Tadpoles, Predation and Pond Habitats in the Tropics

Tadpoles involved in predator-prey interactions were studied in tropical wet forest in Costa Rica under laboratory and field conditions. Larvae of the frog Leptodactylus pentadactylas and naiads of the odonate Pantala flavescens are important predators on larvae of several species of frogs. The predators discriminate the prey on the basis of size and species, but not type of habitat in which predation occurs. A graphical model is proposed to illustrate the relationships between species diversity and habitat complexity as they affect the composition of tadpole communities. The model is used to evaluate the relative importance of abiotic and biotic factors in determining the use of specific kinds of aquatic habitats by frogs with larval stages. Predation by permanent aquatic predators (primarily fish) is considered to be the most important biotic factor influencing the temporal and spatial composition of tadpole communities. The development and maintenance of predatory feeding modes, including cannibalism, in certain tadpoles is examined in light of the model. MOST TADPOLES are generalized herbivores (Jenssen 1967) that either scrape plant material from a substrate or filter planktonic food directly from the water. Only a few species are known to be carnivorous although some instances of cannibalism among tadpoles have been reported (Bragg 1964). We were surprised, therefore, to find a well-developed predator-prey system in which tadpoles of one species were carnivores on other tadpoles. This finding was unusual not only because documented instances of tadpoles feeding on other tadpoles are relatively rare, but also because the carnivorous tadpoles were found in relatively small puddles. The predator-prey interactions studied occur in small rain-filled tropical puddles characteristically utilized by opportunistic breeders. Experiments were run to study the relative ability of predators to capture prey and their preference for certain prey species, to ascertain the influence of microhabitat on predator-prey interactions, and to evaluate the influence of prey size on their ability to escape predation. Results of these experiments led to a consideration of tadpole habitats and to those factors controlling the diversity of tadpole communities. A model is used to illustrate the relationship between pond complexity and predation as they affect the species composition of a tadpole community. The predatory feeding mode of tadpoles is considered in light of this model. METHODS AND MATERIALS Observations and experiments were made during two weeks in June 1973 (WRH and RWM) and two weeks in August 1973 (DLW and RWM) in the vicinity of the Osa Field Station, Rincon de Osa, Puntarenas Province, Costa Rica. The station is surrounded by the remnants of the lowland wet forests that once covered much of the Golfo Dulce region. This area receives more than 4000 mm of rain each year and is the only remaining large tract of wet forest on the Pacific coast of Middle America. Most of the work was done in the immediate vicinity of the airfield at Rincon, an area of disturbed second-growth vegetation surrounded by relatively undisturbed wet forest. Our studies were conducted during the rainy season when most of the anuran species known from the area were breeding. Breeding sites used by the various species included very small (less than 1 m diam.) puddles, usually in disturbed areas; small temporary ponds (less than 20 m diam. and 1 m deep); seepage areas along roads; and some sizable (more than 20 m diam. and 1 m deep), more persistent ponds. Larvae of the following species were commonly found in the smallest ponds: Physalaemus pustulosus, Leptodactylus poecilocbilus, Leptodactylus pentadactylus, and Smilisca phaeota. Bufo marinus sometimes used these temporary ponds but usually bred in more permanent sites. Hyla rosenb&rgi called from concealed sites near the puddles but only bred in small mud depressions near seepage areas along roads or near small temporary ponds. Most of the other 37 frog species at Rincon bred in large aquatic sites (permanent ponds, rivers, streams, etc.) 100 BIOTROPICA 7(2): 100-111 1975 or had some form of terrestrial development. Observations were made in the field and laboratory, but all experiments conducted at the field station used freshly caught material. The two major tadpole predators used were larvae of Leptodactylus pentadactylus and naiads of the odonate Pantala flaves cens (Libellulidae). Both predator and prey tadpoles and naiads were kept by species in holding trays of plastic bags before each experiment. At the conclusion of the experiments, the predators and the remaining prey were preserved. Later these were staged (Gosner I960) and measured in the laboratory. All measurements, unless otherwise specified, are in millimeters. EXPERIMENTAL DESIGN AND RESULTS CAPTURE ABILITY AND PREFERENCE: The first experiment was designed to test the effectiveness of the predatory tadpole Leptodactylus pentadactylus in capturing larvae of two common co-inhabitants of temporary ponds, and its preference for one species over the other, although the experimental design did not specifically test this aspect. Larvae of Bufo marinus and Physalaemus pustulosus were used as prey. Experiments were run in three plastic trays (19 x 12 x 7 cm) filled with clear water 2.5 cm deep. The first run on 14 June used three experimental units including 12 hatchling Bufo, 6 hatchling Bufo and 6 small Physalaemus, and 12 small Physalaemus, respectively. A single L. pentadactylus larva was added to each tray and maintained in it for two hours. The experiments were repeated at the same time on 18 and 19 of June so that each individual predator was exposed to all three prey conditions. Sizes of predators and prey and results are listed in table 1. Comparison of the numbers of prey individuals of Bufo marinus and Physalaemus pustulosus capmred by L. pentadactylus in the containers of pure prey species indicated that significantly (P= 0.05) more Bufo were eaten than Physalaemus. In the containers where both prey were offered, again significantly more individuals of Bufo were eaten. It is possible that the statistical differences relating to numbers of each type of prey eaten reflect their differential success at avoiding predation rather than predator choice or preference, or perhaps a combination of both. Unequivocably, however, it is biologically significant that the predator ate both types of prey (see discussion). HABITAT: A second series of experiments, designed to determine the effect of habitat on feeding efficiency, were run using tadpoles of L. pentadactylus as the predator and Bufo marinus, Smilisca phaeota, Physalaemus pustulosus, and Hyla rosenbergi as prey. Four of the same type of trays used in the previous experiment were filled to a depth of 5 cm with clear water, turbid water, clear water over a rocky bottom, or clear water over leafy substrate, respectively, conditions matching the natural habitats used by the larvae. The rocks were sufficiently large and the leaves sufficiently loose so that both predators and prey could hide. Twelve prey of one species and three predators were added to each habitat tray. Each experiment was run for one hour and repeated on three successive days so that each set of predators was exposed to each habitat type. The sizes of the predators and prey, summary of experimental results, and results of an analysis of variance for a three-way factorial experiment are presented in table 2. The groups of predators did not vary in their feeding efficiency from day to day. The type of habitat was not significant with respect to the number of prey consumed by the predators. There were no significant prey by day interactions or day by habitat interactions. Two results were statistically significant. First, the predators ate more of some prey species than others. The mean numbers of each prey eaten were: TABLE 1. Predator capture ability and preference experiments* B. marirms P. pustulosus Single-species trays Mixed-species trays 15 of 36 14 of 18 6 of 36 5 of 18 X X = 3.90" = 4.32 Stage Body length Total length Maximum width Beak width Predator•L. pentadactylus Prey •B. marinus Prey •P. pustulosus 36-39 20-26 24-26 13.4-16.8 2.45.0 2.14.1 50.0-61.1 4.7-11.1 5.99.9 1.5-3.5 1.5-2.7 1.7-2.0 a Specimen data (measurements in millimeters). b 0.05 level of significance. Tadpoles, Predation and Pond Habitats 101 TABLE 2. Habitat experiments showing total prey consumed over four days by four sets of predatory Leptodactylus pentadactylus. Stage Total Habitat Length Clear Turbid Rocks Leaves Predator L. pentadactylus Prey Bufo marinus 33-36 26-27 42.0-53.5 7.9-11.9 Expt. B. Predator L. pentadactylus Prey Physalaemus pustulosus 31-36 25-27 40.7-51.8 7.9-11.9 Expt. C. Predator L. pentadactylus Prey Smilisca phaeota 34-36 25 43.0-47.0 8.0-10.5