Antipredator behaviour of hatchling snakes: effects of incubation temperature and simulated predators

ANIMAL BEHAVIOUR, 1998, 56, 547–553 Article No. ar980809

Antipredator behaviour of hatchling snakes: effects of incubation temperature and simulated predators JOANNA BURGER

Division of Life Sciences, Rutgers University (Received 7 April 1997; initial acceptance 18 July 1997; final acceptance 15 December 1997; MS. number: A7901)

ABSTRACT All animals that are exposed to predators must distinguish dangerous from nondangerous threats and respond correctly. In reptiles, emerging hatchlings are vulnerable to a wide range of predators, particularly if they emerge during daylight. In these experiments I tested the response of pine snake, Pituophis melanoleucus, hatchlings incubated at 22–23, 27–28, or 32–33C to visual and vibratory stimuli to examine antipredator behaviour. Emerging hatchlings were exposed to one of five conditions: (1) hawk model, (2) white head model with no facial features, (3) white head model with black eyes, (4) a person, or (5) a vibration without a visual stimulus. I tested the null hypotheses of no differences in response as a function of predator type or incubation temperature. Emergence behaviour when undisturbed was affected by incubating temperature, and antipredatory behaviour was affected by both predator type and incubation temperature. Pine snake hatchlings responded more protectively (withdrawal into tunnels) than defensively (striking), responded with less intensity to a vibration compared with visual predator stimuli, and required longer to respond to a head model without eyes than to all other predator types. Given the relatively small size of hatchlings, it is adaptive for them to withdraw into the nest rather than attack a predator. Hatchlings from eggs that were incubated at medium temperatures required less time to emerge from their underground nests when undisturbed, and had stronger protective responses than snakes incubated at other temperatures. These results suggest that hatchlings incubated at medium temperatures are generally less vulnerable to predators than hatchlings incubated  1998 The Association for the Study of Animal Behaviour at higher or lower temperatures. because they do not have effective locomotion, and cannot escape by rapid movement; thus, they respond to snake predators by crouching and becoming immobile (Wassersug & Sperry 1977; Heinen 1994). In experimental studies, Heinen (1994) showed that American toads, Bufo americanus, that crouched or remained immobile were less likely to be eaten than those that did not. In addition to defence, prey essentially try to avoid detection, interception and capture (Webb 1986). Hatchling snakes have three general methods of responding to predators. They can either engage in offensive behaviour such as hissing and striking at predators (Bowers et al. 1993), they can feign death (Knoll 1977), or they can withdraw or retreat from the predator. No one mechanism of predator avoidance may be ‘best’ (Endler 1986), although potential prey can effectively protect against predators by interrupting the predatory event as early as possible. Snakes or turtles that are emerging from underground burrows or hiding places could respond to predators either by withdrawing into the burrow, slithering away rapidly, or exhibiting aggressive defence behaviours such as hissing or striking at the predator. In

All animals must deal with predators, and young animals are particularly vulnerable, either because they are smaller than adults, or are less equipped to deal with such threats. In altricial species of vertebrates, neonates can rely on their parents to defend them against predators, but in precocial species that have no parental care, the young must cope with predators from birth (Burghardt 1984). Most reptiles, amphibians and fish display no parental care once the eggs are laid, leaving the young to avoid predators on their own. It is thus important for young to distinguish predators from nonpredators, and to respond accordingly, without wasting time and energy on nonpredators. This ability is adaptive for all young, regardless of whether they have attentive parents. Young reptiles and amphibians are vulnerable to predators both because of their small size, and because they have not learned to avoid predators (either passively or actively, Endler 1986). Unlike neonatal snakes, newly metamorphosed amphibians are vulnerable to predators Correspondence: J. Burger, Division of Life Sciences, Rutgers University, Piscataway, NJ 08854-8082, U.S.A. (email: burger@ biology.rutgers.edu). 0003–3472/98/090547+07 $30.00/0

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548 ANIMAL BEHAVIOUR, 56, 3

all of these cases, the evolution of antipredator behaviour suggests that unsuccessful predation attempts are the rule for interactions among predators and prey (Vermeij 1982). Turtle and snake neonates that emerge from underground nests are particularly vulnerable to predators, both before they emerge to the surface, and immediately after (Burger 1977; Greene 1988; Burger et al. 1992). Hatchling turtles experience high predation rates following emergence, although some species possess defensive behaviours (clawing, biting), which may deter some predators (Britson & Gutzke 1993). Snakes are among the most precocial of vertebrates, and some species engage in defensive or threat responses (hissing, striking) from the moment they are born (Burghardt 1978; Herzog & Burghardt 1986; Greene 1988). Furthermore, snakes can learn to discriminate between a dangerous and a nondangerous organism (Drummond & Garcia 1995). A wide range of hatchling turtles, lizards and snakes that lack experience with predators display defensive behaviour (Greene 1988). A number of other factors besides age affect antipredator behaviour, including size, temperature, stimulus intensity, learning and habituation (Greene 1986, 1988). Incubation temperature affects a wide range of behaviour, such as emergence, locomotion and foraging ability (Burger 1991a). I examined the antipredator behaviour of pine snake, Pituophis melanoleucus, hatchlings in the laboratory by exposing them to visual and vibratory stimuli while they were emerging from their underground burrows. The stimuli included: (1) hawk model, (2) white head model with no facial features, (3) white head model with black eyes, (4) a person, or (5) a vibration without a visual stimuli. The hawk model was of a species that could prey on young pine snakes in nature, the head models with and without eyes were used to test whether the presence of eyes was critical, and the person was used because people account for considerable losses of snakes in the New Jersey Pine Barrens (Zappalorti & Burger 1985). Vibration was used because it might signal the approach of a mammalian predator such as a fox, Vulpes fulva, or raccoon, Procyon lotor. I tested the null hypothesis that there were no differences in hatchling response as a function of the type of simulated predator. Because incubation temperature has been found to influence the behaviour of pine snake hatchlings (Burger 1989a, 1990a, 1991a, b), I also tested the null hypothesis of no differences in response as a function of incubation temperature. Although ambient temperature affects defensive behaviour in snakes (Keogh & DeSerto 1994), no one has examined the effect of incubation temperature on subsequent antipredator behaviour of reptiles. In the wild, pine snake females excavate a long tunnel under the ground, and deposit their clutch in a nest burrow at the end (Burger & Zappalorti 1986, 1992). During incubation, the tunnel gradually fills in, and the hatchlings eventually dig up through the sand to reach the surface (Burger & Gochfeld 1985). Emerging hatchlings are vulnerable to predators before they emerge, while they are emerging, and before they find suitable

cover. Hatchlings emerge very slowly, peering around for some time before they emerge. Depending upon incubation temperature, snakes require 6–33 min to emerge completely once they have broken the soil surface with their noses (Burger 1991a). During this time, hatchlings are vulnerable to predators that might detect their slow movement, or to that of their siblings already above-ground. Pine snake hatchlings are able to discern the odours of their predators, and actively avoid places with these odours when given a choice (Burger 1989b, 1990b, 1991b; Burger et al. 1991a). Furthermore, they can distinguish chemical cues of predators from those of conspecifics. The present set of experiments was designed to test their response to visual and vibratory cues.

METHODS From 1984 to 1992 I conducted field and laboratory experiments on the effects of incubation temperature on behaviour of pine snakes hatchlings. Herein I report on experiments conducted in 1985–1990 on antipredator behaviour. In these years I incubated pine snake eggs at three different temperatures: low (22–23C, N=160), medium (27–28C, N=261), and high (32–33C, N=188). These temperatures are within the range of temperatures found in pine snake nests in the wild which range from 21 to 35 (average of 282.2C, Burger & Zappalorti 1988). I maintained noncycling incubation temperatures even though the temperature in natural nests varies, but other researchers have found no differences when comparing noncycling with cycling incubation temperatures (Bull 1985; Lang et al. 1989). Under appropriate state and local permits, clutches were obtained from natural nests or from females brought into the laboratory to lay. All procedures were approved by the Rutgers University Animal Review Board, followed the ‘Principles of laboratory animal care’ (NIH publication. Number 85–23, revised 1085), and were monitored by the University veterinary staff. Information on hatching rates can be found in Burger & Zappalorti (1988). Females usually lay an average of eight to nine eggs. I divided the eggs from each clutch into thirds, and randomly assigned each third to one of the three temperature groups. The number of eggs per year in each of the three groups was 65–100. Eggs were placed on moist sand (45 ml water with 1000 ml of dry sand) in plastic shoe boxes, covered with moist sphagnum moss and placed in incubators. Every other day the sphagnum moss was squeezed dry, and 25 ml of water was added to the moss to maintain constant hydric conditions. The eggs in each box soon fused together, as they do in the wild. In 1985 I observed the emergence of 148 hatchlings without exposing them to any predator stimulus. During these observations, a snake could rest, explore, dig, or push. I defined exploring as movement in which the snake was tentatively touching different parts of its nest or tunnel, but was not actively pushing sand or digging

BURGER: ANTIPREDATOR BEHAVIOUR OF HATCHLING SNAKES 549

(moving sand with its snout). Thereafter, I tested all hatchlings under one of two sensory conditions: vibration and visual predators (four types). The four types of predators were: hawk (a small stuffed Buteo platypterus), person, head model with large eyes, and head model with no eyes. The head models consisted of a standard lightbulb (6 cm in diameter, and 8 cm long) covered with a white sock: one had no eyes and the other had black eyes (17 mm in diameter). Immediately upon hatching and coming to the edge, I placed each hatchling in an artificial nest and allowed it to emerge on its own. The artificial nest consisted of a cubic plastic container with two openings for emergence and was placed in the bottom of a 5-gallon aquarium. This ‘nest’ was covered with sand to approximate the natural situation. Hatchlings could remain in their nest, or burrow up towards the top to emerge. When they were half-way out of their burrow, my assistants and I exposed them to one of the five tests. The test a particular hatchling experienced was determined by a table of random numbers. The vibratory stimulus consisted of dropping a light stone at one end of the aquarium, 20 cm from the emerging snake; a visual barrier separated the emerging snake from the area where the stone was dropped. We moved all the visual stimuli towards the snakes at a 45 angle, starting 45 cm from the side of the aquarium, and moving over this distance in approximately 4 s. A mirror over the top of the aquarium was positioned so that the observer could see the response of the snake without being visible to the emerging hatchling. We recorded the following information for each test: snake number, age of snake, time of day, incubation temperature, room temperature, test type, time to respond, protective response (scored 1–10), defensive response (scored 1–10), time to resume any activity, and the activity resumed, as well as whether a snake that returned to its nest emerged from its original tunnel or dug a new tunnel (and where the new tunnel was located relative to the ‘predator’). The activity resumed could be the same activity as before the disturbance (score of 1), a different protective response (score of 2), a defensive activity (score of 3), or a different activity altogether, such as poking at the egg shells (score of 4). Snakes can emerge from the same tunnel (score of 1), from a different, but nearby tunnel (score of 2), or from a newly dug distant tunnel (score of 3). The protective response score included: 1: no response; 2: stopped and remained immobile; 3: withdrew slowly, partially into the tunnel; 4: withdrew slowly, but completely into the tunnel; 5: withdrew rapidly into the tunnel; 6: withdrew rapidly into the tunnel and slowly into the nest; 7: withdrew more rapidly into the nest; 8: withdrew into the nest and immediately started to dig a side chamber; 9: withdrew into the nest and started to dig an emergence tunnel; 10: withdrew into the nest and immediately emerged from a new emergence tunnel. The defensive response was scored as: 1: form a loose coil; 2: form a tight coil; 3: short and soft hiss; 4: long and loud hiss; 5: coil and short hiss; 6: coil and long hiss; 7: coil, hiss and short rattle of tail; 8: coil, hiss and long rattle of

tail; 9: coil, hiss, rattle and strike within 5–15 s; 10: coil, hiss, rattle and immediate strike. At the conclusion of the experiments each year, all hatchlings were returned to the field to their original nests and allowed to emerge on their own. We hatched pine snakes in the laboratory as a conservation measure under the auspices of the Endangered and Nongame Species Program (New Jersey Department of Environmental Protection), as poachers can take up to 40% of the clutches, and others are taken by predators (Burger et al. 1992). By hatching them in the laboratory we ensured a higher survival rate than would occur in the wild. Means and standard errors were obtained for the variables, and significant differences among temperature classes were determined with a nonparametric analysis of variance yielding a chi-square statistic. A multiple regression model procedure (SAS, Proc GLM; SAS Institute 1985) was performed on the data to determine the best models explaining variations in protective response, defensive response, time to respond, and time to resume any activity after the disturbance as a function of the independent variables (predator type, incubation temperature and an interaction of these two variables). Variables were selected for the model using a stepwise regression procedure which selects the factor that contributes the most to the R2, and then selects the second variable that increases it the most. Thus, variables that vary colinearly are not entered in the model. RESULTS There were significant models for time to respond, protective response score, defensive response score and time to resume activities (Table 1). Predator type was a significant contributor to all except the model for defensive response, and incubation temperature was a significant contributor to all models except the one for time to resume after the disturbance. An interaction between incubation temperature and predator type existed only for the protective response model (Table 1). Predator type influenced the response of the pine snake hatchlings. They responded to most predator types with an average latency of 2 s, except to the head model without eyes (Fig. 1). They required significantly longer to respond to the white head model than to all other stimuli. However, their protective response score was lower for the vibratory stimulus compared with the visual predator types (Duncan multiple range test). Furthermore, fewer hatchlings withdrew into their tunnel or nest when exposed to the vibration than when exposed to the visual predator models. The intensity of their protective responses are shown in Fig. 2. Over half of the hatchlings responded to the hawk and person model by withdrawing completely into their nests (and some began to dig another entrance out of the nest), but only 36 and 4% did so to the head without eyes and to the vibration, respectively (Fig. 2). Hatchlings responded to the vibration by remaining immobile or giving no response. There were no significant differences in their protective response as a function of predator type.

550 ANIMAL BEHAVIOUR, 56, 3

Table 1. Importance of predator type and incubation temperature to behaviour of pine snake hatchlings

Model F df P r2 Factors Predator type Incubation temperature Type×incubation temperature

Time to respond

Protective response

Defensive response

Time to resume activities

6.25 14,479 0.0001 0.25

6.39 14,479 0.0001 0.24

3.76 14,453 0.04 0.31

3.72 14,303 0.0001 0.23

19.5 (0.0001) 11.6 (0.0001) NS

21.2 (0.0001) 3.5 (0.01) 1.72 (0.05)

NS 3.76 (0.04) NS

12.0 (0.004) NS NS

GLM models are given. NS: nonsignificant.

Both emergence behaviour and antipredator behaviour were influenced by incubation temperature (Tables 1, 2). When hatchlings were undisturbed, the total time to reach the surface once a hatchling began to dig an exit tunnel varied as a function of incubation temperature

% Withdraw

100 80 60 40 20

Time to respond (s)

14 12 10 8 6 4 2 0

Protective responce

7 6 5 4 3 2 1 0

Defensive responce

0

5

DISCUSSION These experiments indicate that there are differences in behaviour as a function of both incubation temperature and predator type; thus I reject both null hypotheses. The results will be discussed in terms of each of these factors.

Incubation Temperature

4 3 2 1 0

(Table 2): hatchlings incubated at medium temperatures required significantly less time to reach the top than did the other hatchlings. Furthermore, the hatchlings incubated at medium temperatures spent less time with their heads out than did the other hatchlings (Table 2). Antipredator behaviour also varied significantly as a function of incubation temperature (Tables 1, 2), although the differences were not always as clear. In general, hatchlings that were incubated at medium temperatures had higher protective and defensive responses, and had a longer latency after the disturbance before they resumed any activity than did the other snakes (Table 2). These differences were clear for the protective response behaviours (Fig. 3, summarized across all predator types): a higher percentage of hatchlings incubated at medium temperatures withdrew completely into the nest and began to dig another side tunnel away from the original tunnel than hatchlings incubated at higher or lower temperatures (Fig. 3). Fewer than 20% of snakes incubated at medium temperatures showed no response or were immobile, while 30% of low-incubation and 38% of high-incubation temperature hatchlings did so.

Vibration

Hawk

Person

Head with eye

Head

Model Figure 1. Behaviour of pine snake hatchlings to different predator models. Values given are means±SE errors.

Hatchlings incubated at medium temperatures took less time to explore their nest and tunnels, required less time to reach the sand surface, and lingered for less time with their heads out than did snakes incubated at the other temperatures. These behaviours relate somewhat to vulnerability; hatchlings that are ready to emerge can reduce the total time they are vulnerable to predators by reaching the sand surface in less time, and remaining visible at the sand surface for less time before finding cover. This is particularly true for hatchlings emerging after siblings have already emerged and are moving about on the

BURGER: ANTIPREDATOR BEHAVIOUR OF HATCHLING SNAKES 551

% Hatchlings

60 50 40 30 20 10 0 60 50 40 30 20 10 0 60 50 40 30 20 10 0 60 50 40 30 20 10 0

High

(a)

(a)

40 30 20 10 0 Medium

(b)

(b)

40 30 20

(c)

% Hatchlings

60 50 40 30 20 10 0

10 0 Low (c)

40 30 20 10 0

(d)

All (d)

40 30 20 10 0

(e)

No Immobile Withdraw Withdraw Begin to response into into dig tunnel nest side tunnel Figure 3. Protective responses of pine snake hatchlings to all predator types as a function of incubation temperature: high, medium and low incubation temperatures, and at all temperatures combined.

No Immobile Withdraw Withdraw Begin to dig response into into side tunnel tunnel nest

Figure 2. Protective behaviour of pine snake hatchlings to (a) hawk model, (b) person, (c) head with eyes, (d) head without eyes and (e) vibration.

surface, attracting the attention of predators. Once the first snake in a nest has emerged enough to be visible to avian or mammalian predators, all the snakes in the nest and sand are vulnerable. Hatchlings that were incubated at medium temperatures required less time for all of these behaviours, and thus their total vulnerability time would be less in the wild. The protective scores of hatchlings incubated at medium temperatures were greater, while their defensive scores were lower than snakes incubated at high temperatures. Hatchlings incubated at high and medium temperatures responded significantly quicker than those incubated at low temperatures, but snakes incubated at medium temperatures remained motionless in the tunnel

or nest following disturbance longer than did hatchlings incubated at high or low temperatures. Taken altogether, hatchlings incubated at medium temperatures were quicker to withdraw into their nests or tunnels and waited longer to resume activity than other snakes, but a higher percentage immediately began to dig out in the opposite direction from the ‘predator’. Again, the responses of the hatchlings incubated at medium temperatures would reduce their vulnerability to predators by having a stronger protective response and waiting longer to begin emerging again.

Predator Type The major difference in response to predator type was between the vibratory and visual cues: hatchlings responded with lower protective responses, and a lower percentage of snakes withdrew into the tunnel and nest, in response to the vibration than they did to visual predators, although the time to respond was similar. In

552 ANIMAL BEHAVIOUR, 56, 3

Table 2. Emergence behaviour of pine snakes (1985) and response of hatchlings pine snakes to a predator as a function of incubation temperature (1986–1990). Values given are means±SE Incubation temperature

Emergence behaviour Number of snakes Minutes to rest Minutes to explore Minutes to dig Minutes to push Total to reach top Minutes with nose out Minutes with head out Antipredator behaviour Number of snakes Protective response* Defensive response† Time to respond Time to resume if snake withdrawn Activity resumed‡ Emerge from other tunnel§

Low

Medium

High

χ2 (P)

54 14.4±16.8 10.3± 2.7 13.6± 4.6 12.0± 2.6 50.3±16.0 0.9± 2.2 0.8± 0.5

46 8.3± 2.1 6.2± 0.8 15.8± 3.2 7.4± 1.4 37.7± 7.5 1.1± 0.3 0.3± 0.1

48 10.6± 1.5 12.4± 3.7 17.9± 2.7 9.5± 1.0 50.4± 6.2 2.4± 1.2 0.4± 0.1

NS 8.64 (0.01) NS NS 16.2 (0.005) NS 2.9 (0.08)

106 5.6± 0.4 1.6± 0.4 13.7±11.0 44.0±11.0 2.3± 0.2 2.4± 0.2

215 5.9± 0.2 2.4± 2.2 2.3± 0.7 60.6±10.0 1.9± 0.1 2.5± 0.2

140 4.6± 0.3 4.0± 0.8 2.3± 0.4 47.6±12.0 1.5± 0.1 2.2± 0.4

13.5 6.8 9.6 8.8 28.1

(0.001) (0.03) (0.008) (0.02) (0.0001) NS

*Where 1=no response, 8=rapid withdrawl and 10=complete withdrawl into the nest. †Where 1=poor coil and 10=strong strike response. ‡Where 1=same activity as before disturbance and 4=different activity. §Where 1=emerge from same tunnel and 3=emerge from newly dug distant tunnel.

most cases, the hatchlings may well be able to sense the slight vibrations of an approaching predator before it is visible, and remaining immobile or continuing to emerge may be warranted. Their response suggests that, in the absence of a visual cue, they do not withdraw into their nest, but freeze or move away. The similarity of response for the different visual predator types was surprising, although the time to respond was greater for the head model without eyes than to the other predator types. These data may indicate that the presence of any predator that moves within their visual field provokes an immediate response. Hatchling pine snakes also have a greater tendency to respond protectively by immediate withdrawal into their tunnels and nests than to behave defensively. This is clearly adaptive as most predators would be larger than the hatchlings, and more familiar than the hatchlings with above-ground surroundings. Without previous experience with seeking cover or cover types, the hatchlings would be quite vulnerable to most predators. Eyes appear to affect defensive behaviour of snakes (Herzog & Bern 1992) and lizards (Burger & Gochfeld 1990; Burger et al. 1991b). Garter snakes, Thamnophis sirtalis, have been shown to direct significantly more strikes at the side of a model with eyes than to the side without eyes, and direct their strikes at the eyes (Herzog & Bern 1992). Similarly, Burger et al. (1991b) showed that black iguanas, Ctenosaurus similus, retreat sooner from an approaching person with larger ‘eyes’ than they do from a person with eyes of normal size. The above experiments suggest that eyes are important both for defensive and offensive antipredator responses. Eyes are clearly important for predation, and in rattlesnakes, Crotalis viridis, predatory behaviour involves integration of information

from the eyes (Chiszar et al. 1986; Haverly & Kardong 1996), rather than just chemical cues as are used by natricine snakes (Halpern & Kubie 1983). In this experiment, hatchling pine snakes required longer to respond to the head without eyes than they did to the one with eyes, but the eventual responses were similar. Furthermore, all of the other predator types had eyes, to which all hatchlings responded equally quickly. These experiments corroborate the results of Herzog & Bern (1992) with garter snakes. Pine snake hatchlings without previous experience with predators responded differently to different ‘predator types’, and their behaviour was also influenced by incubation temperature. Overall, however, their responses to the predator models was to withdraw into their nests and tunnels, and wait before attempting to emerge again, rather than hissing, striking, or attacking the predators. Hatchlings incubated at medium temperatures seemed to have the lowest vulnerability time while emerging, and to behave more protectively than hatchlings incubated at either low- or high-incubation temperatures.

Acknowledgments I especially thank R. T. Zappalorti for continued interest, a wealth of field information, logistical help and field companionship; this is part of our on-going studies with pine snakes. I thank M. Gochfeld for helpful comments on the manuscript, and for spelling me in the laboratory so that I could get some sleep; as well as W. Boarman, B. Lauro, M. Caffrey, C. Safina, J. Saliva and T. Benson for laboratory and field assistance.

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