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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
In the citing paper
“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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“However the application of fecal hormone methods to avian species has been constrained by a persistent effect of low sample mass on measures of steroid metabolite concentration (Cyr and Romero, 2008; Goymann et al., 2006; Millspaugh and Washburn, 2004; Tempel and Gutierrez, 2004; Washburn et al., 2004).”
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“The collection of fresh and uncontaminated biological samples may also be dif fi cult in the wild, and physiological levels may not remain stable over time in exposed matrices (e.g. faecal glucocorticoid metabolites; Millspaugh & Washburn, 2004).”
BackgroundCapture—recapture of white‐tailed deer using DNA from fecal pellet groups
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“Additional information can be obtained from pellet groups including genetic diversity, habitat use, forage preference, movements, stress hormone levels and disease (Robbins et al. 1975, Collins and Urness 1981, Millspaugh et al. 2002, Millspaugh and Washburn 2004, Harris et al. 2010).”
BackgroundBauer, C. M., Glassman, L. W., Cyr, N. E., & Romero, L. (2011) · Comparative biochemistry and physiology. Part A, Molecular & integrative physiology · doi:10.1016/j.cbpa.2011.07.009 · Cited by 43
“…fecal pellets allowed for a better estimate of FGM concentrations during the previous period (Cyr and Romero, 2008) and also increased sample mass to avoid small fecal samples that can produce disproportionately higher FGM levels than large samples (Millspaugh and Washburn, 2004; Goymann, 2005).”
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Comparing plasma and faecal measures of steroid hormones in Adelie penguins Pygoscelis adeliae
Ninnes, C. E., Waas, J. R., Ling, N., Nakagawa, S., Banks, J. C., Bell, D. G., Bright, A., Carey, P. W., Chandler, J., Hudson, Q. J., et al. (2010) · Journal of Comparative Physiology B · doi:10.1007/s00360-009-0390-0 · Cited by 39
“In addition, it should be noted that there are other confounding factors that can potentially inXuence the results of faecal hormone measurements, such as sample age and sample storage methods (reviewed by Millspaugh and Washburn 2004 ), which were standardised in this study.”
BackgroundInfluentialSzott, I. D., Pretorius, Y., Ganswindt, A., & Koyama, N. F. (2019) · Wildlife Research · doi:10.1071/wr19045 · Cited by 60
Investigation of techniques to measure cortisol and testosterone concentrations in coyote hair
Schell, C. J., Young, J. K., Lonsdorf, E. V., Mateo, J. M., & Santymire, R. M. (2017) · Zoo Biology · doi:10.1002/zoo.21359 · Cited by 45
Bashaw, M. J., Sicks, F., Palme, R., Schwarzenberger, F., Tordiffe, A. S. W., & Ganswindt, A. (2016) · BMC Veterinary Research · doi:10.1186/s12917-016-0864-8 · Cited by 47
“Giraffes in captivity might reasonably be expected to have different baseline levels of GC and/or respond differently to stressors than wild giraffes [72], so field studies should seek withinindividual patterns of FGM that can be attributed to particular events.”
BackgroundOsada, K., Miyazono, S., & Kashiwayanagi, M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00276 · Cited by 39
Laver, P. N., Ganswindt, A., Ganswindt, S. B., & Alexander, K. A. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.08.011 · Cited by 39
“Non-invasive hormone monitoring, especially through excretions such as feces, urine and saliva, is already a well-established approach [14,46,45,28,34,24, 51,32].”
Using odor cues to elicit a behavioral and hormonal response in zoo‐housed African wild dogs
Rafacz, M. L., & Santymire, R. M. (2013) · Zoo Biology · doi:10.1002/zoo.21107 · Cited by 43
A novel method for the measurement of glucocorticoids in dermal secretions of amphibians
Santymire, R. M., Manjerovic, M. B., & Sacerdote-Velat, A. B. (2018) · Conservation Physiology · doi:10.1093/conphys/coy008 · Cited by 48
“…to stressors, the challenge is that capturing and restraining animals often induces a stress response and can increase GC production rapidly, in under 5 min for some birds and small mammals (Touma and Palme, 2005; Harper and Austad, 2000; Mostl and Palme, 2002; Millsburgh and Washburn, 2004).”
BackgroundBurgess, E. A., Hunt, K. E., Kraus, S. D., & Rolland, R. M. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2017.07.026 · Cited by 40
Nilsson, P. B., Hollmén, T. E., Atkinson, S., Mashburn, K. L., Tuomi, P. A., Esler, D., Mulcahy, D. M., & Rizzolo, D. J. (2008) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2008.01.002 · Cited by 35
“Fecal samples may be used to investigate baseline concentrations of GCM when it is difficult or impossible to obtain a blood sample within a few minutes of capture (Hiebert et al., 2000; Goymann et al., 2002.; Millspaugh and Washburn, 2003).”
BackgroundNarayan, E. (2019) · Scientific Reports · doi:10.1038/s41598-019-42448-8 · Cited by 36
Alibhai, S. K., Jewell, Z. C., & Evans, J. W. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172065 · Cited by 41
Wilkening, J. L., Ray, C., & Varner, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119327 · Cited by 56
Kalbitzer, U., & Heistermann, M. (2013) · Methods in Ecology and Evolution · doi:10.1111/2041-210x.12054 · Cited by 41
Herring, G., & Gawlik, D. (2007) · TheScientificWorldJournal · doi:10.1100/tsw.2007.242 · Cited by 36
Narayan, E. J., Parnell, T., Clark, G., Martin-Vegue, P., Mucci, A., & Hero, J. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.10.002 · Cited by 35
“…with the assessment of FCM measures arise when considering a range of other variables including normal seasonal and daily rhythms, body condition, sample storage and treatment techniques, assay selection, social arrangements, reproductive status, sample age and condition, and sample mass [28].”
Unravelling complex associations between physiological state and movement of African elephants
Jachowski, D., Montgomery, R., Slotow, R., & Millspaugh, J. (2013) · Functional Ecology · doi:10.1111/1365-2435.12118 · Cited by 35
Self-citationLilley, T. M., Laaksonen, T., Huitu, O., & Helle, S. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.11.015 · Cited by 36
“Because maternal levels of circulating testosterone likely vary according to the reproductive state of animals [7,34], the oestrous cycle phase of females was recorded according to vaginal cytology [20].”
Lobato, E., Moreno, J., Merino, S., Morales, J., Tomás, G., Martı́nez, J., Vásquez, R., Kuchar, A. C., Möstl, E., & Osorno, J. (2010) · Journal of Ornithology · doi:10.1007/s10336-009-0488-x · Cited by 35
“Steroid metabolites concentrations in excreta constitute an integrated parameter of steroid levels over a long period of time (Goymann 2005) and may provide an accurate measure of long-term glucocorticoid levels (see Millspaugh and Washburn 2004).”
Assessment of fecal steroid and thyroid hormone metabolites in eastern North Pacific gray whales
Lemos, L. S., Olsen, A. Y., Smith, A., Chandler, T. E., Larson, S., Hunt, K. E., & Torres, L. G. (2020) · Conservation Physiology · doi:10.1093/conphys/coaa110 · Cited by 38
“02 g can produce anomalously inflated results (Millspaugh and Washburn, 2004; Hayward et al., 2010; Ayres et al., 2012).”
BackgroundMethodGoldstein, E. J., Millspaugh, J., Washburn, B., Brundige, G., & Raedeke, K. (2005) · Journal of Wildlife Diseases · doi:10.7589/0090-3558-41.2.416 · Cited by 34
Self-citationPilorz, V., Steinlechner, S., & Oster, H. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.08.010 · Cited by 33
der Weyde, L. K. V., Martin, G. B., & Paris, M. C. J. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.12.022 · Cited by 31
Environmental and Intrinsic Correlates of Stress in Free-Ranging Wolves
Molnar, B., Fattebert, J., Palme, R., Ciucci, P., Betschart, B., Smith, D. W., & Diehl, P.-A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137378 · Cited by 48
“Cortisol is the main secreted glucocorticoid in numerous mammals [13], and fecal cortisol metabolites (FCM) are successfully used as an index of stress in several species [15], including the dog (Canis lupus familiaris) [22].”
BackgroundInfluentialThe effect of ACTH upon faecal glucocorticoid excretion in the koala
Davies, N., Gillett, A. K., McAlpine, C., Seabrook, L., BAXTER, G. S., Lunney, D., & Bradley, A. J. (2013) · Journal of Endocrinology · doi:10.1530/joe-13-0123 · Cited by 32
“…in their environment is of great importance to conservation biologists as stress can alter behaviour, reduce resistance to disease and adversely affect population performance (including impacting survival and reproduction; Munck et al. 1984, Wingfield & Farner 1993, Millspaugh & Washburn 2004).”
Ozella, L., Anfossi, L., Di Nardo, F., & Pessani, D. (2017) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.12.002 · Cited by 32
“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).”
Being stressed outside the park—conservation of African elephants (Loxodonta africana) in Namibia
Hunninck, L., Ringstad, I. H., Jackson, C. R., May, R. F., Fossøy, F., Uiseb, K., Killian, W., Palme, R., & Røskaft, E. (2017) · Conservation Physiology · doi:10.1093/conphys/cox067 · Cited by 36
“We hypothesized that elephant populations in the partially protected KR had increased levels of stress caused by anthropogenic disturbances including human–elephant impacts (crop raiding and physical injuries) compared to elephants inside ENP (Millspaugh and Washburn, 2004).”
BackgroundMadliger, C. L., & Love, O. P. (2016) · Oikos · doi:10.1111/oik.03354 · Cited by 30
“However, this supposition ignores that GC physiology is often context-dependent and can vary independently of environmental variation, a characteristic that is highly relevant to their interpretation (Millspaugh and Washburn 2004, Bonier et al. 2009, Dantzer et al. 2014, Madliger and Love 2014).”
BackgroundMethodological considerations for measuring glucocorticoid metabolites in feathers
Berk, S. A., McGettrick, J. R., Hansen, W. K., & Breuner, C. W. (2016) · Conservation Physiology · doi:10.1093/conphys/cow020 · Cited by 32
“The small sample artefact has been a consistent problem in the faecal CORT literature (Millspaugh and Washburn, 2004; Tempel and Guitierrez, 2004; Cyr and Romero, 2008).”
BackgroundAmrein, M., Heistermann, M., & Weingrill, T. (2014) · International Journal of Primatology · doi:10.1007/s10764-014-9765-5 · Cited by 35
“The measurement of fGCM is widely used as a non-invasive tool to investigate adrenocortical activity and thus physiological stress load (Heistermann et al. 2006; Lane 2006; Millspaugh and Washburn 2004; Rangel-Negrin et al. 2009).”
MethodTingvold, H. G., Fyumagwa, R., Bech, C., Baardsen, L. F., Rosenlund, H., & Røskaft, E. (2013) · African Journal of Ecology · doi:10.1111/aje.12069 · Cited by 30
Poessel, S. A., Biggins, D. E., Santymire, R. M., Livieri, T. M., Crooks, K. R., & Angeloni, L. M. (2011) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2011.04.018 · Cited by 37
“FGM analyses: (1) reflect an average concentration of circulating hormones over a certain time period before collection, due to the slower excretion rate of metabolized hormones into the feces, while blood-based analyses measure glucocorticoids at the time of collection, so that the impact of capture, handling and res…”
MethodKeady, M., Prado, N. A., Lim, H. C., Brown, J. L., Paris, S., & Muletz‐Wolz, C. R. (2021) · Animal Microbiome · doi:10.1186/s42523-021-00146-9 · Cited by 43
“FGMs are a measure of adrenal cortex activity and are frequently used to study stress in wildlife studies due to the non-invasive nature, though FGM should be interpreted cautiously [113, 114] due to the metabolic functions of glucocorticoids [45, 46] and non-stress related factors affecting FGM levels.”
BackgroundNugraha, R. T. P., Heistermann, M., Agil, M., Purwantara, B., Supriatna, I., Gholib, G., van Schaik, C. P., & Weingrill, T. (2016) · Primates · doi:10.1007/s10329-016-0583-6 · Cited by 35
“…of Syiah Kuala, Banda Aceh, Indonesia 5 Department of Anthropology, University of Zurich, Zurich, Switzerland captive and free-ranging animals (e.g. Millspaugh and Washburn 2004; Hodges et al. 2010; Hodges and Heistermann 2011; Sheriff et al. 2011; Weingrill et al. 2011; Ozella et al. 2015; Marty…”
BackgroundLunde, E. T., Bech, C., Fyumagwa, R., Jackson, C. R., & Røskaft, E. (2016) · African Journal of Ecology · doi:10.1111/aje.12302 · Cited by 25
Effects of population density on corticosterone levels of prairie voles in the field
Blondel, D. V., Wallace, G., Calderone, S., Gorinshteyn, M., Mary, C. M. S., & Phelps, S. M. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.09.002 · Cited by 35
“This is a common pattern across taxa when performing methanol-based fecal CORT extractions on samples less than 0.02g (Millspaugh and Washburn, 2004; Tempel and Gutierrez, 2004).”
BackgroundValidation of Fecal Glucocorticoid Metabolite Assays for South African Herbivores
Chinnadurai, S. K., Millspaugh, J. J., Matthews, W. S., Canter, K., Slotow, R., Washburn, B. E., & WOODS, R. J. (2009) · Journal of Wildlife Management · doi:10.2193/2008-430 · Cited by 30
“Compared with field observations, such as behavioral monitoring, collection of fecal material is straightforward, provided critical collection and storage protocols are followed (Millspaugh and Washburn 2004).”
BackgroundSelf-citationCrowley, S. M., Hodder, D. P., Johnson, C. J., & Yates, D. E. (2018) · Ecological Indicators · doi:10.1016/j.ecolind.2018.01.061 · Cited by 36
Vynne, C., Booth, R. K., & Wasser, S. K. (2014) · Journal of Mammalogy · doi:10.1644/12-mamm-a-247 · Cited by 32
Physiological stress in the Eurasian badger (Meles meles): effects of host, disease and environment.
George, S., Smith, T. E., Cana, P. S. S. M., Coleman, R., & Montgomery, W. (2014) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2014.02.017 · Cited by 30
“Enzyme immunoassays have been widely used to measure hormone excretion (Millspaugh and Washburn, 2004; Möstl and Palme, 2002; Palme et al., 2005).”
BackgroundMethodWoodruff, J. A., Lacey, E. A., Bentley, G. E., & Kriegsfeld, L. J. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.07.008 · Cited by 28
“Fecal samples provide a temporally more comprehensive picture of baseline GC concentrations than blood samples (Harper and Austad, 2000; Millspaugh and Washburn, 2004; Touma and Palme, 2005) and can be obtained non-invasively without altering GC levels through the act of sample collection.”
BackgroundLegagneux, P., Gauthier, G., Chastel, O., Picard, G., & Bêty, J. (2011) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2011.04.009 · Cited by 32
Woodruff, J. A., Lacey, E. A., & Bentley, G. E. (2010) · Journal of Experimental Zoology Part A Ecological Genetics and Physiology · doi:10.1002/jez.621 · Cited by 27
Soto-Gamboa, M. R., Gonzalez, S., Hayes, L. D., & Ebensperger, L. A. (2009) · Journal of Experimental Zoology Part A Ecological Genetics and Physiology · doi:10.1002/jez.546 · Cited by 29
“Although the best option is to collect fecal samples after defecation and freeze them immediately (Wasser et al., 2000; Millspaugh and Washburn, 2004), this may not be possible under field conditions.”
BackgroundKahn, P., Guyer, C., & Mendonça, M. (2007) · Copeia · doi:10.1643/0045-8511(2007)2007[614:hbsatc]2.0.co;2 · Cited by 30
“However, monitoring of fecal metabolites is confounded by a multitude of other factors (Millspaugh et al., 2001; Millspaugh and Washburn, 2004).”
BackgroundNarayan, E. J., & Vanderneut, T. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00018 · Cited by 31
Assay validation and interspecific comparison of salivary glucocorticoids in three amphibian species
Hammond, T. T., Au, Z. A., Hartman, A. C., & Richards‐Zawacki, C. L. (2018) · Conservation Physiology · doi:10.1093/conphys/coy055 · Cited by 33
“disturbance of vulnerable species (Millspaugh and Washburn, 2004; Wikelski and Cooke, 2006).”
BackgroundBarja, I., Escribano‐Ávila, G., Lara‐Romero, C., Virgós, E., Benito, J., & Rafart, E. (2012) · Animal Biology · doi:10.1163/157075612x642914 · Cited by 31
“As previous studies indicate that glucocorticoid metabolite levels vary due to bacterial activity and environmental conditions (Millspaugh and Washburn, 2004), we performed an experiment to test whether the time lapse between the collection and freezing of faecal samples affects cortisol metabolite…”
BackgroundMethodInfluentialMoagi, L. L., Bourne, A., Cunningham, S., Jansen, R., Ngcamphalala, C. A., Ganswindt, A., Ridley, A., & McKechnie, A. (2021) · bioRxiv · doi:10.1101/2021.02.17.431578 · Cited by 28
Snow roosting reduces temperature-associated stress in a wintering bird
Shipley, A. A., Sheriff, M. J., Pauli, J. N., & Zuckerberg, B. (2019) · Oecologia · doi:10.1007/s00442-019-04389-x · Cited by 35
Gholib, G., Heistermann, M., Agil, M., Supriatna, I., Purwantara, B., Nugraha, R. T. P., & Engelhardt, A. (2018) · Primates · doi:10.1007/s10329-018-0653-z · Cited by 33
“2003; Millspaugh and Washburn 2004).”
Pohlin, F., Brabender, K., Fluch, G., Stalder, G. L., Petit, T., & Walzer, C. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00664 · Cited by 32
“…has mainly focused on the quantification of glucocorticoid steroid hormones (i.e., cortisol and corticosterone), the primary mediators of the HPA axis (Möstl and Palme, 2002; Millspaugh and Washburn, 2004; Schwarzenberger, 2007; Busch and Hayward, 2009; Sheriff et al., 2011; Dantzer et al., 2014).”
BackgroundEnkephalin knockout male mice are resistant to chronic mild stress
Melo, I., Drews, E., Zimmer, A., & Bilkei‐Gorzo, A. (2014) · Genes, Brain and Behavior · doi:10.1111/gbb.12139 · Cited by 27
Fürtbauer, I., Solman, C., & Fry, A. (2019) · Domestic Animal Endocrinology · doi:10.1016/j.domaniend.2018.12.009 · Cited by 27
Batson, W. G., Gordon, I. J., Fletcher, D. B., PORTAS, T., & Manning, A. D. (2017) · Journal of Zoology · doi:10.1111/jzo.12494 · Cited by 35
Clercq, N. D., Bussche, J. V., Croubels, S., Delahaut, P., & Vanhaecke, L. (2014) · Journal of Chromatography A · doi:10.1016/j.chroma.2014.02.033 · Cited by 27
Santos, J. P. V., Acevedo, P., Carvalho, J., Queirós, J., Villamuelas, M., Fonseca, C., Gortázar, C., López-Olvera, J., & Vicente, J. (2018) · Ecological Indicators · doi:10.1016/j.ecolind.2018.02.047 · Cited by 26
Stability of Avian Fecal Corticosterone Metabolite Levels in Frozen Avian Feces
Herring, G., & Gawlik, D. (2009) · doi:10.2193/2008-398 · Cited by 26
Being “hangry”: food depletion and its cascading effects on social behaviour
Fattorini, N., Brunetti, C., Baruzzi, C., Macchi, E., Pagliarella, M. C., Pallari, N., Lovari, S., & Ferretti, F. (2018) · Biological Journal of the Linnean Society · doi:10.1093/biolinnean/bly119 · Cited by 23
Narayan, E. J. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.12.008 · Cited by 25
Casas, F., Benítez-López, A., Tarjuelo, R., Barja, I., Viñuela, J., García, J. T., Morales, M., & Mougeot, F. (2016) · SCIENCE NATURE · doi:10.1007/s00114-016-1416-6 · Cited by 25
“…metabolite levels in faeces can improve our ability to detect disturbance effects on wild animals without disturbing or jeopardizing their safety, which is particularly important when they are threatened species (Millspaugh and Washburn 2004; Walker et al. 2005; Madliger and Love 2013).”
BackgroundSpercoski, K., Morais, R. N., Morato, R., de Paula, R. D., Azevedo, F. C., Junior, J. A. M., Santos, J. P., Reghelin, A. L., Wildt, D., & Songsasen, N. (2012) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2012.08.002 · Cited by 25
Kummrow, M., Smith, D. A., Crawshaw, G. J., & Mastromonaco, G. F. (2010) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2010.04.022 · Cited by 29
Evaluation of adrenocortical function in Florida manatees (Trichechus manatus latirostris)
Tripp, K. M., Verstegen, J., Deutsch, C. J., Bonde, R. K., de Wit, M., Manire, C. A., Gaspard, J. C., & Harr, K. E. (2010) · Zoo Biology · doi:10.1002/zoo.20311 · Cited by 20
Burgess, E., Hunt, K., Kraus, S., & Rolland, R. (2016) · Conservation Physiology · doi:10.1093/conphys/cow024 · Cited by 24
“…concentrations include the following: whether field storage conditions adequately preserve the sample hormone after collection (see Woods, 1975; Millspaugh and Washburn, 2004; Ziegler and Wittwer, 2005); the efficiency of the technique used to extract hormones from the sample (see Lynch et…”
MethodInfluentialStress hormone metabolites predict overwinter survival in yellow-bellied marmots
Wey, T., Lin, L., Patton, M., & Blumstein, D. (2015) · Acta Ethologica · doi:10.1007/s10211-014-0204-6 · Cited by 24
“For example, both levels of circulating GCs in blood plasma, which are typically influencing within a few minutes of an acute stressor, and levels of GCmetabolites in feces, which reflect the processing and integration of GCs over a longer timescale, are now widely used measures of stress (Harper and Austad 2000; Mill…”
MethodGraham, C., Narayan, E. J., McCallum, H. I., & Hero, J. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.05.012 · Cited by 22
“Over the past decade, there has been considerable interest in measuring 58 stress hormone metabolites (cortisol in mammals and corticosterone in amphibians, reptiles 59 and birds) in urine and/or faeces as an index of the relatedness of both stress and reproductive 60 success in various wild animals [4-6].”
BackgroundCarzon, P., Clua, E., Dudzinski, K., & Delfour, F. (2023) · Biological Conservation · doi:10.1016/j.biocon.2023.109948 · Cited by 23
Stabach, J., Cunningham, S. A., Connette, G., Mota, J. L., Reed, D., Byron, M., Songer, M., Wacher, T., Mertes, K., Brown, J. L., et al. (2019) · bioRxiv · doi:10.1371/journal.pone.0221843 · Cited by 23
Eckardt, W., Stoinski, T. S., Rosenbaum, S., & Santymire, R. M. (2019) · Ecology and Evolution · doi:10.1002/ece3.5115 · Cited by 23
“We use noninvasive monitoring of FGM, which is widely recognized as an useful measure of stress (Ayres et al., 2012; Millspaugh & Washburn, 2004; Sapolsky, Romero, & Munck, 2000; Walker, 2005) and validated previously in this study population (Eckardt et al., 2016).”
MethodChanges in African Elephant (Loxodonta africana) faecal steroid concentrations post-defaecation
Webber, J. T., Henley, M. D., Pretorius, Y., Somers, M. J., & Ganswindt, A. (2018) · Bothalia · doi:10.4102/abc.v48i2.2312 · Cited by 29
“Faecal steroid analysis does, however, come with its challenges; for example hormone metabolites might not be evenly distributed throughout a faecal sample, necessitating thorough mixing of sample material after collection (Millspaugh & Washburn 2004; Wasser et al. 1996).”
BackgroundIglesias-Merchán, C., Horcajada-Sánchez, F., Dı́az-Balteiro, L., Escribano‐Ávila, G., Lara‐Romero, C., Virgós, E., Planillo, A., & Barja, I. (2018) · Environmental Monitoring and Assessment · doi:10.1007/s10661-018-6573-y · Cited by 24
“In this context, non-invasivemethodologies have been developed to index physiological stress levels for an array of different animals (Keay et al. 2006; Millspaugh and Washburn 2004).”
BackgroundStabach, J. A., Boone, R. B., Worden, J. S., & Florant, G. L. (2014) · Biological Conservation · doi:10.1016/j.biocon.2014.12.003 · Cited by 27
Rimbach, R., Link, A., Heistermann, M., Gómez‐Posada, C., Galvis, N. F., & Heymann, E. (2013) · Conservation Physiology · doi:10.1093/conphys/cot031 · Cited by 23
“11a No. 91-55, Bogotá, Colombia 3Departamento de Ciencias Biológicas, Universidad de Los Andes, Cra.”
BackgroundMonello, R., Millspaugh, J., Woods, R., & Gompper, M. (2010) · Journal of Zoology · doi:10.1111/j.1469-7998.2010.00717.x · Cited by 23
Self-citationKhonmee, J., Brown, J. L., Rojanasthien, S., Aunsusin, A., Thumasanukul, D., Kongphoemphun, A., Siriaroonrat, B., Tipkantha, W., Punyapornwithaya, V., & Thitaram, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091633 · Cited by 22
“The ease of fecal collection without animal disturbance and that data reflect pooled values over time makes this a particularly attractive approach for zoo-held species [22,23].”
BackgroundPrice, E. C., Coleman, R., Ahsmann, J., Glendewar, G., Hunt, J., Smith, T. E., & Wormell, D. (2019) · American Journal of Primatology · doi:10.1002/ajp.23033 · Cited by 25
“Fecal cortisol may give a better picture of baseline cortisol levels as it is less affected by daily acute events and as such represents the effects of underlying individual, social, and environmental factors affecting cortisol production (Heistermann, 2010; Millspaugh & Washburn, 2004).”
BackgroundChristofoletti, M. D., Pereira, R. J. G., & Duarte, J. M. B. (2009) · European Journal of Wildlife Research · doi:10.1007/s10344-009-0350-8 · Cited by 29
“They may be related to variations in formed metabolites, animal’s diet, different extraction methods, and immunoassays (Keay et al. 2006; Millspaugh and Washburn 2004; Möstl and Palme 2002; Palme 2005; Palme et al. 1996; Schwarzenberger et al. 1996; Touma and Palme 2005).”
BackgroundMethodCoping with style: individual differences in responses to environmental variation
Mazza, V., Dammhahn, M., Eccard, J. A., Palme, R., Zaccaroni, M., & Jacob, J. (2019) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-019-2760-2 · Cited by 23
“We completed the extraction only when the sample mass was sufficient to provide a 0.05 g aliquot (e.g. Millspaugh and Washburn 2004; Blondel et al. 2016).”
MethodInfluentialRazal, C., Bryant, J. L., & Miller, L. J. (2017) · Animal Behavior and Cognition · doi:10.12966/abc.03.05.2017 · Cited by 26
“These methods are valuable techniques and potentially more accurate by not having increased GC secretion caused by captureinduced stress (Millspaugh & Washburn, 2004; Millspaugh et al., 2001).”
MethodWilkening, J. L., Ray, C., & Varner, J. (2016) · Ecology and Evolution · doi:10.1002/ece3.1857 · Cited by 41
“Glucocorticoid metabolites (GCMs) can be detected in the feces of birds and mammals.”
BackgroundCikanek, S. J., Nockold, S., Brown, J. L., Carpenter, J. W., Estrada, A., Guerrel, J., Hope, K., Ibáñez, R., Putman, S., & Gratwicke, B. (2014) · PLoS ONE · doi:10.1371/journal.pone.0090218 · Cited by 21
Edwards, K. L., McArthur, H. M., Liddicoat, T., & Walker, S. L. (2014) · Conservation Physiology · doi:10.1093/conphys/cot037 · Cited by 24
“Faecal measures of hormone concentration are becoming widely used, because they are relatively easy to obtain and can be collected non-invasively, thus minimizing the impact of sampling on the animal (Millspaugh and Washburn, 2004).”
Background
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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