Levels of fecal glucocorticoid metabolites do not reflect environmental contrasts across islands in black-tailed deer (Odocoileus hemionus sitkensis) populations Soizic Le Saout, Marlène Massouh, JeanLouis Martin, Hélène Presseault-Gauvin, Eva Poilvé, Steeve D. Côté, Denis Picot, et al. Mammal Research ISSN 2199-2401 Mamm Res DOI 10.1007/s13364-016-0294-9
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Author's personal copy Mamm Res DOI 10.1007/s13364-016-0294-9
ORIGINAL PAPER
Levels of fecal glucocorticoid metabolites do not reflect environmental contrasts across islands in black-tailed deer (Odocoileus hemionus sitkensis) populations Soizic Le Saout 1 & Marlène Massouh 1 & Jean-Louis Martin 1 & Hélène Presseault-Gauvin 2 & Eva Poilvé 3 & Steeve D. Côté 4 & Denis Picot 3 & Hélène Verheyden 3 & Simon Chamaillé-Jammes 1
Received: 24 November 2015 / Accepted: 25 August 2016 # Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2016
Abstract Animals face stressful situations to which they can respond by mounting a physiological response. Few studies have compared the relative effects of two or more stressors on this response. We compared how low food abundance and hunting affected levels of fecal glucocorticoid metabolites (FGM), an indicator of stress, in Sitka black-tailed deer (Odocoileus hemionus sitkensis) on the Haida Gwaii archipelago (Canada). We monitored monthly FGM levels over a year on three islands: on two, there was no hunting but deer were exposed to increased risk of severe food depletion; and on one, deer had access to abundant food but were exposed to a few days of hunting each year. Based on the context of the study, we tentatively predicted that FGM levels would be higher in low food abundance/safe islands. We also predicted that FGM levels would be higher in winter when food is rarer, particularly in low food abundance/safe islands. The three
deer populations presented similar average FGM levels and seasonal variations. Our predictions were therefore not supported. Our results rather suggested that environmental contrasts, perceived by us as large (increased risk of starvation on ELI and Kunga islands) or associated with differences in animal behavior (human avoidance on Reef island), did not lead to increased stress responses. We discuss plausible explanations, including the down-regulation of the stress response in depleted environments and the lack of stress response to low hunting pressure when behavioral responses to risk are unlikely to be costly. Keywords Cortisol . Corticosterone . Food depletion . HPA axis . Predation risk . Ungulate
Introduction Communicated by: Dries Kuijper Electronic supplementary material The online version of this article (doi:10.1007/s13364-016-0294-9) contains supplementary material, which is available to authorized users. * Simon Chamaillé-Jammes
[email protected] 1
CEFE UMR 5175, CNRS – Université de Montpellier – Université Paul-Valéry Montpellier – EPHE, 1919 route de Mende, 34293 Montpellier Cedex 5, France
2
Canada Research Chair in Evolutionary Demography and Conservation, Département de biologie, Université de Sherbrooke, Sherbrooke, QC J1K 2R1, Canada
3
CEFS UR 035, INRA, 24 Chemin de Borde Rouge, Auzeville, BP CS 52627, 31326 Castanet-Tolosan Cedex, France
4
Département de biologie and Centre d’études nordiques, Université Laval, Laval, QC G1V 0A6, Canada
Animals are continuously challenged by their environment and by the need to find food, avoid predation and parasites, or find mates. Various physiological processes have evolved to contribute to an individual’s homeostasis and thereby allowing individuals to face these challenges (McEwen and Wingfield 2003). Those challenges are referred to as stressors when the adaptive capacity of the individual to deal with them is low, either because of the strength of the challenge (e.g., exceptional weather conditions) and/or because of a reduced capacity of the individual itself (e.g., poor body condition) (Koolhaas et al. 2011). In vertebrates, a family of steroid hormones—the glucocorticoids (GC)—often qualifies as stress hormones, orchestrating the mobilization and re-allocation of energy that is required when the animal copes with stress challenges (Wingfield et al. 1998). Recent reviews of the effects of various stressors on GC levels can be found in Baker
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et al. (2013), Boonstra (2013), Clinchy et al. (2013), Creel et al. (2013), and Wingfield (2013). A rapid increase (over a few minutes) in GC levels is generally seen as an adaptive response to some acute stressor. Baseline GC levels have also been shown to sometimes increase over the long run under chronic stress. Prolonged exposure to high levels of GC may have deleterious effects with negative impacts on growth, immunity, or reproduction (Wingfield et al. 1997; Bonier et al. 2009). Behavioral or physiological adjustments should thus have evolved to limit long-term changes in baseline GC levels. Indeed, examples of baseline GC levels resistant to chronic stress, or habituation and down-regulation of the GC response to stressful events, have been found (e.g., Rich and Romero 2005). Thus, regulation of GC baseline levels is a key process determining how animals cope and succeed in responding to stress over the long term, but the determinants of baseline GC levels over the long run remain uncertain. Despite the large amount of recent research performed on the expression and regulation of the stress response via changes in GC levels, few studies have compared the relative effect of different stressors on baseline GC levels, particularly in the wild. This appears crucial, however, to understand whether some stressors have stronger effects on GC levels. For instance, because wild individuals commonly face a trade-off between finding food and avoiding predation (Lima and Dill 1990), one may wonder whether long-term changes in food availability or predation risk would have a stronger influence on baseline GC levels. In a unique study, Clinchy et al. (2004) manipulated food availability for song-sparrows (Melospiza melodia) in two sites with contrasting predation risk. They found that both food availability and predation risk affected baseline corticosterone levels, but most interestingly, that increased food availability or reduced predation risk led to similar baseline GC levels. A few other studies also shed light, although sometimes with contrasting results, on this issue. Creel et al. (2009) for instance showed that in the Greater Yellowstone Ecosystem (USA) elk (Cervus elaphus) fecal GC metabolites (FGM) were neither related to elk/wolf (Canis lupus) ratio (an index of predation risk) nor to elk population size (an index of density-dependent food availability). Monclùs et al. (2009) showed that spatial variation in FGM levels in rabbits (Oryctolagus cuniculus) of the Donana Biological Reserve (Spain) was best explained by an index of predator pressure, although a model with only food availability performed only slightly less well. In short, it is still unclear whether food availability or predation risk similarly affects baseline GC levels, or under what conditions could the magnitude of their effects vary. Although natural predators and hunters may not impose similar risk onto prey (Cromsigt et al. 2013), hunting does increase GC levels in prey at least temporarily (Bateson and Bradshaw 1997), and the question of the relative importance of resource availability and hunting in driving GC levels of prey also arises.
Here, we studied the relative effects of low food abundance and hunting risk on baseline GC levels in black-tailed deer (Odocoileus hemionus columbianus) in three neighboring islands of the Haida Gwaii archipelago (Canada). On two islands (East Limestone and Kunga islands), deer live at high population density in forests with a severely depleted understory and are not hunted. On the third island (Reef island), deer were severely culled in 1997 and now benefit from a rich forest understory, which has regenerated, but are still regularly exposed to short hunting events. We monitored FGM levels on each island over 1 year. Because there is yet relatively little knowledge on the relative effects of food availability and predation risk on GC levels, we tentatively predicted that FGM levels would be higher on the food-poor, safe islands than on the food-rich, risky island (prediction 1). Indeed, as during the last ~15 years hunting occurred annually only during a few days, we hypothesized that deer, although potentially responding with an acute response to the presence of hunters, could have mostly adjusted behaviourally and would display an only moderate increase in baseline GC levels. We also predicted that FGM levels would increase in winter when food is limited, and that this would be particularly marked on the low food abundance/safe islands, where deer could be at a higher risk of winter starvation (prediction 2). We ascertained seasonal and inter-island differences in diet quality by measuring fecal nitrogen content. As deer were sometimes observed consuming seaweeds, which possibly could affect stress physiology (e.g., Archer 2005), we conducted a micro-histological study of the feces to quantify seaweed consumption and evaluate its effect on GC levels.
Material and methods Study area The study was conducted on the East coast of the Haida Gwaii archipelago (British Columbia, Canada), on three islands located within 15 km from each other: East Limestone (41 ha, WGS84–52.91 N 131.61 W), Kunga (395 ha, WGS84– 52.77 N 131.57 W), and Reef (249 ha: WGS84–52.87 N 131.52 W) islands. The climate is cool temperate, oceanic, and humid-perhumid with narrow temperature variations around the average annual value of 8 °C (Pojar 2008). All islands were uninhabited, and human presence was restricted to the presence of rare tourist visits in summer and occasional research activities (from March to July and from September to October during the study period). Between March and early July 2011, East Limestone and Kunga islands served as base camps for research conducted on the three islands, although human activities were much more intense on East Limestone than on Kunga.
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Deer were introduced on Haida Gwaii c. 100 years ago and reached the study islands over 60 years ago (Vila et al. 2004). There, in the absence of predation (natural and human), deer built up high-density populations (estimated to be >30 deer/km2 in 1996 (Daufresne and Martin 1997) and dramatically reduced forest understory cover by >90 % (Martin et al. 2010)). In 1997, a cull was initiated on Reef island to protect its biodiversity. The deer population was reduced by >70 % within 3 years of the first hunt (Gaston et al. 2008), and regular hunting had since then limited population growth (current density 17 ind/km2 (95 % CI 10–29), Le Saout et al. 2014a). The last hunt took place in June 2010, 6 months prior to the beginning of the study, and no hunting occurred during the study period. Researchers, however, were present with daily fieldwork activities taking place on Reef from May to July 2011 as well as in September and October 2011. The understory on Reef had partially recovered and now offers rich and dense food resources to deer (Chollet et al. 2015). No cull occurred on East Limestone and Kunga islands, and plants that persist in the understory were mostly 2 % of seaweeds were collected in October 2011 on Kunga island. There was no relationship between FGM levels estimated in a sample, and the proportion of seaweed epidermis found once corrected for seasonal and island variations (F9,76 = 0.03, P = 0.86).
Discussion Our study revealed no differences between mean annual FGM levels of deer across the three islands. Even at the monthly time scale, little differences were detected, suggesting that the absence of overall difference among the islands was not an artifact of averaging over the year. Therefore, our prediction that FGM levels would be higher on low food abundance/safe islands (prediction 1) was not supported; neither was the more general prediction that we would observe differences between island categories (poor/safe vs. rich/risky). A first possible explanation for our results is that the methodological approach we used might have had little power to detect differences in GC levels. During this study, it was not logistically feasible to directly validate the relationship between GC plasmatic levels and FGM levels and test the sensitivity of the antibody. We found no previous tests of those for black-tailed deer. The reliability of our interpretation of the results depends on this however. Only adrenocorticotropichormone (ACTH) challenges with the R4866 antibody, conducted on black-tailed deer (see for instance Millspaugh et al.
2002 for ACTH challenge on white-tailed deer with another antibody), would allow confirming the robustness of the methodological approach used here. A second possible explanation for a lack of contrasts in FGM levels across the islands is that the differences in environmental conditions were too low to induce noticeable changes in FGM levels. Although resources available to deer on poor/safe islands are much lower than on the rich/risky islands (Le Saout 2013; Chollet et al. 2015), another study conducted simultaneously to this one revealed that during springtime, deer on poor/safe islands benefit from a flux of hardly visible plant tissue, immediately consumed by deer, produced by perennial species highly tolerant of herbivory and able to survive via underground structures (e.g., rhizomes). Food subsidies were also provided by canopy trees or, indirectly, by plants in refuges (i.e., litterfall and seed bank), as well as by seaweeds (Le Saout et al. 2014a). Thus, deer living on these islands may not be food-stressed during spring and summer time. In winter, deer will be in energydeficit (Le Saout et al. 2014a), but our prediction (prediction 2) that FGM levels would increase at the end of winter (March) when food availability/quality is at the lowest was not supported. Many ungulate species are adapted to face strong seasonality in resource availability, and this may have led to physiological adjustments preventing the seasonal increase in GC levels during the lean period, which would increase energy use and could be detrimental over the long run. Overall, although we cannot compare our results with others that would have been conducted on black-tailed deer using the same antibody, as none were available, we found that mean monthly FGM levels (~ 10–30 ng/g) were in the low range of those found in other ungulates using enzyme immunoassays (e.g., Millspaugh et al. 2001; Washburn and Millspaugh 2002; Millspaugh and Washburn 2003; Pereira et al. 2006; Moll et al. 2009; Forristal et al. 2012). This could suggest that deer in poor/safe islands were not under particularly high GC-based physiological stress. We found no relationship between seaweed consumption and FGM levels and thus ruled out that these marine subsidies could explain the low FGM levels observed. In these poor/safe islands, FGM levels increased during springtime when vegetation quantity and quality also increased. Because the parturition season starts in June, these results are consistent with the observation that GC levels increase during late gestation/early lactation in many species (Touma and Palme 2005; Baker et al. 2013). This reproduction-induced increase in FGM levels can be caused by an increase in plasma steroid-binding globulins (Breuner and Orchinik 2002), but also possibly because of an increased stressful mismatch between energetic needs and resource availability (Touma and Palme 2005). The fact, that this increase was barely noticeable on the resource-rich Reef island but most marked on the island with the poorest resource availability (East Limestone island), suggests that FGM levels
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during that period might indeed be affected by resource availability. Note however that the differences between islands here could have been biased by the sampling process, as the proportion of samples coming from reproductive females may have varied across months and across islands. We could have inadvertently sampled more females in some months, and/or the population sex-ratio might also vary among populations. For instance, sex ratio may be more female-biased on Kunga island than that on East Limestone island (Le Saout et al. 2014a), and this might explain the observed differences in FGM levels during springtime. In any case, the springtime increase in FGM levels on poor/safe islands suggests that our assay allows capturing meaningful ecological variation in FGM levels, and that the contrast in resource availability between poor/safe islands and the rich/risky island is not sufficient to induce differences in FGM levels larger than those imposed by reproduction. The contrast in risk between islands may also have been too low to induce differences in FGM levels. This is surprising given that deer display great differences in behavior between the poor/safe and the rich/risky islands, with marked peopleavoidance on the risky island. These results suggest that deer adjust behaviorally but not physiologically to long-term and unpredictable risk. This is likely to be selected under the current conditions as changes in behavior are unlikely to be costly (food is plentiful on Reef and encounters are rare), whereas increased in baseline GC levels might on the long run has deleterious consequences (Wingfield et al. 1997, Bonier et al. 2009). Studies showing that predation risk is a good predictor of GC levels exist (see review in Clinchy et al. 2013); thus, clarifying the conditions under which predators or hunting may induce a chronic stress response is required (see Boonstra 2013). This might however be complex to study as the perception of risk may persist even in the absence of predators (for this system, see discussion in ChamailléJammes et al. 2014; Le Saout et al. 2015) or may not return immediately as predators return (see Le Saout et al. 2014b), and thus, answering this question might require experimental manipulation over generations. Finally, the lack of support for our prediction that FGM levels would be higher in poor/safe islands could be tentatively explained by the fact that maintaining low GC levels (i.e., the down-regulation of the stress response) may be adaptive to limit the energy expenditure (Wingfield et al. 1998; Rich and Romero, 2005). This would help deer to survive in resourcelimited environments. This argument was made by Taillon and Côté (2008) who found that FGM levels of white-tailed deer fawns were lower when fed a poorer diet and suggested that this could be an adaptive response to limit the fast depletion of proteins and fat during winter. Kitaysky et al. (1999) showed that kittiwakes (Rissa tridactyla) from a resource-poor environment had, before egg incubation started, similar baseline GC levels as birds from a richer environment, but
produced a lower response to an acute stressor (handling). Forristal et al. (2012) also found that elk at non-feedgrounds had lower FGM levels than elk at feedgrounds, but this was caused by higher densities at feedgrounds leading to higher aggression rates. The similarity in FGM levels between high(East Limestone and Kunga islands) and low-density (Reef island) populations, however, indicates that densitydependent effects on FGM levels are not driving FGM levels in our study populations. A proper test of the down-regulation hypothesis requires combining measures of baseline FGM levels with stressresponse curves to acute stressors, which we could not conduct here. To conclude, our results, if our methodological approach is confirmed to be robust, are in line with those from Clinchy et al. (2004), to our knowledge the only experimental comparison of the effects of resource availability and risk on GC levels. Clinchy et al. (2004) indeed found that baseline GC levels in song sparrows were similar between poor/safe and rich/risky environments. We suggest that the underlying mechanisms leading to these apparently similar results are likely to be different, however. Clinchy et al. (2004) demonstrated that variations in resource availability and predation risk were both able to induce a stress response, and that this stress response could sometimes be of the same magnitude (note also that they demonstrated synergistic effects of these stressors, something we could not address here because of the inability to find high food abundance/safe and low food abundance/risky islands). Our study rather suggests that environmental contrasts, perceived by us as large (increased risk of starvation on ELI and Kunga islands) or associated with differences in animal behavior (human avoidance on Reef island), may not lead to increased stress responses. This comparison demonstrates that further studies comparing the effect of various stressors in a common context are required. Ecologists should aim at filling this gap, particularly in the context of an increased need to understand and predict the effects of environmental changes—which are often multifactorial—on animal life histories (Angelier and Wingfield 2013). Acknowledgments This project was funded by the project 2010BLAN-1718 (BAMBI) of the Agence Nationale de la Recherche. We acknowledge the Groupement de Recherche International BDynamique de la biodiversité et traits d’histoire de vie^ and the BUnderstanding Canada program^ from the Government of Canada for the additional financial support. We are indebted to Gwaii Haanas and particularly to C. Bergman for the logistical, technical, and scientific support. Various aspects of this work have benefited from help from members of the Laskeek Bay Conservation Society and of the Research Group on Introduced Species (particularly A. Brown, E. Harris, J. Pattison, B. and K. Rowsell), S. Chollet, T. Verchère, L. Ostermann, M. Hyatt, C. ValléeDubuc, L. Vasilinda, M. Gillingham, K. Tipper, J. Morin, T. and R. Husband, I. Ben-Taleb, B. Buatois, R. Leclerc, D. Cornelis, G. Ganem, J. Michaux, S. Morand, B. Cargnelutti, N. Cebe, M. Hewison, G. Janeau,
Author's personal copy Mamm Res N. Morellet, J.-L. Rames, H. Schwantje, J.-P. Tremblay, M. Pautasso, S. Benhamou, K. Parker, M.-A. Giroux, J. Raven, M.M. Garcia-Rovés, A. Salomon, D. Habault, and R. Fernique. F. Pelletier facilitated this research and made helpful comments on the manuscript. Two anonymous reviewers also helped improving the manuscript.
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