The thermal environment of arboreal pools and its effects on the metabolism of the arboreal, oophagous tadpoles of a Taiwanese tree frog, Chirixalus eiffingeri (Anura: Rhacophoridae)

Abstract

We have studied seasonal and diurnal fluctuations of water temperature in bamboo stumps and the effect of temperature on the energy metabolism of arboreal, oophagous tadpoles of Chirixalus eiffingeri. We collected tadpoles (Gosner stage 28–29) in February and August from Chitou, Taiwan and acclimated them to 12 and 22°C. Using a closed system, we measured tadpole oxygen consumption ($\text{V}\text{̇}\text{o}{}_2$) at 12, 17 and 22°C. The water temperature was lowest in February (11–13°C), increased rapidly during March and April and was highest from May to August (20–24°C). Diel fluctuations in the temperature of the pools of water in bamboo stumps mirrored fluctuations in air temperature. Tadpoles collected in February and August exhibited metabolic compensation in that tadpoles acclimated at 12°C had significantly higher $\text{V}\text{̇}\text{o}{}_2$ than those acclimated at 22°C. There are at least two possible explanations for the presence of metabolic compensation in C. eiffingeri tadpoles. Firstly, the larval period of C. eiffingeri ranges from 40 to 78 days, a tadpole could experience relatively large fluctuations in body temperature (up to 10°C) during the development. As a result, C. eiffingeri tadpoles most likely evolved metabolic compensation to maintain activity levels under different thermal environments. Secondly, because arboreal pools are small, thermally unstratified and, aquatic microhabitats, tadpoles are unable to behaviorally select preferred temperatures. As a result, metabolic compensation allows tadpoles to regulate their physiological functions.

Introduction

Aquatic ectotherms have evolved various behavioral, biochemical and physiological strategies to minimize the effect of ambient temperature fluctuations on the rate at which their life functions proceed. For example, animals reared at cool temperatures may have higher metabolic rates at a given temperature than animals with a warmer thermal history (Bullock, 1955, Fry, 1958, Rome et al., 1992, Ultsch et al., 1999). Metabolic compensation is one of the physiological strategies commonly used by fishes and invertebrates to minimize the effects of ambient temperature fluctuations on physiological homeostasis. Based on these observations, we might expect the aquatic larvae of amphibians to be capable of metabolic compensation. However, available data show conflicting results: a temperate ranid, Rana berlandieri and Xenopus laevis are capable of metabolic acclimation (Feder, 1985), but another temperate ranid, Rana pipiens, is not (Parker, 1967). In addition, tadpoles of an Australian frog, Limnodynastes peroni, also showed no evidence of undergoing thermal metabolic acclimation (Marshall and Grigg, 1980). The ability of a species to modify its standard metabolic rate through thermal acclimation is correlated with the amount of variation in environmental temperature it experiences on a time scale of weeks–months (Feder, 1982a). Thus, metabolic acclimation seems to provide the greatest benefits to species that experience the greatest thermal fluctuation (Feder, 1985). Therefore, more data are needed on the prevalence and possible advantages of metabolic acclimation to tadpoles, and more studies should be conducted on a variety of species that live under different thermal regimes.

In this study, we determined the prevalence of metabolic thermal acclimation in rhacophorid tree frog tadpoles (Chirixalus eiffingeri) that live in arboreal pools, by studying their thermal physiology. We determined the temperature of the arboreal water pools in bamboo stumps by measuring the diurnal, seasonal air and water temperatures. We also measured the oxygen consumption ($\text{V}\text{̇}\text{o}{}_2$) of tadpoles collected early (February) and late (August) in the breeding season and acclimated to 12 and 22°C.

Chirixalus eiffingeri, a small frog with a snout-vent length of 30–40 mm, is endemic to Taiwan and two adjacent small islands, Iriomote and Ishigaki (Kuramoto, 1973, Ueda, 1986, Lue, 1990). Chirixalus eiffingeri has a prolonged breeding season from February to August (Kam et al., 1996) and female frogs lay 2–3 clutches of eggs each breeding season. During the breeding season, females deposit fertilized eggs on the inner walls of bamboo stumps or tree holes, just above the waterline (Kam et al., 1998a). Upon hatching, tadpoles drop into the pool of water where they grow and develop until metamorphosis. The water pools in bamboo stumps, like other arboreal pools (Laessle, 1961, Wassersug et al., 1981, Caldwell and Olivéra, 1999) typically contain small volumes (approx. 250 ml) of stagnant water (Kam et al., 1996). In addition, their physiochemical characteristics should be quite different from those of ponds, streams and rivers (Noland and Ultsch, 1981, Nie et al., 1999). The tadpole stage lasts from 40–60 days (Kam et al., 1998b). Tadpoles are obligatorily oophagous, with trophic eggs provided by female frogs.