Locomotion in Amphibian Larvae (or “Why Aren't Tadpoles Built Like Fishes?”)

Abstract

SYNOPSIS. A variety of morphological features that affect locomotion distinguish larvae of the three living amphibian orders from fishes and their larvae. The oddest amphibian larvae are anuran tadpoles. With their globose bodies, concealed forelimbs, abruptly compressed and terminally tapered tails, tadpoles not only differ radically from fishes but they—unlike caecilians or salamanders—also differ radically from their adults. Tadpoles typically have less axial musculature and much simpler myotomes than fishes. Surprisingly, in terms of mechanical (propeller) efficiency and maximum sprint speeds, tadpoles still perform as well as many teleosts of comparable sizes. From a consideration of hydromechanics, no amphibian larvae appear to be designed for sustained swimming at high speeds. High maneuverability, rather than sustainable speed, are important for amphibian larval survival. Two key features of tadpoles are the absence of caudal vertebrae and unexposed pectoral appendages. With only a notochord to serve as a skeleton, the tadpole tail is extremely flexible. Because of this exceptional flexibility, tadpoles can fold their tails up against the body and turn rapidly with virtually no displacement of their center of mass. Caudal flexibility can be regulated by muscle activity in the tadpole to effect turning. Lateral appendages are not needed for this movement and are free to develop directly into their adult morphology; the anterior ones develop under cover of an opercular fold where they do not contribute to drag. A case is presented, based on the ecology of metamorphosis, that anuran transformation should be as brief as possible. With no bone to resorb, metamorphosis of the anuran caudal appendage can, indeed, be very rapid. The basic kinematics of constant velocity straightforward swimming for tadpoles and salamander larvae is reviewed, as well as the kinematics and electromyography of starting, stopping, and turning in tadpoles. An attempt is made to relate swimming kinematics to the characteristic morphologies of amphibian larvae. Swimming speed in Rana, Bufo and Aynbystoma larvae, which swim only intermittently, is modulated by changing tail beat frequency. However, Xenopus, which swims constantly by sculling with its tail, regulates swimming speed (at low to intermediate velocities) by varying the length of the propulsive wave in its tail. Xenopus and Rana differ in the morphology of their notochord, spinal cord, spinal nerves, and spinal motor pool distribution within the spinal cord. These differences may underlie the different way these larvae regulate swimming. They may also reflect their phylogenetic history.