Amphibian respiration and olfaction and their relationships: from Robert Townson (1794) to the present

Abstract

The present review examines the developments in the elucidation of the mechanisms of amphibian respiration and olfaction. Research in these two areas has largely proceeded along independent lines, despite the fact that ventilation of the nasobuccopharyngeal cavity is a basic element in both functions. The English naturalist Robert Townson demonstrated, in the 1790s, that amphibians, contrary to general belief, ventilated the lungs by a pressure-pump mechanism. Frogs and other amphibians respire by alternatively dilating and contracting the buccopharyngeal cavity. During dilatation, with the mouth and glottis closed, air is sucked in through the open nostrils to fill the cavity. During contraction of the throat, with nostrils closed and glottis open, the air in the buccopharyngeal cavity is pressed into the lungs. During expiration, the glottis and nostrils open and air is expelled from the lungs ‘by their own contraction from a state of distention’. Herholdt (1801), a Danish army surgeon, independently described the buccal pressure-pump mechanism in frogs, his experiments being confirmed by the commissioners of the Société Philomatique in Paris. Haro (1842) reintroduced a suction mechanism for amphibian respiration, which Panizza (1845) refuted: excision of the tympanic membranes prevented lung inflation, the air in the buccopharyngeal cavity leaving through the tympanum holes. Closure of the holes with the fingers restored lung inflation. The importance of cutaneous respiration in frogs and other amphibians was discovered by Spallanzani (1803), who found that frogs might survive excision of the lungs and that the amounts of exhaled carbon dioxide were small compared with those eliminated through the skin. Edwards (1824) confirmed and extended Spallanzani's findings, and Regnault & Reiset (1849) attempted to establish the relative importance of skin and lungs as respiratory organs in frogs. The problem was solved by Krogh (1904a) who measured respiration through the skin and lungs separately and simultaneously. Krogh (1904a) confirmed that carbon dioxide was chiefly eliminated through the skin, correlated with its high diffusion rate in water and tissue, whereas the pattern of oxygen uptake varied seasonally, the pulmonary uptake being lower than the cutaneous during autumn and winter, but substantially higher during the breeding period. Dolk & Postma (1927) confirmed this respiratory pattern. More recently, Hutchison and coworkers have examined the relative role of pulmonary and cutaneous gas exchange in a large number of amphibians, equipped with head masks for the separate measurement of the lung respiration in normally ventilating animals (Vinegar & Hutchison, 1965; Guimond & Hutchison, 1968; Hutchison, Whitford & Kohl, 1968; Whitford & Hutchison, 1963, 1965, 1966). As early as 1758, Rösel von Rosenhof suggested that the lungs of frogs in water functioned as hydrostatic organs that permitted the animal to float at the surface or rest on the bottom of the pond. The suggestion was inspired by observations made in the second half of the seventeenth century by members of the Royal Academy of Sciences in Paris. The French anatomists demonstrated that a tortoise, presumably the European freshwater turtle Emys orbicularis, could regulate its buoyancy by changing the volume of the lungs, to descend passively or ascend in the water. The hydrostatic function of the lungs has been repeatedly rediscovered, by Emery (1869) in the frog, by Marcacci (1895) in frogs, toads and salamanders, by Whipple (1906b) in a newt, by Willem (1920, 1931) in frogs and Xenopus laevis, by Speer (1942) in several anurans and urodeles, and finally by de Jongh (1972) in Xenopus laevis. In the second half of the nineteenth century a number of important papers appeared which confirmed and extended Townson's (1794) and Panizza's (1845) analysis of the normal respiratory movements in frogs. Lung ventilation cycles, interspaced by oscillatory movements of the throat, might periodically be replaced by a sequence predominated by inspirations, resulting in lung inflation, followed by exhalations that restored normal lung volume. Babák (1912a) established that inflations were reactions to the experimental manipulations, and that in resting, undisturbed frogs, lung ventilations normally occurred singly, interspaced by series of approximately 10–50 buccal oscillations. Extensive comparative studies early in the century showed that the respiratory mechanisms and patterns were basically similar in all anurans and urodeles investigated. The modern era of investigations in amphibian respiration began with the work of de Jongh & Gans (1969). They recorded pressures in the buccal cavity, lungs and visceral cavity and electrical activity of some 15 muscles possibly associated with respiration in the bullfrog Rana catesbeiana. The respiration recorded in the frogs was predominated by cycles of lung inflation and deflation, consistent with substantially but not excessively disturbed frogs. Studies by other investigators on various anuran species showed respiratory patterns that varied strongly with respect to the frequency and degree of lung inflations, presumably reflecting degrees to which the experimental conditions affected the breathing.

The elucidation of the role of the buccopharyngeal ventilation in amphibian olfaction can be traced to the realization in the 1890s that the nasal cavity has a double function in being both the seat of the sense of smell and part of the respiratory passages. The ability of amphibians to smell and to react to air-borne or water-borne chemical cues in the environment thus depends on the oscillatory movements of the buccal floor which ventilate the nasal cavity. Experimental evidence for a sense of smell was, however, lacking, and it was first furnished in urodele feeding early in the present century. Despite the demonstration of the fundamental role of the nasobuccal oscillatory ventilation in olfactory responses to food in newts, the oscillatory throat movements in amphibians continued, however, to be referred to as respiratory. Evidence concerning the role of the buccopharyngeal ventilation in respiration had been circumstantial until Whitford & Hutchison (1963, 1965, 1966) determined the relative importance of cutaneous and pulmonary/buccopharyngeal respiration in lunged and lungless salamanders. In lungless salamanders, the buccopharyngeal mucosa accounted for approximately 25% of the total oxygen consumption, and it was concluded that buccopharyngeal oscillatory ventilation in salamanders is primarily respiratory in function, a possible olfactory function being secondary. During the last decades an extensive literature has accumulated on the role played by olfaction in the life of urodeles, but also in feeding in anurans. Often the descriptions of behaviour elicited by air-borne or water-borne odours also note increased oscillatory movements of the buccal floor, indicating the importance of the ventilation of the nasal cavity. In the elucidation of the functional significance of buccal oscillations in vertebrate evolution, the reptiles are of particular interest because such oscillations are also known in chelonians, crocodiles and some lizards. Olfaction plays a role in the life of chelonians and crocodiles which respire by means of suction mechanisms. The throat movements are thus not concerned with the ventilation of the lungs but presumably with olfaction. It is thus indicated that in lower vertebrates, including the amphibians, the shallow oscillatory movements of the buccal floor primarily serve to establish olfactory contact with the surrounding medium, air or water, whereas a respiratory function is secondary.