Can Newts Cope with the Heat? Disparate Thermoregulatory Strategies of Two Sympatric Species in Water

Many ectotherms effectively reduce their exposure to low or high environmental temperatures using behavioral thermoregulation. In terrestrial ectotherms, thermoregulatory strategies range from accurate thermoregulation to thermoconformity according to the costs and limits of thermoregulation, while in aquatic taxa the quantification of behavioral thermoregulation have received limited attention. We examined thermoregulation in two sympatric newt species, Ichthyosaura alpestris and Lissotriton vulgaris, exposed to elevated water temperatures under semi-natural conditions. According to a recent theory, we predicted that species for which elevated water temperatures pose a lower thermal quality habitat, would thermoregulate more effectively than species in thermally benign conditions. In the laboratory thermal gradient, L. vulgaris maintained higher body temperatures than I. alpestris. Semi-natural thermal conditions provided better thermal quality of habitat for L. vulgaris than for I. alpestris. Thermoregulatory indices indicated that I. alpestris actively thermoregulated its body temperature, whereas L. vulgaris remained passive to the thermal heterogeneity of aquatic environment. In the face of elevated water temperatures, sympatric newt species employed disparate thermoregulatory strategies according to the species-specific quality of the thermal habitat. Both strategies reduced newt exposure to suboptimal water temperatures with the same accuracy but with or without the costs of thermoregulation. The quantification of behavioral thermoregulation proves to be an important conceptual and methodological tool for thermal ecology studies not only in terrestrial but also in aquatic ectotherms.     

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.     

Thermal ecophysiology of a native and an invasive gecko species in a tropical dry forest of Mexico

For ectotherms, thermal physiology plays a fundamental role in the establishment and success of invasive species in novel areas and, ultimately, in their ecological interactions with native species. Invasive species are assumed to have a greater ability to exploit the thermal environment, higher acclimation capacities, a wider thermal tolerance range, and better relative performance under a range of thermal conditions. Here we compare the thermal ecophysiology of two species that occur in sympatry in a tropical dry forest of the Pacific coast of Mexico, the microendemic species Benedetti's Leaf-toed Gecko (Phyllodactylus benedettii) and the invasive Common House Gecko (Hemidactylus frenatus). We characterized their patterns of thermoregulation, thermoregulatory efficiency, thermal tolerances, and thermal sensitivity of locomotor performance. In addition, we included morphological variables and an index of body condition to evaluate their effects on the thermal sensitivity of locomotor performance in these species. Although the two species had similar selected temperatures and thermal tolerances, they contrasted in their thermoregulatory strategies and thermal sensitivity of locomotor performance. Hemidactylus frenatus had a higher performance than the native species, P. benedettii, which would represent an ecological advantage for the former species. Nevertheless, we suggest that given the spatial and temporal limitations in habitat use of the two species, the probability of agonistic interactions between them is reduced. We recommend exploring additional biotic attributes, such as competition, behavior and niche overlap in order assess the role of alternative factors favoring the success of invasive species.     

The ecological consequences of unpalatable prey: phytoplankton response to nutrient and predator additions

Thermoregulation is thought to be the most important factor influencing habitat selection by terrestrial ectotherms, at least in temperate climates. The cost-benefit model of thermoregulation predicts that ectotherms should invest more in thermoregulation when the costs of doing so are low (when the thermal quality of the habitat is high). However, the extent to which ectotherms vary their thermoregulatory behaviour according to the thermal quality of habitats is currently unknown. We studied the relationship between habitat use and thermoregulation in 53 black rat snakes using temperature-sensitive radio-transmitters. Among the habitats available to black rat snakes, edges had the highest thermal quality, retreat sites and forest were intermediate, and open habitats had the lowest thermal quality. Black rat snakes experienced more favourable body temperatures while in barns (retreat sites) than in edges, and in edges than in forest. During the day, the effectiveness and the extent of thermoregulation by the snakes were equal in barns and forest, but much lower in edges. In fact, black rat snakes selected thermally favourable microhabitats less than their availability while in edges. Therefore, more favourable body temperatures were not necessarily achieved in thermally superior habitats by increased thermoregulation, but simply because favourable temperatures were encountered more often in those habitats. This result is contrary to the central prediction of the cost-benefit model of thermoregulation and we suggest that this model should be modified to put more emphasis on other costs of thermoregulation, such as increased predation risk or lost foraging opportunities.     

Influence of climate on the presence of colour polymorphism in two montane reptile species

The coloration of ectotherms plays an important role in thermoregulation processes. Dark individuals should heat up faster and be able to reach a higher body temperature than light individuals and should therefore have benefits in cool areas. In central Europe, montane local populations of adder (Vipera berus) and asp viper (Vipera aspis) exhibit a varying proportion of melanistic individuals. We tested whether the presence of melanistic V. aspis and V. berus could be explained by climatic conditions. We measured the climatic niche position and breadth of monomorphic (including strictly patterned individuals) and polymorphic local populations, calculated their niche overlap and tested for niche equivalency and similarity. In accordance with expectations, niche overlap between polymorphic local populations of both species is high, and even higher than that of polymorphic versus monomorphic montane local populations of V. aspis, suggesting a predominant role of melanism in determining the niche of ectothermic vertebrates. However, unexpectedly, the niche of polymorphic local populations of both species is narrower than that of monomorphic ones, indicating that colour polymorphism does not always enable the exploitation of a greater variability of resources, at least at the intraspecific level. Overall, our results suggest that melanism might be present only when the thermoregulatory benefit is higher than the cost of predation.     

The effect of environmental gradients on the bed site selection of roe deer (<Emphasis Type="Italic">Capreolus capreolus</Emphasis>)

A wildlife species’ selection of bedding sites is often characterised by strong trade-offs, as habitat quality, predator avoidance and foraging needs should be achieved simultaneously. Human activities often represent major threats in addition. In areas of intensive agriculture, e.g. mowing is one of the main causes of mortality of roe deer (Capreolus capreolus) fawns due their hiding strategy. For a species’ offspring, the selection of bedding sites is particularly crucial and thus, identifying how and when animals use such habitats is important for management. We used a long-term dataset of marked roe deer fawns in Switzerland (1971–2015) to reveal the characteristics of optimal bedding sites within the first two weeks of a fawn’s life in three contrasting landscapes and the potential trade-offs that may occur. We hypothesised that roe deer adjust the selection of bedding sites to current environmental conditions and available habitat to achieve sufficient levels of predator avoidance and thermoregulation necessary for the fawn’s survival, as well as the availability of sufficient food resources for the mother doe. We found that, in general, grassland habitats with medium vegetation height (20–50 cm) and habitats in close proximity to the edge of the forest were favoured to achieve those basic requirements. However, the use of bed site habitats differed between the three contrasting landscapes in dependence of elevation and hence vegetation phenology. Our results provide essential information to reduce mortality rates caused by mowing and improve the reproductive success of this species.     

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 (T_b), operative (T_e) and preferred (T_pref) 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 T_b in the field. This discrepancy could be attributed to the cooler (but more benign) thermal microhabitats that this species occupies.     

Extending the cost-benefit model of thermoregulation: high-temperature environments

The classic cost-benefit model of ectothermic thermoregulation compares energetic costs and benefits, providing a critical framework for understanding this process (Huey and Slatkin 1976 ). It considers the case where environmental temperature (T(e)) is less than the selected temperature of the organism (T(sel)), and it predicts that, to minimize increasing energetic costs of thermoregulation as habitat thermal quality declines, thermoregulatory effort should decrease until the lizard thermoconforms. We extended this model to include the case where T(e) exceeds T(sel), and we redefine costs and benefits in terms of fitness to include effects of body temperature (T(b)) on performance and survival. Our extended model predicts that lizards will increase thermoregulatory effort as habitat thermal quality declines, gaining the fitness benefits of optimal T(b) and maximizing the net benefit of activity. Further, to offset the disproportionately high fitness costs of high T(e) compared with low T(e), we predicted that lizards would thermoregulate more effectively at high values of T(e) than at low ones. We tested our predictions on three sympatric skink species (Carlia rostralis, Carlia rubrigularis, and Carlia storri) in hot savanna woodlands and found that thermoregulatory effort increased as thermal quality declined and that lizards thermoregulated most effectively at high values of T(e).     

Seasonal changes in the thermoregulatory strategies of Rhinella arenarum in the Monte desert, Argentina

We determined and compared the efficiency of thermoregulation of Rhinella arenarum in the Monte desert (Argentina) in two seasons, dry and wet. In the field, we measured body temperatures, micro-habitat temperatures and operative temperatures; while in the laboratory; we measured the selected body temperatures. Our results show a change in the thermoregulatory strategy of R. arenarum that is related to environmental constraints on their thermal niche. R. arenarum has the ability to be plastic and combine two strategies: (i) a moderate thermoregulator in the wet season, where thermal resources are available such that body temperature is maintained within the set points and physiologicial and behavioral processes are optimized; and (ii) a thermoconformer in the dry season where the thermal environment is more homogeneous and there is greater time invested in searching for food.     

The impact of insularity on the thermoregulation of a Mediterranean lizard

The overall biology of ectotherms is strongly affected by the thermal quality of the environment. The particular conditions prevailing on islands have a strong effect on numerous features of animal life. In this study we compared mainland and island populations of the lizard Lacerta trilineata and hypothesized that insularity would affect the thermoregulatory strategy. Continental habitats were of lower thermal quality, experiencing more intense fluctuations and had higher values of operative temperatures. Nevertheless mainland lizards selected for higher body temperatures in the lab and showed more effective thermoregulation during summer than their island peers. Lizards achieved similar body temperatures in the field in both types of habitat, underlining the importance of predation as a potential factor to mainland lizards that failed to reach their higher thermal preferences. Both island and mainland populations of L. trilineata have been adapted to their thermal environment, supporting the labile view on the evolution of thermal physiology for this species.     

Partitioning thermal habitat on a vertical rock,a herculean task

Species occurring in sympatry have to effectively segregate their niche in order to co-exist. In the case of ectotherms in particular, the very important parameter of thermal biology has to be taken into account. Here we investigated the thermoregulatory effectiveness (E) of two endemic Greek lizards (Hellenolacerta graeca and Podarcis peloponnesiacus) that live syntopically on a rocky cliff in the Peloponnese. We presumed that the two species would select different microhabitats, to avoid interspecific competition, and follow a similar thermoregulation pattern as they experience the same conditions. We also expected that E values for both species would differ depending on the season. Overall, we found that the two species had similar E values for each season but differentiated partial thermoregulatory attributes. Though they both occurred in the same types of microhabitat, H. graeca selected higher sites (average 99 cm above ground) than P. peloponnesiacus (average 44 cm). Also, the latter achieved higher preferred temperatures during summer and winter. Finally, the effectiveness of thermoregulation for both species varied interseasonally and received its highest values during summer, in response to the lowest thermal quality that was observed then. Similar studies stress the importance of thermal shifts for ectotherm co-existence.     

Resource selection by an ectothermic predator in a dynamic thermal landscape

Predicting the effects of global climate change on species interactions has remained difficult because there is a spatiotemporal mismatch between regional climate models and microclimates experienced by organisms. We evaluated resource selection in a predominant ectothermic predator using a modeling approach that permitted us to assess the importance of habitat structure and local real‐time air temperatures within the same modeling framework. We radio‐tracked 53 western ratsnakes (Pantherophis obsoletus) from 2010 to 2013 in central Missouri, USA, at study sites where this species has previously been linked to prey population demographics. We used Bayesian discrete choice models within an information theoretic framework to evaluate the seasonal effects of fine‐scale vegetation structure and thermal conditions on ratsnake resource selection. Ratsnake resource selection was influenced most by canopy cover, canopy cover heterogeneity, understory cover, and air temperature heterogeneity. Ratsnakes generally preferred habitats with greater canopy heterogeneity early in the active season, and greater temperature heterogeneity later in the season. This seasonal shift potentially reflects differences in resource requirements and thermoregulation behavior. Predicted patterns of space use indicate that ratsnakes preferentially selected open habitats in spring and early summer and forest–field edges throughout the active season. Our results show that downscaled temperature models can be used to enhance our understanding of animal resource selection at scales that can be addressed by managers. We suggest that conservation of snakes or their prey in a changing climate will require consideration of fine‐scale interactions between local air temperatures and habitat structure.     

Variable history of land use reduces the relationship to specific habitat requirements of a threatened aquatic insect

The hutchinsonian realized niche of a species is the most common tool for selecting the actions needed when restoring habitats and establishing conservation areas of species. However, defining the realized niche of a species is problematic due to variation across spatial and temporal scales. In this study we tested the hypothesis that habitat parameters defining the realized niche of a species can be derived from a regional study and that national changes in land use influence the perception of the realized niche across different landscapes. We described the realized habitat niche of the threatened dragonfly Leucorrhinia pectoralis, in four Estonian landscapes which all have undergone more than 20 years of habitat degradations. We recorded the presence/absence of L. pectoralis and measured 7 habitat variables for 140 lakes and ponds located in one restored and three un-restored landscapes. Lake size and proportion of short riparian vegetation were significantly positive parameters determining the presence of L. pectoralis across landscape types. The species was much more habitat specific in the restored landscape, with larger influence of other habitat parameters. Our data suggest that the realized niche of the species in the un-restored landscapes was constrained by the present-day habitats. The study demonstrate that if a species realized niche is derived from local distribution patterns without incorporating landscape history it can lead to an erroneous niche definition. We show that landscape restoration can provide knowledge on a species’ habitat dependencies before habitat degradation has occurred, provided that restoration mitigation reflects the former landscape characteristics.     

Extreme thermal heterogeneity in structurally complex tropical rain forests

Most terrestrial species on Earth are ectothermic and track temperature at small spatial scales, from sun flecks to cool shaded spots. Current assessments of thermal heterogeneity in complex environments are predominately characterized by ambient temperature. This omission of solar radiation may lead to inaccurate conclusions regarding thermoregulation and distribution of species. We use thermal cameras to gather data on temperature heterogeneity in structurally complex rain forest environments. Using thermographic photographs, we capture the multidimensionality of climate created by vegetation by collecting over 76,000 temperature samples within approximately 1 m² quadrats. The method was tested against three standard methods that record air temperature to determine possible omissions in capturing thermal heterogeneity in four geographic locations—Colombia, Borneo, Madagascar, and Australia. Across all locations, there was greater thermal heterogeneity in surface temperature than captured from ambient temperature technologies. Spatial variability in surface temperature on 1 d was greater than temporal variability of ambient temperature across the entire month, with extreme deviation from ambient temperatures. Importantly, when compared to the lower bounds for optimal performance for five tropical Anolis species, this technology captured thermal regimes that support the thermoregulatory needs of these species, whereas ambient air temperature methods suggested that these species would be in thermal debt. Sampling surface temperature at high resolutions across space in combination with intensive sampling of ambient temperature and informed spatial modeling should improve our understanding of the distribution of ectothermic species living within thermally heterogeneous environments.     

Thermal ecology of two sympatric saxicolous lizards of the genus Phymaturus from the Payunia region (Argentina)

We evaluated the thermal biology of two sympatric saxicolous species of the genus Phymaturus, endemic from the Argentine Payunia region. Taking into account that the distributional range of Phymaturus roigorum (the largest species) is greater than the range of P. payuniae, we evaluated the habitat (type of rocks) used by these species. We recorded body temperature and operative temperatures in different habitats, and we determined the preferred body temperature in the laboratory. We compared the thermal quality of habitats occupied and not occupied by Phymaturus payuniae, and the accuracy and effectiveness of thermoregulation between species.     

Factors affecting the distribution of lumbricids (Oligochaeta) in associations at peat and mineral sites in northern England

Summary The roles of thermal and hydric stress in habitat selection by two species of short-horned grasshoppers was investigated through field and laboratory studies and computer simulation experiments. Psoloessa delicatula was found to possess an elaborate repertoire of thermoregulatory postures and shade seeking behavior. This grasshopper was found in habitats in the shortgrass prairie in which bare patches of ground were common. It was found to regulate its body temperature to a relatively constant level over the course of a sunny day. Eritettix simplex was found in patches of dense vegetation, and its body temperature was usually similar to ambient temperature. During controlled laboratory experiments, E. simplex nymphs lost water rapidly and thus were presumed to be restricted to more mesic environments where desiccation stress is less. A thermal energy budget model was constructed and showed that the habitat selected by P. delicatula would allow behavioral thermoregulation whereas the habitat selected by E. simplex should preclude regulation of body temperature by behavioral means.     

Effects on the thermoregulatory efficiency of two native lizards as a consequence of the habitat modification by the introduction of the exotic tree Acacia longifolia

Habitat modification alters several aspects of the original fauna, among them the opportunity for thermoregulation. Here, we studied the thermal biology of sympatric populations of two lizard species (Liolaemus multimaculatus and Liolaemus wiegmannii) in two different situations; a grassland without trees (natural habitat) and in a grassland plus the exotic tree Acacia longifolia (modified habitat), aiming to assess whether the structural alteration of native Pampean coastal grasslands of Argentina affects the thermal biology of these lizards. Field body temperatures, laboratory preferred temperatures, micro-environmental temperatures, operative temperatures, thermoregulatory efficiency and spatial distribution of each species were analyzed in both habitats. Environmental operative temperature was 0.64 °C lower in the modified habitat (Te=38.39 °C) than in the natural (Te=39.03 °C). Thermoregulatory efficiency (E) of L. wiegmannii was lower in modified sites (E=0.58) than in natural sites (E=0.70). This difference may be because this lizard occupied shaded microhabitats under acacias, with suboptimal thermal features. In contrast, L. multimaculatus in the modified habitat restricted its activity to open microenvironments that retained a similar structure to that of the native habitat, while maintaining high thermoregulatory efficiency in both habitat types (E_modified=0.92; E_natural=0.96). Although these two lizard species are phylogenetically close, they respond differently to human-induced changes in their thermal environments. The introduction of A. longifolia into coastal grasslands for L. wiegmannii in particular, this introduction converts its native habitat into a suboptimal thermal environment.     

Cooler performance breadth in a viviparous skink relative to its oviparous congener

Susceptibility of species to climate change varies depending on many biological and environmental traits, such as reproductive mode and climatic exposure. For example, wider thermal tolerance breadths are associated with more climatically variable habitats and viviparity could be associated with greater vulnerability relative to oviparity. However, few examples exist detailing how such physiological and environmental traits together might shape species thermal performance. In this study we compared the thermal tolerance and performance of two sympatric skink congeners in Hong Kong that differ in habitat use and reproductive mode. The viviparous Sphenomorphus indicus lives on the forest floor while the oviparous Sphenomorphus incognitus occupies stream edges. We quantified the thermal environments in each of these habitats to compare climatic exposure and then calculated thermal safety margins, potential daily activity times within each species’ thermal optimal range, and possible climate change vulnerability. Although we did not detect any differences in thermal tolerance range or thermal environments across habitats, we found cooler performance in S. indicus relative to S. incognitus. Moreover, while optimal activity time increases for both skinks under a warming scenario, we project that the thermal safety margin of S. indicus would narrow to nearly zero, thus losing its buffering capacity to potential extreme climate events in the future. This research is thus consistent with recent studies emphasizing the vulnerability of viviparous reptiles to a warming climate. The results together furthermore highlight the complexity in how environmental and physiological traits at multiple spatial scales structure climate change vulnerability of ectothermic species.     

Thermoregulation of two sympatric species of horned lizards in the Chihuahuan Desert and their local extinction risk

Thermoregulatory studies of ectothermic organisms are an important tool for ecological physiology, evolutionary ecology and behavior, and recently have become central for evaluating and predicting global climate change impacts. Here, we present a novel combination of field, laboratory, and modeling approaches to examine body temperature regulation, habitat thermal quality, and hours of thermal restriction on the activity of two sympatric, aridlands horned lizards (Phrynosoma cornutum and Phrynosoma modestum) at three contrasting Chihuahuan Desert sites in Mexico. Using these physiological data, we estimate local extinction risk under predicted climate change within their current geographical distribution. We followed the Hertz et al. (1993, Am. Nat., 142, 796–818) protocol for evaluating thermoregulation and the Sinervo et al. (2010, Science, 328, 894–899) eco-physiological model of extinction under climatic warming. Thermoregulatory indices suggest that both species thermoregulate effectively despite living in habitats of low thermal quality, although high environmental temperatures restrict the activity period of both species. Based on our measurements, if air temperature rises as predicted by climate models, the extinction model projects that P. cornutum will become locally extinct at 6% of sites by 2050 and 18% by 2080 and P. modestum will become extinct at 32% of sites by 2050 and 60% by 2080. The method we apply, using widely available or readily acquired thermal data, along with the modeling, appeared to identify several unique ecological traits that seemingly exacerbate climate sensitivity of P. modestum.     

Thermally mediated body temperature, water content and aggregation behaviour in the intertidal gastropod Nerita atramentosa

Intertidal organisms are vulnerable to global warming as they already live at, or near to, the upper limit of their thermal tolerance window. The behaviour of ectotherms could, however, dampen their limited physiological abilities to respond to climate change (e.g. drier and warmer environmental conditions) which could substantially increase their survival rates. The behaviour of ectotherms is still mostly overlooked in climate change studies. Here, we investigate the potential of aggregation behaviour to compensate for climate change in an intertidal gastropod species (Nerita atramentosa) in South Australia. We used thermal imaging to investigate (1) the heterogeneity in individual snail water content and body temperature and surrounding substratum temperature on two topographically different habitats (i.e. rock platform and boulders) separated by 250 m at both day- and night-times, (2) the potential relationship between environment temperature (air and substratum) and snail water content and body temperature, and (3) the potential buffering effect of aggregation behaviour on snail water content and body temperature. Both substratum and snail temperature were more heterogeneous at small spatial scales (a few centimetres to a few metres) than between habitats. This reinforces the evidence that mobile intertidal ectotherms could survive locally under warmer conditions if they can locate and move behaviourally in local thermal refuges. N. atramentosa behaviour, water content and body temperature during emersion seem to be related to the thermal stability and local conditions of the habitat occupied. Aggregation behaviour reduces both desiccation and heat stresses but only on the boulder field. Further investigations are required to identify the different behavioural strategies used by ectothermic species to adapt to heat and dehydrating conditions at the habitat level. Ultimately, this information constitutes a fundamental prerequisite to implement conservation management plans for ectothermic species identified as vulnerable in the warming climate.