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.
“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
The non-invasive method of faecal hormone sampling permits monitoring of the animal's endocrine status without capturing or handling the animals, which may compromise accurate assessment of stress.
“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
Samples were frozen immediately after collection at −20 °C.
“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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“Noninvasive genetic sampling of feces and hair follicles is increasingly used (Taberlet & Luikart 1999) as is noninvasive fecal glucocorticoid metabolite measurement (Millspaugh & Washburn 2004).”
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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 71 · see citing works
“FCM was extracted from Koala faecal samples using the methods as previously described for other mammals [23; 30; 49].”
Lucas, J. R., Freeberg, T., Egbert, J., & Schwabl, H. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.012 · Cited by 64 · see citing works
“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. (2012) · Animal Conservation · doi:10.1111/j.1469-1795.2011.00503.x · Cited by 63 · see citing works
“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 · see citing works
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 · see citing works
Williams, E., Chadwick, C., Yon, L., & Asher, L. (2018) · Animal Welfare · doi:10.7120/09627286.27.3.235 · Cited by 59 · see citing works
“…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., & Herzog, M. (2012) · Environmental Science and Technology · doi:10.1021/es300668c · Cited by 58 · see citing works
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 61 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
“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., & Armstrong, D. (2009) · Zoo Biology · doi:10.1002/zoo.20248 · Cited by 56
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 · see citing works
“(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 50 · see citing works
“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. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.10.017 · Cited by 55 · see citing works
“…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 · see citing works
Jachowski, D. S., & Singh, N. J. (2015) · Conservation Physiology · doi:10.1093/conphys/cov035 · Cited by 54 · see citing works
“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 54 · see citing works
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 51 · see citing works
“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 56 · see citing works
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 · see citing works
“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., Oswald, S., Voigt, C., Palme, R., Braasch, A., Bauch, C., & Becker, P. (2008) · Journal of Avian Biology · doi:10.1111/j.0908-8857.2008.04265.x · Cited by 49 · see citing works
“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 57 · see citing works
- 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
- Health Sciences › Veterinary › Small Animals › 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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