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Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation
Abstract
Fecal glucocorticoid metabolite analyses are increasingly being used by a variety of scientists (e.g., conservation biologists, animal scientists) to examine glucocorticoid (i.e., stress hormone) secretion in domestic and wild vertebrates. Adrenocortical activity (i.e., stress response) is of interest to conservation biologists because stress can alter animal behavior, reduce resistance to disease, and affect population performance. The noninvasiveness of fecal-based assessments is attractive, particularly when studying endangered species, because samples can often be obtained without disturbing the animal. Despite such advantages, many confounding factors inhibit the utility of this technique in addressing conservation problems. In particular, interpretation of fecal glucocorticoid metabolite (FGM) measures may be confounded by the length of time animals are held in captivity, normal seasonal and daily rhythms, body condition, sample storage and treatment techniques, diet of the animal, assay selection, animal status (i.e., social ranking, reproductive status), sample age and condition, and sample mass. Further complicating interpretation and utility of these measures is the apparent species-specific response to these factors. The purpose of this paper is to discuss the factors that confound interpretation of FGM measures, summarize research that addresses these issues, and offer an agenda for future research and interpretation. We urge conservation biologists to carefully c…
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“Sample collection took place immediately after defecation to avoid bacterial and microbial degradation (Millspaugh and Washburn, 2004).”
From Effect of weather conditions and presence of visitors on adrenocortical activity in captive African penguins (Spheniscus demersus) (2017) · cites this paper as Millspaugh and Washburn, 2004
In the citing paper
“This non-invasive method permits the monitoring of the animal's endocrine status without the necessity to capture or handle the animals, which may compromise the accurate assessment of stress (Millspaugh and Washburn, 2004;Goymann, 2012).”
From Effect of weather conditions and presence of visitors on adrenocortical activity in captive African penguins (Spheniscus demersus) (2017) · cites this paper as Millspaugh and Washburn, 2004
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“Samples were gathered in cryovials and frozen immediately after collection at À20 °C (Millspaugh and Washburn, 2004;Palme et al., 2005;Sheriff et al., 2011).”
From Effect of weather conditions and presence of visitors on adrenocortical activity in captive African penguins (Spheniscus demersus) (2017) · cites this paper as Millspaugh and Washburn, 2004
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“In addition, the point sample provided by a blood measure might not be representative of long-term hormone levels due to the pulsatile secretion pattern of glucocorticoids in blood (Harper and Austad, 2000; Monfort et al., 1993; Windle et al., 1998).”
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Items 201–300 of 474
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“…environmental moisture which allows the growth of microbes and fungi, change in metabolite affinity for antibodies, and the different chemical stability of each hormone (Matkovics 1972; Woods 1975; Neumann et al. 2002; Terio et al. 2002; Washburn and Millspaugh 2002; Millspaugh and Washburn 2004).”
BackgroundResultJesmer, B. R., Goheen, J. R., Monteith, K. L., & Kauffman, M. J. (2017) · Ecological Applications · doi:10.1002/eap.1608 · Cited by 19
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“A negative relationship between fecal sample mass and FGM concentration has been found previously [Millspaugh and Washburn, 2004, but see Goymann, 2005], leading to the suggestion of only analyzing larger fecal samples (>20 mg dried mass).”
Scarlata, C. D., Elias, B. A., Godwin, J., Powell, R. A., Shepherdson, D. J., Shipley, L. A., & Brown, J. L. (2012) · Journal of Mammalogy · doi:10.1644/11-mamm-a-223.1 · Cited by 21
“In addition, fecal data provide a pooled estimate of hormone production from the previous 12–24 h, dampening acute fluctuations in secretion (Millspaugh and Washburn 2004).”
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“Such physiological methods need thorough calibration in terms of season, level of human disturbance, habitat conditions and other confounding factors (Kotrschal et al. 1998; Millspaugh and Washburn 2004; Romero 2004; Baltic et al. 2005).”
Ajó, A. F., Hunt, K., Dillon, D., Uhart, M., Sironi, M., Rowntree, V., & Buck, C. (2021) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2021.113828 · Cited by 19
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“2011) or fecal (Millspaugh and Washburn 2004) metabolite analysis, though there are many unresolved issues”
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“They contain pooled hormone metabolite concentrations rather than a discrete amount of hormone secreted at a specific time, as occurs in blood samples (Millspaugh and Washburn, 2004).”
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“Additionally, faecal steroid metabolites typically reflect integrated circulating hormone secretion over a period of time, rather than a point sample and this may be useful in reducing the episodic pattern of secretion of hormones such as testosterone and oestradiol (Millspaugh and Washburn, 2004).”
BackgroundPhysiological effects of radiotransmitters on mourning doves
Schulz, J. H., Millspaugh, J., Washburn, B., Bermudez, A. J., Tomlinson, J., Mong, T., & He, Z.-Q. (2005) · doi:10.2193/0091-7648(2005)33[1092:peorom]2.0.co;2 · Cited by 19
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“It is known that fGCM concentrations can differ between males and females [16]; thus sex was added as a fixed factor.”
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“Interestingly, this same pattern was reported in fecal samples for both mourning doves (Millspaugh & Washburn, 2004) and California spotted owls (Tempel & Gutierrez, 2004), reinforcing the need to correct for extraction efficiency.”
BackgroundCan physiological stress alter population persistence? A model with conservation implications
Fefferman, N. H., & Romero, L. M. (2013) · Conservation Physiology · doi:10.1093/conphys/cot012 · Cited by 53
“, 2000); they are relatively easy to measure in free-living animals (Wingfield and Romero, 2001; Millspaugh and Washburn, 2004); and increases in glucocorticoids are often correlated with factors of conservation concern, such as pollution (e.”
BackgroundNogueira, S. S. D. C., Calazans, S. G., Costa, T. S. O., Peregrino, H., & Nogueira-Filho, S. L. G. (2011) · doi:10.1016/j.applanim.2011.04.002 · Cited by 18
Urinary cortisol responses to unusual events in captive chimpanzees (Pan troglodytes)
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Noninvasive monitoring of ovarian endocrine activity in the chinchilla (Chinchilla lanigera)
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“Therefore, biochemical and physiological validations are required before routine procedures can be established for a determined species in order to demonstrate the assay accuracy (Holt and Pickard, 1999; Monfort, 2003; Millspaugh and Washburn, 2004).”
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Webster, K. N., Narayan, E. J., & de Vos, N. (2016) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2016.07.012 · Cited by 21
Wong, E. P., Yon, L., Purcell, R. S., Walker, S. L., Othman, N., Saaban, S., & Campos‐Arceiz, A. (2016) · Conservation Physiology · doi:10.1093/conphys/cow070 · Cited by 14
“…between defecation and sample collection by a researcher), and this variation is mediated by environmental factors such as ambient temperature and moisture (Millspaugh and Washburn, 2004, 2003) as well as by the effects of bacterial activity (e.g. Wasser et al., 2000; Möstl and Palme, 2002).”
BackgroundOzella, L., Anfossi, L., Di Nardo, F., & Pessani, D. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.06.014 · Cited by 17
“Samples were gathered in cryovials and frozen immediately after collection at -20 °C (Millspaugh and Washburn, 2004; Palme et al., 2005; Sheriff et al., 2011).”
BackgroundMethodMillspaugh, J. J., Rittenhouse, C. D., Montgomery, R. A., Matthews, W. S., & Slotow, R. (2015) · Journal of Zoology · doi:10.1111/jzo.12224 · Cited by 18
Self-citationKhonmee, J., Brown, J. L., Rojanasthien, S., Thumasanukul, D., Kongphoemphun, A., Siriaroonrat, B., Tipkantha, W., Punyapornwithaya, V., & Thitaram, C. (2014) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2014.02.008 · Cited by 17
“Most studies of wildlife utilize non-invasive steroid metabolite monitoring to assess endocrine function as an alternative to blood sampling (Huber et al., 2003; Millspaugh and Washburn, 2004).”
BackgroundFecal Hormones as a Non-Invasive Population Monitoring Method for Reindeer
Morden, C., Weladji, R., Ropstad, E., Dahl, E., Holand, Ø., Mastromonaco, G., & Nieminen, M. (2011) · Journal of Wildlife Management · doi:10.1002/jwmg.185 · Cited by 17
“We stored blood and fecal samples at 208 C until analysis to slow microbial activity and reduce immunoreactivity problems (Millspaugh and Washburn 2004, Palme 2005, Capezzuto et al. 2008).”
MethodLèche, A., Busso, J. M., Navarro, J. L., Hansen, C., Marin, R., & Martella, M. B. (2011) · Journal für Ornithologie · doi:10.1007/s10336-011-0661-x · Cited by 19
“Non-invasive methods to measure adrenocortical activity have the advantage that samples can be easily taken without disturbing the animals studied, therefore avoiding an increase in GC release induced by the sampling procedure ( Millspaugh and Washburn 2004 ).”
BackgroundPereira, R. J. G., Granzinolli, M. A. M., & Duarte, J. M. B. (2009) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2009.12.012 · Cited by 20
“2 mL of 80% methanol) to avoid that higher concentration of methanol per unit of sample mass result in greater extraction of fecal androgens and glucocorticoids (Millspaugh and Washburn, 2004).”
BackgroundMethodResultInfluentialPhysiological Stress Response of Captive White‐Tailed Deer to Video Collars
Moll, R. J., Millspaugh, J. J., Beringer, J., Sartwell, J., WOODS, R. J., & VerCauteren, K. C. (2009) · Journal of Wildlife Management · doi:10.2193/2008-266 · Cited by 19
Self-citationKlich, D., Łopucki, R., Gałązka, M., Ścibior, A., Gołębiowska, D., Brzezińska, R., Kruszewski, B., Kaleta, T., & Olech, W. (2021) · Acta veterinaria Scandinavica · doi:10.1186/s13028-021-00589-9 · Cited by 19
“Fecal glucocorticoid metabolite analyses are increasingly used in a variety of studies to examine stress hormone secretion in domestic and wild vertebrates [32, 33].”
BackgroundEleftheriou, A., Palme, R., & Boonstra, R. (2020) · Animals · doi:10.3390/ani10071120 · Cited by 19
“Knowing when these trap-induced rises in FCMs manifest in feces is also of practical use because they can artificially increase FCMs and lead to erroneous results about baseline adrenocortical activity [19].”
BackgroundPlangsangmas, T., Brown, J. L., Thitaram, C., Silva‐Fletcher, A., Edwards, K. L., Punyapornwithaya, V., Towiboon, P., & Somgird, C. (2020) · Animals · doi:10.3390/ani10010157 · Cited by 18
“Thus, noninvasive approaches that quantify GC metabolites in urine or feces have been developed to assess acute and chronic stress responses in many species [6,7].”
BackgroundGelling, M., Johnson, P., Moorhouse, T., & Macdonald, D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041081 · Cited by 16
“However, numerous factors affect the corticosteroid response, including time of day, season, breeding condition and feeding [29].”
BackgroundComparison of Endocrine Response to Stress Between Captive-Raised and Wild-Caught Bighorn Sheep
Coburn, S., Salman, M., Rhyan, J., Keefe, T., McCollum, M. P., Aune, K., Spraker, T., & Miller, L. (2010) · Journal of Wildlife Management · doi:10.2193/2008-152 · Cited by 16
Fardell, L. L., Bedoya‐Pérez, M. A., Dickman, C. R., Crowther, M. S., Pavey, C. R., & Narayan, E. J. (2021) · Die Naturwissenschaften · doi:10.1007/s00114-020-01716-8 · Cited by 15
Wolf, T. E., Mangwiro, N., Fasina, F. O., & Ganswindt, A. (2020) · PLoS ONE · doi:10.1371/journal.pone.0234971 · Cited by 21
“In different animal species different bacteria may be present in the faeces which further metabolize fGCMs differently [16,43].”
BackgroundHein, A. C., Palme, R., Baumgartner, K., von Fersen, L., Woelfing, B., Greenwood, A. D., Bechshøft, T., & Siebert, U. (2020) · Conservation Physiology · doi:10.1093/conphys/coaa012 · Cited by 19
“Nevertheless, a seasonal influence of the HPA axis reactivity is described for many seasonally breeding vertebrates including black bears (Harlow et al., 1990; Wingfield and Romero, 2010; Romero, 2002; Millspaugh and Washburn, 2004; Jachowski et al., 2015).”
BackgroundInfluentialParry-Jones, K., Webster, K. N., & Divljan, A. (2016) · Australian Mammalogy · doi:10.1071/am15030 · Cited by 18
Parnell, T., Narayan, E. J., Nicolson, V. N., Martin-Vegue, P., Mucci, A., & Hero, J. (2015) · Conservation Physiology · doi:10.1093/conphys/cov053 · Cited by 19
“This methodology has not been sufficiently tested for wider field applications, and crucial contextual factors that may influence species-specific FCM measurements remain untested (Millspaugh and Washburn, 2004; Barja et al., 2012).”
BackgroundA review of factors influencing the stress response in Australian marsupials
Hing, S., Narayan, E. J., Thompson, R. C. A., & Godfrey, S. S. (2014) · Conservation Physiology · doi:10.1093/conphys/cou027 · Cited by 59
“…(CBG) bound or albumin bound] and biological confounders (e.g. diurnal or seasonal fluctuations, reproduction, diet, pain and exercise) need also be considered when interpreting results and management implications (Millspaugh and Washburn, 2004; Palme, 2005; Lane, 2006; Evans et al. , 2013).”
InfluentialHogan, L. A., Lisle, A., Johnston, S., Goad, T., & Robertston, H. (2013) · doi:10.1670/11-290 · Cited by 15
“Urinary measurements have the advantage over fecal methods by providing a reduced lag time for hormone excretion and simplified processing (Millspaugh and Washburn, 2004).”
BackgroundConservation Physiology Tools: Their Role in Assessing Habitat Quality in Birds
Albano, N. (2012) · Ardeola · doi:10.13157/arla.59.2.2012.197 · Cited by 16
Manuel, J., & Daniel, R. (2011) · InTech eBooks · doi:10.5772/17051 · Cited by 10
“…activity, several aspects must be considered before undertaking a new study, and/or focusing on a new species, or applying a new immunoassay (Millspaugh and Washburn, 2004; Buchanan and Goldsmith, 2004; Palme, 2005; Touma and Palme, 2005; Wielebnowski and Watters, 2007; Hayward et al.,…”
BackgroundJankowski, M., Wittwer, D., Heisey, D., Franson, J., & Hofmeister, E. (2009) · Physiological and Biochemical Zoology · doi:10.1086/596513 · Cited by 15
Pimm, R., Dutton, C., O'Handley, S., & Mastromonaco, G. (2015) · Zoo Biology · doi:10.1002/zoo.21185 · Cited by 15
LaDue, C. A., Hunt, K. E., Kiso, W. K., & Freeman, E. W. (2023) · Conservation Physiology · doi:10.1093/conphys/coad019 · Cited by 16
Larm, M., Hovland, A. L., Palme, R., Thierry, A., Miller, A. L., Landa, A. M., Angerbjörn, A., & Eide, N. E. (2021) · Polar Biology · doi:10.1007/s00300-021-02917-1 · Cited by 15
Graham, K., Burgess, E., & Rolland, R. (2021) · Conservation Physiology · doi:10.1093/conphys/coaa133 · Cited by 14
Fecal Metabolomics as a Novel Noninvasive Method for Short-Term Stress Monitoring in Beef Cattle
Valerio, A., Casadei, L., Giuliani, A., & Valerio, M. (2019) · Journal of Proteome Research · doi:10.1021/acs.jproteome.9b00655 · Cited by 16
Roads and urban areas as physiological stressors of spiny-tailed lizards, Uromastyx acanthinura
Kechnebbou, M., Martín, J., Chammem, M., Arregui, L., & Nouira, S. (2019) · Journal of Arid Environments · doi:10.1016/j.jaridenv.2019.103997 · Cited by 14
Crossey, B., Ganswindt, A., & Chimimba, C. T. (2018) · Wildlife Biology · doi:10.2981/wlb.00469 · Cited by 13
“2004) and the potential uneven distribution of hormone metabolites throughout a faecal sample (Millspaugh and Washburn 2004).”
BackgroundStevenson, E. T., Gese, E. M., Neuman‐Lee, L. A., & French, S. S. (2017) · Journal of Comparative Physiology B · doi:10.1007/s00360-017-1125-2 · Cited by 17
“, cortisol and corticosterone) are steroid hormones that are elevated in response to stressors (Dalmau et al. 2007; Millspaugh and Washburn 2004; Möstl et al. 1999; von der Ohe and Servheen 2002) and can provide a quantitative means for evaluating physiological stress in animals (von der Ohe and Servheen 2002).”
BackgroundInfluentialVarner, J., Lambert, M. S., Horns, J. J., Laverty, S. M., Dizney, L. J., Beever, E. A., & Dearing, M. D. (2015) · International Journal of Wildland Fire · doi:10.1071/wf15038 · Cited by 15
“We used abundance and physiological stress as more sensitive predictors of habitat suitability than occupancy because they provide a more detailed and mechanistic understanding of how this species is affected by the disturbance (Millspaugh and Washburn 2004; Beever et al. 2013).”
MethodHaskell, S., & Ballard, W. (2008) · doi:10.1139/z08-039 · Cited by 14
Mahoney, J., Klug, P. E., & Reed, W. L. (2018) · Conservation Physiology · doi:10.1093/conphys/coy036 · Cited by 14
“…or new) can be used to analyze stable isotopes and stress response (i.e. corticosterone or cortisol) (Bortolotti et al., 2008; Richards et al., 2008; Carlitz et al., 2016), and faecal samples can be used for analyzing stress and reproduction (Millspaugh and Washburn, 2004; Schwarzenberger, 2007).”
BackgroundAnfossi, L., Ozella, L., Di Nardo, F., Giovannoli, C., Passini, C., Favaro, L., Pessani, D., Mostl, E., & Baggiani, C. (2014) · Anal. Methods · doi:10.1039/c4ay01407c · Cited by 13
Using piecewise regression to identify biological phenomena in biotelemetry datasets
Wolfson, D. W., Andersen, D. E., & Fieberg, J. (2022) · Journal of Animal Ecology · doi:10.1111/1365-2656.13779 · Cited by 20
“Most research on internal physiological responses have been limited to quantifying levels of glucocorticoids (e.g., cortisol and corticosterone: Baker et al., 2013; Bennitt et al., 2019; Millspaugh & Washburn, 2004; Vas et al., 2015; Wasser et al., 2000).”
BackgroundAugustine, L., Miller, K., Peters, A. M., Franklin, A. D., Steinbeiser, C. M., Brown, J. L., & Prado, N. A. (2020) · Zoo Biology · doi:10.1002/zoo.21559 · Cited by 11
Madliger, C., & Love, O. (2016) · Ecological Applications · doi:10.1002/eap.1401 · Cited by 13
Jachowski, D. S., Washburn, B. E., & Millspaugh, J. J. (2015) · Wildlife Society Bulletin · doi:10.1002/wsb.592 · Cited by 14
Self-citationAnnual pattern of fecal corticoid excretion in captive Red-tailed parrots (Amazona brasiliensis)
Popp, L. G., Serafini, P. P., Reghelin, A. L. S., Spercoski, K. M., Roper, J. J., & de Morais, R. N. (2008) · Journal of Comparative Physiology B · doi:10.1007/s00360-007-0241-9 · Cited by 14
“…have all been monitored by fecal corticosteroids analysis in a variety of bird species (Wasser et al. 1997, 2000; Kortrschal et al. 1998, 2000; Hirschenhauser et al. 2000, 2005; Carere et al. 2003; Dehnhard et al. 2003; Millspaugh and Washburn 2004; Scheiber et al. 2005; Touma and Palme 2005).”
BackgroundMotorized backcountry recreation and stress response in Mountain Caribou (Rangifer tarandus caribou)
Freeman, N. L. (2008) · cIRcle (University of British Columbia) · doi:10.14288/1.0066622 · Cited by 14
Evaluation of stress in farmed Atlantic salmon (Salmo salar) using different biological matrices
Keihani, R., Gomes, A. S., Balseiro, P., Handeland, S. O., Gorissen, M., & Arukwe, A. (2024) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2024.111743 · Cited by 14
“The use of fecal cortisol metabolites (FCM) or fecal glucocorticoid metabolites (FGM) in terrestrial animals has a relatively long history (Cook, 2012; Millspaugh and Washburn, 2004; Palme, 2005).”
BackgroundSadok, I., Ożga, K., Klich, D., Olech, W., Krauze‐Gryz, D., Beliniak, A., & Łopucki, R. (2023) · Scientific Reports · doi:10.1038/s41598-023-49940-2 · Cited by 12
“…gaps relate in particular to the possibility of applying the achievements of modern analytics (commonly used, for example, in medicine) in the study of wild and endangered animal species in order to better understand their physiological condition and to make their conservation more effective 27 .”
BackgroundWeather and land cover create a predictable “stress-scape” for a winter-adapted bird
Shipley, A. A., Sheriff, M., Pauli, J., & Zuckerberg, B. (2021) · Landscape Ecology · doi:10.1007/s10980-021-01354-z · Cited by 12
“kit (MP Biomedicals, Solon, Ohio) to measure FCMs (Wasser et al. 2000; Millspaugh and Washburn 2004), Fig.”
BackgroundMethodRosenblatt, E., Debow, J., Blouin, J., Donovan, T., Murdoch, J., Creel, S., Rogers, W., Gieder, K., Fortin, N., & Alexander, C. (2021) · Conservation Physiology · doi:10.1093/conphys/coab048 · Cited by 12
“The monitoring of stress and nutrition in wildlife populations provides valuable insight into the physiological impacts of landscape conditions on wildlife populations (Von Der Ohe and Servheen, 2002; Millspaugh and Washburn, 2004; Romero, 2004; Garcia Pereira et al., 2006).”
BackgroundNon-Invasive Measurement of Thyroid Hormones in Domestic Rabbits
Chmurska-Gąsowska, M., Sowińska, N., Pałka, S. E., Kmiecik, M., Lenarczyk-Knapik, J., & Migdał, Ł. (2021) · Animals · doi:10.3390/ani11051194 · Cited by 18
“Feces should be frozen as soon as possible after collection, due to the proven effects that fecal bacteria have on hormone metabolism [30,31] and the possibility of cross-reacting metabolites appearing [32], which may lead to false results relating to hormones or their metabolites.”
BackgroundNoninvasive measures of physiological stress are confounded by exposure
Lafferty, D. J. R., Zímová, M., Clontz, L. M., Hackländer, K., & Mills, L. S. (2019) · Scientific Reports · doi:10.1038/s41598-019-55715-5 · Cited by 13
Rizo‐Aguilar, A., Guerrero, J. A., Montoya-Lara, A. M. P., & Valdespino, C. (2014) · Mammalian Biology · doi:10.1016/j.mambio.2014.08.002 · Cited by 14
Labrada-Martagón, V., Zenteno-Savín, T., & Mangel, M. (2014) · Conservation Physiology · doi:10.1093/conphys/cot035 · Cited by 12
“…and application of less invasive methods (Hammond, 1990; Fossi et al., 1992; Jensen et al., 2003; Hunt et al., 2004; Mashburn and Atkinson, 2004; Millspaugh and Washburn, 2004; Sanvito et al., 2004; Bush et al., 2005; Al-Habsi et al., 2006; Sulikowski et al., 2006, 2012; Awruch et al., 2008a;…”
BackgroundMethodInfluentialLi, Y., Wang, C.-Y., Huang, S., Liu, Z., & Wang, H. (2021) · doi:10.1016/j.livsci.2020.104389 · Cited by 12
Neuman-Lee, L. A., Terletzky, P., Atwood, T., Gese, E., Smith, G. D., Greenfield, S. M., Pettit, J., & French, S. S. (2017) · Journal of Experimental Zoology Part A Ecological and Integrative Physiology · doi:10.1002/jez.2112 · Cited by 11
Hing, S., Narayan, E., Thompson, R., & Godfrey, S. (2017) · Journal of Zoology · doi:10.1111/jzo.12428 · Cited by 11
Mercer-Bowyer, S., Kersey, D. C., & Bertone, J. J. (2017) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.250.3.316 · Cited by 15
Circadian Rhythm and Stress Response in Droppings ofSerinus canaria
Turriani, M., Bernabò, N., Barboni, B., Todisco, G., Montini, L., & Berardinelli, P. (2016) · Veterinary Medicine International · doi:10.1155/2016/3086353 · Cited by 9
“Samples can be collected at regular intervals through time, thus providing an accurate assessment of stress without the bias of capture-induced increases in CORT [22, 31, 40, 41].”
Biochemical and clinical responses of Common Eiders to implanted satellite transmitters
Latty, C., Hollmen, T., Petersen, M., Powell, A., & Andrews, R. D. (2016) · The Condor · doi:10.1650/condor-16-7.1 · Cited by 11
de Bruin, P. R., Medger, K., Bennett, N. C., & Ganswindt, A. (2014) · African Zoology · doi:10.1080/15627020.2014.11407619 · Cited by 13
“…of controlling for the interval between defecation, sampling, and freezing of the collected material to minimize the potential risk of inadvertent changes in steroid metabolite composition due to active bacterial enzymes present in the faeces (Möstl et al. 1999; Millspaugh & Washburn 2004).”
BackgroundMethodInfluentialStress hormone concentration in Rocky Mountain populations of the American pika (Ochotona princeps)
Wilkening, J. L., Ray, C., & Sweazea, K. L. (2013) · Conservation Physiology · doi:10.1093/conphys/cot027 · Cited by 21
“In many cases, faecal samples can be collected relatively easily without disturbing or endangering the animal, which allows for repeated sampling over time (Mostl and Palme, 2002; Millspaugh and Washburn, 2004).”
BackgroundBody condition, hormonal correlates and consequences for survival in common tern chicks
Braasch, A., Palme, R., Hoppen, H., & Becker, P. (2011) · Journal of Comparative Physiology · doi:10.1007/s00359-011-0663-4 · Cited by 11
“Tempel and Gutie ´rrez 2004) to avoid confounding influences of (1) higher extraction efficiency ( Millspaugh and Washburn 2004 ), (2) relative water loss by evaporation in small samples or (3) small variations in the weight of the tissue papers the samples were taken up with.”
BackgroundInfluentialGladbach, A., Gladbach, D., Koch, M., Kuchar, A. C., Möstl, E., & Quillfeldt, P. (2011) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-011-1169-3 · Cited by 11
“1998), although faeces have the advantage to provide a time-integrated measure of hormone levels compared to point measures in serum analyses (Millspaugh and Washburn 2004).”
BackgroundAccessible ecophysiological tools for seabird conservation
Whitehead, E. A., & Dunphy, B. J. (2022) · Aquatic Conservation Marine and Freshwater Ecosystems · doi:10.1002/aqc.3890 · Cited by 11
Non-Invasive Monitoring of Adrenocortical Activity in Three Sympatric Desert Gerbil Species
Navarro‐Castilla, Á., Garrido, M., Hawlena, H., & Barja, I. (2021) · Animals · doi:10.3390/ani11010075 · Cited by 11
“, handling/blood-sampling), so it has proved to be a suitable alternative to blood sampling [19].”
BackgroundNavarro, J. L., Lèche, A., Costa, N. S. D., Cortez, M. V., Marin, R. H., & Martella, M. (2019) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2018.04.012 · Cited by 10
“However, prior to its use, this non-invasive technique must be correctly validated for each species (Millspaugh and Washburn, 2004), since the excreta contains multiple GC metabolites, and little or nothing of the hormone in its native state (Palme et al., 2005).”
BackgroundGholib, G., Agil, M., Supriatna, I., Purwantara, B., Heistermann, M., & Engelhardt, A. (2017) · doi:10.21157/j.ked.hewan.v11i2.6830 · Cited by 10
Wang, W., He, L., Liu, S., Wronski, T., & Hu, D. (2016) · acta ethologica · doi:10.1007/s10211-015-0232-x · Cited by 11
“Despite the usefulness of measuring FGM in wildlife species (Millspaugh and Washburn 2004), many confounding factors inhibit the utility of this technique.”
BackgroundKhonmee, J., Brown, J. L., Taya, K., Rojanasthien, S., Punyapornwithaya, V., Thumasanukul, D., Kongphoemphun, A., Siriaroonrat, B., Tipkantha, W., Pongpiachan, P., et al. (2014) · Theriogenology · doi:10.1016/j.theriogenology.2014.07.012 · Cited by 10
“Today, the relative ease of fecal collection and storage facilitates the noninvasive study of reproductive activity through evaluation of excreted hormonal metabolites [11–14].”
BackgroundSantos, J., Vicente, J., Villamuelas, M., Albanell, E., Serrano, E., Carvalho, J., Fonseca, C. M. D., Gortázar, C., & Lopez‐Olvera, J. R. (2014) · Ecological Indicators · doi:10.1016/j.ecolind.2014.05.021 · Cited by 12
Evans, N., Narayan, E. J., & Hero, J. (2013) · Australian Journal of Zoology · doi:10.1071/zo13032 · Cited by 9
“FCMs were then extracted from bilby faecal samples, as previously described for other mammals (Wielebnowski et al. 2002; Millspaugh and Washburn 2004) and validated recently for the greater bilby (Narayan et al. 2012).”
BackgroundMethodVALIDATION OF A FECAL GLUCOCORTICOID METABOLITE ASSAY FOR COLLARED PECCARIES (PECARI TAJACU)
Coradello, M. A., de Morais, R. N., Roper, J. J., Spercoski, K. M., Massuda, T., Nogueira, S. S. D. C., & Nogueira-Filho, S. L. G. (2012) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2011-0046.1 · Cited by 10
“Animal welfare has been receiving increasing attention during recent years,(3) and various methods to assess the welfare of free-ranging and captive wild animals have been carried out.(7,8,12,16,17,20,30,33,55,61) Nevertheless, there is a lack of knowledge about similar reactions in neotropical wild animals,(39) and m…”
Influence of Radiotransmitters on Fecal Glucocorticoid Levels of Free‐Ranging Male American Kestrels
Pereira, R. J. G., Granzinolli, M. A. M., de Barros, F. M., & Duarte, J. M. B. (2009) · Journal of Wildlife Management · doi:10.2193/2008-184 · Cited by 11
“We tried to obtain as many fecal samples as possible during each collecting day (about 3–6 samples/4-hr period) to avoid problems associated with glucocorticoid measurement of extremely small fecal samples (Millspaugh and Washburn 2004).”
MethodConservation Genetics in Mammals: Integrative Research Using Novel Approaches
Ortega, J., & Maldonado, J. (2020) · doi:10.1007/978-3-030-33334-8 · Cited by 10
Deng, H., Jin, X., Hu, D., & Liu, D. (2014) · Animal Biology · doi:10.1163/15707563-00002432 · Cited by 8
Grundei, L.-L., Wolf, T. E., Brandes, F., Schütte, K., Freise, F., Siebert, U., Touma, C., & Pees, M. (2024) · Animals · doi:10.3390/ani14081234 · Cited by 8
“Samples with less than 0.02 g dried weight were excluded from the study [51].”
MethodInfluentialInstability of fecal glucocorticoid metabolites at 4°C: Time to freeze matters.
Carbillet, J., Palme, R., Maublanc, M., Cèbe, N., Gilot-Fromont, E., Verheyden, H., & Rey, B. (2023) · Journal of Experimental Zoology Part A Ecological and Integrative Physiology · doi:10.1002/jez.2704 · Cited by 9
Hickmott, A. J., Boose, K. J., Wakefield, M. L., Brand, C. M., Snodgrass, J. J., Ting, N., & White, F. J. (2022) · Microbiology · doi:10.1099/mic.0.001226 · Cited by 14
“Therefore, FGMC are capturing the stress an individual experienced in the preceding 48 h before a faecal sample was collected [51].”
BackgroundShultz, S., Britnell, J., & Harvey, N. (2021) · Ecology and Evolution · doi:10.1002/ece3.8331 · Cited by 9
“GCs have been used as an indicator of stress, commonly under the assumption that chronic elevation compromises health and ultimately fitness (Millspaugh & Washburn, 2004).”
MethodHow do humans impact yellow-bellied marmots? An integrative analysis
Morgan, A., Monclús, R., Nelson, J. L., Foli, E., Li, C., & Blumstein, D. T. (2021) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2021.105495 · Cited by 9
“Changes in antipredator behaviour may lead to altered population dynamics (Frid and Dill, 2002) as well as physiological responses can further alter behavioural processes leading to reduced population performance (Millspaugh and Washburn, 2004).”
BackgroundFecal Glucocorticoid Metabolites as Biomarkers in Equids: Assay Choice Matters
Hinchcliffe, D., Lea, J. M. D., Palme, R., & Shultz, S. (2021) · Journal of Wildlife Management · doi:10.1002/jwmg.22066 · Cited by 11
Blecher, A. S., Scheun, J., & Ganswindt, A. (2021) · MethodsX · doi:10.1016/j.mex.2021.101229 · Cited by 9
Ensminger, D. C., Pritchard, C. E., Langkilde, T. L., Gingery, T. M., Banfield, J. E., & Walter, W. D. (2020) · Wildlife Biology · doi:10.2981/wlb.00683 · Cited by 10
“Consequently, glucocorticoids are being used in ecology and conservation as an index of the physiological state and health of an animal (Millspaugh and Washburn 2004, Busch and Hayward 2009).”
BackgroundMurray, M. J., Young, M., & Santymire, R. M. (2019) · Conservation Physiology · doi:10.1093/conphys/coz116 · Cited by 8
“Typically, juveniles have higher GC values than adults most likely because they are growing and have a faster metabolic rate (Millspaugh and Washburn, 2004).”
BackgroundWhipple, A., Ray, C., Wasser, M., Kitchens, J., Hove, A., Varner, J., & Wilkening, J. L. (2020) · Conservation Physiology · doi:10.1093/conphys/coab024 · Cited by 9
Metadata
- Authors
- Millspaugh, J. J., & Washburn, B. E.
- Affiliations
- University of Missouri (US)
- Animal and Plant Health Inspection Service (US)
- Corresponding author
- Millspaugh, Joshua J.
- Venue
- General and Comparative Endocrinology
- Publisher
- Elsevier BV
- Published
- 2004-09
- Volume
- 138
- Issue
- 3
- Pages
- 189-199
- ISSN
- 0016-6480 (ISSN-L)
- OpenAlex
- W2168394255
- Cited by
- 553
- References
- 0
- Citations by year
- 2026: 19 · 2025: 20 · 2024: 24 · 2023: 25 · 2022: 18 · 2021: 43 · 2020: 25 · 2019: 25 · 2018: 32 · 2017: 25 · 2016: 30 · 2015: 25 · 2014: 43 · 2013: 37 · 2012: 31
- FWCI
- 3.53
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- General and Comparative Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Lincoln (University of Nebraska) (submittedVersion)
- Funders
- University of Missouri
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Behavior and Welfare Studies
- Physical Sciences › Environmental Science › Ecology › Wildlife Ecology and Conservation
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- fecal glucocorticoid metabolites, stress hormones, glucocorticoid secretion, adrenocortical function, conservation biology, seasonal rhythms, body condition, assay selection, social ranking, reproductive status, threatened species, wildlife disturbance, surrogate species
- MeSH terms
- Age Factors, Animals, Conservation of Natural Resources, Ecology, Feces, Female, Glucocorticoids, Male, Reproduction, Seasons, Sex Factors, Specimen Handling, Zoology, Reproducibility of Results, Clinical Laboratory Techniques
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