Behavioral and Physiological Thermoregulation of Crocodilians

AMER. ZOOL..19:239-247 (1979). Behavioral and Physiological Thermoregulation of Crocodilians E. NORBERT SMITH Northeastern Oklahoma State University, Tahlequah, Oklahoma 74464 SYNOPSIS. Crocodilians, like other reptiles, regulate their body temperatures by a combination of behavioral and physiological mechanisms. Behaviorally, they seek warm surface water or bask when cool and avoid overheating by the evaporation of water from their dorsum, evaporation of water by gaping or by retreating to deep, cool water. Physiologically, crocodilians increase cutaneous thermal conductance by increasing blood flow to the skin (and subdermal musculature) during warming. This hastens the warming process. Cutaneous blood flow is reduced during general cooling and locally if the body temperature exceeds skin temperature. This enables crocodilians to increase body temperature significantly while basking in cool shallow water. Large crocodilians appear to be able to alter their rates of heat exchange to a larger extent than small ones and they can do so with less cardiovascular involvement. Large crocodilians, with their lower surface/volume ratio, are capable of producing sufficient metabolic heat to elevate their body temperature above water temperature. INTRODUCTION It is often advantageous for animals to have a high and stable body temperature. Biochemical reactions are hastened by high temperatures, resulting in rapid digestion and assimilation of food, faster conduction of neural impulses, better coordination, and more rapid growth and healing. Disadvantages include rapid depletion of stored energy due to the high rate of metabolism and a reduced safety margin between body temperature and upper lethal temperature. Animals can achieve a high and stable body temperature by either endothermy or ectothermy. Endothermic birds and mammals increase thermal insulation and produce Much of the original research was supported by the National Geographic Society, Welder Wildlife Foundation and Caesar Kleberg Foundation. Recent support has been from N1H (MBS) Grant No. 5 S06 RR08123 and NIH National Institute of General Medical Science MARC Grant No. 5 T32 GM07694. This research would not have been possible without the analysis, critical review and encouragement of Stanley Robertson, Physicist, Northeastern Oklahoma State University. W. W. Reynolds and Larry Crawshaw critically reviewed an early version of the paper and offered several helpful suggestions. I respectfully acknowledge my sincere appreciation to William W. Reynolds, The Pennsylvania State University, for organizing and for the invitation to participate in this symposium. Page charges were paid by N.S.F. Grant PCM 78-05691 to W. W. Reynolds. 239 significant heat endogenously. This effectively uncouples their body temperature from the thermal environment, but depletes large amounts of stored energy during exposure to severe cold. Ectotherms obtain body heat from the environment but little stored energy is required under low temperature conditions. Neither approach is unequivocally advantageous. Intergrades benefiting from both approaches are numerous. Facultative or partial endotherms include hibernating mammals, birds and mammals exhibiting torpor, incubating pythons, many insects and certain large marine fish. Most extant reptiles are fully ectothermic, relying on heat from outside the body. Only in active reptiles exceeding about 5 Kg is a significant amount of endogenous heat produced. Early studies of reptilian thermoregulation dealt with behavioral thermoregulation of lizards (Mazek-Fialla, 1941; Strel'nikov, 1944; Bogert, 1949; Pearson, 1954). During the 1950's and 1960's, preferred and lethal temperatures of numerous reptiles were described (Brattstrom, 1965). In the 1960s, emphasis in reptilian thermoregulation studies began shifting from behavior to physiology. Bartholomew and his students at UCLA demonstrated that several species of lizards are able to alter their rates of heat exchange physiologically (Bar-

240 E. NORBERT SMITH tholomevv and Tucker, 1963; 1964; Bartholomew and Lasiewski, 1965; Bartholomew et al., 1965). More recently, similar phenomena have been observed in fishes (Reynolds, 1977; Reynolds and Casterlin, 1978). Crocodilian thermoregulation Thermoregulation of crocodilians was poorly studied until the present decade. Mcllhenny (1935) reported much of the natural history of alligators and mentioned that they "sunned" or "basked" when air temperature exceeded water temperature. Colbert et al., (1946) established preferred and lethal temperatures for alligators, and Cott (1961) reported thermoregulatory behavior in the Nile crocodile, Crocodilus niloticus. Coulson and Hernandez (1964) reported effects of temperature on biochemical reactions in alligators. Of the crocodilians, alligators have received the most attention (review by Lang, 1976). Alligators range far from the tropics and survive in temperate winters. Throughout much of their range they are the largest ectotherm. Animals living at latitudinal or thermal extremes often show highly refined anatomical, physiological and behavioral adaptations that make them well suited for study. Spotila (1973) reported behavioral thermoregulation of alligators, using telemetry to monitor body temperatures. He stressed the importance of water to minimize extreme fluctuations in body temperatue and developed a "heat energy budget" (Spotila et al., 1972), and extrapolated dinosaurs (Spotila, 1973). Unfortunately, insufficient data regarding physiological variables (Smith, 19766), and various conceptual errors, severely limit the utility of their mathematical model. Behavioral thermoregulation Crocodilians, like most other reptiles, rely on a combination of behavioral and physiological mechanisms to regulate their body temperature. Crocodilians gain heat by radiation, conduction, and metabolism. Metabolic heat is significant in large crocodilians. Thermal conduction from air or water is an important avenue of heat exchange. Heat may be lost by the evaporation of water. Although its thermoregulatory significance in crocodilians was denied by Neill (1971), basking is generally recognized as occuring when air temperature exceeds water temperature. How does a wet crocodilian determine when the dry bulb air temperature exceeds the water temperatuere? Recent studies with alligators showed that alligators pause parallel to the shore with the dorsum exposed to the air in a "pre-basking" posture. After the dorsum was dry, alligators either crawled out to bask or retreated to deeper water (Smith, 1975«) depending on skin or core temperature. This behavior along with the response to local heating and cooling (Smith et al., 1978) suggests crocodilians possess cutaneous thermal receptors. Crocodilians bask in part to increase body temperature (Cott, 1961; Smith, 1975a; Grigg and Alchin, 1976; Drane et al., 1977; Johnson et al., 1978). They may also derive other benefits from basking, as has been suggested for turtles (Cagle, 1950). Forced prolonged basking is lethal (Colbert and Cowles, 1946) when excessive core temperatures are reached. Semi-aquatic basking is accomplished in alligators by maintaining a high floating posture (Smith, 1975a). My research with the American alligator, Alligator mississippiensis, over the past ten years, provides insight into crocodilian thermoregulation in general. Unlike many crocodilians, the American alligator ranges well into temperate climates. Throughout much of its range in North America, it is the largest ectotherm. In contrast to their present endangered status, alligators were once abundant and ecologically important reptiles (Mcllhenny, 1935; Giles and Childs, 1949; Craighead, 1968). Field studies were conducted in southern Texas at the Welder Wildlife Refuge (San Patricio County) and in central Texas at the Waco Zoo. Multichannel radio telemetry (Smith, 1974) was used to monitor subdermal ventral and dorsal temperatures, deep body temperature and heart rate. At the zoo and in the field, non-telemetered and telemetered alligators showed the

CROCODILIAN THERMOREGULATION 241 same thermoregulatory behavior. Figure 1, showing the relation between various environmental and telemetrically measured temperatures, clearly demonstrates that basking may be triggered when air temperatue exceeds water temperature. On three separate occasions, basking commenced when air temperature exceeded water temperature. A drop in air temperature (by intermittent cloud cover) resulted in retreat into the warmer water. Alligators were observed leaving the water at night and on heavily overcast days when the air was cooler than the water, indicating behavioral drives other than thermoregulation play a role in terrestrial activity. Small- to medium-size alligators (up to 50 100 kg) are essentially ectothermic poikilotherms. That is, in an environmental chamber or water bath where radiant heating and evaporative losses are minimal, body temperature will approximate environmental temperature. Similar results have been observed for a wide variety of reptiles and fish. In their natural environment where animals are free to select optimal microhabitats from the available temperature mosaic, 40-1 ENVIRONMENTAL a high degree of regulation of body temperature has been found. Similar results have been observed for alligators. Figure 2 illustrates the relation between body temperature at the end of basking and water temperature. Solid circles are daily mean body temperatures. The solid line represents no regulation or complete equilibrium (T b =T w ). The dashed line is the least squares best fit for the data points. A true homeotherm would exhibit a line parallel to the lower axis indicating complete independence of body temperature from water temperature. The slope of alligator body temperatures indicates that the alligator, by a combination of behavioral and physiological thermoregulation, is able to reduce changes in body temperature to 1/13th the amount that the water temperature changes. This indicates a high degree of thermoregulation indeed. Seasonal variation of alligator thermoregulatory behavior is profound. Alligators in southern Texas rarely bask in the summer. Basking sites are often used in spring and fall. Basking occurs occasionally on warm days during winter. Daily activity changes from nocturnal in summer to diurnal at other seasons. Crocodilians often crawl out to bask on warm mud banks, where conductive heat exchange occurs. An alligator moved to a new warm spot each time the telemetrically measured ventral subdermal temperature began to 35 UJ TELEMETRIC a. a. LJ a. g33i 32-29 30 31 32 33 34 9 II 13 15 17 TIME OF DJT FIG. I. Environmental and telemetric measurements of a mature male alligator. (Redrawn from Smith. 1975c/) WATER TEMPERATURE 'C FIG. 2. Relation between body temperature after basking and water temperature of a mature male alligator. The dashed line represents the least squares fit and the solid line indicates T B = T w.

242 E. NORBERT SMITH drop. Each relocation resulted in a temporary increase of subdermal temperature, as heat was absorbed and conducted to the interior of the alligator (Smith, 1975a). Water is important in the thermoregulation of crocodilians. Thermal gradients in natural water are often steep. Shallow surface water can be used to gain heat, while deep water provides a retreat from high temperatures. Alligators dig a hole in response to high temperatures. Alligators can take thermally significant postures with respect to water surface as shown in Figure 3. An efficient method of evaporative cooling (Smith, 1975a) was periodic submergence enabling a high floating posture to lower body temperature by evaporation of water. Alligators construct elaborate hibernating dens, often shared by several individuals. Dens provide protection from freezing temperatures. Nothing has been written about crocodilian body temperature during hibernation. PHYSIOLOGICAL THERMOREGULATION In crocodilians, as in other reptiles, physiological thermoregulation often enhances or extends the effects of behavioral thermoregulation. Physiological thermoregulation can be defined as changes that cause the thermal response of live animals to differ from dead animals. It includes passive and active elements. Passive elements include physical processes over which the animal may have no control such as the effects of temperature on blood viscosity, pacemaker activity and metabolism. Physiological thermoregulation also includes active elements over which the animal exerts control. Important active mechanisms of physiological thermoregulation include changes in amount and distribution of blood flow, endogenous heat production, and evaporation of body water. Each of these are important to crocodilians and will be discussed in turn. Amount of blood jlow Although the stroke volume (ml/heartbeat) varies slightly as heart rate changes, general trends in cardiac output (ml/min) can be established by measurement of heart rate (Reynolds, 1977; Reynolds and Casterlin, 1978) for fish, reptiles and mammals. Bartholomew and Lasiewski (1965) observed a marked hysteresis when body temperature, during warming and cooling, was plotted against heart rate. Similar results were observed in several lizards (Bartholomew and Tucker, 1963, 1964), and fish (Reynolds, 1977; Reynolds and Cas- FIG. 3. Thermoregulatory postures of alligators with respect to water surface. A high float, B common float, C submerged breathing, D- complete submergence.

CROCODILIAN THERMOREGULATION 243 terlin, 1978). Heart rate for any body temperature during warming generally exceeded the heart rate during cooling at the same body temperature. This was taken as indicative of increased blood How during warming. Spray and Belkin (1972) attributed the hysteresis to artifactual thermal lag of the cloacal temperature of iguanas. Simultaneous measurement of heart, stomach, and cloacal temperature in alligators indicated that a significant hysteresis does exist, suggesting increased warming blood flow (Smith, 1976a). CHANGING PATTERNS OF BLOOD FLOW Inanimate objects and dead animals heat and cool at the same rate (other factors, such as evaporation, being equal). Live animals heat and cool faster than dead animals largely due to blood flow (Reynolds and Casterlin, 1978). Crocodilians generally heat faster than they cool, resulting from a change in thermal conductance altered by blood flow. Ischemic skin (e.g., during cooling) conducts heat poorly. During warming, cutaneous vasodilation increases blood flow and heat transport (Smith, 1976rt). Xenon clearance studies (Smith et al., 1978; Grigg and Alchin, 1976) and direct heat flow measurements (Smith, 19766) clearly indicate that patterns of blood flow are altered during warming and cooling. The results of heating and cooling experiments can be compared in several ways. The rate change ( C/min) at the mid-temperature is useful only if the size of the temperature step is the same for all experiments. This is seldom the case. A thermal time constant (Smith, 1976a; Reynolds and Casterlin, 1978) or half-time (Spigarelli et al., 1977) has more utility because neither is strongly dependent upon the size of the temperature step. In the relation between thermal time constant and body weight for several alligators, certain trends are apparent: Heat exchange in water exceeds heat exchange in air (Fig. 4), due to the higher thermal conductance and specific heat of water. Large alligators require longer to heat and cool than small alligators, due to mass (s/v ratio) and suri oo. Alligator mississippiensis 80 60 ft i> 4 0 =30 (- 20 I 0 8.6 8 I 2 3 4 5 6 8 10 Body weight in kilograms FIG. 4. Log-log relation between thermal time constant and body mass. Open circles represent cooling. Closed circles are warming. Dashed lines indicate water experiments. Solid lines represent air measurement. (Redrawn from Smith, 197(V;) face area differences. Interestingly, hatchling alligators heat and cool at the same rate (Smith and Adams, 1978) while large alligators heat faster than they cool, indicating that large crocodilians are better physiological thermoregulators than are small ones. Indirect evidence indicates a similar situation for marine iguanas (White, 1973): Large iguanas depend on a combination of behavioral and physiological thermoregulation, while juveniles depend predominantly on behavioral thermoregulation. It is adaptive for large crocodilians to heat faster than they cool. A high body temperature obtained by basking of a large crocodilian (100 Kg) drops very slowly upon entrance to cold water requiring hours. In contrast, even if a 100 g crocodilian could cool at 10% of the warming rate, a thermal equilibration could be delayed for only a few minutes. The cutaneous vascular response of crocodilians appears to be different from that of other reptiles. The response appears to be local in all reptiles. Portions of the skin heated show vasodilation. The skin of lizards shows increased bloodflowas body temperature increases (Morgareidge and White, 1969; Weathers amd Mor-

244 E. NORBERT SMITH gareidge, 1971; Baker et al., 1972). In crocodilians, cool portions of the skin show reduced blood flow even if body temperature increases (Smith et al., 1978; Grigg and Alchin, 1976). This is presumably adaptive for crocodilians especially during aquatic basking. Mechanisms of this response remain to be elucidated. It is particularly interesting that heart rate response follows the thermoregulatory requirements much more closely than it follows oxygen requirements. Heart rate during warming is often twice as high as it is during cooling at the same body temperature (but cf., Reynolds, 1977). Oxygen consumption is greater during cooling than it is during warming. This difference between oxygen utilization and heart rate is illustrated by an 8-fold (at 16.5 C) increase in oxygen pulse during cooling (Smith, 19756). The available evidence seems to suggest that the cardiovascular system in crocodilians (and probably other reptiles) is more important in heat transport than oxygen transport. This is not to say that oxygen transport is unimportant in reptiles, but the available evidence indicates heart rate follows thermal requirements more closely than oxygen demands. Of course, this is in contrast to the way we generally interpret the cardiovascular responses of endothermic birds and mammals. In mammals and birds the cardiovascular response is important in thermoregulation but oxygen demands take precedence. ENDOGENOUS HEAT PRODUCTION Crocodilians grow very large larger in fact than any other living reptile. Large size increases thermal inertia, reduces the surface/volume ratio and enhances retention of endogenous heat. Large crocodilians produce less heat per kilogram of tissue than small crocodilians, but the effect of s/v ratio predominates. EVAPORATION OF WATER Crocodilian integument is not impervious to water. The effect of cutaneous evaporation is insignificant for thermoregulation. However, several crocodilians hold their mouths open (gape) when hot. This was denied by Neill (1971), but recent studies have documented both. t.h& extent and the, effect of gaping (Spotila et al., 1977). Gaping exposes moist mucosa of the mouth to evaporation. This can reduce head temperature significantly. Thermal and physiological characteristics of theoretical crocodilians Although much remains to be done, enough measurements exist to make several generalizations about thermal and physiological responses of crocodilians. By comparing time constants and whole body conductance of alligators (Table 1) several conclusions may be drawn. Large alligators heat and cool more slowly, but large animals heat in a small fraction of the time required to cool, while small alligators heat and cool at nearly equal rates. High conductance results in reduced thermal time constant. Conductance and thermal time constant are reciprocally related, as indicated by comparison (Table 1) of T W /T C and C c /C w, which implies endogenous heat production is not important in crocodilian thermoregulation in the size range for which we have data. Heating and cooling time constant ratios may be estimated from cooling and warming conductance ratios. Knowledge of area-specific blood flow (ml/cmvmin) and total body mass permit calculation of the total cutaneous blood flow during heating and cooling (Table 2). Small alligators heat and cool at the same rate because they are unable to alter cutaneous blood How in response to heating and cooling. Cardiac output values for crocodilians of different sizes are unavailable. One can make assumptions about cardiac output and the way it would scale with mass. In all probability, cardiac output (CO.) can be represented alleometrically as: CO. = am". Values of a and b differ during heating and cooling. For mammals, b usually is near 0.75. If one assumes alligator cardiac output is similar to that of iguanas, a model relating cardiac output and percent CO. to the

CROCODILIAN THERMOREGULATION 245 TABLE 1. Relation between thermal time constants, whole body conductance and body mass for crocodiltans. Body mass (Kg) 0.05 0.10 0.50 1.00 5.00 10.0 50.0 100 500 1000 a Smith, 1976a. b Robertson and Thermal time constant (T) in air 3 Warming (min) 9.40 11.8 20.0 25.1 42.5 53.3 90.4 113.5 192.4 241.5 Smith, 1979. Cooling (min) 9.40 12.7 25.4 34.4 69.0 93.1 186.9 252.3 506.6 683.9 Ratio T W/T C 1.00 0.93 0.79 0.73 0.62 0.57 0.48 0.45 0.38 0.35 Warming 0.143 0.123 0.088 0.076 0.054 0.047 0.033 0.029 0.021 0.018 Whole body conductance at 25 C (Cal/cmVmin/ D C) b Cooling 0.169 0.133 0.077 0.061 0.035 0.028 0.016 0.013 0.007 0.006 Ratios c c /c w 1.18 1.08 0.88 0.80 0.65 0.60 0.49 0.45 0.36 0.33 skin during warming and cooling can be made. Implied in results published by Baker et al. (1972) is a value of a = 70 ml/min during warming and a = 35 ml/min during cooling. A doubling of cooling CO. during warming is further supported by heart rate hysteresis (Smith, 1976a)- In the relation of percent cardiac output to the skin during warming and cooling as a function of body mass (Fig. 5), it should be noted that while the actual value of cardiac output might be in error by as much as 50%, the weight-specific trends remain valid; i.e., actual data may shift the curves up or down but will not alter the shapes of the curves. Several trends are evident. Blood flow to the skin is slight no matter what value of b is used for small animals. Percent CO. to the skin is greater during warming than during cooling. This is true for alligators of all sizes, but diminishes for small and very large animals if b is 0.75 to 1.0. Finally, for values of b between 0.75 and 1.0, very large animals require less cardiovascular effort to thermoregulate than do smaller animals. This is particularly important as b approaches 1.0. FURTHER RESEARCH Crocodilians are relatively easy to maintain and work with and come in a wide variety of species and sizes. Many are cur- IABI.K 2. Relation between body mass and cutaneous blood flow in alligators. Body mass (Kg) 0.05 0.10 0.50 1.00 5.00 10.0 50.0 100 500 1000 Skin thickness (cm)" 0.026 0.033 0.061 0.080 0.15 0.19 0.35 0.46 0.85 1.10 Cutaneous blood How Warming Cooling Warming Cooling (ml/cmvmin)" (ml/min) c 0.0006 0.0010 0.0056 0.0085 0.012 0.014 0.015 0.015 0.015 0.015 0.0006 0.0010 0.0029 0.0035 0.0043 0.0044 0.0045 0.0045 0.0045 0.0045 0.082 0.22 3.53 8.50 35.10 65.00 204.0 324.0 947.0 1503 0.082 0.22 1.83 3.50 12.6 20.4 61.2 97.1 284.0 451.0 a Skin thickness (s) in cm and Mass(M) in Kg S = 0.080M" 1 ". Data lor alligators 48gto 124 Kg, Smith rial, 1978. b Obtained from Figure 9: Smith et al., 1978. c ' Obtained by multiplying Area by cutaneous blood (low ml/cmvmin. (A= lo^'m m7 \ Benedict, 1932).

246 E. NORBERT SMITH x O 3 O Q or < 20 I 8 I 6 14 I 2 10 8 6 4 2 UJ _ o 0 or 0.01 a^ b = 1 0. b = 0.75 # b = 0.67 warming " ^ ^ cooling * ^ ^* ^ warming ^^^ O.I 1.0 10 100 BODY MASS IN KILOGRAMS ing for different values of b (see text), cooling ^ ^ " ^ ^ cooling 1000 FIG. 5. Relation between body mass and percent cardiac output to the skin during warming and coolrently in danger of extinction and most are of economic importance. Only a few have been studied in depth. Much work is needed. Parallel studies need to be made of the other species of crocodilians. The relative importance of the cardiovascular system for heat and oxygen transport needs to be quantified. Very large individuals need to be studied to confirm validity of extrapolation. The mechanism of the seemingly anomalous reduction of cutaneous blood flow in an area of cool skin while body temperature increases needs to be studied. Data are badly needed relating cardiac output during heating and cooling to body mass. In summary, much has been learned but much more is to be gained from careful research of these "last of the ruling reptiles." Better knowledge of the thermal physiology of crocodilians will aid in management for their survival, help us to understand reptilian thermoregulation broadly, and shed additional light on the physiology of large extinct reptiles. REFERENCES Baker, L. A., W. W. Weathers, and F. N. White. 1972. Temperature-induced peripheral blood flow changes in lizards. J. Comp. Physiol. 80:313-323. Bailholomew, G. A. and R. C. Lasiewski. 1965. Healing and cooling rates, heart rate and simulated diving in the Galapagos marine iguana. Comp. Biochem. Physiol. 16A:573-582. Bartholomew, G. A. and V. A. Tucker. 1963. Control of changes in body temperature, metabolism, and circulation by the agamid lizard, Amphibolurus barbatw>. Physiol. Zool. 36:199-218. Bartholomew, G. A. and V. A. Tucker. 1964. Size, body temperature, thermal conductance, oxygen consumption and heart rate in Australian varanid liaards. Physiol. Zool. 37:341-354. Bartholomew, G. A., V. A. Tucker, and A. K. Lee. 1965. Oxygen consumption, thermal conductance and heart rate in the Australian skink, Tiliqua scincoides. Copeia. 1965:169-173. Benedict, F. G. 1932. The physiology of large reptiles. Carnegie Inst. Wash. Publ. 425. Bogert, C. M. 1949. Thermoregulation in reptiles a factor in evolution. Evolution. 3:195-211. Brattstrom, B. H. 1965. Body temperatures of reptiles. Amer. Midi. Nat. 73:376-422. Cagle, F. R. 1950. The life history of the slider turtle, P\eudemy\ \mpta tramtil (Holbrook). Ecol. Monogr.

20:31-54. Colbert, E. H., R. B. Cowles, and C. M. Bogert. 1946. Temperature tolerances in the American alligator and their bearing on the habits, evolution, and extinction of the dinosaurs. Bull. Am. Mus. Nat. Hist. 86:327-374. Cott, H. B. 1961. Scientific results of an inquiry into ecology and economic status of the Nile crocodile, Crocodilus niloticus, in Uganda and northern Rhodesia. Trans. Zool. Soc. London. 29:211-337. Coulson, R. A. and T. Hernandez. 1964. Biochemistry of the alligator: A study of metabolism in slow motion Louisiana St. Univ. Press, Baton Rouge. Craighead, E. C, Sr. 1968. The role of the alligator in shaping plant communities and maintaining wildlife in the southern Everglades. Florida Natur. 41:3-7,69-74,94. Drane, C. R., J. W. Webb, and P. Heuer. 1977. Patterns of heating in the body trunk and tail of Crocodilus porosus. J. Thermal Biol. 2:127-130. Giles, L. W. and V. L. Childs. 1949. Alligator management of the Sabine National Wildlife Refuge. J. Wildlife Manag. 13:16-28. Grigg, G. C. and J. Alchin. 1976. The role of the cardiovascular system in thermoregulation of Crocodilus johnstom. Physiol. Zool. 49(l):24-36. Johnson, C. R., W. G. Voigt, and E. N. Smith. 1978. Thermoregulation in crocodilians 111. Thermal preferenda, voluntary maxima, and heating and cooling rates in the American alligator, Alligator mississippiensis. Zool. J. Linn. Soc. 62:179-188. Lang, J. W. 1976. In E. A. Mcllhenny's The alligator's life history. Soc. for the Study of Amphibians and Reptiles. Mazek-Fialla, K. 1941. Die korpertemperatur poikilotherme tiere in Abhangigkeit vom Weinklima. Zeits. Wiss. Zool. 154:170-246. Mcllhenny, E. A. 1935. The alligator's life history. Christopher Publishing House, Boston. Morgareidge, K. R. and F. N. White. 1969. Cutaneous vascular changes during heating and cooling in the Galapagos marine iguana. Nature 223:587-591. Neill, W. T. 1971. The last of the ruling reptiles alligators, crocodiles, and their kin. Columbia Univ. Press, New York. Pearson, O. P. 1954. Habits of the lizard, Liolaemus multiformis multiformis, at high altitudes in southern Peru. Copeia 1954:111-116. Reynolds, W. W. 1977. Thermal equilibration rates in relation to heartbeat and ventilatory frequencies in largemouth blackbass, Micropterus salmoides. Comp. Biochem. Physiol. 56A: 195-201. Reynolds, W. W. and M. E. Casterlin. 1978. Estimation of cardiac output and stroke volume from thermal equilibration and heartbeat rates in fish. CROCODILIAN THERMOREGULATION 247 Hydrobiologia 57:49-52. Robertson, S. L. and E N. Smith. 1979. Thermal indications of cutaneous blood flow in the American alligator. Comp. Biochem. Physiol. (In press) Smith, E. N. 1974. Multichannel temperature and heart rate radio telemetry transmitter. J. Appl. Physiol. 36(2):252-255. Smith, E. N. 1975a. Thermoregulation of the American alligator, Alligator mississippiensis. Physiol. Zool. 48:177-194. Smith, E. N. 19756. Oxygen consumption, ventilation, and oxygen pulse of the American alligator during heating and cooling. Physiol. Zool. 48:326-337. Smith, E. N. 1976a. Heating and cooling rates of the American alligator, Alligator mississippinesis. Physiol. Zool. 49:37-48. Smith, E. N. 19766. Cutaneous heat flow during heating and cooling in Alligator mississippinesis. Am. J. Physiol. 230:1205-1210. Smith, E. N. and S. R. Adams. 1978. Thermoregulation of small alligators. Herpetologica 34:406-408. Smith, E. N., S. Robertson, and D. G. Davies. 1978. Cutaneous blood flow during heating and cooling in the American alligator. Am. J. Physiol. 235(3):R160-R167. Spigarelli, S. A., M. M. Thommes, and T. L. Beitinger. 1977. The influence of body weight on heating and cooling of selected Lake Michigan fishes. Comp. Biochem. Physiol. 56A:51-57. Spotila, J. R., O. H. Soule, and D. M. Gates. 1972. The biophysical ecology of the alligator: Heat energy budget and climate space. Ecology. 53:1094-1102. Spotila, J. R. 1973. Behavioral thermoregulation of the alligator Body temperatures of free roaming individuals under natural conditions. In J. W. Gibbons and R. R. Sharitz (eds.), Thermal ecology, pp. 332-334. U. S. Technical Information Service, Springfield, Va., Oak Ridge National Laboratory. Spotila, J. R., K. M. Terpin, and P. Dodson. 1977. Mouth gaping as an effective thermoregulatory device in alligators. Nature 265:235-236. Spray, D. C. and D. B. Belkin. 1972. Heart ratecloacal temperature hysteresis in iguana is a result of thermal lag. Nature 239:337-338. Strel'nikov, I. D. 1944. Znachenie solnechnoi radiastsif v e'kologii vysokogornykh reptilii (Importance of solar radiation in ecology of high mountain reptiles.) Zool. Zh. (USSR) 23.250-257. Weathers, W. W. and K. R. Morgareidge. 1971. Cutaneous vascular responses to temperature change in the spiny-tailed iguana, Ctenosaura hemilopha. Copeia 1971:548-551. White, F. N. 1973. Temperature and the Galapagos marine iguana: Insights into reptilian thermoregulation. Comp. Biochem. Physiol. 45A:503-513.