The ZoologicalSocietyZoological Society of Japan
Se\rces ZooLoGlcAL MAGAzsNE 91: 239-244 Cl982)
Predatory Behavior and Learning in the Lacertid Lizard, Tahydrornus tachydrornoldes, teward Unpalatable Prey Insects
YuTAKA JoHKI AND TosHITAKA HIDAKA
Department of Zoology, Faculty of Science, Kyoto University, Sakyo, Kyoto 606 japan
Reeeived February 15, 1982
Revised version received April 15, 19B2
ABSTRACT The prey recognition system in the predatory behavior of TL tachydrornoides was analyzed experimentally using unpalatable Pi yeria moths and edible mealworms. None of the Pryeria moths were either killed or eaten, while all the mealworms attacked were eaten. The learning of visual avoidance by 71 tachydromoides, in which the }izard associates the unpalatability of Prbleria meth with its appearance and avoids it, seemed to exist, but its process appeared to be very slow. In the course of predatory behavior, the lizard first recognized the prey visually, but then checked it strictly through chemical cues. This suggested that not only visual but also other sensory cues such as olfactory and learn- gustatory stimuli deTived from the prey were neeessary for theefficient ayoidance ing in this lizard. (ZooL Mag. 91: 239-244, 1982)
lizard. In the we carried Lizards are Largely insectiyorous and are this presentpaper, using the same supposed to be the main diurnal predators out feeding experiments order to of insects as well as birds. It is known that lizard species as the predator, in of our study many species arnong tihem can recognize cornpare the results previous attempt to the and learn the coloration of their prey and to rnake an generalize of behavior in this lizard. (Swiezawska, 1949; Sexton, 1960, 1964; process predatory of same species, R sinica, were Benes, 1969; Boyden, !976). Co!or discrim- Adults the used as experimenta1 food for the following ination and learning in lizards were recently two reasons. First, it is evident that this reviewed by Burghardt (1977). Nevertheless, unpalatable for lizards from studies on the coler recognition and learning moth isan prey eur observations, and second, in lizards, in particular with reference to the preliminary of vs meaning and the evolution of coloration in they are different types prey (moths
same the insects, are still lagging behind caterpillars), although belonging to the prey 'specles. compared with those in birds. In our previous study (Johki and Materials Hidaka, 1979) using the laeertid lizard, a com- Tkikydromus tachydromoides Schlegel as the 71ihydromus tachydromoides is lacertid lizard in Japan and predator and the unpa}atabie larvae of the mon, terrestrial many insects moth, Pryeria sinica Moore (Lepidoptera, is an important pr'edator of 1975). Zygaenidae), as the prey, it was concluded and spiders (Jackson and Telford, that not only visual eues but also other Eleven adults of l: tachydromoldes at eaptured ip the factors such as olfactory and gustatory cues least one-year of age were Kyoto in May, 1977, played an important role in the process of Ginkaku-ji area of four months until recognition and choiee of prey insects in and were reared for about
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' ･ 240 . Y. JoHKI AND T. HIDAKA ' ' ' ' the experiment started. Only three kinds substances which are supposed to'play a of foods, mealworms Petri diph contal.ning water, and was sprayed months earlier than in nature by rearing the - w'ith water once a day to prevent dryness. pupae under shott-day cenditions {Ishii' ' etaL in .T. he experimental prey, adult Ptyeria prep.). ' . sinica, belongs to the family Zygaenidae ･ Experimental Procedure ' ' (Lepidoptera), all species of which aTe daY- The experiment was conducted as fiying and whose 1arvae have relatively pre- cohsPicuous color in several viously described (Johki and Hidaka, 1979)' patterns. ' but mealworms were chosen as the species of. Zygaenidae such as Zygnenci spp., palatqble control insects this time. One experimenta1 both adulbs and larvae secrete poisonous .., "abdomen-elevation" Fig. 1. Adult male Prv,eria sinica exhibiting the behavior. ' NII-Electronic Library Service The ZoologicalSocietyZoological Society of Japan 241 Predatory Be havior of Tlakydromus Lizard + prey, adu]t P. sinica was given once a day ]ikewise show the progress of visual to each lizard by dropping it within 10 cm olfactory avoidance learning, and a daily of the lizard's snout, and the response of decrease in the ratio of SnfW will sihow the lizards was observed. Each lizard was the process of establishment of avoidance allowed two minutes to respond to the prey, learning through the overall sensory }n- because this duration of time was shown in formation, the course of out observations so far to be Results suffieient for the !izard's response to occut. The step at which the lizard interrupted Response of lizards tQ Ptyeria moths The results of the experiment are predatory behavlor was recorded, Imrne- diately after a two-minute trial, the contro! presented in Table 1 on visual, olfactory and gustatory senses DayWASmTSnKE was analyzed in the following way. When 123456789101112131415811101010811710571089451547105588633e783575521oo2122131254411oooooooooeoeooeooooooooooooooooooooo disturbance by an experimenter or any other accidenta1 agent was unlikely, inter- "watching" "approaching" ruptions at {W) or (A) could be regarded as occurring by some visual suppression, interruptions at "smelling" NII-Electronic Library Service The ZoologicalSocietyZoological Society of Japan 242 Y. JoHKI AND T, HIDAKA either kil]ed or eaten. The frequency of in the ratios of Sm/W, TVW and SnXW, re- "W'' "K'' response at each step from to spective]y. SmtW was almost 100 % early decreased almost Iinearly. in the experimental period, but it decreased Learning of 1izards as the experiment proceecled. Although Figures 3a, b, c show the daily change TIW also had a tendency tG decrease from 100 % ln the process of the experiment, it Table 2. Response of 1lakydromus tachordro- fiuctuated slightly and began to increase moides to Pryeria moths (same data as again at the end of the experimental period. Table 1 but rearranged for each lizard). Unlike these ratios, SnlW was very low in Lizard No.WA Sm T Sn KE the early peried, gradually increased, reaching a peak on days 5-6, and then 1 12 9 9 83426457245512o5332oo1oooooooooooooooooooooo decreased again, stabi)izing at O % in the last 7 6 4 44375611379 stage of the experiment. 911l3151718192122 8 5 71215111581310 510881441210 Discussion Analysis of the lizards' ayoidance learn- ing process toward their prey based on visual and ehemieal senses is the main subject of this study. Especially, the process of visual avoidance learning in sueh an insectivorous predator will be important in discussing tihe meaning of body color in insects, Total117 89 68 50 22 Oo As described in Lhe Results. the daily % lOOaevuttUew--o 50hv=o=eeLL o W A Sm T Sn K E Step ot Response Fig. 2. Response curve of Ilrkydromustachydromoldes to Pryen-a moths and control mealworms based on Tables 1 and 2. The incidence of each step response (total of eleven lizards) is shown as the percentage "watching" to the number of steps. NII-Electronic Library Service The ZoologicalSocietyZoological Society ofJapanof Japan 243 Predatory Be havior of 71rkydromus Lizard change in Lhe Sm/W ratio can be regarded as the lizards' learnlng to associabe the visual showing the process of visual learning in character of the prey with its unpalatability. lizards, the daily ehange in T/W as visual + It is thus suggested that the appearance of "warn- olfaetory learning and the daily change ln the Piyeria moth is functioning as a Sn/W as overall learning. If these assump- ing signal", at least for T. tachydromoides. `twarning the cen- tions are correct, then the daily decline of Here slgnal" includes body coler coloration), Sm/W (Fig. 3a) will mean a reduced degree spicuous (warning of facility in transition from the visual to bee-iike shape, abdomen-elevation behavior the next (olfacto'ty in this ease) step in the which may be the threatening (Blest, 1964}, predatory behavior. This probably represents and so on. The process of vlsual avoidance learning in {Ilahydromus, however, seems to be very slow beeause a steady decrease in SmlW started only from day 7 (Fig. 3a). The TIW ratio also had a tendency to end of the experimenta1 .91eclNEut decline, but at the period it increased again (Fig. 3b). This may be due to vague olfactory avoidance learning. The SnYW ratio, an index to the overall learning of lizards, is low in the early stage of the experiment then the following increase in Sn/W 3e) solxH (Fig. . × will be interpreted as a decrease in shyness /. . toward the Pryeria moth, and the following x . re-decline of SntW as caused by the unpleas- /v'/'ant experience. After day 10, none of them D-i"100 attacked the P) yeria moths. The patterns of the daily change in Smi W and SntW are similar to those in our previous work yvas not detected, This fact coincides with Benes' (1969) report that in the whiptail lizard. Cnemidophorus tigris, the seasonal o 1 5 ro l5 effect on feeding behavior was not quali- OAY tative but quantitative. In our previous study, it was co'n- Fig.3, Daily changes in the ratio, NII-Electronic Library Service The ZoologicalSocietyZoological Society of Japan 244 Y. JOHKI AND T. HIDAKA visua}ly, but there followed a tecognized the evolution of warning co]oratlon in strict cheek through chemical cues, We butterfiies. Part I. Behavior 35: 45-60 eonfirm such charaeteristics again in this (1969). Part II. Amer, IVitt. 104: 323- work, 335 (1970). JAcKsoN. D. R. AND S. R. TELFoRD, JR. Acknowledgrnent (l975) Food habibs and predatory role of the' Japanese Iacertid, 71]hydromus This work was supported in part by a taehydromoides. Copeia 1975: 343-351. Grant-in-Aid for Special Project Research on JOHKI, Y. AND T, HIDAKA (1979) Function Mechanisms of Animal Behavior from the "warning of the colorEtion" in larvae of japanese Ministry of Education, Science and a diurnal moth, Pv),eria sinica MooRE Culture. {Lepidoptera, Zygaenidae). Appt. Ent. Zool. 14: 164-172. References JoNEs, D. A., J. PARsoNs AND M. RoTHsclLD BENEs, E. S. (1969) Behavioral evidence for (1962> Release of hydro- cyanic from coloT discriminatien by the whiptail acid crashed tissues of all stages in lizard, Cnemidophorus tigris. Copeia the lifetyle of speeies of the Zygaenidae 1969: 707-722. (Lepidoptera). Nature 193: 52-53. BLEST. A. D. (1964) Protective display and RoTHSCHILD, sound production in some New World M. (1971)Speculation about mimicry with Henry Ford. Ecological arctiid and ctenuehid moths, Zoolegica N, YL 49: 161-18L Genetics and Evotution. ed. by R. BOYDEN, T. C. (1976) But･terfly palatability CREED, Blackwell. Oxford, pp. 203- 223. and mimicry: Experiments with Ameiva SExToN. O. J. Experimental lizards. Evotution 30: 73-81. (1960) studies of artifieial batesian mimics. BULLINI. L., V. SBORDONI AND P. Behaviour 15: 224-252. RAGAZZINI (1969) Mimetismo mUl- Differential leriano in popolazioni italiane de (1964) predation by the lizard, Anotis caroiinensis upon Zygnena ephiattes (L.) (Lepidoptera, uniceloured and Zygaenidae}. Arch. ZooJ. Ital. 54: 181- po]ycoloured insects 214. after an interval of no contact. Anim. Behav. 12: BURGHADT, G. M. <1977) Learning proeess 101-110, SWIEZAwsKA, K. in reptiles. Biology of the Reptilia, ed. (1949)Colour-discrimina- tien of the sand lizard, Lacerta agr'tis, by C. GANs, Vol. 7 pp. 555-681. L. Bull. Int. Acod. Pol. Sei. Let. COPPINGER, R. P. (1969 and 1970) The Ser.B, effect of experience and novelty on Sci, Nat, 11; 1-20. avian feeding behavior with referenee to NII-Electronic Library Service