Article

Stressed Snakes Strike First: Hormone Levels and Defensive Behavior in Free Ranging Cottonmouths (Agkistrodon piscivorus)

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Abstract

Stress is believed to be an important factor mediating animal behavior. Here we explore the relationship between concentrations of a stress hormone and defensive behavior of a snake. The cottonmouth (Agkistrodon piscivorus) is an abundant, large-bodied pitviper that is well known for its intense defensive behaviors. The defensive behaviors and hormonal ecology of cottonmouths have been studied extensively, but the interaction between these is not well understood. We conducted field trials, recording the snake’s behavior and obtaining blood samples to quantify plasma CORT concentrations, both upon first encountering a snake and after a 30 minute standardized confinement stressor. We found that snakes with elevated levels of baseline CORT at first encounter were more likely to strike than exhibit a threat display when approached in the field. However, this behavior was not related to the magnitude of the snake’s CORT increase following confinement, suggesting that more stress-prone snakes are not more defensive. Post-stressor antipredator behavior was also not related to any of our CORT measures. This study suggests that baseline CORT levels can be important correlates of defensive behavior. If this is a causative relationship, environmental challenges that increase baseline stress levels of populations may elevate cottonmouth defensive behavior. This would increase costs associated with defensive behavior (energetic, lost opportunity, etc.) and have important consequences for animal-human interactions.

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... Only two studies have examined the relationship between antipredator behavior and corticosterone in snakes, both using North American vipers. The tendency to strike in Cottonmouths (Agkistrodon piscivorus) increased with higher baseline levels of corticosterone, but striking did not increase with corticosterone in response to confinement (Herr et al. (2017). However, there was no relationship between antipredator behavior and corticosterone when Southern Pacific Rattlesnakes (Crotalus helleri) were treated with slow-release corticosterone implants (Claunch et al. (2017). ...
... This is the first study to explore the relationship between antipredator behavior and the steroid corticosterone response in pythons, expanding on previous work on garter snakes (Moore et al., 2000) and vipers (Claunch et al., 2017;Herr et al., 2017). In alignment with previous studies (Johnson, 1975;Greene, 1988;Herzog and Burghardt, 1986), our results support our first hypothesis that there are specieslevel differences in antipredator behavior (Table 1; Fig. 3). ...
... Although only a single data point, it is interesting that the single Children's Python that struck also had the highest corticosterone concentrations (Fig. 2). While Herr et al. (2017) found that cottonmouths (Agkistrodon piscivorus) with higher corticosterone concentrations were more likely to strike, Claunch et al. (2017) found no effect of corticosterone implants on antipredator behavior in male Pacific Rattlesnakes, although they did find a correlation with testosterone. ...
Article
It has long been known that even closely related species can vary in their antipredator behavior, and in the last two decades there has been mounting interest in how these differences might relate to the hormonal stress response. We tested the relationship between fear-based aggression, a form of antipredator behavior, and plasma corticosterone levels in three species of python [Children's Python (Antaresia childreni), Ball Python (Python regius), Bismarck Ring Python (Bothrochilus boa)]. We recorded the amount of striking in response to perturbation before and after a controlled, stressful confinement. We also measured plasma corticosterone levels prior to confinement, after confinement, and after confinement plus an adrenocorticotropin hormone (ACTH) injection, the later to induce a maximal corticosterone response. We performed among species analyses using two mixed models, and we determined between individual variance within each species to estimate repeatability. Bismarck Ring Pythons struck more than either Ball Pythons or Children's Pythons, and Ball Pythons had a suppressed corticosterone response compared to Children's and Bismarck Ring Pythons. Thus, mean species fear-based aggression correlated with species level differences in corticosterone profile. We also found evidence suggesting behaviors are repeatable within individuals. Our results point to a need for further exploration of aggression, anti-predator behavior, and corticosterone profile.
... We obtained blood samples from four reptile species: cottonmouth snakes (Agkistrodon piscivorus), western rattlesnakes (Crotalus oreganus), eastern fence lizards (Sceloporus undulatus), and northern Bahamian rock iguanas (Cyclura cychlura). Most animals were adults at the time of capture, as determined by size (cottonmouths and rattlesnakes: > 50 cm SVL; Herr et al., 2017; fence lizards: > 5 cm SVL; Angilletta et al., 2004; rock iguanas: > 18 cm SVL; Iverson and Mamula, 1989). Some cottonmouths (n = 6) and rattlesnakes (n = 6) were subadults at the time of capture. ...
... Each snake was then placed in a 5-gallon plastic bucket until 30 min (cottonmouths) or 60 min (rattlesnakes) had passed since the initial encounter with the snake, and a second blood sample was then taken. This protocol induces a significant increase in CORT concentrations (Herr et al., 2017). ...
... Given that steroid hormones are known to remain stable in plasma for decades when stored at −20°C (Stroud et al., 2007), we do not expect there to be any issues with prolonged sample storage. CORT concentrations of cottonmouths, rattlesnakes, and eastern fence lizards were measured using an enzyme immunoassay (Corticosterone High Sensitivity EIA Kits, Immunodiagnostic Systems (IDS) Inc., Scottsdale, AZ, USA) which has previously been validated for cottonmouths (Herr et al., 2017) and eastern fence lizards (Trompeter and Langkilde, 2011), and has a sensitivity limit of 0.17 ng/mL. Prior to testing the rattlesnake samples, we validated the immunoassay for this species by demonstrating parallelism of pooled sample dilution curves compared to a CORT control curve (provided in the kit) and achieving a 99.9% recovery rate of a CORT control sample added to a pooled sample of rattlesnake plasma. ...
Article
There is growing interest in the use of glucocorticoid (GC) hormones to understand how wild animals respond to environmental challenges. Blood is the best medium for obtaining information about recent GC levels; however, obtaining blood requires restraint and can therefore be stressful and affect GC levels. There is a delay in GCs entering blood, and it is assumed that blood obtained within 3 minutes of first disturbing an animal reflects a baseline level of GCs, based largely on studies of birds and mammals. Here we present data on the timing of changes in the principle reptile GC, corticosterone (CORT), in four reptile species for which blood was taken within a range of times 11 minutes or less after first disturbance. Changes in CORT were observed in cottonmouths (Agkistrodon piscivorus; 4 min after first disturbance), rattlesnakes (Crotalus oreganus; 2 min 30 sec), and rock iguanas (Cyclura cychlura; 2 min 44 sec), but fence lizards (Sceloporus undulatus) did not exhibit a change within their 10-minute sampling period. In both snake species, samples taken up to 3 to 7 minutes after CORT began to increase still had lower CORT concentrations than after exposure to a standard restraint stressor. The "3-minute rule" appears broadly applicable as a guide for avoiding increases in plasma CORT due to handling and sampling in reptiles, but the time period in which to obtain true baseline CORT may need to be shorter in some species (rattlesnakes, rock iguanas), and may be unnecessarily limiting for others (cottonmouths, fence lizards).
... A major caveat to using CORT as a metric for assessing population health is that the effects of high levels of CORT are not consistent across taxa (Cockrem, 2013), and their effects on organismal health are often assumed rather than measured. Knowledge of the effects of CORT on organismal survival, specifically in the context of defensive behavior against potential predators, is limited (Herr et al., 2017;Spencer et al., 2015;Thaker et al., 2010). There is an obvious need to evaluate the direct effects of CORT on traits influencing various aspects of fitness (Breuner et al., 2008), especially in the context of chronic CORT elevation, where sustained high CORT levels may have damaging effects (Baker et al., 2013). ...
... To investigate the effects of CORT on rattlesnake physiology and behavior, we implanted radio-telemetered male C. helleri with CORT-filled or blank implants and subsequently measured circulating CORT, testosterone (T), and defensive behaviors for 30 days post-implantation. If CORT plays a role in mediating traits related to survival and reproduction, then rattlesnakes implanted with CORT should have decreased T (Moore and Jessop, 2003;Jones and Bell, 2004;Wingfield and Sapolsky, 2003), increased defensive behavior (Herr et al., 2017), and an increase in both baseline and stress-induced CORT levels (Dupoué et al., 2013;Sykes and Klukowski, 2009). ...
... A recent study found that strike frequency of brown tree snakes (Boiga irregularis) increased in sites with frequent and longterm survey activity (Spencer et al., 2015), which may be related to stress or baseline CORT levels (although these were not directly assessed). To our knowledge, only one study has examined the relationship between CORT and defensive behavior in an ectotherm, finding a positive correlation between defensive behavior and baseline CORT in cottonmouths (Agkistrodon piscivorus), but not with acutely stressed CORT (Herr et al., 2017). Contradicting these results, our experimental elevation of baseline CORT in rattlesnakes had no effect on defensive behavior. ...
Article
In the face of global change, free-ranging organisms are expected to experience more unpredictable stressors. An understanding of how organisms with different life history strategies will respond to such changes is an integral part of biodiversity conservation. Corticosterone (CORT) levels are often used as metrics to assess the population health of wild vertebrates, despite the fact that the stress response and its effects on organismal function are highly variable. Our understanding of the stress response is primarily derived from studies on endotherms, leading to some contention on the effects of chronic stress across and within taxa. We assessed the behavioral and hormonal responses to experimentally elevated stress hormone levels in a free-ranging, arid-adapted ectotherm, the Southern Pacific rattlesnake (Crotalus helleri). Plasma CORT was significantly elevated in CORT-implanted snakes 15 days after implantation. Implantation with CORT did not affect testosterone (T) levels or defensive behavior. Interestingly, we observed increased defensive behavior in snakes with more stable daily body temperatures and in snakes with higher plasma T during handling (tubing). Regardless of treatment group, those individuals with lower baseline CORT levels and higher body temperatures tended to exhibit greater increases in CORT levels following a standardized stressor. These results suggest that CORT may not mediate physiological and behavioral trait expression in arid-adapted ectotherms such as rattlesnakes.
... While high levels of corticosterone play a primary role in energy mobilization in mammals, it is unclear how high levels impact reptiles, as their energetic demands are very different [72,73]. Some species may maintain higher baseline corticosterone concentrations in predator rich environments [74,75], preparing the animal for necessary antipredator behaviors [76]. Furthermore, corticosterone levels may play a role in mediating life history trade-offs. ...
... Some studies have shown that elevated corticosterone levels are associated with changes in reptile behavior [76,82,83]. In our study, there was no correlation between the behaviors observed and FGM concentrations. ...
Article
Modern herpetoculture has seen a rise in welfare-related habitat modifications, although ethologically-informed enclosure design and evidence-based husbandry are lacking. The diversity that exists within snakes complicates standardizing snake welfare assessment tools and evaluation techniques. Utilizing behavioral indicators in conjunction with physiological measures, such as fecal glucocorticoid metabolite concentrations, could aid in the validation of evidence-based metrics for evaluating snake welfare. We increased habitat cleaning, to identify behavioral or physiological indicators that might indicate heightened arousal in snakes as a response to the disturbance. While glucocorticoid metabolite concentrations increased significantly during a period of increased disturbance, this increase was not associated with a significant increase in tongue-flicking, a behavior previously associated with arousal in snakes. Locomotion behavior and the proportion of time spent exposed were also not affected by more frequent habitat cleaning. These results demonstrate the need to further investigate the behavioral and physiological responses of snakes to different aspects of animal care at a species and individual level. They also highlight the need to collect baseline behavioral and physiological data for animals, in order to make meaningful comparisons when evaluating changes in animal care.
... While high levels of corticosterone play a primary role in energy mobilization in mammals, it is unclear how high levels impact reptiles, as their energetic demands are very different [72,73]. Some species may maintain higher baseline corticosterone concentrations in predator rich environments [74,75], preparing the animal for necessary antipredator behaviors [76]. Furthermore, corticosterone levels may play a role in mediating life history trade-offs. ...
... Some studies have shown that elevated corticosterone levels are associated with changes in reptile behavior [76,82,83]. In our study, there was no correlation between the behaviors observed and FGM concentrations. ...
Article
Full-text available
Modern herpetoculture has seen a rise in welfare-related habitat modifications, although ethologically-informed enclosure design and evidence-based husbandry are lacking. The diversity that exists within snakes complicates standardizing snake welfare assessment tools and evaluation techniques. Utilizing behavioral indicators in conjunction with physiological measures, such as fecal glucocorticoid metabolite concentrations, could aid in the validation of evidence-based metrics for evaluating snake welfare. We increased habitat cleaning, to identify behavioral or physiological indicators that might indicate heightened arousal in snakes as a response to the disturbance. While glucocorticoid metabolite concentrations increased significantly during a period of increased disturbance, this increase was not associated with a significant increase in tongue-flicking, a behavior previously associated with arousal in snakes. Locomotion behavior and the proportion of time spent exposed were also not affected by more frequent habitat cleaning. These results demonstrate the need to further investigate the behavioral and physiological responses of snakes to different aspects of animal care at a species and individual level. They also highlight the need to collect baseline behavioral and physiological data for animals, in order to make meaningful comparisons when evaluating changes in animal care.
... Different cohorts exploit different ecological niches and thus experience different types of stressors (Shine 1991;Forsman 1995;Vincent et al. 2004;Isaac and Gregory 2013). The impact of stressors on chronic and acute stress responses has been studied in captive snakes (Schuett et al. 2004;Bonnet et al. 2013;Dupoué et al. 2014;Cusaac et al. 2016;Claunch et al. 2017;Van Waeyenberge et al. 2018) and in several species in natural conditions (Moore et al. 2000;Fauvel et al. 2012;Palacios et al. 2012;Holding et al. 2014;Owen et al. 2014;Herr et al. 2017;Bonnet et al. 2020). However, possible differences of stress response among groups, within or among populations, have rarely been investigated. ...
... To obtain basal levels, we minimized the time elapsed since the detection of a given snake until blood was actually retrieved (Herr et al. 2017). Snakes were detected from a short distance and expeditiously and carefully seized by hand. ...
Article
Theoretically, animals integrate intrinsic and extrinsic factors to respond appropriately to the wide range of stressors they encounter during their life span. We examined how stress response varies between sexes and among morphotypes in wild dice snakes (Natrix tessellata). We also considered reproductive and feeding status and antipredator behavior. We used two indicators of stress (glucose [GLUC] and corticosterone [CORT] levels) at eight sampling time intervals (immediately after capture, up to 17 h after) and a large sample size ( N = 113 snakes). Concentrations of both markers increased sharply after capture (an equivalent of predation). This acute phase occurred earlier for GLUC (30 min) compared to CORT (60 min). Then the values plateaued to very high levels without decline over time, indicating prolonged saturation of the hypothalamus-pituitary-adrenal axis. In contrast to our expectations, we found no effect of sex, morphotype, or reproductive status. Yet the CORT stress response of those individuals displaying death-feigning (DF) antipredator behavior was attenuated compared to those that did not. Low stress hormones levels may facilitate the expression of DF (high levels supporting fleeing behavior). The presence of partially digested material in the stomach was associated with higher blood GLUC during the plateau. Assaying blood GLUC requires very little blood but was as good as CORT at gauging acute stress response. The prolonged plateau suggests that captivity should be minimized during field studies.
... However, we found a positive inter-specific correlation between FID and baseline CORT. This coincides with findings at the individual level in, for example, tree lizards and cottonmouth snakes (Thaker et al., 2009;Herr et al., 2017), showing that pre-stress circulating CORT levels enhance antipredator behavioral responses through the preparatory effects of corticosterone. ...
Article
Understanding how vulnerable species are to new stressors, such as anthropogenic changes, is crucial for mitigating their potential negative consequences. Many studies have investigated species sensitivity to human disturbance by focusing on single behavioral or physiological parameters, such as flight initiation distance and glucocorticoid levels. However, little is known about the differential effect that modulating factors might have on behavioral versus physiological stress responses across species. This lack of knowledge make difficult to understand the relationship between both types of reactions, and thus to assess to what extent a behavioral reaction is representative of an internal physiological stress response or vice versa. We collected published data on bird flight initiation distances (FID) and corticosterone (CORT) responses, the two most frequently used indicators of stress reaction. We then investigated how spatio-temporal factors or species-specific characteristics relate to these behavioral and physiological stress responses, and potentially modify the relationship between them. Additionally, we evaluated the strength of the correlation between the two stress responses (behavioral and physiological). Our findings showed that FID and CORT responses were poorly correlated across species, and the lack of correlation was attributable to modulating factors (e.g. latitude and body mass) which influence behavior and physiology differently. These modulating factors, therefore, should be taken into consideration to better interpret FID and CORT responses in the context of species vulnerability to stress.
... Long-distance translocation of snakes from urban and rural environments to less-disturbed areas generally provides people with a good moral feeling (compared to the negative stigma associated with killing the snake); however, it often results in poor snake health and survival (Barve et al., 2013;Butler et al., 2005;Devan-Song et al., 2016). Furthermore, snakes are more likely to elevate defensive behaviours and bite when experiencing higher baseline stress levels (Herr, Graham, & Langkilde, 2017), which requires further study within the context of snakebite management and conflict. Snakes translocated to natural areas outside of their home ranges still sometimes move into surrounding human settlements (Butler et al., 2005), which also requires further investigation as to whether that represents an increase in risk for potential snakebite and conflict within human populated areas near to the receiving natural areas. ...
Article
Full-text available
1. Snakebite, which was reclassified as a neglected tropical disease by the World Health Organization in 2017, afflicts at least 1.8-2.7 million people worldwide each year. Understanding the habits of medically significant snakes can help us better construct preventative measures which reduce snake-human conflicts and snakebite. 2. As a case study, using radio-telemetry, we monitored a single focal Bungarus candidus individual for 102 days within a suburban landscape (a university dormitory complex) in Nakhon Ratchasima, Thailand. 3. Daily location checks revealed the telemetered snake sheltered within human settlement habitat 75% of the time it was tracked, where we also documented active foraging , a predation event and interactions with humans. 4. Despite being captured and relocated to an adjacent forest on two occasions, the focal animal promptly returned to the dormitories. Translocation as a management tool requires meaningful discussion at the local level and further study, considering the costs and potential limitations for effectiveness. 5. This case study provides brief insight into the ecology and behaviour of one of Asia's most medically significant snake species and highlights challenges current conflict management practices face locally. Our observations appear to lend credibility to preventative measures such as increasing awareness, encouraging the use of flashlights and carefully maintaining buildings so that snakes cannot enter through crevices or plumbing. Snake-human conflict prevention and mitigation techniques require further evaluation to determine the effectiveness of prescribed management methods.
... Generally, reptiles often exhibit stress responses to handling and captivity (Franklin et al., 2003;Moore et al., 1991;Schuett et al., 2004). Many studies have confirmed that blood levels of corticosterone increase after capture and confinement in several snake species (Bailey et al., 2009;Dayger et al., 2013;Herr et al., 2017;Mathies et al., 2001;Schuett et al., 2004;Sykes & Klukowski, 2009). ...
Article
Hertz et al. (1993) designed what is now the most widely used protocol to analyse the thermal strategies and efficiency of small squamates. Preferred temperature range (Tp) is one of the most important variables required for determining the thermal efficiency index, and is calculated by monitoring the body temperature of the individuals in an enclosure containing a thermal gradient. Although thermoregulation studies of lizards have traditionally employed thermal gradients under laboratory conditions, this approach is not suitable for snakes given that such thermal gradients do not accurately represent their natural thermal environment and thus may result in snakes selecting suboptimal temperatures. Here, we compare the results of this thermal efficiency protocol using a laboratory thermal gradient (LG) and a semi-captivity thermal gradient (SCG) in the rattlesnake Crotalus polystictus. We found traces of seasonal variation in the SCG Tp, but this could not be assessed in the LG. Tp from the LG was much higher (29 – 34.3 °C) than from the SCG (22.5-30.9 °C). Values for the accuracy of thermoregulation (db) and thermal quality of the environment (de) indices from the LG were consistently higher than from the SCG. However, the efficiency of thermoregulation (E) was higher when calculated from the SCG. Tp estimates were wider than most that have been obtained from other snake species, suggesting that C. polystictus is eurythermic. The Blowin Demers and Weatherhead index was nearly identical in both gradients. Results from the LG indicated that C. polystictus is an inaccurate and inefficient thermoregulator, due to the higher temperatures chosen in this environment. In contrast, results from the SCG suggested that it is a highly accurate and active thermoregulator. We suggest that the LG could represent a stressful environment for snakes, and, as a consequence, they might select higher temperatures to increase anti-predatory performance at the expense of less efficient thermoregulation. Generally, a thermal gradient that more accurately replicates the natural habitat of snake species should reduce stress and result in more robust estimates of thermoregulatory variables.
... In some studies, Eastern Fence Lizards responded significantly to handling confinement lasting 30 minutes (Graham et al. 2012), whereas others required a minimum of one hour (Dunlap, 1995;Dunlap and Wingfield 1995). Many other species of reptiles and birds sampled during the breeding season quickly respond to handling stress, typically demonstrating elevated corticosterone after 30-60 minutes of handling time (Moore et al. 1991;Romero and Wingfield 1998;Schuett et al. 2004;Romero et al. 2006;Herr et al. 2017), and some species do not respond at all (Cree et al. 2000). Our results provide some evidence that thirty minutes of handling time may not have been sufficient to induce increased plasma corticosterone during the breeding season in male Eastern Fence Lizards. ...
Article
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Landscape disturbances can alter habitat structure and resource availability, often inducing physiological responses by organisms to cope with the changing conditions. Quantifying the endocrine stress response through measurement of glucocorticoids has become an increasingly common method for determining how organisms physiologically respond to challenges imposed by their environment. We tested the hypothesis that Eastern Fence Lizards cope with fire disturbance effects by modulating their secretion of corticosterone (CORT). We measured the baseline and stress-induced plasma corticosterone of male Eastern Fence Lizards in a chronosequence of fire-altered habitats (recently burned, recovering from burn, and unburned). Although habitat use by lizards differed among burn treatments, including differences in use of canopy cover, leaf litter, and vegetation composition, we did not detect a significant effect of fire-induced habitat alteration on plasma CORT concentration or on body condition. Additionally, we found no effect of blood draw treatment (baseline or stress-induced), body temperature, body condition, or time taken to collect blood samples on concentration of plasma CORT. Low intensity burns, which are typical of prescribed fire, may not be a sufficient stressor to alter CORT secretion in Eastern Fence Lizards (at least during the breeding season). Instead, lizards may avoid allostatic overload using behavioral responses and by selecting microsites within their environment that permit thermoregulatory opportunities necessary for optimal performance and energy assimilation.
... For example, mate choice and competition trials frequently involve experimentally pairing and separating animals from mates at trial conclusion (e.g., Chen & Lu, 2011;Cheong et al., 2008;Friesen et al., 2014;Shine, Webb, Lane, & Mason, 2006). Studies focused on learning and behavioral responses to predation can include the need for repeated recapture of test subjects (e.g., Brust, Wuerz, & Krüger, 2013;Herr, Graham, & Langkilde, 2017;Langkilde, 2010). ...
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Minimizing disturbance of study animals is a major consideration in ethological and ecological research design. One nearly universal type of disturbance is the handling of study animals as a component of trial setup. Even low to moderate levels of handling can be a substantial stressor to study animals, which may negatively affect their offspring via maternal effects. Understanding how routine human handling and manipulation may affect the outcome of research studies is therefore critical for interpreting study outcomes. We tested whether repeatedly handling and manipulating (i.e., manually disengaging) amplexed pairs of wood frogs (Rana sylvatica [Lithobates sylvaticus]), which have an explosive breeding season, would affect their reproductive output and offspring fitness. Handling and manipulation did not alter any parameter that we measured: reproductive timing, hatching success, and offspring larval duration, survival, and size at metamorphosis. These results suggest that handling and manipulation by researchers may have a negligible effect on wood frog reproduction and offspring fitness. It is possible that many species that are commonly used in reproductive studies because they suppress behavioral and physiological responses during the mating season are likewise unaffected by human handling. Nevertheless, researchers should examine possible consequences of methodological interventions on their study species in order to determine any potential influence on their results. Having a broad understanding of these effects on species that have robust or dampened stress responsiveness during the breeding season would be useful for making generalizations about potential effects.
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Using venom for predation often leads to the evolution of resistance in prey. Understanding individual variation in venom resistance is key to unlocking basic mechanisms by which antagonistic coevolution can sustain variation in traits under selection. For prey, the opposing challenges of predator avoidance and resource acquisition often lead to correlated levels of risk and reward, which in turn can favor suites of integrated morphological, physiological and behavioral traits. We investigate the relationship between risk-sensitive behaviors, physiological resistance to rattlesnake venom, and stress in a population of California ground squirrels. For the same individuals, we quantified foraging decisions in the presence of snake predators, fecal corticosterone metabolites (a measure of "stress"), and blood serum inhibition of venom enzymatic activity (a measure of venom resistance). Individual responses to snakes were repeatable for three measures of risk-sensitive behavior, indicating that some individuals were consistently risk-averse whereas others were risk tolerant. Venom resistance was lower in squirrels with higher glucocorticoid levels and poorer body condition. Whereas resistance failed to predict proximity to and interactions with snake predators, individuals with higher glucocorticoid levels and in lower body condition waited the longest to feed when near a snake. We compared alternative structural equation models to evaluate alternative hypotheses for the relationships among stress, venom resistance, and behavior. We found support for stress as a shared physiological correlate that independently lowers venom resistance and leads to squirrels that wait longer to feed in the presence of a snake, whereas we did not find evidence that resistance directly facilitates latency to forage. Our findings suggest that stress may help less-resistant squirrels avoid a deadly snakebite, but also reduces feeding opportunities. The combined lethal and non-lethal effects of stressors in predator-prey interactions simultaneously impact multiple key traits in this system, making environmental stress a potential contributor to geographic variation in trait expression of toxic predators and resistant prey. Key Contribution: Even through prey resistance to predator venom is often the result of a coevolutionary relationship, few studies have examined whether such resistance forms an integrated phenotype with other prey traits. Here, we show that stress and body condition modulate venom resistance and a measure of boldness in ground squirrels preyed upon by venomous rattlesnakes. Stress may explain some population variation in venom resistance and provide a route to variable outcomes of coevolution.
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In amphibians, as in other vertebrates, exposure to stressors triggers an increase in plasma glucocorticoids. Glucocorticoids are believed to mediate behavioral transitions critical to coping with stressors. A common amphibian behavioral response to a variety of different stressors is inactivity. With a series of experiments, we tested the hypothesis that stress-induced decreases in locomotory activity are mediated by the glucocorticoid hormone, corticosterone (CORT). With the use of a plethodontid salamander (Red-legged Salamander, Plethodon shermani), we demonstrated that handling, a stressor, resulted in decreased locomotory activity. Next, subjects were treated with a dermal patch containing either oil vehicle or CORT. The amount of CORT used was chosen to elevate plasma CORT acutely to physiologically relevant levels relative to treatment with oil patches. Activity was measured in response to different amounts of CORT, at different times after CORT exposure, and in the presence of different chemosensory cues. One experiment also included treatment with the glucocorticoid receptor blocker, mifepristone. Although handling resulted in reduced activity, we could discern no effect of acute elevations of CORT on activity. These results suggest that acute stress-induced changes in locomotory activity are not mediated by CORT in Red-legged Salamanders.
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Translocation, a management and conservation strategy used commonly in which animals are moved from their sites of origin to other localities, has proven controversial. We examined the physiological and behavioral impacts of repeated handling and short-distance translocation on rattlesnakes, which are often translocated from areas of human use because of a perceived threat to people. Northern Pacific Rattlesnakes (Crotalus oreganus oreganus) were radiotracked for 2 months, during which time one of three treatments was imposed weekly: translocation, walk and release at that day's capture site (handling control), and undisturbed control. At both the beginning (spring) and the end (summer) of the study, blood samples were obtained before and after an acute handling stressor, and plasma concentrations of corticosterone (CORT) and testosterone (T) were determined. All rattlesnakes showed a CORT stress response, but baseline and stressed concentrations of neither hormone were affected by either translocation or handling. However, the response of both hormones to stress differed between spring and summer, with a greater increase in CORT and a detectable decrease in T occurring in summer. Activity range size was affected by translocation, whereas no effects on snake behaviors recorded during observer approach were detected. Rattlesnakes appear quite resilient to the potential impacts of frequent handling or short-distance translocation.
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The rapid increase of human activity in wild and developed areas presents novel challenges for wildlife. Some species may use human-dominated landscapes because of favourable resources (e.g. high prey availability along roadsides); however, use of these areas may increase exposure to anthropogenic stressors, such as human disturbance or noise, which can negatively affect reproduction or survival. In this case, human-dominated landscapes may act as an ecological trap.We evaluated whether American kestrel Falco sparverius reproductive failure was associated with human disturbance (traffic conditions and land development) or other common predictors of reproductive outcome, such as habitat and clutch initiation date. Also, we examined relationships among human disturbance, corticosterone (CORT) concentrations and nest abandonment to explore potential mechanisms for stress-induced reproductive failure.Twenty-six (36%) of 73 kestrel nesting attempts failed and 88% of failures occurred during incubation. Kestrels nesting in higher disturbance areas were 9·9 times more likely to fail than kestrels nesting in lower disturbance areas. Habitat and clutch initiation date did not explain reproductive outcome.Females in higher disturbance areas had higher CORT and were more likely to abandon nests than females in lower disturbance areas. There was no relationship between male CORT and disturbance or abandonment. Females spent more time incubating than males and may have had more exposure to anthropogenic stressors. Specifically, traffic noise may affect a cavity-nesting bird's perception of the outside environment by masking auditory cues. In response, incubating birds may perceive a greater predation risk, increase vigilance behaviour, decrease parental care, or both.Synthesis and applications. Proximity to large, busy roads and developed areas negatively affected kestrel reproduction by causing increased stress hormones that promoted nest abandonment. These results demonstrate that species presence in a human-dominated landscape does not necessarily indicate a tolerance for anthropogenic stressors. Managers should carefully consider or discourage projects that juxtapose favourable habitat conditions with areas of high human activity to decrease risk of ecological traps. Noise mitigation, while locally effective, may not protect widespread populations from the pervasive threat of traffic noise. Innovative engineering that decreases anthropogenic noise at its source is necessary.
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Predators often induce shifts in the traits of nearby prey, and these trait shifts are important in mediating a variety of evolutionary and ecological processes. However, little is known about the spatial and temporal scales over which predators induce trait shifts. We empirically determined the spatial scale of predator avoidance by measuring the habitat use and growth rates of snails (Physa acuta) held at varying distances from a caged pumpkinseed sunfish (Lepomis gibbosus). Refuge use was highest near the fish and gradually decayed to background level, with a characteristic response range of 1.0 m. Snail growth rates were negligible near the predator but increased with greater separation from fish. The dependence of behavior on the age of chemical cues was measured in a mesocosm experiment in which water was withdrawn from a tank holding pumpkinseeds and held for varying lengths of time before being added to experimental mesocosms with snails. Fresh cues elicited the strongest habitat shifts relative to well-water controls, and avoidance behavior decayed in an exponential manner with increasing cue age. The characteristic lifetime of avoidance behavior was 41 h. Taken together, these results allow us to begin to describe the behavioral landscape created by mobile predators.
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The way of life of amphibians and reptiles, in contrast to that of birds and mammals, is based on low energy flow. Many of the morphological and physiological characteristics of ectothermal tetrapods that are normally considered to be primitive are in fact adaptations that facilitate a life of low energy demand. Their modest energy requirements allow amphibians and reptiles to exploit various adaptive zones unavailable to birds and mammals. Small body size is the most important of these; 80% of all lizard species and 90% of salamanders have adult body masses less than those of small birds and mammals. An elongate body form, a widespread and successful morphotype among amphibians and reptiles, is energetically unfeasible for endotherms. Amphibians and reptiles also are better suited than birds and mammals to ecological situations characterized by periodic shortages of food, water, or oxygen. At the ecosystem level, the most important consequence of the low energy requirements of amphibians and reptiles is their efficiency of biomass production, which greatly exceeds that of birds and mammals. Their secondary production makes amphibians and reptiles as important as birds or mammals in terrestrial ecosystems.
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How foragers balance risks during foraging is a central focus of optimal foraging studies. While diverse theoretical and empirical work has revealed how foragers should and do manage food and safety from predators, little attention has been given to the risks posed by dangerous prey. This is a potentially important oversight because risk of injury can give rise to foraging costs similar to those arising from the risk of predation, and with similar consequences. Here, we synthesize the literature on how foragers manage risks associated with dangerous prey and adapt previous theory to make the first steps towards a framework for future studies. Though rarely documented, it appears that in some systems predators are frequently injured while hunting and risk of injury can be an important foraging cost. Fitness costs of foraging injuries, which can be fatal, likely vary widely but have rarely been studied and should be the subject of future research. Like other types of risk-taking behaviour, it appears that there is individual variation in the willingness to take risks, which can be driven by social factors, experience and foraging abilities, or differences in body condition. Because of ongoing modifications to natural communities, including changes in prey availability and relative abundance as well as the introduction of potentially dangerous prey to numerous ecosystems, understanding the prevalence and consequences of hunting dangerous prey should be a priority for behavioural ecologists.
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Warning displays are defined as signals designed to intimidate predators or indicate a proclivity to fight. However, support for the idea that warning behaviors signal an intent to fight is largely based on anecdotes and isolated observations, and a complete understanding of antipredator behavior will only be achieved if specific hypotheses are experimentally tested. Herein, we tested in a North American viperid snake, the cottonmouth (Agkistrodon piscivorus (Lacepede, 1789)), the hypothesis that warning displays serve as a reliable signal to potential predators that a snake will strike. The cottonmouth exhibits two stereotypical warning displays during predator confrontation, i.e., mouth gaping and tail vibrations, making it an ideal study organism to experimentally test the relationship between warning displays and defensive striking. To test this idea, we recorded the sequence of defensive behavior - gaping, tail vibrating, and striking - of cottonmouths towards a standardized predatory stimulus in the laboratory. As predicted, snakes that gaped during the trials were subsequently more likely to strike than snakes that did not. In contrast, striking behavior was independent of the occurrence of tail vibrations. Our results suggest that gaping behavior - but not tail-vibrating behavior - may provide an honest signal to would-be predators.
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The migratory and foraging behavior of individually marked bighorn ewes (Ovis canadensis) was studied to test the hypothesis that forage quality determined seasonal range selection. Forage quality was monitored through analysis of fecal crude protein. Ewes in the study population utilized two distinct ranges differing in elevation and possibly predation risk. Pregnant ewes migrated in May from the low-elevation winter range to lambing areas at higher elevation, before plant growth had started there. In so doing, they moved from a range of high-quality forage to one of low-quality forage, apparently to avoid predation on newborn lambs. Non-pregnant adult ewes migrated later. Most yearling ewes (which are not pregnant) migrated with the adult ewes to the lambing areas, but returned to the winter range within a few days, then migrated again to high-elevation areas in June. Forage quality was higher at high elevation from mid-June at least through July, but forage availability appeared to be lower than in the winter range. Seasonal range selection is likely determined by a combination of nutritional and antipredator constraints. The antipredator strategy of bighorn ewes does not always allow them to utilize the range with the best forage.
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Predation is a central organizing process affecting populations and communities. Traditionally, ecologists have focused on the direct effects of predation--the killing of prey. However, predators also have significant sublethal effects on prey populations. We investigated how fluctuating predation risk affected the stress physiology of a cyclic population of snowshoe hares (Lepus americanus) in the Yukon, finding that they are extremely sensitive to the fluctuating risk of predation. In years of high predator numbers, hares had greater plasma cortisol levels at capture, greater fecal cortisol metabolite levels, a greater plasma cortisol response to a hormone challenge, a greater ability to mobilize energy and poorer body condition. These indices of stress had the same pattern within years, during the winter and over the breeding season when the hare:lynx ratio was lowest and the food availability the worst. Previously we have shown that predator-induced maternal stress lowers reproduction and compromises offspring's stress axis. We propose that predator-induced changes in hare stress physiology affect their demography through negative impacts on reproduction and that the low phase of cyclic populations may be the result of predator-induced maternal stress reducing the fitness of progeny. The hare population cycle has far reaching ramifications on predators, alternate prey, and vegetation. Thus, predation is the predominant organizing process for much of the North American boreal forest community, with its indirect signature--stress in hares--producing a pattern of hormonal changes that provides a sensitive reflection of fluctuating predator pressure that may have long-term demographic consequences.
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Animals may exhibit a variety of defensive behaviors in the presence of indirect predator cues. Such behavior offers immediate fitness benefits but may also incur substantial foraging and reproductive costs. We measured shifts in space use (vertical climbing) by the wolf spider Pardosa milvina induced by chemotactile cues (silk and excreta) from a co-occurring predatory wolf spider Hogna helluo. We then measured foraging and reproductive costs, as well as survival benefits, of this behavior. For 2 weeks, we maintained mated adult female Pardosa in plastic containers with one of three treated peat moss substrates: a container previously occupied by a conspecific for 3 days, a container previously occupied by an adult Hogna for 3 days, and a container devoid of either cue (control). We measured prey capture efficiency, body condition, egg sac production, egg sac weight, and egg number for individuals in each treatment. We also counted the number of Pardosa that survived and exhibited climbing behavior in the presence of a live Hogna with and without silk and excreta cues. Pardosa climbed container walls significantly more often in the presence of Hogna silk and excreta relative to other treatments. Pardosa exposed to Hogna cues coupled with live Hogna survived significantly longer than spiders that had no predator cues available. Pardosa placed in containers with Hogna cues, but no Hogna, lost weight more quickly, ate fewer prey, were in poorer body condition, produced lighter egg sacs, and produced fewer eggs than spiders in control or conspecific treatments. Copyright 2002.
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Elevated plasma corticosterone during stressful events is linked to rapid changes in behavior in vertebrates and can mediate learning and memory consolidation. We tested the importance of acute corticosterone elevation in aversive learning of a novel stressor by wild male eastern fence lizards (Sceloporus undulatus). We found that inhibiting corticosterone elevation (using metyrapone, a corticosterone synthesis blocker) during an encounter with a novel attacker impaired immediate escape responses and limited learning and recall during future encounters. In the wild and in outdoor enclosures, lizards whose acute corticosterone response was blocked by an earlier metyrapone injection did not alter their escape behavior during repeated encounters with the attacker. Control-injected (unblocked) lizards, however, progressively increased flight initiation distance and decreased hiding duration during subsequent encounters. Aversive responses were also initially higher for control lizards exposed to a higher intensity first attack. Further, we demonstrate a role of corticosterone elevation in recollection, since unblocked lizards had heightened antipredator responses 24-28 h later. Exogenously restoring corticosterone levels in metyrapone-injected lizards maintained aversive behaviors and learning at control (unblocked) levels. We suggest that the corticosterone mediation of antipredator behaviors and aversive learning is a critical and general mechanism for the behavioral flexibility of vertebrate prey.
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Baseline glucocorticoid (cort) levels are increasingly employed as physiological indices of the relative condition or health of individuals and populations. Often, high cort levels are assumed to indicate an individual or population in poor condition and with low relative fitness (the Cort-Fitness Hypothesis). We review empirical support for this assumption, and find that variation in levels of baseline cort is positively, negatively, or non-significantly related to estimates of fitness. These relationships between levels of baseline cort and fitness can vary within populations and can even shift within individuals at different times in their life history. Overall, baseline cort can predict the relative fitness of individuals and populations, but the relationship is not always consistent or present.
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Snake bite is a well-known occupational hazard amongst farmers, plantation workers, and other outdoor workers and results in much morbidity and mortality throughout the world. This occupational hazard is no more an issue restricted to a particular part of the world; it has become a global issue. Accurate statistics of the incidence of snakebite and its morbidity and mortality throughout the world does not exist; however, it is certain to be higher than what is reported. This is because even today most of the victims initially approach traditional healers for treatment and many are not even registered in the hospital. Hence, registering such patients is an important goal if we are to have accurate statistics and reduce the morbidity and mortality due to snakebite. World Health Organization/South East Asian Region Organisation (WHO/SEARO) has published guidelines, specific for the South East Asian region, for the clinical management of snakebites. The same guidelines may be applied for managing snakebite patients in other parts of the world also, since no other professional body has come up with any other evidence-based guidelines. In this article we highlight the incidence and clinical features of different types of snakebite and the management guidelines as per the WHO/SEARO recommendation.
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The use of the "arms race" analogy as a conceptualization of evolutionary predator-prey interactions has been criticized because of the lack of evidence that predators can and do adapt to increased antipredator ability of prey. We present evidence that the garter snake Thamnophis sirtalis has evolved resistance to tetrodotoxin (TTX) in response to the toxicity of the newt Taricha granulosa on which the snake feeds. A bioassay (locomotor performance before and after injection of TTX) was used to obtain repeated measures of resistance for individual snakes. We studied interpopulation and interspecific variation by comparing resistance in Thamnophis sirtalis from populations occurring sympatrically and allopatrically with Taricha granulosa, and in Thamnophis ordinoides (which does not feed on the newt) occurring sympatrically with Taricha granulosa. We also examined intrapopulation variation in TTX resistance using snakes from a population known to feed on Taricha granulosa. Resistance differed significantly among individuals and litters; repeatability and heritability estimates of the assay were significantly different from zero, demonstrating the potential for response to selection. The population of Thamnophis sirtalis that occurs with Taricha granulosa exhibited levels of resistance much greater than either of the other groups. These results suggest that the predator-prey arms race analogy may be applicable to this system.
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The use of the "arms race" analogy as a conceptualization of evolutionary predatorprey interactions has been criticized because of the lack of evidence that predators can and do adapt to increased antipredator ability of prey. We present evidence that the garter snake Thamnophis sirtalis has evolved resistance to tetrodotoxin (TTX) in response to the toxicity of the newt Taricha granulosa on which the snake feeds. A bioassay (locomotor performance before and after injection of TTX) was used to obtain repeated measures of resistance for individual snakes. We studied interpopulation and interspecific variation by comparing resistance in Thamnophis sirtalis from populations occurring sympatrically and allopatrically with Taricha granulosa, and in Thamnophis ordinoides (which does not feed on the newt) occurring sympatrically with Taricha granulosa. We also examined intrapopulation variation in TTX resistance using snakes from a population known to feed on Taricha granulosa. Resistance differed significantly among individuals and litters; repeatability and heritability estimates of the assay were significantly different from zero, demonstrating the potential for response to selection. The population of Thamnophis sirtalis that occurs with Taricha granulosa exhibited levels of resistance much greater than either of the other groups. These results suggest that the predator-prey arms race analogy may be applicable to this system.
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Non-native species introductions are becoming increasingly common, and can impose novel threats to the native communities they invade. Populations exposed to such environmental perturbations often exhibit elevated physiological stress levels including increased levels of circulating glucocorticoids, such as corticosterone (CORT). Red imported fire ants, Solenopsis invicta, are a globally important invader. Native fence lizards, Sceloporus undulatus, have developed behavioral strategies to mitigate potentially lethal impacts of frequent attack by these predatory ants. We conducted staged encounters between fence lizards and fire ants in the field to assess the role that physiological stress levels and prior exposure to this invader plays in driving lizard escape behavior. This study reveals that both population-level exposure to fire ants, and the physiological stress response to ant attack, affect the behavioral response of lizards. Lizards from fire ant invaded areas are more likely to adaptively respond to fire ant attack than lizards from uninvaded sites. Lizards from both sites exhibit elevated levels of CORT following attack by fire ants, and by experimentally elevating lizard CORT levels we were able to trigger a survival-inducing behavioral response to fire ant attack. Elevated CORT levels can have important consequences for populations, including suppressing immune function, growth and reproduction. However, our study suggests that this physiological stress response to invaders may permit native species to survive initial invasion by promoting an adaptive behavior response to this novel threat (supported by NSF grant DEB-0949483 to TL).
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1. Rapid, effective and enduring responses of physiology and behaviour to perturbations of the environment are key to robustness of an organism (ability to resist perturbations) and resilience (ability to resist and recover quickly from perturbations) so that the normal life cycle can be resumed quickly. 2. Perturbations of the environment can be labile (i.e. eventually subside) or permanent such as when human activity changes the environment in the long term, for example, deforestation, urbanization, etc. 3. Hormonal responses to labile perturbation factors (LPFs) allow organisms to cope during the perturbation and then return to the normal life cycle. These hormonal responses are called stress responses especially in cases when major changes in physiology and behaviour occur (emergency life-history stage). 4. Permanent perturbations require more than just temporary acclimation resulting in changes in range, adaptation or in some cases local extinction. Perturbations can be abiotic, biotic and social, but these are not mutually exclusive. 5. Here I focus on the effects of abiotic perturbation factors and their effects on the hypothalamo-pituitary—adrenal/interrenal axis in vertebrates. There is a great need for more field investigations of responses of free-living populations to perturbations of the environment, especially now that it appears the frequency and intensity of these events is increasing. However, such studies will require a high degree of opportunism on the part of the investigators to take advantage of unpredictable events when they occur.
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Crotaline snakes (family Viperidae, subfamily Crotalinae) are unique among snakes in the pos-session of facial pits situated on each side of the head between the nostril and the eye (Klauber, 1972). These organs are depressions with highly innervated membranes at their bases that have a heat-sensing function and that transmit informa-tion to the part of the brain that receives visual data (Desmoulins, 1824; Bullock and Diecke, 1956; Barrett, 1970; Hartline et al., 1978). Thus, pitvipers can detect temperatures through the radiant heat energy emitted by objects and/or organisms relative to the background tempera-ture. This thermoreceptive sense is not specific to crotalines: some booids also have the capac-ity to detect temperature variation but the ther-mal receptors are situated on the labial scales, and hence are called labial pits. The significance of this thermoreceptive or-gan on the predatory strike of booid and viperid snakes has been established (De Cock Buning, 1983; Kardong and Mackessy, 1991; Shine and Sun, 2003). However, no evidence has been pro-vided on alternative functional roles played by thermal pits (Greene, 1992), specifically on de-fense. It has been suggested that thermal pits might help snakes in detecting predators (De Cock Buning, 1983), in finding optimal basking sites for thermoregulation (Goris and Nomoto, 1967; Herbert and Hayes, 1992), and in locat-ing winter dens (Sexton et al., 1992). Because we lack empirical studies on the role of these pits in a non-predatory context, this study provides further understanding on the function of thermal pits. We conducted a simple experiment to test the influence of warm thermal cues on the defensive strike of a pitviper species, the cottonmouth (Agkistrodon piscivorus). Visual cues are of paramount im-portance in releasing a defensive strike (Scudder and Chiszar, 1977). In addition, cottonmouths are preyed upon by predators with different thermal profiles (e.g., ectotherms, endotherms). Thus, we predicted that there would be no dif-ference in the striking response of cottonmouths tested with a warmed versus a non-warmed arti-ficial arm. We collected 21 cottonmouths, 14 females and 7 males (x±σ ; SVL = 74.25±3.33 cm), on the Savannah River Site, South Carolina, USA, during spring 2003. After capture, we fasted each snake for 7 days to eliminate the effect of recent feeding on defensive behavior (Her-zog and Bailey, 1987). The snakes were indi-vidually housed in identical polyethylene con-tainers (Rubbermaid™ [58 × 42 × 14-cm high]) within an environmental chamber (12L:12D, 26 • C) with water dish (provided ad-libitum) and bark mulch as a substrate. We did not dis-turb snakes prior to the experiment. Snout-vent length of the specimens was within a range of 60 to 100 cm SVL, and all were mature individ-uals (Blem, 1997). We performed all trials in the individual housing container that we previously placed in a larger plastic-walled arena (82 × 52 × 34-cm). All trials were performed between 1200 and 1600 hrs. The experimental stimulus con-sisted in tapping on the snake mid-body three successive times at 1-sec intervals with a pair of snake tongs (Midwest Productions™) cus-tomized to look like a human arm (Gibbons and © Koninklijke Brill NV, Leiden, 2005. Amphibia-Reptilia 26 (2005): 264-267 Also available online -www.brill.nl
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Few studies of venomous snakes have addressed how anti-predator behavior may be affected by experience with a potential predator. Because defensive strikes may be costly to snakes, individuals with the ability to learn to discriminate among potentially harmful and non-harmful predatory stimuli should be favored by natural selection. In large venomous snakes, adults are capable of successfully defending themselves against most potential predators, whereas neonates suffer higher predator-induced mortality and are faced with a large diversity of predators. Consequently, we hypothesized that the relative costs of habituation to potential predatory stimuli should vary ontogenetically. This hypothesis predicts that adults should habituate rapidly to non-harmful predatory stimuli, whereas neonates should consistently employ active defensive displays (e.g. striking) because they are at higher risk. To test this prediction, we examined daily changes in the defensive behavior of adult and neonate cottonmouths (Agkistrodon piscivorus) towards a standardized non-harmful predatory stimulus. As predicted, adults and neonates differed in their tendencies to habituate: adults decreased defensiveness over days while neonates did not. Adults showed habituation of striking components but not of warning displays. Our results support the hypothesis that there may be ontogenetic differences in predator perception.
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Venomous snakes are often perceived as aggressive antagonists, with the North American cottonmouth having a particularly notorious reputation for such villainy. We designed tests to measure the suite of behavioral responses by free-ranging cottonmouths to encounters with humans. When confronted, 23 (51%) of 45 tested tried to escape, and 28 (78%) of 36 tested used threat displays and other defensive tactics; only 13 of 36 cottonmouths bit an artificial hand used in the tests. Our findings challenge conventional wisdom about aggressive behavior in an animal perceived as more dangerous than it is. Changing irrational negative attitudes about venomous snakes is a necessary step toward quelling the recently documented global decline in reptiles.
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Squamates (lizards and snakes) have independently evolved viviparity over 100 times, and exhibit a wide range of maternal investment in developing embryos from the extremes of lecithotrophic oviparity to matrotrophic viviparity. This group therefore provides excellent comparative opportunities for studying endocrine and immune involvement during pregnancy, and their possible interactions. We studied the cottonmouth (Agkistrodon piscivorus), since they exhibit limited placentation (e.g., ovoviviparity), allowing comparison with squamate species hypothesized to require considerable maternal immune modulation due to the presence of a more extensive placental connection. Furthermore, the cottonmouth's biennial reproductive cycle provides an opportunity for simultaneously comparing pregnant and non-pregnant females in the wild. We document significantly elevated concentrations of progesterone (P4) and significantly lower concentrations of estradiol (E2) in pregnant females relative to non-pregnant females. Pregnant females had lower plasma bacteria lysis capacity relative to non-pregnant females. This functional measure of innate immunity is a proxy for complement performance, and we also determined significant correlations between P4 and decreased complement performance in pregnant females. These findings are consistent with studies that have determined P4's role in complement modulation during pregnancy in mammals, and thus this study joins a growing number of studies that have demonstrated convergent and/or conserved physiological mechanisms regulating viviparous reproduction in vertebrates.
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Animals respond to stressors by producing glucocorticoid stress hormones, such as corticosterone (CORT). CORT acts too slowly to trigger immediate behavioral responses to a threat, but can change longer-term behavior, facilitating an individual's survival to subsequent threats. To be adaptive, the nature of an animal's behavior following elevated CORT levels should be matched to the predominant threats that they face. Seeking refuge following a stressful encounter could be beneficial if the predominant predator is a visual hunter, but may prove detrimental when the predominant predator is able to enter these refuge sites. As a result, an individual's behavior when their CORT levels are high may differ among populations of a single species. Invasive species impose novel pressures on native populations, which may select for a shift in their behavior when CORT levels are high. We tested whether the presence of predatory invasive fire ants (Solenopsis invicta) at a site affects the behavioral response of native eastern fence lizards (Sceloporus undulatus) to elevated CORT levels. Lizards from an uninvaded site were more likely to hide when their CORT levels were experimentally elevated; a response that likely provides a survival advantage for lizards faced with native predatory threats (e.g. birds and snakes). Lizards from a fire ant invaded site showed the opposite response; spending more time moving and up on the basking log when their CORT levels were elevated. Use of the basking log likely reflects a refuge-seeking behavior, rather than thermoregulatory activity, as selected body temperatures were not affected by CORT. Fleeing off the ground may prove more effective than hiding for lizards that regularly encounter small, terrestrially-foraging fire ant predators. This study suggests that invasive species may alter the relationship between the physiological and behavioral stress response of native species.
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Variation in an animal's response to a predator likely reflects the complex interaction of factors that influence predation risk. Due to their high degree of behavioral variation and simplified bauplan, snakes offer a unique model for investigating the influence of sex and body size on antipredator behavior. We examined variation in antipredator behavior within a cottonmouth (Agkistrodon piscivorus leucostoma) population. Behavioral responses to human-induced predation risk were compared across a continuous scale of body size. Defensive responses significantly declined with increasing body size. After controlling for body size, no differences between the sexes were detected. Although this study suggests that variation in antipredator behavior is, in part, related to body size, some studies on snakes have not found this relationship. Likewise, some studies have demonstrated differences between sexes. Such disparate patterns of variation indicate a need for future comparative studies examining the complex interaction of factors that may influence predator--prey relationships. Copyright 2004.
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Stressful events typically induce glucocorticoid production that suppresses unnecessary physiological and behavioural functions. The glucocorticoid production also temporally activates alternative behavioural and physiological pathways. These responses are generally adaptive changes to avoid the negative effects of stressors. However, under low food availability, these behavioural and physiological modifications might lead to energetic costs. We therefore predict that these responses should not be activated when there are energetic constraints (e.g., low food availability). We experimentally tested whether food deprivation modifies corticosterone-induced behavioural and physiological responses in captive male common lizards. We measured corticosterone-induced responses in terms of body mass, metabolic rate, activity level and basking behaviour. We found that corticosterone-induced various behavioural and physiological responses which were dependent on food availability. Well-fed lizards treated with corticosterone were active earlier, and increased their basking behaviour. These behavioural modifications did not occur in food-deprived lizards. This inactivation of stress-related behavioural changes probably allows the lizard to save energy.
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1. Prey responses to high predation risk can be morphological or behavioural and ultimately come at the cost of survival, growth, body condition, or reproduction. These sub-lethal predator effects have been shown to be mediated by physiological stress. We tested the hypothesis that elevated glucocorticoid concentrations directly cause a decline in reproduction in individual free-ranging female snowshoe hares, Lepus americanus. We measured the cortisol concentration from each dam (using a faecal analysis enzyme immunoassay) and her reproductive output (litter size, offspring birth mass, offspring right hind foot (RHF) length) 30 h after birth.
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In response to stressful events, most vertebrates rapidly elevate plasma glucocorticoid levels. Corticosterone release stimulates physiological and behavioral responses that can promote survival while suppressing behaviors that are not crucial to immediate survival. Corticosterone also has preparatory effects for subsequent stressors. Using male tree lizards (Urosaurus ornatus), we tested our prediction that elevated corticosterone is important for mediating and enhancing antipredator behaviors. Male tree lizards express developmentally fixed polymorphisms that are mediated by early organizational actions of steroid hormones, and thus we also tested the hypothesis that morph-specific differences in antipredator behaviors of adults are independent of circulating corticosterone levels. Plasma corticosterone levels were elevated exogenously for 12-16 h using non-invasive dermal patches, and we then compared the behavioral responses of these corticosterone-patched males to control-patched males during a simulated encounter with a caged predator (collared lizard, Crotaphytus nebrius) in outdoor enclosures. Elevating corticosterone did not alter the antipredator behavioral repertoire of each male morph, but did enhance their responses during the predator encounter: all corticosterone-patched males responded more quickly, hid longer, and displayed more toward the predator than control-patched males. With the corticosterone patch, the non-territorial and wary orange morph was still behaviorally the most wary morph, responding more quickly and hiding longer than either the bolder orange-blue or mottled morphs. Smaller males were generally warier than larger males, regardless of the endocrine treatment or color morph type. In sum, elevated circulating corticosterone enhances antipredator responses for all male tree lizard morphs, without altering morph-specific or size-specific differences in their behavioral responses.