RESPIRATION IN EARLY TETRAPODS-THE FROG IS A RED HERRING.

Abstract

The key feature of the fish-tetrapod transition is the invasion of the land. Utilization of the resources there available requires solution of four special problems: locomotion, control of the milieu interieur, internal fertilization, and the use of gaseous rather than liquid sources and sinks for the respiratory gases. The last problem will be dealt with here. It may most simply be stated as How did the earliest tetrapods breathe? The recent literature contains two views regarding the breathing methods of the earliest amphibians, namely (1) that cutaneous respiration must have been important during the transition period (Szarski, 1962; Hughes, 1966; Rahn, 1966) and (2) that these animals had lungs that were filled by a quick pulsatile contraction of the buccal cavity, often described as air swallowing or pulse pumping, rather than by an aspiration mechanism (Cox, 1967; McMahon, 1969). There are certain obvious objections to these views. Cutaneous respiration seems inherently implausible as a breathing method for the earliest amphibians such as Ichthyostega (Romer, 1966). These fossils appear (1) to have been of very large size, i.e., 3 to 4 feet long, and (2) to have lived in coal swamps which presumably indicated a fairly warm climate; (3) many such forms, furthermore, show ossification on the flanks and belly and the epidermis of larger specimens was probably thicker and more keratinized. Pulse pumping as a method for replenishing the contents of the lungs is also unlikely because of the stiff flanks, containing solid, well-articulated ribs and often a sheathing of bony scales; Willem (1931) has already argued from similar evidence that stegocephalians used aspiration plus pulse pumping. The statements in the literature apparently represent an extrapolation from frog physiology rather than a response to observations of the fossil record. Do Recent frogs represent a red herring? Under the circumstances, it seems most appropriate to review the mechanisms of gas exchange, the options available to the transitional forms, and the probability and sequence for the changes that actually occurred. Such a review, within the framework of recent electromyographical analyses of air-pumping mechanics in the breathing of fishes, frogs, turtles, and crocodilians, is here offered. It suggests that the classical observations on frogs do not by themselves furnish a suitable base for speculations about the behavior and physiology of the earliest amphibians.