Amphibian Temperature Regulation Studies in the Field and Laboratory

Transcription

1 AMER. ZOOL., 19: (1979). Amphibian Temperature Regulation Studies in the Field and Laboratory BAYARD H. BRATTSTROM Department of Biology, California State University, Fullerton, California, SYNOPSIS. Studies on thermoregulation in the laboratory and field have come a long way from the early work done between 1940 and While some physiological studies on amphibians have progressed at the same rate as those on reptiles, field studies have been far behind. Laboratory studies have largely delt with thermal acclimation, evaporative water loss, and thermal and moisture gradient behavior. Field studies, following early summaries of body temperatures of field animals, have stressed behavioral thermoregulation; yet, detailed studies on behavioral thermoregulation in amphibians have been completed for only a handful of species. A few studies have placed behavioral and physiological thermoregulation into an ecological or energetic framework; these studies are reviewed, and suggestions are made for future work. INTRODUCTION The study of temperature regulation in amphibians is complicated by the requirement of amphibians to maintain a moist skin or to occur in an aquatic environment. Numerous studies have dealt with problems of amphibians in maintaining body water, avoiding dehydration and adaptations of anurans to the desert (Seymour and Lee, 1974; McClanahan, 1975; Shoemaker and McClanahan, 1975). While these studies have been concerned with water conservation, they are intimately tied to problems of temperature regulation. In an amphibian involved in avoiding dehydration, these responses may take precedence over thermoregulatory ones (Tracy, 1975). Thermoregulation may be compromised by demands of hydroregulation, while in other situations, thermoregulatory demands may predominate. The amphibian's integument also functions in osmoregulation and respiration (Houston, 1971; Wakeman and Ultsch, I thank Dr. W. W. Reynolds for organizing, and inviting me to this symposium. Page charges for publication of this paper were supported by N.S.F. grant No. PCM to W. W. Reynolds. The figures were prepared by Mark Zolle supported by a grant from the Department of Biology, California State University, Fullerton. I wish to thank Mark for his drawing and W. W. Reynolds, Victor Hutchison, and Lon McClanahan for comments and remarks on the manuscript. 1975; Mullen and Alvarado, 1976; Walters and Greenwald, 1977). These processes are, of course, intimately tied to the problems of osmo- and thermoregulation (Reves, 1977). While I argued some years back, "Pity the poor frog, nobody studies his physiology," I would now suggest that the situation, "Pity the poor frog, his behavioral and physiological problems are so complicated and interrelated, it is amazing that we can understand them and that he is alive at all!!" Since I have recently reviewed temperature regulation in amphibians (Brattstrom, 1970a), I propose here to update the field to expose some problems in our approach, and to suggest some directions for future research. BEHAVIORAL THERMOREGULATION IN THE FIELD In a review of body temperatures of amphibians, I confirmed the old notion that many amphibians are poor thermoregulators (Brattstrom, 1963). For many of these species, water conservation, or restriction to aquatic environments, forces them into an essentially non-thermoregulatpry mode (Fig. 1). The best some aquatic amphibians may be able to do is to seek out warmer or cooler portions of their environment. This thermoregulation behavior may push them into environments which conflict with their respiratory and osmoregulatory demands {e.g., a warm area of a 345

2 346 BAYARD H. BRATTSTROM pond that is low in oxygen) (Houston, 1971; Wakeman and Ultsch, 1975; Mullen and Alvarado, 1976; Reves, 1977; Shoemaker and Nagy, 1977). Many other amphibians, however, have been shown to be fairly active thermoregulators, interplaying water economy and thermoregulation to allow them to be more active longer. This presumably allows time for more feeding, reproduction, and growth (Lillywhiteetal., 1973). In my initial review of amphibian body temperatures, I presented data on several species of frogs (especially Rana cascadae, pipiens, and clamitans) observed basking in the sun (Fig. 1), in water or on moist soil (Brattstrom, 1963). These frogs behaved like typical heliothermic lizards, with body temperatures above ambient. The frogs were apparently utilizing evaporative water loss to maintain body temperatures below lethal levels. Later, Lillywhite (1970, 197 la, 1974) who monitored body temperatures by telemetry, demonstrated behavioral thermoregulation in Rana catesbeiana which included diurnal basking complete with posturing. Brattstrom (1970a) demonstrated that the basking Australian hylid frog, Hyla(=Litoria) caerulea, could maintain a fairly constant body temperature by evaporative cooling under forced basking, even when the heat load was increased. The frog apparently could regulate the amount of water passing through its skin, as a function of heat load. Another Australian hylid, Hyla Moris, could not do this. Basking anurans use a variety of mechanisms (skin sculpturing, water movements over the skin, mucous secretions, activity, and cranial co-ossification) to reduce or facilitate evaporative water loss and cutaneous gas exchange during thermoregulatory basking (Lillywhite, 19716; Heatwole and Newby, 1972; Christensen, 1974; Lillywhite and Licht, 1974, 1975; Sievertetal., 1974). Lillywhite (1975) showed the important role of blood circulation in maintaining levels of skin hydration during basking. As long as water can enter the frog and be effectively evaporated from the skin (thus precluding desiccation), many anurans, especially Rana catesbeiana, can maintain fairly constant body temperatures. Tracy (1976) suggests that such basking plays less of a role in the behavioral thermoregulation of adult Rana pipiens and that behavioral thermoregulation in this species is poor; and his field data and computer simulations indicate that the body temperatures of this species are always near ambient. Evaporative water loss is apparently too high for effective basking thermoregulation especially at high radiant levels, low relative humidities, high air temperatures, and high wind speeds. Tracy (1975) also showed that a bullfrog, Rana catesbeiana, placed in the sun in a cage, maintained its body temperature within 4 C. He argues that this was not thermoregulation as the frog was passive and not shuttling (as it couldn't do). But, he noted, by noon it became dehydrated and stopped producing urine. I suggest that perhaps the frog was maintaining its body temperature fairly constant by physiological thermoregulation (evaporative cooling), as it was restrained from doing any behavioral thermoregulation. Basking has only been reported for a few other amphibian species. Valdivieso and Tamsitt(1974) showed that the montane Colombian frog, Hyla labialis, is a thermophilic heliotherm whose body temperatures are usually higher than ambient due to basking or absorbing solar radiation that filters through clouds. Adults and subadults were active in the morning and early afternoon. Terrestrial juveniles were active at all hours, but were most active at night. This is in contrast to observations on toads (Seymour, 1972; Lillywhite et al., 1973) in which the juveniles often have higher body temperatures than adults, and spend considerable time basking. Seymour (1972) suggests that the young of the desert toad, Bufo debilis, utilize basking thermoregulation for rapid feeding, accelerated digestion, and rapid deposition of fat prior to winter dormancy. Lillywhite et al. (1973) showed that youngb. boreas basked, except when food was withheld. Orientation to a heat source could be elicited in starving animals by feeding them, suggesting that one advantage of such behavior is acceleration of the digestive processes. Growth studies at a variety of temperatures indi-

3 AMPHIBIAN THERMOREGULATION 347 cated that energy ingestion, linear growth, weight increase and gross conversion efficiencies were all maximal at 27 C and were nearly identical to that of toads allowed to thermoregulate in a photothermal gradient (25.6 ). Diurnal behavior of small toads and of tadpoles, compared with the more nocturnal adults, may have evolved to maximize growth rates of younger individuals, shortening the time to adult size (Brattstrom and Warren, 1953; Brattstrom, 1962). While Bufo boreas, and most amphibians, bask only on wet soil, Lilly white et al., (1973) observed some toads basking on dry soil. Perhaps the water storage ability of B. boreas allows it to bask on dry soil, and then move to wet soil or water to replenish water loss. Several species of Australian hylid and leptodactylid frogs bask (Johnson, 1970, I97la,b). These include montane rapidstream-dwelling frogs, diurnal tropical frogs, and semi-desert diurnal and nocturnal frogs. The diversity of frogs that utilize basking suggests that it may occur in different species for different reasons and that the mechanisms of reducing the problems of dehydration and cutaneous gaseous exchange may be different. Seymour and Lee (1974) have suggested that such xeric Australian frogs as Hyla(=Litoria) rubella and caerulea may solve water and thermoregulatory problems by excreting urates, as in other xeric frogs (Loveridge, 1970; McClanahan, 1975; Shoemaker and McClanahan, 1973; Shoemaker and McClanahan, 1975; Blaylock et al., 1976; Drewes et al., 1977). The tacky and moist-looking skin of many hylid frogs from different deserts (such as H. caerulea from Australia, Phyllomedusa spp. in the New World) elicits speculation as to its function. The arboreal, desert-dwelling Argentinian P. sauvagei, not only has utilized certain aspects of nitrogen excretion and osmoregulation to survive in the desert (Shoemaker and McClanahan, 1975), but also uses evaporative cooling in a subtle manner. The skin of this frog is hydrophobic and contains numerous alveolar glands containing lipids (Blaylock et al., 1976). Secretion of lipids onto the integument is followed by a complex wiping movement which spreads the secretion over the body of the frog. The frogs then remain motionless. This lipid material reduces evaporative water loss up to 30 C, above which evaporative water loss begins to increase and then increases precipitously between 35 and 40 C. At 40 ambient temperatures, skin and core temperatures of the frogs remained at C. Small increases in water loss resulted in depressions of surface temperature corresponding to the release of clear fluid onto the skin surface (McClanahan et al., 1978). This frog thus uses a skin-surface-protective device to reduce water loss while living in the desert, yet as ambient temperatures rise and the possibility of thermal death approaches, the protective nature of this substance breaks down and the skin becomes available for evaporative cooling to maintain body temperatures below lethal levels. BEHAVIORAL THERMOREGULATION STUDIES IN THE LABORATORY Studies on behavioral thermoregulation of adult amphibians in the laboratory have been concerned largely with the role of evaporative water loss and the behavior of amphibians in thermal gradients. Thermal gradients are difficult to set up for amphibians because of the necessity to avoid dehydration to the animals. It is also difficult to determine whether an animal is responding to a thermal or a moisture gradient. Spotila (1972) in a study of plethodontid salamanders in thermal and relative-humidity gradients, comparing gradient studies with field studies, indicated that these salamanders do avoid extremes and exhibit thermal preferenda, which.were species-specific and not significantly affected by acclimation temperature or photoperiod. Dehydration was greater at higher temperatures, and in apparent compensation, the salamanders selected the highest relative humidity in the gradient (Spotila, 1972). Thus, the salamanders seem to be interplaying thermal and moisture responses.

4 348 BAYARD H. BRATTSTROM Feder and Pough (1975) studied temperature selection in red-backed salamanders, Plethodon cinereus. Animals acclimated to low temperatures selected high temperatures in the gradient, and those acclimated to high temperatures selected lower temperatures; acclimation of temperature selection was faster than acclimation of critical thermal maxima. This suggests that after exposure to, for example, low temperatures, there is value or at least a behavioral response of a salamander to seek warmer areas. This would facilitate rapid feeding and digestion following a period of cold weather and possible starvation. Hutchison and Hill (1978) showed that preferred temperatures of bullfrog (R. catesbeiana) tadpoles varies in a complicated manner with stage of development and thermal acclimation. While the mean T b was 20.7 and the modal T b 21.0 C, there was a tendency for earlier stages, acclimated at lower temperatures, to select lower preferred temperatures. At later stages, and especially with tadpoles acclimated to high temperatures, there was a preference for higher temperatures. This latter response may be associated with the high temperatures selected near metamorphosis, and high temperatures tolerated by recently metamorphosed juveniles. Hutchison and Hill (1978) further suggest that for those species with plasticity of their preferred temperatures, with changes in acclimation temperatures, survival is enhanced by avoidance of lethal temperatures, and energetic efficiencies are maximized through maintenance of body temperatures at or near physiological and biochemical optima. Plasticity is thus one strategy for circumventing serious consequences of rapid temperature change or thermokinetic extremes. One problem with thermal gradients constructed for aquatic organisms is vertical thermal stratification. Reynolds and Casterlin (1976), Reynolds (1977) and Casterlin and Reynolds (1977, 1978) have solved this problem by use of a device which allows an animal to control water temperature. The animal controls its own body temperature by its movements between chambers of water monitored by photocells and associated circuitry which controls heating and cooling equipment. Thus by its own behavior an animal can seek out its preferred temperature by manipulating the temperature of the water until it reaches its preferendum. In a study of R. pipiens tadpoles, Casterlin and Reynolds (1978) showed that while the tadpoles had a bimodal aspect of temperature regulation (with highs during day and again at night and lows during dusk transitions), the preferred temperatures and modal preferenda were between 27 and 28 C. These data are similar to results from typical thermal gradients (Lucas and Reynolds, 1976) and adult modal field body temperatures (Brattstrom, 1963). It seems to me that the development of effective thermal gradients or use of shuttleboxes will provide an opportunity for critical studies on the roles of photoperiod, acclimation, and energy metabolism on behavioral thermoregulation. The shuttlebox device (Reynolds, 1977) also may be adaptable to studying simultaneous responses to several factors (i.e.., choices between high temperature-high oxygen water vs. high temperature-low oxygen water against a choice of low temperatures and different oxygen levels). Some of the studies of Lilly white et al. (1973) on B. boreas juveniles were carried out in a laboratory photothermal gradient. Behavior of these toadlets differed under different soil and starvation conditions. Since it is also clear that acclimation and photoperiod may affect some amphibians, it may be important to mention here that length of time that animals are exposed to the gradient (number of hours or days in the gradient), the number of animals used at any one time, acclimation influences, gradient size, shape, and thermal consistency, and desiccation levels may also affect responses of animals to a gradient, so caution should be taken in construction, experimental design, and data interpretation of thermal gradient studies. PHYSIOLOGICAL THERMOREGULATION STUDIES IN THE LABORATORY Most laboratory studies on amphibians

5 AMPHIBIAN THERMOREGULATION 349 haye dealt with physiological aspects other than thermoregulation. Considering the kinds of studies that have been done on reptiles, it is surprising to find so few studies on amphibian thermoregulation. In heating and cooling studies on the bullfrog,/?, catesbeiana, (Tripp and Lustick, 1974) in water and air, there was no difference in heating and cooling of frogs in water, but there was in air. Heart rates were higher during heating than during cooling in water, while there was no difference in heart rates during heating and cooling in air. The majority of physiological studies in amphibians have understandably been metabolic studies on the relationship of metabolism to gas exchange, surface area, and habitat. Most of these studies were done at a variety of temperatures, and thus contribute to our understanding of the physiology of amphibians and the relative importance of behavioral and physiological thermoregulation to enhance or curtail certain aspects of the animals' physiology (see the following papers for current physiological and environmental approaches to old problems; Clausen, 1973; Bennett and Wake, 1974; Guttman, 1974; Turney and Hutchison, 1974; Heath, 1976; Pitkin, 1977; Weathers and Snyder, 1977). In addition, the interplay between these responses sometimes provides solutions to, or problems for, other physiological responses of the animal. Recent studies have made us aware of the increasing importance of the role of anaerobic respiration in stress activity and in normal behavior. Guttman (1974), for example, has shown that the toad, B. valliceps, can stand anoxia longer than B. woodhousei. He suggests that this allows B. valhceps to endure its longer winter dormancy better than B. woodhousei (also see Armentrout and Rose, 1971). Turney and Hutchison (1974) have shown in R. pipiens that of stressed energy, 69 and 73% was supported anaerobically at 25 and at 15 C, respectively. They suggest that the inefficiency of the breathing cycle of this frog, coupled with limitations of the respiratory surface and separate gas exchange pathways, have placed extreme restrictions on the capacity of the frog to meet oxygen demands, thus forcing the animal to incur a relatively large oxygen debt during maximal activity. Other studies with anaerobic respiration (Bennett and Licht, 1973, 1974; Seymour, 1973; Bennett, 1978) suggest that slow-moving amphibians such as B. boreas produce small amounts of lactate and do not exhaust. In contrast, fast-moving jumping forms such as R. pipiens have high levels of lactate generation, but are unable to sustain maximal activity. Aquatic species rely largely on air-gulping during activity and show little anaerobiosis. The rate of lactate production is also directly correlated with predatory avoidance. Noxious-tasting, aggressive, or cryptically-colored amphibians have low anaerobic scopes for activity while others rely upon anaerobiosis for rapid flight (R. pipiens) or rapid avoidance behavior {Batrachoceps attenuatus). In fact, rapid activity in amphibians appears to be possible only at the expense of extensive anaerobiosis (Bennett, 1978). In my opinion, two important lines of research are developing from these studies. First, is the question of how the enzymes and enzymatic pathways that are involved in aerobic and anaerobic respiration (Bennett, 1974, 1978; Baldwin et al., 1977) respond to the thermoregulatory demands of the animal and whether the same enzymes and pathways are used at all temperatures. Many organisms, including amphibians, compensate aspects of their metabolism so that they are more efficient at specific temperatures than would be predicted otherwise. The studies on such compensation mechanisms in amphibians have largely been restricted to adaptations by amphibian larvae, especially in embryonic temperature adaptations in northern and alpine frogs (Licht, 1971; McLaren and Cooley, 1972; Packard, 1972; Brown, 1975; Kuramoto, 1975a,b). A perhaps equally important aspect of metabolic compensation is that shown by high elevation populations of adult salamanders (Fitzpatrick and Brown, 1975) and anurans (Packard and Bahr, 1969; Packard, 1971, 1972) though in recent studies on Pseudacris triseriata, the compensation may not be in oxygen con-

6 350 BAYARD H. BRATTSTROM sumption but in differences in breeding seasons, and activity times (Packard, 1971). A considerable body of literature on amphibian physiology has been concerned with thermal resistances and the effect of thermal histories on thermal tolerances. Studies on the rate and range of thermal acclimation have provided us with information on the physiological plasticity of amphibians, and on genetic limits on thermal tolerances. These data have also been shown to have zoogeographic implication (see reviews in Brattstrom, 1970a, b). Recent studies have extended these ideas {e.g., Pough and Wilson, 1970; Farrell, 1971; Fitzpatrick et al., 1971; Holzman and McManus, 1973; Pough, 1974; Burke and Pough, 1976; Feder, 1978; Hoppe, 1978). Importantly, others are looking at acclimation effects on tissues (Shertzer etal., 1975; Lascano et al., 1976; Lagerspetz, I977a,b; Ballantyne and George, 1978) and blood parameters (Weathers, 1975, 1976). Interestingly, Ballantyne and George (1978) have shown that acclimation to cold (from 21 to 5 C over one month) in R. pipiens can raise muscle mitochondrial content. Whether this is an adaptation for dormancy is unknown, but worthy of continued study. These studies hopefully will contribute to our understanding of the physiology of the amphibian in solving its simultaneous problems of temperature, water, gas, and ionic regulation (Fig. 1). They are already giving us a clue to the basis for the marked seasonal differences seen in some amphibians. Lagerspetz, (19776), for example has shown that there is a temperature and seasonal effect on CNS activity mediated by the thyroid via the autonomic nerves. These seasonal differences may be important for spring reproductive effort and winter survival. PHYSIOLOGICAL STUDIES ON TEMPERATURE REGULATION IN THE FIELD Body temperatures taken of amphibians in the field are important, but this is not studying thermoregulation. As pointed out by Heath (1964, 1965) these data describe only the limits and possible preferenda of the animals. Studying thermoregulation involves monitoring behavior at the same time as body temperature (i.e.., watching for emergence, and then recording body temperature of emerging animals). Of all the field body temperatures recorded (Brattstrom, 1963, 1970a; Lillywhite et al., 1973), behavioral thermoregulation was sufficiently documented for only a few species (B. boreas, Acris crepitans, H. regilla, R. catesbeiana, Taricha rivularis). A more effective way to study this type of thermoregulation is by the use of telemetry. Lillywhite (1970, 1971a, 1974, 1975) has used this and other techniques to effectively study behavioral thermoregulation in the field and the lab. While body temperature is a function of environmental inputs and of physiological responses and interactions, in these studies body temperature was usually the only physiological parameter measured. It is important to measure several physiological parameters of amphibians simultaneously with modified technology and with patience. One area of field investigations not yet touched with amphibians is the construction of time/activity budgets in the field. This will be an essential step in the construction of time/activity/energy budgets and in appreciating the role played by amphibians in total community energy budget. This will be a difficult task due to the secretiveness and nocturnality of many amphibians and will require patience since many amphibians spend a lot of time being inactive. Yet, this may be an important part of energy conservation in amphibians. ENERGY METABOLISM AND ENERGY BUDGETS Considerable interest has developed recently on the relative roles of energy production in amphibians (Hutchison et al., 1977; Bennett, 1978). We now have studies on energy metabolism in amphibians involving size, season, fat deposition and > FIG. 1. Diagrams of body-environment interactions of three types of amphibians. Above, a basking (heliothermic) anuran (partly after Pough, 1974; Tracy, 1975, 1976). Middle, a cryptic salamander or largely nocturnal anuran. Below, an aquatic amphibian; (larval or adult).

7 AMPHIBIAN THERMOREGULATION 351 'particular DIURNAL AND BASKING AMPHIBIAN CONVECTIVE HEAT LOSS THERMAL RADIATION FROM ATMOSPHERE SCATTERED AND REFLECTED SUNLIGHT WATER LOSS THERMAL RADIATION TO ENVIRONMENT EVAPORATIVE HEAT LOSS HEAT CONDUCTION TO OR FROM GROUND THERMAL RADIATION TO ENVIRONMENT WATER INPUT FROM SOIL CONVECTIVE HEAT GAIN AND LOSS GASEOUS EXCHANGE THERMAL RADIATION FROM VEGETATION THERMAL RADIATION FROM GROUND WATER INPUT FROM SOIL SECRETIVE OR NOCTURNAL AMPHIBIAN EVAPORATIVE HEAT LOSS GASEOUS EXCHANGE HEAT CONDUCTION TO OR FROM GROUND AQUATIC AMPHIBIAN BEHAVIORAL RE8PONSE TO AND FROM WARM WATER GASEOUS EXCHANGE CONVECTIVE AND CONDUCTIVE HEAT TO AND FROM WATER

8 352 BAYARD H. BRATTSTROM utilization, and reproductive effort (Seymour, 1973; Seymour and Lee, 1974; Fitzpatrick and Atebara, 1974; Beckenback, 1975; Tracy, 1975, 1976; Feder, 1976). Recent studies on feeding behavior and digestion efficiencies have also contributed to our understanding of the energy utilization of amphibians (Lillywhite et al., 1973; Sternthal, 1974; Tracy, 1975; Smith, 1976). Fitzpatrick (1973) has studied energy budgets in the salamander Eurycea bislineata, and Smith (1976) has produced an energy budget (Fig. 2) for the toad/?, terrestris. Assuming a digestive assimilation efficiency of 74%, about half of that energy goes into metabolic costs and half into production. Of the latter, about half goes ENVIRONMENT = INGESTION into growth and half into reproductive effort (Fig. 2). The latter, of course, may be variously partitioned at different ages and seasons. Burton and Likens (1975) have determined that the energy flow through the salamander population in a New Hampshire forest is 11,000 KCal/ha/yr, equal to 0.02% of the net primary productivity and about 20% of the energy flow through birds and mammals in the forest. On the other hand, salamanders are 60% efficient in converting ingested energy into new tissue, and produce more new tissue annually than do bird populations. If we had some time/activity budgets for more amphibians, we could begin to develop time/activ C 74 7 C UNASSIMILATED ENERGY ASSIMILATED ENERGY 38 7 O 36 7 O METABOLIC COSTS o r. O-36 7o GROWTH PRODUCTION OF TISSUES I O-36 7 O REPRODUCTION 3O.6 7 O f LEAN DRY BIOMASS 54 7 n FAT ACCUMULATION FIG. 2. An energy budget for the toad, Buju ttrre\ln\ (modified after Smith, 1976).

9 AMPHIBIAN THERMOREGULATION 353 ity/energy budgets and begin to approach the problem of the cost of thermoregulation. While many workers have noted seasonal changes in "winter" and "summer" frogs (Brattstrom, 1970a), it has only been in light of renewed interest in energetics that new approaches to seasonal changes in metabolism have been made (Fitzpatrick, 1971; Harri, 1973; Harri and Talo, 1975a,b; Shertzer, et al., 1975; Weathers, 1975, 1976; Lagerspetz, 1977a,6). In terms of energy metabolism, and thus the costs for a variety of functions, it is also important to know how an amphibian may be partitioning the utilization of its energy with season. Thus Lillywhite et al. (1973) suggest that behavioral thermoregulation and energy partitioning in juvenile toads (B. boreas) maximize growth, and shorten the time to reach adult size. This is also apparently true for B. terrestris (Smith, 1976). In adults, energy is largely partitioned into reproductive effort (production of eggs and sperm, and cost of reproductive behavior). In addition, amphibians must also prepare for cold winters or long periods of dormancy underground (Seymour, 1973). Seasonal differences in metabolism of adult amphibians probably represent an interplay between energy utilization for reproduction and preparation for winter. Recent studies (Pasanen and Koskela, 1974; Koskela and Pasanen, 1975; Byrne and White, 1975) have demonstrated marked and interesting changes in liver and muscle glycogen, blood glucose, and body lipids. In R. catesbeiana lipid reserves become exhausted from the time of emergence through the breeding season (Byrne and White, 1975). Lipid reserves then increase prior to and into dormancy, while blood glucose levels rise during the breeding season and are lowest upon emergence from dormancy (Fig. 3). These may not be the same kind of changes seen in other amphibians (Reno etal., 1972; Seymour, 1973; Gehlbach etal., 1973), but the physiological strategies used are probably a function of the different seasonal activities employed by different amphibians. Depressed metabolism, fat deposition and utilization, and ability to endure anoxia (or have low oxygen demands) probably allow m t- z 3O I < ~ «LIVER BLOOD GLYCOGEN GLUCOSE ^ LIVER LIPIDS FAT BODIES V \T \ a * II It, 1 X t 1 > 1» / 1 t / 1 1 / 1 / / 1 1 / 1 1/.' «./-'" EMERGENCE BREEDING DORMANCY FIG. 3. Seasonal changes in lipid reserves, and blood glucose levels in the bullfrog, Rana catesbeiana (Simplified after Byrne and White, 1975). amphibians to survive harsh periods. At this time, thermoregulation and its costs are probably low. The costs and benefits of thermoregulation are highest during seasonal activity and help in growth, energy metabolism, and reproductive effort. Much more needs to be done; modeling efforts (Tracy, 1975) may be an important next step. SPECIAL ASPECTS AND PROBLEMS Some anurans prefer temperatures exceeding 30 C (e.g., H. Smithi, rubella, Phyllomedusa sauvagei; Brattstrom, 1970a,b; Johnson, 1970, 1971a,6; Seymour and Lee, 1974; McClanahan ««/., 1978). Interesting physiological processes may occur in frogs at high temperatures, (Stephenson, 1967; Harri and Talo, I975a,b) implying the necessity of measurements at >30 C. Kluger (1977) demonstrated that H. cinerea developed a fever (increase of 2 C.in body temperature) following injections of killed Gram-negative bacteria (Aeromonas hydrophila). Casterlin and Reynolds (1977) demonstrated a similar "behavioral fever" (significant mean increases in preferred temperature) in tadpoles of R. catesbeiana and R. pipiens, following similar injections with the same bacteria. These studies have implications both for understanding the

10 354 BAYARD H. BRATTSTROM adaptive advantage of fever in diseased frogs, and as a means of studying hypothalamic control of thermoregulation. I think we need a new look at the endocrinology of amphibians with respect to metabolism, energy demands and seasonal activities. This is especially true now that we know that season and temperature affect nervous and endocrine system activities (Lagerspetz, 1977<z, b). I have said little about thermoregulation in tropical amphibians, largely due to the dearth of studies. Tropical amphibians may be different. Selection pressures in the tropics may place higher demands on social behavior and reproductive modes than on physiology. REFERENCES Armentrout, D. and F. L. Rose Some physiological responses to anoxia in the Great Plains Toad, Bufo cognatus. Comp. Biochem. Physiol. 39A: Baldwin, J., G. Friedman, and H. Lillywhite Adaptation to temporary muscle anoxia in Anurans: Activities of glycolytic enzymes in muscles from species differing in their ability to produce lactate during exercise. Aust. J. Zool. 25: Ballantyne, J. S. and J. C. George An ultrastructural and histological analysis of cold acclimation in vertebrate skeletal muscle. J. Thermal Biol. 3: Beckenback, A Influence of body size and temperature on the critical oxygen tension of some plethodontid salamanders. Physiol. Zool. 48: Bennett, A. F Enzymatic correlates of activity metabolism in anuran amphibians. Amer. J. Physiol. 226: Bennett, A. F Activity metabolism of the lower vertebrates. Ann. Rev. Physiol. 400: Bennett, A. F. and P. Licht Relative contributions of anaerobic and aerobic energy production during activity in Amphibia. J. Comp. Physiol. 87: Bennett, A. F. and P. Licht Anaerobic metabolism during activity in amphibians. Comp. Biochem. Physiol. 48A: Bennett, A. F. and M. H. Wake. Metabolic correlates of activity in the Caecilian, Geotrypetes seraphini. Copeia 1974: Blayiock, L. A., R. Ruibal, and K. Platt-Aloia Skin structure and wiping behavior of phyllomedusine frogs. Copeia 1976: Brattstrom, B. H Thermal control of aggregation behavior in tadpoles. Herpetologica 18: Brattstrom, B. H Preliminary review of the thermal requirements of amphibians. Ecology 44: Brattstrom, B. H. 1970a. Amphibia. In G. C. Whittow (ed.), Comparative physiology of thermoregulation, pp Academic Press, New York. Brattstrom, B. H Thermal acclimation in Australian amphibians. Comp. Biochem. Physiol. 35: Brattstrom, B. H. and J. W. Warren Observations on the ecology and behavior of the Pacific tree frog, Hyla regilla. Copeia. 1955: Brown, H. A. 1975a. Temperature development ot the tailed frog, Ascaphus truei. Comp. Biochem. Physiol. 50A: Brown, H. A Embryonic temperature adaptations of the Pacific treefrog, Hyla regilla. Comp. Biochem. Physiol. 51A: Burke, E. M. and F. H. Pough The role of fatigue in temperature resistance of salamanders. J. Thermal Biol. 1: Burton, T. M. and G. E. Likens Energyflow and nutrient cycling in salamander populations in the Hubbard Brook Experimental Forest, New Hampshire. Ecology 56: Byrne, J. J. and R. J. White Cyclic changes in liver and muscle glycogen tissue lipid and blood glucose in a natural occurring population of Rana catesbeiana. Comp. Biochem. Physiol. 50A: Casterlin, M. E. and W. W. Reynolds Behavioral fever in anuran amphibian larvae. Life Sci. 20: Casterlin, M. E. and W. W. Reynolds Behavioural thermoregulation in Rana piptens tadpoles. J. Thermal Biol. 3: Christensen, C Adaptations in the water economy of some anuran amphibia. Comp. Biochem. Physiol. 47A: Clausen, D. L The thermal relations of the tailed frog, Ascaphus truei, and the Pacific treefrog, Hyla regilla. Comp. Biochem. Physiol. 44A: Drewes, R. C, S. S. Hillman, R. W. Putnam, and O. M. Sokol Water, nitrogen and ion balance in the African treefrog Chiromantu, petersi Boulenger (Anura: Rhacophoridae), with comments on the structure of the integument. J. Comp. Physiol. 116B: Eddy, F. B. and P. McDonald Aquatic respiration of the crested newt, Tnturus cristatus. Comp. Biochem. Physiol. 59A: Farrell, M. P Effect of temperature and photoperiod acclimations on the water economy of Hyla crucifer. Herpetologica 27: Feder, M. E Lunglessness, body size and metabolic rate in salamanders. Physiol. Zool. 49: Feder, M. E Environmental variables and thermal acclimation in neotropical and temperate zone salamanders. Physiol. Zool. 51:7-16. Feder, M. E. and F. H. Pough Temperature selection by red backed salamanders, Plethodon c. cinereus (Green) (Caudata: Plethodontidae). Comp. Biochem. Physiol. 50A: Fitzpatrick, L. C Influence of sex and reproductive condition on metabolic rates in the Allegheny Mountain salamander, Desmognathus ochrophaeus. Comp. Biochem. Physiol. 40A: Fitzpatrick, L. C Influence of seasonal temperatures on the energy budget and metabolic rates of the northern two-lined salamander, Eurycea bis-

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