The Cardiovascular Control of Heat Exchange: Consequences of Body Size

For blood flow to be an effective agent for the control of heatexchange, it must occur in a region of the body where conductionresistance in the tissues is relatively high, and in an environmentwhere external resistance to heat exchange is relatively low.If either of these conditions is not met, control of heat exchangeby blood flow is not possible. Very small reptiles should notbe able to control heat exchange by blood flow in any environment,unless they control blood flow specifically to appendages. Verylarge reptiles should be able to control heat exchange by bloodflow only under certain conditions, such as in water, very highwinds, or intense radiative heating. Otherwise, they shouldhave little control. An optimum body size should exist for areptile's ability to control heat exchange using blood flow.In air, this optimum body size for alligators appears to beabout 5 kg. Theoretically, the optimum size should be substantiallylarger than 5 kg for reptiles heating and cooling in water.     

Redistribution of blood within the body is important for thermoregulation in an ectothermic vertebrate (<Emphasis Type="Italic">Crocodylus porosus</Emphasis>)

Changes in blood flow are a principal mechanism of thermoregulation in vertebrates. Changes in heart rate will alter blood flow, although multiple demands for limited cardiac output may compromise effective thermoregulation. We tested the hypothesis that regional differences in blood flow during heating and cooling can occur independently from changes in heart rate. We measured heart rate and blood pressure concurrently with blood flow in the crocodile, Crocodylus porosus. We measured changes in blood flow by laser Doppler flowmetry, and by injecting coloured microspheres. All measurements were made under different heat loads, with and without blocking cholinergic and β-adrenergic receptors (autonomic blockade). Heart rates were significantly faster during heating than cooling in the control animals, but not when autonomic receptors were blocked. There were no significant differences in blood flow distribution between the control and autonomic blockade treatments. In both treatments, blood flow was directed to the dorsal skin and muscle and away from the tail and duodenum during heating. When the heat source was switched off, there was a redistribution of blood from the dorsal surface to the duodenum. Blood flow to the leg skin and muscle, and to the liver did not change significantly with thermal state. Blood pressure was significantly higher during the autonomic blockade than during the control. Thermal time constants of heating and cooling were unaffected by the blockade of autonomic receptors. We concluded that animals partially compensated for a lack of differential heart rates during heating and cooling by redistributing blood within the body, and by increasing blood pressure to increase flow. Hence, measures of heart rate alone are insufficient to assess physiological thermoregulation in reptiles.     

Heat transfer in a microvascular network: the effect of heart rate on heating and cooling in reptiles (Pogona barbata and Varanus varius)

Thermally-induced changes in heart rate and blood flow in reptiles are believed to be of selective advantage by allowing animal to exert some control over rates of heating and cooling. This notion has become one of the principal paradigms in reptilian thermal physiology. However, the functional significance of changes in heart rate is unclear, because the effect of heart rate and blood flow on total animal heat transfer is not known. I used heat transfer theory to determine the importance of heat transfer by blood flow relative to conduction. I validated theoretical predictions by comparing them with field data from two species of lizard, bearded dragons (Pogona barbata) and lace monitors (Varanus varius). Heart rates measured in free-ranging lizards in the field were significantly higher during heating than during cooling, and heart rates decreased with body mass. Convective heat transfer by blood flow increased with heart rate. Rates of heat transfer by both blood flow and conduction decreased with mass, but the mass scaling exponents were different. Hence, rate of conductive heat transfer decreased more rapidly with increasing mass than did heat transfer by blood flow, so that the relative importance of blood flow in total animal heat transfer increased with mass. The functional significance of changes in heart rate and, hence, rates of heat transfer, in response to heating and cooling in lizards was quantified. For example, by increasing heart rate when entering a heating environment in the morning, and decreasing heart rate when the environment cools in the evening a Pogona can spend up to 44 min longer per day with body temperature within its preferred range. It was concluded that changes in heart rate in response to heating and cooling confer a selective advantage at least on reptiles of mass similar to that of the study animals (0. 21-5.6 kg).     

Physiological and ecological implications of a simple model of heating and cooling in reptiles

A model of heat exchange in reptiles is used to investigate the role of blood flow in controlling rates of heating/cooling in animals in complex thermal environments. The model suggests an allometry of heating and cooling time constants and of the effects of blood flow on those time constants that accords with published data. The model suggests a simple physical reason for the increased effect of blood flow on time constants in large animals. Two tools (the model and an impulse response method) are presented to allow projection of body temperatures in complex thermal habitats. Application of the model to ecologically important situations suggest that mass, blood flow, and shuttling schedules affect the rate of heating and cooling and the effect of blood flow on the range of body temperatures experienced.     

Changes in heart rate are important for thermoregulation in the varanid lizard Varanus varius

Laboratory studies and a single field study have shown that heart rate in some reptiles is faster during heating than during cooling at any given body temperature. This phenomenon, which has been shown to reflect changes in peripheral blood flow, is shown here to occur in the lizard Varanus varius (lace monitor) in the wild. On a typical clear day, lizards emerged from their shelters in the morning to warm in the sun. Following this, animals were active, moving until they again entered a shelter in the evening. During their period of activity, body temperature was 34-36 degrees C in all six study animals (4.0-5.6 kg), but the animals rarely shuttled between sun and shade exposure. Heart rate during the morning heating period was significantly faster than during the evening cooling period. However, the ratio of heating to cooling heart rate decreased with increasing body temperature, being close to 2 at body temperatures of 22-24 degrees C and decreasing to 1.2-1.3 at body temperatures of 34-36 degrees C. There was a significant decrease in thermal time constants with increasing heart rate during heating and cooling confirming that changes in heart rate are linked to rates of heat exchange.     

Can Reptile Embryos Influence Their Own Rates of Heating and Cooling?

Previous investigations have assumed that embryos lack the capacity of physiological thermoregulation until they are large enough for their own metabolic heat production to influence nest temperatures. Contrary to intuition, reptile embryos may be capable of physiological thermoregulation. In our experiments, egg-sized objects (dead or infertile eggs, water-filled balloons, glass jars) cooled down more rapidly than they heated up, whereas live snake eggs heated more rapidly than they cooled. In a nest with diel thermal fluctuations, that hysteresis could increase the embryo’s effective incubation temperature. The mechanisms for controlling rates of thermal exchange are unclear, but may involve facultative adjustment of blood flow. Heart rates of snake embryos were higher during cooling than during heating, the opposite pattern to that seen in adult reptiles. Our data challenge the view of reptile eggs as thermally passive, and suggest that embryos of reptile species with large eggs can influence their own rates of heating and cooling.     

Integration of autonomic and local mechanisms in regulating cardiovascular responses to heating and cooling in a reptile (<Emphasis Type="Italic">Crocodylus porosus</Emphasis>)

Reptiles change heart rate and blood flow patterns in response to heating and cooling, thereby decreasing the behavioural cost of thermoregulation. We tested the hypothesis that locally produced vasoactive substances, nitric oxide and prostaglandins, mediate the cardiovascular response of reptiles to heat. Heart rate and blood pressure were measured in eight crocodiles (Crocodylus porosus) during heating and cooling and while sequentially inhibiting nitric-oxide synthase and cyclooxygenase enzymes. Heart rate and blood pressure were significantly higher during heating than during cooling in all treatments. Power spectral density of heart rate and blood pressure increased significantly during heating and cooling compared to the preceding period of thermal equilibrium. Spectral density of heart rate in the high frequency band (0.19–0.70 Hz) was significantly greater during cooling in the saline treatment compared to when nitric-oxide synthase and cyclooxygenase enzymes were inhibited. Cross spectral analysis showed that changes in blood pressure preceded heart rate changes at low frequencies (<0.1 Hz) only. We conclude that the autonomic nervous system controls heart rate independently from blood pressure at higher frequencies while blood pressure changes determine heart rate at lower frequencies. Nitric oxide and prostaglandins do not control the characteristic heart rate hysteresis response to heat in C. porosus, although nitric oxide was important in buffering blood pressure against changes in heart rate during cooling, and inhibition caused a compensatory decrease in parasympathetic stimulation of the heart.     

Physiological thermoregulation in a crustacean? Heart rate hysteresis in the freshwater crayfish Cherax destructor

Differential heart rates during heating and cooling (heart rate hysteresis) are an important thermoregulatory mechanism in ectothermic reptiles. We speculate that heart rate hysteresis has evolved alongside vascularisation, and to determine whether this phenomenon occurs in a lineage with vascularised circulatory systems that is phylogenetically distant from reptiles, we measured the response of heart rate to convective heat transfer in the Australian freshwater crayfish, Cherax destructor. Heart rate during convective heating (from 20 to 30 degrees C) was significantly faster than during cooling for any given body temperature. Heart rate declined rapidly immediately following the removal of the heat source, despite only negligible losses in body temperature. This heart rate 'hysteresis' is similar to the pattern reported in many reptiles and, by varying peripheral blood flow, it is presumed to confer thermoregulatory benefits particularly given the thermal sensitivity of many physiological rate functions in crustaceans.     

Regional blood flow in sea turtles: implications for heat exchange in an aquatic ectotherm

Despite substantial knowledge on thermoregulation in reptiles, the mechanisms involved in heat exchange of sea turtles have not been investigated in detail. We studied blood flow in the front flippers of two green turtles, Chelonia mydas, and four loggerhead turtles, Caretta caretta, using Doppler ultrasound to assess the importance of regional blood flow in temperature regulation. Mean blood flow velocity and heart rate were determined for the water temperature at which the turtles were acclimated (19.3 degrees-22.5 degrees C) and for several experimental water temperatures (17 degrees-32 degrees C) to which the turtles were exposed for a short time. Flipper circulation increased with increasing water temperature, whereas during cooling, flipper circulation was greatly reduced. Heart rate was also positively correlated with water temperature; however, there were large variations between individual heart rate responses. Body temperatures, which were additionally determined for the two green turtles and six loggerhead turtles, increased faster during heating than during cooling. Heating rates were positively correlated with the difference between acclimation and experimental temperature and negatively correlated with body mass. Our data suggest that by varying circulation of the front flippers, turtles are capable of either transporting heat quickly into the body or retaining heat inside the body, depending on the prevailing thermal demands.     

Evaluating thermoregulation in reptiles: the fallacy of the inappropriately applied method

Given the importance of heat in most biological processes, studies on thermoregulation have played a major role in understanding the ecology of ectothermic vertebrates. It is, however, difficult to assess whether body temperature is actually regulated, and several techniques have been developed that allow an objective assessment of thermoregulation. Almost all recent studies on reptiles follow a single methodology that, when used correctly, facilitates comparisons between species, climates, and so on. However, the use of operative temperatures in this methodology assumes zero heat capacity of the study animals and is, therefore, appropriate for small animals only. Operative temperatures represent potentially available body temperatures accurately for small animals but can substantially overestimate the ranges of body temperature available to larger animals whose slower rates of heating and cooling mean that they cannot reach equilibrium if they encounter operative temperatures that change rapidly through either space or time. This error may lead to serious misinterpretations of field data. We derive correction factors specific for body mass and rate of movement that can be used to estimate body temperature null distributions of larger reptiles, thereby overcoming this methodological problem.     

Field test of a paradigm: hysteresis of heart rate in thermoregulation by a free-ranging lizard (Pogona barbata).

The discovery that changes in heart rate and blood flow allow some reptiles to heat faster than they cool has become a central paradigm in our understanding of reptilian thermoregulation. However, this hysteresis in heart rate has been demonstrated only in simplistic laboratory heating and cooling trials, leaving its functional significance in free-ranging animals unproven. To test the validity of this paradigm, we measured heart rate and body temperature (Tb) in undisturbed, free-ranging bearded dragons (Pogona barbata), the species in which this phenomenon was first described. Our field data confirmed the paradigm and we found that heart rate during heating usually exceeded heart rate during cooling at any Tb. Importantly, however, we discovered that heart rate was proportionally faster in cool lizards whose Tb was still well below the 'preferred Tb range' compared to lizards whose Tb was already close to it. Similarly, heart rate during cooling was proportionally slower the warmer the lizard and the greater its cooling potential compared to lizards whose Tb was already near minimum operative temperature. Further, we predicted that, if heart rate hysteresis has functional significance, a 'reverse hysteresis' pattern should be observable when lizards risked overheating. This was indeed the case and, during heating on those occasions when Tb reached very high levels (> 40 degrees C), heart rate was significantly lower than heart rate during the immediately following cooling phase. These results demonstrate that physiological control of thermoregulation in reptiles is more complex than has been previously recognized.     

Heat loss regulation: role of appendages and torso in the deer mouse and the white rabbit

Thermal conductance was subdivided into the component conductances of the appendages and torso using a heat transfer analysis for the deer mouse, Peromyscus maniculatus, and the white rabbit, Oryctolagus cuniculus. Our analysis was based on laboratory measurements of skin temperature and respiratory gas exchange made between air temperatures of 8 and 34 degrees C for the deer mouse, and from published data for the white rabbit. Two series conductances to heat transfer for each appendage and torso were evaluated: internal (hin), for blood flow and tissue conduction to the skin surface, and external (hex), for heat loss from the skin surface to the environment. These two series conductances were represented in a single, total conductance (htot). The limit to htot was set by hex and was reached by the torso htot of both animals. The increase in torso htot observed with air temperature for the mouse suggests that a pilomotor change in fur depth occurred. A control of htot below the limit set by hex was achieved by the hin of each appendage. Elevation of mouse thermal conductance (C) resulted from increases in feet, tail, and torso htot. In contrast, the rabbit showed no change in torso htot between 5 and 30 degrees C and ear htot exclusively increased C over these air temperatures. We suggest that the hyperthermia reported for the rabbit at 35 degrees C resulted from C reaching the physical limit set by torso and near hex. Thus the ear alone adjusted rabbit C, whereas the feet, tail, and the torso contributed to the adjustment of mouse C.     

Hysteresis of heart rate and heat exchange of fasting and postprandial savannah monitor lizards (Varanus exanthematicus)

Reptiles are ectothermic, but regulate body temperatures (T(b)) by behavioural and physiological means. Body temperature has profound effects on virtually all physiological functions. It is well known that heating occurs faster than cooling, which seems to correlate with changes in cutaneous perfusion. Increased cutaneous perfusion, and hence elevated cardiac output, during heating is reflected in an increased heart rate (f(H)), and f(H), at a given T(b), is normally higher during heating compared to cooling ('hysteresis of heart rate'). Digestion is associated with an increased metabolic rate. This is associated with an elevated f(H) and many species of reptiles also exhibited a behavioural selection of higher T(b) during digestion. Here, we examine whether digestion affects the rate of heating and cooling as well as the hysteresis of heart rate in savannah monitor lizards (Varanus exanthematicus). Fasting lizards were studied after 5 days of food deprivation while digesting lizards were studied approximately 24 h after ingesting dead mice that equalled 10% of their body mass. Heart rate was measured while T(b) increased from 28 to 38 degrees C under a heat lamp and while T(b) decreased during a subsequent cooling phase. The lizards exhibited hysteresis of heart rate, and heating occurred faster than cooling. Feeding led to an increased f(H) (approximately 20 min(-1) irrespective of T(b)), but did not affect the rate of temperature change during heating or cooling. Therefore, it is likely that the increased blood flows during digestion are distributed exclusively to visceral organs and that the thermal conductance remains unaffected by the elevated metabolic rate during digestion.     

Thermoregulatory responses to thermal stimulation of the preoptic anterior hypothalamus in the red fox (Vulpes vulpes)

The preoptic anterior hypothalamus (POAH) thermoregulatory controller can be characterized by two types of control, an adjustable setpoint temperature and changing POAH thermal sensitivity. Setpoint temperatures for shivering (T_shiver) and panting (T_pant) both increased with decreasing ambient temperature (T_a), and decreased with increasing T_a. The POAH controller is twice as sensitive to heating as to cooling. Metabolic rate (MR) increased during both heating and cooling of the POAH. Resting temperature of the POAH was lower than internal body temperature (T_b) at all temperatures. This indicates the presence of some form of brain cooling mechanism. Decreased T_b during POAH heating was a result of increased heat dissipation, while higher T_b during POAH cooling was a result of increased heat production and reduced heat dissipation. The surface temperature responses indicated that foxes can actively control heat flow from body surface. Such control can be achieved by increased peripheral blood flow and vasodilation during POAH heating, and reduced peripheral blood flow and vasoconstriction during POAH cooling. The observed surface temperature changes indicated that the thermoregulatory vasomotor responses can occur within l min following POAH heating or cooling. Such a degree of regulation can be achieved only by central neural control. Only surface regions covered with relatively short fur are used for heat dissipation. These thermoregulatory effective surface areas account for approximately 33% of the total body surface area, and include the area of the face, dorsal head, nose, pinna, lower legs, and paws.     

Hemodynamic effects of blood loss during a passive response to a stressor in the conscious rabbit

In the conscious rabbit, exposure to an air jet stressor increases arterial pressure, heart rate, and cardiac output. During hemorrhage, air jet exposure extends the blood loss necessary to produce hypotension. It is possible that this enhanced defense of arterial pressure is a general characteristic of stressors. However, some stressors such as oscillation (OSC), although they increase arterial pressure, do not change heart rate or cardiac output. The cardiovascular changes during OSC resemble those seen during freezing behavior. In the present study, our hypothesis was that, unlike air jet, OSC would not affect defense of arterial blood pressure during blood loss. Male New Zealand White rabbits were chronically prepared with arterial and venous catheters and Doppler flow probes. We removed venous blood until mean arterial pressure decreased to 40 mmHg. We repeated the experiment in each rabbit on separate days in the presence and absence (SHAM) of OSC. Compared with SHAM, OSC increased arterial pressure 14 +/- 1 mmHg, central venous pressure 3.3 +/- 0.4 mmHg, and hindquarter blood flow 34 +/- 4% while decreasing mesenteric conductance 32 +/- 3% and not changing heart rate or cardiac output. During normotensive hemorrhage, OSC enhanced hindquarter and renal vasoconstriction. Contrary to our hypothesis, OSC (23.5 +/- 0.6 ml/kg) increased the blood loss necessary to produce hypotension compared with SHAM (16.8 +/- 0.6 ml/kg). In nine rabbits, OSC prevented hypotension even after a blood loss of 27 ml/kg. Thus a stressful stimulus that resulted in cardiovascular changes similar to those seen during freezing behavior enhanced defense of arterial pressure during hemorrhage.     

Cooling rates of living and killed chicken and quail eggs in air and in helium-oxygen gas mixture

1. In a helium atmosphere, heat is dissipated from a surface 3.5 times faster than it is in air. Eggs in a helium-oxygen atmosphere cool only 1.4 times faster than they cool in air. This signifies that internal resistance to heat flow is a significant factor in the cooling rates of eggs. 2. Heat flow occurs inside an egg in two ways: by conduction through the tissues and in flowing blood. Killing an embryo stops the latter, but not the former. Eggs cool more slowly after they have been killed, signifying that blood flow can be an important component in an egg's internal flows of heat. 3. Blood flow should be a relatively more important component of heat flow in large eggs than in small eggs. The difference in conductance between living and killed eggs is larger in 60 g chicken eggs than it is in 10 g quail eggs.     

Effects of exercise and heat stress on regional blood flow in pregnant sheep

Radioactive microspheres were used to measure cardiac output and blood flow to most major tissues, including those in the pregnant uterus, in late-pregnant ewes at rest and during treadmill exercise (approximately 3-fold increase in metabolic rate for 30 min) in thermoneutral (TN) (dry bulb temperature (Tdb) = 13 degrees C, wet bulb temperature (Twb) = 10 degrees C) and mildly hot (MH) (Tdb = 40 degrees C, Twb = 27 degrees C) environments. Exercise caused major increases in blood flow to respiratory muscles, nonrespiratory limb muscles, and adipose tissue, and flow was decreased to some gastrointestinal tissues, spleen, pancreas, and to placental and nonplacental tissues in the pregnant uterus. Heat exposure had relatively little effect on these exercise-induced changes, except that flow was further increased in the respiratory muscles. Results are compared with those of a similar study on nonpregnant sheep in which changes in muscle, skin, and visceral flows during exercise were attenuated by heat exposure. It is suggested that redistribution of blood flow from the pregnant uterus, which in resting ewes took 22% of cardiac output, is a significant buffer against the potentially deleterious effects of combined exercise and heat stress on blood flow to exercising muscles and thermoregulatory tissues.     

Vascular Patterns in Iguanas and Other Squamates: Blood Vessels and Sites of Thermal Exchange

Squamates use the circulatory system to regulate body and head temperatures during both heating and cooling. The flexibility of this system, which possibly exceeds that of endotherms, offers a number of physiological mechanisms to gain or retain heat (e.g., increase peripheral blood flow and heart rate, cooling the head to prolong basking time for the body) as well as to shed heat (modulate peripheral blood flow, expose sites of thermal exchange). Squamates also have the ability to establish and maintain the same head-to-body temperature differential that birds, crocodilians, and mammals demonstrate, but without a discrete rete or other vascular physiological device. Squamates offer important anatomical and phylogenetic evidence for the inference of the blood vessels of dinosaurs and other extinct archosaurs in that they shed light on the basal diapsid condition. Given this basal positioning, squamates likewise inform and constrain the range of physiological thermoregulatory mechanisms that may have been found in Dinosauria. Unfortunately, the literature on squamate vascular anatomy is limited. Cephalic vascular anatomy of green iguanas (Iguana iguana) was investigated using a differential-contrast, dual-vascular injection (DCDVI) technique and high-resolution X-ray microcomputed tomography (μCT). Blood vessels were digitally segmented to create a surface representation of vascular pathways. Known sites of thermal exchange, consisting of the oral, nasal, and orbital regions, were given special attention due to their role in brain and cephalic thermoregulation. Blood vessels to and from sites of thermal exchange were investigated to detect conserved vascular patterns and to assess their ability to deliver cooled blood to the dural venous sinuses. Arteries within sites of thermal exchange were found to deliver blood directly and through collateral pathways. The venous drainage was found to have multiple pathways that could influence neurosensory tissue temperature, as well as pathways that would bypass neurosensory tissues. The orbital region houses a large venous sinus that receives cooled blood from the nasal region. Blood vessels from the nasal region and orbital sinus show anastomotic connections to the dural sinus system, allowing for the direct modulation of brain temperatures. The generality of the vascular patterns discovered in iguanas were assessed by firsthand comparison with other squamates taxa (e.g., via dissection and osteological study) as well as the literature. Similar to extant archosaurs, iguanas and other squamates have highly vascularized sites of thermal exchange that likely support physiological thermoregulation that “fine tunes” temperatures attained through behavioral thermoregulation.     

Effects of temperature on the metabolic response to feeding in Python molurus

As ectothermic vertebrates, reptiles undergo diurnal and seasonal changes in body temperature, which affect many biological functions. In conjunction with a general review regarding the effects of temperature on digestion in reptiles, we describe the effects of various temperatures (20-35 degrees C) on the metabolic response to digestion in the Burmese python (Python molurus). The snakes were fed mice amounting to 20% of their body weight and gas exchange (oxygen uptake and CO(2) production) were measured until digestion had ended and gas exchange returned to fasting levels. Elevated temperature was associated with a faster and larger metabolic increase after ingestion, and the time required to return to fasting levels was markedly longer at low temperature. The factorial increase between fasting oxygen consumption (VO(2)) and maximal VO(2) during digestion was, however, similar at all temperatures studied. Furthermore, the integrated SDA response was not affected by temperature suggesting the costs associated with digestion are temperature-independent. Other studies on reptiles show that digestive efficiency is only marginally affected by temperature and we conclude that selection of higher body temperatures during digestion (postprandial thermophilic response) primarily reduces the time required for digestion.