and Toads in Deserts seem unlikely desert denizens. But those living in dry climes reveal a diverse and unusual array of adaptations to life at the extremes

by Lon L. McClanahan, Rodolfo Ruibal and Vaughan H. Shoemaker

ith their moist skin and aquat- smooth skins are called frogs. Most than can other vertebrates, are jeopar- ic tendencies, frogs and toads amphibians lay their eggs in water and dized in this situation. W seem best suited to life in or have larvae that lead a Þshlike exis- Amphibians also diÝer from other near bodies of water. Yet these crea- tence until they undergo metamorpho- vertebrates in the way they excrete tures are found in arid regions through- sis. Once equipped with legs and lungs, wastes. The kidneys of desert out the worldÑfrom the Colorado Des- they spend at least some time on land. are challenged to conserve water while ert in California to African savannas. Despite the ability to survive on terra eliminating the nitrogen waste pro- To survive in such climates, they have Þrma, most amphibians inhabit sites duced during the metabolism of pro- developed behavioral and physiological near fresh water or areas of elevated tein and other nitrogen-containing mechanisms that allow them to con- humidity and rainfall. Relatively few compounds. Birds and reptiles have serve water and remain cool. live in arid regions. This geographic dis- solved this problem by synthesizing The range of adaptations that we and tribution reßects the physiology of am- uric acid, a poorly soluble, nitrogen- other researchers have observed chal- phibians: they are generally ill suited to rich compound. This waste can be ex- lenges some of the classical views of face the rigors of the desert. creted as a solid precipitate, and little anuran, or and toad, physiology. Other terrestrial vertebrates, includ- water is lost. Mammals incorporate their Most of our previous knowledge was ing reptiles, birds and mammals, have based on temperate species. The study an integument, or skin, that can pro- of desert-dwelling amphibians has of- tect them against desiccation. The out- fered insights into the remarkable di- er part, known as the stratum corne- versity of these animals. um, is composed of multiple layers of Some 300 million years ago amphib- ßattened, dead epidermal cells. This ians were the Þrst vertebrates to invade skin deters water loss. Unlike these the land, and they maintain a strong other vertebrates, amphibians typically connection to fresh water. Modern am- have a stratum corneum consisting phibians include salamanders, caecil- only of a single-cell layer. This very per- iansÑlegless amphibians that resemble meable skin oÝers some beneÞts. Am- wormsÑand anurans. Contrary to most phibians do not drink but absorb water peopleÕs perception, no biological dis- across the skin from moist surfaces, tinction separates frogs and toads: ter- such as wet rocks or leaves, and soil as restrial anurans with warty skins are well as from pools. Oxygen and carbon usually called toads; aquatic forms with dioxide pass readily through the skin; for example, lungless salamanders rely on the integument for gas exchange. At the same time that it is ideally LON L. MCCLANAHAN, RODOLFO RUIBAL and VAUGHAN H. SHOEMAKER suited to absorb water, the thin amphib- have spent more than 20 years studying ian skin is a perfect conduit for evapo- desert frogs and toads. Their association ration. Under moderate conditions of began in 1965, when McClanahan was a temperature and humidity, most am- graduate student working with Ruibal at phibians cannot survive for more than the University of California, Riverside, a day in circulating air because they and Shoemaker arrived there as an as- quickly dehydrate. Even anurans, which sistant professor. The three of them can tolerate much larger water losses formed a lasting friendship that led to research ventures in North and South American deserts. In particular, they dis- covered bizarre adaptations TREE FROG Phyllomedusa sauvagei is in the unique habitat of the Gran Chaco in Argentina and Paraguay. Ruibal and one of several species of frog adapted Shoemaker are professors of biology at to arid regions. This South American Riverside; McClanahan is professor of anuran can survive in hot, dry environ- biology at the California State University ments because it tolerates high body at Fullerton and director of the universi- temperatures. It also conserves water tyÕs Ocean Studies Institute. by losing little liquid through its skin or from its excretory system.

82 SCIENTIFIC AMERICAN March 1994 Copyright 1994 Scientific American, Inc. waste nitrogen into urea, a water-solu- the skin and urinary bladder. Increased above 40 degrees C, the frogsÕ bodies ble molecule. They conserve precious permeability of the bladder permits the do not exceed 30 degrees C, because water by creating urine that has a high animals to restore water lost by evapo- they undergo evaporative cooling. H. concentration of dissolved materials, ration by reclaiming water stored as di- cadaverina can store up to 25 percent primarily urea and salts. This ability is lute urine. In addition, dehydrated frogs of its body weight in the form of dilute particularly well developed in desert and toads absorb water through the urine. As it loses water through evap- rodents. The kangaroo rat, for instance, skin much more readily than when they oration, water from urine is recycled produces urine that is 14 times as con- are hydrated. These responses are me- back into the body. When these re- centrated as blood; Australian desert diated by a posterior pituitary hormone serves are exhausted, the frogs return mice achieve ratios of 20 or more. called arginine vasotocin. to the seep and take in more water. Like mammals, adult anurans usually The seeps also provide a place for produce urea, but in contrast to mam- owever useful in the short term, mating and egg development. On sum- mals, they cannot make urine that is these protective measures do mer days the frogs remain in clumped more concentrated than blood. They H not permit anurans to survive masses near water holes. The reasons therefore require a great deal of water without water for a long time in hot, for clustering in this fashion are not to eliminate their waste. Most amphib- dry environments. Thus, frogs and clear. We think huddling may decrease ians are also less tolerant of high body toads in these regions have evolved ad- the amount of water lost by an individ- temperatures than are other terrestrial ditional strategies. Perhaps the most ual. As evening approaches, the frogs vertebrates. Birds, mammals and des- straightforward adaptation to life in slowly disperse and start to feed at the ert lizards can maintain body tempera- dry lands is to stay near what little wa- waterÕs edge in preparation for night, tures of about 40 degrees Celsius. But ter is available, and many species of when they chorus, mate and lay eggs in many frogs and toads die at tempera- amphibians do just that. Springs, seeps, the pond. If rain forms other pools, the tures of 35 degrees C or less. canyons that drain higher ground as frogs will spread out and lay eggs in Terrestrial frogs and toads share well as man-made impoundments are these waters as well. some characteristics that help to oÝset all permanent water sources where The red-spotted toad, Bufo puncta- the handicaps imposed by their perme- frogs can be found. tus, uses the canyon waters of the Col- able skin and ineÛcient kidneys. When The frog Hyla cadaverina, or the Cal- orado Desert for spawning. But unlike water is unavailable, these animals stop ifornia tree frog, found in the Colorado H. cadaverina, these toads do not per- producing urine and allow wastes to Desert, is one such oasis dweller. These manently reside in a moist environ- accumulate in the body ßuids. Dehydra- frogs live near seeps and water holes. ment. Using transmitters, we tracked tion also results in beneÞcial changes in Although air temperatures often soar toads that moved up to 100 meters

Copyright 1994 Scientific American, Inc. SCIENTIFIC AMERICAN March 1994 83 away from the water. Even in the mid- cies: at one site we found eight individ- tively cool during the day. Studies us- dle of a summer day, we discovered uals in the same cranny. ing implanted location and tempera- toads burrowed in the coarse soil of Because B. punctatus is unable to tol- ture sensors conÞrmed this theory. We rock crevices far from water. These erate temperatures higher than 35 de- tracked one toad from September, late crevices provide a shelter that is shared grees C, we presumed that the toads in the active season, until December, with other members of the same spe- seek microhabitats that remain rela- one of the colder months. At night dur-

Anuran Adaptations in Arid Regions

COLORADO DESERT Hyla cadaverina (top left) This frog lives near permanent water supplies in the desert. It can store up to 25 percent of its body weight as dilute urine. If it loses water through its skin, the frog can reabsorb water from the bladder.

Scaphiopus couchi (top center) This species of spadefoot toad in- habits areas of the desert where there are no year-round water sources. To survive the dry season, the toad buries itself as deep as one meter underground. Some spadefoots have survived two-year droughts in this manner.

Bufo punctatus (top right) This toad can travel 100 meters from water sources, looking for food. To stay cool, it finds rock crevices and, like H. cadaverina, re- cycles water from urine. The toad can tolerate losing 40 percent of its body water (in contrast, camels can survive a 20 percent depletion).

GRAN CHACO REGION laevis (bottom left) This toad survives dry periods by burrowing into mud and becoming entombed. It then constructs a multilayered cocoon (left side of panel) to resist water loss. At the beginning of the rainy season, the toad pulls the cocoon over its head and eats it (right side of panel). Afterward L. laevis emerges.

Phyllomedusa sauvagei (bottom right) This tree frog coats itself with a waxy substance to prevent water loss. It also excretes uric acid to conserve water. P. sauvagei is the only anuran known to drink wa- ter—most absorb it through their skin. It does so by letting drops roll into its nearly closed mouth.

84 SCIENTIFIC AMERICAN March 1994 Copyright 1994 Scientific American, Inc. ing the warm season, it traveled 85 me- time air temperatures routinely exceed- Habitat selection also proved vital when ters from its burrow to a small stream; ed the critical limits for the toad, but the toad became inactive in winter, early in the morning the toad returned its body temperature never rose above protecting it from cold nightly temper- to the same burrow. 31 degrees C. Reduced temperatures in atures. In December, when air tempera- The strategy is clearly successful. the burrow as well as evaporation con- tures ranged from 12 degrees C at sun- During the toadÕs active months, day- trolled the toadÕs body temperature. set to four degrees C at sunrise, the toadÕs body temperature inside the bur- row remained constant at 25 degrees C. Not only does B. punctatus choose NORTH AMERICA protective habitats, it possesses a char- acteristic that allows it to abandon its water source and forage for during hot summer nights. The toads can store 40 percent of their body weight as dilute urine. If all the bladder reserves are used, the toads have an- other safety feature: they can tolerate the loss of up to 40 percent of their body water. Humans can survive only a 10 percent loss of their body water; camels, 20 percent.

ost areas of the desert lack permanent water sources. Am- M phibians that live in such re- gions do not retreat to rocky crevices; they burrow underground. The soil protects anurans from the extreme sur- face heat during the dry season. They obtain water through the soil, and as the earth dries, they conserve water be- cause little is lost to evaporation. We Þrst studied the ecology of bur- rowing toads in southeastern Arizona. COLORADO DESERT Three species of Scaphiopus, or spade- foot toads, are abundant in this area and can easily be found after the sum- mer rains bring them out of the bur- SOUTH AMERICA row. Although some toads emerge dur- ing light rains, the majority come out during the evening of the Þrst heavy downpour, when temporary ponds form. We wondered what cues might trigger this exodus. We determined that gently and silently moistening the soil by pouring water on it did not elicit a response, whereas sprinkling the soil to imitate rain caused the animals to surface. The toads came out even when the ground was kept dry with plastic. Sound alone is a suÛcient cue. After they have left the burrow, adults make their way to the ponds to breed. Toads captured on the way often have GRAN CHACO a stomach full of termites that have si- multaneously emerged from their un- derground nests. Spadefoots have a prodigious appetite and can consume 55 percent of their body weight in a single night. One meal of lipid-rich ter- mites can provide enough energy to maintain a toad for more than a year; it may even be suÛcient to allow a fe- male to produce eggs. Once in the water, the toads usually stay about 24 hours, just long enough to mate and lay eggs. They then leave and sometimes travel miles to take up

Copyright 1994 Scientific American, Inc. SCIENTIFIC AMERICAN March 1994 85 screams loudly and bites when threat- Comparison ý PHYLLOMEDUSA SAUVAGEI ened. The is known as kururœ- of Nitrogen Excretion* chin’, or Òthe toad that shrieks,Ó in Guaran’, the language of Paraguay. ost amphibians, such as Unlike spadefoot toads, the kururœ- M the northern leopard frog, 3 GRAMS URIC ACID chin’ remain in ponds during times of excrete nitrogen as urea in so- drought. As water evaporates, they bur- lution, using ample water. Des- DESERT KANGAROO RAT row to a shallow depth and become en- ert-dwelling mammals use less tombed as the mud dries. The toads water to excrete the same then start to produce a multilayered amount of urea. Desert frogs, 2.1 GRAMS UREA cocoon. The kururœ-chin’ is not alone such as Phyllomedusa sauva- in this practice. Various other burrow- gei, resemble mammals in that NORTHERN LEOPARD FROG ing species in Australia, Africa and they use little water; they differ Mexico are known to form cocoonsÑ in that they excrete nitrogen indeed, it seems cocoon formation 0 12 36 60 84 108 132 156 180 waste as precipitated uric acid. 2.1 GRAMS UREA evolved independently several times. WATER (MILLILITERS) *per gram of nitrogen All anurans periodically shed the outermost cell layer of their skin after a replacement layer has been formed. residence in shallow burrows. On wind- body weight. The soil adjacent to the During cocoon formation, however, the less nights they forage on the still toads was also fairly moist, and the outermost layer of skin is not shed and damp desert ßoor. The toads return to forces binding water to soil were suÛ- stays in place as additional layers grow the burrow after feeding, reburying ciently weak, so that water could move beneath. Indeed, the kururœ-chin’ forms themselves in the friable soil. By late osmotically into the animal. a new layer every 24 hours until it is summer they disappear and are not In late June, just before the Þrst enclosed by a multilayered cocoon of seen until they unearth themselves the rains, the toads were still in excellent ßat cells with dried mucus between next summer. In parts of the Colorado condition but contained high concen- each layer. When plotted against time, Desert, one of the spadefoot toads, trations of urea in both plasma and evaporative water loss during cocoon Scaphiopus couchi, was found to sur- urine. By then the soil had dried so formation shows a hyperbolic decline vive for nearly two years without rain. much that water could not pass from as each layer forms. Fat reserves are suÛcient because the soil to animalÑunless there was enough In the laboratory the kururœ-chin’ will toad drastically lowers its metabolic buildup in the total solute concentra- construct a cocoon if it is deprived of rate during its retreat underground. tion in the toads to overcome the in- water and placed in a quiet, dark place. We considered whether spadefoot creased forces binding water to the soil. Time-lapse Þlming shows that the toad toads could regulate the composition moves only slightly as the cocoon thick- of their body ßuids while below ground. he accumulation of urea in the ens; after a few weeks, it remains mo- So before the rain came, we tried to lo- spadefootsÕ body ßuids tilts this tionless for days on end. But even when cate toads by digging near the dried- T exquisite osmotic balance. In lab- ensconced in its fully formed cocoon, out ponds where they breed; we even oratory studies we have found that the the kururœ-chin’ retains its unnerving used a bulldozer to excavate a large toads can produce and store urea on ability to shriek when disturbed. If the area. We did not Þnd any toads. Fortu- demand. If they are placed in relatively toad is gently moistened with water, it nately, one of the local ranchers in- dry soil, they make more urea than will awaken and start to shed the co- formed us that he occasionally uncov- when they are in wetter soils. This same coon in one piece. The animal uses its ered toads when digging holes for strategy of storing urea is used by legs to roll the cocoon up from the pos- fence posts, some at the depth of near- frogs that can adapt to brackish water terior part of the body, over its head. ly one meter. Moreover, the burrowed (there are no truly marine frogs). In this The kururœ-chin’ then promptly eats creatures were surprisingly far, at 100 case, the accumulation of urea makes the entire wet casing. meters, from the vanished pond. the body ßuids more concentrated than Perhaps the most striking anuran Armed with this information, we those ßuids surrounding the animal, adaptation to life in the desert was dis- were able to Þnd some sites where bur- causing water to enter the creature by covered serendipitously. In 1970 we re- ied toads could be excavated and stud- osmosis. For the same reason, some ceived a surprising reprint from John ied. At a location in Arizona, we dug up marine Þshes such as sharks and coela- P. Loveridge of the University of Zim- toads at various times during the year. canths also retain elevated concentra- babwe (then Rhodesia). It described ex- We took samples of plasma and urine tions of urea in the body ßuids. periments showing that the gray tree and analyzed them for electrolytes, A bizarre burrowing toad from the frog, Chiromantis xerampelina, could urea and total solute concentration. In family has an even more survive for long periods in open, dry addition, we measured the volume of elaborate survival tactic than the spade- containers. The frog lost weight at a urine in the bladder and the moisture foot toad. Unlike spadefoots, these ani- fraction of the rate of other frogsÑ content of the soil at the burrow site. mals do not store high concentrations rates similar to those of a lizard kept We discovered that from the time the of urea in their body ßuids; they de- under identical conditions. Loveridge toads burrowed in September until we pend on a cocoon to prevent water also noted that most of the dry mass unearthed them in March the solute loss. These toads inhabit the Gran Cha- of the frogÕs urine was uric acid. concentration in plasma and urine was co, a semiarid region that extends from His Þndings were heretical. All frogs typical of fully hydrated anurans. Fur- north-central Argentina into Paraguay, and toads were thought to have water- thermore, in March most individuals where they live in temporary ponds permeable skinsÑwith the exception had retained a lot of dilute urine in that Þll up during the summer rains. of cocoon-forming burrowersÑand to their bladdersÑan amount equivalent One of the creatures, Lepidobatrachus excrete nitrogen as urea. LoveridgeÕs to between 25 and 50 percent of their laevis, is voracious and pugnacious. It description suggested a frog with a

86 SCIENTIFIC AMERICAN March 1994 Copyright 1994 Scientific American, Inc. COLOR CHANGE permits Chiromantis xerampelina to endure sunÕs rays. The frog also survives the heat by storing large direct sunlight. By abandoning its dark, protective coloring volumes of water in its bladder and then using the reserve (left) and adopting white (right), the tree frog reflects the for evaporative cooling. reptileÕs impermeable skin and a rep- large blob of semisolid urine while be- of the tree frogÕs adaptations. We re- tileÕs capacity to excrete uric acid. ing handled. A quick trip to the spec- measured the evaporative water loss in At the time the paper appeared, we trophotometer revealed that the major PhyllomedusaÑwith care and patience were beginning studies of amphibians component was uric acid. Studies of ni- this timeÑand found that Phyllomedu- in the Gran Chaco. We were impressed trogen balance in Phyllomedusa and sa, like Chiromantis, could reduce its with the diversity of the amphibian Chiromantis have amply conÞrmed the water loss to very low levels when it was fauna living in this region, which in- beneÞts of uric acid excretion. In both allowed to perch and behave normally. cluded a green arboreal frog, Phyllome- species, about 80 percent of the waste We had observed that the frog uses dusa sauvagei, known locally as rana nitrogen is emitted as uric acid or urate each foot in turn to wipe its entire body. verde. Whereas most frogs living in arid salts. In addition, sodium and potassi- After this ritual, rana verde looks as if regions must remain underground or um precipitate along with uric acid, it consisted of plastic. Water dripped near water, except during the rainy sea- which further increases the excretory onto the creatureÕs skin beads up, as it son, Phyllomedusa and Chiromantis can capacity of the kidneys. Thus, these does on a waxed surface. Histological remain perched in trees, where they frogs can feed while deprived of water studies revealed the presence in the feed. P. sauvagei is active before the on- for long periods. Across species, there skin of a novel form of gland, which set of summer rains in Paraguay, and appears to be a wide range in the abili- was interspersed between the mucous Chiromantis can be found during the ty to synthesize uric acid: from 230 glands and poison glands that are typi- dry season in Zimbabwe. Because of milligrams per kilogram per day in P. cally found in frogs. The glands are tiny LoveridgeÕs work, we made crude mea- sauvagei to only 40 milligrams per ki- and numerous, about 30 per square surements of water loss in P. sauva- logram per day in P. bicolor, which in- millimeter of skin; they stain intensely gei in the laboratory, but we observed habits tropical regions of Brazil. when treated with lipid-soluble dyes. nothing unusual. The ability to make and excrete uric It is now clear that the waterproofing A few weeks later one frog voided a acid turned out to be only one aspect process involves the synchronous dis-

WIPING ITS SKIN with each of its four legs, in turn, allows Once coated, the frog appears to be made of plastic. The pro- Phyllomedusa sauvagei to completely cover itself (left) with tective lipid is produced in tiny skin glands that are shown the waxy substance that it secretes to prevent water loss. magnified 150 times and dyed red in this micrograph (right).

Copyright 1994 Scientific American, Inc. SCIENTIFIC AMERICAN March 1994 87 charge of these glands, im- PHYLLOMEDUSA ed to any particular habitat. mediately followed by wiping. SAUVAGEI Some instances are clearly The coating, a rather heteroge- PHYLLOMEDUSA the result of human interven- neous mixture of lipids, is pri- PAILONA tion. Various places that were marily wax ester. Like Phyllo- PHYLLOMEDUSA once home to spadefoot toads medusa, insects and plants use IHERENGI in southern California are now a variety of waxes to retard wa- housing tracts. We have seen PHYLLOMEDUSA ter loss. Curiously, Chiroman- TRINITATUS widespread destruction of the tis does not have lipid glands. habitat of Phyllomedusa in the The mechanism by which it PHYLLOMEDUSA Gran Chaco, where trees are BICOLOR prevents evaporation remains cut for fuel. Air and water con- obscure. PACHYMEDUSA tamination, the introduction of DACNICOLOR predatory Þshes and even con- hyllomedusa and Chiro- AGALYCHNIS sumption of frog legs contrib- mantis are able to sur- ANNAE ute as well. In some cases, hu- vive in very hot environ- 0 50 100 150 200 250 300 mans encourage survival. The P MILLIGRAMS OF NITROGEN ments. They accomplish this PER KILOGRAM OF BODY WEIGHT PER DAY great abundance of spadefoot remarkable feat by controlling toads in southwestern Arizona their body temperature. Before URIC ACID EXCRETION UREA ACCUMULATION is probably the result of cattle the summer rains, the air may URIC ACID PRODUCTION varies greatly. Frogs in arid re- tanks constructed by ranchers exceed 40 degrees C. Body gions, such as P. sauvagei, convert 80 percent of their to catch runoÝ from thunder- temperatures of P. sauvagei nitrogen waste into semisolid uric acid, reducing the urea storms. Such facilities serve as were found to track air temper- in the blood and saving water. Tropical frogs, such as P. breeding sites. ature, except during the hot- bicolor, convert 20 percent. (Pachymedusa dacnicolor and Yet populations of anurans test parts of the hottest days. Agalychnis annae are closely related to Phyllomedusa.) have declined or disappeared At these times, the frogs re- in relatively undisturbed or mained about 40 degrees CÑtwo to the day. Chiromantis, however, can be protected places. Although a portion of four degrees cooler than the air and observed sitting in the full sun. Chiro- such events may represent natural ßuc- three to Þve degrees cooler than a ther- mantis minimizes the eÝects of solar tuation, concern grows that amphibian mometer constructed to match the size, radiation by undergoing a dramatic col- decline may indicate subtle environ- shape and absorptive characteristics of or change. It forsakes its gray or brown mental deterioration on a global scale. the frog. protective coloration and instead be- The complex life cycles and reproduc- The frogs achieve such thermoregu- comes white to reßect sunlight. tive specializations of amphibians may lation by controlling evaporation rates. We wondered if Phyllomedusa could make them doubly susceptible. Desert- Laboratory work has shown that the take advantage of the light rain that adapted species appear no better able frogs can match evaporative heat loss frequently precedes a heavy downpour. to withstand the eÝects of human ac- to increases in ambient heat over a wide Because its skin is waterproofed, the tivity than are their counterparts in wet range of temperatures, wind speeds and animal cannot absorb moisture that conditions. Even creatures that spend relative humidities. The mechanism ap- way. Therefore, we performed experi- most of the year underground must pears to be analogous to sweating. Mi- ments in which water was dripped on Þnd abundant food and suitable aquat- croscopic observation of the skin shows its head. Astonishingly, we observed ic breeding sites when they emerge. To periodic discharge from many of the Phyllomedusa lift its head to gulp drops prevent further extinctions, it is imper- gland ducts that dot the skin. We pre- of water. Experiments using water with ative that we understand the panoply sume but have not conclusively dem- dyes incapable of diÝusing through the of and limits to the devices that frogs onstrated that mucous glands are re- skin showed coloration in the esopha- and toads use to thrive in all habitats. sponsible. Pharmacological studies of gus, stomach and small intestineÑthe Chiromantis indicate the glands are water had clearly been ingested, not controlled by sympathetic nerves that absorbed. Phyllomedusa is the only FURTHER READING stimulate beta-adrenergic receptors. anuran known to drink. The regulation of body temperature BEHAVIOR AND THERMAL RELATIONS OF THE RBOREAL ROG HYLLOMEDUSA requires the most water during the dry he study of amphibians in des- A F P SAUVAGEI. Lon L. McClanahan and period, just before the summer rains. erts and semiarid regions has re- Vaughan H. Shoemaker in National Ge- The frogs obviate this problem because T vealed extensive and diverse spe- ographic Research, Vol. 3, No. 1, pages they can tolerate high body tempera- cializations for terrestrial existence. 11Ð21; Winter 1987. tures. On most days, there is no need The emerging picture of anuran physi- PHYSIOLOGICAL ECOLOGY OF AMPHIB- to evaporate water for thermoregula- ology deÞes the stereotype based on IANS IN ARID ENVIRONMENTS. Vaughan tion; on very warm days, thermoregu- earlier studies of temperate species. H. Shoemaker in Journal of Arid Envi- lation is required for a few hours. Similarly, amphibians in other habitats ronments, No. 14, Vol. 2, pages 145Ð 153; March 1988. Like other frogs, Phyllomedusa and have other capabilitiesÑsuch as toler- EXCHANGE OF WATER, IONS, AND RESPI- Chiromantis can store large volumes of ance to freezingÑthat were unknown RATORY GASES IN TERRESTRIAL AMPHIB- water in the bladder and use it to oÝ- until recently [see ÒFrozen and Alive,Ó IANS. Vaughan H. Shoemaker, with set loss through evaporation. When by Kenneth B. Storey and Janet M. Sto- Stanley S. Hillman, Stanley D. Hillyard, bladder reserves are exhausted, the rey; SCIENTIFIC AMERICAN, December Donald C. Jackson, Lon L. McClanahan, frogs allow body temperatures to reach 1990]. Despite this diversity, or per- Philip C. Withers and Mark L. Wygoda even higher levels, thereby reducing the haps because of it, there is evidence in Environmental Physiology of the Am- need for evaporative cooling. Phyllome- of a worldwide reduction in some am- phibians. Edited by Martin E. Feder and Warren W. Burggren. University of Chi- dusa appears to remain shaded while phibian populations and the extinction cago Press, 1992. perched in trees, at least for most of of others. The decline is not restrict-

88 SCIENTIFIC AMERICAN March 1994 Copyright 1994 Scientific American, Inc.