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.     

Heating and cooling rates of eastern diamondback rattlesnakes,Crotalus adamanteus

• 1.Establishing if and how organisms modulate temperature changes is an important component of understanding their thermal biology.
• 2.We used temperature-sensitive radio-transmitters to monitor heating and cooling rates between 5 and 35 °C of four Crotalus adamanteus in the laboratory.
• 3.We found no difference between heating and cooling rates in C. adamanteus. Additionally, rates of temperature change mirrored those of a biophysical model, further suggesting a lack of physiological thermoregulation.
• 4.Our findings contrast previously published studies that demonstrate active temperature control of similarly sized reptiles and demonstrate a need for more investigations of physiological thermoregulation in reptiles.

     

Modern theoretical and practical problems of homoiothermia and thermoregulation

The adjuncts to the existing determinations of homoiothermia are made on the basis of new data, the principles of temperature adaptation of humans and homoiothermal animals are presented. The main purposes of the thermoregulation system of homoiothermal animals and humans in various temperature excesses are formulated. The arguments are advanced in favor of the fact that in the thermoneutral zone the thermoregulation system goes from the principles of regulating the temperature homeostasis by one or several temperature points of a body to the regulation by the fluctuations of the total heat content of an organism, which increases the sensitivity and the accuracy of the thermoregulation system operation. The physiological mechanisms are described of determining (measuring) the total heat content of a body.     

Model of human/liquid cooling garment interaction for space suit automatic thermal control

The Wissler human thermoregulation model was augmented to incorporate simulation of a space suit thermal control system that includes interaction with a liquid cooled garment (LCG) and ventilation gas flow through the suit. The model was utilized in the design process of an automatic controller intended to maintain thermal neutrality of an exercising subject wearing a liquid cooling garment. An experimental apparatus was designed and built to test the efficacy of specific physiological state measurements to provide feedback data for input to the automatic control algorithm. Control of the coolant inlet temperature to the LCG was based on evaluation of transient physiological parameters that describe the thermal state of the subject, including metabolic rate, skin temperatures, and core temperature. Experimental evaluation of the control algorithm function was accomplished in an environmental chamber under conditions that simulated the thermal environment of a space suit and transient metabolic work loads typical of astronaut extravehicular activity (EVA). The model was also applied to analyze experiments to evaluate performance of the automatic control system in maintaining thermal comfort during extensive transient metabolic profiles for a range of environmental temperatures. Finally, the model was used to predict the efficacy of the LCG thermal controller for providing thermal comfort for a variety of regiments that may be encountered in future space missions. Simulations with the Wissler model accurately predicted the thermal interaction between the subject and LCG for a wide range of metabolic profiles and environmental conditions and matched the function of the automatic temperature controller for inlet cooling water to the LCG.     

Perioperative normothermia depends on intraoperative warming procedure, extent of the surgical intervention and age of the experimental animal

The maintenance of a physiological body temperature during and early after surgical interventions in experimental animals such as rodents is often neglected. Therefore the positive influence of an adequate use of warming blankets (WB) on the rectal body temperature in rats was investigated during two different surgical interventions, with a special focus on possible differences between young adult (2.5+/-0.14 months) and adult animals (9.3+/-0.13 months). Anesthesia was induced with isoflurane short inhalation and maintained with ketamine and domitor intramuscularly. Animals were divided into ten groups according to (a) the age of the animals, (b) the temperature of the WB and (c) the kind of surgical intervention (either an intravenous [i.v.] cannulation of the right external jugular vein or an intra-aortal implantation of a telemetric transmitter or both). Results clearly show that the surface temperature of the WB has a major impact on the perioperative thermoregulation. The rectal body temperature of animals operated on a cooler WB dramatically decreased depending on the age of the rat and also on the extent of the surgical intervention. The opening of the abdominal cavity in older rats resulted in a severe hypothermia: they lost 5.6 degrees C compared to 3.2 degrees C in the young adult rats. The implantation of the i.v. catheter had no serious effect on the thermoregulation. In conclusion, the results clearly show that an adequate perioperative warming system positively influences the postoperative outcome in young adult and most notably in adult rats and thus enables early postoperative experiments without effects on measured parameters.     

MK801 impairs thermoregulation in the heat

The effects of MK801 (dizocilpine), a glutamate NMDA receptor antagonist, on thermoregulation in the heat were studied in awake rats exposed to 40 degrees C ambient temperature until their body core temperature reached 43 degrees C. Under these conditions, MK801-treated rats exhibited enhanced locomotor activity and a steady rise in body core temperature, which reduced the heat exposure duration required to reach 43 degrees C. Since MK801-treated rats also showed increased striatal dopaminergic metabolism at thermoneutrality, the role of dopamine in the MK801-induced impairment of thermoregulation in the heat was determined using co-treatment with SCH23390, a dopamine D1 receptor antagonist. SCH23390 normalized the locomotor activity in the heat without any effect on the heat exposure duration. These results suggest that the MK801-induced impairment of thermoregulation in the heat is related to neither a dopamine metabolism alteration nor a locomotor activity enhancement.     

东亚飞蝗耐高温能力及其体温调节行为

为明确东亚飞蝗Locusta migratoria manilensis的耐高温能力和体温调节行为, 采用高温饲养、提供辐射热源和风力等方法, 对东亚飞蝗各发育期的高温耐受能力、体温（body temperature, Tb）与环境温度（air temperature, Ta）和辐射温度（radiant temperature, Tr）的关系、飞蝗对辐射热的选择行为、体温升高速率以及辐射角度和风力对体温的影响进行了研究。结果表明: 东亚飞蝗44℃下饲养, LT90 最长为326.4 h; 50℃下, LT90可达20.6 h。无辐射热条件下, Tb随Ta的上升而升高, 当Ta升至32℃, 蝗虫出现体温调节行为; Ta以0.5℃/min速率上升时, 出现体温波动的个体数占试虫总数的53.7%, Tb平均波动温差为1.15℃, 平均波动时间为5.2 min, Tb平均波动起始温度为47.2℃, 成虫致死时间略长于若虫。有辐射热条件下, 随笼顶辐射温度的逐渐升高, 飞蝗趋向选择温度相对较低的笼底, 试虫体温调节较无辐射热条件下强; 辐射角度和风力均对飞蝗的体温有显著影响。结果显示东亚飞蝗对高温的耐受能力较强, 并且具有明显的体温调节行为, 可调节体温达到最佳生理状态。     

Comparative effects of temperature and thermoregulation on candidate strains of entomopathogenic fungi for Moroccan locust <Emphasis Type="Italic">Dociostaurus maroccanus</Emphasis> control

Strains IMI 330189 of Metarhizium acridum (Driver & Milner) J.F. Bisch., Rehner & Humber (Hypocreales: Clavicipitaceae) and EABb 90/2-Dm of Beauveria bassiana (Bals.-Criv.) Vuill. (Hypocreales: Cordycipitaceae) are a promising biocontrol tool of Dociostaurus maroccanus (Thunberg) (Orthoptera: Acrididae), although the effects of thermoregulation and Moroccan locust-fever on the infection process of these fungi remain unknown. In vitro experiments, measuring conidial germination and hyphal growth either at constant or at fluctuating temperatures simulating thermoregulatory conditions, indicated that strain IMI 330189 had greater fitness at temperatures above 27 °C and the strain EABb 90/2-Dm was better adapted to the temperature range of 10–25 °C. These effects were mirrored in vivo, where locust thermoregulation caused a marked reduction in the virulence of EABb 90/2-Dm in comparison to no thermoregulation conditions (average survival time: 6.10 vs. 15.83 days; mortality: 100% vs. 73.7%) but only a moderate reduction in the virulence of IMI 330189 (average survival time: 4.57 vs. 8.26 days; mortality: 100% vs. 100%). Thermal gradient experiments revealed that the strain IMI 330189 induced behavioral fever in D. maroccanus (preferred temperatures approximately 4 °C above the uninfected control), although it only led to a slight reduction in virulence. Strain EABb 90/2-Dm did not induce such a clear behavioral response. Under the temperature conditions of the main breeding areas of the Moroccan locust, strain IMI 330189 is likely a better candidate for use in biocontrol, although strain EABb 90/2-Dm could be also a good alternative in more temperate environments either as a stand-alone one or in mixed combinations of the two fungal strains, potentially providing more effective control over a broader range of temperatures.     

Landscape effects on the thermotolerance of carabid beetles and the role of behavioral thermoregulation

Physiological thermotolerance and behavioral thermoregulation are central to seasonal cold adaptation in ectothermic organisms. For species with enhanced mobility, behavioral responses may be of greater importance in the cold stress response. Employing the carabid beetles as a study organism, the current study compared physiological thermotolerance and behavioral thermoregulation in carabid species inhabiting cereal fields in different landscape contexts, from fine grain heterogeneous “complex” landscapes to homogenous “simple” landscapes. Physiological thermotolerance was determined via measurement of the CT_min and chill coma temperature. Behavioral responses to cold temperature exposure were determined employing a purpose built arena, and thoracic temperature measured to estimate the efficacy of the behavior as a form of behavioral thermoregulation. Results revealed an influence of landscape composition on the cold tolerance of carabid beetles, although species differed in their sensitivity to landscape intensification. A reduced effect of landscape on the thermotolerance of larger carabid beetles was observed, thought to be the consequence of greater mobility preventing local acclimation to microclimatic variation along the landscape intensification gradient. Investigation into behavioral thermoregulation of the 3 largest species revealed burrowing behavior to be the main behavioral response to cold stress, acting to significantly raise carabid body temperature. This finding highlights the importance of behavioral thermoregulation as a strategy to evade cold stress. The use of behavioral thermoregulation may negate the need to invest in physiological thermotolerance, further offering explanation for the lack of landscape effect on the physiological thermotolerance of larger carabids.     

Seasonal changes of thermoregulatory efficiency in Djungarian hamsters

In their natural habitat, Djungarian hamsters are faced with dramatic seasonal changes. This requires various morphological and physiological adaptations allowing cope with harsh climate and food shortage, particularly in winter. These seasonal changes are controlled by the photoperiod and can be observed also in the laboratory at room temperature. The aim of the present study was to investigate if the efficiency of thermoregulation also depends on the photoperiod. For this reason, Djungarian hamsters were transferred to short-day conditions (SDC) with 8 h light and 16 h darkness. Two-thirds of the animals were classified as responders showing the typical seasonal changes – decrease of body mass, fur change, testes regression, vagina closing. The total activity per day did not change but, the nocturnal activity was spread over the longer dark time. The body temperature decreased, and the animals showed regular daily torpor. To investigate the thermoregulatory efficiency, body temperatures were correlated with motor activity. The obtained regression coefficients describe formally the effect of motor activity on body temperature, a measure for the efficiency of thermoregulation. In SDC, the coefficients were elevated, both during rest and activity, i.e. the same amount of activity did produce a larger increase in body temperature. Under field conditions, this might be an additional mechanism to compensate the bigger in winter heat loss. Also, the high coefficients may support the increase in body temperature at the end of a torpor phase by a bout of motor activity. The results show that, seasonal changes of thermoregulatory efficiency are an effective accessory way to cope with different temperatures in hamsters’ natural environment.     

Climate dependent heating efficiency in the common lizard

Regulation of body temperature is crucial for optimizing physiological performance in ectotherms but imposes constraints in time and energy. Time and energy spent thermoregulating can be reduced through behavioral (e.g., basking adjustments) or biophysical (e.g., heating rate physiology) means. In a heterogeneous environment, we expect thermoregulation costs to vary according to local, climatic conditions and therefore to drive the evolution of both behavioral and biophysical thermoregulation. To date, there are limited data showing that thermal physiological adjustments have a direct relationship to climatic conditions. In this study, we explored the effect of environmental conditions on heating rates in the common lizard (Zootoca vivipara). We sampled lizards from 10 populations in the Massif Central Mountain range of France and measured whether differences in heating rates of individuals correlated with phenotypic traits (i.e., body condition and dorsal darkness) or abiotic factors (temperature and rainfall). Our results show that heat gain is faster for lizards with a higher body condition, but also for individuals from habitats with higher amount of precipitation. Altogether, they demonstrate that environmentally induced constraints can shape biophysical aspects of thermoregulation.     

Ontogeny of thermoregulation in precocial birds

The aim of this paper is to summarise the results of earlier experiments on thermoregulation and heat balance in birds, to present new results concerning thermoregulation during the perinatal period in precocial embryos and to develop a model of the ontogeny of thermoregulation over the whole lifespan of birds. The ontogeny of thermoregulation in precocial birds is characterised by three phases with different efficiency of the system. In the prenatal phase, all control elements of the thermoregulatory system can function, but the efficiency of the system is low. It is postulated that endothermic reactions during the prenatal period do not have a proximate (immediate), but rather an ultimate influence on the efficiency of thermoregulation. They may support adaptivity to expected environmental conditions and may be involved in epigenetic adaptation processes. During the early postnatal phase, the thermoregulatory system develops and matures. Summit metabolism and resting metabolic rate and their thermoregulatory set points increase. Preferred temperature is significantly different during different behavioural activities. The phase of full-blown homeothermy starts at approximately the 10th day of life. It is characterised by an activation order of thermoregulatory control elements and by secondary chemical thermoregulation. The influence of thermal and non-thermal climatic factors on heat production and heat loss may be described by mathematical models.     

An alternative heat-budget model relevant to heat transfer in fishes and its practical use for detecting their physiological thermoregulation

Previous studies have detected activity-independent fish thermoregulation or conservation mechanisms by applying a mathematical model to body temperature data collected with electronic tags. This model is inadequate, due to its inability to separate quantitatively the effects of physiological thermoregulation from those of physical thermal inertia (the low thermal conductance of the body). In this paper, we have developed an alternative mathematical model that separates these effects. We have then applied it to published electronic tagging data from a large, free-swimming blue shark, Prinoca glauca, to demonstrate physiological thermoregulation. Resultant estimated body-temperature curves indicate that the fish could adjust its whole-body heat-transfer coefficient by changes in arterial blood flow over a range of one order of magnitude. To look at the physical effect on thermoregulation, body temperature for a smaller hypothetical fish was calculated. The estimated temperature was significantly lower than the actual value, indicating that an ectothermic fish like the blue shark cannot achieve physiological thermoregulation without assistance from thermal inertia. In addition, the blue shark returns to cooler depths without recovering its body temperature to the normal surface-temperature level, indicating that this behavior contributes to maximization of the rate of body-temperature recovery. Furthermore, the model indicated that the time for body-temperature recovery is irrelevant to the initial body temperature. Thus, the model made it possible to quantify thermophysiological manipulation. In addition, it was also useful in the comparison of thermoregulatory mechanisms between fishes of different sizes or species.     

中华鳖新孵幼体的热耐受性、体温昼夜变化和运动能力的热依赖性

研究中华鳖新孵幼体的热耐受性、体温及温度对运动能力的影响 .结果表明 ,在干燥和潮湿环境下 ,选择体温分别为 2 8.0℃和 30 .3℃ ;潮湿环境下 ,临界高温和低温分别为 40 .9℃和 7.8℃ .在缺乏温度梯度的热环境中 ,水温对幼鳖体温的影响比气温更直接 ,体温和环境温度的昼夜变化相一致 ,说明幼鳖生理调温能力很弱 .在有温度梯度的热环境中 ,幼鳖能通过行为调温将体温维持到较高且较恒定的水平 ,导致体温昼夜变化不明显 .幼鳖运动能力有显著的热依赖性 ,在一定温度范围内随体温升高而增强 .体温31.5℃时 ,幼鳖的运动表现最好 ,最大续跑距离、单位时间跑动距离和单位时间停顿次数分别为 1.87m、4 92m·min-1和 6 .2次·min-1.体温过高时 ,运动能力下降 .当体温为 33 .0℃时 ,最大续跑距离、单位时间跑动距离和单位时间停顿次数分别为 1.30m、4.2 8m·min-1和 7.7次·min-1.     

On the significance of structural vegetation elements for caterpillar thermoregulation in two peat bog butterflies: Boloria eunomia and B. aquilonaris

Purpose

Temperature profoundly impacts on distribution and habitat-use of organisms. The development of ectothermous caterpillars does not depend on host plant quality only, but also on the availability of suitable thermal conditions. Selection for thermally favorable microclimates (i.e. behavioral thermoregulation) is a primary mechanism of temperature control, and caterpillars can be either (or alternately) temperature conformers (i.e. passively adopting ambient temperature conditions) or thermoregulators (i.e. able to some extent to elevate or decrease their body temperature relative to ambient temperature). Here, we addressed the functional significance of different structural vegetation elements for the behavioral thermoregulation by caterpillars of two butterfly species.

Results

Weather conditions influenced the caterpillar detection probability within host plant patches, indicating that caterpillars can hide and use suitable microclimates provided by vegetation structures to cope with weather variations. This is why we (1) evaluated the heterogeneity in temperature conditions provided by these structures, (2) quantified the influence of ambient temperature and light intensity on caterpillar body temperature, and (3) tested how position on structure, substrate color and exposition influenced caterpillar body temperature. As expected, vegetation structures provided heterogeneous temperature and sun exposition conditions, while caterpillar body temperature was dependent on ambient temperature and light intensity. But body temperature was additionally influenced by the position on vegetation structures, substrate color and exposition.

Conclusions

These results suggest that there is no unique and fixed structure in the vegetation subsuming the best thermal conditions for caterpillars. We argue that a better understanding of the thermal properties of vegetation structures is essential for correctly understanding caterpillar habitat-use and the behavioral mechanisms driving their body thermoregulation. Conceptually this means that thermal conditions should be included in the definition of a species' functional habitat. Practically this may influence the choice of appropriate habitat management for species of conservation concern.     

Physiological thermoregulation in bigeye tuna,Thunnus obesus

Synopsis Although a growing body of evidence has indicated that tuna can thermoregulate and have body temperatures that are decoupled from immediate changes in ambient temperature, demonstrating the extent and time-course of body temperature changes in tuna moving through their natural environments has proved to be elusive. Here we use body temperature data telemetered from free-ranging fish to demonstrate short-latency physiological thermoregulation in bigeye tuna. We used a recently developed modeling system to determine the magnitude and time-course of the whole-body thermal conductivity changes that would result in the body temperature changes observed in fish in the wild. The results indicate rapid, 100 to 1000-fold changes in whole-body thermal conductivity that occur in response to quickly changing ambient temperatures. Coupling this physiological response with behavioral thermoregulation expands the foraging space of these animals by permitting activity in wide ranges of water temperatures and depths.Paper from the International Union of Biological Societies symposium The biology of tunas and billfishes: an examination of life on the knife edge, organized by Richard W. Brill and Kim N. Holland.     

Melatonin and chlorpromazine: thermal selection in the mudpuppy, Necturus maculosus.

Intraperitonel (IP) injections of melatonin (4 mg kg^?1) and chlorpromazine (25 mg kg^?1), which blocks the breakdown of endogenous melatonin, significantly decreased temperatures selected by salamanders in a linear thermal gradient and eliminated the normal diel cycle in behavioral thermoregulation shown by control animals. Both endogenous and exogenous melatonin may play a crucial role in both physiological and behavioral thermoregulation of vertebrates.     

Responses to Rapid Temperature Change in Vertebrate Ectotherms

Vertebrate ectotherms often encounter rapid, large scale changesin body temperature. In this paper, I discuss the direct effectsof changing body temperature on physiological parameters, aswell as corrective responses initiated by the animal. For manybiological functions, mean body temperature provides a usefulmeasure of the thermal effects produced by an altered environmentaltemperature. Under most conditions, the fins and body surfaceof fish are more important avenues of heat exchange than thegills. The local thermal sensitivity of peripheral blood vesselsresults 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, enzymeconformation, ionic and osmotic relationships, spontaneous activitylevels and nervous system function. Compensatory mechanismsinclude behavioral thermoregulation, by which animals seek toavoid stressful thermal environments, and autonomic restorativeresponses such as high temperature panting in reptiles. Waterbreathers may initiate anticipatory responses to minimize arterialoxygen fluctuations during termperature change. The organizationof the central neuronal network underlying the above regulatoryresponses is unclear. Both air and water breathers are ableto initiate compensatory acid-base responses, but the strategiesutilized by the two groups are quite different. Altered bodytemperature initiates long-term acclimation responses, and ifrapid, can also trigger stress responses.     

Are black-box models of thermoregulatory control obsolete? The importance of borrowed knowledge.

Black-box models of thermoregulatory control have gained increasing importance in describing the properties of the biological thermostat and in devising working hypotheses for further experimental analysis. Incorporation of knowledge acquired independently from the systems analysis approach into black-box models of thermoregulation has proven useful in improving their predictive ability. The pieces of "borrowed knowledge" from independent analysis which are currently utilized in devising models of homeothermic thermoregulation comprise: the proportional control property of the biological thermostat, the Sherringtonian principles of synaptic interaction, the multiple input control of thermoregulatory effectors with differential input-effector coupling, the lack of significant thermosensory contribution from the hypothalamus in birds, the existence of warm and cold receptors and the thermal characteristics of their responses, and the Q10-type temperature dependence of temperature signal transmission within the central nervous system. Consideration of these pieces of borrowed knowledge has resulted in black-box models of temperature regulation in which explicit set-point terms are avoided.     

Thermoregulation and microhabitat use in mountain butterflies of the genus Erebia: Importance of fine-scale habitat heterogeneity

Mountain butterflies have evolved efficient thermoregulation strategies enabling their survival in marginal conditions with short flight season and unstable weather. Understanding the importance of their behavioural thermoregulation by habitat use can provide novel information for predicting the fate of alpine Lepidoptera and other insects under ongoing climate change. We studied the link between microhabitat use and thermoregulation in adults of seven species of a butterfly genus Erebia co-occurring in the Austrian Alps. We captured individuals in the field and measured their body temperature in relation to microhabitat and air temperature. We asked whether closely related species regulate their body temperature differently, and if so, what is the effect of behaviour, species traits and individual traits on body to air and body to microhabitat temperature differences. Co-occurring species differed in mean body temperature. These differences were driven by active microhabitat selection by individuals and also by species–specific habitat preferences. Species inhabiting grasslands and rocks utilised warmer microclimates to maintain higher body temperature than woodland species. Under low air temperatures, species of rocky habitats heated up more effectively than species of grasslands and woodlands which allowed them to stay active in colder weather. Species morphology and individual traits play rather minor roles in the thermoregulatory differences; although large species and young individuals maintained higher body temperature. We conclude that diverse microhabitat conditions at small spatial scales probably contribute to sympatric occurrence of closely related species with different thermal demands and that preserving heterogeneous conditions in alpine landscapes might mitigate detrimental consequences of predicted climate change.