HERPETOLOGICAL JOURNAL, Vol. 14, pp. 79-87 (2004)

THERMAL EFFECTS ON THE ANTIPREDATOR BEHAVIOUR OF : A REVIEW AND PROPOSED TERMINOLOGY

AKIRA MORI1 AND GORDON M. BURGHARDT2

1 Department of Zoology, Graduate School of Science, Kyoto Un iversity, Sakyo, Kyoto 606-8502,

1 Departments of Psychology, and Ecology and Evolutionary Biology, University of Tennessee, Knoxville, 3 7996-0900 TN, USA

The effects of temperature on the antipredator responses of snakes have been extensively studied during the last two decades. Several contradictory results have accumulated concerning the effectsof temperature on the propensity of snakes to perform variousbehaviour patterns.We review this literature and discuss fourpossible factorsrelated to these apparently contradictory results: (I) inconsistency in terms used to characterize antipredator behaviour; (2) erroneous citations; (3) interspecific differences; and (4) variable experimental designs. The last two factorsreflect biologically important phenomena, whereas the firsttwo are artificial"noise" that causes confusion and hinders scientificinterpretation. To resolve inconsistency in wording, we propose a consistent terminology for the antipredator responses of snakes. Antipredator responses were characterized from three dimensions: (I) categorization fromthe viewpoint of

whether prey move towards or away from predators (response is considered as either "approach", "neutral", or "withdrawal"); (2) categorization from the viewpoint of how much movement is involved in the behaviour (response is considered either "locomotive", "active-in­ place'', or "static"); and (3) categorization in terms of the apparent function (response is characterized as either "threatening'', "cryptic", or "escape"). Antipredator responses of snakes, not only in relation to temperature but also in any situation, canbe well characterized fromthese three perspectives using the proposed terminology. Key words: defences,predator-prey interaction, , temperature effect

INTRODUCTION concerning the effects of temperature on the perform­ Various factors influence the antipredator responses ance of antipredator responses (e.g. striking) have that animals use when confronted with a predator. Al­ appeared in the literature, even among closely related though the behavioural repertoire and past experiences (see below). Such variable results among the of the individual are important, much studies could be attributable to differences in terminol­ intraspecific variation is due to contextual factors such ogy, responses measured, subject species, and as the presence of conspecifics, the nature and number experimental design. In thepresent paper we review and of the predators, the structureof the habitat, and climatic synthesize previous studies on temperature-dependent parameters such as light, humidity, and, especially for antipredator responses in snakes. In addition, we sug­ gest a consistent terminology for characterizing ectotherms, temperature (e.g. Burghardt & Schwartz, 1999; Magurran, 1999). antipredator responses of snakes to eliminatethis confu­ During the last two decades, more than a dozen ex­ sion. This will aid communication between different perimental studies have explored the effects of researchers studying different species in varying ways temperature on the antipredator responses of snakes. and will help clarifythe biologically significantsources of differences in antipredator responses among snakes. Because performance capabilities of ectotherrnic ani­ mals are temperature-dependent (Stevenson et al., REVIEW OF PREVIOUS PAPERS 1985), antipredator responses that vary with tempera­ ture are usually considered adaptations for coping with We located twenty-fourpapers that mentioned or sys­ physiological constraints. For instance, some snakes tematically examined thermal dependency of simplyflee at high body temperature and exhibitless lo­ antipredator responses of snakes (Table 1 ). Most stud­ comotive antipredator responses at low body ies dealt with North American snakes: exceptions are temperature, because physiological mechanisms do not Natrix in Europe, in Japan, Gloydius in allow themto crawl fast enough to avoid predation (e.g. , and Pseudonaja in Australia. Taxonomically, the Hailey & Davies, 1986; Mori & Burghardt, 2001 ). How­ subjects include colubrids - especially natricines - a ever, in the past decade, contradictory results few crotalines and one elapid. Except fora few earlier studies, the results are based on well-designed experi­ Correspondence: A. Mori, Department of Zoology, Graduate ments conducted either in the field or in the laboratory. School of Science, Kyoto University, Sakyo, Kyoto 606- The most overt discrepancy among the studies was 8502, Japan. E-mail: [email protected] the inclination of the snakes to exhibit strikes and/or 80 A. MORI AND G. M. BURGHARDT

bites. Several studies found that snakes are more apt to and create a potential source of confusion in subsequent strike at low temperature (Arnold & Bennett, 1984; studies. Fitch, 1965; Goode & Duvall, 1989 [but only in preg­ nant females]; Heckrotte, 1967; Shine et al., 2000), (3) INTERSPECIFIC DIFFERENCES IN RESPONSE TO whereas others showed that snakes tend to strike at high TEMPERATURE temperature (Keogh & DeSerto, 1994; May et al., 1996; It is not surprising that different species may respond Schieffe lin & de Queiroz, 1991; Shine et al., 2002). In differently to changes in temperature (Shine et al., addition, some studies failedto find any temperature ef­ 2000). Snakes have adapted to various ecological niches fects on the tendency to strike, bite, or bluff(Gibbons & with tremendous physiological, morphological, and be­ Dorcas, Goode & Duvall, 1989 (in males and 2002; havioural specialization (Greene, 1997), and show non-pregnant females); Mori & Burghardt, Mori 2001; varied antipredator responses even among closely re­ 1996; Scribner & Weatherhead, 1995; Whitaker et al., lated species (Bowers et al., 1993; Herzog & Burghardt, These apparently contradictory results and et al., 2000). 1986) or among populations of the same species associated confusion can be attributed to the following (Burghardt & Schwartz, 1999; Mori & Burghardt, four factors. 2000). Thus, it is likely that closely related species have evolved different adaptive responses to changes of tem­ (I) INCONSISTENCY OF WORDING CONCERNING THE perature. The absence of temperature effects may simply CHARACTERIZATION OF ANTIPREDA TOR RESPONSES reflect the low tendency in performing the focused re­ Many adjectives have been used to express the pro­ sponses (e.g. strike in Rhabdophis tigrinus: Mori & pensity to perform antipredator responses by snakes: Burghardt, 2001). In addition, when interspecific com­ "aggressive", "offensive", "defensive'', "passive'', parisons are made, we should keep in mind the fact that "threatening", "static", "active", "retaliatory" and so species have different preferred body tempera­ on. Heckrotte ( 1967) used the term, "defensive"behav­ tures (Lillywhite1987; Mori et al., 2002, and the iour, apparently to indicate biting, and Goode & Duvall references therein), and thus, "low" body temperature (1989 ) regarded the snakes that more rapidly escalated for a given species may not be necessarily "low" for an­ to striking as being more "defensive." On the other other species. In some species (e.g. T. ordinoides and R. hand, Arnold & Bennett (1984) applied the term "de­ tigrinus) consistent individual differences in response to fensive" to responses such as head-hide and body-ball. temperature can also occur (Brodie & Russell, 1999; The term "defensive" behaviour has also been used as a Mori & Burghardt, 2001). synonym of antipredator behaviour, or even used for any kind of behaviour that protects an animal from (4) DIFFERENCES IN EXPERIMENTAL DESIGN conspecifics as well as predators (Edmunds, 1974; The most important problem underlying inconsistent Immelmann & Beer, 1989). results may arise from differences in experimental de­ Another example of confusion is found in the term sign. This is not a minor problem, because it underlies "active". Arnold & Bennett (1984) used "active" de­ an important issue in understanding the behavioural fe nce for head-hide and body-ball, whereas Hailey & mechanisms of animals. In most studies, flight responses Davies ( 1986) used "active" defence for escape re­ are observed or enhanced at higher temperatures (Table sponse and called balling a "static" defence. Kissner et 1). Among the eight studies using Th amnophis, how­ al. ( 1997) labeled rattling by rattlesnakes as "active" ever, this trend was observed only in five (Brodie & defense in contrast to crypsis. Prior & Weatherhead Russell, 1999; Fitch, 1965; Heckrotte, 1967; Passek & (1994) considered biting an "active" defence. Gillingham, 1997; Shine et al., 2000). This does not necessarily imply that the remaining three studies (2) ERRONEOUS OR EQUIVOCAL CITATIONS (Arnold & Bennett, 1984; Schieffelin & de Queiroz, Keogh & DeSerto (1994) mentioned that the study 1991; Scribner & Weatherhead, 1995) showed the ab­ by Arnold & Bennett ( 1984) showed an increased flight sence of an increased flight response at higher response of Th amnophis radix at higher temperature. In temperature. Rather, this difference in results is clearly fact, Arnold & Bennett (1984) did not include a flight related to differences in experimental protocols. In the response in their variables; their experimental protocol latter studies they had no opportunity to show flight re­ did not allow them to record any kind of flight response sponses because the snakes were continuously followed (see below). Passek & Gillingham ( 1997) mentioned by the stimulus (human hand) (Scribner & Weatherhead, that their results are inconsistent with the findings of 1995) or were scored after they became exhausted Schieffelin & de Queiroz (1991 ). However, both studies (Arnold & Bennett, 1984) or motionless (Schieffelin & showed that energetically costly responses involving de Queiroz, 1991). These authors did not include much movement are more frequently exhibited as tem­ "flight" in the available options ofbehavioural variables. perature increases, and thus, their "inconsistency" is Another potentially confounding factor is the effect of equivocal. As has already been pointed out by test order of stimulus and thermal condition (Burghardt Schieffelin & de Queiroz ( 1991 ), a cursory examination & Schwartz, 1999). As pointed out by various authors of previous studies may lead to erroneous conclusions (Arnold & Bennett, 1984; Schieffelin & de Queiroz, TERMINOLOGY FOR SNAKE ANTIPREDATOR RESPONSES 81

1991), the temperature effects observed by Arnold & In this perspective, strike and neck-butting are consid­ Bennett (1984) may have been confounded with order ered approach responses, body-flatten, tail-vibration, effects, which resulted in thermal effects different from and immobilization are categorized as neutral re­ those obtained by Schieffelin & de Queiroz ( 1991 ). Bal­ sponses, and flightis considered a withdrawal response. ancing testing order of different conditions is typically Second, antipredator responses can be categorized the mo st effective means of dealing with the test order fromthe viewpoint of how much movement is involved problem (but see Burghardt & Schwartz, 1999, for prob­ in the behaviour. From this viewpoint, the flight re­ lems that mightstill exist even with balanced test orders, sponse is considered the most "locomotive" reaction, such as differential habituation effects). whereas immobilization or freezing is characterized as The inconsistencies in results noted above may also the most "static" response. Several common responses reflect differences in the internal conditions of the ani­ such as strike and tail-vibration would be considered mals. Snakes often shift antipredator responses "active-in-place" responses because they involve move­ sequentially (Bowers et al., 1993; Duvall et al., 1985; ment of body parts without any locomotion. This · Schieffelin & de Queiroz, 1991). This behavioural se­ categorization partially reflects the amount of energy quence may reflect motivational and/or physiological requited for performing various antipredator responses. changes of snakes throughout the interaction between This strictlybehavioural typology in terms ofmovement the prey and the predator. The snakes tested by Arnold dols not rule out the possibility that different responses & Bennett (1984) were undoubtedly in the final stage of have varying energetic consequences for different the sequence because behaviours were recorded when snakes. We envision that phylogenetic analyses of the snakes were exhausted after being chased down a antipredator repertoires and their contextual deploy­ track, whereas the snakes tested by Schieffelin & de ment could be useful adjuncts to studies of metabolism, Queiroz ( 1991) were in earlier stages of the sequence. muscle physiology, and foraging mode. Passek & Gillingham ( 1997) quickly uncovered com­ Third, antipredator responses can be viewed in terms mon garter snakes in retreats, and the flight response of their apparent function. If a response involves any they observed represented the initial stage of the behavioural element apparently designed to deter the in­ antipredator behavioural sequence. It is also possible truding predator from attempting predation, the that captive-induced motivational and/or physiological response can be called "threatening". Representative modification, such as recent feeding (Ford & threatening responses are strike, bluff, hissing, rattling, Shuttlesworth, 1986; Herzog & Bailey, 1987) and other and body-flatten. In this system, antipredator responses unintentional treatments, could affect the responses of such as immobilization and head-hide are considered snakes (Shine et al., 2000). "cryptic" because these behaviours rely on reducing the probability that the predator will recognize the animal as PROPOSED TERMINOLOGY prey. Snakes that are aposernatically coloured or The above four factors can be divided into two cat­ marked may be immobile, as are cryptic prey, but may egories. Differences in results due to interspecific engage in some behaviour to enhance the antipredator differences and differences in experimental design po­ display (e.g. Greene, 1973; Mori & Hikida 1991). Func­ tentially reflect biologically significant phenomena, tional interpretations are more difficult to confirm than whereas inconsistency of wording and erroneous cita­ the mere description used in the other two perspectives tions represent artificial "noise" that can create but are also a key aspect of biological inquiry. Flight is confusion and hinderun derstanding. To remove confu­ considered a protective response labeled as "escape": sion caused by semantic differences attached to words althoughthe snake may reveal its presence, it acts to re­ used to characterize the responses we have attempted to duce the probability of capture not by actual deterrence, integrate the terminology and provide new defmitions but by removing itself from the situation. Other exam­ applicable to antipredator responses of snakes. Defin­ ples of"escape" responses are evasive movements such ing behaviour patterns from multiple viewpoints would as reversal of direction during flight(e.g. Brodie, 1993 ). be useful to understand the nature of those behaviours We do not use the word "defensive" as the antonym of (Drummond, 1981 ). We begin by showing that "threatening" in order to avoid confusion (see above). antipredator responses can be characterized in at least APPLICATION three dimensions. First, they can be viewed from changes in the dis­ It is useful to characterize antipredator responses tance between predators and prey. If a behaviour from all three perspectives. As an example, we did this involves prey movement that reduces this distance, it for the antipredator behaviours of R. tigrinus recorded can be called an "approach" response. Conversely, if a in Mori & Burghardt (2000, 2001). One of the most behaviour involves prey movement that increases this characteristic behaviours is the neck arch, in which the distance, it can be called a "withdrawal" response. All snake raises the head slightly and strongly bends the an­ responses that do not involve active movement by the terior part of the neck region ventrally so that the snout prey that decreases or lengthens the distance between is directed to, and makes contact with, the substrate. We the prey and the predator we term "neutral" responses. would label this a neutral, static, threatening response TABLE 1. Review of the temperature effects (either ambient or body temperature) on antipredatorresponses in snakes. Terminology of responses followsorigina l description of each reference. 00 N a, only pregnantfe males showed temperature effects; b, no effect ofwater temperature on flight distance; c, no effect of water temperature on strike; d, no effectof body temperature on flee; e, no effectof body temperature on gape; f, the description of the original paper is unclear; g, no effect of temperature on bluff; h, time until strikeis longer at intermediatetemperatur e; i, no effect of temperature on response (flee, bite, gape etc.); n.a., not applicable.

Responses Species Age class Observation Procedure Authority Lower temperature Higher temperature

Rhabdophis adult body-flatten, neck-arch escape anecdotal n.a Fukada (1961) tigrinus

Thamnophis unknown threatening behaviour, strike speedy escape anecdotal n.a Fitch ( 1965) sirta/is flatten, coil, aggressive > T. sirtalis various defensive behaviour, bite flight anecdotal n.a. Heckrotte(1 967) � R. tigrinus various feigndeath n.a field restraint Mutoh (1983) 0 � T. radix neonate offensive (high score), strike defensive (low score) laboratory tap or hold after Arnold & Bennett > aggressive, body-flatten active defence,head-hide ceasing to move (1984) z body-ball (scoring) t:I

Regina adult shorter flight distance longer flight distance field approach Layne & Ford (1984) p septemvittata � t:c:I Natrixmaura various static defence, ball active defence, escape laboratory place on arena Hailey & Davies (1986) � 0 Crotalus viridi,sA adult short durationto strike long duration to strike field grasp by tongs Goode & Duvall (1989) more defensive less defensive � static defence attempt to escape E; >-3 T.sirtalis various head-hide strike, tail-wave, bite laboratory poke andtap by finger Schieffe lin & de Queiroz (except passive static defence aggressive coil (scoring) (1991) neonate) (low score) aggressive static defence more active (highscore)

Nerodia sipedonb various n.a n.a field approach Weatherhead & Robertson (1992)

Coluber various passive defensivedisplay strike laboratory touch then thrust hand Keogh & DeSerto constrictor head-hide, tight coil (high score) (scoring) (1994) (low score)

Lampropeltis ditto ditto ditto ditto ditto ditto ca//igaster

Pituophis ditto ditto ditto ditto ditto ditto melanoleucus Table I continued ...

Sistrurus adult (?) negative, no reaction positive, rattle field step closely Prior & Weatherhead catenatus remain stationary rattle while flee (1994)

N. sipedon< various more refuge-seeking n.a. laboratory chase while swimming Scribner & Weatherhead more predator-disorienting in water (1995) """3 tr.1 T.sirtalis< ditto more predator-disorienting n.a. ditto ditto ditto � T.sauritus< ditto ditto n.a. ditto ditto ditto 0z t""' S. miliarius'1 various n.a. strike field approach or tap on head May et al. (1996) 0 a Rhabdophis adult & body-flatten, neck-flatten flee laboratory pin by hook or tap by Mori et al. (1996) -<: tigrinus neonate neck-arch, immobilize hand 'T1 0 Crotalus viridi� � v. adult closer distancebefore ratt ling longer distance before field approach Kissner et al. (1997) t/) rattling z > sirtalis< body-flatten � T. adult (?) flee, bite (?)f field approach or grab by Passek & Gillingham tr.1 hand (1997) > z T. ordinoides neonate fewerreversals more reversals laboratory tap by hand Brodie & Russell """3 crawled short distance crawled long distance (1999) =a

Pseudonaja texti/is various shorter flightdistance longer flightdistance field approach Whitaker & Shine f;l tJ remain stationary flee (1999) > """3 T.sirta/is adult remain still, strike flee field peck by finger Shine et al. (2000) 0 body flatten � � tr.1 P. textilis&- b adult n.a. n.a. laboratory wave or touch with Whitaker et al. (2000) t/) "'C stimuli 0 z R. tigrinus adult body-flatten, neck-flatten flee laboratory pin by hook Mori & Burghardt t/) tr.1 neck-arch, immobilize (2001) t/) dorsal facingposture

Gloydius adult & no overt response flee, strike,tail-twitching field approach and tapby Shine et al. (2002) shedaoensis juvenile stick

Agkistrodon various n.a. n.a field standbeside, step on, Gibbons & Dorcas piscivorusi and pick up (2002)

00 \,;J 84 A. MORI AND G. M. BURGHARDT

TABLE 2. Characterization of antipredator responses of Rhabdophis tigrinus tigrinus (afterMori & Burghardt, 200 I) and other common antipredator responses of snakes from three independent viewpoints. Definitions of terminologyare presented in text.

BEHAVIOUR CHANGE OF DISTANCE: AMoum OF MOVEMENT: APPARENT FUNCTION:

Withdrawal (W) Static (S) Escape (E) Neutral (N) Active-in-place (Ac) Cryptic (C) Approach (Ap) Locomotive (L) Threatening (T)

Strike Ap Ac T Neck-flatten N s T Body-flatten N s T Neck-arch N s T Neck-butting Ap Ac T Jerk N Ac T Immobile N s c Flee w L E Reversals NIW L E Head hide N s c Tail vibration N Ac T Rattling N Ac T Feign death N s c Hissing N s T Cloacal discharge N s T Body thrash N L T

TABLE 3. Characterization of anti predator responses of snakes observed in temperature-effect studies listed in Table I. Responses in parentheses indicate the increased tendency of the responses at the temperature. Ac, active-in-place; Ap, approach; C, cryptic; E, escape; High, higher temperature; L, locomotive; Low, lower temperature; N, neutral; S, static; T, threatening; W, withdrawal. Definitions of terminology are presented in text. •Only in pregnant females.

CHANGE OF AMOUNT OF APPARENT DISTANCE MOVEMENT FUNCTION

Authority Low High Low High Low High

Fukada (1961) N w s L T E Fitch (1965) N, Ap w S, Ac L T E Heckrotte ( 1967) Ap w Ac L T E Mutoh (1983) N s c Arnold & Bennett (1984) N, Ap N S, Ac s T c Layne & Ford (1984) (W) (L) Hailey & Davies (1986) N w s L c E

Goode & Duvall (1989) • Ap w Ac L T E Schieffelin & de Queiroz (1991) N N, Ap s Ac c T Weatherhead & Robertson ( 1992) Keogh & DeSerto (1994) N Ap s Ac c T Prior & Weatherhead (1994) N N, W s Ac, L c T, E Scribner & Weatherhead ( 199 5) May et al. ( 1996) Ap Ac T Mori et al. ( 1996) N w s L T, C E

Kissner et al. (1997) • (C) (T) Passek & Gillingham ( 1997) N w s L T E Brodie & Russell (1999) (W) (L) Whitaker & Shine ( 1999) N w s L c E Shine et al. (2000) N, Ap w S, Ac L T, C E Whitaker et al. (2000) Mori & Burghardt (2001) N w s L T, C E Shine et al. (2002) N Ap, N, W s Ac, L c T, E Gibbons & Dorcas (2002) TERMINOLOGY FOR SNAKE ANTIPREDA TOR RESPONSES 85

(Table 2). Although neck-arch may not deter predation needs to be more recognition and careful consideration by itself, it may attractthe attention of the predator to the of the various factors that can affect behavioural re­ nuchal glands, and the secretions from the glands may sponses, especially when the animal has several act as a predator deterrent (Mori et al., 1996; Mori & behaviouraloptions that change sequentially. These fac­ Burghardt, 2000, 200 l ). Thus, functionally, neck-arch tors can include changes in internal factors such as can be regarded as a threatening response. Another char­ motivation and physiological condition (stress level,re­ acteristic behaviour of R. tigrinus is neck butting, in cent feeding, reproductive state, ecdysis). Most which the snake swings its head backwards with erratic behavioural responses are the results of an interaction movements so that the dorsal part of the neck region is between external and internal factors (Mook, 1996). Al­ butted against the stimulus object. This behaviour is though it may not be possible to control all the internal labeled as an approach, active-in-place, threatening re­ factors during an experiment, such internal factors sponse. These three perspectives also help characterize should be considered when comparing studies. As with the nature of components revealed by principal compo­ any complex behaviour that varies within and across nents analysis of behaviour at different temperatures species, it is importantto eliminate any artificial confu­ (see Mori & Burghardt, 2001). sion and precisely focusour attention on the real sources Using this terminology, some of the antipredator re­ of differences. The aim of the present paper is not only sponses listed in Table 1 are characterized as follows. to review the literature on the thermal effects on Head hide: neutral, static, cryptic response; tail vibra­ antipredator responses in snakes, but also to call re­ tion: neutral, active-in-place, threatening response; searchers' attention to the existing confusion of rattling: neutral, active-in�place, threatening response terminology and propose a resolution. We have to admit (Table 2). Death feigning is one of the most dramatic that our proposed terminological categorization par­ and complex antipredator responses in snakes. Because tially relies on a subjective judgment of the adaptive such immobility may induce predators to divert their at­ function of the snake's behaviour (e.g. threat, escape) tention from the dead prey or make them not recognize it and thereby infer the animal's "intention". Such judge­ as "food"(Burghardt & Greene, 1988), this behaviour is ments are actually at the heart of much behavioural considered neutral, static, and cryptic. Other common research, but such testable inferences can be usefully antipredator responses in snakes (Greene, 1988) can be derived through a judicious application of critical an­ effectively characterized {Table 2). thropomorphism (Rivas & Burghardt, 2002). We hope As an overview of the temperature effects on that our attemptto remove terminological confusionwill anti predator responses of snakes, all the antipredator re­ help to clarify biologically relevant mechanisms that · sponses listed in Table 1 are characterized from the cause different behavioural responses of snakes under three viewpoints and summarized in Table 3. General different thermal conditions, and in other contexts as tendencies, as well as the similarities and discrepancies, well. in antipredator responses among the previous studies are easily understood using this table. In the change of dis­ ACKNOWLEDGEMENTS tance dimension, withdrawal is a predominant response We are grateful to P. R. Andreadis, L. Almli, R. at higher temperature and never observed at lower tem­ Mehta and J. Placyk fortheir usefulcomments on earlier peratures. Obviously, all studies except forone (Arnold draftsof the manuscript. The research was partially sup­ & Bennett, 1984), which did not include flight as a re­ ported by a grant from the Japan-US Cooperative sponse variable, show the same tendency in the amount Science Program (Japan Society for the Promotion of of movement: as temperature increases, snakes change Science awarded to AM, and the National Science their responses from static to locomotive ones. In the Foundation, INT-95 13100 awarded to GMB). 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