Skip to main content
NCBI home page
Conservation Physiology logoLink to Conservation Physiology
. 2024 Apr 13;12(1):coae012. doi: 10.1093/conphys/coae012

Biological validation of faecal corticosterone metabolites as a non-invasive stress assessment in translocated California valley quail (Callipepla californica)

Sarah A Currier 1, Jeffrey G Whitt 2, Kelly S Reyna 3,✉
Editor: Steven Cooke
PMCID: PMC11015821  PMID: 38616893

Abstract

US quail species are vulnerable to population declines as a result of climate change, habitat loss and habitat fragmentation, all of which can result in physiological stress. Additionally, population restoration techniques (PRTs), like translocations, also induce stress. Traditional assessments of avian stress hormone levels include capturing and handling birds to extract blood, methods that are inherently stressful and can compound stress analyses. However, the stress hormone corticosterone (CORT) is metabolized from the blood and excreted in faeces as faecal corticosterone metabolites (FCMs). FCMs have been used as a non-invasive measurement of stress hormone levels in a variety of species, but must be validated for each species. The objective of this study was to biologically validate the use of FCMs as a non-invasive measurement of CORT levels in California valley quail (Callipepla californica). Reference and treatment quail were acclimated for 3 weeks in an outdoor aviary. Subsequently, treatment quail were subjected to a simulated 48-h translocation, a common and stress hormone-inducing PRT. Faecal samples were collected every 4 h and processed using an enzyme immunoassay. Mean FCM concentrations of treatment quail (41.50 ± 16.13 ng/g) were higher than reference FCM concentrations (24.07 ± 10.4 ng/g). These results biologically validate the use of FCMs as a non-invasive method to assess CORT levels in California valley quail, demonstrate diurnal variation in quail CORT levels, and confirm that quail translocations are a stress-inducing PRT. Ultimately, this research validates a new non-invasive tool for stress response measurement to advance quail research, management and conservation.

Keywords: biological validation, California valley quail, conservation, corticosterone, faecal corticosterone metabolites, physiology, population restoration, stress hormones, translocation

This study biologically validates the use of faecal corticosterone metabolites as a non-invasive method for detecting stress in quail, demonstrates diurnal variation in quail stress levels, confirms that translocations elevate stress, which likely impacts success, and establishes a new non-invasive tool for stress measurement in quail research, management and conservation.

Introduction

Stress assessments are often overlooked in US quail population declines and population restoration. US quail populations are vulnerable to decline as a result of unpredictable stressors like extreme weather, climate change (Guthery et al., 2000; Reyna and Burggren, 2017; Tanner et al., 2017; Reyna, 2019; Wilsey et al., 2019; Whitt and Reyna, 2022), habitat loss and habitat fragmentation (Brennan and Covington, 1994; Hernández et al., 2013; Pope and Heekin, 2017), all of which induce physiological stress responses. For example, elevated stress hormone levels have been observed in birds as a result of anthropogenic disturbances (Thiel et al., 2011; Jankowski et al., 2014; Arlettaz et al., 2015) and extreme climatic events (Wingfield et al., 2017), which are expected to increase in frequency and severity due to global climate change (Seneviratne et al., 2012; Masson-Delmotte et al., 2021). Climate change can also exacerbate the effects of other stressors (Felton et al., 2009; Şekercioğlu et al., 2012).

Quail respond to stressors using two pathways: (1) a rapid, short-term response, mediated by the autonomic nervous system, which involves a rapid release of catecholamine from the adrenal medulla, and (2) a slower, long-term response, mediated by the hypothalamic–pituitary–adrenal (HPA) axis, which involves the release of corticosterone (CORT, 17-deoxycortisol) from the adrenal cortex (Creel, 2001; Suorsa et al., 2003; Tempel and Gutiérrez, 2004; Cockrem, 2007, 2013; Sheriff et al., 2011; Wingfield et al., 2017; Palme, 2019; Romero and Gormally, 2019; van Vliet et al., 2020). As a stress response, elevated CORT levels act as a catalyst that transitions quail into survival mode whilst suppressing nonessential functions. However, long-term elevated CORT levels disrupt normal bodily functions and can lead to disease and death (Blas and Fairhurst, 2022). Accordingly, CORT’s role in the stress response, and the detectability of its metabolites using non-invasive methods, make it a common proxy for assessing the magnitude of an animal’s stress response (Sheriff et al., 2010; Ellis et al., 2012).

Prolonged or repeated exposure to stressors can directly influence bird populations by altering foraging, predator avoidance, fledging and reproduction, (Cyr and Romero, 2007; Crespi et al., 2013; Martin et al., 2017; Wingfield et al., 2017). Stressor persistence can induce a type 1 allostatic overload, where energy demand exceeds energy availability (Blas and Fairhurst, 2022), and birds decrease or eliminate behaviours (e.g. reproduction) not immediately necessary for survival (McEwen and Wingfield, 2003). Reproduction may be interrupted through several different, but complimentary pathways, including increasing production of gonadotropin-inhibitory hormone, reducing production of gonadotropin-releasing hormone (GnRH), and decreasing sensitivity of pituitary gonadotrope cells to GnRH and of ovaries to luteinizing hormone (Sapolsky et al., 2000; Wingfield and Sapolsky, 2003; Dickens and Bentley, 2014; Son et al., 2014). For example, capturing and holding wild European starlings (Sturnus vulgaris) blocked a time-sensitive seasonal increase in HPA axis activity, preventing the transition from early gonadal development to an active breeding state, which inhibited breeding (Dickens and Bentley, 2014). The resultant reduction in reproduction in birds contributes to population declines.

Chronic stress can also disrupt acute stress responses, including the fight or flight response, due to a decrease in the sensitivity of the HPA axis (Rich and Romero, 2005; Romero and Butler, 2007; Dickens et al., 2009). For example, European starlings caught in the wild and placed into captivity lost the ability to produce a fight or flight response when exposed to a loud noise as a stressor (Dickens and Romero, 2009). In addition, when the fight or flight response was chronically stimulated, it negatively impacted cardiovascular health, leading to hypertension due to surplus catecholamine exposure (Rupp, 1999). Population restoration techniques (PRTs), like translocations, are also stressors that can increase CORT levels. US quail species are economically important gamebirds (Johnson et al., 2012; Wszola et al., 2020) and part of a $3.7 billion per year upland gamebird hunting industry (Sportsmen’s Alliance, 2021). For >150 years, translocations have been used in attempts to bolster populations (Hernández et al., 2013; Gomez and Reyna, 2017; Whitt et al., 2017). Quail translocations are rarely successful (Perez et al., 2002; Scott et al., 2013; Whitt et al., 2017), especially when used for reintroduction (Martin et al., 2017). Despite translocations rarely having long-term success, there is increasing interest in translocation of wild quail (Stephenson et al., 2011; Martin et al., 2017; Sisson et al., 2017). Numerous hypotheses have been proposed for the low success rate (Sokos et al., 2008; Martin et al., 2017), but little is known about how stress influences translocation success.

Translocation consists of capturing, handling, holding, transporting and releasing quail to a novel site, each of which can result in acute and chronic stress, independent of other processes (Buchanan, 2000; Fazio and Ferlazzo, 2003; Jones et al., 2005; Teixeira et al., 2007; Dickens et al., 2009, 2010; Wingfield and Romero, 2011; Batson et al., 2017; Martin et al., 2017). For example, short translocations may induce an acute stress response; however, the duration of a quail translocation is typically 1–3 days, which increases the occurrence of a chronic stress response as indicated by chronically elevated CORT levels (Dickens et al., 2010). Both chronic and acute stress responses can inhibit survival of translocated animals through increased energy requirements, capture myopathy, dispersal distance and weight loss (Armstrong and Seddon, 2008; Dickens et al., 2010; Breed et al., 2019), which lead to a failure of the translocation by increasing susceptibility to disease and death (Dickens et al., 2010; Martin et al., 2017).

Weight loss has been observed when translocating wild birds to novel environments (Rich and Romero, 2005; Dickens et al., 2009; Fischer et al., 2018), and is a response to chronic stress. For example, European starlings lost 5–15% of their body weight after being exposed to a 14-day regime of multiple stressors during a translocation (Awerman and Romero, 2010). California valley quail (C. californica) exhibited a mean weight loss of 14.3% when translocated from Idaho to Texas (Reyna et al., 2020). This is important because body mass can influence survival and the overall success of translocations. For example, Cirl buntings (Emberiza cirlus) with a higher body weight at capture were more likely to survive in their new habitat than those with lower body weights (Fountain et al., 2017). Reducing stressors during translocation could reduce weight loss and increase post-release survival (Warwick et al., 2006).

The traditional method of measuring stress in birds requires capturing, handling and extracting blood samples, inherently stress-inducing actions (Arnold et al., 2008), followed by measuring blood CORT levels. It is assumed that if this process occurs within 3 min of initial handling, CORT levels will be indicative of the physiological condition of the bird prior and will not represent the elevated stress incurred during the procedure (Littin and Cockrem, 2001; Cockrem and Silverin, 2002). However, CORT levels quickly rise during handling and peak within 15–30 min. In addition, handling associated with blood extractions adds to the cumulative stress experienced by the bird, and nearby birds, independent of the extraction (Dickens et al., 2010; O’Dell et al., 2014; Wein et al., 2017).

Steroid hormones, like CORT, can also be measured from urine, faeces, hair and feather samples (Bortolotti et al., 2008; Sheriff et al., 2011). One effective, non-invasive and increasingly popular method to evaluate a stress response is by measuring faecal corticosterone metabolites (FCMs; Romero and Remage-Healey, 2000; Tempel and Gutiérrez, 2004; Möstl et al., 2005; Dickens et al., 2009; Sheriff et al., 2010). Measuring FCMs as an assessment of CORT levels has been successful in a wide range of avian studies (Washburn et al., 2003; Fletcher et al., 2018; Sokół and Koziatek-Sadłowska, 2020). Excretion of FCMs varies between species, as does the suitability of different immunoassays to accurately detect CORT; therefore methods must be validated for each species (Palme et al., 1996; Wasser et al., 2000; Palme, 2019). Physiological validation of measuring FCM concentrations requires injecting a known quantity of CORT into an animal (Touma and Palme, 2005), an invasive and stressful procedure (Palme, 2019; Mohlman et al., 2020). Biological validation of measuring FCM concentrations is a non-invasive procedure where faeces is collected before and after an event that increases HPA activity for an extended time, resulting in increased blood CORT levels (Touma and Palme, 2005; Palme, 2019).

The goal of this study was to biologically validate the use of FCMs as a non-invasive assessment of CORT levels in California valley quail using a simulated translocation as the stressor. This is the first biological validation of FCMs as a tool to detect elevated CORT levels in a new world quail species. Mohlman et al. (2020) performed a physiological validation of FCMs with northern bobwhite (Colinus virginianus), another new world quail, but were unsuccessful at a biological validation due to an ineffective biological stressor.

Materials and Methods

Flight-ready captive-reared valley quail (n = 63 females, n = 57 males), 16–24 weeks in age, were acquired from a breeder (ZKD Game Birds, West Point, TX, USA) in October, 2020. Thirteen valley quail (n = 5 females, n = 7 males) were selected at random to use for biological validation, with the remainder used for diurnal FCM analysis. Quail were housed and acclimated in groups in an outdoor aviary (Quail Hotel, Fannin Fabrication, Bonham, TX, USA), where they were provided with natural perches and dust baths for 3 weeks (Hawkins et al., 2001). Mean temperature during this period was 16.4°C. Birds were provided with gamebird feed (Gamebird Starter and Grower, M-G Inc., Weimar, TX, USA) and water ad libitum. This mimicked the time and conditions in which quail were held prior to the first shipment of trapped birds during a 2019 translocation of valley quail (Reyna et al., 2020). Acclimation was assumed when birds exhibited typical behaviour (e.g. eating, drinking, roosting, grooming; Reyna and Newman, 2018).

To biologically validate FCMs in valley quail, reference (low stress) faecal samples were obtained from acclimated valley quail. The floor of the aviary was lined with a plastic sheet. The birds were observed from ~50 m away with binoculars to record the sex of the bird, and to ensure collected faecal samples were fresh (<1 h old) and uncontaminated. Once collected, individual faecal samples were placed into a plastic storage bag (Ziploc freezer quart, S. C. Johnson & Son, Inc., Racine, WI) and labelled with the date, time and sex of the bird. Because individual birds could not be matched to collected faecal samples, reference sample data were pooled following FCM analysis. Ambient temperature, relative humidity and presence of direct sunlight were recorded on the plastic storage bag, since these factors can degrade hormone detection probability (Shipley et al., 2019). Immediately after collection and labelling, samples were stored in a freezer at −20°C until FCM analysis (Wasser et al., 1988; Messmann et al., 1999; Khan et al., 2002).

For biological validation, quail were transported to the animal care facility at Texas A&M University-Commerce to undergo a simulated 48-h translocation, a stressful event (Martin et al., 2017). Each quail was given a unique leg band and had their age, sex, and weight recorded. Quail were held individually in research-approved breeding pens located in a temperature- (20 ± 2°C), humidity- (45 ± 15%) and light-controlled room with a 12 L:12 D photoperiod. To ensure accuracy and reduce contamination, faecal samples were collected from the underlying waste pan trays 4–5 times daily (Millspaugh and Washburn, 2004; Mohlman et al., 2020). The frequency of faeces collection ensured a representative sample, since FCMs may fluctuate diurnally (Breuner et al., 1999). Individual faecal samples were placed in a plastic storage bag and labelled with the bird ID number, sex, time, and date of collection. Steroid hormone concentrations can be affected by storage duration (Millspaugh and Washburn, 2004) and bacteria (Lexen et al., 2008). Therefore, treatment faecal samples were immediately stored in a freezer (−20°C) until FCM analysis (Wasser et al., 1988; Messmann et al., 1999).

FCM concentrations of reference and treatment quail faecal samples were measured using an Enzyme Immunoassay (EIA) Kit (K-014H, Arbor Assays, Ann Arbor, MI, USA). The kit was validated for use on CORT extracted from dry faecal extracts on a multi-species design (DeVries and Jawor, 2013; Fletcher et al., 2018), and included detailed instructions for extracting CORT from faecal samples and analysing FCM concentrations. To determine the assays suitability for valley quail, 10 faecal extracts were pooled from the valley quail simulated translocation, and a serial dilution (n = 6 dilutions) was performed. FCM concentrations from the pooled faecal extracts were parallel to the slope of the standard curve, verifying suitability for valley quail. The sensitivity of the EIA was determined to be 18.19 pg/ml. Optical density was calculated using a Synergy LX Multi-mode microplate reader (Bio Tek Instruments, USA), and entered into MyAssay web (https://www.myassay.com), to calculate FCM concentration in picograms per millilitre. FCM concentrations reported in picograms per millilitre were converted to nanogramme/gramme for comparison to other studies.

All animals were handled in accordance with procedures outlined in the Guide for the Care and Use of Laboratory Animals (National Research Council, 2010), and Texas A&M University-Commerce Animal Use Protocol P20–013.

Statistical analysis

Because birds could not reliably be distinguished without technicians approaching close enough to elicit visible agitation and warning calls from the reference birds, we pooled samples for statistical comparison. All statistical analyses were conducted in R (version 4.0.2, R Foundation, Austria). Shapiro–Wilk’s statistical test was used to check for normality (Zar, 1996). Welch’s 2-sample t-test was used to calculate the P-value, mean and 95% confidence interval between 2 variables with normal distributions. Mann–Whitney U-test was used to compare 2 variables with non-normal distributions. Kruskal–Wallis test was used to compare multiple variables with non-normal distributions, followed by Dunn’s test with Bonferroni correction for pairwise comparisons. Correlations were tested using Pearson’s product–moment correlation with Bonferroni correction (Zar, 1996). All weight data are presented as mean ± standard deviation (SD). Results were significant at alpha < 0.05.

Results

Mean ± SD FCM concentrations (n = 13 quail; 70 faecal samples) of valley quail during the simulated translocation were 41.50 ± 16.13 ng/g, and higher than reference FCM concentrations (24.07 ± 10.4 ng/g; n = 13 quail; 27 faecal samples; Mann–Whitney U, Z = 4.20, P < 0.001; Fig. 1). Mean 48-h weight loss was 17.8 ± 6.3 g, or 12 ± 4.4% of initial body mass.

Figure 1.

Figure 1

Open in a new tab

Biological validation of using FCMs in translocated California valley quail. FCM concentrations (mean ± SD) were extracted from faeces collected from acclimated quail (n = 13 birds, 27 samples) prior to (Reference) and during a 48-h simulated translocation (treatment, 70 samples). FCM concentrations from treatment birds were higher than reference FCM concentrations (Mann–Whitney U, Z = 4.20, P < 0.001). Asterisk indicates statistical difference.

Valley quail with higher initial body mass prior to the simulated translocation experienced lower mean FCM concentrations (r2 = 0.14, P < 0.001), and lower percentage of initial mass lost (r2 = 0.13, P < 0.001) during the simulated translocation. FCM concentrations positively correlated with percent of initial body mass loss (r2 = 0.27, P < 0.001). No difference in FCM concentrations (Mann–Whitney U, Z = 0.15, P = 0.44), total mass lost (Welch’s t-test, P = 0.58) or percentage of initial mass lost (Welch’s t-test, P = 0.29) was observed based on sex.

Valley quail FCMs varied diurnally during the simulated translocation (Fig. 2), with higher concentrations from 10:00 to 18:00 and lower concentrations from 20:00 to 06:00 (Kruskal–Wallis, H = 62.3, P < 0.001). Mean FCM concentrations were not different between the first 24 h and last 24 h (Mann–Whitney U, Z = 1.86, P = 0.32).

Figure 2.

Figure 2

Open in a new tab

Diurnal variation in FCM concentrations from California valley quail during a simulated 48-h translocation. Treatment FCM concentrations correlated with photoperiod (12 L:12 D) and quail circadian rhythm. Letters indicate statistical groupings. Faecal sample numbers ranged from 9 to 37 per hour due to faecal dropping frequency.

Discussion

This study was the first biological validation of FCMs as a non-invasive assessment of a stress response for a new world quail species. When exposed to a simulated translocation, valley quail experienced a 72.4% increase in FCMs compared to reference concentrations, indicating that this protocol successfully detected an increase in FCMs during a stressful event. These results are comparable to the 73% increase in FCMs recorded in northern bobwhites, another new world quail, during a physiological validation (Mohlman et al., 2020). However, the increase in FCM levels recorded for both of these new world quail is lower than FCM levels recorded in other avian species. This is not surprising because excretions of metabolites can vary between species (Palme et al., 1996; Wasser et al., 2000; Palme, 2019). For example, experimentally stressed European starlings showed a ~100% increase in FCMs (Cyr and Romero, 2008). Following capture and holding for a veterinary examination, African penguins (Spheniscus demersus) showed a 155–349% increase in FCMs. Wild Dickcissels (Spiza americana) experienced a 1700% increase in FCM concentrations within 24 h of having leg harness transmitters attached (Suedkamp Wells et al., 2003). Valley quail and northern bobwhite quail are both new world quail, and their similar stress response during validation, and variation from other taxa, was expected. This emphasizes the need to validate FCM for individual species.

The correlation of weight loss with FCM levels further supports the association of chronic stress with weight loss in birds (Cyr and Romero, 2007; Dickens et al., 2009; Awerman and Romero, 2010). Quail in our study lost 11.6% of body weight during the 48-h simulated translocation, results consistent with weight loss in translocated starlings (5–15%) and wild valley quail (14.3%) in an actual translocation of similar duration (Reyna et al., 2020), indicating that translocation weight loss may be a result of a chronic stress response to handling and captivity. Similar to our study, Reyna et al. (2020) reported that heavier valley quail lost less weight than lighter valley quail during a translocation. Heavier birds may be healthier overall, and future studies may benefit from considering a minimum weight for translocation.

By collecting faecal samples 4–5 times daily during the simulated translocation, we were able to capture diurnal variation in FCM concentrations. Although not previously observed in new world quail (Mohlman et al., 2020), diurnal variation in CORT metabolites has been recorded in a variety of species (Florant and Weitzman, 1980; de Jong et al., 2001; Touma et al., 2004; Bosson et al., 2009; Sheriff et al., 2009), generally corresponding to the circadian rhythm of the animal. The diurnal variation in valley quail FCM concentrations followed a pattern similar to the variation in plasma CORT observed in broiler chickens (de Jong et al., 2001), with lower concentrations at night and elevated concentrations during the day. This trend was expected since valley quail are active in the day and inactive during the night (Leopold, 1977).

This study verifies that translocations are stressful events for quail that result in significant weight loss, results that suggest stress influences translocation success. Chronic stress is associated with increased mortality in starlings (Cyr and Romero, 2007; Dickens et al., 2010), and animal weight at release is a predictor of survival in cirl buntings (Fountain et al., 2017). Further, increased CORT levels can inhibit reproduction, a primary indicator of translocation success (Griffith et al., 1989; Dickens et al., 2010). Future studies could benefit by focusing efforts on stress mitigation to increase long-term translocation success.

The use of FCM as a non-invasive measurement in new world quail could be extended beyond translocations to benefit quail conservation. There is considerable environmental and economic interest in conserving and restoring populations of quail and other gamebird species. Increased plasma CORT can be indicative of environmental disturbances and habitat-related metabolic challenges (Homyack, 2010; Shipley et al., 2022). For example, FCMs have been used as an indicator of declining habitat quality in greater sage-grouse (Centrocercus urophasianus; Rabon et al., 2021). FCMs have also been used to detect elevated CORT levels associated with extreme weather events, noise related to fossil fuel extraction (Cinto Mejia et al., 2019) and other anthropogenic disturbances (Thiel et al., 2008, 2011; Blickley et al., 2012; Arlettaz et al., 2015; Formenti et al., 2015). Through the use of innovative field collection methods (Shipley et al., 2019), FCMs may be used to assess chronic stress levels in wild quail populations, evaluate responses to multiple stressors (e.g. extreme drought) and map stress levels across a landscape to identify focus areas for conservation (Rabon et al., 2021). Ultimately, the use of FCMs could alert quail biologists to the presence of environmental stressors before population demographics are impacted (Ellis et al., 2012). Clearly, FCMs have enormous potential as a non-invasive indicator of stress levels in quail and as a tool for improving quail research, restoration, management and conservation.

Acknowledgements

We thank C. Vandenberg for assisting with bird logistics, J. Delgado-Acevedo for project guidance and Arbor Assays for technical support.

Contributor Information

Sarah A Currier, The Quail Research Laboratory, Ted and Donna Lyon Center for Gamebird Research, Texas A&M University-Commerce, Commerce, TX, 75429, USA.

Jeffrey G Whitt, The Quail Research Laboratory, Ted and Donna Lyon Center for Gamebird Research, Texas A&M University-Commerce, Commerce, TX, 75429, USA.

Kelly S Reyna, The Quail Research Laboratory, Ted and Donna Lyon Center for Gamebird Research, Texas A&M University-Commerce, Commerce, TX, 75429, USA.

Author Contributions

All authors contributed equally to the experimental design. S.C. maintained the animals and completed all laboratory work. S.C. and J.W. performed the statistical analyses. All authors contributed equally to writing and revising this manuscript.

Conflicts of Interest

The authors have no conflicts of interest to declare.

Funding

This work was supported by the Texas A&M University System; Texas A&M AgriLife Extension; Texas A&M University-Commerce; and the Ted and Donna Lyon Center for Gamebird Research.

Data Availability

The data underlying this article will be shared on reasonable requests to the corresponding author.

REFERENCES

  1. Arlettaz R, Nusslé S, Baltic M, Vogel P, Palme R, Jenni-Eiermann S, Patthey P, Genoud M (2015) Disturbance of wildlife by outdoor winter recreation: allostatic stress response and altered activity–energy budgets. Ecol Appl 25: 1197–1212. 10.1890/14-1141.1. [DOI] [PubMed] [Google Scholar]
  2. Armstrong DP, Seddon PJ (2008) Directions in reintroduction biology. Trends Ecol Evol 23: 20–25. 10.1016/j.tree.2007.10.003. [DOI] [PubMed] [Google Scholar]
  3. Arnold JM, Oswald SA, Voigt CC, Palme R, Braasch A, Bauch C, Becker PH (2008) Taking the stress out of blood collection: comparison of field blood-sampling techniques for analysis of baseline corticosterone. J Avian Biol 39: 588–592. 10.1111/j.0908-8857.2008.04265.x. [DOI] [Google Scholar]
  4. Awerman JL, Romero LM (2010) Chronic psychological stress alters body weight and blood chemistry in European starlings (Sturnus vulgaris). Comp Biochem Physiol A Mol Integr Physiol 156: 136–142. 10.1016/j.cbpa.2010.01.010. [DOI] [PubMed] [Google Scholar]
  5. Batson WG, Gordon IJ, Fletcher DB, Portas TJ, Manning AD (2017) The effect of pre-release captivity on the stress physiology of a reintroduced population of wild eastern bettongs. J Zool 303: 311–319. 10.1111/jzo.12494. [DOI] [Google Scholar]
  6. Blas J, Fairhurst GD (2022) Chapter 38 - Stress ecophysiology. In: Scanes CG, Dridi S, eds. Sturkie’s Avian Physiology (Seventh Edition). Elsevier, San Diego, pp. 1049–1098, 10.1016/B978-0-12-819770-7.00003-7. [DOI] [Google Scholar]
  7. Blickley JL, Word KR, Krakauer AH, Phillips JL, Sells SN, Taff CC, Wingfield JC, Patricelli GL (2012) Experimental chronic noise is related to elevated fecal corticosteroid metabolites in Lekking male greater sage-grouse (Centrocercus urophasianus). PloS One 7: e50462. 10.1371/journal.pone.0050462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bortolotti GR, Marchant TA, Blas J, German T (2008) Corticosterone in feathers is a long-term, integrated measure of avian stress physiology. Funct Ecol 22: 494–500. 10.1111/j.1365-2435.2008.01387.x. [DOI] [Google Scholar]
  9. Bosson CO, Palme R, Boonstra R (2009) Assessment of the stress response in Columbian ground squirrels: laboratory and field validation of an enzyme immunoassay for fecal cortisol metabolites. Physiol Biochem Zool 82: 291–301. 10.1086/597530. [DOI] [PubMed] [Google Scholar]
  10. Breed D, Meyer LCR, Steyl JCA, Goddard A, Burroughs R, Kohn TA (2019) Conserving wildlife in a changing world: understanding capture myopathy—a malignant outcome of stress during capture and translocation. Conserv Physiol 7: coz027. 10.1093/conphys/coz027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brennan LA, Covington WW (1994) Broad-scale population declines in four species of North American quail: an examination of possible causes. In: sustainable ecological systems: implementing an ecological approach to land management. USDA Forest Service General Technical Report RM-247: 44–50. [Google Scholar]
  12. Breuner CW, Wingfield JC, Romero LM (1999) Diel rhythms of basal and stress-induced corticosterone in a wild, seasonal vertebrate, Gambel’s white-crowned sparrow. J Exp Zool 284: 334–342. 10.1002/(SICI)1097-010X(19990801)284:3<334::AID-JEZ11>3.0.CO;2-#. [DOI] [PubMed] [Google Scholar]
  13. Buchanan KL (2000) Stress and the evolution of condition-dependent signals. Trends Ecol Evol 15: 156–160. 10.1016/S0169-5347(99)01812-1. [DOI] [PubMed] [Google Scholar]
  14. Cinto Mejia E, McClure CJW, Barber JR (2019) Large-scale manipulation of the acoustic environment can alter the abundance of breeding birds: evidence from a phantom natural gas field. J Appl Ecol 56: 2091–2101. 10.1111/1365-2664.13449. [DOI] [Google Scholar]
  15. Cockrem JF (2007) Stress, corticosterone responses and avian personalities. J Ornithol 148: 169–178. 10.1007/s10336-007-0175-8. [DOI] [Google Scholar]
  16. Cockrem JF (2013) Corticosterone responses and personality in birds: individual variation and the ability to cope with environmental changes due to climate change. Gen Comp Endocrinol 190: 156–163. 10.1016/j.ygcen.2013.02.021. [DOI] [PubMed] [Google Scholar]
  17. Cockrem JF, Silverin B (2002) Variation within and between birds in corticosterone responses of great tits (Parus major). Gen Comp Endocr 125: 197–206. 10.1006/gcen.2001.7750. [DOI] [PubMed] [Google Scholar]
  18. Creel S (2001) Social dominance and stress hormones. Trends Ecol Evol 16: 491–497. 10.1016/S0169-5347(01)02227-3. [DOI] [Google Scholar]
  19. Crespi EJ, Williams TD, Jessop TS, Delehanty B (2013) Life history and the ecology of stress: how do glucocorticoid hormones influence life-history variation in animals? Funct Ecol 27: 93–106. 10.1111/1365-2435.12009. [DOI] [Google Scholar]
  20. Cyr NE, Romero LM (2007) Chronic stress in free-living European starlings reduces corticosterone concentrations and reproductive success. Gen Comp Endocr 151: 82–89. 10.1016/j.ygcen.2006.12.003. [DOI] [PubMed] [Google Scholar]
  21. Cyr NE, Romero LM (2008) Fecal glucocorticoid metabolites of experimentally stressed captive and free-living starlings: implications for conservation research. Gen Comp Endocrinol 158: 20–28. 10.1016/j.ygcen.2008.05.001. [DOI] [PubMed] [Google Scholar]
  22. DeVries MS, Jawor JM (2013) Natural variation in circulating testosterone does not predict nestling provisioning rates in the northern cardinal, Cardinalis cardinalis. Anim Behav 85: 957–965. 10.1016/j.anbehav.2013.02.019. [DOI] [Google Scholar]
  23. Dickens MJ, Bentley GE (2014) Stress, captivity, and reproduction in a wild bird species. Horm Behav 66: 685–693. 10.1016/j.yhbeh.2014.09.011. [DOI] [PubMed] [Google Scholar]
  24. Dickens MJ, Delehanty DJ, Romero LM (2009) Stress and translocation: alterations in the stress physiology of translocated birds. Proc R Soc Lond B Biol Sci 276: 2051–2056. 10.1098/rspb.2008.1778. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Dickens MJ, Delehanty DJ, Romero LM (2010) Stress: an inevitable component of animal translocation. Biol Conserv 143: 1329–1341. 10.1016/j.biocon.2010.02.032. [DOI] [Google Scholar]
  26. Dickens MJ, Romero LM (2009) Wild European starlings (Sturnus vulgaris) adjust to captivity with sustained sympathetic nervous system drive and a reduced fight-or-flight response. Physiol Biochem Zool 82: 603–610. 10.1086/603633. [DOI] [PubMed] [Google Scholar]
  27. Ellis RD, McWhorter TJ, Maron M (2012) Integrating landscape ecology and conservation physiology. Landsc Ecol 27: 1–12. 10.1007/s10980-011-9671-6. [DOI] [Google Scholar]
  28. Fazio E, Ferlazzo A (2003) Evaluation of stress during transport. Vet Res Commun 27: 519–524. 10.1023/B:VERC.0000014211.87613.d9. [DOI] [PubMed] [Google Scholar]
  29. Felton A, Fischer J, Lindenmayer DB, Montague-Drake R, Lowe AR, Saunders D, Felton AM, Steffen W, Munro NT, Youngentob Ket al. (2009) Climate change, conservation and management: an assessment of the peer-reviewed scientific journal literature. Biodivers Conserv 18: 2243–2253. 10.1007/s10531-009-9652-0. [DOI] [Google Scholar]
  30. Fischer CP, Wright-Lichter J, Romero LM (2018) Chronic stress and the introduction to captivity: how wild house sparrows (Passer domesticus) adjust to laboratory conditions. Gen Comp Endocrinol 259: 85–92. 10.1016/j.ygcen.2017.11.007. [DOI] [PubMed] [Google Scholar]
  31. Fletcher K, Xiong Y, Fletcher E, Gustafsson L (2018) Glucocorticoid response to both predictable and unpredictable challenges detected as corticosterone metabolites in collared flycatcher droppings. PloS One 13: e0209289. 10.1371/journal.pone.0209289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Florant GL, Weitzman ED (1980) Diurnal and episodic pattern of plasma cortisol during fall and spring in young and old woodchucks (Marmota monax). Comp Biochem Physiol A Physiol 66: 575–581. 10.1016/0300-9629(80)90002-X. [DOI] [Google Scholar]
  33. Formenti N, Viganó R, Bionda R, Ferrari N, Trogu T, Lanfranchi P, Palme R (2015) Increased hormonal stress reactions induced in an Alpine black grouse (Tetrao tetrix) population by winter sports. J Ornithol 156: 317–321. 10.1007/s10336-014-1103-3. [DOI] [Google Scholar]
  34. Fountain K, Jeffs C, Croft S, Gregson J, Lister J, Evans A, Carter I, Chang YM, Sainsbury AW (2017) The influence of risk factors associated with captive rearing on post-release survival in translocated cirl buntings Emberiza cirlus in the UK. Oryx 51: 332–338. 10.1017/S0030605315001313. [DOI] [Google Scholar]
  35. Gomez LJ, Reyna KS (2017) An evaluation of northern bobwhite conservation research: a call for large-scale studies. Proceedings of the National Quail Symposium 8: 119–131. [Google Scholar]
  36. Griffith B, Scott JM, Carpenter JW, Reed C (1989) Translocation as a species conservation tool: status and strategy. Science 245: 477–480. 10.1126/science.245.4917.477. [DOI] [PubMed] [Google Scholar]
  37. Guthery FS, Forrester ND, Nolte KR, Cohen WE, Kuvlevsky WP (2000) Potential effects of global warming on quail populations. Proceedings of the National Quail Symposium 4: 198–204. [Google Scholar]
  38. Hawkins P, Morton DB, Cameron D, Cuthill I, Francis R, Freire R, Gosler A, Healy S, Hudson A, Inglis I (2001) Laboratory birds: refinements in husbandry and procedures. Laboratory Animals 35: S1–S163. [PubMed] [Google Scholar]
  39. Hernández F, Brennan LA, DeMaso SJ, Sands JP, Wester DB (2013) On reversing the northern bobwhite population decline: 20 years later. Wildl Soc Bull 37: 177–188. 10.1002/wsb.223. [DOI] [Google Scholar]
  40. Homyack JA (2010) Evaluating habitat quality of vertebrates using conservation physiology tools. Wildl Res 37: 332–342. 10.1071/WR08093. [DOI] [Google Scholar]
  41. Jankowski MD, Russell RE, Franson JC, Dusek RJ, Hines MK, Gregg M, Hofmeister EK (2014) Corticosterone metabolite concentrations in greater sage-grouse are positively associated with the presence of cattle grazing. Rangel Ecol Manage 67: 237–246. 10.2111/REM-D-13-00137.1. [DOI] [Google Scholar]
  42. Johnson JL, Rollins D, Reyna KS (2012) What’s a quail worth? A longitudinal assessment of quail hunter demographics, attitudes, and spending habits in Texas. Proceedings of the National Quail Symposium 7: 294–299. [Google Scholar]
  43. Jones SM, Lockhart TJ, Rose RW (2005) Adaptation of wild-caught Tasmanian devils (Sarcophilus harrisii) to captivity: evidence from physical parameters and plasma cortisol concentrations. Aust J Zool 53: 339–344. 10.1071/ZO05043. [DOI] [Google Scholar]
  44. Jong IC, Voorst AS, Erkens JH, Ehlhardt DA, Blokhuis HJ (2001) Determination of the circadian rhythm in plasma corticosterone and catecholamine concentrations in growing broiler breeders using intravenous cannulation. Physiol Behav 74: 299–304. 10.1016/S0031-9384(01)00562-5. [DOI] [PubMed] [Google Scholar]
  45. Khan MZ, Altmann J, Isani SS, Yu J (2002) A matter of time: evaluating the storage of fecal samples for steroid analysis. Gen Comp Endocr 128: 57–64. 10.1016/S0016-6480(02)00063-1. [DOI] [PubMed] [Google Scholar]
  46. Leopold AS (1977) The California Quail. University of California Press, Berkeley, CA, 10.1525/9780520907775. [DOI] [Google Scholar]
  47. Lexen E, El-Bahr SM, Sommerfeld-Stur I, Palme R, Mostl E (2008) Monitoring the adrenocortical response to disturbances in sheep by measuring glucocorticoid metabolites in the faeces. Wien Tierarztl Monatsschr 95: 64–71. [Google Scholar]
  48. Littin KE, Cockrem JF (2001) Individual variation in corticosterone secretion in laying hens. Br Poultry Sci 42: 536–546. 10.1080/00071660120070613. [DOI] [PubMed] [Google Scholar]
  49. Martin JA, Applegate RD, Dailey TV, Downey M, Emmerich B, Hernández F, McConnell MM, Reyna KS, Rollins D, Ruzicka REet al. (2017) Translocation as a population restoration technique for northern bobwhites: a review and synthesis. Proceedings of the National Quail Symposium 8: 11–16. 10.7290/nqsp08mg04. [DOI] [Google Scholar]
  50. Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Chen Y, Goldfarb L, Gomis MI, Matthews JBR, Berger Set al. (2021) Climate Change 2021: the physical science basis. In V Masson-Delmotte, P Zhai, A Pirani, SL Connors, C Péan, S Berger, N Caud, Y Chen, L Goldfarb, MI Gomis, et al., eds,Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland. [Google Scholar]
  51. McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43: 2–15. 10.1016/S0018-506X(02)00024-7. [DOI] [PubMed] [Google Scholar]
  52. Messmann S, Bagu E, Robia C, Palme R (1999) Measurement of glucocorticoid metabolite concentrations in faeces of domestic livestock. J Vet Med A Physiol Pathol Clin Med 46: 621–631. 10.1046/j.1439-0442.1999.00256.x. [DOI] [PubMed] [Google Scholar]
  53. Millspaugh JJ, Washburn BE (2004) Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. Gen Comp Endocr 138: 189–199. 10.1016/j.ygcen.2004.07.002. [DOI] [PubMed] [Google Scholar]
  54. Mohlman JL, Navara KJ, Sheriff MJ, Terhune TM, Martin JA (2020) Validation of a noninvasive technique to quantify stress in northern bobwhite (Colinus virginianus). Conserv Physiol 8: coaa026. 10.1093/conphys/coaa026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Möstl E, Rettenbacher S, Palme R (2005) Measurement of corticosterone metabolites in birds’ droppings: an analytical approach. Ann N Y Acad Sci 1046: 17–34. 10.1196/annals.1343.004. [DOI] [PubMed] [Google Scholar]
  56. National Research Council (2010) Guide for the Care and Use of Laboratory Animals, EdEighth. The National Academies Press, Washington, DC, USA. [Google Scholar]
  57. O’Dell D, Carlo M, Kimmitt A, Bikowski E, Morris K, Dolby A (2014) A comparison of techniques measuring stress in birds. Va J Sci 65: 133–149. [Google Scholar]
  58. Palme R (2019) Non-invasive measurement of glucocorticoids: advances and problems. Physiol Behav 199: 229–243. 10.1016/j.physbeh.2018.11.021. [DOI] [PubMed] [Google Scholar]
  59. Palme R, Fischer P, Schildorfer H, Ismail MN (1996) Excretion of infused 14C-steroid hormones via faeces and urine in domestic livestock. Anim Reprod Sci 43: 43–63. 10.1016/0378-4320(95)01458-6. [DOI] [Google Scholar]
  60. Perez RM, Wilson DE, Gruen KD (2002) Survival and flight characteristics of captive-reared and wild northern bobwhites in South Texas. Proceedings of the National Quail Symposium 5: 81–85. [Google Scholar]
  61. Pope M, Heekin P (2017) How ecological disturbances may influence mountain quail in the Pacific Northwest. Proceedings of the National Quail Symposium 4: 206. 10.7290/nqsp04unlt. [DOI] [Google Scholar]
  62. Rabon JC, Nuñez CMV, Coates PS, Ricca MA, Johnson TN (2021) Ecological correlates of fecal corticosterone metabolites in female greater sage-grouse (Centrocercus urophasianus). Can J Zool 99: 812–822. 10.1139/cjz-2020-0258. [DOI] [Google Scholar]
  63. Reyna KS (2019) Acute exposure to hyperthermic oscillating temperatures during pre-incubation influences northern bobwhite development, hatching, and survival. PloS One 14: e0219368. 10.1371/journal.pone.0219368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Reyna KS, Burggren WW (2017) Altered embryonic development in northern bobwhite quail (Colinus virginianus) induced by pre-incubation oscillatory thermal stresses mimicking global warming predictions. PloS One 12: e0184670. 10.1371/journal.pone.0184670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Reyna KS, Newman WL (2018) Comparative analysis of behavioural response of captive-reared and wild-trapped northern bobwhites to simulated predator attacks. Avian Biol Res 11: 16–23. 10.3184/175815617X15102246785440. [DOI] [Google Scholar]
  66. Reyna KS, Whitt JG, Currier SA, SP SM, Rushing GT, Conley JT, Vandenberg CA, Moser EL (2020) California Quail Translocation from Idaho to Texas. Texas A&M University Commerce, The Quail Research Laboratory, College of Agricultural Sciences and Natural Resources. [Google Scholar]
  67. Rich EL, Romero LM (2005) Exposure to chronic stress downregulates corticosterone responses to acute stressors. Am J Physiol Regul Integr Comp Physiol 288: R1628–R1636. 10.1152/ajpregu.00484.2004. [DOI] [PubMed] [Google Scholar]
  68. Romero LM, Gormally BMG (2019) How truly conserved is the “well-conserved” vertebrate stress response? Integr Comp Biol 59: 273–281. 10.1093/icb/icz011. [DOI] [PubMed] [Google Scholar]
  69. Romero LM, Remage-Healey L (2000) Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): corticosterone. Gen Comp Endocr 119: 52–59. 10.1006/gcen.2000.7491. [DOI] [PubMed] [Google Scholar]
  70. Romero ML, Butler LK (2007) Endocrinology of stress. Int J Comp Psychol 20: 89–95. [Google Scholar]
  71. Rupp H (1999) Excess catecholamine syndrome: pathophysiology and therapy. Ann N Y Acad Sci 881: 430–444. 10.1111/j.1749-6632.1999.tb09391.x. [DOI] [PubMed] [Google Scholar]
  72. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory and preparative actions. Endocr Rev 21: 55–89. [DOI] [PubMed] [Google Scholar]
  73. Scott JL, Hernández F, Brennan LA, Ballard BM, Janis M, Forrester ND (2013) Population demographics of translocated northern bobwhites on fragmented habitat. Wildl Soc Bull 37: 168–176. 10.1002/wsb.239. [DOI] [Google Scholar]
  74. Şekercioğlu ÇH, Primack RB, Wormworth J (2012) The effects of climate change on tropical birds. Biol Conserv 148: 1–18. 10.1016/j.biocon.2011.10.019. [DOI] [Google Scholar]
  75. Seneviratne S, Nicholls N, Easterling D, Goodess C, Kanae S, Kossin J, Luo Y, Marengo J, McInnes K, Rahimi M, et al. (2012) Changes in climate extremes and their impacts on the natural physical environment. In: Field CB, Barros VR, Stocker TF, Qin D, Dokken DJ, Ebi KL, Mastrandrea MD, Mach KJ, Plattner GK, Allen SK, et al., eds. Managing the Risks of Extreme Events and Disasters to Advance Climate Change Adaptation, A Special Report of Working Groups I and II of the Intergovernmental Panel on Climate Change (IPCC). Cambridge University Press, Cambridge, UK, 10.1017/CBO9781139177245.006. [DOI] [Google Scholar]
  76. Sheriff MJ, Bosson CO, Krebs CJ, Boonstra R (2009) A non-invasive technique for analyzing fecal cortisol metabolites in snowshoe hares (Lepus americanus). J Comp Physiol B 179: 305–313. 10.1007/s00360-008-0314-4. [DOI] [PubMed] [Google Scholar]
  77. Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166: 869–887. 10.1007/s00442-011-1943-y. [DOI] [PubMed] [Google Scholar]
  78. Sheriff MJ, Krebs CJ, Boonstra R (2010) Assessing stress in animal populations: do fecal and plasma glucocorticoids tell the same story? Gen Comp Endocrinol 166: 614–619. 10.1016/j.ygcen.2009.12.017. [DOI] [PubMed] [Google Scholar]
  79. Shipley AA, Sheriff MJ, Pauli JN, Zuckerberg B (2019) Snow roosting reduces temperature-associated stress in a wintering bird. Oecologia 190: 309–321. 10.1007/s00442-019-04389-x. [DOI] [PubMed] [Google Scholar]
  80. Shipley AA, Sheriff MJ, Pauli JN, Zuckerberg B (2022) Weather and land cover create a predictable “stress-scape” for a winter-adapted bird. Landsc Ecol 37: 779–793. 10.1007/s10980-021-01354-z. [DOI] [Google Scholar]
  81. Sisson DC II, Terhune TM II, Palmer WE, Thackston R (2017) Contributions of translocation to northern bobwhite population recovery. Proceedings of the National Quail Symposium 8: 151–159. 10.7290/nqsp08hese. [DOI] [Google Scholar]
  82. Sokół R, Koziatek-Sadłowska S (2020) Changes in the corticosterone level in tooting male black grouse (Tetrao tetrix) infected with Eimeria spp. Poult Sci 99: 1306–1310. 10.1016/j.psj.2019.10.074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Sokos CK, Birstas PK, Tsachalidis EP (2008) The aims of galliforms release and choice of techniques. Wildlife Biol 14: 412–422. 10.2981/0909-6396-14.4.412. [DOI] [Google Scholar]
  84. Son YL, Ubuka T, Narihiro M, Fukuda Y, Hasunuma I, Yamamoto K, Belsham DD, Tsutsui K (2014) Molecular basis for the activation of gonadotropin-inhibitory hormone gene transcription by corticosterone. Endocrinology 155: 1817–1826. 10.1210/en.2013-2076. [DOI] [PubMed] [Google Scholar]
  85. Sportsmen’s Alliance (2021) Economic Impact of Hunting and Shooting in 2020 Technical Report. Southwick Associates, Fernandina Beach, Florida, USA. [Google Scholar]
  86. Stephenson JA, Reese KP, Zager P, Heekin PE, Nelle PJ, Martens A (2011) Factors influencing survival of native and translocated mountain quail in Idaho and Washington. J Wildl Manag 75: 1315–1323. 10.1002/jwmg.189. [DOI] [Google Scholar]
  87. Suedkamp Wells KM, Washburn BE, Millspaugh JJ, Ryan MR, Hubbard MW (2003) Effects of radio-transmitters on fecal glucocorticoid levels in captive dickcissels. Condor 105: 805–810. 10.1093/condor/105.4.805. [DOI] [Google Scholar]
  88. Suorsa P, Huhta E, Nikula A, Nikinmaa M, Jäntti A, Helle H, Hakkarainen H (2003) Forest management is associated with physiological stress in an old–growth forest passerine. Proc R Soc Lond B Biol Sci 270: 963–969. 10.1098/rspb.2002.2326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Tanner EP, Elmore RD, Fuhlendorf SD, Davis CA, Dahlgren DK, Orange JP (2017) Extreme climatic events constrain space use and survival of a ground-nesting bird. Glob Chang Biol 23: 1832–1846. 10.1111/gcb.13505. [DOI] [PubMed] [Google Scholar]
  90. Teixeira CP, Azevedo CSD, Mendl M, Cipreste CF, Young RJ (2007) Revisiting translocation and reintroduction programmes: the importance of considering stress. Anim Behav 73: 1–13. 10.1016/j.anbehav.2006.06.002. [DOI] [Google Scholar]
  91. Tempel DJ, Gutiérrez RJ (2004) Factors related to fecal corticosterone levels in California spotted owls: implications for assessing chronic stress. Conserv Biol 18: 538–547. 10.1111/j.1523-1739.2004.00372.x. [DOI] [Google Scholar]
  92. Thiel D, Jenni-Eiermann S, Braunisch V, Palme R, Jenni L (2008) Ski tourism affects habitat use and evokes a physiological stress response in capercaillie Tetrao urogallus: a new methodological approach. J Appl Ecol 45: 845–853. 10.1111/j.1365-2664.2008.01465.x. [DOI] [Google Scholar]
  93. Thiel D, Jenni-Eiermann S, Palme R, Jenni L (2011) Winter tourism increases stress hormone levels in the capercaillie Tetrao urogallus. Ibis 153: 122–133. 10.1111/j.1474-919X.2010.01083.x. [DOI] [Google Scholar]
  94. Touma C, Palme R (2005) Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann N Y Acad Sci 1046: 54–74. 10.1196/annals.1343.006. [DOI] [PubMed] [Google Scholar]
  95. Touma C, Palme R, Sachser N (2004) Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Horm Behav 45: 10–22. 10.1016/j.yhbeh.2003.07.002. [DOI] [PubMed] [Google Scholar]
  96. Vliet HEJ, Stutchbury BJM, Newman AEM, Norris DR (2020) The impacts of agriculture on an obligate grassland bird of North America. Agric Ecosyst Environ 287: 106696. 10.1016/j.agee.2019.106696. [DOI] [Google Scholar]
  97. Warwick H, Morris P, Walker D (2006) Survival and weight changes of hedgehogs (Erinaceus europaeus) translocated from the Hebrides to mainland Scotland. Lutra 49: 89–102. [Google Scholar]
  98. Washburn BE, Millspaugh JJ, Schulz JH, Jones SB, Mong T (2003) Using fecal glucocorticoids for stress assessment in mourning doves. Condor 105: 696–706. 10.1093/condor/105.4.696. [DOI] [Google Scholar]
  99. Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett CM, Bechert U, Millspaugh JJ, Larson S, Monfort SL (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen Comp Endocrinol 120: 260–275. 10.1006/gcen.2000.7557. [DOI] [PubMed] [Google Scholar]
  100. Wasser SK, Risler L, Steiner RA (1988) Excreted steroids in primate feces over the menstrual cycle and pregnancy. Biol Reprod 39: 862–872. 10.1095/biolreprod39.4.862. [DOI] [PubMed] [Google Scholar]
  101. Wein Y, Bar Shira E, Friedman A (2017) Avoiding handling-induced stress in poultry: use of uniform parameters to accurately determine physiological stress. Poult Sci 96: 65–73. 10.3382/ps/pew245. [DOI] [PubMed] [Google Scholar]
  102. Whitt J, Reyna K (2022) Relationships between meteorological and other variables and bobwhite spring call counts. NQSP 9: 196–209. 10.7290/nqsp09EIlv. [DOI] [Google Scholar]
  103. Whitt JG, Johnson JA, Reyna KS (2017) Two centuries of human-mediated gene flow in northern bobwhites. Wildl Soc Bull 41: 639–648. 10.1002/wsb.829. [DOI] [Google Scholar]
  104. Wilsey C, Bateman B, Taylor L, Wu JX, LeBaron G, Shepherd R, Koseff C, Friedman S, Stone R (2019) Survival by Degrees: 389 Bird Species on the Brink. National Audubon Society, New York, NY, USA. [Google Scholar]
  105. Wingfield JC, Pérez JH, Krause JS, Word KR, González-Gómez PL, Lisovski S, Chmura HE (2017) How birds cope physiologically and behaviourally with extreme climatic events. Philos Trans R Soc Lond B Biol Sci 372: 20160140. 10.1098/rstb.2016.0140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Wingfield JC, Romero LM (2011) Adrenocortical responses to stress and their modulation in free-living vertebrates. In Y Prakash, ed,Comprehensive Physiology. John Wiley & Sons, Ltd, Rochester, pp. 211–234 [Google Scholar]
  107. Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15: 711–724. 10.1046/j.1365-2826.2003.01033.x. [DOI] [PubMed] [Google Scholar]
  108. Wszola LS, Gruber LF, Stuber EF, Messinger LN, Chizinski CJ, Fontaine JJ (2020) Use and expenditures on public access hunting lands. J Outdoor Recreat Tour 29: 100256. 10.1016/j.jort.2019.100256. [DOI] [Google Scholar]
  109. Zar JH (1996) Biostatistical Analysis, Ed3rd. Pearson, Upper Saddle River, NJ, USA. [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data underlying this article will be shared on reasonable requests to the corresponding author.

Articles from Conservation Physiology are provided here courtesy of Oxford University Press

RESOURCES