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Skin Breathing in Vertebrates It can supplement or replace breathing through lungs or gills. Special adaptations of the skin and the circulatory system help to regulate the cutaneous exchange ofox ygen and carbon dioxide by Martin E. Feder and Warren W. Burggren erhaps because people breathe al­ Among amphibians it is not unusual in the air and become useless. The ade­ Pmost exclusively with their lungs, for at least 30 percent of the total oxy­ quacy of the skin as an air-breathing respiration is often thought of as gen uptake and as much as 100 percent organ seems to have escaped the atten­ taking place only in specialized organs: of the carbon dioxide elimination to tion of many biologists who assume if not in the lungs, then in the gills of take place across the skin. Frog larvae, that lungs were a prerequisite for the fishes and crustaceans, the tracheae of for example, exchange approximately evolution of terrestrial animals. insects or the book lungs of spiders. 60 percent of their respiratory gases Commoner types of fishes also rely Yet whenever a relatively thin mem­ through their skin even though they on cutaneous gas exchange. Sharks, brane separates the respiratory me­ also have both gills and lungs. trout, cod and goldfish-to name a dium (the air or water an animal Amphibians that spend almost all few-acquire between 5 and 30 per­ breathes) from living cells or flowing their time on land rather than in water cent of their total oxygen by way of blood, oxygen can enter the cells and face potentially life-threatening diffi­ the skin. Apparently neither the struc­ the blood and carbon dioxide can culties because the same characteris­ ture of the integument nor the shape leave them. The recent findings we tics that make skin an effective mem­ of the body determines the extent shall discuss here suggest that the skin brane for gas exchange also facilitate to which a particular fish breathes serves as an effective and highly regu­ water loss. Nevertheless, cutaneous through its skin. Both the flat, scale­ lated organ of gas exchange in many gas exchange has been found in every less plaice and the elongated, heav­ vertebrates. species of terrestrial amphibian exam­ ily scaled reed fish derive about a third Cutaneous gas exchange has long in­ ined for this capacity. In fact, the skin of their required oxygen cutaneously. trigued physiologists. Pioneering stud­ is the sole respiratory organ in adult Reptiles have been shown to take ad­ ies were made by August Krogh at the salamanders of the family Plethodon­ vantage of cutaneous gas exchange as turn of the century in Denmark. Krogh tidae. Scores of these species inhabit well. In spite of their thick shells, some obstructed the airflow to the lungs of terrestrial environments as diverse as freshwater turtles rely heavily or even frogs and observed that the skin could the ground litter of New England totally on cutaneous gas exchange, supply enough oxygen to the blood woods and the canopy of tropical rain particularly while passing the winter in during the winter, when frogs are nor­ forests. Although some tropical pleth­ ice-covered ponds. Snakes inhabiting mally quiescent; during other seasons, odontids may attain a body mass of both fresh and salt water typically ex­ however, lungs proved to be neces­ 150 grams and a body length of 24 ploit their skin as a respiratory organ. sary. Krogh's research on blood circu­ centimeters, they accomplish all respi­ These reptiles often dive for long peri­ lation through capillaries earned him ratory gas exchange between tissue ods and supplement oxygen stores in the 1920 Nobel prize in physiology and environment by way of their skin. the lungs and blood with oxygen ac­ or medicine. quired by way of the skin. Roger S. Numerous experimental studies in kin breathing has been looked for Seymour of the University of Adelaide the 1960's and 1970's examined the in other vertebrates, from fishes to in Australia has even suggested that partitioning of gas exchange among an mammals.S It has been demonstrated some sea snakes use their skin to elimi­ animal's respiratory organs: the skin, experimentally, for example, that am­ nate nitrogen during prolonged deep lungs and gills, if present. For exam­ phibious (air breathing) fishes rely on dives, thereby preventing decompres­ ple, by placing plastic masks over their skin for as much as half of their sion sickness (the formation of nitro­ the faces of salamanders, Victor H. gas exchange, particularly if they ven­ gen bubbles in blood) as they surface. Hutchison and his students at the Uni­ ture onto land: gills typically collapse Many reptiles that live in arid environ- versity of Rhode Island were able to determine what proportion of the an­ imal's total oxygen is taken in through the skin and what proportion of the THREE SKIN-BREATHING VERTEBRATES are depicted on the opposite page: a lung­ total carbon dioxide is eliminated less salamander, a plaice and a sea snake. The salamander Ensatina eschscholtzii lives in the forests of California and Oregon; it is about five centimeters long when fully developed. The through it. The results of these and skin is the sole respiratory organ in adults of this species. The plaice Pleuronectes platessa, many other such experiments provide a commercially valuable flatfish of the �orth Atlantic, takes in 27 percent of its oxygen a surprisingly long list of vertebrate through the skin. The fish can grow to a weight of five kilograms and a length of 90 centi­ skin breathers. meters. The sea snake Pelamis platurus absorbs more than a third of its oxygen and excretes Probably the best-known of these more than three-fourths of its metabolic carbon dioxide cutaneously. The snake reaches a skin breathers are the amphibians. length of about a meter; it ranges the tropical Pacific Ocean, between America and Africa. 126 © 1985 SCIENTIFIC AMERICAN, INC J , © 1985 SCIENTIFIC AMERICAN, INC CAT SHARK Scyliorhinus canicula BROWN TROUT Salmo trutta GOLDFISH Carassius carassius PLAICE Pleuronectes platessa EUROPEAN EEL Anguilla anguilla REEDFISH Calamoichthys calabaricus MUDSKIPPER Periopthalmus cantonensis TIGER SALAMANDER Ambystoma tigrinum MUDPUPPY Necturus maculosus BULLFROG (LARVA) Rana catesbeiana BULLFROG (ADULT) Rana catesbeiana HELLBENDER Cryptobranchus alleganiensis LUNGLESS SALAMANDER Ensatina eschscholtzii SEA SNAKE Pelamis platurus ELEPHANTS-TRUNK SNAKE 1----"""'""-------, Acrochordus javanicus BOA CONSTRICTOR Constrictor constrictor SOUTHERN MUSK TURTLE Sternotherus minor RED-EARED TURTLE Pseudemys scripta GREEN LIZARD Lacerta viridis CHUCKWALLA Sauromalus obesus BIG BROWN BAT Eptesicus fucus MAN Homo sapiens ! I I I ! 10 20 30 40 50 60 70 80 90 100 PERCENT OF TOTAL GAS EXCHANGE CUTANEOUS GAS EXCHANGE is widespread among verte­ ous excretion of carbon dioxide (gray bars) typically accounts for a brates. Although it is most prominent in amphibians, this mode of larger fraction of total gas exchange than cutaneous oxygen uptake respiration is also important in many other animal groups. Cutane- does (colored bars)in those cases where both gases were measured. 128 © 1985 SCIENTIFIC AMERICAN, INC ments, where dehydration is a constant a c danger, have countered this problem by evolving thick scales, a shell or AIR leathery skin. A few species, such as the chuckwalla lizard (Sauromalus obe­ sus) of the southwestern deserts of the U.S., do exhibit some cutaneous gas exchange regardless of their thick, pro­ tective skin. Although cutaneous respiration is often significant and even crucial in lower vertebrates, the skin is seldom an important avenue for gas exchange b d among higher vertebrates such as birds 100 .------------------------. and mammals. Even if the furred or feathered integument of such crea­ tures were as permeable as the skin of frogs, the higher vertebrates would 50 need lungs to sustain their much great­ er metabolic rate. Lungs offer a larger and thinner surface for gas exchange O L-----------------------� than the skin can provide. Yet there DISTANCE ALONG DISTANCE ALONG are exceptions to this generalization. EXCHANGE SURFACE EXCHANGE SURFACE Clyde F. Herreid II and his colleagues at Duke University found that in bats CUTANEOUS OXYGEN UPTAKE is limited by the thickness of the skin's diffusion as much as 12 percent of total carbon barrier : the distance between the respiratory medium (air or water) and the blood. Oxygen dioxide elimination may take place can diffuse quickly through the thin alveolar membrane of the mammalian lung (a); blood­ (dark red) across the thin, well-vascularized wing cell hemoglobin is rapidly oxygenated and blood in adjacent capillaries is com­ pletely saturated with oxygen (b). Because diffusion of oxygen through the thicker skin (c) is membranes. much slower, the blood in capillaries under the skin is never fully saturated with oxygen (d). Young mammals and birds are often born or hatched with thin skin, richly supplied with blood and lacking fur or feathers. Cutaneous respiration may and gills. They have emphasized the Scheid, Randall Gatz and Eugene therefore be more important in the de­ circumstances under which cutaneous Crawford of the Max Planck Institute veloping forms of such higher verte­ gas exchange would be precluded and for Experimental Medicine in Gottin­ brates than it is in the adults. There is pointed to the thick skin or scales and gen have shown that cutaneous gas ex­ probably significant cutaneous gas ex­ the limited cutaneous surface area change is diffusion-limited. That is, the change in the mammalian embryo and of most vertebrates as characteris­ diffusion of respiratory gases through fetus; gas exchange through the shell tics likely to hinder cutaneous gas ex­ the relatively thick skin of vertebrates and the shell membrane is the major change. The thrust of most of these is so slow that it is not able to transfer avenue of respiration available for the contentions rests on the physical prin­ oxygen and carbon dioxide as rapidly eggs of birds and indeed of all egg-lay­ ciples governing gas exchange.

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