Skin Breathing in Vertebrates

Home , Breathing gas, Cutaneous respiration, Reedfish, Telmatobius culeus

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 effectivemem 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) fishesrely 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 fivecentimeters 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 fivekilograms 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.

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 significantcutaneous 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. as the gases are transported from or to ing vertebrates [see "How Bird Eggs Oxygen and carbon dioxide pass the skin by the blood and the respirato Breathe," by Herman Rahn, Amos Ar through the membrane of a gas ex ry medium. and Charles V. Paganelli; SCIENTIFIC changer by means of a physical proc Other studies demonstrated anoth AMERICAN, February, 1979]. ess called diffusion. Diffusion is de er problem encountered by cutaneous VVhat about cutaneous gas exchange fined as the equilibrating flow of mat gas exchange. Equilibration between in people? Human skin certainly does ter, through the random movement of the gas concentrations in the blood not serve as a respiratory organ for the molecules in a fluid or gas, from a re flowing through capillaries inside the general benefit of the body tissues. Yet gion of high concentration to one of skin and in the respiratory medium the skin, like any living tissue, con low concentration. Because the gas outside the skin is governed by Fick's sumes oxygen and generates carbon di exchange membranes of lungs and law of diffusion: the rate of gas ex oxide. All the respiratory gases con gills are typically very thin (less than change is proportional to the differ sumed or produced by skin cells, as a thousandth of a millimeter in the hu ence between the partial pressure of well as an undetermined additional man lung), equilibration with the res the gas in the respiratory medium and quantity of carbon dioxide from capil piratory medium is achieved extreme its partial pressure in the blood. (P ar lary blood flowing through the skin, ly rapidly. A more important limita tial pressure, the pressure of a gas in a are exchanged directly between skin tion to gas exchange in lungs and gills solution or a gas mixture, reflects both and air. In fact, the permeability of the is the speed with which the blood car the concentration of the gas and its sol skin is exploited medically when drugs ries oxygen away from the exchange ubility.) /'( gas will therefore diffuse are administered by applying patches surface or delivers carbon dioxide to through the skin only if its local partial to the skin. it. Rapid diffusion makes it possible pressure on one side of the skin is for animals with lungs or gills to regu greater than its partial pressure on the n spite of their number, studies of late gas exchange by simply increas other side; the greater the difference is, I cutaneous gas exchange generally ing or decreasing blood flow through the faster it will diffuse. have discounted the prevalence of skin the respiratory organ. As studies by Donald C. Jackson breathing among vertebrates by stress In contrast, increasing the flow of and his colleagues at Brown Universi ing its limitations. For example, inves blood to the skin has been thought to ty have shown, this relation may have tigators have tended to contrast the have little effect on total gas exchange fateful consequences for skin-breath skin to the elegantly structured lungs in vertebrates. Johannes Piiper, Peter ing vertebrates. If the respiratory me-

© 1985 SCIENTIFIC AMERICAN, INC 129 dium surrounding a skin-breathing an needs or the environment varies. To shapes arose to equip these organisms imal has a greater partial pressure gether these mechanisms support a re with enough skin for adequate. cutane of carbon dioxide than the animal's markably effective capability for con ous gas exchange. blood, the animal will actually gain trolling cutaneous gas exchange. Other species of amphibians perma ' carbon dioxide from the environment One obvious way to regulate skin nently bear numerous skin folds that instead of losing it. Similarly, if high breathing depends on the fact that cu also increase the surface area for cuta temperature or activity increases car taneous gas exchange is limited in part neous gas exchange. The most spectac bon dioxide production, many skin by the total skin surface area. Conse ular of these is the Lake Titicaca frog, breathing amphibians cannot immedi quently a change in surface area can Telmatobius culeus, which inhabits ately excrete the excess; they must first increase or decrease the amount of gas the lake for which it is named in the wait for the internal carbon dioxide exchanged through the skin. In spite of Andes between Peru and Bolivia. As partial pressure to rise above the exter a rigid internal skeleton and a relative Victor Hutchison and his colleagues nal partial pressure. Fick's law governs ly fixed form, many vertebrates exhibit at the University of Oklahoma discov the diffusion of oxygen as well. Our seasonal changes in surface area that ered, the Lake Titicaca frog is so well own studies have shown that amphibi augment cutaneous gas exchange pre adapted for skin respiration that it ans may actually lose oxygen when cisely in this way. does not need to ventilate its lungs at their blood contains more oxygen than For example, some male amphibi all. One major explanation for this the water surrounding them. ans engage in elaborate and strenuous ability is the pendulous folds of skin Human beings can excrete excess courtship rituals that may include re that protrude from its hind limbs and carbon dioxide by simultaneously in peated body movements lasting for trunk. Other species in the genus Tel creasing blood flowto the lungs and hours. Associated with this behavior is matobius and in other genera of frogs raising the respiration rate while main a greatly increased requirement for have similar skin folds. In some types taining a constant partial pressure of oxygen uptake and carbon dioxide of amphibians such as the hellbender, carbon dioxide in the blood. The in elimination. Apparently in response to Cryptobranchus a lleganiensis, a large ternal gas partial pressures of skin the increased respiratory burden, parts aquatic salamander, the skin folds are breathing animals, on the other hand, of the skin in these amphibians gradu minute but numerous and are richly seem to be poorly controlled and sub ally become enlarged or develop out invested with capillaries. ject to the ever changing balance be growths during the courtship season. A second adaptation enhancing the tween external gas concentrations and Such surfaces act as accessory gas-ex capability for cutaneous gas exchange internal demands for gas exchange. change organs. is a reduction in the thickness of the Changes in the skin structure to this skin to lessen its resistance to the diffu he fact remains that in spite of the end appear in the male hairy frog, As sion of respiratory gases. In addition to Tdaunting limitations imposed by tylosternus robustus. Tiny dermal papil being devoid of such physical barriers the diffusion process, vertebrates do lae that superficially resemble hair ap as hair, feathers or scales, amphibian rely on cutaneous gas exchange to a pear on its hindquarters. The enlarged skin is typically only between 10 and significant degree. We recognized that tail fin and the dorsal crest developed 50 micrometers (millionths of a meter) this paradox could be resolved by con by males of many species of newts dur thick. Actually the significant morpho sidering the different mechanisms ver ing the courtship season also could logical factor governing diffusion in tebrates have at their disposal to regu contribute to the total amount of gas this connection is not the total thick late cutaneous gas exchange. Some of diffusing through the skin. The male ness of the skin but rather the thick these mechanisms seem obvious, al skin enlargements typically regress ness of the "diffusion barrier," the dis though they had seldom been recog when the breeding season ends. More tance between the respiratory medium nized as potentially important in this over, such structures do not occur at outside the skin and the blood flow respect. Other suggested regulatory all in the relatively quiescent females ing through the cutaneous capillar processes are subtler. The various reg of these species. ies. Hence any morphological change ulatory mechanisms can be divided that reduces the distance between the into two categories: mechanisms that n addition to these seasonal changes bloodstream and the respiratory medi are permanent morphological adap I in cutaneous surface area amphib um helps to increase gas exchange. tations or responses to long-term ians have evolved a number of per We demonstrated through a simple changes (days, weeks or months) in manent morphological characteristics experiment that such changes are in the environment or in the animal's that promote skin breathing. Many deed possible within a fraction of an physiology, and mechanisms that are amphibians have what seem to be dis amphibian's lifetime. Frog larvae were called on from minute to minute as proportionately elongated bodies or reared in two enclosures, one contain an organism's immediate respiratory tails. It has been argued that such ing well-aerated water and the other

HELLBENDER (Cryptobrallchus allegie1/sis)is a large aquatic sal U.S. It reaches a length of about 70 centimeters. Although the hell amander found in swift-flowing streams of the eastern and central bender has lungs, it breathes primarily through its very wrinkly skin.

130 © 1985 SCIENTIFIC AMERICAN, INC © 1985 SCIENTIFIC AMERICAN, INC © 1985 SCIENTIFIC AMERICAN, INC There are megabit chips. And there allowing for lower operating costs and Now we're talking computer are megabit chips. All of them can reduced cooling requirements. POW ER, because these new chips access more than 1 million bits of infOl� The AT&T megabit chip is smaller with micro-parts could work at pico mation. But not all of them can access than a dime, yet has more than speeds (trillionths of a second). Cur these 1 million bits of information AT&T 2 million elements on it. Among those rent estimates suggest 10-picosecond fast. And fast to AT&T is 20 million 2 million-plus elements are more than transistors. bits per second. 20,000 spare memory cells for AT&T will not let the chips fall That means we can pour out safety's sake. If for where they may. We'll put them where 1,048,576 bits much faster than you can some reason there's a they'll do the most good -in the say "byte." And we can do it because bad cell in a chip, a powerful and reliable digital systems only the AT&T megabit chip has a computer-controlled creating the general-purpose informa fast column access mode. test targets the cell tion technology we call Universal The "Trickle-Down" Theory Vs. and its whole row or Information Services. Our continu The "Spigot" Theory Actual size column -for replace- ing flow of advanced technology is one Most other megabit chips use a ment. A laser redundancy technique, reason why AT&T is the right choice. "page mode" to access their memory pioneered by AT&T, then disconnects cells. When a chip is in this mode, its the offenders and automatically fastest data rate is about 10 million replaces the entire memory row or bits per second. column from the spares. But the fast column cycle, developed Cleanliness Is Next To Goodliness by AT&T Bell Laboratories, pours out A speck of dust on a megabit chip is data twice as fast. And not only does like a boulder on a railroad track. data flow out faster, getting data out is To keep our chip clean, it has to be easier with the fast column, because made in a room that's C-L-E-A-N. access timing requirements are less And an AT&T class-1O clean room is demanding. Valid data are always one of the cleanest rooms in the world available during the entire access -where the air contains fewer than cycle. 10 particles of dust in a cubic foot of air. And speed, ease of use and timing And the largest particle must be tolerance will make it easier for AT&T smaller than 11150 the diameter of a to design new and improved products human hair.That makes our room and high-speed systems around the 10,000 times cleaner than a hospital megabit chip. operating room. The Megabit Special 'lb keep our air clean, we have to Because this megabit chip is keep it moving. Ours is constantly cir designed for manufacturability, you culated and filtered by fans that could might want to know what, besides its inflate the Goodyear blimp in only 30 fast column, makes it special. It's seconds. made using an advanced CMOS You Ain't Seen Nothing Yet Complementary Metal-Oxide Semi Looking toward the year 2000, conductor-process that makes it pos today's technology predicts submicron sible to provide high performance at design widths, with lines only 400 • reduced power consumption. atoms wide. Chips containing 100 mil - As a matter of fact, it uses 118 the lion components-50 times the current - power per bit of most 256K DRAMs. amount -could have tiny regions with The lower power requirement is a plus capabilities that more than match the for any system using the megabit- megabit chip. AT.T The right choice.

© 1985 AT&T Technologies, Inc. © 1985 SCIENTIFIC AMERICAN, INC INCREASED SKIN SURFACE AREA is a prominent morpho exchange that the Titicaca frog does not need to breathe through logical adaptation in two skin-breathing frog species. Pendulous its lungs at all. The male hairy frog, Astylosternus robustus (right), folds of skin have evolved on the Lake Titicaca frog Telmatobius sprouts dermal papillae on its hindquarters as an accessory gas-ex culeus (left). These loose folds provide so much skin area for gas change organ to meet the respiratory demands of the mating season.

contammg water with approximately ment suddenly increases (as it does cruited and cutaneous carbon dioxide half the oxygen concentration of the during activity), or if it suddenly en elimination resumed immediately. aerated water. After four weeks the counters a region of water that has a More recent experiments conducted diffusion barrier in larvae reared in the high carbon dioxide concentration? by Gary Malvin and Michael P. Hlas well-aerated water was 40 microme In most of the vertebrates we have tala of the University of Washington ters, a typical value. In contrast, the examined not all skin capillaries are School of Medicine have also demon diffusion barrier averaged only 20 mi constantly perfused with blood. Skin strated that frogs control capillary crometers in animals reared in the oxy that is distant from underlying capil blood flow in their skin. These investi gen-poor water. Furthermore, the cu laries or that is underlain by non per gations revealed that frogs can reduce taneous capillary network of the ox fused capillaries does not contribute to gas loss through the skin by from 15 to ygen-deprived larvae was finer and overall gas exchange; the functional 30 percent when they are exposed to denser. It appears these larvae under surface area of the skin at any given an atmosphere devoid of oxygen, pre went an acclimatory change that aug time consists only of those skin re sumably by decreasing the amount of mented their capacity for cutaneous gions that overlie perfused cutaneous blood-perfused skin. gas exchange. capillaries. Even vertebrates with a relatively The initiation of blood flow through ust as important as morphological thick skin can carryon significant cuta capillaries (what is called capillary J adaptations and capillary blood neous gas exchange as long as evolu recruitment) can occur in seconds. flow are physiological processes or tion has led to advantageous place (Blushing is a classic, if nonrespirato behavioral responses that affect the ment of the cutaneous capillaries. In ry, example of this in humans.) Capil partial pressures of the respiratory the scaly skin of some lizards, for ex lary recruitment in the skin of amphib gases in the blood within the skin or in ample, the cutaneous capillaries eith ians was documented many years ago the respiratory medium outside the er underlie the skin between the scales by Piotr Poczopko and his colleagues skin. The most important of these are or run under the scale's hinges, where in Poland. They found that in frogs processes that regulate the flow of the scale is thinnest. In some snakes breathing gas with an elevated carbon either the respiratory medium or the the cutaneous capillaries penetrate the dioxide concentration, and in frogs blood along the diffusion barrier. scale itself. The dermal scales of fishes prevented from using their lungs, the Ventilation, the flow of the respira are generally covered by a layer of liv number of perfused skin capillaries in tory medium into or past a gas-ex ing tissue, an arrangement that places creased by nearly a third. change organ, is clearly critical in cutaneous capillaries above the diffu Further experimental confirmation lungs and internal gills. If ventilation sion-resistant scale and very close to that capillary recruitment is linked to stops, gas exchange in these internal the respiratory medium. cutaneous gas exchange has emerged organs declines precipitously because recently from our own studies of bull oxygen is quickly depleted (its partial Adaptations such as skin folds, der frogs. Working at the University of pressure falls) and carbon dioxide is I\. mal papillae and generally thin Massachusetts at Amherst, we ob rapidly accumulated (its partial pres skin, as well as the specialized circula served that when frogs submerged in sure increases) in the respiratory medi tion that may serve these structures, water were exposed to air, the number um enclosed within the body. Ventila obviously develop slowly over days or of perfused skin capillaries rapidly fell tion in the context of cutaneous gas weeks, if not time measured on an evo by 60 percent; simultaneously carbon exchange, on the other hand, has of lutionary scale. How can a vertebrate dioxide elimination by way of the skin ten been considered unnecessary; after regulate cutaneous gas exchange in fell by 44 percent. When the frogs were all, the skin of a vertebrate in air or stantaneously if its oxygen require- returned to water, capillaries were re- in a large body of water is in constant

The performance of a polymeric adhesive depends on the properties and composition of its surface. Now a scientist at the General Motors Research Laboratories has developed and validated a theory that describes the coupled effects of diffusion and chemical reaction on the changing surfaces not only of adhesives, but of chemicallyreacting surfactant systems in general.

HE USE OF adhesives in the adhesive performance. Dynamic Surface Properties T production of an automobile The understanding of time ...... Experimental __ ..• • pt t • promises to make both the product dependent surface tension has been ..----� •• dibutyl·IA=1.O> 1 and the process more efficient. Both advanced by the work of Dr. Robert § weight and operations can be re Foister, a scientist at the General duced_ In practice, however, steel Motors Research Laboratories. and other metallic surfacesare often Investigation of dynamic surface .� contaminated by process lubricants. properties of thermosetting adhe I A durable bond depends on the abil sives led him to develop a general 10 20 30 40 50 ity of an adhesive to displace con theory of adsorption kinetics in Time (min) taminants and to wet the substrate. binary, chemically reacting surfac Theoretical .30 Assuring intimate contact tant systems. The significance of i .25 between adhesive and substrate this theory is that it includes the .3 .20 requires detailed knowledge of adhe coupled effects of surfactant diffu

.15 sive surface tension, since it is this sion and chemical reaction, mak

.10 property that controls displacement ing it possible for the first time to j� .05 of contaminants and wetting. Up describe quantitatively the chang 1 to now the surface tension of an ing surfaces of such systems. i5 0.2 0.4 0.6 0.8 1.0 adhesive has typically been as In a typical adhesive that poly Time (dimensionless) sumed constant. In reality, though, merizes, or "cures;' by chemical Figure1: Experimental measurements of spread ing pressure v. time for dialkylaminopropyl surface-active components in the reaction (Figure 2), a surface-active amines with various DamMhler numbers(A), adhesive collect preferentially at curing agent (Solute 1) reacts with and co"esponding theoretical calculations of the interface and also react, so the host resin to form a second sur/ace concentrations. that the surface composition varies surface-active species (Solute 2) Figure 2: Evolution of an adhesive surface: with time, giving rise to dynamic that is also reactive. Both solutes Surface-active Solute 1 (red) reacts with host resin (pink tone) to form sur/ace active Solute surface tension. Variations can be migrate to the surface, lowering 2 (brown). large enough to significantly affect the surface tension. Diffusion to the surface is driven by a potential energy gradient between the sur face and the bulk, with the solute Vapor Phase molecules experiencing a lower energy at the surface. P'!"".,..------j nl"""'l.... 'r" "2""��r-i 1-r��""1""!.... �-r- -K-Surface Dr. Foister derived appropri Sub· ;.�Z:;��I] surface ate transport equations to describe diffusion and chemical reaction in the bulk, in a subsurface region, and • • • at the surface itself. The transport • •• • equations can be solved analytically • • • • • if the chemical rate equations are • • .. assumed to be first order in the • Bulk • • concentrations of reacting species, • • and if the subsurface and surface • .. concentrations can be related to one another by a linear adsorption • • • .. .. Solute 1. isotherm. For more complicated iso therms, a set of coupled, non-linear Initial liquid/vapor surface Maximum surface Near·complete reaction • integral equations is generated. concentration of Solute 1 of Solute 1 Solute 2.

© 1985 SCIENTIFIC AMERICAN, INC These must be solved numerically. prolong the time to maximum, and Analytical solution for the spe would increase the value of the cial case of the linear isotherm surface concentration at the max indicated that the change with time imum (see Figure 1, Theoretical). in surface concentration (and con As a practical consequence, this sequently in surface tension) is would improve wetting by mini composed of two terms: first the mizing the surface tension. THE diffusive flux of Solute 1 into the In experimentsusing a series MAN subsurface from the bulk, and sec of dialkylaminopropylamine curing BEHIND ond the depletion of this solute agents (dimethyl-, diethyl-, and due to chemical reaction. Hence, dibutyl-) in a host epoxy resin THE the surface concentration of Solute matrix, good agreement has been WORK 1 exhibits a maximum with time demonstrated between theoretical Dr. Foister is a Staff Research (Figure 2). This maximum in sur predictions for surface concentra Scientist in the Polymers Depart face concentration corresponds to tion and the measured dynamic ment at the General Motors a minimum in surface tension. spreading pressure, which is the Research Laboratories. change in adhesive system surface Dr. Foister received his under tension due to the curing agent graduate degree from Guilford MODIFYING the transport (Figure 1 , Experimental). College, and holds a Ph.D. in equations to include binary "I expect;' says Dr. Foister, Physical Chemistry from the Uni adsorption isotherms allowed for "that the physical insights gained versity of North Carolina at Chapel consideration of competitive adsorp from this analysis can be applied Hill. His thesis dealt with the role tion of the two reacting and diffus to other reactive surfactant systems of liquid inertia in the intrinsic ing solutes. By solving these equa by using specifically tailored iso viscosities of rod-likepolymers. tions numerically and conducting therms and chemical reaction He did post-doctoral work in dimensional analysis, Dr. Foister schemes. Predicting surface Canada as a Fellow at McGill Uni identified various. dimensionless behavior can certa inly help us versity in Montreal, and in the parameters as predictors of system design better adhesives for specific Applied Chemistry Division of the behavior. The most important of applications, but it is also pertinent Pulp and Paper Research Institute these parameters was a dimension to the performance of anti-oxidants of Canada, working on the micro less number (,\), of the Damkohler and anti-ozonants in synthetic rub rheology of colloidal dispersions. type, involving terms representa ber, for example. And applied to Dr. Foister joined General tive of reaction, diffusion, and interfaces in biological systems, a Motors in 1980. He is the leader adsorption. suitably modified theory may prove of the Structural Adhesives Group valuable in understanding the phe in the GMR Polymers Department. k (Tm a)2 ,\ = ------'-'---"'--'-'-'---- nomenon of enzyme activitY,' His current research interests center 4D on surface chemistry and adhesion. Here k is the reaction rate constant of Solute 1 , D its diffu General Motors sivity, Tm its "surface capacity" (the maximum number of molecules absorbed per unit surface area), and a its "surface affinity"(a mea sure of its energy of adsorption). For an adhesive, lowering ,\ by reducing k (the reactivity of the curing agent), for example, would

© 1985 SCIENTIFIC AMERICAN, INC a b velocities would suffice to dissipate the diffusion boundary layer in air. To test our hypothesis we immo bilized bullfrogs in wire-mesh enve lopes to ensure that spontaneous b.ody movements would not dissipate the boundary layer and that their cutane ous surface area would be constant and maximal. We then placed each an imal, sandwiched in its envelope, in a leakproof chamber. The chamber was filled with water so that only the frog's nostrils were above the surface. We could measure the decline in oxygen concentration in the air and the water compartments and so calculate the re c spective pulmonary and cutaneous oxygen consumption. By actuating a stirrer at the bottom of the chamber we could ventilate the skin with the sur rounding water. The results support our hypothesis. When we stopped ventilating the skin, the cutaneous oxygen consumption (determined by measuring the oxy gen concentration in the water) de clined by about a third. This result is clearly in conflict with the notion that ventilation is unimportant in cutane ous gas exchange.

As we have stressed, the extent of cu I\. taneous gas exchange is deter mined by many variables other than MICROSCOPIC MORPHOLOGICAL RESPONSES that facilitate skin breathing under ventilation, including the skin's func adverse conditions are shown in two pairs of photomicrographs. The capillary network in tional surface area and the oxygen the skin of frog larvae becomes finer and denser when the larvae live in oxygen-poor water partial pressure on the inside of the (a) than it does when they live in oxygen-rich water (b). The distance between capillaries diffusion barrier. Might the decrease and the surface of the skin in frog larvae can also vary depending on the oxygen content in cutaneous oxygen consumption as of the water: the capillaries of larvae reared in oxygen-poor water are closer to the skin sur face (c) than the capillaries of larvae raised in water having a high oxygen concentration (d). sociated with the stopping of venti lation in fact be due to one of these other factors? contact with an "infinite pool" of res boundary layer, allowing hot water Our previous experiments had im piratory medium containing abun again to come in contact with the skin pressed on us the importance of func dant stores of oxygen and only small and again to cause pain until the tional surface area and capillary re amounts of carbon dioxide. boundary layer is reestablished. Even cruitment. We therefore repeated the Yet the Lake Titicaca frog waves its in an infinite pool (or finite tub) of hot ventilation experiments with frogs in large skin folds and the hellbender water, stagnation of the medium next which we could observe the relative rocks its body. Moreover. both ani to the skin can limit heat transfer. numbers of perfused and nonperfused mals increase the freq uency of these We envision a similar relation for capillaries. The amount of oxygen tak movements when the concentration of the exchange of respiratory gases, par en in through the skin could have been oxygen in the water decreases. Are ticularly in water. If both the animal lessened by a reduction in the number these behaviors unrelated to respira and the water are stationary, oxygen of perfused capillaries in the frog's tion or might they serve to augment diffusing out of water adjacent to the skin. We found the opposite to be the cutaneous gas exchange by ventilating skin and into the bloodstream would case: whenever stirring was stopped, the skin? create a diffusion boundary layer of the frogs recruited additional skin cap As we examined these peculiar be low oxygen partial pressure. Because illaries. Because capillary recruitment haviors we reflected on the physical the rate of diffusion is proportional should increase cutaneous gas ex considerations that influence the ex to the difference in oxygen partial change, the decline in cutaneous oxy change of heat. Heat exchange is often pressures on each side of the diffu gen consumption, observed whenever severely limited in still air or water and sion barrier, cutaneous gas exchange ventilation stopped, cannot be due to is facilitated when the medium (or the would decrease. Movement of either changes in functional surface area. heat emitter) is moving. If, for exam the animal, the water or both could In a third experiment we measured ple, one sinks into a tub of hot water dissipate the boundary layer and there the partial pressure of oxygen in blood and remains still, one feels pain as heat by increase the diffusion of oxygen carried by arteries leading to the skin. enters the skin. As the heat leaves the across the skin. We calculated that the If the partial pressure of oxygen in layer of water surrounding the skin, diffusion boundary layer should offer creased every time stirring stopped, the fluid forms a relatively cool bound a significant resistance to gas exchange this could explain the observed drop in ary layer. Any rapid movement of the at water flow velocities of four centi the rate of oxygen diffusing from the skin or the water will dissipate the meters per second or less. Much lower water into the blood. Stirring had no

138 © 1985 SCIENTIFIC AMERICAN, INC effect on the blood's oxygen partial it would best promote gas exchange, to the skin by way of the cutaneous pressure, however. The results sug Amphibians, moreover, are unique arteries, 'gest that the formation of a diffusion in having cutaneous arteries, which di Graham Shelton and his colleagues boundary layer was indeed responsi rect transfer of deoxygenated blood at the University of East Anglia in En ble for the decrease in cutaneous oxy to the skin. Blood can leave the single gland have shown that amphibians can gen uptake, and that skin ventilation ventricle of an amphibian heart by ei channel deoxygenated blood into the could serve to regulate gas exchange ther of two routes, One way is through pulmocutaneous arteries and thence by dissipating the layer. the systemic arteries, which carry oxy selectively to either the lungs or the genated blood directly to the brain, skin for gas exchange, The basis for he partial pressures of oxygen and muscles, viscera and ultimately to the such ability may lie in the structure of Tcarbon dioxide in blood within skin. The second route is through the the heart and in the muscular sphinc cutaneous capillaries vary according to pulmocutaneous arteries, which sup ters that surround the pulmonary and whether or not the blood is oxygenat ply deoxygenated blood to the lungs cutaneous arteries after they diverge ed. This provides another possible reg by way of the pulmonary arteries and from the common pulmocutaneous ulatory device. By controlling whether the blood flowing to the skin is prima rily oxygenated or deoxygenated, an .5 organism could presumably regulate the amount of oxygen and carbon di (/J oxide diffusing through the skin. w - --' .4 Cutaneous gas exchange would be 0 � �- most effective if only deoxygenated -0: � --':;) blood flowed to the skin, in the same :::!o way that only deoxygenated blood �I ,3 r-- 00: - flows to the' lungs in mammals, The WW �e.. partial pressure differentials across the :;)� (/J<{ r-- skin of both oxygen and carbon diox zo: OC) ,2 ide would be largest in this circum Uo: stance. The skin of most vertebrates, ZW we.. however, is no differentfrom any other C) >- ,1 living tissue: it receives blood only � from the major systemic arteries, which typically deliver oxygenated blood, Because the difference between .0 the oxygen partial pressure of oxygen 2 3 4 5 6 EXPERIMENTAL TRIAL ated blood and that of the respiratory medium is often rather small, oxygen uptake from the environment is nor mally limited by the very blood the 12 skin cells need to live, Even under this seemingly major constraint the skin 0: W may nonetheless be important in car I- w 10 bon dioxide elimination because car � :::; bon dioxide levels in arterial blood --' may still be considerably greater than � 0: 8 they are in the environment. This w explains in part why carbon diox e.. UNSTIRRED WATER (/J ide elimination typically exceeds oxy w (( gen consumption in cutaneous gas ex <{ --' 6 change among vertebrates, --' c:: Some vertebrates are indeed able to <{ () e UNSTIRRED WATER direct a fraction of their deoxygenated z w 4 • STIRRED WATER blood into the systemic arteries and e.. thereby augment cutaneous gas ex 0 change, Amphibians and reptiles, for example, have an incompletely divid .2 2 3 4 5 6 7 ed heart that allows deoxygenated STIRRED WATER EXPERIMENTAL TRIAL blood to flowto the skin without first

traversing the lungs, Comparative SKIN VENTILATION affects cutaneous gas exchange. A frog, immobilized in a wire anatomists have traditionally regard mesh envelope, was immersed in a water-filled chamber so that only its nostrils were above ed this arrangement as a primitive and the surface (top left). The skin could be ventilated by actuating a magnetic stirrer at the bot inefficient one, Kjell Johansen of the tom of the chamber. Cutaneous oxygen uptake could be monitored by measuring the de University of Aarhus in Denmark, crease in concentration of oxygen in the chamber. (A surface layer of mineral oil prevented Fred White of the Scripps Institution aeration of the water.) Cutaneous oxygen exchange (top right) was greater when the water was stirred (gray bars) than when the water was left still (colored bars). The reduction in of Oceanography and others have sug oxygen consumption when the water was still was shown not to result from a decrease in gested that the opposite is true. They capillary blood flow. A frog's leg was led through the side of the container so that the capil argue that the heart structure of am laries in the web of the foot could be seen under a microscope. The number of blood-filled phibians and reptiles is actually an im capillaries that intersected a line in the microscope's eyepiece was counted while the water portant adaptation that allows these was stirred and while it was left still (bottom left). In the absence of stirring, and thus of vertebrates to distribute blood where skin ventilation, the number of blood-perfused capillaries actually increased (bottom right).

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© 1985 SCIENTIFIC AMERICAN, INC (/"----- SYSTEMIC CIRCUIT-----�\ artery. The sphincters may act as valves that shunt blood flow one way (/"----GAS -EXCHANGE CIRC UIT ----�\ or the other. In any case the exact dis r------�--�----,,--� tribution depends on the level of oxy gen and carbon dioxide prevailing at these two respiratory organs. Working with Nigel West of the University of Saskatchewan, we meas ured the distribution of pulmocutane ous blood between the skin and the lungs by implanting electromagnetic flow transducers aroun-d the pulmo nary and cutaneous arteries of anes thetized toads. When we simulated the oxygen and carbon dioxide partial 1 1 pressures typically found in the lungs of toads holding their breath, the toads diverted blood from the lungs to the skin. This response facilitates cutane ous gas exchange. Such a reaction must also be re lied on by frogs whenever pulmonary /' PULMOCUTANEOUS . breathing is hindered, as it is when a ARTERIES frog is underwater. Recently Robert Boutilier, Mogens Glass and Norbert Heisler of the Max Planck Institute in PULMONARY Gottingen conducted a series of exper VEINS iments similar to ours on intact, un anesthetized bullfrogs. They injected microscopic radioactive spheres into the bullfrogs' circulatory systems. The spheres, which were slightly larg er than red blood cells, lodged in capil laries through which blood flowed. The distribution of blood flowbetween VENTRICLE the lungs, skin and other body tissues could then be calculated from the radioactive emissions of the various � body tissues exposed by dissection. When frogs dived in oxygenated wa ter after breathing gas mixtures low in oxygen, pulmocutaneous blood was AIR LOW O,lHIGH CO, AIR preferentially distributed to the skin rather than to the lungs. Conversely, when frogs with air-filledlungs were submerged in water containing little W f oxygen, pulmocutaneous blood was :J 2 �� distributed from the skin to the lungs. 0::2: o Clearly amphibians can regulate cu -'a: LLW taneous blood flow both to optimize -'CL �Ul cutaneous gas exchange and to coor a:a: Ww dinate the respiratory activity of the f-f a: 20 skin with that of the lungs. « :::! -' -' � o Although skin breathing may ac n count for only a small compo nent of total gas exchange in certain AMPHIBIAN CIRCULATORY SYSTEM, diagrammed here, allows deoxygenated blood animals, in others it can play a major (blue) to reach the skin and thereby promotes the diffusion of oxygen through the skin and into the blood. Most of the deoxygenated blood delivered to the skin comes from the heart if not vital role. The sheer diversity of by way of the cutaneous arteries (top); a small quantity is mixed into oxygenated blood (red) species that resort at least in part to in the ventricle of the heart and is transported by the systemic arteries to the skin. (Some cutaneous gas exchange should be oxygenated blood also finds its way into the pulmocutaneous arteries.) In spite of the fact sufficient to convince one that skin that a single ventricle pumps both oxygenated and deoxygenated blood into the arteries, a breathing is commonplace rather than segregation of blood is maintained: primarily oxygenated blood is routed to the systemic exceptional in vertebrates. Through circuit and primarily deoxygenated blood is routed to the gas-exchange circuit. Part of the closer investigation cutaneous gas ex primarily deoxygenated blood in the pUlmocutaneous arteries can then be shunted to either change has emerged as a well-regulat the lungs or the skin, depending on which organ is better suited for respiration at the time. ed, energetically inexpensive process Electromagnetic cuffs measuring the blood flow within the cutaneous and pulmonary arter ies recorded (bottom) the decrease in pulmonary arterial flow and the increase in cutaneous that can respond to immediate, pro arterial flow when the lungs were flushed with gas rich in carbon dioxide and poor in oxy longed and evolutionary changes in an gen. Muscular sphincters around the arteries may act as valves and so regulate the flow. animal's respiratory requirements.

142 © 1985 SCIENTIFIC AMERICAN, INC The butterfly and the74 7. Near Los Angeles International Airport, where 74 7's reach for the sky, one of the smallest endan gered species in the world reaches for its dinner. The El Segundo Blue lives on wild buckwheat ...on land that's part of an oil refinery. The people who work thereprotect the area and plant buckwheat yearin, year out. Now, for a creature little bigger than your fingernail, some of the danger of being endangered is past. Do people really care that much for a tenth of a gram of beauty? People Do.

Chevron ===

fur more information write:People Do-B, p. o. Box 7753, San Francisco, Calif. 94120