAS |
Southgate, R., and Carthew, S. M. (2006). Diet of the bilby (Macrotis lagotis) in relation to substrate, fire and rainfall characteristics in the Tanami Desert. Wildlife Research 33, 507–519.
| Diet of the bilby (Macrotis lagotis) in relation to substrate, fire and rainfall characteristics in the Tanami Desert.Crossref | GoogleScholarGoogle Scholar |
Thaker, M., Vanak, A. T., Lima, S. L., and Hews, D. K. (2010). Stress and aversive learning in a wild vertebrate: the role of corticosterone in mediating escape from a novel stressor. American Naturalist 175, 50–60.
| Stress and aversive learning in a wild vertebrate: the role of corticosterone in mediating escape from a novel stressor.Crossref | GoogleScholarGoogle Scholar | 19922261PubMed |
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 | 1:CAS:528:DC%2BD2MXhtVWjtL%2FE&md5=f64bd5a90b8813fd5abf527bb8ce065dCAS | 16055843PubMed |
Touma, C., Sachser, N., Mostl, 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 | 1:CAS:528:DC%2BD3sXhsVCgt74%3D&md5=502996cdeaee712b0fce5df8b83a177eCAS | 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 | 1:CAS:528:DC%2BD2cXkvFOitg%3D%3D&md5=f530a828ccc6a8176a0851b9ef6f4230CAS | 14733887PubMed |
Turner, J. W., Nemeth, R., and Rogers, C. (2003). Measurement of fecal glucocorticoids in parrotfishes to assess stress. General and Comparative Endocrinology 133, 341–352.
| Measurement of fecal glucocorticoids in parrotfishes to assess stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvVOrs7s%3D&md5=606453e1ebbc772090d9a3e1185f0620CAS | 12957478PubMed |
Washburn, B. E., and Millspaugh, J. J. (2002). Effects of simulated environmental conditions on glucocorticoid metabolite measurements in white-tailed deer feces. General and Comparative Endocrinology 127, 217–222.
| Effects of simulated environmental conditions on glucocorticoid metabolite measurements in white-tailed deer feces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmslaltLY%3D&md5=2b888317c3ba91df0048f92e3e9a6eddCAS | 12225762PubMed |
Wasser, S. K., Papageorge, S., Foley, C., and Brown, J. L. (1996). Excretory fate of estradiol and progesterone in the African elephant (Loxodonata africana) and patterns of fecal steroid concentrations throughout the estrous cycle. General and Comparative Endocrinology 102, 255–262.
| Excretory fate of estradiol and progesterone in the African elephant (Loxodonata africana) and patterns of fecal steroid concentrations throughout the estrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XivV2qur4%3D&md5=53fc9ae961f331608d284ddbea2c6871CAS | 8998970PubMed |
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 |