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AMER. ZOOL.,19:225-237 (1979). Responses to Rapid Temperature Change in Vertebrate Ectotherms LARRY I. CRAWSHAW Departments of Rehabilitation Medicine and Pharmacology, College of Physicians and Surgeons, Columbia University, New York, Netu York 10032 SYNOPSIS Vertebrate ectotherms often encounter rapid, large scale changes in body temperature. In this paper, I discuss the direct effects of changing body temperature on physiological parameters, as well as corrective responses initiated by the animal. For many biological functions, mean body temperature provides a useful measure of the thermal effects produced by an altered environmental temperature. Under most conditions, the fins and body surface of fish are more important avenues of heat exchange than the gills. The local thermal sensitivity of peripheral blood vessels results in vasomotor adjustments which can alter thermal conductivity. Acid-base balance is challenged by changes in body temperature. Shifts in body temperature also alter metabolic demands, enzyme conformation, ionic and osmotic relationships, spontaneous activity levels and nervous system function. Compensatory mechanisms include behavioral thermoregulation, by which animals seek to avoid stressful thermal environments, and autonomic restorative responses such as high temperature panting in reptiles. Water breathers may initiate anticipatory responses to minimize arterial oxygen fluctuations during termperature change. The organization of the central neuronal network underlying the above regulatory responses is unclear. Both air and water breathers are able to initiate compensatory acid-base responses, but the strategies utilized by the two groups are quite different. Altered body temperature initiates long-term acclimation responses, and if rapid, can also trigger stress responses. INTRODUCTION In this paper, I will explore some of the events that ensue when the thermal environment of a vertebrate ectotherm is rapidly altered. This paper is not intended as a comprehensive review; rather, it is intended to provide insights into some important aspects of the myriad changes that take place following body temperature changes in these animals. The topics treated have been placed in two broad categories: 1) the direct effects that an altered environmental temperature has upon the various tissues of the animal, and 2) homeostatic mechanisms, which the I thank Drs. E. R. Nadel, S. S. Hillman, W. W. Reynolds, E. N. Smith, G. L. Florant and Mr. D. E. Lemons for providing helpful criticism and discussion of this paper. During preparation of this article, the author was supported by NSF Grant PCM 7609658 and N1H Grant 1-R01 NS15318-01 and the general fund of the Department of Rehabilitation Medicine. The supportive and stimulating atmosphere created by Drs. J. A. Downey and L. J. Cote is most appreciated. This publication and the symposium were made possible by NSF Grant PCM 7805691 to W. W. Reynolds. animal actively initiates to minimize or eliminate the deleterious effects of rapid thermal change. In the first category, I will cover the effect of changing environmental temperature on heat balance, acid-base balance, metabolic rate, peripheral blood flow, locomotor activity, ion and water flux, enzyme systems and the nervous system. In the second category, I will evaluate some of the active adjustments made by ectotherms in the face of changing temperature: behavioral thermoregulation, autonomic thermoregulation, feed-forward (anticipatory) autonomic adjustments, neuronal mechanisms underlying the three preceding adjustments, acid-base adjustments, hormonal responses and long-term acclimation. DIRECT EFFECTS OF ALTERED ENVIRONMENTAL TEMPERATURE Heat exchange The predominant modes of head transfer depend upon the nature of the surrounding environment. For aquatic ani- 225 226 LARRY I. CRAWSHAW mals, conduction (and its facilitation by that most of the heat exchange in fish occonvection) is of primary importance. In curred at the gills, but recent measureterrestrial animals, radiation and evapora- ments on sea ravens (Hemitripterus amerition are also substantial factors. Because of canus) indicate that 70-90% of the metathe high thermal conductance and heat bolic heat is lost through the body wall and capacity of water, thermal shifts in aquatic fins (Stevens and Sutterlin, 1976). Slightly organisms are typically more rapid. With lower estimates (40-70%) were arrived at the exception of thermally stable environ- (Sorenson and Fromm, 1976) by measurments, the temperatures found in various ing heat transfer at isolated-perfused gill portions of the body of an ectotherm are arches of rainbow trout, and by utilizing a determined by a complex weighting of tubular heat exchange model. Crawshaw thermal environments encountered in the (1976) demonstrated that different body sites were differentially affected by temrecent past. Experiments designed to investigate peratures at the gills and body surface of rapid temperature changes in ectotherms carp. When the mouth, buccal cavity and often involve a step change from one con- gills (inspiratory temperature) were mainstant temperature to another. A deep body tained at one temperature and the retemperature (such as that in the esoph- maining body surface at another, internal agus, stomach, rectum, heart or brain) is temperatures attained stable values. The monitored to assess the rapidity with which relative influence of inspiratory temperathe animal's body temperature is altered by ture was as follows: brain temperature, the new environment. Although such point 68%; deep dorsal muscle temperature, measurements appear easy to characterize 50%; intestinal temperature, 30%. in terms of Newton's law of excess temperWhen water temperature changes ature (Bartholomew and Tucker, 1963; rapidly, the body surface and fins account Stevens and Fry, 1970, 1974), they belie for a particularly large proportion of the the speed with which the whole animal's heat transfer. Consider the heat loss by the tissue temperatures change. Generalized carp illustrated in Figure 1. Fifty percent effects of changing temperature on such of the change in mean body temperature parameters as metabolic rate or acid-base occurred in about 1.25 min, with a loss in balance are well indicated by the mean tis- body heat content of: sue temperature of an animal. Such de(558g) (0.83 cal-g--1 "C"1) (4.2°C) terminations have been made by placing = 1945cal(8138J) ectotherms in a calorimeter at a temperature different from that of the constant Where: 558g = mass of 1carp 0.83 cal-g--' "C" temperature holding tank. Results from = specific heat of whole animal such experiments on a carp, (Cyprinus car4.2°C = change in T b pio), a lamprey (Lampetra tridentata) and a turtle {Pseudemys scripta) show the rapidjty The heat loss through the gills during with which mean body temperature (Tb) this period can be estimated by assuming a changes as compared to changes in core cardiac output of 0.020 ml-g-~'min~' for temperature (Fig. 1). this fish (Randall, 1970), and that 85% of General aspects of heat exchange in ec- the excess heat in the blood is lost during totherms can be found in a number of passage through the gills (Stevens a>nd sources (Bakken and Gates, 1975; Stevens Sutterlin, 1976). and Sutterlin, 1976; Erskine and Spotila, (0.85) (558g) (0.02 ml-g-^mirr 1 ) 1977). One area of recent interest involves (1.25 min) (9.2°C) the amount of heat transfer occurring at (0.92 cal-g--|OC-') the gills in fish. It was previously thought (1.06 g-ml-1) = 106 cal (443.5J) FIG. 1. Changes in mean body temperature (Tb), brain temperature (Tbr). dorsal muscle temperature (Tdm). intestine temperature (Tln), heart temperature (T,,e) and heart rate (HR) following placement of (a) a lamprey, (b) a carp and (c) a turtle at one temperature into a calorimeter of another temperature. (From Lemons and Crawshaw, 1978; Crawshaw, 1976; and Crawshaw et al., 1978) 227 ECTOTHERM RESPONSES TO TEMPERATURE CHANGE m • 0 *' ( a ) . 2 0 6 kg Lamprey I 2 3 4 5 6 7 8 9 10 II 12 13 14 15 16 25 ( b ) 0.556 kg CARP 500 r k^OO I 300 -S; 20 200 8 i 100 0L | I5L 35 30 25 25 l 5 20 ( c ) . 8 4 7 kg TURTLE * HR 15 10 5 0 2 4 6 8 MINUTES 10 12 228 LARRY I. CRAWSHAW Where: 9.2°C = mean temperature dif- ature, although effective in altering beference between gills and envi- havioral thermoregulation (Myhre and ronment Hammel, 1969), does not affect heating 0.92 cal-g-- lo C-' = specific heat and cooling rates in this animal. Also unafof blood (Stevens and Sutterlin, fected is the rate at which marginal vessels 1976) refill after the blood is expressed by appli1.06 g-ml~' = density of blood cation of gentle pressure (Hammel, per0.85 = proportion of excess heat sonal communication). Spray and May lost during passage through gills (1972), however, provide suggestive eviThus, when this carp was placed in cooler dence for the involvement of a regulatory water, about 5%, (106 cal/1945 cal) of the system: thermal hysteresis was abolished in heat exchange that occurred during the the turtle (Chrysemys picta belli) following first 1.25 min took place at the gill surface. section of the dorsal roots innervating its In reptiles and amphibians, evaporation carapace. Unless the sectioning in some and radiation are also important modes of way interfered with the sympathetic innerheat transfer. In these animals, as well as in vation of the peripheral vessels, their data the aquatic vertebrates, skin blood flow is suggest the necessity of sensory input for critical in determining the rate at which the thermal hysteresis. heat is delivered to the body surface and dissipated to the environment. These pe- Cardiovascular system ripheral blood vessels dilate when the skin is heated and constrict when the skin is The heart-rate hysteresis, typically seen cooled. These characteristic responses when vertebrate ectotherms are heated have been documented visually (Cowles, and cooled (Reynolds, 1977) — heart rates 1958; Heath etal., 1968; Voigt, 1975), and are typically higher at a given body temwith i:i:!Xe clearance (Morgareidge and perature during heating—is largely due to White, 1969; Weathers and White, 1971) two factors. First, heart temperature in several species of reptiles. changes more rapidly than body temperMost vertebrate ectotherms heat faster ature (see Fig. lc), producing a direct than they cool (Bartholomew and Tucker, thermal effect (underestimated by mea1963; Fry and Hochachka, 1970; Spray surements of cloacal or intestinal temperand May, 1972; Spigarelli et al., 1977; see ature) on the tissue of the heart (Spray and Smith, 1979 [this series] for a discussion of Belkin, 1972). Second, cutaneous blood thermal relationships in crocodilians), al- How increases in response to heating prothough the opposite effect is sometimes duce an augmented cardiovascular deseen (Spray and May, 1972; Reynolds, mand, which is met by increasing heart 1977). This thermal hysteresis is occasion- rate (Weathers and White, 1971). Voigt ally referred to as physiological control or (1975) found that the desert tortoise thermoregulation, implying active control (Gopherus agassizii) is chronically vasodiby the animal (Bartholomew et al., 1965; lated, and therefore heats and cools at the Smith, 1976; Reynolds and Casterlin, same rate in the laboratory. Nevertheless, 1978), but little evidence exists to implicate heating rates in the field were up to ten the involvement of a thermally sensitive times faster than cooling rates, leading regulatory system (which entails sensors, Voigt to suggest that in the case of terrescomparators and effectors). Rather, local trial ectotherms, behavioral postures and vasomotor effects alter thermal conductiv- activities can be more important than ity at the body surface. The Australian physiological adjustments in the determiskink (Tiliqufi scincoides) heats faster than it nation of thermal exchange rates. cools (Bartholomewetal., 1965). When the Specialized anatomical arrangement of skin of these animals is warm, the vessels the vasculature can also beneficially alter on the margin of the ventral scales dilate, heat exchange in ectotherms. The most producing a visibly reddened belly. Ma- familiar example is the vascular counternipulation of anterior brainstem temper- current heat exchanger present in tuna ECTOTHERM RESPONSES TO TEMPERATURE CHANGE and lamnid sharks. The exchanger allows the maintenance of temperatures well above ambient in deep muscles (Carey, 1973; Dizon and Brill, this symposium). The heat exchanger also functions very effectively as a barrier to environmentally induced thermal fluctuation; this is likely its primary function in small tuna. Skipjack tuna {Katsuwonus pelamis) exchange heat with the environment at only half the rate of typical fish (Stevens et at., 1974). Acid-base balance As animals heat or cool, important changes occur in their acid-base status. The effect of this changed status is quite different for animals that breathe air or water. These effects have been the subject of several recent, excellent reviews (Randall, 1974; Rahn, 1976; Reeves, 1977), which should be consulted for a more detailed exposition. If the temperature of vertebrate blood is increased in vitro (with a constant CO2 content), pH decreases and PCo2 increases. The pH change is due mainly to a temperature induced increase in the dissociation of histidine imidazole groups of proteins. The altered pH, and the change in CO2 solubility predict changes observed in Pco-2These temperature related changes are such that protein charge states remain constant (Reeves, 1976). These acid-base alterations are actively defended by ectotherms, and are referred to as the maintenance of a constant relative alkalinity (Rahn, 1976) oralphastat regulation (Reeves, 1972, 1977). Enzyme optima follow a similar temperature dependence (Hazel et al., 1978), and apparent Michaelis-Menten constants (Km values) of different vertebrate M4-lactate dehydrogenases are conserved only if the pH of the assay medium is varied in a manner consistent with the changes described above (Yancey and Somero, 1978). These changes occur automatically, because of the effects of temperature on chemical equilibria. Their maintenance requires adjustment of the animal's acid-base metabolism, and will be discussed under the category of active adjustments. 229 Metabolic rate Many studies document the increased metabolic rate that vertebrate ectotherms maintain at higher body temperatures (Whittow, 1970). Much evidence is based on acclimated animals; less well-appreciated is the fact that rapid, but relatively small thermal alterations can produce large metabolic changes. Thus, Meuwis and Heuts (1957) observed that the respiratory frequency of carp (Cyprinus carpio) doubled following a temperature increase from 32°C to 36°C. As thermal acclimation occurred, the ventilation rate decreased. Forty-eight hours after the temperature increase, the ventilation rate was only elevated by 15 percent. Instantaneous temperature compensation Large metabolic changes following shifts in body temperature are minimized in some animals by mechanisms of instantaneous temperature compensation. Such mechanisms are most highly developed in intertidal invertebrates (Newell, 1969), but are probably present to some extent in vertebrate ectotherms. Postulated modes of operation of "instantaneous" thermal compensation include thermal effects on enzyme-substrate interaction and thermally induced alterations in enzyme structure (Hazel and Prosser, 1974). These changes operate to counteract the usual accelerant effect of increased temperature on chemical reactions. Osmotic and ionic balance Water breathers may encounter disruptions of osmotic and ionic balance following moderate or large temperature shifts. These disruptions are most pronounced when temperatures near the upper or lower survival limit are encountered anddepend upon both the rate and amplitude of temperature change. In fish, gills are a major site for both active and passive ionic exchange with the environment, and the large scale respiratory changes that occur during alterations in body temperature in- 230 LARRY I. CRAWSHAW duce problems in electrolyte balance (Houston, 1973). In the eel {Anguilla anguilla), Motais and Isaia (1973) found that water flux increased with increasing acclimation temperature. Rapid increases in temperature produced fluxes greater than those present in animals acclimated to the increased temperature, while decreases in temperature produced exactly the opposite effect. These effects would be predicted from the changes in respiratory activity induced by thermal changes. Diffusion and transport processes at the membrane sites are also temperature-dependent. In goldfish (Carassius auratus) and salt water adapted flounders (Platichthysjiesus) passive Na+ flux exhibited a much smaller temperature dependence (Qm=2) than active Na + /K + exchange mechanisms (Qi<>=3 — 6) (Maetz, 1.972; Maetz and Evans, 1972). At low temperatures then, active exchange mechanisms may have insufficient capacity in relation to passive ion movements, while at high temperatures, survival problems may be related to high absolute levels of ion flux. Ion transport mechanisms are also affected by hormone secretions, which will be discussed subsequently. Activity via the hypothalamic thermoregulatory centers, since cooling of the anterior brainstem in brown bullheads (Ictalurus nebulosus) led to decreased activity (Crawshaw and Hammel, 1974). Nervous system function In addition to effects on the motor centers, temperature changes involving the whole organism affect all aspects of nervous system function. Most sensitive are highly organized systems involving many synapses. Conditioned reflexes are more sensitive than direct reflexes, which are in turn more sensitive than peripheral nerve conduction (Prosser, 1973; Lagerspetz, 1974). Since physiological regulatory systems involve intricate neural networks, the complexity of the homeostatic responses to thermal change in ectotherms can be readily appreciated. HOMEOSTATIC MECHANISMS Behavioral thermoregulation Vertebrate ectotherms possess a number of interacting homeostatic systems which serve to minimize the deleterious effects of rapid temperature change. Thermal stresses can often be abated by appropriate selection of a microclimate, and such behavioral thermoregulation is often a major determinant of the overall activity pattern of ectotherms (Whittow, 1970). The ability to sense peripheral temperature change is well-developed in ectotherms (liardach, 1956; Dizon etal., 1974; Dizon et al., 1976), and has been implicated in the regulation o( body temperature in these animals (Myhre and Hammel, 1969; Crawshaw and Hammel, 1971, 1974). The temperature of the anterior brainstem (Myhre and Hammel, 1969; Crawshaw and Hammel, 1971, 1973, 1974) and spinal cord (Duclaux etal., 1973) is also important in this regard. Temperature change by itself raises the level of spontaneous activity in fish (Peterson and Anderson, 1969; Olla and Studholm, 1971; Stevens, 1972), thus increasing the metabolic rate. Friedlander et al. (1976), studying goldfish, found the cerebellum to be an important mediator of activity level. The behavioral sequence of events which followed whole animal heating or cooling (hyperexcitability, motor incoordination, disequilibrium and areflexia) was also induced by heating or cooling the cerebellum. In cerebellectomized fish, less heating or cooling was needed to elicit hyperexcitability and the subsequent lack of coordination. Further, electrical activity of inhibitory cerebellar interneurons and Purkinje neurons was disturbed by the same alteration in body temperature as the Autonomk thermoregiihition behavioral events. Thermal effects on sponCertain reptiles and amphibians appaitaneous activity are probably not mediated ently utilize the sensing and integrating 231 ECTOTHERM RESPONSES TO TEMPERATURE CHANGE portions of the above thermoregulatory were immobilized with gallamine triethionetwork to modulate evaporative heat loss dide, indicating that the observed effects in warm environments. These reptiles in- were not secondary to induced changes in crease evaporative heat loss by panting and activity. Very rapid changes in ambient frothing when very high temperatures are water temperature (3°C in 15 seconds) encountered (Schmidt-Nielsen and Daw- produce alterations in ventilatory minute son, 1964; Cloudsley-Thompson, 1968, volume in carp (Cyprinus carpio) which are 1970). Autonomic thermoregulatory re- rate sensitive (Crawshaw, 1976) and altersponses, like behavioral thermoregulatory ations in ventilation and cardiac frequenresponses, are influenced by ambient, cies in lampreys (Lampetra tridentata) which brainstem and core temperatures (Craw- occur too rapidly to be due to changes in ford and Barber, 1974; Morgareidge and brain temperature or mean body temperHammel, 1975). Panting thresholds in the ature (Lemons and Crawshaw, 1978). lizard {Amphibolurus muricatus) are elevated Similar changes do not occur in the turtle by increased acclimation temperatures and (Pseudemys scripta) (Fig. 2). longer photoperiods (Heatwole et al., 1975). The cutaneous mucous glands of the bullfrog (Rana catesbeiana) function during basking to keep the animal's integument moist. It appears that these 8! glands are influenced by thermoregulatory IK) neuronal networks, since mucous dis0.206 kg charge rates are increased by heating of LAMPREY the head and decreased by brain transection below the level of the anterior 1 ^ 90 hypothalamus (Lillywhite, 1971). I Feed-forward autonomic adjustments in water breathers As compared to air, water has a low oxygen content, low diffusion rate and a high viscosity. In water breathing ectotherms the maintenance of an adequate oxygen supply is of paramount importance, and the maintenance of blood oxygen levels takes precedence over CO2 elimination (which occurs readily because of its high solubility) (Randall, 1974). There is some evidence that the thermoregulatory system is involved in maintaining oxygen supplies during conditions of rapid thermal change. Increasing and decreasing the anterior brainstem temperature of the California scorpionfish (Scorpaena guttata) caused proportional increases and decreases in the ventilatory minute volume. These changes were related to the absolute temperature, and not the rate of change (Crawshaw et al., 1973). The temperature of the spinal cord has been shown to affect heart rate (Iriki et al., 1976; Nagai and Iriki, 1977). In some experiments the fish SB 80 280k I 23° ,. 180 0.821kg TURTLE u > ^20 0 1 2 3 4 TIME (MIN) FIG. 2. Changes in ventilatory and circulatory parameters when ectotherms encounter rapid decreases in water temperature. Temperature change was initiated at t=0, and took about 20 sec to complete. The decrease was 3°C for the lamprey and carp and 10°C for the turtle. 232 LARRY I. CRAWSHAW Behavioral and autonomic responses to temperature change in fish and mammals have many similarities. Both response systems are similarly controlled in that peripheral and anterior brainstem temperatures are transduced and integrated to produce a restorative response of the appropriate direction and magnitude. In both classes, the absolute peripheral temperature and the rate of peripheral temperature change are important inputs to the thermoregulatory centers (Cabanac, 1975). In the anterior brainstem only the absolute temperature appears important in the determination of the regulatory response (Hammel, 1968). Fish and mammals both utilize behavioral responses to avoid noxious temperatures; failing this, autonomic responses are activated. In mammals, these responses (such as shivering or panting) serve to maintain internal temperature. Although most fish cannot maintain a constant internal temperature, they could utilize the thermoregulatory network to anticipate the physiological changes which inevitably accompany thermal change. This feed-forward system would allow water breathers to initiate restorative responses in important regulated variables without the necessity of incurring a deficit to furnish the appropriate error signal. Water breathing vertebrates may have evolved such a control system, subsequently modified by air breathers in the development of endothermy. The rapid increases in ventilation and heart rate which occur following increases in surface, anterior brainstem and spinal cord temperatures could serve to maintain arterial PO2 levels during the inevitable increases in metabolism. Prompt decreases in cardiovascular and respiratory activity following the detection of decreased temperatures could minimize the expenditure of energy necessary for gill ventilation and active ion transport during periods of rapidly falling metabolic requirements. Neurons involved in temperature regulation The characteristics of peripheral temperature sensitive neurons in amphibians (Spray, 1974) appear very similar to the well-studied corresponding neurons in mammals (Hensel, 1973a). The identification of central neurons involved in temperature regulation has been difficult. Although both warm and cold sensitive neurons have been located in the anterior brainstem of fish (Greer and Gardner, 1970, 1974; Nelson, 1978), reptiles (Cabanac et al., 1967) and mammals (Hensel, 19736), it is unclear whether these neurons are actually involved in thermoregulation. Pekin ducks do not respond to anterior brainstem heating or cooling with thermoregulatory responses, yet a normal population of warm and cold sensitive neurons was found when the hypothalamus of a conscious duck was probed with microelectrodes (Simon et al., 1977). Feed-forward autonomic adjustment in air breathers It has been suggested that reptiles also utilize the thermoregulatory network to anticipate metabolic deficits, since alterations of the anterior brainstem temperature produce changes in blood pressure (Rodbard et al., 1950; Heath et al., 1968) and oxygen uptake (Siegel and Privitera, 1976) in turtles. Although the metabolic requirements of reptiles do indeed increase with temperature, it seems unlikely that active regulation is involved in anticipating oxygen requirements. Rather, in these air breathing ectotherms acid-base regulation is more primary. The effects that anterior brainstem temperature manipulations have on blood pressure and O2 uptake in reptiles is difficult to interpret, but non-specific excitation of systems involving behavioral arousal or vascular resistance could be involved. Acid-base regulation in air breathers In air breathers, appropriate acid-base balance is maintained in the face of thermal change (while maintaining a constant total CO2 concentration) by altering the ratio of pulmonary ventilation to metabolic CO2 production. The turtle (Pseudemys scripta) has been shown to make such adjustments promptly after shifts in body 233 ECTOTHERM RESPONSES TO TEMPERATURE CHANGE temperature Jackson and Kagen, 1976). These adjustments allow reptiles not only to tolerate, but actively to initiate large changes in body temperature. Thus Pearson and Bradford (1976) report that the Active gill ion exchange mechanisms are utilized by fish for ionic regulation: C1~V H C ( V exchange, and Na+/NH4+ or H + exchange (Evans, 1975; Maetz, 1976). It has been suggested that these exchange iguanid lizard (Liolaemus multiformis) basks mechanisms are involved in the pH adin early morning sunlight and raises its justments induced by thermal shifts (Ranbody temperature from 5°C to 30°C in dall and Cameron, 1973). There is a large about 30 minutes, and Crawshaw et al. body of suggestive data, but this hypothesis (1978) found that turtles (Pseudemys scripta) has not been clearly demonstrated to date. acclimated to 3°C for three weeks, selected It is of interest, however, that the trout water above 30°C in less than one hour. (Salmo gairdneri), which has a rather poor Other factors favoring adjustment to rapid ability to tolerate alterations in body temthermal change in reptiles include oxygen perature, also has a relatively weak Cl~/ availability and a greatly decreased ex- HCO:i~ exchange process (Janssen and change of ions and water between the Randall, 1975). The eurythermal killifish animal and the environment. (Fundulus heteroclitus) has a very active Amphibians occupy an intermediate po- C1 ~/HCO:i~ exchange, present not only on sition between reptiles and fish, since the the gill surface, but also on the opercular skin and the lungs are both important res- epithelium (Karnaky and Kinter, 1977; piratory organs. Mackenzie and Jackson Deghan et al., 1977). However, pH imbal(1978) determined that acid-base regulation during temperature change in the 20 30 40 50 bullfrog (Rana catesbeiana) was accom1 >-10°C plished by ventilatory adjustments. Skin 30 40 50 CO2 conductance (skin CO2 loss/transt7°C cutaneous Pco2) w a s n ° t significantly affected by temperature. Acid-base regulation in water breathers Water breathers face a difficult problem in making acid-base adjustments to altered body temperature. Since water has a relatively low O2 content and a high CO2 solubility, fish closely regulate arterial PO2 levels, with arterial PC02 remaining at fixed levels slightly ( 2 - 5 mm Hg) above the PC02 of the breathing medium (Randall and Cameron, 1973; Janssen and Randall, 1975). Changes in ventilation cannot be utilized to maintain blood pH at appropriate levels, and following a rapid shift in body temperature water breathers experience an acid-base imbalance. This imbalance is corrected by alterations in bicarbonate excretion (Randall and Cameron, 1973; Cameron, 1976; Romanenko and Kotsar, 1976), which may take hours or days to complete. In Figure 3 a Davenport diagram (Cameron, 1976) depicts the acid-base events in a salmonid following a change from 10°C to 17°C water. 8 .2 4 ° 22 1 I I |/| 7-9 I I I /I 10 C ,2 I I -I 80 PH I I I I I I I I X I FIG. 3 . D a v e n p o r t d i a g r a m showing acid-base events caused by a temperature increase in a salmonid. T h e normal animal acclimated to 10°C has values corresponding to point A, with an O H " / H + ratio of about 33. T h e passive pH change caused by pK temperature-dependence causes a shift to B, with dpH/°C=0.003. Subsequent reduction of HCO,* by exchange lor Cl~ leads to a new steady state at C, which yields the same O H " / H + ratio of 33. Broken lines with numbers show P c ( h isolines. Figure and adapted caption from Cameron (1976). 234 LARRY I. CRAWSHAW ances considerably greater than those produced by rapid alterations of body temperature are tolerated during exercise or manipulation of pH or PC02 within the arteries or in the inspired water (Janssen and Randall, 1975; Daye and Garside, 1975; Wood etal., 1977). The central nervous system sites and modes of sensitivity involved in ectotherm acid-base regulation are unclear, although the theoretical requirements of such a system have been discussed (Reeves, 1976). Stress responses Large, rapid shifts in ambient temperature elicit generalized stress responses. Chowers et al. (1964), found that rapid lowering of the ambient temperature to 0°C elicited cortisol secretion in dogs, as did acute lowering of the preoptic/anterior hypothalamic temperature. Gradual cooling (over 45 minutes) produced no elevation in plasma cortisol. The corticoid stress response in fish is also affected by increasing or elevated temperatures (Strange et al., 1977). Such responses are particularly important in fish and amphibians, since adrenal and pituitary hormones produce alterations in ion permeability and ion transport (Evans, 1975; 1978; Sawyer et al., 1978), as well as generalized effects on metabolism. Long-term acclimation As the acute physiological responses are mobilized to meet the demands of altered body temperature, long-term adjustments are initiated which enable the animal to operate more efficiently at the new body temperature (Hazel and Prosser, 1974). The overall acclimation response involves a complex interaction between physiological, hormonal and cellular processes, and takes place over a period of hours and days. The central nervous system is important in the response (Lagerspetz, 1974), but its exact role remains unclear, as does the nature of the primary inducing stimulus at the cellular level. It is clear that many changes involve "feedback to the genetic material. . ., and subsequently to the protein synthetic system" (Hazel and Prosser, 1974). CONCLUDING REMARKS Dynamic situations, such as rapidly changing temperatures, are difficult to investigate and are therefore studied less than steady state conditions. Most animals, however, regularly experience changing environmental conditions to which they must sense and respond appropriately. The rate of thermal change provides an important input in the elicitation of regulatory responses and is critical in the determination of stressful and lethal conditions. 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