An application of randomization for detecting evidence of thermoregulation in timber rattlesnakes (Crotalus horridus) from northwest Arkansas

Most reptiles maintain their body temperatures within normal functional ranges through behavioral thermoregulation. Under some circumstances, thermoregulation may be a time-consuming activity, and thermoregulatory needs may impose significant constraints on the activities of ectotherms. A necessary (but not sufficient) condition for demonstrating thermoregulation is a difference between observed body temperature distributions and available operative temperature distributions. We examined operative and body temperature distributions of the timber rattlesnake (Crotalus horridus) for evidence of thermoregulation. Specifically, we compared the distribution of available operative temperatures in the environment to snake body temperatures during August and September. Operative temperatures were measured using 48 physical models that were randomly deployed in the environment and connected to a Campbell CR-21X data logger. Body temperatures (n=1,803) were recorded from 12 radiotagged snakes using temperature-sensitive telemetry. Separate randomization tests were conducted for each hour of day within each month. Actual body temperature distributions differed significantly from operative temperature distributions at most time points considered. Thus, C. horridus exhibits a necessary (but not sufficient) condition for demonstrating thermoregulation. However, unlike some desert ectotherms, we found no compelling evidence for thermal constraints on surface activity. Randomization may prove to be a powerful technique for drawing inferences about thermoregulation without reliance on studies of laboratory thermal preference.     

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.     

Body temperature null distributions in reptiles with nonzero heat capacity: seasonal thermoregulation in the American alligator (Alligator mississippiensis)

Regulation of body temperature may increase fitness of animals by ensuring that biochemical and physiological processes proceed at an optimal rate. The validity of current methods of testing whether or not thermoregulation in reptiles occurs is often limited to very small species that have near zero heat capacity. The aim of this study was to develop a method that allows estimation of body temperature null distributions of large reptiles and to investigate seasonal thermoregulation in the American alligator (Alligator mississippiensis). Continuous body temperature records of wild alligators were obtained from implanted dataloggers in winter (n=7, mass range: 1.6-53.6 kg) and summer (n=7, mass range: 1.9-54.5 kg). Body temperature null distributions were calculated by randomising behavioural postures, thereby randomly altering relative animal surface areas exposed to different avenues of heat transfer. Core body temperatures were predicted by calculations of transient heat transfer by conduction and blood flow. Alligator body temperatures follow regular oscillations during the day. Occasionally, body temperature steadied during the day to fall within a relatively narrow range. Rather than indicating shuttling thermoregulation, however, this pattern could be predicted from random movements. Average daily body temperature increases with body mass in winter but not in summer. Daily amplitudes of body temperature decrease with increasing body mass in summer but not in winter. These patterns result from differential exposure to heat transfer mechanisms at different seasons. In summer, alligators are significantly cooler than predictions for a randomly moving animal, and the reverse is the case in winter. Theoretical predictions show, however, that alligators can be warmer in winter if they maximised their sun exposure. We concluded that alligators may not rely exclusively on regulation of body temperature but that they may also acclimatise biochemically to seasonally changing environmental conditions.     

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.     

Conflicts between courtship and thermoregulation: the thermal ecology of amorous male garter snakes (Thamnophis sirtalis parietalis, colubridae)

Thermoregulatory behavior is an important component of daily activities for many reptiles, especially for small heliothermic (sun-basking) species that inhabit cold climates. However, the relative costs and benefits of thermoregulation depend on numerous factors, such that reptiles may sometimes accord a low priority to precise control of body temperatures. We observed and radio tracked garter snakes (Thamnophis sirtalis parietalis) in central Manitoba during the mating season (spring). Previous studies on this species have documented precise behavioral regulation of body temperatures during summer. In contrast, the courting snakes that we studied in springtime spent little time in overt thermoregulatory behavior. Body temperatures were extremely variable (both in outdoor enclosures and in the field) despite abundant opportunities for more precise thermal control. These small elongate reptiles cool so quickly (relative to the time periods needed for effective courtship) that any benefit to higher body temperatures would be transitory at best. Experiments show that hotter males are no better at obtaining matings or at detecting predators. Thus, male garter snakes concentrate on courtship rather than on basking. In the face of conflicting priorities, reptiles may often forgo precise thermoregulation because its benefits are too low, and its costs too high, compared with alternative behaviors.     

Thermoregulatory behavior and orientation preference in bearded dragons

The regulation of body temperature is a critical function for animals. Although reliant on ambient temperature as a heat source, reptiles, and especially lizards, make use of multiple voluntary and involuntary behaviors to thermoregulate, including postural changes in body orientation, either toward or away from solar sources of heat. This thermal orientation may also result from a thermoregulatory drive to maintain precise control over cranial temperatures or a rostrally-driven sensory bias. The purpose of this work was to examine thermal orientation behavior in adult and neonatal bearded dragons (Pogona vitticeps), to ascertain its prevalence across different life stages within a laboratory situation and its interaction with behavioral thermoregulation. Both adult and neonatal bearded dragons were placed in a thermal gradient and allowed to voluntarily select temperatures for up to 8 h to observe the presence and development of a thermoregulatory orientation preference. Both adult and neonatal dragons displayed a non-random orientation, preferring to face toward a heat source while achieving mean thermal preferences of ~ 33–34 °C. Specifically, adult dragons were more likely to face a heat source when at cooler ambient temperatures and less likely at warmer temperatures, suggesting that orientation behavior counter-balances local selected temperatures but contributes to their thermoregulatory response. Neonates were also more likely to select cooler temperatures when facing a heat source, but required more experience before this orientation behavior emerged. Combined, these results demonstrate the importance of orientation to behavioral thermoregulation in multiple life stages of bearded dragons.     

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.     

Behavioural thermoregulation by the endangered crocodile lizard (Shinisaurus crocodilurus) in captivity

Understanding the factors that may affect behavioural thermoregulation of endangered reptiles is important for their conservation because thermoregulation determines body temperatures and in turn physiological functions of these ectotherms. Here we measured seasonal variation in operative environmental temperature (T_e), body temperature (T_b), and microhabitat use of endangered crocodile lizards (Shinisaurus crocodilurus) from a captive population, within open and shaded enclosures, to understand how they respond to thermally challenging environments. T_e was higher in open enclosures than in shaded enclosures. The T_b of lizards differed between the open and shaded enclosures in summer and autumn, but not in spring. In summer, crocodile lizards stayed in the water to avoid overheating, whereas in autumn, crocodile lizards perched on branches seeking optimal thermal environments. Crocodile lizards showed higher thermoregulatory effectiveness in open enclosures (with low thermal quality) than in shaded enclosures. Our study suggests that the crocodile lizard is capable of behavioural thermoregulation via microhabitat selection, although overall, it is not an effective thermoregulator. Therefore, maintaining diverse thermal environments in natural habitats for behavioural thermoregulation is an essential measure to conserve this endangered species both in the field and captivity.     

Some like it hot: Intra-Population Variation in behavioral Thermoregulation in Color-Polymorphic pygmy Grasshoppers

Ectothermic animals rely on external heat sources and behavioral thermoregulation to control body temperature, and are characterized by possessing physiological and behavioural traits which are temperature dependent. It has therefore been suggested that constraints on the range of body temperatures available to individuals imposed by phenotypic properties, such as coloration, may translate into differential fitness and selection against thermally inferior phenotypes. In this paper, I report an association between thermal preferences and thermal capacity (the ability to warm up when insolated) across different genetically coded color morphs of the pygmy grasshopper Tetrix subulata. Data on behavioral thermoregulation of individuals in a laboratory thermal gradient revealed a preference for higher body temperatures in females than in males, and significant variation among colour morphs in preferred body temperatures in females, but not in males. The variation in females was in perfect accordance with estimates of morph-specific differences in thermal capacity. Thus, dark morphs not only attain higher temperatures when exposed to augmented illumination, but also prefer higher body temperatures, compared to paler morphs. This intra-population divergence probably reflects an underlying variation among colour morphs in temperature optima, and is consistent with the notion that coloration, behaviour and physiology evolve in concert.     

A review of the energetics of pollination biology

Pollination biology is often associated with mutualistic interactions between plants and their animal pollen vectors, with energy rewards as the foundation for co-evolution. Energy is supplied as food (often nectar from flowers) or as heat (in sun-tracking or thermogenic plants). The requirements of pollinators for these resources depend on many factors, including the costs of living, locomotion, thermoregulation and behaviour, all of which are influenced by body size. These requirements are modified by the availability of energy offered by plants and environmental conditions. Endothermic insects, birds and bats are very effective, because they move faster and are more independent of environmental temperatures, than are ectothermic insects, but they are energetically costly for the plant. The body size of endothermic pollinators appears to be influenced by opposing requirements of the animals and plants. Large body size is advantageous for endotherms to retain heat. However, plants select for small body size of endotherms, as energy costs of larger size are not matched by increases in flight speed. If high energy costs of endothermy cannot be met, birds and mammals employ daily torpor, and large insects reduce the frequency of facultative endothermy. Energy uptake can be limited by the time required to absorb the energy or eliminate the excess water that comes with it. It can also be influenced by variations in climate that determine temperature and flowering season.     

Thermoconformity strategy in the freshwater turtle Hydromedusa tectifera (Testudines,Chelidae) in its southern distribution area

Ectotherm species are not capable of generating metabolic heat; therefore, they present different strategies for regulating their body temperatures, ranging from a precise degree of thermoregulation to a passive thermoconformity with ambient temperatures. In reptiles, aerial basking is the most common mechanism for gaining heat. However, among aquatic reptiles, such as freshwater turtles, aquatic basking is also frequent. Hydromedusa tectifera is a turtle of exclusively aquatic and nocturnal habits widely distributed in South America. We studied the relationship between body temperature (Tb) of H. tectifera and its habitat, and explored the effects of sex, life stage and body size and mass on Tb. Fieldwork was conducted in two streams of a mountain area of central Argentina. We recorded cloacal temperature, size and mass of 84 turtles. We also determined individuals’ sex and life stage (adult/juvenile). Regarding ambient temperatures, we measured water temperature on the surface (Tsurf) and at depth of turtle capture (Tdepth) and air temperature. Mean Tb was 18.58 °C (Min = 10.20 °C; Max = 25.70 °C). Tsurf and Tdepth were highly correlated. Multi-model analysis using Akaike criterion indicated that Tb was strongly associated with water temperature, whereas air temperature and body size and mass did not show a significant effect. There was also no effect of turtle sex or life stage on Tb. Our results indicate that H. tectifera is a thermoconformer and eurythermal species. A nocturnal pattern of activity and a fully aquatic lifestyle are suggested as determinant factors.     

Thermoregulatory abilities of Alaskan bees: effects of size, phylogeny and ecology

1. The thermoregulatory capabilities of 18 species of Alaskan bees spanning nearly two orders of magnitude of body mass were measured. Thoracic temperature, measured across the temperature range at which each species forages, was regressed against operative (environmental) temperature to determine bees' abilities to maintain relatively constant thoracic temperatures across a range of operative temperatures (thermoregulatory performance).
2. Previous studies on insect thermoregulation have compared thoracic temperature with ambient air temperature. Operative temperature, which integrates air temperature, solar radiation and effects of wind, was estimated by measuring the temperature of a fresh, dead bee in the field environment. It is suggested that this is a more accurate measure of the thermal environment experienced by the insect and also allows direct comparisons of insects under different microclimate conditions, such as in sun and shade.
3. Simple regression analysis of species and family means, and analysis of phylogenetically based independent contrasts showed thermoregulatory capability, ability to elevate thoracic temperature, and minimum thoracic temperature necessary for initiating flight all increased with body size.
4. Bumble-bees were better thermoregulators than solitary bees primarily as a consequence of their larger body size. However, their thermoregulatory abilities were slightly, but significantly, better than predicted from body size alone, suggesting an added role of pelage and/or physiology. Large solitary bees were better thermoregulators than small solitary bees apparently as a result of body-size differences, with small bees acting as thermal conformers.     

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.     

Amphibian Temperature Regulation Studies in the Field and Laboratory

Studies on thermoregulation in the laboratory and field havecome a long way from the early work done between 1940 and 1960.While some physiological studies on amphibians have progressedat the same rate as those on reptiles, field studies have beenfar behind. Laboratory studies have largely delt with thermalacclimation, evaporative water loss, and thermal and moisturegradient behavior. Field studies, following early summariesof body temperatures of field animals, have stressed behavioralthermoregulation; yet, detailed studies on behavioral thermoregulationin amphibians have been completed for only a handful of species.A few studies have placed behavioral and physiological thermoregulationinto an ecological or energetic framework; these studies arereviewed, and suggestions are made for future work.     

Incubation regimes of cold-climate reptiles: the thermal consequences of nest-site choice, viviparity and maternal basking

Cold-climate reptiles show three kinds of adaptation to provide warmer incubation regimes for their developing embryos: maternal selection of hot nest sites; prolonged uterine retention of eggs; and increased maternal basking during pregnancy. These traits may evolve sequentially as an oviparous lineage invades colder climates. To compare the thermal consequences of these adaptations, I measured microhabitat temperatures of potential nest sites and actual nests of oviparous scincid lizards ( Bassiana duperreyi ), and body temperatures of pregnant and non-pregnant viviparous scincid lizards ( Eulamprus heatwolei ). These comparisons were made at a site where both species occur, but close to the upper elevational limit for oviparous reptiles in south-eastern Australia. Viviparity and maternal basking effort had less effect on mean incubation temperature than did maternal nest-site selection. Eggs retained in utero experienced bimodal rather than unimodal diel thermal distributions, but similar mean incubation temperatures. Often the published literature emphasizes the ability of heliothermic (basking) reptiles to maintain high body temperatures despite unfavourable ambient weather conditions; this putative ability is central to many hypotheses on selective forces for the evolution of viviparity. In cold climates, however, opportunities for maternal thermoregulation to elevate mean body temperatures (and thus, incubation temperatures) above ambient levels may be severely limited. Hence, at least over the broad elevational range in which oviparous and viviparous species live in sympatry, maternal selection of 'hot' nests may be as effective as is viviparity in providing favourable incubation regimes.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 145–155.     

Latitudinal variation in thermal ecology of North American ratsnakes and its implications for the effect of climate warming on snakes

Behavioral thermoregulation is expected to be critical in determining the capacity of reptiles to respond to climate warming and how that response will vary with latitude. We used radio-telemetry to compare behavioral thermoregulation among ratsnake (Elaphe obsoleta) populations in Texas, Illinois, and Ontario, a latitudinal distance of >1500 km. Despite numerous specific differences among populations, overall the thermal ecology was surprisingly similar during the months that snakes in all three populations were active. Preferred temperatures varied only slightly across the snakes’ range, the extent of thermoregulation was similar, and by varying when during the day and season they thermoregulated, snakes in all three populations realized body temperatures within their preferred temperature range 15–20% of the time. The ability to use fine-scale behavioral thermoregulation (i.e., selective use of habitats and microclimates) to a similar extent and achieve similar outcomes across such a wide latitudinal and climatic gradient is made possible by large-scale differences in timing of activity (ratsnakes in Texas switch to nocturnal activity during summer, whereas in Illinois and Ontario activity is exclusively diurnal and hibernation lasts 5–7 months). Modeling indicated that a 3 °C increase in ambient temperature will generally improve thermal conditions for all three populations. Our empirical analyses suggest that the snakes’ ability to respond to climate warming will be determined more by their capacity to adjust when they are active than by changes in the extent of fine-scale behavioral thermoregulation. The ability to adjust timing of activity appears to make many snakes fundamentally different from lizards. As such, the consequences of climate warming may be very different for these two groups of reptiles.     

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.     

Impact of global warming at the range margins: phenotypic plasticity and behavioral thermoregulation will buffer an endemic amphibian

When dispersal is not an option to evade warming temperatures, compensation through behavior, plasticity, or evolutionary adaptation is essential to prevent extinction. In this work, we evaluated whether there is physiological plasticity in the thermal performance curve (TPC) of maximum jumping speed in individuals acclimated to current and projected temperatures and whether there is an opportunity for behavioral thermoregulation in the desert landscape where inhabits the northernmost population of the endemic frog Pleurodema thaul. Our results indicate that individuals acclimated to 20°C and 25°C increased the breath of their TPCs by shifting their upper limits with respect to when they were acclimated at 10°C. In addition, even when dispersal is not possible for this population, the landscape is heterogeneous enough to offer opportunities for behavioral thermoregulation. In particular, under current climatic conditions, behavioral thermoregulation is not compulsory as available operative temperatures are encompassed within the population TPC limits. However, for severe projected temperatures under climate change, behavioral thermoregulation will be required in the sunny patches. In overall, our results suggest that this population of Pleurodema thaul will be able to endure the worst projected scenario of climate warming as it has not only the physiological capacities but also the environmental opportunities to regulate its body temperature behaviorally.     

Modeling body temperature and thermal inertia of large-bodied reptiles: Support for water-filled biophysical models in radiotelemetric studies

Radiotelemetric studies of snakes often use temperature-sensing transmitters to measure the body temperatures associated with microhabitat selection. By combining this information with standard operative temperatures obtained through the use of copper models, researchers are provided with a more detailed view of the thermal environment. Here, we provide data from three independent experiments that support the additional use of water-filled biophysical models to more accurately model the body temperature and thermal inertia of larger-sized free-ranging reptiles. With the use of copper and water-filled biophysical models, researchers can evaluate both standard operative temperatures and simulations of body temperature within different microhabitats, respectively.     

A Face in the Crowd: A Non-Invasive and Cost Effective Photo-Identification Methodology to Understand the Fine Scale Movement of Eastern Water Dragons

Ectothermic vertebrates face many challenges of thermoregulation. Many species rely on behavioral thermoregulation and move within their landscape to maintain homeostasis. Understanding the fine-scale nature of this regulation through tracking techniques can provide a better understanding of the relationships between such species and their dynamic environments. The use of animal tracking and telemetry technology has allowed the extensive collection of such data which has enabled us to better understand the ways animals move within their landscape. However, such technologies do not come without certain costs: they are generally invasive, relatively expensive, can be too heavy for small sized animals and unreliable in certain habitats. This study provides a cost-effective and non-invasive method through photo-identification, to determine fine scale movements of individuals. With our methodology, we have been able to find that male eastern water dragons (Intellagama leuseurii) have home ranges one and a half times larger than those of females. Furthermore, we found intraspecific differences in the size of home ranges depending on the time of the day. Lastly, we found that location mostly influenced females’ home ranges, but not males and discuss why this may be so. Overall, we provide valuable information regarding the ecology of the eastern water dragon, but most importantly demonstrate that non-invasive photo-identification can be successfully applied to the study of reptiles.