Behavioral Ecology Vol. 15 No. 2: 365-370
Behavioral Ecology vol. 15 no. 2 © International Society for Behavioral Ecology 2004; all rights reserved
Size-based variation in antipredator behavior within a snake (Agkistrodon piscivorus) population
Department of Zoology and Sam Noble Oklahoma Museum of Natural History, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019, USA
Address correspondence to E. D. Roth. E-mail: eric.d.roth-1{at}ou.edu. J. A. Johnson is now at the Department of Biology, University of South Florida, 4202 East Fowler Avenue, SCA 110, Tampa, FL 33620, USA.
Received 7 March 2003; revised 16 May 2003; accepted 30 June 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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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.
Key words: Agkistrodon piscivorus leucostoma, antipredator behavior, body size, cottonmouth, intraspecific variation, snakes.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Variation in antipredator behavior has been demonstrated across a diversity of taxa, both between and within species or populations (reviewed by Edmunds, 1974
; see also Arnold and Bennett, 1984; Ducey and Brodie, 1991; Labra and Leonard, 1999; Randall et al., 1995). Examining patterns of variation may enhance our understanding of predator-prey interactions and provide insight into factors influencing antipredator behavior. Optimality theory suggests that the behavioral response of an individual to a predator is influenced by the risk of predation (Cooper and Vitt, 2002; Lima and Dill, 1990; Ydenberg and Dill, 1986). Furthermore, differences in individual physiology, morphology, and ecology may affect an individual's response to predation risk. For example, studies have demonstrated that antipredator behaviors can vary relative to sex (Clutton-Brock, 1991; Magurran and Nowak, 1991; Shine et al., 2000) and body size (Gomes et al., 2002; Krause et al., 1998; Puttlitz et al., 1999). However, these factors operate within an ecological context and are subject to complex interactions with other intrinsic (e.g., age, reproductive condition, and experience or learning) and extrinsic factors (e.g., predator type and density, habitat characteristics, temperature, and social context) (reviewed by Endler, 1986). Variation in antipredator behavior likely reflects these complex interactions and their influence on predation risk (reviewed by Lima, 1998; Lima and Dill, 1990). The complexity of predator-prey relationships dictates a need for comparative studies from which further generalizations of antipredator behavior may be established.
Snakes exhibit a diverse suite of antipredator behaviors (reviewed by Greene, 1988; see also Weldon et al., 1992), that can vary with body size (Carpenter and Gillingham, 1975; Gutzke et al., 1993; Hailey and Davies, 1986; Shine et al., 2002; Sweet, 1985; Whitaker and Shine, 1999; Whitaker et al., 2000), sex (Herzog and Burghardt, 1986; King, 2002; Scudder and Burghardt, 1983; Shine et al., 2000; Webb et al., 2001), reproductive state (Goode and Duvall, 1989; Graves, 1989), body temperature (Brodie and Russell, 1999; Goode and Duvall, 1989; Layne and Ford, 1984; Passek and Gillingham, 1997; Shine et al., 2000, 2002; Webb et al., 2001; Whitaker and Shine, 1999), body condition (Andrén, 1982), and a variety of extrinsic factors (Duvall et al., 1985; Shine et al., 2000, 2002; Whitaker and Shine, 1999). Furthermore, relationships among these variables are often inconsistent between species and populations. Given the numerous factors that may influence antipredator behavior, interpreting variation among and within taxa is problematic. However, it is likely that some factors are more influential than others, and these factors may be more useful when constructing general models of antipredator behavior.
In reptiles, antipredator behavior has been shown to vary through ontogeny (reviewed by Greene, 1988; see also Vitt, 2000), specifically with body size (Cooper and Vitt, 1985; Fox, 1978; Huey and Pianka, 1977). Differential survivorship of alternative strategies can lead to divergent behavioral phenotypes, especially in pre-reproductive stages (Fox, 1978). Because predation is most likely the greatest threat to juvenile survivorship, behavioral phenotypes that reduce the effects of predation are no doubt subject to natural selection. Given that body size may strongly influence predation risk (e.g., Blomberg and Shine, 2000; Janzen et al., 2000; Shine et al., 2001; Tucker et al., 1999; Vitt, 2000), variation in antipredator behavior likely reflects different selection pressures on different body sizes. Snakes are ideal models to investigate the effects of body size on behavioral variation because, unlike birds and mammals, morphology remains relatively constant with sex and age, but body size varies enormously.
Investigations into ontogenetic variation of snake antipredator behavior have typically focused on differences between small and large or juvenile and adult snakes (e.g., Shine et al., 2002; Sweet, 1985; Whitaker and Shine, 1999; Whitaker et al., 2000). Although such studies are effective in demonstrating variation, dichotomous comparisons are limited in their ability to adequately address variation in antipredator behavior across the entire continuum of body size or age. For example, variation within groups may be further explained by body size, but these patterns may remain obscured by simple between-group comparisons. Furthermore, comparative studies including neonates must be interpreted with caution. Neonates may have difficulty in perceiving and responding to predation risk because of inexperience with predatory encounters and underdeveloped morphological and physiological traits (reviewed by Morafka et al., 2000; see also Pough 1977, 1978). Additionally, neonates may possess a limited behavioral repertoire simply because certain behaviors have yet to develop (Greene, 1988). Due to developmental limitations and extreme ontogenetic differences in ecology, direct comparisons in antipredator behavior between neonates and other age groups may further confound behavioral interpretations. Thus, studies that explore variation within the non-neonate component of a population may be of great comparative value.
Here we examined the influence of body size and sex on antipredator behaviors of a western cottonmouth (Agkistrodon piscivorus leucostoma) population. We explored variation in antipredator behavior across a continuous scale of body size and attempted to minimize the influence of developmental limitations by examining only individuals greater than 1 year of age.
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METHODS |
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We collected 46 western cottonmouths from Huntsville, Texas, USA, at the Center for Biological Field Studies, Sam Houston State University. We maintained the snakes in the laboratory for 3–16 months before experimental testing in individual 51 x 38 x 18 cm plastic cages. We fed cottonmouths one mouse per week except for the 2 weeks before testing, as recent eating may alter antipredator behavior (Herzog and Bailey, 1987
; Shine et al., 2002). Water was provided ad libitum. The light dark cycle varied naturally with the time of year, and temperatures in the laboratory were 21–32°C. Upon completion of the study, animals were sexed with a cloacal probe and snout-vent length (SVL) was recorded using the squeeze box technique (Quinn and Jones, 1974). We maintained subjects in the laboratory for future observations.
Experimental design
We tested 46 snakes, ranging from 30.5–82.5 cm in SVL, in a randomized order on 16 November 2002 between 1300–2000 h in their individual cages. Two hours before testing, all subjects were habituated to room temperature (27–28°C). At this temperature, we subjected individual cottonmouths (23 males, 23 nongravid females) to a 60-s experimental trial executed in three consecutive 20-s stages separated by 1-min intervals. The three stages of the experiment were designed to mimic a predation event with an escalating level of predation risk over time. Similar to other antipredator snake studies (e.g., Burghardt and Greene, 1988; Herzog et al., 1989; Gibbons and Dorcas, 2002; Scudder and Burghardt, 1983; Shine et al., 2000, 2002), humans were used as the threat stimulus to generate antipredator responses. During the first stage, we removed the top of the cage, exposing the snake to the two observers. During the second stage, we approached and harassed the snake with gentle nudges to the snout using a welding glove placed on the end of a pair of 1-m snake tongs as the threat stimulus (similar to methods of Gibbons and Dorcas, 2002). For the third stage, we picked up the snake at mid-body with the tongs for approximately 5 s, released the snake, and then repeated this process.
We quantified seven common behaviors (escape behavior, defensive posturing, tail vibrations, musk release, mouth gapes, strikes, and bites) often considered antipredator responses (e.g., Gibbons and Dorcas, 2002; Greene, 1988, 1997; Klauber, 1997). Each behavioral category was given a score of 0–2 based on predefined scoring criteria. Categorical scores were awarded by a consensus of the two observers at the end of each stage. For each category, individuals failing to exhibit a response were awarded zero points. Otherwise, we scored the categories as follows. Escape behavior was defined as any attempt to move away from the threat stimulus. Slow but directed movements away from the threat stimulus were awarded 1 point, whereas quick movements in the same manner were awarded 2 points. Defensive posturing was defined as the classical striking coil (Klauber, 1997) or S-curve in the neck as the snake appears ready to strike. Brief or intermittent defensive posturing <10 s was scored as 1 point., whereas defensive posturing 
10 s was scored as 2 points. Vibrating the tail generally in short bursts of 1–2 s was defined as a tail vibration. We awarded 1 point for one or two tail vibrations and 2 points for more than two tail vibrations. Because musking behavior was difficult to quantify, we scored any musk release as 2 points. Cottonmouths will briefly mouth gape to display the white inside lining of the mouth. We scored one mouth gape as 1 point and more than one mouth gape as 2 points. A strike was defined as a quick forward thrust toward the threat stimulus. This action was occasionally followed with biting behavior. Bites and strikes were scored in the same manner as mouth gapes.
Total points were recorded for each 20-s stage with a maximum of 2 points for each behavioral category (i.e., maximum of 14 points per 20-s stage). We then totaled scores from the three stages for the 60-s trial to create a total behavioral index score for each cottonmouth. This score represents a measure of cumulative response to escalating levels of predation risk.
Data analysis
Although index scores for each behavior were based on an ordinal scale, the numerous combinations of ordinal values allowed for by our experimental protocol generated a large spread of possible values in the data set, simulating a pseudo-interval value (total behavioral index score). Total behavioral index scores and SVL measurements were then log10 transformed to further conform to assumptions of normality (Sokal and Rohlf, 1995). Although parametric analysis on pseudo-interval data is problematical, the F test is fairly robust to violations of normality and related assumptions (discussed in Underwood, 1997). Thus, we report parametric statistics when analyzing total behavioral index scores.
We used a simple regression to test for a relationship between body size (log SVL: independent variable) and antipredator behavior (log total behavioral index score: dependent variable). We performed an ANCOVA to test for behavioral differences (log total behavioral index score: dependent variable) between the sexes (independent variable) with body size (log SVL) as the covariate. For each individual we calculated the proportion of points each behavioral category contributed to the total behavioral index score. All proportions were arcsine transformed before statistical analysis (Sokal and Rohlf, 1995). We performed a repeated-measures ANOVA to test for proportional differences between behavioral categories. If behaviors are considered separately, index scores for each behavior more closely resemble ordinal data and do not meet the assumptions of normality. Thus, to further examine each behavior separately, Spearman rank analyses (corrected for ties) were applied to test for correlations between non-transformed index scores and SVL.
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RESULTS |
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Time in captivity was randomly distributed across all body sizes and was not correlated with total behavioral index scores (Spearman rank: rs =.063, p =.6713). Thus, any effects due to differences in time in captivity were negligible and were not considered in further analyses. A negative relationship (Figure 1) existed between body size and antipredator behavior (simple regression: r2 =.23, F1,44 = 12.78, p <.001). No interaction between body size and sex was evident (ANCOVA: F1,42 = 0.52, p =.47). Thus, the interaction term was removed from the model, and main effects were compared. Effects of body size (SVL: covariate) were significant (ANCOVA: F1,43 = 12.28, p <.005). However, no significant differences in relative antipredator behavior were detected between sexes (ANCOVA: F1,43 = 0.01, p =.96). The repeated-measures ANOVA revealed differences in the relative contribution of each behavioral category (F6,270 = 23.59, p <.0001; Figure 2) to the total behavioral index score. The most common behavior was escape, which significantly differed from all other behavioral categories (Fisher's protected least significant difference: p <.0001). Graphical relationships between body size (SVL) and each behavior are depicted in Figure 3. Spearman rank correlations revealed significant negative relationships with body size for tail vibrations (rs = -.308, p <.05) and musk (rs = -.513, p <.001). The negative correlations with body size for posture (rs = -.265, p =.0758) and mouth gapes (rs = -.272, p =.068) were marginally significant. No correlation was found with body size for escape (rs =.117, p =.4308), strikes (rs = -.121, p =.4174), or bites (rs = -.09, p =.5457).
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DISCUSSION |
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As body size increased, total behavioral index scores decreased. To interpret this result, it is important to consider how behavioral index scores were generated. Index scores for each individual were based on the number of antipredator behaviors recorded and the degree to which each behavior was exhibited throughout the trial. Essentially, this index score represents behavioral diversity with varying levels of intensity. However, the sequence of behavioral categories is not random, but occurs in a generalized progression. For example, an individual usually responds to an initial threat stimulus with an escape behavior or another passive response. An aggressive defense, such as a strike or bite, rarely occurs without an escape attempt or some initial progression of passive behaviors, which are presumably intended to warn, threaten, or distract the predator (Greene, 1988
). This hierarchical system of antipredator behavior is common among snakes (for discussion, see Duvall et al., 1985). An increase in diversity and intensity of behavior is indicative of a hierarchical progression of antipredator tactics. Our behavioral index scores provided a quantitative measure of defensive response, recorded across a sequence of events, which were designed to mimic an escalating predation threat.
Our results demonstrate that antipredator behavior varies with body size, and increases in body size were associated with a decrease in the level of defensive response. Ontogenetic variation in antipredator behavior is common among reptiles (reviewed by Greene, 1988), but is is unknown why defensive response declines with increasing body size. This may result from reduced predation risk in larger individuals (e.g., Blomberg and Shine, 2000; Janzen et al., 2000; Shine et al., 2001; Tucker et al., 1999; Vitt, 2000), simply because small predators that could easily kill a small cottonmouth might not be able to subdue and consume a larger cottonmouth. Furthermore, smaller individuals may have locomotor limitations related to speed or endurance (reviewed by Carrier, 1996; see also Garland and Losos, 1994) that affect their ability to escape. Indeed, as a general rule, body size in snakes is positively related to locomotor performance (Finkler and Claussen, 1999; Hailey and Davies, 1986; Jayne and Bennett, 1990; Kelley et al., 1997; Pough, 1977, 1978; Scribner and Weatherhead, 1995) and inversely related to predation risk (Mushinsky and Miller, 1993; Shine et al., 2001). Similar to our results, many snake studies indicate that defensive responses decline with increasing body size (Bogert, 1941; Carpenter and Gillingham, 1975; Gutzke et al., 1993; Hailey and Davies, 1986; Shine et al., 2002; Sweet, 1985; but see Layne and Ford, 1984). Shine et al. (2000) found no direct effects of body size on defensive response but suggested that body size indirectly influenced antipredator behavior through temperature because larger snakes were typically warmer. This explanation does not account for our size-based behavioral variation because all snakes were habituated to the same temperature before testing.
Behavioral variation was exhibited across a continuous scale of body size (SVL) within the non-neonate component of a cottonmouth population. Although a highly significant relationship with antipredator behavior was demonstrated, body size only accounted for a small portion of the variance (r2 =.225). Some residual variation is likely attributable to relatively crude behavioral quantification and possibly could be minimized with refined scoring techniques and detailed video analysis. Nonetheless, given the complexity of interactions (physiological, morphological, and ecological) that can influence antipredator behavior, it is surprising that body size alone accounted for more than one-fifth of the variation in total behavioral index scores.
With the effect of body size removed, we found no differences in behavioral index scores between sexes. Numerous other snake studies also failed to find sex-based differences in antipredator behavior (Hailey and Davies, 1986; Layne and Ford, 1984; Whitaker and Shine, 1999). However, our study is limited in scope because it did not include gravid females and only compared the sexes within a laboratory setting at a snapshot in time during the fall season when reproductive activity is presumably low. How reproductive state and experimental conditions interact to influence motivational state and physiology of our study subjects is unknown. Gravid snakes may exhibit reduced locomotor performance (Seigel et al., 1987, but see Brown and Weatherhead, 1997) and differences in antipredator behavior (Goode and Duvall, 1989). Additionally, other studies have suggested sex differences in snake antipredator behavior (Herzog and Burghardt, 1986; King, 2002; Scudder and Burghardt, 1983; Shine et al., 2000, Webb et al., 2001) and warrant future research of sex-based influences.
Similar to the results of a field study on cottonmouth defensive behavior (Gibbons and Dorcas, 2002), proportional comparisons of different antipredator behaviors reveal a general pattern of hierarchical decision making: (1) if detected by predator, then retreat (escape behavior), (2) if threatening stimulus persists, employ passive deterrents (tail vibration, defensive posturing, mouth gape, musk release), and (3) if the threat further escalates, then engage in aggressive defense (strikes, bites). Our data support this interpretation as behavioral proportions generally declined across this hierarchical gradient (Figure 2). Within this gradient, mouth gapes represented the lowest mean proportion of behavioral index scores. The mouth gape is a common cottonmouth antipredator behavior (Gibbons and Dorcas, 2002) and was frequently exhibited by our experimental subjects in response to threat stimuli. The low mean proportion of mouth gapes in this study was likely an artifact of our testing methods. Threat stimuli, such as gentle nudges to the snout, were applied in close proximity to the subject and may have inhibited this type of warning behavior.
Examination of each antipredator behavior independently may provide further insight into why total behavioral index scores based on the additive quantification of seven antipredator behaviors generally declined with increasing body size. As body size increased, snakes were equally likely to exhibit escape behavior. This may be expected because escape behavior is an early response in the hierarchical progression. All snakes, despite differences in body sizes, were tested in the same size arena or cage. This method controlled for any confounding effects of absolute cage size but may be prone to influences of relative cage size (i.e., larger snakes were tested in arenas that were smaller relative to their SVL). Escape behavior results demonstrate that all snakes are equally likely to flee despite differences in body size and relative cage size. However, further experiments examining the influence of absolute and relative testing arena size would be of interest.
The next sequence of hierarchical responses, which include passive deterrents or warning behaviors, generally declined with increasing body size. Although a gradual decline is graphically exhibited, aggressive defense behaviors (strikes and bites) did not significantly vary with body size. Thus, most of the variation in total behavioral index scores may be explained by the significant negative correlation between passive deterrents or warning behaviors and body size. Reasons for the lack of correlation between aggressive defense behaviors and body size are unclear. Natural selection pressures due to predation risk may still vary across body sizes but may be mediated by different mechanisms, producing convergent behaviors. For example, larger snakes may be reluctant to strike simply because perceived predation risk is much lower. Smaller snakes may have a higher perceived predation risk, but a strike effectively decreases the distance between a snake and the predator and increases the vulnerability of the head and neck region to predatory attack. In both cases low index scores for strikes and bites may be predicted.
Although behavioral index scores generally declined with increasing body size, we cannot rule out that the relationship between body size and antipredator behaviors was indirect, as body size is related to numerous other confounding variables (Peters, 1983; Werner and Gilliam, 1984). For example, an alternative explanation for our results is that the significant negative relationship between behavioral index scores and body size is reflective of experience, and thus with differences in age. Younger snakes may exhibit an elevated response to all potential predators, whereas older snakes are better able to evaluate predation risk from experience and respond accordingly. However, this explanation assumes that the smaller snakes from our study were younger and less experienced. All snakes from our study were greater than 1 year of age (subadult to adult). Body size is a relatively poor predictor of age, especially in adult snakes. In reptiles, body size and growth rates are asymptotic (Andrews, 1982; Shine and Charnov, 1992) and may be influenced by rates of resource acquisition, daily temperature patterns, and other intrinsic and extrinsic variables (reviewed by Andrews, 1982; see also Madsen and Shine, 2000). Additionally, age is not always a good predictor of experience with predators. Experience may also depend on relative predator densities and activity patterns within an individual's home range.
Another alternative explanation is that lower behavioral index scores exhibited by larger snakes are the result of differential survivorship and simply represent a subset of behaviors exhibited by smaller snakes. However, given this explanation, we would expect a greater variance in behavioral scores at smaller sizes with a decreasing variance in behavioral scores for the larger sizes. Our results do not support this interpretation, as the variance around the best-fit line (Figure 1) is relatively uniform through all sizes. Furthermore, this explanation again assumes that larger snakes are older, which, as we have previously stated, may be an improper assumption.
Although handling and maintaining animals in captivity may affect antipredator behavior (Greene, 1988), our laboratory setup allowed us to reduce potential influences of extrinsic factors. Under these controlled conditions, we were able to demonstrate a size-based relationship with antipredator behavior. Although such size-based relationships are common among snakes (Bogert, 1941; Carpenter and Gillingham, 1975; Gutzke et al., 1993; Hailey and Davies, 1986; Shine et al., 2002; Sweet, 1985), some field studies on cottonmouths (Gibbons and Dorcas, 2002) and other snakes (Layne and Ford, 1984; Shine et al., 2000) revealed no size-based differences. It is plausible that complex ecological interactions in a natural setting may negate the influence of body size. However, failure to detect body size influences on antipredator behavior in free-ranging snakes may instead result from logistical difficulties in controlling for confounding variables (e.g., differences in microhabitat type, body temperature, recent experience), and obtaining adequate sample sizes. Complementary comparative field and laboratory studies are needed to explain variation in behavioral responses and address patterns of antipredator behavior within a fluctuating environment.
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ACKNOWLEDGEMENTS |
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This research was funded in part by the Graduate Student Senate of the University of Oklahoma. We thank M.L. Thies, director of the Center for Biological Field Studies, for housing and other accommodations. We are also grateful to D.B. Shepard and L.J. Vitt for comments on earlier versions of this manuscript. This study was conducted under the University of Oklahoma Animal Care and Use Committee permit (A3240-01), approved May 2001, and collection permit (SPR-0499-028).
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