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Natural History

Salamanders without Lungs:
Family Plethodontidae

by Aaron Dickey

As lunged salamanders metamorphose, they lose their gills and thus begin to rely on the lungs for a certain amount of oxygen uptake -- the percentage depends on lung tidal volume, and temperature (Whitford and Hutchison 1965, 1966). Most carbon dioxide is released through the skin in all salamanders. After metamorphosis, the lungs still serve a hydrostatic function when a terrestrial salamander such as Ambystoma tigrinum returns to the water (e.g. for breeding); and in purely aquatic pond dwellers, lungs are available for buoyancy throughout the entire life cycle of the animal.

Wilder and Dunn (1920) proposed that buoyancy would not be advantageous to the larvae of plethodontid ancestors developing in these swift mountain waters. Such animals would be readily displaced downstream and out of their environment. On the other hand, lungless larvae and larvae with reduced lungs would tend to sink to the stream bottom where they could establish and maintain their position against the water current. Such a rheotropic response is indicated by several authors including the current defendants of the hypothesis (Beachy and Bruce 1992, Bruce et al. 1994).

The cold, swift, and thus well oxygenated waters would have further facilitated the switch from lungs to skin. Thus, emerging terrestrial adults would be completely reliant on cutaneous gas exchange due to adaptations of the larval form, a theory which held up for nearly 70 years before recently being challenged.

The Challenge:
John Ruben and Arthur Boucot from Oregon State University challenge this theory on the basis of late Mesozoic Appalachian topography and climate (Ruben and Boucot 1989). Citing geological and paleontological evidence from Dunbar (1964) and Stanley (1986), they claim that Appalachia was a flat peneplain throughout the middle and late Mesozoic. Thus, Appalachian stream habitats have not been stable since the mid-Mesozoic, a fundamental assumption to the long held scenario. Our current mountains of the area appeared during the Late Cenozoic upwarp between 3 and 10 Mya.

Without mountains, evolving Protoplethodontids would have lacked the cool, fast, and well oxygenated streams now known to the area. In fact, the challengers cite evidence claiming the area would have been subtropical year-round (Kauffman 1973; Frakes 1979). Larval Protoplethodontids would not have likely lost their lungs in such warm, slow, and oxygen poor environments.

Whitford and Hutchison (cited above), performed experiments on gas exchange in various ambystomatid salamanders. They concluded that the species with less buccopharyngeal volume and thus less lung tidal volume relative to the size of the animal, relied on their skin for more oxygen uptake. Ruben and Boucot modified their data as well as the data of (Bishop 1943) to show that the species with narrower heads relative to snout-vent length have higher percent oxygen consumption performed by the skin.

"The time of origin for plethodontid salamanders is a point of debate. The Plethodontids are first found in the fossil record in the early Miocene, and some authors have estimated that the Plethodontids are more recent than the Cretaceous (Naylor 1980; Carroll 1988). In contrast, there are data on ribosomal RNA evolution that suggest that the Plethodontidae is a much older lineage (Larson and Wilson 1989)" -- taken from (Beachy and Bruce 1992).

Bruce, R. C., C. K. Beachy, P. G. Lenzo, S. P. Pronych, and R. J. Wassersug. 1994. Effects of lung reduction on rheotactic performance in amphibian larvae. Journal of Experimental Zoology 268:377-380.

Lombard, R. E. and D. B. Wake. 1986. Tongue evolution in the lungless salamanders, family plethodontidae. IV. Phylogeny of plethodontid salamanders and the evolution of feeding dynamics. Systematic Zoology 35:532-551.

Ruben, J. A. and A. J. Boucot. 1989. The origin of the lungless salamanders (Amphibia: plethodontidae). American Naturalist 134:161-169.

Whitford, W. G., and V. H. Hutchison. 1966. Cutaneous and pulmonary gas exchange in ambystomatid salamanders. Copeia 1966:573-577.

Wilder, I. W., and E. R. Dunn. 1920. The correlation of lunglessness in salamanders with a mountain brook habitat. Copeia 84:63-68.

Dunbar, C. O. 1964. Historical geology. 2d ed. Wiley, New York.

Carroll, R. L. 1988. Vertebrate paleontology and evolution. W. H. Freeman, New York.

Frakes, L. A. 1979. Climates throughout geologic time. Elsevier, Amsterdam.

Kauffman, E. G. 1973. Cretaceous Bivalvia. Pages 353-383 in A. Hallam, ed. Atlas of palaeobiogeography. Elsevier, Amsterdam.

Larson, A., and A. C. Wilson. 1989. Patterns of ribosomal RNA evolution in salamanders. Molecular Biology and Evolution 6:131-154.

Naylor, B. G. 1980. Radiation of the Amphibia Caudata: are we looking too far into the past? Evolutionary Theory 5:119-126.

Stanley, S. M. 1986. Earth and life through time. Freeman, New York.

Wake, D. B. 1966. Comparative osteology and evolution of the lungless salamanders, family Plethodontidae. Memoirs of the Southern California Academy of Sciences 4:1-111.

Whipple, I. L. 1906. The ypsiloid apparatus of urodeles. Biological Bulletin 10:255-297.

Whitford, W. G., and V. H. Hutchison. 1963. Cutaneous and pulmonary gas exchange in the spotted salamander, Ambystoma maculatum. Biological Bulletin 124: 344-354.

Whitford, W. G., and V. H. Hutchison. 1965. Gas exchange in salamanders. Physiological Zoology 38:228-242.