Effects of Prey Type on the Feeding Behavior of Alsophis portoricensis (Serpentes: Colubridae)

Alsophis portoricensis can inject the secretion of its Duvernoy's gland (=venom) into its prey, constrict it, or swallow it alive. We studied the differences in prey-handling behavior of Alsophis portoricensis when feeding on two of its natural prey species, the lizard Anolis cristatellus and the frog Eleutherodactylus coqui. Subduing time was higher for lizards, but swallowing and handling times were longer for frogs. Alsophis struck Anolis most frequently on the trunk, whereas it attacked Eleutherodactylus preferentially on the head or the limbs. Alsophis portoricensis was equally successful in preventing both prey types from escaping after first seizing them. Snakes never constricted either prey type, but envenomated most Anolis and only one Eleutherodactylus. Alsophis always swallowed lizards head-first, but ingested frogs head-first or tailor side-first indiscriminately. This diversity in Alsophis feeding behavior may result from differences in external morphology and retaliatory power between Anolis cristatellus and Eleutherodactylus coqui. Predators may show variation in their feeding behavior when they encounter different prey types. These variations may be related to the antipredator mechanisms presented by the prey, microhabitat differences among prey types, or to the risk of injury or predation to the predator (Formanowicz and Brodie, 1988; Lima and Dill, 1990). Because feeding is an energy-consuming activity, a predator may minimize the amount of energy invested and/or maximize the amount of energy gained per prey item (Schoener, 1971; Stephens and Krebs, 1986; Pianka, 1988). Some snakes exhibit variation in their feeding behavior according to prey type. In captivity, mangrove snakes (Boiga dendrophila, Colubridae) subdue large anoles by pressing them against the substrate, but hold large snakes in their jaws and chew them (Rocco, 1988). Pitvipers (e.g., Crotalus spp., Agkistrodon piscivorus, Porthidium godmani, Bothrops jararaca, Viperidae) usually release mammals after striking them, but retain their hold on fish, amphibians, reptiles, and birds (Klauber, 1956; O'Connell et al., 1981; Campbell and Sol6rzano, 1992; Hayes, 1992; Sazima, 1992). Tigersnakes (Notechis scutatus, Elapidae) swallow frogs after biting, but release rodents following the initial strike (Shine, 1991). Alsophis is the most geographically widespread genus of colubrid snakes in the West Indies. Species of Alsophis are largely grounddwelling, diurnal, active foragers (Henderson 1 Present Address: Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, California 94720, USA. and Sajdak, 1986). Although Alsophis is catholic in its diet, Anolis lizards and Eleutherodactylus frogs are the most common prey items found in Alsophis stomach contents (Henderson and Crother, 1989; Schwartz and Henderson, 1991). The Puerto Rican racer, Alsophis portoricensis, has a generalized diet, which is probably the main reason for its variable feeding behavior. Alsophis is capable of injecting the secretion of its Duvernoy's gland (=venom) into its prey, constricting it, or swallowing it while it struggles (Rodriguez-Robles, 1992). Herein we report the effects of prey type on the feeding behavior of Alsophis portoricensis. MATERIALS AND METHODS We used 20 snakes (body mass [BM] = 21.8154.6 g) collected at the Cambalache Forest Reserve (11 snakes) and at Caja de Muertos Island Natural Reserve (9 snakes), Puerto Rico. Snakes were housed individually in plastic cages (61 cm wide x 31 cm high x 32 cm deep) with newspaper substrates and water ad libitum. Snakes were maintained at a temperature of 2427 C with no regular light/dark regime. Animals used as prey were the polychrid (Frost and Etheridge, 1989) lizard, Anolis cristatellus, and the leptodactylid frog, Eleutherodactylus coqui, both of which are natural prey items of Alsophis portoricensis (Rodriguez-Robles and Thomas, 1992; M. Canals and J. Gillingham, pers. comm.). Anolis cristatellus is a diurnal, trunk-ground anole (Rand, 1964) usually found in open forests and fields and disturbed sites. The Puerto Rican coqui, Eleutherodactylus coqui, is a nocturnal frog, typically active from dusk to dawn year-round, that occurs in mesic forests where it uses all parts of the terrestrial habitat, from ground to J. A. RODRiGUEZ-ROBLES AND M. LEAL tree tops (Stewart, 1985). Both species are widespread throughout Puerto Rico and are broadly sympatric with Alsophis portoricensis, except for Caja de Muertos, where no frogs occur (Schwartz and Henderson, 1991). Snakes from Caja de Muertos, however, did not show any difference in prey-handling behavior of E. coqui when compared to snakes from mainland Puerto Rico (Rodriguez-Robles and Leal, unpubl. obs.). Snakes were used only once for each prey type. Eleven snakes were used for both prey items, whereas six snakes were used only for lizards and three only for frogs. Snakes were weighed (BM ? 0.1 g) and all items measured (snoutvent length [SVL] to nearest mm) and weighed (BM ? 0.1 g) immediately prior to the feeding trials. Using a stop watch and an audio tape recorder, we recorded 17 and 14 complete sequences of Alsophis portoricensis feeding on Anolis cristatellus (SVL = 30-68 mm, BM = 0.6-10.3 g) and Eleutherodactylus coqui (SVL = 25-58 mm, BM = 1.4-9.5 g), respectively. Testing was conducted in completely bare cages. All trials consisted of introducing a single prey item into the cage of an individual snake. If no attack occurred within 1-3 h we removed the prey. Snakes were tested not less than three days after the previous meal. We recorded subduing time (elapsed time from first seizure of prey to commencement of ingestion), swallowing time (time from beginning to completion of ingestion), and handling time (subduing plus swallowing time), the site of the first attack (i.e., head, trunk, limbs), whether or not the prey escaped after being first grasped by the snake, and direction of ingestion (i.e., head-, tail-, or side-first). In Alsophis portoricensis, venom injection is dictated by a stationary bite with spasmodic and forceful chewing of the prey (Thomas and Prieto-Hernandez, 1985; Rodriguez-Robles, 1992). We noted if a snake injected venom into its prey during a feeding episode. To minimize the confounding effects of variation in body mass between predators and prey when comparing handling, subduing, and swallowing times of lizards and frogs, we used an index that we called relative prey mass. Relative prey mass (RPM) was defined as the residuals (unitless) from the linear regressions of prey mass on snake mass. Because prey mass was sometimes less than the average for a given mass of predator (points below the regression line), and it was sometimes above the average (points over the regression line), RPM had both negative and positive values. We did not use the ratio of prey to snake mass to scale our data to avoid the statistical problems associated with the analysis of ratios (Packard and Boardman, 1987). We plotted (log-transformed) subduing, swallowing, and handling times against RPM for both Anolis and Eleutherodactylus to examine the effects of RPM on these variables. Statistical procedures follow Sokal and Rohlf (1981).