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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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“Faecal cortisol (and/or metabolite) determinations in free-ranging animals have become an important tool in wildlife conservation (Keay et al., 2006; Millspaugh and Washburn, 2004; Romano et al., 2010).”
Health surveillance in wildlife reintroductions
Mathews, F., Moro, D., Strachan, R., Gelling, M., & Buller, N. (2006) · doi:10.1016/j.biocon.2006.04.011 · Cited by 153
Ayres, K. L., Booth, R. K., Hempelmann, J. A., Koski, K. L., Emmons, C. K., Baird, R. W., Balcomb-Bartok, K., Hanson, M. B., Ford, M. J., & Wasser, S. K. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036842 · Cited by 139
Carlstead, K., & Brown, J. L. (2005) · Zoo Biology · doi:10.1002/zoo.20050 · Cited by 176
Measuring corticosterone in feathers: Strengths, limitations, and suggestions for the future
Romero, L. M., & Fairhurst, G. D. (2016) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2016.05.002 · Cited by 147
Dantzer, B., Fletcher, Q. E., Boonstra, R., & Sheriff, M. J. (2014) · Conservation Physiology · doi:10.1093/conphys/cou023 · Cited by 467
“However, several confounding factors that can limit the utility of FGM measures are sometimes overlooked, though they have been highlighted in detail (Buchanan and Goldsmith, 2004; Millspaugh and Washburn, 2004; Palme, 2005; Sheriff et al., 2011b; Goymann, 2012).”
BackgroundAnalysis of fecal glucocorticoids in the North Atlantic right whale (Eubalaena glacialis).
Hunt, K., Rolland, R., Kraus, S., & Wasser, S. (2006) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2006.03.012 · Cited by 142
“Provided fecal assays are well-validated and interpreted with care (Millspaugh and Washburn, 2004; Mostl and Palme, 2002; Wasser et al., 2000; Young et al., 2004), they have proven to have considerable practical utility in the Weld, correlating with a variety of known stressors in many mammalian…”
BackgroundConsequences of brown bear viewing tourism : A review
Penteriani, V., López-Bao, J., Bettega, C., Dalerum, F., Delgado, M. D. M., Jerina, K., Kojola, I., Krofel, M., & Ordiz, A. (2017) · Biological Conservation · doi:10.1016/j.biocon.2016.12.035 · Cited by 141
“Stress can alter behaviour, reduce resistance to disease and, thus, may affect population performance (Millspaugh and Washburn, 2004).”
BackgroundMuehlenbein, M. P., Ancrenaz, M., Sakong, R., Ambu, L. N., Prall, S. P., Fuller, G. A., & Raghanti, M. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033357 · Cited by 149
Zemanova, M. A. (2020) · Wildlife Biology · doi:10.2981/wlb.00607 · Cited by 176
“Stress can be quantified by measuring the level of glucocorticoids, a class of steroid hormones (Millspaugh and Washburn 2004).”
BackgroundBaugh, A. T., Schaper, S. V., Hau, M., Cockrem, J. F., de Goede, P., & van Oers, K. (2011) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2011.12.012 · Cited by 128
“Fecal CORT measurements, however, represent a combination of stressed and non-stressed contributions [33,37].”
BackgroundAshley, N. T., Barboza, P. S., Macbeth, B. J., Janz, D. M., Cattet, M., Booth, R. K., & Wasser, S. K. (2011) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2011.03.029 · Cited by 139
“The study of stress has become increasingly integrated into the population assessments of wild vertebrates as a biomarker of health [51,64,89].”
BackgroundInfluentialWarinner, C., Speller, C., Collins, M. J., & Lewis, C. M. (2015) · Journal of Human Evolution · doi:10.1016/j.jhevol.2014.10.016 · Cited by 178
“…other steroid hormones can be routinely and non-invasively collected from wildlife fecal samples to study adrenocortical activity (Mostl and Palme, 2002; Millspaugh and Washburn, 2004), human coprolites may also provide insight into the physiological stress and reproduction of ancient populations.”
Hair cortisol: a parameter of chronic stress? Insights from a radiometabolism study in guinea pigs
Keckeis, K., Lepschy, M., Schöpper, H., Moser, L. B., Troxler, J., & Palme, R. (2012) · Journal of Comparative Physiology B · doi:10.1007/s00360-012-0674-7 · Cited by 119
“…and biological effects along with interspecies differences in metabolism and excretion, the validation of this technique for any given species is crucial for reliable application and the interpretation of results (Millspaugh and Washburn 2004; Palme 2005; Sheriff et al. 2011; Touma and Palme 2005).”
InfluentialShutt, K. A., Setchell, J. M., & Heistermann, M. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.08.008 · Cited by 118
“They also have important applications for addressing conservation issues (Foley, Papageorge & Wasser 2001; Millspaugh & Washburn 2004; Cockrem 2005; Wasser & Hunt 2005).”
Non-invasive monitoring of physiological markers in primates
Behringer, V., & Deschner, T. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.02.001 · Cited by 145
“Hormones are unevenly distributed throughout a fecal sample necessitating a thorough homogenisation before extraction (Millspaugh and Washburn, 2004; Palme, 2005).”
BackgroundInfluentialLemos, L. S., Angarica, L., Hauser‐Davis, R. A., & Quinete, N. (2023) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph20136237 · Cited by 124
“Another disadvantage of using fecal samples is that relatively higher sample sizes are required, as low masses can lead to inflated results [50,51].”
BackgroundEvaluating habitat quality of vertebrates using conservation physiology tools.
Homyack, J. A. (2010) · Wildlife Research · doi:10.1071/wr08093 · Cited by 109
Meter, P. E. V., French, J. A., Dloniak, S. M., Watts, H. E., Kolowski, J. M., & Holekamp, K. E. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.11.001 · Cited by 112
“Whereas endocrine studies have traditionally been used in conservation to monitor reproduction in rare or threatened species, hormones are now being used to monitor stress physiology as an indicator of how animals cope with social and ecological challenges in their daily lives (Millspaugh and Washburn, 2004; Walker et…”
InfluentialConservation and behavioral neuroendocrinology
Cockrem, J. F. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.03.008 · Cited by 106
Shutt, K. A., Heistermann, M., Kasim, A., Todd, A. F., Pafčo, B., Profosouva, I., Petrželková, K. J., Fuh, T., Dicky, J.-F., Bopalanzognako, J.-B., et al. (2014) · Biological Conservation · doi:10.1016/j.biocon.2014.02.014 · Cited by 109
“This seems to be the case in Magellanic penguins (Spheniscus magellanicus) exposed to tourism (Walker et al., 2005) and is well documented in research investigating the stress impacts of wildlife tourism on other animal species (Fowler, 1999; Millspaugh and Washburn, 2004; Müllner et al., 2004).”
BackgroundGoymann, W., Trappschuh, M., Jensen, W., & Schwabl, I. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.006 · Cited by 99
Can non-invasive glucocorticoid measures be used as reliable indicators of stress in animals?
Lane, J. M. (2006) · Animal Welfare · doi:10.1017/s0962728600030657 · Cited by 107
Wey, T. W., & Blumstein, D. T. (2012) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-012-1358-8 · Cited by 100
“Fecal glucocorticoid metabolites (FGMs) can provide an integrated measure of stress hormone production over time and have been used as a non-invasive measure of baseline or chronic stress in wildlife populations (Millspaugh and Washburn 2004; Keay et al. 2006).”
MethodLattin, C. R., Reed, J. M., DesRochers, D. W., & Romero, L. M. (2011) · Journal of Avian Biology · doi:10.1111/j.1600-048x.2010.05310.x · Cited by 175
“All techniques for measuring CORT to date have limitations (e.g. Millspaugh and Washburn 2004), so continued validation work is necessary for establishing the benefits and limitations of measuring CORT in feathers.”
Repeatability of baseline corticosterone concentrations.
Romero, L. M., & Reed, J. M. (2008) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2007.10.001 · Cited by 92
“Alternatively, researchers can collect a general measure of corticosterone by analyzing fecal steroid metabolites (Millspaugh and Washburn, 2004).”
Lobato, E., Merino, S., Moreno, J., Morales, J., Tomás, G., la Puente, J. M., Osorno, J. L., Kuchar, A., & Möstl, E. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.10.010 · Cited by 87
“sample, given that separation of droppings in parts is not practicable for a large number of samples and mixed samples may be more representative of the amount of excreted CORT metabolites (Millspaugh and Washburn, 2004).”
BackgroundHigh faecal glucocorticoid levels predict mortality in ring-tailed lemurs ( Lemur catta )
Pride, R. E. (2005) · Biology Letters · doi:10.1098/rsbl.2004.0245 · Cited by 144
Female field voles with high testosterone and glucose levels produce male-biased litters
Helle, S., Laaksonen, T., Adamsson, A., Paranko, J., & Huitu, O. (2007) · Animal Behaviour · doi:10.1016/j.anbehav.2007.08.015 · Cited by 80
“Prior to these analyses, the potential dependence of female testosterone and corticosterone concentrations on oestrus cycle phase (Millspaugh & Washburn 2004; Cavigelli et al. 2005) was examined by general linear models, where oestrus cycle was treated as a four-level fixed effect (prooestrus,…”
BackgroundMethodInfluentialFranceschini, M. D., Rubenstein, D. I., Low, B., & Romero, L. M. (2008) · Animal Conservation · doi:10.1111/j.1469-1795.2008.00175.x · Cited by 89
“this technique in wildlife field studies and in investigating conservation issues ( Millspaugh & Washburn, 2004; Palme, 2005; Touma & Palme, 2005; Keay et al., 2006).”
BackgroundMethodInfluentialArlettaz, R., Nusslé, S. C., Baltić, M., Vogel, P., Palme, R., Jenni‐Eiermann, S., Patthey, P., & Genoud, M. (2014) · Ecological Applications · doi:10.1890/14-1141.1 · Cited by 101
“…physiological factors, such as body condition, age, reproductive status, gender (Wingfield et al. 1995, Wasser et al. 1997, Goymann et al. 2002, Millspaugh and Washburn 2004, Touma and Palme 2005), and even habituation to predictable or unpredictable stressors (Wingfield et al. 1997, Fowler…”
BackgroundEffects of human activity on physiological and behavioral responses of an endangered steppe bird
Tarjuelo, R., Barja, I., Morales, M. B., Traba, J., Benítez‐López, A., Casas, F., Arroyo, B., Delgado, M. P., & Mougeot, F. (2015) · Behavioral Ecology · doi:10.1093/beheco/arv016 · Cited by 87
Molecular ecology of marine turtles: New approaches and future directions
Lee, P. L. M. (2008) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/j.jembe.2007.12.021 · Cited by 85
Zwijacz-Kozica, T., Selva, N., Barja, I., Silván, G., Martínez-Fernández, L., Illera, J., & Jodłowski, M. (2013) · ACTA THERIOLOGICA · doi:10.1007/s13364-012-0108-7 · Cited by 84
“Because glucocorticoid metabolite levels vary with sample age and environmental conditions (Millspaugh and Washburn 2004), only fresh droppings were collected.”
BackgroundBlas, J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-407160-5.00033-6 · Cited by 98
Cizauskas, C. A., Turner, W. C., Pitts, N., & Getz, W. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0120800 · Cited by 82
“Steroid hormones can be detected in blood and their metabolites can be detected in feces; however, measurements of hormone metabolites in feces are often best in wildlife because fecal collection can often be done noninvasively and is free from stress hormone feedback mechanisms, and fecal samples reflect longer term…”
BackgroundDantzer, B., McAdam, A. G., Palme, R., Boutin, S. A., & Boonstra, R. (2011) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2011.08.010 · Cited by 86
“However, the ease of collection belies some of the difficulties associated with measuring FHM in free-ranging animals [5,23,41,46].”
BackgroundNarayan, E. J., Molinia, F. C., Christi, K. S., Morley, C., & Cockrem, J. F. (2010) · Australian Journal of Zoology · doi:10.1071/zo10010 · Cited by 82
Cornale, P., Macchi, E., Miretti, S., Renna, M., Lussiana, C., Perona, G., & Mimosi, A. (2015) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2015.05.002 · Cited by 79
Fair, P., Schaefer, A., Romano, T., Bossart, G., Lamb, S., & Reif, J. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2014.07.002 · Cited by 79
“Long term monitoring of populations can provide useful information required to draw inferences for valid interpretation of stress hormone levels (Millspaugh and Washburn, 2004).”
BackgroundPhysiology in conservation translocations
Tarszisz, E., Dickman, C. R., & Munn, A. J. (2014) · Conservation Physiology · doi:10.1093/conphys/cou054 · Cited by 83
“Despite the benefits of acute or immediate responses to stressors, persistent or chronic exposure to stressors (or the perception of stressors) can have a range of deleterious effects (Millspaugh and Washburn, 2004; Dhabhar, 2009).”
BackgroundStress Response of Working African Elephants to Transportation and Safari Adventures
Millspaugh, J. J., Burke, T., van Dyk, G., Slotow, R., Washburn, B. E., & WOODS, R. J. (2007) · Journal of Wildlife Management · doi:10.2193/2006-015 · Cited by 75
Self-citationClark, F. E., Fitzpatrick, M., Hartley, A., King, A. J., Lee, T., Routh, A., Walker, S. L., & George, K. (2012) · Zoo Biology · doi:10.1002/zoo.20396 · Cited by 75
Beyond Glucocorticoids: Integrating Dehydroepiandrosterone (DHEA) into Animal Welfare Research
Whitham, J. C., Bryant, J. L., & Miller, L. J. (2020) · Animals · doi:10.3390/ani10081381 · Cited by 97
“For example, the researcher must consider how much time has passed between defecation and collection, as exposure to the elements may impact bacterial metabolism and either increase or decrease metabolite concentrations [10,138].”
BackgroundBean, T. G., Boxall, A. B. A., Lane, J. M., Herborn, K. A., Pietravalle, S., & Arnold, K. E. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0575 · Cited by 62
Cyr, N. E., & Romero, L. M. (2008) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2008.05.001 · Cited by 70
Broin, F. D., Hamel, S., Mastromonaco, G. F., & Côté, S. D. (2019) · Functional Ecology · doi:10.1111/1365-2435.13514 · Cited by 82
Rimbach, R., Heymann, E. W., Link, A., & Heistermann, M. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.05.010 · Cited by 69
“In many species basal stress hormone levels are affected by a variety of intrinsic factors (for review see (Goymann, 2012; Keay et al., 2006; Millspaugh and Washburn, 2004)) such as age (Sapolsky, 1992; Seraphin et al., 2008), sex (Raminelli et al., 2001; Sapolsky, 1992; Touma et al., 2003),…”
BackgroundEffect of Monitoring Technique on Quality of Conservation Science
Jewell, Z. C. (2013) · Conservation Biology · doi:10.1111/cobi.12066 · Cited by 69
“Noninvasive genetic sampling of feces and hair follicles is increasingly used (Taberlet & Luikart 1999) as is noninvasive fecal glucocorticoid metabolite measurement (Millspaugh & Washburn 2004).”
MethodSnaith, T. V., Chapman, C., Rothman, J., & Wasserman, M. (2008) · American Journal of Primatology · doi:10.1002/ajp.20601 · Cited by 68
Wielebnowski, N. C., & Watters, J. V. (2007) · Israel Journal of Ecology and Evolution · doi:10.1560/ijee.53.3.439 · Cited by 72
Vaz, J., Narayan, E. J., Kumar, R., Thenmozhi, K., Thiyagesan, K., & Baskaran, N. (2017) · PLoS ONE · doi:10.1371/journal.pone.0174711 · Cited by 102
Narayan, E. J., Webster, K. N., Nicolson, V. N., Mucci, A., & Hero, J. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.03.021 · Cited by 74
“FCM was extracted from Koala faecal samples using the methods as previously described for other mammals [23; 30; 49].”
Lucas, J. R., Freeberg, T. M., Egbert, J. R., & Schwabl, H. G. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.012 · Cited by 57
“Having said this, we acknowledge the caveats offered by a number of authors (e.g., Goymann, 2005; Millspaugh and Washburn, 2004; Touma and Palme, 2005) that several levels of validation are important to verify the validity of fCort measurements.”
BackgroundFactors influencing degradation of DNA and hormones in maned wolf scat
Vynne, C., Baker, M. R., Breuer, Z. K., & Wasser, S. K. (2011) · Animal Conservation · doi:10.1111/j.1469-1795.2011.00503.x · Cited by 67
“Old or poor-quality samples may also influence the amount of measurable hormone from a sample (Millspaugh & Washburn, 2004).”
BackgroundElevated levels of stress hormones in crop-raiding male elephants
Ahlering, M., Millspaugh, J. J., WOODS, R. J., Western, D., & Eggert, L. S. (2010) · Animal Conservation · doi:10.1111/j.1469-1795.2010.00400.x · Cited by 60
Self-citationLi, C., Jiang, Z., Tang, S., & Zeng, Y. (2007) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2007.01.014 · Cited by 51
Williams, E., Chadwick, C., Yon, L., & Asher, L. (2018) · Animal Welfare · doi:10.7120/09627286.27.3.235 · Cited by 59
“…92 measure of GC, are confounded by a number of factors, including those directly related to the sample 93 (e.g. age of sample, collection method) and biological factors (e.g. sex, age and reproductive status 94 of the animal), which can complicate interpretation (Millspaugh & Washburn, 2004).”
BackgroundMercury Exposure May Suppress Baseline Corticosterone Levels in Juvenile Birds
Herring, G., Ackerman, J. T., & Herzog, M. P. (2012) · Environmental Science & Technology · doi:10.1021/es300668c · Cited by 62
Behavioral responses of bison and elk in Yellowstone to snowmobiles and snow coaches.
Borkowski, J., White, P. J., Garrott, R. A., Davis, T. L., Hardy, A., & Reinhart, D. J. (2006) · Ecological Applications · doi:10.1890/1051-0761(2006)016[1911:brobae]2.0.co;2 · Cited by 58
“…are not surprising given recent findings that many factors influence cortisol excretion independent of direct effects on adrenal responses, including age, sex, seasonal patterns in GC secretion, body condition, diet, social ranking, and reproductive status (Millspaugh and Washburn 2004).”
BackgroundKersey, D. C., Wildt, D. E., Brown, J. L., Snyder, R. J., Huang, Y., & Monfort, S. L. (2011) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2011.06.013 · Cited by 63
Non-invasive Methods for Measuring and Monitoring Stress Physiology in Imperiled Amphibians
Narayan, E. J., Forsburg, Z. R., Davis, D. R., & Gabor, C. R. (2019) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2019.00431 · Cited by 64
“Measuring GCs via urine is becoming more frequently used over fecal measurements and reduces labor costs (Millspaugh and Washburn, 2004), and uGMs are ideal for amphibian species where fecal samples may not be easy to obtain in the wild.”
BackgroundGlucocorticoids and gut bacteria: “The GALF Hypothesis” in the metagenomic era
Morris, D. J., & Ridlon, J. M. (2017) · Steroids · doi:10.1016/j.steroids.2017.06.002 · Cited by 63
Malcolm, K., McShea, W., Deelen, T. V. V., Bacon, H., Liu, F., Putman, S., Zhu, X., & Brown, J. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.01.014 · Cited by 56
“Feces have long been used as a non-invasive tool for monitoring HPA activity in wildlife 71 [6, 15, 34, 35, 37], and analyses of excreted glucocorticoid metabolites have helped identify 72 environmental, management, and social variables that are potentially stressful [8, 27, 32, 40].”
Santymire, R. M., & Armstrong, D. M. (2009) · Zoo Biology · doi:10.1002/zoo.20248 · Cited by 52
Kumar, V., Palugulla Reddy, V., Kokkiligadda, A., Shivaji, S., & Umapathy, G. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2014.03.024 · Cited by 55
“(Millspaugh and Washburn, 2004; Keay et al., 2006).”
Voellmy, I. K., Gonçalves, I. B., Barrette, M.-F., Monfort, S. L., & Manser, M. B. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.08.008 · Cited by 53
“Sex, body condition, reproductive stage (Keay et al., 2006; Millspaugh and Washburn, 2004), and social context (Creel et al., 2013) are all likely to affect both adrenal activity and time required to respond to potential predators.”
Hämäläinen, A., Heistermann, M., Fenosoa, Z. S. E., & Kraus, C. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.10.017 · Cited by 70
“…the major peak of immunoreactivity was detected around fraction 50 at a position where in other primate species metabolites of testosterone elute (Möhle et al., 2002), indicating a substantial co-measurement of steroids not deriving from Table 2 Fecal glucocorticoid concentrations (as detected…”
BackgroundMethodSanticchia, F., Dantzer, B., van Kesteren, F., Palme, R., Martinoli, A., Ferrari, N., & Wauters, L. A. (2018) · Journal of Animal Ecology · doi:10.1111/1365-2656.12853 · Cited by 48
Jachowski, D. S., & Singh, N. J. (2015) · Conservation Physiology · doi:10.1093/conphys/cov035 · Cited by 54
“Regardless of the sampling technique, all approaches must be validated, and some sort of physiological baseline or basal physiological state must be established with which to compare subsequent samples (Millspaugh and Washburn, 2004).”
InfluentialJuliana, J. R. S., Khokhlova, I. S., Wielebnowski, N. C., Kotler, B. P., & Krasnov, B. R. (2014) · Journal of Animal Ecology · doi:10.1111/1365-2656.12217 · Cited by 58
Comparative patterns of adrenal activity in captive and wild Canada lynx (Lynx canadensis)
Fanson, K. V., Wielebnowski, N. C., Shenk, T. M., & Lucas, J. R. (2011) · Journal of Comparative Physiology B · doi:10.1007/s00360-011-0597-8 · Cited by 55
“thermore, several of these factors may also affect metabolism and/or excretion of GCs (Millspaugh and Washburn 2004; Sheriff et al. 2011; Touma and Palme 2005; Wielebnowski and Watters 2007).”
BackgroundPhysiological Stress in Koala Populations near the Arid Edge of Their Distribution
Davies, N., Gramotnev, G., McAlpine, C., Seabrook, L., BAXTER, G. S., Lunney, D., Rhodes, J. R., & Bradley, A. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0079136 · Cited by 59
Brown, M., Lappin, M., Brown, J. L., Munkhtsog, B., & Swanson, W. (2005) · Journal of Wildlife Diseases · doi:10.7589/0090-3558-41.4.691 · Cited by 51
Burke, T., Page, B. R., van Dyk, G., Millspaugh, J. J., & Slotow, R. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002417 · Cited by 46
“The protocol for collecting, storing and processing the samples and the extraction of cortisol from the samples is extensively described elsewhere [11,38].”
MethodSelf-citationAcute Lead Toxicosis in Mourning Doves
Schulz, J. H., Millspaugh, J., Bermudez, A. J., Gao, X.-M., Bonnot, T., Britt, L., & Paine, M. (2006) · doi:10.2193/0022-541x(2006)70[413:altimd]2.0.co;2 · Cited by 50
Self-citationArnold, J. M., Oswald, S. A., Voigt, C. C., Palme, R., Braasch, A., Bauch, C., & Becker, P. H. (2008) · Journal of Avian Biology · doi:10.1111/j.0908-8857.2008.04265.x · Cited by 72
“the age of the sample (Millspaugh and Washburn 2004).”
Valenzuela-Molina, M., Atkinson, S., Mashburn, K., Gendron, D., & Brownell, R. (2018) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2018.02.015 · Cited by 48
Suzuki, K., Yamada, H., Kobayashi, T., & Okanoya, K. (2012) · Journal of Experimental Zoology Part A Ecological Genetics and Physiology · doi:10.1002/jez.1748 · Cited by 56
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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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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