Thermoregulation In Lizards Research Articles

Glyphosate-based herbicide (GBH) challenged thermoregulation in lizards (Eremias argus), compensatory warming could mitigate this effect

Chemical pollution and global warming are two major threats to reptiles, and these two factors can interact with each other. Glyphosate have attracted worldwide attention due to their ubiquitous occurrence, yet their impact on reptiles remains unknown. We designed a crossover experiment with different external GBH exposures (control/GBH) x different environmental temperatures (current climate treatment/warmer climate treatment) over 60 days to simulate environmental exposure in the Mongolian Racerunner lizard (Eremias argus). Preferred body temperature and active body temperature data were collected to calculate the accuracy of thermoregulation, while liver detoxification metabolic enzymes, oxidative stress system function, and the non-targeted metabolome of the brain tissue were assessed. Warmer-treated lizards adjusted their physiological levels and behavioral strategies in response to increased ambient temperatures and maintained body temperature homeostasis at moderate thermal perturbations. GBH-treated lizards suffered from oxidative damage to the brain tissue and abnormal histidine metabolism, thus their thermoregulatory accuracy reduced. Interestingly, at elevated ambient temperatures, GBH treatment did not affect on their thermoregulatory, possibly through several temperature-dependent detoxification mechanisms. Importantly, this data suggested that the subtle toxicological effects of GBH may threaten increasingly thermoregulation behavior of E. argus with species-wide repercussions, as climate change and exposure time extension.

Negative effects of the spatial clumping of thermal resources on lizard thermoregulation in a fragmented habitat

In ecosystems threatened by the expansion of croplands, habitat fragmentation and climate change, two of the main extinction drivers, may have thermoregulation-mediated interacting effects on demographic trends of terrestrial ectotherms. We studied the thermal biology of a metapopulation of the widespread Mediterranean lacertid Psammodromus algirus in ten fragments of evergreen or deciduous oak forests interspersed among cereal fields. We obtained thermoregulation statistics (selected temperature range, body and operative temperatures, thermal quality of the habitat, and precision, accuracy, and effectiveness of thermoregulation) that could be compared among fragments and with conspecific populations living in unfragmented habitat. We also measured the selection (use vs. availability) and spatial distribution of sunlit and shaded patches used for behavioral thermoregulation in fragments, and we estimated operative temperatures and thermal habitat quality in the agricultural matrix surrounding the fragments. Variation of the thermal environment was much larger within fragments than among them, and thermoregulation was accurate, precise, and efficient throughout the fragmented landscape; its effectiveness was similar to that of previously studied unfragmented populations. The average distance between sunlit and shaded patches was shorter in deciduous than in evergreen fragments, producing a more clumped distribution of the mosaic of thermal resources. Consequently, in evergreen habitat the cost of thermoregulation was higher, because lizards were more selective in their choice of sunlit sites (i.e. they used sunlit patches closer to shade and refuge than expected at random, and the extent of such selection was larger than at deciduous habitat). Temperatures available in croplands were too high to allow lizard dispersal, at least in the post-breeding season. This result confirms the role of croplands as a thermal barrier that promotes inbreeding and associated fitness losses in isolated fragments, and it forecasts a dark future for populations of forest lizards in agricultural landscapes under the combined effects of habitat fragmentation and global warming.

Lizard thermoregulation revisited after two decades of global warming

Abstract Although the effects of global warming on thermoregulation are usually explored using predictions of climate envelop modelling, such effects should best be analysed empirically, studying the same population with the same methods after a long enough period of temperature rise. We used a 30‐year long database about body temperatures (Tbs) of field‐active Psammodromus algirus lizards inhabiting a well‐conserved temperate open forest, and we focused on the summers of 1997 and 2017 to compare Tbs, environmental operative temperatures (Tes), their proximity to the selected thermal range (Tsel), and the selection of sunlit and shaded patches all along the day. From these data, we estimated the precision (standard deviation of Tbs), accuracy (average distance between Tbs and Tsel) and effectiveness (extent to which Tbs are closer to Tsel than Tes) of thermoregulation. Of the highest 5% of all Tbs in the database, 95% were recorded in 2017, when the adjustment to Tsel was much better for Tbs selected in a laboratory thermogradient than for field Tbs (percentages of Tbs above Tsel of 2% and 52% respectively). In 2017, especially after 12:00 h, the selection of shaded patches (87% of lizards in full shade vs. <1% in full sun) was more intense than in 1997, contributed more to overall thermoregulation, and produced a larger difference between Tes and Tbs. In spite of this, Tbs were lower—and closer to Tsel—in 1997 (when most shaded patches offered favourable thermal opportunities, with Tes within or below Tsel) than in 2017 (when only 33% of full shade Tes, and 8% of all Tes, were within or below Tsel). As a consequence, estimates of the accuracy and effectiveness of thermoregulation decreased over the 20‐year period examined. We conclude that given the low availability of Tes within or below Tsel, lizards cannot longer prevent the rise of their Tbs above Tsel, at least in hot summer days. Thus, the effects of global warming are already hindering the ability of lizards to buffer environmental change by behavioural means, even in temperate forests with a fine‐grained mosaic of sun and shade patches. Read the free Plain Language Summary for this article on the Journal blog.

Thermoregulation comparisons between a threatened native and an invasive lizard species

Lizard thermoregulation is costly and is largely behavioural. Podarcis raffonei, endemic of few islets of the Aeolian archipelago (southern Italy), is one of the most threatened lizards in Europe, its survival being under threat also due to the presence of the congeneric P. siculus, a successful invader characterised by behavioural plasticity and effectiveness and precision at regulating body temperature (Tb). We tested whether thermoregulation behaviour diverges between the two species by analysing (i) the heating rates under a standard thermal condition, and (ii) the temperature at which lizards ended basking (Tfinal) along a thermal gradient. Overall, we found behavioural differences between the two lizards (i.e. P. siculus exhibited lower Tfinal), although both species had comparable heating rates and thermoregulated in the same thermal conditions. The invasive P. siculus had lower Tfinal and, since heating rates were similar between species, it expended less time basking than native P. raffonei. We speculate that the observed thermal ecology differences could provide a selective advantage to P. siculus in the harsh island environment.

Comparative thermal ecophysiology in Pristidactylus scapulatus populations from the Puna region of Argentina

Reptiles are important models for understanding fundamental aspects of physiological ecology and for assessing how environmental change can impact biodiversity. Abiotic factors (micro-environmental temperatures, operative temperatures, thermal quality) may vary geographically along an altitudinal and latitudinal gradient, and therefore the different thermal resources available for thermoregulation also vary. Comparative analyses among populations provide an opportunity to understand how variation in abiotic factors can affect different ecophysiological traits of a species at different geographical points. Our objective was to carry out a comparative study between two populations of Pristidactylus scapulatus in the Puna region of Argentina, providing the first data available on thermal ecophysiology, thermoregulatory efficiency and locomotor performance of the species. We determined field body temperature, micro-environmental temperatures and operative temperatures. In the laboratory, we measured preferred temperatures and calculated the index of thermoregulatory efficiency. In addition, we recorded critical temperature (minimum and maximum) and we estimated the thermal sensitivity of locomotion by measuring sprint speed at different body temperatures; based on these data we calculated the optimal temperature for performance, the optimal performance breadth and thermal safety margin. Air temperatures and operative temperatures were different between sites. However, we only found differences between populations in the minimum critical temperatures, with these being lower at higher latitude. We note that P. scapulatus populations adjust optimal temperatures of performance to field body temperatures and preferred temperatures, which could reduce the costs of thermoregulation in lizards with limited daily activity and who inhabit sites with variable and unpredictable environment temperatures. We conclude that Pristidactylus scapulatus has thermal sensitivity in locomotor performance, is a moderate thermoregulator with respect to the environment and is a eurithermic lizard, which has thermal flexibility in the cold.

Habitat shapes the thermoregulation of Mediterranean lizards introduced to replicate experimental islets.

Both environmental temperatures and spatial heterogeneity can profoundly affect the biology of ectotherms. In lizards, thermoregulation may show high plasticity and may respond to environmental shifts. In the context of global climate change, lizards showing plastic thermoregulatory responses may be favored. In this study, we designed an experiment to evaluate the extent to which lizard thermoregulation responds to introduction to a new environment in a snapshot of time. In 2014, we captured individuals of the Aegean Wall lizard (Podarcis erhardii) from Naxos Island (429.8 km2) and released them onto two small, lizard-free islets, Galiatsos (0.0073 km2) and Kampana (0.004 km2) (Aegean Sea, Greece). In 2017, we returned to the islets and estimated the effectiveness (E), accuracy and precision of thermoregulation measuring operative, preferred (Tpref) and body temperatures. We hypothesized that the three habitats would differ in thermal quality and investigated the extent to which lizards from Naxos demonstrate plasticity when introduced to the novel, islet habitats. Thermal parameters did not differ between Galiatsos and Naxos and this was reflected in the similar E and Tpref. However, lizards from Kampana deviated in all focal traits from Naxos, resulting in higher E and a preference for higher Tpref. In sum, Naxos lizards shifted their thermoregulatory profile due to the idiosyncratic features of their new islet habitat. Our results advocate a high plasticity in lizard thermoregulation and suggest that there is room for effective responses to environmental changes, at least for Podarcis lizards in insular habitats.

From conceptual to computational: Cost and benefits of lizard thermoregulation revisited

A classic paper detailed conceptual analyses of behavioral thermoregulation (Huey and Slatkin, 1976) and has served as the theoretical foundation for hundreds of investigative studies. Most recently, investigators have revisited this theoretical presentation to offer additional interpretation for both heterogeneity and spatial structure of temperature and how it may influence energetic costs (Sears and Angilletta, 2015). Interestingly, this foundational presentation by Huey and Slatkin, over 40 years ago, has never received formal computational analyses to address mathematically the postulates of this conceptual model. Here we use functions that closely mimic those that were described by Huey and Slatkin to provide both a theoretical and computational analysis for the cost and benefits of lizard thermoregulation. We demonstrate both the utility and inherent accuracy of their analyses using a model that was developed conceptually without the use of now readily available computational tools. But contrary to Huey and Slatkin's analyses, we provide a mathematical proof that perfect thermoregulation is never an optimal strategy and show by computational analysis that thermoregulatory strategy (k ) may decrease, not increase, with increasing cost.

Living in sympatry: The effect of habitat partitioning on the thermoregulation of three Mediterranean lizards

The ability for effective, accurate and precise thermoregulation is of paramount importance for ectotherms. Sympatric lizards often partition their niche and select different microhabitats. These microhabitats, however, usually differ in their thermal conditions and lizards have to adapt their thermoregulation behavior accordingly. Here, we evaluated the impact of habitat partitioning on the thermal biology of three syntopic, congeneric lacertids (Podarcis peloponnesiacus, P. tauricus and P. muralis) from central Peloponnese, Greece. We assessed thermoregulation effectiveness (E) using the three standard thermal parameters: body (Tb), operative (Te) and preferred (Tpref) temperatures. We hypothesized that the microhabitats used by each species would differ in thermal quality. We also predicted that all species would effectively thermoregulate, as they inhabit a thermally challenging mountain habitat. As expected, the partition of the habitat had an effect on the thermoregulation of lizards since microhabitats had different thermal qualities. All three species were effective and accurate thermoregulators but one of them achieved smaller E values as a result of the lower Tb in the field. This discrepancy could be attributed to the cooler (but more benign) thermal microhabitats that this species occupies.

Seasonal patterns of body temperature and microhabitat selection in a lacertid lizard

In temperate areas, seasonal changes entail a source of environmental variation potentially important for organisms. Temperate ectotherms may be adapted to the seasonal fluctuations in environmental traits. For lizards, behavioural adaptations regarding microhabitat selection could arise to improve thermoregulation during the different seasons. However, little is still known about which traits influence microhabitat selection of lizards and their adaptation to seasonality. Here we used Podarcis guadarramae to study the role of potential intrinsic (body size, sex, age) and environmental traits (air and substrate temperatures, wind speed, and sunlight) in the seasonal changes of body temperatures and microhabitat selection of lizards. We measured body temperatures of lizards in the same habitat during the four seasons and compared the climatic variables of the microhabitats selected by lizards with the mean climatic conditions available in their habitat. Body temperatures were similar for adult males, adult females, and juveniles within each season, being significantly higher in summer than in the other seasons, and in spring than in winter. The same pattern was found regarding substrate and air temperatures of the selected microhabitats. Wind speed and air temperature did not affect body temperatures, while body length was marginally significant and substrate temperatures and season did affect the body temperatures of lizards. Our results during the whole year support the idea that the seasonality could be the most important factor affecting body temperatures of these temperate species. Regarding microhabitat selection, environmental constraints, as environmental temperatures and wind speed, affected the seasonal changes on behavioural thermoregulation of lizards. This effect was similar between sexes and age classes, and was independent of body size. In addition, importance of sunlight exposure of the selected microhabitats (full sun, filtered sun, or shade) also changed between seasons. Hence, environmental constraints were the main forces driving seasonal changes in microhabitat selection.

Thermal constraints and the influence of reproduction on thermoregulation in a high‐altitude gecko (Quedenfeldtia trachyblepharus)

AbstractTemperature plays a crucial role for ectotherm performance and thus for fitness. Terrestrial ectotherms, including reptiles, regulate their body temperature mainly by behavioural means. At high altitude, however, thermal constraints make precise thermoregulation costly. The cost–benefit model of lizard thermoregulation predicts that thermally challenging environments should favour the evolution of thermoconformity. Yet, several species maintain high and stable body temperatures even in cool environments. We studied the Atlas Day Gecko, Quedenfeldtia trachyblepharus, a cold‐adapted lizard endemic to the High Atlas Mountains of Morocco. We quantified thermoregulation in gravid females, non‐gravid adult females, and adult males during the active season. Geckos thermoregulated during their active season, and thermoregulated with more effectiveness early in the season than late in the season. In the laboratory, the preferred body temperature ranges of gravid females, non‐gravid females, and males were not significantly different. In the field, however, gravid females had smaller deviations from the preferred body temperature and maintained higher body temperatures than males and non‐gravid females. Our study suggests that cold‐adapted reptiles adjust their thermoregulatory behaviour in response to thermal constraints and reproductive status.

Effects of Ectoparasitism on Behavioral Thermoregulation in the Tropical lizards Anolis cybotes (Squamata: Dactyloidae) and Anolis armouri (Squamata: Dactyloidae)

A febrile response, or a raised body temperature in response to infection, has been widely documented in various species of reptiles in laboratory trials. However, whether and how behavioral fever is achieved in nature remains almost entirely unknown. Here, we examine whether two species of lizard in the cybotoid clade of Hispaniolan trunk-ground anoles (Anolis cybotes and Anolis armouri) change their basking behavior in response to infestation by the chigger mite, Eutrombicula alfreddugesi. We examined body temperature and basking behavior in wild populations of A. cybotes and A. armouri from four localities that spanned a 2,000-m elevational transect in the Sierra de Baoruco, Dominican Republic. Although basking rate increased with elevation, we found that it did not correlate with mite load. Body temperature was also unrelated to parasite load. Thus, we found that E. alfreddugesi infestation did not induce behavioral fever in these anoles. We found a strong altitudinal pattern in chigger infestations: Infestations levels were highest in lizards from mid-elevation and dropped dramatically at low and high elevation (particularly in the latter). We discuss possible mechanisms for this altitudinal pattern in chigger infestation and discuss the relationship between infection and behavioral thermoregulation in lizards.

Seasonal changes in thermal biology of Podarcis lilfordi (Squamata, Lacertidae) consistently depend on habitat traits

During spring and summer, we studied the thermal ecology of two populations of the Balearic lizard, Podarcis lilfordi, from two coastal islets of Menorca (Balearic Islands, Spain): Aire and Colom. We calculated the accuracy of thermoregulation, that is, the extent to which body temperatures are close to species' thermal optima, the thermal quality of the habitat as the proximity of operative temperatures to thermal optima and effectiveness of thermoregulation, as the extent to which accuracy is higher than thermal quality of the habitat. We found that seasonality affects thermoregulation differently, depending on the lizard population. Those effects are consistent for all thermal parameters under study. The effects of seasonality were significantly stronger in Aire than in Colom islet. Many factors may be responsible for this different effect of seasonality, from differences on physiological traits to differences in the environmental conditions of the two islets, as their resource availability, predator pressure or habitat structure. Identifying the factors that boost or inhibit those seasonal changes would be important to understand thermoregulation in lizards. Slight changes on two similar populations can lead to great differences in thermal ecology of conspecific ectotherms.

The effect of body size on the thermoregulation of lizards on hot, dry Mediterranean islands

Body size shapes the overall biology of organisms. We assessed the impact of size on temperature regulation in populations of normal-sized and large-bodied insular Mediterranean lizards (Podarcis gaigeae, Lacertidae). We hypothesized that large lizards would achieve higher body temperatures and thermoregulate more effectively than their smaller kin. Large- and small-bodied lizards share the same thermoregulation pattern, achieving similar body temperatures in the field. Large lizards, however, prefer higher set-point temperatures. Lizards in both populations thermoregulate effectively, but large lizards thermoregulated less effectively than normal-sized lizards. The particular conditions at the islet that harbors the large-bodied population (harsh intraspecific competition) seem to account for this pattern.

Termorregulación de lagartos en la formación de profesores de ciencias naturales y educación ambiental

Se estudiaron las propuestas científicas sobre termorregulación en lagartos para integrar un modelo a partir del cual, mediante un cuestionario y análisis de contenido, se analizaron las explicaciones sobre el fenómeno presentadas por profesores de ciencias en formación pertenecientes a un programa de Licenciatura en Ciencias Naturales. Los modelos de los profesores distan del modelo científico. Con base en ello se presenta una propuesta y se argumenta sobre la importancia de hacer objeto de trabajo dicha temática en la formación de esos profesores.

Patterns of body temperatures: Is lizard thermoregulation chaotic?

We surveyed body temperature ( T b) fluctuations of 23 species of thermoregulating lizards (9 families, 305 individuals) for pattern similarities. Here we report that the T b time-series patterns of all species and almost all individuals met both qualitative criteria and quantitative criteria (positive Lyapunov exponent and capacity and/or correlation dimensions less than 5, and Hurst exponent not equal to 0.5) for deterministic chaos. Chaotic thermoregulation appears controlled, but at unpredictable times becomes disturbed and exhibits nonlinear behaviors before returning to control. This chaotic pattern of regulation is common to sufficiently diverse species to suggest that it is likely a primitive lacertilian, and perhaps reptilian, physiological characteristic.

Experimental support for the cost–benefit model of lizard thermoregulation: the effects of predation risk and food supply

Huey and Slatkin's (Q Rev Biol 51:363-384, 1976) cost-benefit model of lizard thermoregulation predicts variation in thermoregulatory strategies (from active thermoregulation to thermoconformity) with respect to the costs and benefits of the thermoregulatory behaviour and the thermal quality of the environment. Although this framework has been widely employed in correlative field studies, experimental tests aiming to evaluate the model are scarce. We conducted laboratory experiments to see whether the common lizard Zootoca vivipara, an active and effective thermoregulator in the field, can alter its thermoregulatory behaviour in response to differences in perceived predation risk and food supply in a constant thermal environment. Predation risk and food supply were represented by chemical cues of a sympatric snake predator and the lizards' food in the laboratory, respectively. We also compared males and postpartum females, which have different preferred or "target" body temperatures. Both sexes thermoregulated actively in all treatments. We detected sex-specific differences in the way lizards adjusted their accuracy of thermoregulation to the treatments: males were less accurate in the predation treatment, while no such effects were detected in females. Neither sex reacted to the food treatment. With regard to the two main types of thermoregulatory behaviour (activity and microhabitat selection), the treatments had no significant effects. However, postpartum females were more active than males in all treatments. Our results further stress that increasing physiological performance by active thermoregulation has high priority in lizard behaviour, but also shows that lizards can indeed shift their accuracy of thermoregulation in response to costs with possible immediate negative fitness effects (i.e. predation-caused mortality).

Thermoregulatory behaviour in Tropidurus torquatus (Squamata, Tropiduridae) from Brazilian coastal populations: an estimate of passive and active thermoregulation in lizards

AbstractGeographical variation in the degree of thermoregulatory behaviour of the lizard Tropidurus torquatus was studied in 10 restinga populations along approximately 1500 km of Brazilian coast. An index of thermoregulation was estimated using the difference between body and environmental (air and substrate) temperatures and the percentage of negative values for these differences (proportion of body temperatures lower than environmental temperatures). In most populations, the lizards primarily used active thermoregulation, through behavioural means, and mainly in relation to substrate temperatures. Along the restingas, the degree of active thermoregulation increased as a function of the increase in the local environmental temperatures along the restingas. Behavioural thermoregulation of T. torquatus helps the lizards to maintain their body temperatures within an optimal range in which to perform their normal daily activities.

Experimental support for the cost–benefit model of lizard thermoregulation

According to Huey and Slatkin’s [Q Rev Biol 51:363–384, 1976] cost–benefit model of behavioural thermoregulation, lizards should adjust their thermoregulatory strategy between active thermoregulation and thermoconformity (no thermoregulation) according to the costs (time and energy spent thermoregulating, exposure to predators), benefits (optimised physiological performance) and thermal quality of environment associated with a given situation. However, Gilchrist’s [Am Nat 146:252–270, 1995] model of thermal specialisation suggests that apparently costly mechanisms of behavioural thermoregulation can greatly increase fitness if the optimal body temperature is achieved. Field studies of ectotherm thermoregulatory strategies under extreme cold conditions and experiments testing the effects of cool environments on thermoregulatory behaviour are surprisingly scarce. We conducted laboratory experiments to test if common lizards Zootoca vivipara (an active thermoregulator in the field) are able to switch between active thermoregulation and thermoconformity in response to different thermal environments. We found that lizards in treatments with an opportunity to reach their preferred body temperature thermoregulated accurately, maintained their level of daily activity and improved their body condition considerably. In contrast, lizards in the treatment where the preferred body temperature could not be reached became thermoconformers, decreased their daily activity (except for gravid females) and did not increase their body condition. Our results show that lizards can indeed change their thermoregulatory strategy but stress that maintaining the preferred body temperature and, thus, optimising the physiological performance have high priority in lizard behaviour.

Using spreadsheets to teach aspects of biology involving mathematical models

Some aspects of biology, for example the Hardy-Weinberg simulation of population genetics or modelling heat flow in lizards, have an undeniable mathematical basis. Students can find the level of mathematical skill required to deal with such concepts to be an insurmountable hurdle to understanding. If not used effectively, spreadsheet models designed to help to overcome such mathematical difficulties present a further hurdle in terms of IT skills. This paper describes examples of how spreadsheet simulations can be designed to reduce the problem of the IT interface obscuring real subject teaching. Two sets of questions designed to help students to meet learning outcomes associated with the Hardy-Weinberg model and with thermoregulation in lizards are presented together with suggested answers. This approach has been successfully used on an introductory genetics course and a control systems course within a Biosciences degree at Canterbury Christ Church University College.

Behavioral sensitivity to corticosterone in juveniles of the wall lizard, Podarcis muralis

Reptiles exposed to stressful conditions respond with increases in plasma levels of corticosterone (CORT). The outcome of such hormonal fluctuations can affect the organism's physiology and behavior; however, relatively few studies in reptiles have progressed past the effects of stress on the plasma levels of CORT. The purpose of this study was to investigate the effects of CORT on lizard behavior. We focused on activity and thermoregulation of juveniles of the wall lizard, Podarcis muralis. Juveniles with experimentally elevated plasma CORT concentrations showed a higher moving rate and spent a greater amount of time moving. They also spent more time being involved in attempts to escape from a terrarium. This enhanced locomotor activity was associated with significant changes in thermoregulatory behavior, as CORT-increased individuals had reduced thermoregulatory activity than the controls. The same pattern of results was obtained in nature and under laboratory conditions. Thus, CORT levels appear to mediate an important trade-off between locomotor activity and thermoregulation. To our knowledge, this is the first time that the effect of CORT on lizard thermoregulation has been examined.