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Considerations of context and scale when using fecal glucocorticoids to indicate stress in large mammals: a study of wild American plains bison.

Conservation biologists, ecologists, and wildlife managers are concerned about the impacts of natural and anthropogenic disturbances on wild animals, especially in species with high conservation value (Frid and Dill, 2002; Russell et al., 2009). Such disturbances, which vary in scale and intensity, commonly include vehicle traffic, hunting, natural disasters, and habitat treatments. The impacts could be measured in terms of range shifts or changes in habitat use, but ultimately the key response variable is fitness (Gill et al., 2001; Acevedo-Whitehouse and Duffus, 2009). It is difficult, however, to directly measure fitness in wild populations. Instead, the stress response, which is assumed to be related to fitness, is increasingly being used to quantify the effects of disturbances on focal animal populations (Wingfield and Farner, 1976; Marra and Holberton, 1998; Romero and Wikelski, 2001; Cabezas et al., 2007; Jaatinen et al., 2013). The particular appeal of studying the stress response is that sampling can be noninvasive, thereby avoiding the problem of behavioral responses to researchers being confounded with those to the disturbance stimuli in question.

Field endocrinology was in use nearly 40 years ago, and glucocorticoids (GCs) have been used increasingly as indicators of generalized stress at the population level (Wingfield and Farner, 1976; Marra and Holberton, 1998; Romero and Wikelski, 2001; Cabezas et al., 2007; Jaatinen et al., 2013). These hormones, such as cortisol and corticosterone, are regulated by the hypothalamic-pituitary-adrenal axis and mobilize energy in an organism during stressful events (Wingfield and Romero, 2001). During acute stress, GCs are generally considered beneficial to the organism by enhancing physiological functions such as immunity and memory development (Sapolsky et al., 2000). However, organisms experiencing chronic stress often have depressed immune systems, decreased body condition, and reduced reproduction. This is because GCs mobilize energy away from these nonessential processes to support the central nervous system (Sapolsky et al., 2000; Dhabhar, 2009).

Because of the importance of GCs in regulating multiple physiological systems, researchers have developed minimally invasive procedures for testing GC levels (Walker et al., 2005; Kersey and Dehnhard, 2014). One of the least invasive procedures uses fecal samples, which reflect the composite GC deposition and excretion over a defined period of time (Tempel and Gutierrez, 2004; Goymann, 2005). That can be informative for certain study purposes, but interpreting a fecal GC level as a stress indicator can be challenging in the absence of additional knowledge about the individual, such as body condition, sex, diet, and age (von der Ohe and Servheen, 2002; Goymann, 2005). In addition, using GCs as indicators of stress can lead to conflicting results when the measured GC levels are positively, negatively, or not correlated with typical measures of fitness (Bonier et al., 2009a; Dickens and Romero, 2013). It seems that the interpretation of these measures is context-dependent and thus other metrics, such as immune function, must also be taken into account (Jaatinen et al., 2013; Schoech et al., 2013).

The field of stress physiology has been searching for correlates of the energetic and stress state of animal groups to better interpret up-scaled ecological patterns (Jessop et al., 2013). Research thus far has focused more on physiological than environmental covariates, such as habitat quality for example (Breuner et al., 2013; Schoech et al., 2013). In our study of a wild herd of American plains bison (Bison bison), we hoped to determine whether environmental covariates could explain variations in the fecal concentrations of corticosterone (CORT), thus elucidating spatiotemporal variations in the stress state of the herd. Our study population, in the Henry Mountains (HM) of southern Utah, was established in the early 1940s with 20 animals (15 females, 5 males) translocated from Yellowstone National Park (Popov and Low, 1950; Nelson, 1965) and now numbers ~325 adults (posthunt). These bison are unique in that they range freely on public land where they comingle with cattle and are legally hunted, but they are disease free and genetically pure (Ranglack et al., 2015a, 2015b), making them extremely valuable to bison conservation (Sanderson et al., 2008). The HM bison have, however, become a focus of contention due to their summer use of low-elevation habitats (van Vuren, 2001; Ranglack and du Toit, 2015 b) that are considered key winter range for cattle, leading to intense conflict with local ranchers, especially during dry years (Ranglack et al., 2015b; Ranglack and du Toit, 2015a).

This pattern of habitat use is counterintuitive. We would expect bison to prefer the high-elevation areas of the HM during the hot summer when lower ambient temperatures, shade from tree cover, proximity to water, and availability of green grass should be attractive habitat attributes. However, the mule deer (Odocoileus hemionus) population in the HM, which is renowned for its exceptional trophy quality, keeps to the high-elevation habitats in the summer, to which hunters and recreationists are consequently drawn to scout for upcoming hunts or photographic opportunities. The bison are also hunted and so are extremely wary of human presence. We thus hypothesize that bison spatial ecology is driven by stress avoidance behavior in response to human disturbance. To test our hypothesis, we analyzed site-specific fecal CORT concentrations for comparison with a suite of physiological and environmental covariates that, we assumed, could influence a stress response at the herd level.

MATERIALS AND METHODS--Study Area--The HM study area in south-central Utah [38[degrees]5'N, 100[degrees]50'W] includes arid, semi-arid, and alpine habitats. Bison and cattle are the only large grazers in the region. A small herd (~20 animals) of elk (Cervus canadensis) is present, although the Utah Division of Wildlife Resources actively manages against elk by issuing hunting permits. Mule deer are common on the HM, but their preference for forbs implies negligible levels of competition with the grazers (van Vuren and Bray, 1983). Black-tailed jackrabbits (Lepus californicus) and desert cottontail (Sylvilagus audubonii) are common in the low and mid elevations and have significant impacts on forage availability for bison and cattle (Ranglack et al., 2015b). Mountain lions (Puma concolor) and coyotes (Canis latrans) use the study area, but their populations are controlled by government and private entities. Detailed descriptions of the study area can be found in Nelson (1965) and van Vuren and Bray (1986).

Sample Collection--Satellite-download global positioning system telemetry collars and traditional very high frequency radio-collars were deployed on 63 female and 19 male bison in the HM area in January 2011. Effort was taken to ensure that the collars were distributed representatively among groups throughout the HM area. From May 2012 to April 2013, both types of telemetry--very high frequency and global positioning system--were used to locate bison without visibility bias between open vs. closed habitat types, with effort taken to balance observations among all habitat types to the extent possible. Observations were primarily collected during the summer (May-August), with opportunistic observations throughout the remainder of the seasonal cycle, depending on accessibility. Direct observation of bison proved difficult in the winter as the bison tended to use a large roadless area with extremely rough topography that made access prohibitively difficult.

Adult female body condition was scored between 1 and 5, with 1 being poor condition and 5 being excellent, following the visual condition scoring scale used for African buffalo (Syncerus caffer) (Prins, 1996). Body condition was then averaged to derive one score for the herd at that time and place. The habitat the bison were occupying was classified into one of 12 habitat types: alpine meadow, aspen woodland, barren ground, recently burned, chaining, coniferous woodland, grass-shrub mix, grassland, oakbrush, pmon-juniper woodland, riparian, and shrubland. In addition, the location of each observation was marked using global positioning system and, through the use of a geographical information system, elevation, slope, aspect, distance to roads, and distance to water were associated with each observation. Digital elevation models and locations of roads and water sources were obtained from the Utah Automated Geographic Reference Center, the Bureau of Land Management, and the Utah Division of Wildlife Resources, all at the 30 x 30-m scale. We recorded Euclidean distance (km) to roads and water sources for each pixel, together with aspect and slope from the digital elevation model in ArcGIS (Esri, Redlands, California). Aspect was then reclassified for analysis as a categorical variable with eight levels: N, NE, E, SE, S, SW, W, and NW. Human activity was also indexed through the use of several traffic monitors placed strategically around the HM area by the local Bureau of Land Management office. These data were summarized to derive the average number of crossings per monitor per day.

We collected fecal samples from fresh dung pats after each focal bison group had departed from the area in which it had been observed. When possible, we monitored individuals to allow for collection of known-sex samples, although this proved to be difficult. Approximately five fecal samples were collected from each group, depending on the size of the group, along a transect perpendicular to the movement of the bison group to avoid sampling the same individual twice. Each fecal sample was homogenized and divided into subsamples for analysis of total nitrogen (N) and carbon (C) content (g [kg.sup.-1] dry feces), endoparasite load by using a modified McMaster technique (Zajac and Conboy, 2006), and CORT steroid analysis. The fecal N, C, and CORT subsamples were frozen within 3 h of collection, whereas the endoparasite load subsample was refrigerated until analysis could be completed in the field, generally within 5 h of collection, to prevent degradation of helminth eggs. Fecal N (assayed by the Utah State University Analytical Laboratory) was used as an index of diet quality because it represents dietary crude protein for grazing ungulates (Leslie and Starkey, 1987). Because endoparasite load was only used as an adjunct to tracking bison condition, total egg counts were performed without noting endoparasite species.

We conducted all sampling in accordance with Utah State University Institutional Animal Care and Use Committee--approved protocol 1452 and the Utah Division of Wildlife Resources Certificate of Registrations for Banding, Collection, Depredation, and Salvage permit 6BANC8393.

Fecal CORT Extraction--We mixed phosphate buffer solution at room temperature in equal volume with methanol and added 0.5 ml of this solution to each scintillation vial with the 0.5 g of homogenized fecal sample. We vortexed each sample and placed it onto a shaker for approximately 16 h at 200 rpm. After shaking, we allowed the solution to settle for 1 h. From the top of the supernatant, we decanted 50 ll into 12 x 75-mm polypropylene tubes and centrifuged them for 1 h at 4,000 rpm. The centrifuged supernatant was decanted and frozen at -80[degrees]C until the radioimmunoassay was initiated. The solution and fecal material left behind in the scintillation tubes was dried overnight in a vented 40[degrees]C oven. The dried material was cooled to room temperature and weighed to determine the dry weight of the remaining fecal sample when calculating hormone concentrations (Shideler et al., 1994; Bauman and Hardin, 1998).

Radioimmunoassay--We determined corticosterone concentrations using radioimmunoassay (ImmuChem[TM] Double Anti-body RIA kit, MP Biomedicals, Orangeburg, New York), following the manufacturer's instructions, with the exception of halving the amounts of reagents used per sample. In brief, a standard curve was created with the phosphate-buffered saline--methanol solution and provided standards. We added samples to 10 x 75-mm glass tubes and diluted them 1:5 by using supplied steroid dilutant. We added [sup.125]I and anti-corticosterone antibody to each tube and incubated them for 2 h at room temperature. Then, a precipitant solution was added and the samples were vortexed and centrifuged for 15 min at 2,400 rpm. The tubes were decanted and blotted to remove as much liquid as possible. Each sample was read on a gamma counter for 1 min. Samples were run on a single assay and intra-assay variation was 9.5%. Validations were conducted to test for nonspecific binding, linearity, and interference. Serially diluted samples had average parallelism of 0.9969 and spiked samples had a recovery of 81.5%.

Statistical Analysis--We analyzed the relationship between fecal CORT concentrations and our various covariates in univariate models by using linear regression for continuous variables (elevation, slope, distance to road, distance to water, fecal N, fecal C, parasite load, body condition, date, and traffic) and analysis of variance for categorical variables (sex, season, aspect, and vegetation type), using R version 3.0.2. (R Core Team, Vienna, Austria), with an a level of 0.05. Fecal CORT concentrations were log transformed for analysis to meet assumptions of normality. Date was converted to a continuous variable to examine the effects of both deer and bison hunts, as well as the rut, on CORT levels. As such, date indicated the number of days since the beginning of either deer or bison hunts, or the midpoint of the rut. In this way, we would expect to see a spike in CORT, followed by a decline. Due to the relative scarcity of some habitat types and the difficulty in obtaining observations during the winter season, vegetation types were collapsed into three categories: open (alpine meadow, grass-shrub mix, grassland, riparian, shrubland), closed (aspen woodland, coniferous woodland, oakbrush, coniferous woodland), and disturbed (burned ~10 yr before this study and chaining). Season was classified as early (January-June) and late (July-December). This timing reflects an observed change in bison habitat use and behavior that occurs during the midsummer in preparation for the rutting season (July-August).

RESULTS--In total, 147 fecal samples were used in the analyses. No significant (P < 0.05) relationships were found between the logarithm of fecal corticosterone concentration and slope, distance to water, fecal N, fecal C, parasite load, date, vehicle traffic on the day of sample collection, vehicle traffic during the week before sample collection, and vehicle traffic during the month before sample collection, or the number of days since deer or bison hunting began or the midpoint of the rutting season. Significant (P < 0.05), but positive, relationships were detected for elevation, distance to road, and body condition, although the adjusted [R.sup.2] values were low (0.073, 0.028, and 0.078, respectively), indicating that the relationships had little explanatory power and were likely significant only because of the large sample sizes used in the analysis (Figs. 1 and 2). The analysis of variance found no significant differences (P < 0.05) in log corticosterone concentration across sex, season, aspect, or vegetation type (Fig. 3).

DISCUSSION--Our findings show that for most of the covariates we measured, there was no relationship with fecal CORT concentration. Those covariates that did show significant relationships (elevation, distance to road, body condition) provided little explanatory power and had positive slopes, which is paradoxical to our predictions. If fecal CORT concentration is an index of overall stress, as is generally assumed, then higher values should indicate higher stress. Yet the weak positive relationship with distance to road contradicts the expectation that bison are wary of human presence and should thus be less stressed in areas further from roads. However, it is possible that animals near roads get stressed by traffic and move rapidly away in response, then defecate in locations remote from roads and thereby produce fecal samples with unexpectedly high CORT concentrations for those locations. Alternatively, perhaps the configuration of the road network prevented an adequate high-low gradient of disturbance to detect a road effect on fecal CORT. That is, however, unlikely because the HM is classified as one of the most "roadless" Bureau of Land Management areas in the western USA (Dickson et al.,2014).

Because GC use as indicators of stress at the population level has become more common, it has also become evident that the functional complexity of these hormones makes it difficult to generalize that animals in stressful environments will reliably display elevated concentrations of GCs (Dickens and Romero, 2013). This is likely because the production of GCs is highly context specific (Sapolsky et al., 2000).

Although we extensively measured environmental covariates for each site- and time-specific measure of fecal CORT concentration, we were unable to associate individual animals with most of the samples. Sex, age, body condition, and reproductive status each influence CORT production (von der Ohe and Servheen, 2002). A significant spike in fecal cortisol in bison bulls during (compared to before) and after the rut has been documented (Mooring et al., 2006), but with marked individuals in a focal-animal sampling scheme. Because our samples were nonindividualized and mainly of unknown sex, all the fecal CORT concentrations could indicate was a general herd-level stress response, and the sampled individuals may or may not have been impacted by the stressor. In addition, the body condition score was consistently high at the herd level, but there were individual variations that complicate the application of a herd-level body condition score to an individual fecal CORT concentration.

Furthermore, individuals experiencing chronic stress might exhibit relatively low CORT levels due to sensitization, adaptation, or downregulation of the hypothalamicpituitary-adrenal axis to the stressor (von der Ohe and Servheen, 2002; Rich and Romero, 2005). It might be that differences in CORT baseline level between groups, populations, or both are less significant than differences in the magnitude of response to an acute stressor (Romero et al., 2009; Neuman-Lee et al., 2015). For example, Galapagos marine iguanas (Amblyrhynchus cristatus) from areas of high tourist visitation had baseline levels of corticosterone similar to those from nontourist areas, but after a 30-min stressor the tourist-exposed iguanas had much higher levels than the others, and then only during nonbreeding seasons (French et al., 2010).

Finally, we measured total CORT in fecal samples, but other factors, such as corticosteroid binding globulins, can play an important role in GC metabolism and excretion (Breuner et al., 2013). Nevertheless, the measurement of total CORT has been defended as an adequate index of stress when other metrics, such as immune function, are also taken into account (Schoech et al., 2013). We measured endoparasite loads from fecal egg counts assuming that chronic stress may suppress immune function and thereby allow an increase in parasite load (Dhabhar and McEwen, 1997; Dhabhar, 2009), but we found no relationship between fecal CORT concentration and parasite load.

Our study indicates the potential challenges in measuring fecal CORT in situ with large animals in wild populations. Although fecal CORT is increasingly used as an indicator of the health and energetic status of populations, the context- and scale-dependent nature of fecal CORT can confound applications at the population level and landscape scale (Breuner et al., 2008; Bonier et al., 2009a, 2009b; Dickens and Romero, 2013). Even with an extensive suite of environmental covariates we failed to find any explanatory power in herd-level fecal CORT as a determinant of habitat selection by bison. We conclude that, in large and highly mobile species such as bison, there is a scale mismatch between the physiological stress response of an animal and the spatiotemporal distribution of fresh feces left on the landscape. As researchers continue to measure fecal CORT concentration as an indicator of stress in wild animals, we urge that all conclusions be narrowly drawn and physiological correlates be taken into account at the individual level.

Field and logistical assistance was provided by E. Stevenson, D. Cook, S. Fivecoat, K. Hersey, D. Koons, W. Paskett, and J. Thurston. We also thank C. E. Andrews for help with the Spanish translation of the abstract. Additional thanks to two anonymous reviewers who provided comments that improved the manuscript.

Submitted 27 July 2016. Accepted 22 February 2017.

Associate Editor was Ray Willis.


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Department of Wildland Resources and Ecology Center, Utah State University, Logan, UT 84322 (DHR)

Department of Biology, Utah State University, Logan, UT 84322 (LAN, SSF)

Department of Wildland Resources, Utah State University, Logan, UT 84322 (JTT)

Present address of DHR: Department of Biology, University of Nebraska at Kearney, Kearney, NE 68849

* Correspondent:

Caption: FIG. 1--Relationship between the logarithm of fecal corticosterone concentration (CORT) and various environmental and physiological covariates for a wild American bison population in the Henry Mountains, Utah, USA. Where present, lines indicate significant (P < 0.05) relationships with the shaded area indicating the associated 95% confidence interval. All covariates are measured at the individual level, except for body condition, which was measured at the group level.

Caption: FIG. 2--Relationship between the logarithm of fecal corticosterone concentration (CORT) in wild American bison population in the Henry Mountains, Utah, USA, and date. The light shaded areas indicate periods of deer hunting, and the dark shaded areas indicate periods of bison hunting. The peak of the bison rutting period corresponds roughly with the beginning of the first deer hunting season.

Caption: FIG. 3--Relationship between the logarithm of fecal corticosterone concentration (CORT) and various categorical covariates for a wild American bison population in the Henry Mountains, Utah, USA. Box plot shows median, quartiles, and 1.5 x interquartile range. Points show outliers beyond 1.5x interquartile range.
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Author:Ranglack, Dustin H.; Neuman-Lee, Lorin A.; French, Susannah S.; du Toit, Johan T.
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1USA
Date:Mar 1, 2017
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