Acute corticosterone elevation enhances antipredator behaviors in male tree lizard morphs
Introduction
Most vertebrates respond to stressors with an increase in plasma concentration of glucocorticoids, and the intensity and predictability of stressors can affect the degree and persistence of the glucocorticoid stress response (McEwen and Wingfield, 2003). The rapid modulatory actions of glucocorticoids on the physiology, neurobiology, and behavior of an animal are numerous and increasingly well understood (reviewed in Sapolsky et al., 2000, Wingfield and Ramenofsky, 1999, Wingfield and Romero, 2001). Following Sapolsky et al. (2000), corticosterone release stimulates responses that promote survival, such as increasing blood glucose levels, while suppressing those that are not crucial to immediate survival, such as growth, parts of the immune system and reproduction (see also Wingfield et al., 1998). Glucocorticoid elevation also has preparative actions to facilitate responses during future stressors (Sapolsky et al., 2000) by stimulating appetite, feeding behavior (Dallman et al., 1993, Kitaysky et al., 2003) and liver glycogen deposition over several hours (Dallman et al., 1993, Munck and Naray-Fejes-Toth, 1995), which promote energy accumulation. Glucocorticoid elevations also prepare an animal for future stressful events by mediating aversive learning during current stressful events (mammals: Kavaliers et al., 2003; birds: Sandi and Rose, 1994, Sandi and Rose, 1997; reptiles: Thaker et al., in review).
Numerous reviews indicate that chronic glucocorticoid elevations have deleterious effects (e.g. Kort, 1994, Sandi, 2004, Joels et al., 2007, McEwen, 2007, Sorrells and Sapolsky, 2007, McEwen, 2008), but acute elevations in glucocorticoids, when appropriate, can be adaptive to prepare for unpredictable and unknown stressors (e.g. McEwen, 2008, Koolhaas et al., 1997). For example, male rats that previously experienced a stressful event (2 h restraint) had higher plasma corticosterone levels after exposure to a new stressor (footshocks) 2 d later and had enhanced context-dependent fear conditioning to that new stressor (Cordero et al., 2003). Heightened anxiety shown by rodents as a consequence of acute glucocorticoids can increase cautiousness in novel situations (Adamec et al., 2006). Even chronic glucocorticoids can intensify the fear response in rodents by increasing freezing responses and possibly enhancing vigilance as well (Rosen et al., 2008). In response to a natural stressor such a predator odor, laboratory rats with exogenously elevated circulating corticosterone will increase defensive behaviors (Kalynchuk et al., 2004), although this may not always be the case (Rosen et al., 2008). Maternal corticosterone levels in garter snakes (Thamnophis elegans) can differentially affect antipredator behaviors of offspring depending on their life-history ecotype (Robert et al., 2009). But to our knowledge, no study has experimentally established a link between elevated circulating glucocorticoids in adult reptiles and their subsequent antipredator behaviors to a predator encounter.
If glucocorticoids are important for the expression of antipredator behaviors, then in individuals with different developmentally fixed strategies, elevating glucocorticoids could also differentially induce alternative antipredator behaviors. Within species, individuals can adopt different neuroendocrine and behavioral strategies to cope with stressful events, such that some individuals are proactive while others are reactive (Koolhaas et al., 1999, Korte et al., 2005). Much is known about the glucocorticoid profiles and responses of animals that express fixed alternative strategies (reviewed in Korte et al., 2005), but glucocorticoids are also involved in inducing the expression of condition-dependent tactics. For example, exogenously elevating circulating corticosterone levels in male toads (Bufo cognatus and B. woodhousi) increases the probability that they adopt a non-calling satellite tactic (Leary et al., 2006). Such could be the case in lizards with behavioral alternatives if elevated glucocorticoids induce differential behavioral responses regardless of the strategy of the individual.
Apart from the underlying behavioral strategy or circulating glucocorticoid level, body size of an individual can affect its vulnerability to predators. Increasing body size in reptiles is often associated with greater survivorship from predators (e.g. Blomberg and Shine, 2000, Janzen et al., 2000, Mushinsky and Miller, 1993, Shine et al., 2001, Tucker et al., 1999, Vitt, 2000). Furthermore, the body-size differences in locomotory performance, such as sprint speed and stamina, can also affect the risk of predation for smaller individuals (Webb, 1976, Garland and Losos, 1994, Carrier, 1996, Gerald, 2008; but see Irschick, 2000, Pinch and Claussen, 2003, Brecko et al., 2008 for a lack of size-dependent performance). Thus antipredator behaviors may also be a function of body size.
Here we examined the role of corticosterone in two aspects of the behavior of male ornate tree lizards (Urosaurus ornatus), a species with male alternative tactics. First, we tested the prediction that exogenously elevated corticosterone would enhance antipredator behavioral responses during an encounter with a predator, such that males with higher circulating corticosterone would be warier. Second, we examined the role that corticosterone plays in the expression of the behavioral differences between male tree lizard morphs. Male tree lizard color morphs express alternative reproductive (Moore et al., 1998) and antipredator behavioral tactics (Thaker et al., 2009) and may express alternative stress coping styles, involving, in part, different levels of wariness (see below for details). If the expression of differential wariness during a predator encounter is induced by the endogenous corticosterone response to such a stressor, then exogenously elevating corticosterone to similar levels among morphs should result in similar antipredator responses. However, if male tree lizard morphs express developmentally fixed antipredator alternative tactics, then in the simplest case, morph-specific antipredator responses should be expected even with similar circulating corticosterone levels. Finally, we also expected that the body size (snout–vent length, SVL) of an individual would affect antipredator responses, regardless of the endocrine treatment or morph type.
Section snippets
Alternative behavioral and hormonal tactics in male tree lizards
The ornate tree lizard is a small (4–6 g) iguanid lizard of the southwestern United States and northwestern Mexico. Throat coloration in U. ornatus varies geographically (Hews et al., 1997, Thompson and Moore, 1991a), and is a developmentally fixed polymorphism that is mediated by early organizational actions of steroid hormones (Moore et al., 1998). In our study population, at least 98% of the males can be categorized as one of three throat color morphs: 1) orange-blue (OB) males have an
Results
We found that the antipredator behavioral responses of male tree lizards varied as a function of their endocrine treatment (CORT-patch or Control-patch), morph color (OB, M, O), and body size.
Discussion
Our study found that elevating corticosterone in male tree lizard morphs did not alter the antipredator repertoire of males but did enhance their responsiveness to predators. In response to a staged encounter with a collared lizard predator, males with exogenously elevated corticosterone reacted more quickly, hid for a longer duration and displayed more towards the predator. Plasma testosterone levels were not obviously affected by the corticosterone manipulation and thus treatment differences
Acknowledgments
We thank B. Sullivan and Arizona State University-West for laboratory and enclosure space, and J. Macedonia for assistance in initially collecting C. nebrius. We also thank two anonymous reviewers for helpful comments on an earlier version of this manuscript. Funding for this project was provided to M. Thaker by the Indiana Academy of Sciences and by the School of Graduate Studies at Indiana State University.
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