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.     

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.     

Thermal conductance and its relation to thermal time constants

A large body of thermoregulation studies exists in which the proper relationship between the physiological variable, thermal conductance, and heating or cooling time is not recognized. This is owing, in part, to conflicting definitions of conductance which either fail to relate to mean heat flow through the body surface or which fail to separate body conductance from that of the environment. Here we analyse ectotherm heating and cooling experiments to relate properly, conductance to thermal time constants and to determine how time constants are scaled according to animal size. It appears that the scaling properties are intimately related to peripheral circulation.Since thermal time constants can be unambiguously defined only for objects of constant thermal conductance we have provided simple illustratons of some phenomena related to temperature-dependent conductors and used these to indicate some of the limits of applicability of the time constant concept and its connection to conductance.Conditions described here do not include large radiant heat exchanges, however, convective heat transport and evaporation are considered. The treatment of evaporation should be quite useful to others.     

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).     

The influence of whole body heating and cooling on the aftercontraction effect in the upper limb muscles

The effect of moderate body cooling and heating on the aftercontraction effect (ACE) was studied in muscles differing in their biomechanical functions. In the biceps muscle of the arm (a flexor muscle), the ACE increased with body cooling and tended to decrease with body heating. Heating of the deltoid muscle (an antigravity abductor) resulted in a higher ACE amplitude and shorter ACE duration, which suggests a complex interaction of the postural mechanisms that regulate the heat emission area and heat production. Cooling had no unambiguous effect on the deltoid muscle ACE. In general, ACE programming in response to thermal factors proved to depend on the biomechanical function of the muscle.     

Thermal time constant estimation in warming and cooling ectotherms

(1) Measurement of physiological control of warming and cooling in reptiles requires calculating the thermal time constant (tau) of the animal. (2) Previously reported methods of estimating tau are sensitive to multiple problems including measurement error in operative environmental temperature and equilibrium body temperature, drift of environmental temperatures, requirements for extremely simple thermal environments, and ill conditioning of the estimation techniques themselves. (3) We propose a physiologically based heat transfer model which is less sensitive to common experimental errors, more numerically robust, and can provide physiologically meaningful estimates of time constants. (4) The method presented here allows time constants to be measured for animals subjected to the traditional step change experiment as well as to shorter periods of warming and cooling such as during shuttling.     

Evaluating thermoregulation in reptiles: an appropriate null model

Established indexes of thermoregulation in ectotherms compare body temperatures of real animals with a null distribution of operative temperatures from a physical or mathematical model with the same size, shape, and color as the actual animal but without mass. These indexes, however, do not account for thermal inertia or the effects of inertia when animals move through thermally heterogeneous environments. Some recent models have incorporated body mass, to account for thermal inertia and the physiological control of warming and cooling rates seen in most reptiles, and other models have incorporated movement through the environment, but none includes all pertinent variables explaining body temperature. We present a new technique for calculating the distribution of body temperatures available to ectotherms that have thermal inertia, random movements, and different rates of warming and cooling. The approach uses a biophysical model of heat exchange in ectotherms and a model of random interaction with thermal environments over the course of a day to create a null distribution of body temperatures that can be used with conventional thermoregulation indexes. This new technique provides an unbiased method for evaluating thermoregulation in large ectotherms that store heat while moving through complex environments, but it can also generate null models for ectotherms of all sizes.     

Regional blood flow changes in response to thermal stimulation of the brain and spinal cord in the Pekin duck

Summary In conscious Pekin ducks, carotid and sciatic blood flows, respiratory rate, core and skin temperatures were measured during selective thermal stimulations of the spinal cord and rostral brain stem in thermoneutral (20 °C) and warm (32 °C) ambient conditions.At thermoneutral ambient temperature selective heating of the spinal cord by 2–3 °C (to 43–44 °C) increased the carotid blood flow by 138% and the sciatic blood flow by 46%. Increase in blood flows was correlated with increased breathing rate and beak and web skin temperatures.Selective cooling of the spinal cord at warm ambient temperatures and panting reduced the blood flow in both arteries and decreased the breathing rate.Heating or cooling of the brain stem showed generally very weak but otherwise similar responses as thermal stimulation of the spinal cord. In one duck out of six there was a marked effect on regional blood flow during brain stimulation.The results show that thermal stimulation of the spinal cord exerts a marked influence on regional blood flow important in thermoregulation, whereas the lower brain stem shows only a weak thermosensitivity, and stimulation caused only small cardiovascular changes of no major consequence in thermoregulation.     

Utility of blood flow to the appendages in physiological control of heat exchange in reptiles

1. A heat transfer model was used to examine the possible sites for the cardiovascular control of heat exchange in ectothermic reptiles. 2. Predicted effects of changes in blood flow on heating and cooling remained constant or increased with mass. 3. Predicted sites at which changes in blood flow strongly affect heating and cooling rates differed between small (⩽1 kg) and large (⩾10 kg) reptiles. 4. In small reptiles (⩽1 kg) blood flow to appendages affected heating and cooling rates but blood flow to the torso had little effect on heat exchange. 5. In large animals (⩾10 kg) changing blood flow to either appendages or torso affected heat exchange; small changes in cardiac output have maximum effects when they occur at the appendages, but larger changes in cardiac output can achieve even larger effects by changing torso blood flow.     

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.     

Physiological control of warming and cooling during simulated shuttling and basking in lizards

Differences in warming and cooling rates in basking lizards have long been thought to be brought about by adjustments in heart rate and blood flow. We examined the physiological control of warming and cooling in Iguana iguana, Sceloporus undulatus, and three species of Cordylus by measuring time constants, heart rate, and superficial capillary blood flow. Previously, techniques have not been available to measure time constants in shuttling animals. Using a combination of rapid measurements of temperature and blood flow and numerically intensive parameter-fitting methods, we measured dominant and subdominant time constants in lizards subjected to periods of both simulated basking and simulated shuttling. Cutaneous blood flow and heart rate were measured using laser Doppler flowmeters. Of the three, only the larger I. iguana measurably altered rates of warming and cooling during basking. During shuttling, none of the species effectively controlled warming and cooling. During both basking and shuttling, blood flow and heart rate tended to change in predicted directions. Superficial blood flow correlated with surface temperature while heart rate correlated more closely with core temperature. Changes in superficial blood flow and heart rate varied relatively independently in I. iguana. The techniques used here provide a better understanding of the ability of these species to control thermoregulation.     

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.     

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.     

Brain thermal inertia,but no evidence for selective brain cooling,in free-ranging western grey kangaroos (<Emphasis Type="Italic">Macropus fuliginosus</Emphasis>)

Marsupials reportedly can implement selective brain cooling despite lacking a carotid rete. We measured brain (hypothalamic) and carotid arterial blood temperatures every 5 min for 5, 17, and 63 days in spring in three free-living western grey kangaroos. Body temperature was highest during the night, and decreased rapidly early in the morning, reaching a nadir at 10:00. The highest body temperatures recorded occurred sporadically in the afternoon, presumably associated with exercise. Hypothalamic temperature consistently exceeded arterial blood temperature, by an average 0.3°C, except during these afternoon events when hypothalamic temperature lagged behind, and was occasionally lower than, the simultaneous arterial blood temperature. The reversal in temperatures resulted from the thermal inertia of the brain; changes in the brain to arterial blood temperature difference were related to the rate of change of arterial blood temperature on both heating and cooling (P < 0.001 for all three kangaroos). We conclude that these data are not evidence for active selective brain cooling in kangaroos. The effect of thermal inertia on brain temperature is larger than might be expected in the grey kangaroo, a discrepancy that we speculate derives from the unique vascular anatomy of the marsupial brain.     

Simulation of hand cooling due to touching cold materials

A simple analytical model has been developed to simulate the cooling of the hands due to touching various types of cold material. The model consisted of a slab of tissue, covered on both sides with skin. The only active mechanism was the skin blood flow. The blood flow was controlled by body core temperature, mean skin temperature, and local hand temperature. The blood flowed along the palm before returning via the back of the hand. The control function was adapted from an earlier study, dealing with feet, but enhanced with a cold induced vasodilatation term. The palm of the hand was touching materials that were specified by conductivity and heat capacity. The hand was initially at a steady-state in a neutral environment and then suddenly grabbed the material. The resulting cooling curves have been compared to data from an experiment including six materials (foam, wood, nylon, steel, aluminium and metal at a constant temperature), three temperatures (-10, 0, and 10 degrees C), two thermal states of the body (neutral and 0.4 degrees C raised), and with and without gloves. There was a fair general agreement between the model and the experiment but the model failed to predict three specific effects: the unequal effect of equal 10 degrees C steps in cold surface temperature on the temperature of the palm of the hand, the cooling effect of nylon, and the rapid drop in back of the hand temperature. Nevertheless the overall regression was 0.88 with a standard deviation between model and experiment of about 2.5 degrees C.     

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.     

Skin and core temperature response to partial- and whole-body heating and cooling

1. Human subjects were exposed to partial- and whole-body heating and cooling in a controlled environmental chamber to quantify physiological and subjective responses to thermal asymmetries and transients.

2. Skin temperatures, core temperature, thermal sensation, and comfort responses were collected for 19 local body parts and for the whole body.

3. Core temperature increased in response to skin cooling and decreased in response to skin heating.

4. Hand and finger temperatures fluctuated significantly when the body was near a neutral thermal state.

5. When using a computer mouse in a cool environment, the skin temperature of the hand using the mouse was observed to be 2–3 °C lower than the unencumbered hand.     

Considerations for assessing maximum critical temperatures in small ectothermic animals: insights from leaf-cutting ants

The thermal limits of individual animals were originally proposed as a link between animal physiology and thermal ecology. Although this link is valid in theory, the evaluation of physiological tolerances involves some problems that are the focus of this study. One rationale was that heating rates shall influence upper critical limits, so that ecological thermal limits need to consider experimental heating rates. In addition, if thermal limits are not surpassed in experiments, subsequent tests of the same individual should yield similar results or produce evidence of hardening. Finally, several non-controlled variables such as time under experimental conditions and procedures may affect results. To analyze these issues we conducted an integrative study of upper critical temperatures in a single species, the ant Atta sexdens rubropiosa, an animal model providing large numbers of individuals of diverse sizes but similar genetic makeup. Our specific aims were to test the 1) influence of heating rates in the experimental evaluation of upper critical temperature, 2) assumptions of absence of physical damage and reproducibility, and 3) sources of variance often overlooked in the thermal-limits literature; and 4) to introduce some experimental approaches that may help researchers to separate physiological and methodological issues. The upper thermal limits were influenced by both heating rates and body mass. In the latter case, the effect was physiological rather than methodological. The critical temperature decreased during subsequent tests performed on the same individual ants, even one week after the initial test. Accordingly, upper thermal limits may have been overestimated by our (and typical) protocols. Heating rates, body mass, procedures independent of temperature and other variables may affect the estimation of upper critical temperatures. Therefore, based on our data, we offer suggestions to enhance the quality of measurements, and offer recommendations to authors aiming to compile and analyze databases from the literature.     

Modulation of arterial baroreflex control of heart rate by skin cooling and heating in humans.

The purpose of this study was to examine the effects of skin cooling and heating on the heart rate (HR) control by the arterial baroreflex in humans. The subjects were 15 healthy men who underwent whole body thermal stress (esophageal temperatures, approximately 36.8 and approximately 37.0 degrees C; mean skin temperatures, approximately 26.4 and approximately 37.7 degrees C, in skin cooling and heating, respectively) produced by a cool or hot water-perfused suit during supine rest. The overall arterial baroreflex sensitivity in the HR control was calculated from spontaneous changes in beat-to-beat arterial pressure and HR during normothermic control and thermal stress periods. The carotid baroreflex sensitivity was evaluated from the maximum slope of the HR response to changes in carotid distending pressure, calculated as mean arterial pressure minus neck pressure. The overall arterial baroreflex sensitivity at existing arterial pressure increased during cooling (-1.32 +/- 0.25 vs. -2.13 +/- 0.20 beats. min(-1). mmHg(-1) in the control and cooling periods, respectively, P < 0.05), whereas it did not change significantly during heating (-1.39 +/- 0. 23 vs. -1.40 +/- 0.15 beats. min(-1). mmHg(-1) in the control and heating periods, respectively). Neither the cool nor heat loadings altered the carotid baroreflex sensitivity in the HR control. These results suggest that the sensitivity of HR control by the extracarotid (presumably aortic) baroreflex was augmented by whole body skin cooling, whereas the sensitivities of HR control by arterial baroreflex remain unchanged during mild whole body heating in humans.     

Physiological mechanisms of thermoregulation in reptiles: a review

The thermal dependence of biochemical reaction rates means that many animals regulate their body temperature so that fluctuations in body temperature are small compared to environmental temperature fluctuations. Thermoregulation is a complex process that involves sensing of the environment, and subsequent processing of the environmental information. We suggest that the physiological mechanisms that facilitate thermoregulation transcend phylogenetic boundaries. Reptiles are primarily used as model organisms for ecological and evolutionary research and, unlike in mammals, the physiological basis of many aspects in thermoregulation remains obscure. Here, we review recent research on regulation of body temperature, thermoreception, body temperature set-points, and cardiovascular control of heating and cooling in reptiles. The aim of this review is to place physiological thermoregulation of reptiles in a wider phylogenetic context. Future research on reptilian thermoregulation should focus on the pathways that connect peripheral sensing to central processing which will ultimately lead to the thermoregulatory response.