Escape Behaviors and Flight Initiation Distance in the Common Water Snake Nerodia sipedon

Journal of Herpetology, Vol. 42, No. 3, pp. 493 500, 2008 Copyright 2008 Society for the Study of Amphibians and Reptiles Escape Behaviors and Flight Initiation Distance in the Common Water Snake Nerodia sipedon WILLIAM E. COOPER JR., 1 OMAR ATTUM, AND BRUCE KINGSBURY Department of Biology, Indiana University Purdue University Fort Wayne, Fort Wayne, Indiana 46805, USA ABSTRACT. Escape behavior of the natricine snake Nerodia sipedon when approached by a human was studied in populations in wetlands in Ohio and Michigan. Snakes responded by dropping from vegetation, but not immediately fleeing (44%), by diving beneath the water (37%), or by swimming away with the head above the surface (19%). Flight initiation distance (distance between predator and prey when escape begins) was significantly greater for individuals that dropped than those that dove or swam on the surface. This novel finding suggests that dropping may position snakes well to escape should approach continue and perhaps might serve as a pursuit-deterrent signal. Adult females were warier (had greater flight initiation distance) than adult males or juveniles. Several hypotheses to account for this difference are discussed. Flight initiation distance increased with starting distance (distance between predator and prey when the predator begins to approach). This effect was much stronger than in the few lizard species studied. We propose that degree of risk assessed by snakes may change during approaches because a predator that moves directly toward a snake for a longer distance is more likely to have detected the snake and be attacking than a predator that approaches over a shorter distance. Increase in perceived risk would account for greater flight initiation distance associated with greater starting distance. Flight initiation distance for basking snakes did not vary with air temperature or perch height, contrary to previous findings for body temperature and perch height. Reasons for these findings are discussed. Diverse aspects of snake antipredatory behavior have been studied (e.g., Greene, 1988), arguably most notable among them envenomation (Greene, 1988), rattling and other warning displays (Klauber, 1956; Bellairs, 1970), aposematism and mimicry (Smith, 1975, 1977; Greene and McDiarmid, 1981; Pough, 1988; Brodie, 1993), death-feigning (Myers and Arata, 1961; Platt, 1969), and crypsis (Cott, 1940; Sweet, 1985). Some aspects of escape behavior, including ontogeny of escape destinations (e.g., Sweet, cited in Greene, 1988), effects of time of day, proximity to refuge, and portion of body attacked (Langkilde et al., 2004) on tendency to attempt escape (Duvall et al., 1985; Khan and Tasnim, 1986), and others have been studied. Less is known about factors affecting flight initiation distance, the distance between an approaching predator and prey when the prey begins to flee. According to escape theory (Ydenberg and Dill, 1986; Cooper and Frederick, 2007a), flight initiation distance increases as expected fitness cost of not fleeing increases and decreases as expected fitness cost of escaping increases. Rather than fleeing immediately upon detecting a predator, prey are expected by these models to monitor the predator s approach, fleeing when 1 Corresponding Author. E-mail: cooperw@ipfw. edu cost of remaining equals cost of escaping (Ydenberg and Dill, 1986) or when the prey s expected fitness after the encounter is maximized (Cooper and Frederick, 2007a). Studies of numerous predation risk factors and opportunity cost factors (e.g., loss of foraging and courting opportunities) have confirmed these predictions of escape theory. Predation risk factors for which the predictions have been confirmed include predator approach speed and directness (Burger and Gochfeld, 1990; Cooper, 1997a; Cooper et al., 2003), distance from refuge (Dill, 1990; Cooper, 1997b), turn direction (Cooper, 1998a), conspicuousness (Heatwole, 1968; Cooper, 1998b,c), and others. The prediction that flight initiation decreases as cost of escaping increases has been confirmed when fleeing entails loss of opportunity to feed (Cooper, 2000; Cooper et al., 2003, 2006; Cooper and Pérez-Mellado, 2004) or engage in fitnessenhancing social activities (Díaz-Uriarte, 1999; Cooper, 1999; Cooper and Wilson, 2007). Much less is known about factors that affect flight initiation distance in snakes than other lizards. Flight initiation distance increased with body temperature in Regina septemvittata (Layne and Ford, 1984). Because the range of body temperatures was about 15 32uC, snakes at the lowest temperatures were slowed and may have relied more on crypsis to avoid detection than did warmer, faster snakes. Flight initiation distance did not vary with water temperature

494 W. E. COOPER JR. ET AL. in another natricine, Nerodia sipedon (Weatherhead and Robertson, 1992). Flight initiation distance of basking N. sipedon increased as perch height decreased, perhaps because snakes are less vulnerable to predators when higher above water. Reproductive state affects flight initiation distance in Tropidonophis mairii (Natricinae, Colubridae; Brown and Shine, 2004). Flight initiation distance is greater in gravid than nongravid females because gravid females are slower while escaping because of the added mass of the clutch. The increase in flight initiation distance presumably compensates for increased predation risk (Brown and Shine, 2004). Interestingly, male T. mairii permit closer approach during the breeding period than nonreproductive males, which may be attributable to decreased vigilance (Brown and Shine, 2004). In another natricine, Thamnophis sirtalis, flight initiation distance of males is shorter during courtship than afterwards (Shine et al., 2000, 2003). This relationship also might be the result of decreased vigilance (Shine et al., 2003). Other variables that may affect flight initiation distance in N. sipedon are number of approaching people, directness of approach by people, and habituation to people (Burger, 2001). However, in the latter study, distance to respond, which was not clearly defined, was measured rather than flight initiation distance, and the approach protocol differed from that in other studies of escape in that it included both indirect and direct approach during different portions of some trials. Possible relationships between flight initiation distance and types of escape behaviors used are largely unknown in snakes. Another factor that affects flight initiation distance in some birds (Blumstein, 2003) and lizards (Cooper, 2005) is starting distance (distance between predator and prey when the predator begins to approach). It is important to measure starting distance in circumstances and taxa for which it is known to affect flight initiation distance if only for use as a covariate during assessment of effects of risk and costs on flight initiation distance. Effects of starting distance should also be studied in taxa for which they are unknown because they seem to vary both among taxa and with predator approach speed (Blumstein, 2003; Cooper, 2005, 2007). We studied escape behaviors, starting distance, and flight initiation distance in the Common Water Snake, N. sipedon. Our goals were to examine several types of escape behaviors and factors that might affect flight initiation distance. We studied the following: (1) relationships between escape behaviors and factors that might affect the types of escape behaviors used, as well as their relationships to flight initiation distance; (2) the relationship between starting distance and flight initiation distance; (3) effects of air temperature, perch height, and initial distance from water on flight initiation distance; and (4) possible differences among age and sex groups in frequencies of escape behaviors and flight initiation distance. MATERIALS AND METHODS Study Sites. We studied escape reactions of the semiaquatic N. sipedon in northwestern Ohio and southern Michigan on public and private land (Attum et al., 2007). The study site contains a variety of wetland sizes and types. The upland landscape consists of forested, shrub-scrub, old field, roads, and agricultural and residential habitats. We surveyed 111 wetlands three times each between 28 April and 16 June 2005, typically in early morning and late afternoon, when snakes would be more likely to be observed basking. We believe the probability of pseudoreplication by observing the same snake twice was low based on pilot mark and recapture studies of a similar species, Nerodia erythrogaster neglecta, in the same area. Data Collection. To study escape responses, an investigator simulated threat from a predator by approaching snakes. Although this technique might fail to reveal defensive responses specific to particular natural terrestrial predators (Stuart-Fox et al., 2006), such as birds and large mammals, it has several advantages. First, it permits rapid data collection using standardized methods of approach. Second, it avoids ethical issues that arise when staging encounters using real predators. Third, it allows data to be collected efficiently in habitats where mechanical models of predators are difficult or impossible to operate. It seems reasonable for snakes to respond to human beings as if they were predators because of long-term slaughter of snakes by human beings that presumably subjected snakes to natural selection to avoid being killed by people. Even in many taxa not subject to such frequent killing by human beings, predictions for features of antipredatory behavior included in escape and refuge use theories (escape, Ydenberg and Dill, 1986; Cooper and Frederick, 2007a; refuge use, Martín and López, 1999; Cooper and Frederick, 2007b) have been confirmed repeatedly. The most extensive studies have be done in lizards (e.g., Rand, 1964; Bulova, 1994; Martín and López, 1996; Martín et al., 2003), but predictions of escape and refuge use theories have also been confirmed using human simulated predators in some studies of other reptiles (turtles, (López et al.,

ESCAPE BEHAVIOR OF NERODIA SIPEDON 495 2005a; Martín et al., 2005b) and amphibians (frogs, Martín et al., 2005a) and in a wide range of vertebrate (fish, Dill, 1990; Metcalfe and Steele, 2001; birds, Burger and Gochfeld, 1981; Martín et al., 2006; but for a possible exception, see Blumstein et al., 2004; mammals, Dill and Houtman, 1989; Blumstein and Pelletier, 2005), and invertebrate taxa (crabs, Hemmi, 2005a,b; insects, Cooper, 2006; spiders, Nelson and Formanowicz, 2005; serpulid worms, Dill and Fraser, 1997). Focal surveys were made by walking along the wetland s perimeter and wading through the water. When it was not possible to walk around a portion of a wetland, we used binoculars to survey that area. Once detected, snakes were approached directly. The point where the observer first detected the snake and the observer s location when the snake fled was marked. Starting distance and flight initiation distance was measured in 0.1-m intervals. Approach speed was standardized by placing the heel of the shoe on the moving foot in contact with the tip of the shoe on the planted foot, then moving the other foot forward in the same way, alternating feet at the fastest pace allowing the investigator to maintain stability and a straight path. The same investigator made all approaches. Air temperature and perch height also were recorded. The observer stopped approaching as soon as a snake began to flee. Given the sexual dimorphism (females are conspicuously larger than males), it was not necessary to capture extremely large individuals to sex them. We captured smaller individuals to determine age and sex categories. No sex was recorded for smaller individuals that escaped (34% of all snakes). We classified individuals with snout vent length less than 30 cm as juveniles. For each snake, we recorded initial type of escape behavior: dropping from elevated perch (but not moving away); diving underwater; swimming away along the shoreline; and swimming away across the wetland. Because we detected no differences associated with swimming away along the bank or across the wetland, we combined these two behaviors. Analysis. To ascertain whether age and sex categories differed in types of escape behaviors, we used a single-factor Chi-square test. Simple and multiple regressions were conducted to assess relationships between flight initiation distance and starting distance, air temperature, and perch height. Possible differences in flight initiation distance among age-sex groups and among types of escape behaviors were examined using single-factor analyses of variance and analyses of covariance with starting distance as covariate. A factorial analysis could not FIG. 1. Proportions of individuals of Nerodia sipedon for which flight initiation data were collected that performed various types of escape behaviors. DROP dropped from vegetation into water, DIVE swam completely under water, SWIM swam on surface. be conducted because observations were missing for some cells. Levene s tests were conducted to examine the assumption of homogeneity of variance. When significant heterogeneity of variance was found, data were logarithmically transformed prior to analysis. Significance tests are two-tailed with a 5 0.05. RESULTS The snakes for which types of escape behaviors and flight initiation distances were recorded employed three distinct escape behaviors more than once (Fig. 1): diving (N 5 15); swimming away with head out of water (N 5 29); and dropping from vegetation without further escape (N 5 34). Frequencies were large enough to test for sex differences in adults: diving (six males, eight females); swimming away with head above water (10 males, 13 females); and dropping from vegetation (11 males, 10 females). Frequencies of these three escape behaviors did not differ significantly between the sexes of adults (x 2 2 5 0.45, P. 0.10). Numbers of juveniles were too low for detailed statistical comparison of behavioral frequencies with adults, but seven of 10 juveniles swam away with head above water, two dropped from vegetation, and one dove. The frequency of swimming away was somewhat higher for juveniles than for adults, but a comparison of frequency of swimming away versus pooled other types of escape behaviors detected no significant difference (Fisher exact P, 0.094). Variances of flight initiation distance were heterogeneous among age-sex groups using raw

496 W. E. COOPER JR. ET AL. FIG. 2. Flight initiation distance was greater in female than male Nerodia sipedon; the differences between juveniles and adults of each sex were not significant. M male, F female, J juvenile. data (Levene s F 2,79 5 3.99; P, 0.03) but were homogeneous using logarithmically transformed data (Levene s F 2,79 5 0.52; P. 0.10). Flight initiation distance for transformed data differed significantly among age-sex groups (F 2,79 5 6.47, P, 0.0025; Fig. 2). Females (N 5 41) exhibited significantly greater flight initiation distance than males (N 5 31; P, 0.0021). Flight initiation distance of juveniles (N 5 10) did not differ significantly from that of either sex of adults (P. 0.10). Results were the same with starting distance as a covariate, and starting distance did not vary among the agesex groups (F 2,80 5 0.69, P. 0.10; variances were homogeneous: Levene s F 2,80 5 1.42). Variances of flight initiation distance among types of escape behaviors were significantly heterogeneous (Levene s F 2,75 5 6.64, P, 0.003), but variances were homogeneous for logarithmically transformed data (Levene s F 2,75 5 1.10, P. 0.10). The types of escape behavior performed varied significantly with flight initiation distance (F 2,75 5 6.04; P, 0.004; Fig. 3). Flight initiation distance was significantly greater for snakes that dropped from vegetation than for those that swam along the bank (P, 0.01) or dove under water (P, 0.02). The difference in flight initiation distance between snakes that dove and swam along the bank was not significant. The same pattern of findings was obtained using starting distance as a covariate. Flight initiation distance for basking snakes was strongly affected by starting distance (F 1,93 5 45.44, P, 1 3 10 26 ; r 5 0.57). A similar relationship was found for snakes initially in water (F 1,16 5 5.39, P, 0.034; r 5 0.50). The relationship for all snakes is given by FID 5 0.48 SD 2 0.22, where FID is flight initiation distance and SD is starting distance (Fig. 4). For basking FIG. 3. Flight initiation distance was significantly greater for Nerodia sipedon that escaped by diving than for those that swam along the bank or dropped from vegetation into water. DROP dropped from vegetation into water, DIVE swam completely under water, SWIM swam on surface. snakes, flight initiation distance was not significantly related to air temperature (F 1,91 5 1.45, P. 0.10) or perch height (F 1,72 5 0.00, P. 0.10). DISCUSSION Types of escape behavior and their frequencies did not differ among age and sex groups. It remains possible that other aspects of defense such as location in the habitat and distance from refuges differ among ages, sexes, and reproductive states. Options for escape behaviors may have been determined largely by the locations of snakes when approached and characteristics of the surrounding habitat or by individual differences among snakes in preferred escape behaviors. Many reasons for the greater flight initiation distance by females than males are possible. FIG. 4. Flight initiation distance in Nerodia sipedon increased as starting distance increased.

ESCAPE BEHAVIOR OF NERODIA SIPEDON 497 Females, which are substantially larger than males, may assess greater risk of being detected by a predator at a fixed distance than do males. If gravid females have greater flight initiation distance than nongravid females because litter mass causes escape speed to decrease as in T. mairii (Brown and Shine, 2004), inclusion of gravid females in our study might have raised mean flight initiation distance for all females. We did not record reproductive state, but any gravid females would have been in early stages when embryonic mass is small. Another hypothesis is that flight initiation distance decreases in reproductively active males. This hypothesis for the seasonally breeding N. sipedon predicts findings analogous to those for male T. mairii, in which most males are reproductively active throughout the year (Brown and Shine, 2004). Because our data were collected during early seasonal activity and the beginning of the breeding season, some males were presumably reproductively active and others not. Brown and Shine s (2004) interpretation of greater flight initiation distance by gravid than nongravid female T. mairii is consistent with escape theory. Ydenberg and Dill s (1986) graphical model and optimal escape theory (Cooper and Frederick, 2007) predict that, if other aspects of escape strategy are not altered to compensate for increased risk, flight initiation distance increases as cost of remaining (not fleeing) increases. At a given distance, the cost of remaining is greater for a slower, gravid female than for a nongravid female. In natricines, decreased flight initiation distance in reproductive versus nonreproductive males and in courting than noncourting males have been attributed to decreased vigilance (Shine et al., 2003b; Brown and Shine, 2004). This is certainly a plausible hypothesis, especially during courtship. Another possibility is that opportunity costs are greater for reproductive than nonreproductive and courting than noncourting males. Cost of losing a fertilization opportunity or a combination of that cost with decreased vigilance might account for the differences we observed in males. For the escape cost hypothesis, shorter flight initiation distance by reproductive than nonreproductive male T. mairii may be a consequence of a cost of giving up searching for potential mates or remaining near females not observed by the researchers. Flight initiation distance of male Broad- Headed Skinks (Plestidon laticeps) is shortened during mate-guarding, courting, and aggressive behavior despite awareness of a nearby predator (Cooper, 1999). Opportunity costs of abandoning a female during mate-guarding or courtship or abandoning a rival male that might fertilize nearby females explain the shorter flight initiation distance. In the present study, difference in vigilance between sexes and reproductive states were unlikely because all snakes had clear views of the investigator. Further research is needed to establish the roles of vigilance and escape costs in flight initiation distance of male natricines. Variation in types of escape behavior with flight initiation distance is a novel finding. Although snakes that dropped exhibited greater flight initiation distance than those that swam away with head above water or dove, they did not move away after dropping. Presumably, they would have fled using one of the other behaviors had the investigator continued to approach. Snakes elevated in vegetation may be at greater risk because they are easier to detect there, accounting for greater flight initiation distance. Dropping may position them for effective escape when they are in exposed, elevated locations. Although we did not collect relevant data, snakes basking in vegetation appeared to be more likely to drop during cool periods when swimming or diving would reduce body temperature. In this way they would avoid high thermal escape costs unless forced to swim. An alternative hypothesis not mutually exclusive with the others is that dropping is a pursuit-deterrent signal. Why do some snakes dive when others swim on the surface? Diving may occur when assessed risk is greater because it renders the escaping snake more difficult to detect or invisible. In the lizard Lacerta monticola, pronounced variation in wariness exists because of individual differenceces, even under similar predation threat (López et al., 2005b). If similar variation occurs, warier snakes dive when bolder ones escape on the surface. Or snakes that dove may have been in locations exposing them to greater risk. The effect of starting distance on flight initiation distance is far greater in N. sipedon than in other lizards studied to date. At approach speeds comparable to that in our study of N. sipedon, starting distance had no effect on flight initiation distance in Leiocephalus carinatus (Cooper, 2007), Sceloporus virgatus, or Urosaurus ornatus (Cooper, 2005). The magnitude of the effect in N. sipedon is similar to that of some bird species: The proportion of variance in flight initiation distance explained by starting distance was higher in 16 of 58 avian species from Tasmania and eastern Australia (Blumstein, 2003) than the R 2 5 0.48 for N. sipedon. For birds that take flight frequently, increase in flight initiation distance with starting distance

498 W. E. COOPER JR. ET AL. could be an artifact of the longer time needed to approach from greater starting distance. Blumstein (2003) proposed that cost of monitoring the approach increases with starting distance because prey must cease or devote less attention to current activity longer during longer approaches. Thus, cost of not fleeing increases as starting distance increases, causing flight initiation distance to increase. Although reasonable for active birds, this explanation seems unlikely for a sedentary snake such as N. sipedon. Snakes in our study did not forage or engage in social behaviors, and basking need not be interrupted to monitor an approaching predator. To account for the effect of starting distance, cost of not fleeing must increase or cost of fleeing decrease as starting distance increases. We favor the hypothesis that the strong effect of starting distance in N. sipedon is a consequence of a change in perceived risk. When a predator moves on a straight path toward a prey, flight initiation distance is greater than during approach on an indirect path that bypasses the prey (Cooper, 1997a, 2003a,b; Cooper et al., 2003). During direct approach, prey assess that risk is greater than during indirect approach because the predator is more likely to have detected or to detect the prey and attack if it continues moving in its current direction. Similarly, a predator that continues to approach a prey directly for a greater distance is more likely to have detected and be currently attacking or to continue on its path, leading it to detect and attack the prey. For prey incorporating these factors into risk assessment, flight initiation distance would increase as starting distance increases. Study of effects of starting distance on flight initiation distance has barely begun, but starting distance clearly is an important factor in diverse reptiles. Causes of the relationship are as yet uncertain, and both its causes and importance are likely to vary among prey taxa. Studies of effects of starting distance in additional prey taxa, experiments designed to distinguish between effects caused by increased monitoring costs, assessment of greater risk associated with long starting distances, and studies of effects of movement rates of undisturbed prey in relation to time required for approaches offer fertile ground for future research. Body temperature strongly affected flight initiation distance in the natricine R. septemvittata (Layne and Ford, 1984), but air temperature did not affect it in N. sipedon despite a wide range of air temperatures (9.4 30.6uC). This finding is consistent with lack of effects of air and water temperatures on flight initiation distance in this species (Weatherhead and Robertson, 1992). Nevertheless, an effect of body temperature on flight initiation distance could have been obscured in two ways. Behavioral thermoregulation may have restricted variation in body temperature. Second, a large majority of observations were made between 16 and 25uC, reducing the likelihood of detecting a relationship. The lack of relationship between perch height and flight initiation distance in our study differs from the negative linear relationship observed in N. sipedon by Weatherhead and Robertson (1992). In their study, snakes were perched in willow trees at heights up to 4 m, whereas perch height varied much less in our study (0 2 m). Some snakes were at ground level and others perched on various objects rather than trees directly over water. Thus, there is no contradiction between the findings. The relationship may pertain only to snakes in elevated basking sites over water. Acknowledgments. This work was a byproduct of funding by the U. S. 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