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.