Thermal biology of genus Liolaemus: A phylogenetic approach reveals advantages of the genus to survive climate change

The trends of body temperatures in the field (T_b) and preferred body temperatures in the laboratory (T_pref) of the genus Liolaemus relative to reproductive mode, air temperature (T_air), precipitation, latitude, and elevation were studied using phylogenetic comparative analysis. Results were discussed in the framework of the evolution of thermal physiology and vulnerability to global climate change. Reproductive mode affects T_b but not T_pref. Whereas T_b and T_pref showed a significant association with T_air, there was no relationship with latitude or elevation.     

Is locomotor performance optimised at preferred body temperature? A study of Liolaemus pictus argentinus from northern Patagonia, Argentina

We studied the relationship between locomotor performance and temperature in Liolaemus pictus argentinus, from the Andean-Patagonian forest, Argentina. We determined the running speed in long and sprint runs at four different body temperatures, the panting threshold, and minimum critical temperature. The results are discussed in relation to body temperature in the field and thermal preference in the laboratory (T_pref). L. p. argentinus achieved higher speed in sprint runs than in long runs at all temperatures. In order to know if pregnancy constrains performance in this viviparous species, the differences between pregnant females and the other adults were analysed. Pregnant females were at a disadvantage when running long distances, but in sprint runs they were able to run as efficiently as the rest of the individuals, suggesting that they mainly use sprint runs and this may explain their conspicuous more-withdrawn behaviour. In long runs, the performance optimal temperature for L. p. argentinus (T_o=30.7 °C) was below the 25th percentile for all body temperatures selected in the laboratory (set-point range of T_pref=34.6-37.9 °C), but similar to the mean field body temperature (32.1 °C). However, in sprint runs the T_o (36.3 °C) was within the set-point range of T_pref. The mean panting threshold (42.8 °C) and the mean minimum critical temperature (6.9 °C) were similar to those of other liolaemids. The results are evidence that L. p. argentinus is well-adapted to the temperatures available in their environment and that the species has a T_pref that allows the achievement of maximal locomotor performance in the most frequently used and probably the most important run type, the sprint run.     

Do female newts modify thermoregulatory behavior to manipulate egg size?

Reproductive females manipulate offspring phenotypes by modifying conditions during embryogenesis. In ectotherms, the environmental control over embryogenesis is often realized by changes in maternal thermoregulation during gravidity. To determine if reproduction influences thermoregulatory behavior in species where females lay eggs shortly after fertilization (strict oviparity), we compared preferred body temperatures (T_p) between reproductive (egg-laying) and non-reproductive female newts, Ichthyosaura alpestris. Next, we exposed reproductive females to temperatures mimicking T_p ranges of reproductive and non-reproductive individuals to find out whether the maternally modified thermal regime influences ovum and jelly coat volume, and early cleavage rates at the time of oviposition. In the thermal gradient, reproductive females maintained their body temperatures within a narrower range than non-reproductive individuals. The exposure of ovipositing females to temperatures preferred during their reproductive and non-reproductive period had a negligible influence on egg size and early cleavage rates. We conclude that the modification of maternal thermoregulatory behavior provides a limited opportunity to manipulate egg traits in newts.     

Thermal niche variation among individuals of the poison frog,Oophaga pumilio,in forest and converted habitats

The conversion of natural habitats to human land uses often increases local temperatures, creating novel thermal environments for species. The variable responses of ectotherms to habitat conversion, where some species decline while others persist, can partly be explained by variation among species in their thermal niches. However, few studies have examined thermal niche variation within species and across forest‐land use ecotones, information that could provide clues about the capacity of species to adapt to changing temperatures. Here, we quantify individual‐level variation in thermal traits of the tropical poison frog, Oophaga pumilio, in thermally contrasting habitats. Specifically, we examined local environmental temperatures, field body temperatures (T_b), preferred body temperatures (T_pref), critical thermal maxima (CT_max), and thermal safety margins (TSM) of individuals from warm, converted habitats and cool forests. We found that frogs from converted habitats exhibited greater mean T_b and T_pref than those from forests. In contrast, CT_max and TSM did not differ significantly between habitats. However, CT_max did increase moderately with increasing T_b, suggesting that changes in CT_max may be driven by microscale temperature exposure within habitats rather than by mean habitat conditions. Although O. pumilio exhibited moderate divergence in T_pref, CT_max appears to be less labile between habitats, possibly due to the ability of frogs in converted habitats to maintain their T_b below air temperatures that reach or exceed CT_max. Selective pressures on thermal tolerances may increase, however, with the loss of buffering microhabitats and increased frequency of extreme temperatures expected under future habitat degradation and climate warming. Abstract in Spanish is available with online material.     

Intraspecific alkaloid variation in ladybird eggs and its effects on con- and hetero-specific intraguild predators

Sexual size dimorphism (SSD) is a common phenomenon in animals. In many species females are substantially larger than males. Because body size plays a central role in modulating the body temperature (T _b) of ectotherms, intersexual differences in body size may lead to important intersexual differences in thermoregulation. In addition, because SSD is realized by differences in growth rate and because growth rate is strongly temperature dependent in ectotherms, a conflict between male reproductive behaviour and thermoregulation may affect the expression of SSD. In this study, we investigated the thermal implications of SSD in a reptile exhibiting spectacular female-biased SSD: the northern map turtle (Graptemys geographica). Over three seasons, we collected >150,000 measurements of T _b in free-ranging adult and juvenile northern map turtles using surgically implanted miniature temperature loggers. Northern map turtles exhibited seasonal patterns of thermoregulation typical of reptiles in northern latitudes, but we found that large adult females experienced a lower daily maximum T _b and a narrower daily range of T _b than adult males and small juvenile females. In addition, despite more time spent basking, large adult females were not able to thermoregulate as accurately as small turtles. Our findings strongly suggest that body size limits the ability to thermoregulate accurately in large females. By comparing thermoregulatory patterns between adult males and juvenile females of similar body size, we found no evidence that male reproductive behaviours are an impediment to thermoregulation. We also quantified the thermal significance of basking behaviour. We found, contrary to previous findings, that aerial basking allows northern map turtles to raise their T _b substantially above water temperature, indicating that basking behaviour likely plays an important role in thermoregulation.     

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.     

A test of the thermal coadaptation hypothesis with ultimate measures of fitness in flour beetles

Whole-organism performance of ectotherms depends on body temperature, which is tightly linked to environmental temperatures. Individuals attempting to optimize fitness must thus select appropriate temperatures. The thermal coadaptation hypothesis posits that T_o for traits closely linked to fitness should match temperatures selected by a species (T_set) and should coevolve with T_set. T_o may mismatch T_set if the thermal reaction norm for fitness is asymmetric. In this study, we examined six traits related to fitness in red and in confused flour beetles (Tribolium castaneum and T. confusum, respectively), including longevity, lifetime reproductive success, reproductive rate, and development time at four temperatures between 23 and 32 °C. For reproductive traits, T_o matched T_set whereas for longevity T_o was lower than T_set. Tribolium species have a strongly r-selected life history strategy, therefore reproductive traits are likely more tightly linked to fitness than longevity due to high predation rates at early life stages. We therefore provide support for the thermal coadaptation hypothesis for reproductive traits that are tightly linked to fitness. Our results highlight the importance of knowing the relationships of traits to fitness when studying thermal physiology.     

Energetic constraints on sexual activity in the male edible dormouse (Glis glis)

The aim of this study was to examine to what extent reproductive activity in male edible dormice (Glis glis) might be energetically constrained. Demographic data, morphometric data, and oral body temperature (T _or) measurements were collected in two study areas between 1993 and 2002 in southwest Germany and combined with subcutaneous body temperature (T _sc) registrations of captive dormice. T _sc measurements were collected directly after emergence from hibernation (June) until the end of the mating season (July). Wild edible dormice showed strong fluctuations in their reproductive output between years. Not all males were sexually active each year and the number of litters born was positively correlated with the number of sexually active males, which suggests that sexual activity in males is constrained and in turn limits reproductive success. A comparison of the T _or of sexually quiescent and active males revealed that sexually quiescent males had significantly lower T _or (median: 28.8°C; 25/75% quartiles: 16.4/31.0; n=31) than sexually active males (median: 34.2°C; 25/75% quartiles: 32.0/35.6; n=156). Body condition of sexually active and quiescent males was not different after emergence from hibernation. However, sexually active males showed a significant reduction in their body condition between June and July, the time of mating, while body condition of sexually quiescent males remained constant. Continuous T _sc registrations in captive sexually active male dormice showed strong circadian T _sc fluctuations. Even though daily torpor bouts with T _sc below 20°C occurred in these males, most of the time T _sc fluctuated above 30°C, which is known as the critical body temperature threshold above which testes maturation can take place in this species. These results demonstrate that male dormice incur high costs due to sexual activity and that thermoregulation is determined by a trade-off between energetic savings and reproductive activity.     

Thermal biology of Liolaemus lizards from the high Andes: Being efficient despite adversity

We studied the efficiency of thermoregulation in four high elevation Liolaemus species in the Andes of Salta, Argentina; Liolaemus irregularis, Liolaemus multicolor, Liolaemus albiceps and Liolaemus yanalcu. One of the species, L. irregularis, shows a broad distribution being in allopatry in some localities and in sympatry with L. albiceps, L. multicolor and L. yanalcu at different sites. Together with this variation in assemblages, the degree of phylogenetic relatedness is different with L. irregularis being most closely related to L. albiceps than to the other two species (L. multicolor and L. yanalcu). We measured body (T_b), microenvironmental (T_a, T_s), and operative temperatures (T_e) in the field, and preferred body temperature (T_pref) in laboratory for each one of the species of assemblages. Three out of the four species showed a high thermoregulatory efficiency except for L. yanalcu, a moderate thermoregulator. The species studied here show high T_b in the field compared to most of the recorded Liolaemus species. However, the T_pref values were similar to other Liolaemus species. No evidence of thermal niche segregation between species in sympatry was observed. Our results suggest that the species studied here, despite living at high elevation and harsh climatic conditions are able to behaviorally or physiologically thermoregulate to achieve T_bs close to their T_pref, probably because of low predation risk and perhaps low levels of competition.     

Thermal Preference of the Bush Cricket <Emphasis Type="Italic">Isophya rizeensis</Emphasis>; Testing the Effect of Countergradient Selection

Thermal preference is one of the most crucial components of behavioral thermoregulation in ectotherms, and documenting the adaptation of thermal preference carries great importance for studying the evolution of thermal biology. However there are not many studies focusing on the adaptation of thermal preference in elevational and latitudinal gradients. Isophya rizeensis is a color polymorphic bush cricket species endemic to the mountainous region of northeastern Turkey. Populations of this species are distributed in a wide elevational range between 350 and 2300 m. In this study, we hypothesized that the thermal preference of Isophya rizeensis might follow a countergradient variation where crickets from higher altitudes have higher temperature preferences compared to crickets from lower altitudes. To test this hypothesis, thermal preference values (T _pref ) of crickets from three altitudes groups (low, middle and high) were measured with a thermal gradient experiment. Additionally, body temperatures (T _b ) and environmental temperatures (T _a ) were measured in field. Deviation values of T _b and T _a from T _pref were calculated to investigate the extent of thermoregulation. As Isophya rizeensis is color polymorphic species where morphology pattern changes from lighter to darker types with increasing altitude we also tested whether coloration has any effect on temperature excess (T _ex ) and thermoregulation. Thermal preference values did not differ significantly between three groups and also colouration does not influence the extent of thermoregulation in this species. These results indicate that there is not sufficient evidence for the existence of a countergradient selection related with thermal behavior. However, the deviation of body (D _b ) and environmental (D _a ) temperatures suggest that at higher altitudes thermoregulation might be more efficient than lower altitudes.     

Alternative male reproductive tactics in a natural population of prairie voles <Emphasis Type="Italic">Microtus ochrogaster</Emphasis>

Alternative reproductive tactics have been described in male mammals, but little information exists regarding fitness benefits and whether males change tactics. Adult male prairie voles Microtus ochrogaster (Wagner, 1842) display alternative tactics described as resident and wanderer. Enclosure studies provide conflicting data concerning the relative success of each tactic and whether males display one tactic throughout adulthood. To characterize further residents and wanderers in this species, we examined data collected during 5 years of monitoring a natural population in Illinois, USA. We found that during the breeding period, wandering males survived longer, moved longer distances, and were more likely than residents to have scrotal testes. During the nonbreeding period, wandering and resident males differed only in whether or not they established residency. Data on sources and fates of resident and wandering males revealed that a substantial proportion of males switched tactics. Our estimate of the reproductive contribution of wandering males to the population, which is based on the premise that wandering males typically mate with single females, suggests that wanderers contribute 34–38% of young recruited during March through October and 4–12% in November, when single females are less common. Parentage studies in natural populations are necessary to test our estimates.     

Preferred ambient temperature for old and young men in summer and winter

To investigate the effects of age on thermal sensitivity, preferred ambient temperature (T _pref) was compared between old (71–76 years) and young (21–30 years) groups, each consisting of six male subjects in summer and winter. The air temperature (T _a) was set at either 20° C or 40° C at commencement. The subject was directed to adjust theT _a for 45 min by manipulating a remote control switch to the level at which he felt most comfortable. In the older group, theT _pref was significantly lower in trials starting at 20° C than that starting at 40° C in summer. The fluctuation ofT _pref (temperature difference between maximum and minimumT _a during the last 10 min) was significantly wider in the older group in both summer and winter. Repetition of the same experiment on each subject showed a poorer reproducibility ofT _pref in the older group than in the younger group in summer. Tympanic and esophageal temperatures of the older group kept falling throughout the trial starting at 20° C in summer. These results suggest that thermal sensitivity is decreased with advancing age and that thermal perception in the elderly, especially to cold, is less sensitive in summer.     

Thermal relationships between body temperature and environment conditions set upper distributional limits on oviparous species

We determined the thermal biology of the oviparous Liolaemus boulengeri and the viviparous Liolaemus lineomaculatus populations localised at high and low latitude sites in Patagonia, Argentina. We present data of body temperatures in the field (T_b) and preferred temperature in the laboratory (T_pref), micro-environmental and operative temperatures and the effectiveness of thermoregulation. Liolaemus boulengeri and L. lineomaculatus choose different heat sources for active selection of suitable thermal micro-environments for thermoregulation, and the oviparous L. boulengeri is a more effective thermoregulator (E=0.55) than the viviparous L. lineomaculatus (E=0.43). Even when L. boulengeri is a better thermoregulator and both species show identical timing in the reproductive cycles, there are constraint factors that impose limitations on the southernmost distribution of the oviparous L. boulengeri.     

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.     

Locomotor and energetic consequences of behavioral thermoregulation in the sanguivorous leech Hirudo verbana

Medicinal leeches (Hirudo verbana) thermoregulate with respect to their sanguivorous feeding behavior. Immediate postprandial preferences are for warmer than their initial acclimation temperature (T_a, 21 °C, Petersen et al. 2011), while unfed leeches have a lower preferred temperature (T_pref, 12.5 °C). This may reduce energy expenditure and defer starvation if feeding opportunities are limited. Energetic benefits may have an associated cost if low temperatures reduce mobility and the ability to locate further hosts. These costs could be limited if mobility is unimpaired at low temperatures, or if acclimation can restore locomotor performance to the levels at T_a. The transition from T_a to the unfed T_pref significantly reduced speed and propulsive cycle frequency during swimming, and extension and retraction rates during crawling. Aerobic metabolic rate was also reduced from 0.20±0.03 W kg⁻¹ at T_a to 0.10±0.03 W kg⁻¹ at T_pref. The Q₁₀ values of 1.7–2.9 for energetic and swimming parameters indicate a substantial temperature effect, although part of the decline in swimming performance can be attributed to temperature-related changes in water viscosity. 6 weeks at T_a resulted in no detectable acclimation in locomotor performance or aerobic metabolism. The energetic savings associated with a lower T_pref in unfed leeches effectively doubled the estimated time until depletion of energy reserves. Given that some mobility is still retained at T_pref, and that acclimation is in itself costly, the energetic benefits of selecting cooler temperatures between feedings may outweigh the costs associated with reduced locomotor performance.     

Diel and seasonal variations in the thermal biology of San Cristobal Lava Lizards (Microlophus bivittatus)

Thermal biology, and therefore energy acquisition and survival, of ectotherms can be affected by diel and seasonal patterns of environmental temperatures. Galápagos Lava Lizards live in seasonal environments that are characterized by a warm and wet period when reproductive activity is maximal, and cooler and drier period. With the use of radiotelemetric techniques to record lizard surface temperatures (T_s), we studied the thermal ecology of the San Cristóbal Lava Lizard (Microlophus bivittatus) during both the warm and cool seasons over two years. During the diel activity period and when operative temperatures exceeded T_set-min, at least on rock faces without canopy, 52% or less of the T_s observations fell within the laboratory-determined T_set range (36–40 °C). Therefore, lizards may have avoided very warm midday temperatures in shaded microhabitats and the lag times in changes in T_s values occurred as operative temperatures rose rapidly during late morning warming phase. Lizards effectively thermoregulated during a year with moderate warm season temperatures and during a cool season that was unseasonably warm. In contrast, lizards less effectively thermoregulated during the warmest and coolest years of the study. We did not detect intersexual differences in thermoregulation although males may thermoregulate less effectively than do females during the cool season although we were unable to detect significant differences using our nonparametric statistical techniques.     

Thermal constraints on daily patterns of aggregation and density along an intertidal gradient in the periwinkle Echinolittorina peruviana

Variations in environmental temperature have both direct and indirect effects that affect organisms at levels ranging from intra-cellular physiological processes to ecological patterns. These variations are especially important for intertidal marine ectotherms such as littorinids since they alternate between periods of immersion in seawater, and must also experience long periods of emersion. In central Chile, Echinolittorina peruviana is one of the most conspicuous species on rocky intertidal shores, occurring at high tidal levels and in the splash zone. The species is known to resist direct exposure to the sun for long periods, although juveniles tend to be restricted to protected microhabitats. Adults show seasonal variations in abundance and vertical distribution and may form aggregations that have been shown to help reduce water loss and body temperature. In this study, we evaluate the relationship between daily thermal variations throughout the vertical distribution of this species and how these affect the patterns of density and aggregation. Our results suggest that one of the leading determinants of the spatio-temporal variation of density in E. peruviana may be operative temperature (T_O: the amount of stored heat resulting from the balance between heat fluxes into and out of the body, measured with taxidermic mounts mimicking heat transfer properties of the snail). T_O showed a strong negative relationship with density and a strong positive relationship with aggregation in the highest intertidal level monitored. The strength of these relationships decreased in importance at lower levels. While T_O alone cannot explain the abundance of E. peruviana throughout its range of distribution, our results show that it does have a strong influence that should be considered in addition to other ecological factors affecting the density of intertidal littorinids.     

Could the intrinsic rate of increase represent the fitness in terrestrial ectotherms?

The intrinsic rate of increase (r_m) has been considered as an important indicator of fitness in terrestrial ectotherms since long. It is actually an equivalent to the instantaneous growth rate of the exponential equation for describing the density-independent population growth. In terrestrial ectotherms, r_m has been demonstrated to be temperature-dependent. The temperature at which r_m was maximal, was considered to be the “optimal” temperature for fitness in Amarasekare and Savage (2012), but this definition needs further analysis. Only r_m cannot provide thorough representation of fitness. Because body size can affect the competitive abilities in many terrestrial ectotherms, both population size and body size should be considered in measuring the fitness of ectotherms. The rule of “bigger is better” requires relatively low temperature to increase in body size, whereas relatively high temperature is required for a rapid increase in population size. Thus, there is presumably a trade-off in temperature for adjusting individual body size and population size to achieve maximum fitness. We hypothesized that this temperature could be reflected by the intrinsic optimum temperature for developmental rate in the Sharpe–Schoolfield–Ikemoto model, and it led to a temperature estimate around 20 °C. However, the traditional viewpoint based on the temperature corresponding to the maximal intrinsic rate of increase provides a temperature estimate around 30 °C. This study suggests that a low temperature around 20 °C might authentically represent the optimal ambient temperature for fitness in terrestrial ectotherms. It implies that thermal biologists who are interested in the effect of temperature on the fitness in terrestrial ectotherms should pay more attention to their performance at low temperature rather than high temperature.     

Evidence of maternal effects on temperature preference in side‐blotched lizards: implications for evolutionary response to climate change

Natural populations respond to selection pressures like increasing local temperatures in many ways, including plasticity and adaptation. To predict the response of ectotherms like lizards to local temperature increase, it is essential to estimate phenotypic variation in and determine the heritability of temperature‐related traits like average field body temperature (T_b) and preferred temperature (T_p). We measured T_p of Uta stansburiana in a laboratory thermal gradient and assessed the contribution of sex, reproductive status and throat color genotype to phenotypic variation in T_b of adult lizards. Females had higher T_p than males. However, they temporarily preferred lower temperature when gravid than when nongravid. Using a nested half‐sib design for genetic crosses in the laboratory, we estimated relative contributions of additive genetic variation and maternal effects to T_p of hatchlings. Our results show that maternal effects, but not additive genetic variation, influence T_p of hatchlings in U. stansburiana. Maternal T_p and the presence or absence of blue throat color alleles significantly influenced T_p of hatchlings. We discuss ecological and evolutionary consequences of these maternal effects in the context of rapid climate change and natural selection that we measure on progeny survival to maturity as a function of maternal T_p.     

Thermal dependence of locomotor performance in two cool-temperate lizards

Temperate-zone ectotherms experience varying or very low ambient temperatures and may have difficulty in attaining preferred body temperatures. Thus, adaptations to reduce the thermal dependence of physiological processes may be present. We measured the optimal temperature range for sprint speed and compared it with the selected body temperatures (T _sel) of two sympatric, cool-temperate lizards: the diurnal skink Oligosoma maccanni and the primarily nocturnal gecko Woodworthia (previously Hoplodactylus) “Otago/Southland”. We also investigated whether time-of-day influenced sprint speed. Contrary to results for other reptiles, we found that time-of-day did not influence speed in either species. For each species, the optimal temperature range for sprinting and T _sel overlapped, supporting the ‘thermal coadaptation’ hypothesis. However, the optimal range of temperatures for speed is not always attainable during activity by either species, which have limited opportunities to attain T _sel in the field. The thermal sensitivity of sprint speed in these two species does not appear to have evolved to fully match their current thermal environment. More data on cold-adapted species are needed to fully understand physiological adaptation in ectotherms.