Spontaneous Immobility of the Japanese Lacertid Lizard, Takydromus Tachydromoides

Spontaneous Immobility of the Japanese Lacertid Lizard, Takydromus tachydromoides

AKIRA MORI

Abstract: Frequencies of movement, as an index of propensity for immobility, of Takydromus tachydromoides were measured in the encounters with a potential predator Elaphe quadrivirgata (Session A) or a sympatric non-predator Eumeces latiscutatus (Session B), or in the absence of other animals (Session C). Frequency of movement in Session A was significantly lower than in Sessions B and C. In Session B, T. tachydromoides moved significantly less frequently during the first 10min than during the latter 10min. The lizards previously exposed to E. quadrivirgata reduced their movements in the subsequent Session B with significantly high frequency when compared with animals without such experience. It is suggested that immobility of T. tachydromoides is an adaptive antipredator behavior to avoid detection by a visually orienting predator. Key words: Immobility; Takydromus tachydromoides; Antipredator behavior; Elaphe quadrivirgata; Lacertidae

Lizards employ a variety of morphological mobility of iguanids and gekkonids in which the and behavioral antipredator mechanisms. animal was held so that movement was impossi- Greene (1988) summarized reptilian antipredator ble and restrained until tonic immobility resulted mechanisms and listed 60 phenotypic categories, (e. g., Gallup, 1973; Hennig, 1979; Herzog, including concealing coloration, immobility, 1984), few quantitative studies have locomotor escape, and tail display. It is certain demonstrated immobility of lizards voluntarily that almost all lizard species possess more than exhibited in the presence of a predator. one defensive tactic and several lizards respond Takydromus tachydromoides, a slender, fast- with different antipredator behavior according moving lacertid lizard possessing a long to the environmental and/or situational contexts autotomous tail (Fukada and Ishihara, 1967), which they confront (e. g., Hennig, 1979; Thoen has a brownish body coloration which makes et al., 1986; Greene, 1988). this animal very inconspicuous in grassy areas "S pontaneous immobility" (or freezing) can where it usually lives. In staged predatory en- be distinguished from "tonic immobility" (or counters, this lizard exhibits several antipredator animal hypnosis), a behavioral response to behaviors according to situational contexts restraint in which the animal appears to be (Mori, 1990). As in other animals, the initial unresponsive to stimulation (after Herzog, 1984; response of T. tachydromoides seems to be im- Greene, 1988), yet different definitions of these mobility to avoid detection by a predator. In two wordings are seen in some papers (e. g., this paper, I demonstrate that the spontaneous Brodie et al., 1974). Immobility, often coupled immobility of T. tachydromoides is elicited by with cryptic coloration, is considered to be the in- the presence of a predator. As a result, this itial antipredator response that increases the pro- behavior is interpreted as one of the antipredator bability that the prey will escape detection by tactics of this lizard. visually orienting predators (e. g., Heatwole, 1968; Brodie et al., 1974, Gregory, 1979). On MATERIALSAND METHODS the other hand, tonic immobility is usually the The subjects were 19 adult Takydromus tachy- final behavioral stage which is elicited after exter- dromoides (7 males and 12 females; snout-vent nal restraint (see Arduino and Gould, 1984). length, 46-61mm) collected from Osaka (N=2) Although there are several studies on tonic im- and Kyoto (N=10) Prefectures, and Kuchinoshima (N=4) and Takeshima (N=3) Accepted 6 Mar. 1991 Islands in Kagoshima Prefecture, Japan. 2 Jpn.J.Herpetol.14(1).1991

Lizards from the latter three groups included the maintained between 27.0-30.5°C during the ex- same individuals used in another experiment periment. (Mori, 1990). There were no obvious All trials were recorded with a video tape behavioral differences observed between the four monitor (National NV-8480, VHS type) and a groups. All lizards were housed individually in color video camera (National VZ-C70). Pro- clear plastic cages (315×170×235mm) with a pensity for immobility was evaluated by quanti- water bowl and a shelter, and were maintained fying the frequencies of movement by videotape under a natural photoperiod for two to four analyses. The bottom of the arena was divided months before the experiments. The room into eight equal sections, and the number of temperature varied between 17 and 31℃. They times the lizard changed sections was counted (i. were fed mealworms two or three times per e., amount of movement). The frequency of week. Water was available ad libitum. movement (FM) was calculated for each session

The testing arena (650×400×250mm) was as (amount of movement) / (observed dura- made of white polypropylene corrugated board tion). In all B and C sessions, duration of obser- except for a transparent plastic ceiling, and con- vation was 20min. It is likely that the actual tained a cardboard floor marked with 2cm snake attack affected the behavior of T. tachy- grids. The arena was divided into two chambers dromoides, especially in the frequency of move- (large: 510×400×250mm, and small: ment. Thus, in Session A, observation was ter- 140×400×250mm) by a plastic insert which minated when the snake first attacked or pursued could be removed from the arena by sliding it the lizard. Escape movements of T. tachydro- out through a slit at the front wall. After each moides after the attack of the snake were not in- trial, the arena was washed with water and the cluded in the amount of movement. Conse- cardboard floor was replaced. quently, the observation period varied from 0.33 Trials consisted of three sessions. T. tachy- to 20min (x=8.3min) in Session A. dromoides was introduced into the large Statistical significance was tested by Mann- chamber and a Japanese striped snake, Elaphe Whitney's U-tests or Wilcoxon signed-ranks quadrivirgata (a well known natural predator of tests (between two samples) and Friedman two- T. tachydromoides: Mori and Moriguchi, 1988: way ANOVA (among three samples) followed Session A), or Eumeces latiscutatus (a sympatric by multiple comparisons (Siegel and Castellan, scincid lizard but not a possible predator of T. 1988). tachydromoides: Session B, control for the presence of a non-predator animal) was introduc- RESULTS ed into the small chamber. In Session C, only Two T. tachydromoides never moved for T. tachydromoides was introduced into the 20min in Session A in which the snake also arena in the absence of other animals (control remained motionless. Other 11 lizards remain- for experimental milieu). Each T. tachydro- ed motionless until the snake closely approach- moides was tested in all the three sessions in non- ed, and then, the lizards escaped by running, fixed order. Each session was initiated by the which was followed by the attack of the snake. removal of the insert from the arena and lasted On the other hand, only one individual remained for 20min at most (see below). A ten-minute in- immobile throughout in both Sessions B and C. terval was allowed between sessions. A total of The type of session affected FM of T. tachy- 11 E. quadrivirgata were used for Session A (one dromoides significantly (X2r=19.6, dF=2, to three trials per individual). Temperature was p<0.001). The FM was significantly lower in

TABLE 1. Amount of movement (AM), duration of observation (OD) and frequency of movement (FM=AM/OD) of Takydromus tachydromoides in encounters with Elaphe quadrivirgata (Session A) or Eumeces latiscutatus (Session B) and in the absence of other animals (Session C). The FM is also calculated for the first and latter 10min separately, for Sessions B and C. MORI-LIZARD IMMOBILITY 3

Session A (x=0.59) than in Sessions B and C TABLE2. Frequency of movement (FM) of Taky- (x=2.14 and 2.72, respectively; p<0.05; Table dromus tachydromoides in the encounters with 1). There was no significant difference in FM Eumeces latiscutatus for the first and the latter between Sessions B and C (p>0.05). 10 min of the observation period. T. tachydro- Because duration of observation in Sessions B moides was exposed to a snake (Session A) prior and C (20min) was much longer than in Session to Session B (A-B) or not (B-A). A (x=8.3min), it is possible that the higher FM in the former two sessions may reflect the effect of acclimation of T. tachydromoides to the arena rather than the reducing effect of the presence of a predator in Session A. Therefore, Sessions B and C were partitioned into 2 10-min blocks, and a Wilcoxon signed ranks test was conducted in Sessions B and C separately. The analyzed using the data from 12 trials where Ses- FM for the first 10min in Session B (x=1.61) sion B was conducted prior to Session A. As for was significantly lower than that for the latter Sessions B and C only the first 10min data were 10min (x=2.68; z=-3.00, p<0.01). There used. The FM was significantly affected by the was no significant difference in FM between the type of sessions (x2r=18.2, dF=2, p<0.001). first and latter 10min in Session C (z=-0.57, The FM in Session A (x=0.26) was significantly p>0.05). lower than in Sessions B and C (x=2.17 and Comparison of FM among the three sessions 3.60, respectively; p<0.05; Table 3). There was was made again, but this time only the first no significant difference in FM between Sessions 10 min data were used as for Sessions B and C B and C (p>0.05). As for the latter 10min, because the time effect was significant in Session there was no significant difference in FM bet- B (see above). The type of session significantly ween Sessions B and C (x=3.41 and 3.58 respec- affected the FM (x2r=19.7, dF=2, p<0.001). tively; z=-0.67, p>0.05). The FM in Session A (x=0.59) was significantly lower than in either Session B or C (x=1.61 and DISCUSSION 2.83, respectively; p<0.05). There was no Any behavioral antipredator adaptation significant difference in FM between Sessions B should be accompanied by the ability of the prey and C (p>0.05). to assess potential predation situations accurate- Another factor that may affect FM is the order ly. The primal stage of such situation of sessions. The lizard that had encountered a assessments is to judge whether an animal that snake seemed to immobilize more frequently in the prey confronts is dangerous (i. e., a predator) the subsequent sessions, especially in Session B. or not. It is clear that T. tachydromoides can Order effects were analyzed with Mann- discriminate predators from non-predators and Whitney's U-test for Session B. T. tachydro- reduces its own movement to avoid detection by moides, both in the first and the latter 10min, the former. This behavior may be adaptive moved less frequently in the presence of because in many species of predators including Eumeces latiscutatus after being exposed to a Elaphe quadrivirgata, prey movement is a snake than not (U=14 for the first and 15 for the critical factor in mediating attack (Herzog and latter, P <0.05 for each; Table 2). Burghardt, 1974; Ota, 1986). Finally, FM among the three sessions was Ducey and Brodie (1983) reported that the

TABLE 3. Frequency of movement (FM) of Takydromus tachydromoides observed in Sessions A, B, and C. Only the data of the trials in which Session B was conducted prior to Session A are presented. The FM is also presented for the first and latter 10min separately, for Sessions B and C. See Table 1 for explanations of sessions. 4 Jpn. J. Herpetol. 14 (1). 1991 type of contact with the same predator (body or tongue) affects the response of salamanders. LITERATURE CITED Although the sample size is very small, similar ARDUINO,P. J., JR. ANDJ. L. COULD. 1984. Is tonic results were also obtained in T. tachydromoides: immobility adaptive? Anim. Behav. 32 (3): 921-923. the lizard remained motionless when the snake BRODIE,E. D., JR., J. A. JOHNSONAND C. K. DODD, made contact with its body (2 cases), whereas the JR. 1974. Immobility as a defensive behavior in salamanders. Herpetologica 30 (1): 79-85. lizards which had immobilized started running DUCEY, P. K. AND E. D. BRODIE, JR. 1983. immediately after the snake made contact with Salamanders respond selectively to contacts with the head (3 cases). When to shift from immobili- snakes: Survival advantage of alternative an- ty to running escape may be crucial. If escape is tipredator strategies. Copeia 1983(4): 1036-1041. employed too early, the lizard may attract FUKADA,H. ANDS. ISHIHARA.1967. Autotomy in the predator's attention to itself if otherwise it could lizard, Takydromus tachydromoides (Schlegel). go unnoticed. Contact with the head of the Bull. Kyoto Univ. Educ., Ser. B (31): 27-32. snake increases the immediate strike threat as GALLUP, G. G., JR. 1973. Simulated predation and compared to nearness of a predator (body con- tonic immobility in Anolis carolinensis. Copeia tact), so the running escape may be more advan- 1973(3): 623-624. GREENE,H. W. 1988. Antipredator mechanisms in rep- tageous in such situations. Therefore, en- tiles. In: C. Gans and R. B. Huey (eds.), Biology of countering a predator, T. tachydromoides first the Reptilia. Vol.16, Ecology B, Defense and Life immobilizes to avoid detection, but if the disad- History. p.1-152. Alan R. Liss, Inc., New York. vantage of remaining motionless increases, it GREGORY,P. T. 1979. Predator avoidance behavior of shifts its defensive behavior to the next stages, the red-legged frog (Rana aurora). Herpetologica such as tail vibration or fleeing (Mori, 1990). 35 (2): 175-184. The presence of Eumeces latiscutatus, a non- HEATWOLE,H. 1968. Relationship of escape behavior predator, also affected the behavior of T. tachy- and camouflage in anoline lizards. Copeia 1968(1): dromoides especially in the earlier stage of the en- 109-113. HENNIG, C. W. 1979. The effects of physical environ- counter, but not so much as in the presence of ment, time in captivity, and defensive distance on snakes. Furthermore, T. tachydromoides reduc- tonic immobility, freezing, and flight behaviors in ed its activity much more in the presence of E. Anolis carolinensis. Anim. Learn. Behav. 7 (1): latiscutatus when it had been exposed to a snake 106-110. in the preceding encounter: T. tachydromoides HERZOG,H. A., JR. 1984. Tail autotomy inhibits tonic seems to be warier of another animal in such immobility in geckos. Copeia 1984 (3): 763-764. cases. This seems to reflect the effect of the HERZOG, H. A., JR. AND G. M. BURGHARDT.1974. earlier experience (Gregory, 1979) or the Prey movement and predatory behavior of juvenile responses to the remnants of chemical western yellow-bellied racers, Coluber constrictor substances of the snake in the arena. In either mormon. Herpetologica 30 (3): 285-289. MORI, A. 1990. Tail vibration of the Japanese grass case, the enhanced immobility may be adaptive lizard Takydromus tachydromoides as a tactic because both a recent encounter with a predator against a snake predator. J. Ethol. 8 (2): 81-88. and the presence of predators' odor imply the MORI, A. AND H. MORIGUCHI.1988. Food habits of high probability of the presence of a nearby the snakes of Japan: A critical review. The Snake predator (Thoen et al. 1986). 20(2): 99-113 . OTA, H. 1986. Snake really an able hunter?: Predatory ACKNOWLEDGMENTS.-I wish to thank T. Hidaka for behavior of Japanese striped snake, Elaphe reviewing the manuscript and H. Ota for carefully quadrivirgata, in the field. J. Ethol. 4 (1): 69-71. reading an early draft of this paper. I also thank T. SIEGEL, S. AND N. J. CASTELLAN,JR. 1988. Non- Hayashi, T. Hikida, H. Ota, and H. Takahashi for col- parametric Statistics for the Behavioral Sciences, lecting animals. This research was partially supported 2nd ed. McGraw-Hill Book Company, New York. by a Grant-in-Aid for Special Project Research on 399p. "Bi ological Aspects of Optimal Strategy and Social THOEN,C., D. BAUWENSAND R. F. VERHEYEN.1986. Structures" from the Japan Ministry of Education, Chemoreceptive and behavioural responses of the Science and Culture. common lizard Lacerta vivipara to snake chemical deposits. Anim. Behav. 34 (6): 1805-1813.

Department of Zoology, Faculty of Science, Kyoto University, Kitashirakawa-Oiwakecho, Sakyo-ku, Kyoto, 606 JAPAN MORI-LIZARD IMMOBILITY 5

要旨ニホンカナヘビTakydromus tachy- ナヘビは前半の10分間の方が後半の10分間より dromoidesの不動行動も動く頻度が有意に低かった.直前にシマヘビ

森哲とのセッションを経験したニホンカナヘビは, ニホンカナヘビにおいて ,不動行動をする傾経験しなかった個体よりも,それに続くセッシ向の指標として移動頻度を,その捕食者であるョンBにおいて移動頻度が有意に低かった.ニシマヘビ,非捕食者のニホソトカゲと出会わせホンカナヘビの不動行動は,視覚によって獲物

たとき(セッションA,B),および,ニホンを見つけ出す捕食者に対する適応的な対捕食者カナヘビだけにしたとき(セッションC)との行動であると考えられた. 間で比較した.セッションAにおける移動頻度 (606京都市左京区北白川追分町京都大学はセッションB,Cにおけるそれよりも有意に理学部動物学教室)

低かった.セッションBにおいては,ニホンカ