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Lying in Ambush for Nocturnal Frogs: Field Observations on the Feeding Behavior of Three Colubrid Snakes, Elaphe Quadrivirgata, E

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Lying in Ambush for Nocturnal Frogs: Field Observations on the Feeding Behavior of Three Colubrid Snakes, Elaphe Quadrivirgata, E Japanese Journal of Herpetology 14(3): 107-115., June 1992 (C)1992 by The HerpetologicalSociety of Japan Lying in Ambush for Nocturnal Frogs: Field Observations on the Feeding Behavior of Three Colubrid Snakes, Elaphe quadrivirgata, E. climacophora, and Rhabdophis tigrinus AKIRA MORI, MITSUHIKO TODA, SEISHI KADOWAKI AND HAJIME MORIGUCHI Abstract: The nocturnal activity of Elaphe quadrivirgata, E. climacophora, and Rhabdophis tigrinus hitherto known as diurnal, heliothermic predators, was observed around a breeding pond of the Japanese treefrog, Rhacophorus arboreus. The peak of seasonal nocturnal activity of the snakes largely coincided with that of R. arboreus. Snakes were observed lying motionless on a tree branch, with the anterior part of the body extended and the head directed towards the trunk and/or downward. Often the chin and/or temporal region of the snakes made contact with the surface of the trunk. Predation on R. arboreus by the snakes was directly observed on 10 occasions. These facts suggest that, from the above position, E. quadrivirgata, E. climacophora, and Rhabdophis tigrinus "actively" ambushed Rhacophorus arboreus that used the trees as diel vertical pathways during its breeding season. Possible factors that affect the forag- ing tactics of the snakes are discussed. Key words: Elaphe quadrivirgata; Elaphe climacophora; Rhabdophis tigrinus; Noc- turnal ambush; Foraging tactics Foraging ecology is one of the most important Jaeger and Barnard, 1981; O'Brien et al., 1989). aspects in understanding life history strategies in All snakes hitherto known are carnivorous carnivorous animals. To analyze the putative (Vitt, 1987) and various morphological and feeding adaptations of predators, it is essential physiological adaptations for foraging have been to know not only what they eat but also how demonstrated (Cundall, 1987 for review). they interact with their prey (e. g., where, when, Although these morphological and physiological and how they eat prey). Numerous studies sug- adaptations constrain the flexibility of their gest that predators search for prey by using one foraging tactics, intraspecific shifts in foraging of two basic modes, sit-and-wait and active mode, site, and period in response to en- foraging (McLaughlin, 1989 for review). These vironmental factors are reported in several search modes are generally species-specific partly snakes (Patterson and Davies, 1982; Hailey and because physiological and morphological traits Davies, 1986). However, more basic field obser- constrain the predator's ability to switch modes vations are still extensively necessary to draw any (e. g., Huey and Pianka, 1981; McLaughlin, conclusions about the all-inclusive foraging 1989). On the other hand, there are indications strategy of any snake. that some predators switch between sit-and-wait The Japanese striped snake, Elaphe and active search modes (e. g., Jaeger and Bar- quadrivirgata, (Colubridae) is one of the best nard, 1981; Pietruszka, 1986). Intraspecific studied snakes in Japan and its natural history changes of foraging tactics such as temporal has been well documented (Fukada, 1954, 1958, shifts in foraging habitat and diel activity pat- 1959, 1960, 1985; Ota, 1986; Hasegawa and terns are also reported (e. g., Shine and Moriguchi, 1989; Mori, 1989, 1991; Kadowaki, Lambeck, 1985; Sjoberg, 1989). Based on em- 1992). This snake is mainly a terrestrial and pirical field studies and foraging theories, these diurnal active forager which maintains a relative- intraspecific shifts have been interpreted as ly high activity temperature (mean body responses to changes in environmental factors temperature=28.7C: Fukada, 1985), achieved such as food resource availability in order to in- by basking in the sun (i. e., heliothermy; Pough crease foraging efficiency (e. g., Norberg, 1977; and Gans, 1982). Extensive investigations of stomach contents revealed that the species feeds Accepted 30 Apr. 1992 on various kinds of prey including frogs, lizards, 108 Jpn. J. Herpetol. 14 (3). 1992 small mammals, and reptile eggs (Mori and The vegetation around the pond is mainly com- Moriguchi, 1988 for review). At least two posed of Acer amoenum, Eurya japonica, different foraging tactics are known in E. Magnolia praecocissima, and Castanopsis quadrivirgata: catching diurnally active prey by sieboldii (3-15m high), of which some branches directly chasing it (Ota, 1986) and detecting and hang over the pond (Fig. 1). We visited the subduing nocturnal prey sleeping in its retreat pond two to 29 nights per month usually after (Mori, 1989). Although both of these tactics are midnight. used by a single individual (Mori, personal obser- With a small flashlight, we carefully searched vations), feeding opportunities may also affect for frogs and snakes around the pond. The which foraging mode is employed (Mori, 1989). number of frogs and snakes was counted, and Elaphe climacophora and Rhabdophis location, behavior, and posture of snakes were tigrinus are also common snakes in the Japan recorded. Because of dense vegetative cover in Main Islands (Fukada, 1958; Moriguchi and the higher portions of the trees, vertical censuses Naito, 1982; Kadowaki, 1992). Both species are were restricted to approximately an area below mainly diurnal and the mean body temperature 4m. Some snakes were captured by hand and is 27.7C in the former and 26.8C in the latter brought back to the laboratory where snout-vent (Fukada, 1989). Elaphe climacophora is a ter- (SVL) and tail lengths and body mass (BM) were restrial to semi-arboreal snake feeding on en- dothermic animals, whereas R. tigrinus is a ter- restrial to semi-aquatic snake predominantly ex- ploiting anurans (Fukada, 1959, Sengoku, 1979, Moriguchi and Naito, 1982). However, detailed field observations on feeding behavior of these snakes are meager. Rhacophorus arboreus, one of the food resources for E. quadrivirgata and Rhabdophis tigrinus, is a well-known foam nesting treefrog distributed in Honshu of Japan (Maeda and Matsui, 1989). During the breeding season from April to July, the frogs congregate at still water and breed on trees, among the grass or on the ground above or adjacent to the water, construct- ing foam nests usually on branches and leaves. Breeding activities are usually observed from night to early morning (Toda, 1988). During an ongoing study on the reproductive biology of Rhacophorus arboreus, we observed another foraging tactic of E. quadrivirgata: ambushing, from a tree branch during the night, nocturnal frogs which were congregating at a small pond to breed. In this paper, we present field observa- tions on the feeding behavior of E. quadrivirgata and discuss some proximate factors that may affect the foraging tactics of the snake. Similar feeding behavior of E. climacophora and Rhab- dophis tigrinus, observed at the same study site are also reported. MATERIALSAND METHODS FIG. 1. Schematic map and cross section of a Field work was conducted from May to July breeding pond of the Japanese treefrog, Rhacophorus 1987 and from May to October 1988, 1989 and arboreus. Dashed lines indicate overhead canopy of 1990 at a small pond (17m long) located in the trees. Aa: Acer amoenum, Ac: Aralia cordata, Aj: Botanic Garden (5ha) of Kanazawa University Aucuba japonica, Cs: Castanopsis sieboldii, Ej: Eurya (36°34'N, 136°40'E), Ishikawa prefecture, japonica, Hc: Houttuynia cordata, Io: Idesia polycar- Japan. The Botanic Garden is dominated by pa, Is: Iris pseudacorus, Mp: Magnolia praecocissima, Castanopsis sieboldii and Machilus thunbergii. Rt: Rhus trichocarpa. MORI ET AL. -SNAKE FEEDING BEHAVIOR 109 measured. These snakes were marked by ven- and 12 individuals of E. quadrivirgata, E. tral scale clipping as a permanent marking climacophora, and R. tigrinus were marked, (Brown and Parker, 1976) and painted on the respectively. Marked individuals comprised head with quick-drying paint for a temporary sixty-two % (32/52) of the sightings of E. marking, after which, they were released at the quadrivirgata, 61% (11/18) of E. climacophora, site of capture as soon as possible. In 1989 and and 44% (14/32) of R. tigrinus. It is probable, 1990 snakes were palpated at the time of capture however, that these values were underestimated to recover prey items from the stomach. since ventral or painted markings could not Regurgitated prey was identified to the species always be identified. Both males and females level if possible and returned immediately to the were captured in all species. No juvenile snake snake's stomach. Cloacal body temperature of was observed or captured except for R. tigrinus. some snakes was measured with a thermistor. Most of the snakes were observed from late We believe that these handling procedures did May to early August, when Rhacophorus ar- not affect the normal feeding behavior of the boreus congregated at the breeding pond and snakes. Ambient temperature at about 0.6m was abundant on the surrounding ground and above the ground was measured at a fixed point trees during the night (Fig. 2). In spring of beside the pond during each observation. 1988-1990, it seemed that snakes did not appear at Behavior of several snakes was continuously the pond until the air temperature measured dur- observed through several hours in June 1989 and ing the census exceeded approximately 15 C. July 1990. Measurements of SVL and BM of Few snakes were found at night from mid- frogs being swallowed by snakes were obtained August to September even though the air from data, by referring to individual marking temperature was higher than 15 C. numbers, previously recorded during mark- All E. quadrivirgata were found lying mo- recapture study of the frogs. Brief censuses in tionless on branches 0.7-3.6 meters high (x= 1.8, the Botanic Garden both in the daytime and at N = 52). All E. climacophora but one, which night were also made sporadically to investigate was coiled in the water, were observed lying on food resources used by snakes in this area. branches 0.8-3.0 meters high (x= 1.9, N= 17).
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