Canopy coverage, light, and moisture affect thermoregulatory trade-offs in an amphibian breeding habitat.

When amphibians thermoregulate, they face a fundamental trade-off between the ability to maintain activity and an increased rate of dehydration at higher temperatures. Canopy coverage affects both the thermal and hydric conditions of the environment and can therefore influence amphibian thermoregulation. Frogs require proper conditions to thermoregulate to successfully grow, survive, and reproduce. But while we know how canopy and environmental variables typically affect operative temperature, less is known about effects on amphibian water loss rates. In this study, we measure the effect of canopy coverage on the conditions available for thermoregulation at a breeding pond of the California red-legged frog, Rana draytonii. We use agar frog models to estimate the thermal and hydric capacities frogs would experience in locations with different canopy coverage and microhabitats. At each site, we deployed models under four microhabitat treatments: wet/sun, wet/shade, dry/sun, and dry/shade. We modeled how environmental variables affected operative temperature and evaporative water loss from agar frogs. We found positive effects of air temperature, the sun treatment, and reduced canopy cover on operative temperature, and negative direct or indirect effects of these variables on evaporative water loss, consistent with the hypothesized trade-off between thermoregulatory behavior to increase temperature and the increased desiccation risk due to higher water loss. Additionally, our results indicate that the availability of wet microhabitats can allow frogs to reduce water loss, potentially mitigating the risk of desiccation when thermoregulating to achieve higher operative temperatures. Our findings suggest, that with access to proper microhabitats, amphibians can mitigate the fundamental trade-off and receive benefits of thermoregulating at high temperatures.

Cooling requirements fueled the collapse of a desert bird community from climate change.

Climate change threatens global biodiversity by increasing extinction risk, yet few studies have uncovered a physiological basis of climate-driven species declines. Maintaining a stable body temperature is a fundamental requirement for homeothermic animals, and water is a vital resource that facilitates thermoregulation through evaporative cooling, especially in hot environments. Here, we explore the potential for thermoregulatory costs to underlie the community collapse of birds in the Mojave Desert over the past century in response to climate change. The probability of persistence was lowest for species occupying the warmest and driest sites, which imposed the greatest cooling costs. We developed a general model of heat flux to evaluate whether water requirements for evaporative cooling contributed to species' declines by simulating thermoregulatory costs in the Mojave Desert for 50 bird species representing the range of observed declines. Bird species' declines were positively associated with climate-driven increases in water requirements for evaporative cooling and exacerbated by large body size, especially for species with animal-based diets. Species exhibiting reductions in body size across their range saved up to 14% in cooling costs and experienced less decline than species without size reductions, suggesting total cooling costs as a mechanism underlying Bergmann's rule. Reductions in body size, however, are unlikely to offset the 50 to 78% increase in cooling costs threatening desert birds from future climate change. As climate change spreads warm, dry conditions across the planet, water requirements are increasingly likely to drive population declines, providing a physiological basis for climate-driven extinctions.

Habitat thermal quality for Gopherus evgoodei in tropical deciduous forest and consequences of habitat modification by buffelgrass.

Tortoises of the genus Gopherus evolved in North America and have survived major environmental challenges in the past 40 million years. However, this genus now faces multiple anthropogenic threats, such as the introduction of invasive plant species. Buffelgrass (Cenchrus ciliaris) is considered one of the greatest threats to arid and tropical ecosystems, where gopher tortoises inhabit, because the grass displaces native flora and fauna. Modification of the environment as a result of this invasive plant portends an alteration of the available thermal landscape. The aim of this paper is twofold: 1) to evaluate the thermal quality of the primary habitat of Gopherus evgoodei (tropical deciduous forest [TDF], and 2) determine the potential thermal changes due to habitat modification by buffelgrass. First, we obtained data on body temperature of active tortoises in semi-captivity. Second, we measured the operative environmental temperature during 5 years at three sites south of Sonora, Mexico that support G. evgoodei: a) a pristine TDF (Conserved-TDF); b) a forest patch surrounded by introduced buffelgrass pasture (Partial-TDF); and c) an introduced buffelgrass pasture area (Buffel-Pasture). Our results demonstrate that the intact microhabitats within the TDF provide G. evgoodei with high thermal quality at both spatial and temporal scales. However modified habitat by buffelgrass had higher operative temperatures for G. evgoodei than TDF. The thermal quality of the sites disturbed with buffelgrass can exceed the thermal requirements of G. evgoodei by up to 25 °C. Finally, we discussed potential collateral effects of habitat modification by invasion by buffelgrass.

How will climate change impact fossorial lizard species? Two examples in the Baja California Peninsula.

Global climate change and the associated erosion of habitat suitability are pervasive threats to biodiversity. It is critical to identify specific stressors to assess a species vulnerability to extinction, especially in species with distinctive natural histories. Here, we present a combination of field, laboratory, and modeling approaches to evaluate the potential consequences of climate change on two endemic, fossorial lizards species (Anniella geronimensis and Bipes biporus) from Baja California, Mexico. We also include soil type in our models to refine the suitable areas using our mechanistic models. Results suggest that both species are at high risk of extinction by global climate change based on the thermal habitat suitability. The forecast for species persistence is most grave under the RCP8.5 scenario. On the one hand, suitable habitat for A. geronimensis diminishes at its southern distribution, but potential suitable expands towards the north. On the other hand, the suitable habitat for B. biporus will contract significantly with a concomitant reduction in its potential distribution. Because both species have low mobility and are restricted to low elevation, the potential for elevational and latitudinal dispersal to mitigate extinction risk along the Baja California Peninsula is unlikely. In addition each species has specialized thermal requirements (i.e., stenothermic) and soil type preferences to which they are adapted. Our ecophysiological models in combination with the type of soil are fundamental in developing conservation strategies.

Social Games and Genic Selection Drive Mammalian Mating System Evolution and Speciation.

Mating system theory based on economics of resource defense has been applied to describe social system diversity across taxa. Such models are generally successful but fail to account for stable mating systems across different environments or shifts in mating system without a change in ecological conditions. We propose an alternative approach to resource defense theory based on frequency-dependent competition among genetically determined alternative behavioral strategies characterizing many social systems (polygyny, monogamy, sneak). We modeled payoffs for competition, neighborhood choice, and paternal care to determine evolutionary transitions among mating systems. Our model predicts four stable outcomes driven by the balance between cooperative and agonistic behaviors: promiscuity (two or three strategies), polygyny, and monogamy. Phylogenetic analysis of 288 rodent species supports assumptions of our model and is consistent with patterns of evolutionarily stable states and mating system transitions. Support for model assumptions include that monogamy and polygyny evolve from promiscuity and that paternal care and monogamy are coadapted in rodents. As predicted by our model, monogamy and polygyny occur in sister taxa among rodents more often than by chance. Transitions to monogamy also favor higher speciation rates in subsequent lineages, relative to polygynous sister lineages. Taken together, our results suggest that genetically based neighborhood choice behavior and paternal care can drive transitions in mating system evolution. While our genic mating system theory could complement resource-based theory, it can explain mating system transitions regardless of resource distribution and provides alternative explanations, such as evolutionary inertia, when resource ecology and mating systems do not match.

Water loss and temperature interact to compound amphibian vulnerability to climate change.

Ectotherm thermal physiology is frequently used to predict species responses to changing climates, but for amphibians, water loss may be of equal or greater importance. Using physical models, we estimated the frequency of exceeding the thermal optimum (Topt ) or critical evaporative water loss (EWLcrit ) limits, with and without shade- or water-seeking behaviours. Under current climatic conditions (2002-2012), we predict that harmful thermal (>Topt ) and hydric (>EWLcrit ) conditions limit the activity of amphibians during ~70% of snow-free days in sunny habitats. By the 2080s, we estimate that sunny and dry habitats will exceed one or both of these physiological limits during 95% of snow-free days. Counterintuitively, we find that while wet environments eliminate the risk of critical EWL, they do not reduce the risk of exceeding Topt (+2% higher). Similarly, while shaded dry environments lower the risk of exceeding Topt , critical EWL limits are still exceeded during 63% of snow-free days. Thus, no single environment that we evaluated can simultaneously reduce both physiological risks. When we forecast both temperature and EWL into the 2080s, both physiological thresholds are exceeded in all habitats during 48% of snow-free days, suggesting that there may be limited opportunity for behaviour to ameliorate climate change. We conclude that temperature and water loss act synergistically, compounding the ecophysiological risk posed by climate change, as the combined effects are more severe than those predicted individually. Our results suggest that predictions of physiological risk posed by climate change that do not account for water loss in amphibians may be severely underestimated and that there may be limited scope for facultative behaviours to mediate rapidly changing environments.

The complex drivers of thermal acclimation and breadth in ectotherms.

Thermal acclimation capacity, the degree to which organisms can alter their optimal performance temperature and critical thermal limits with changing temperatures, reflects their ability to respond to temperature variability and thus might be important for coping with global climate change. Here, we combine simulation modelling with analysis of published data on thermal acclimation and breadth (range of temperatures over which organisms perform well) to develop a framework for predicting thermal plasticity across taxa, latitudes, body sizes, traits, habitats and methodological factors. Our synthesis includes > 2000 measures of acclimation capacities from > 500 species of ectotherms spanning fungi, invertebrates, and vertebrates from freshwater, marine and terrestrial habitats. We find that body size, latitude, and methodological factors often interact to shape acclimation responses and that acclimation rate scales negatively with body size, contributing to a general negative association between body size and thermal breadth across species. Additionally, we reveal that acclimation capacity increases with body size, increases with latitude (to mid-latitudinal zones) and seasonality for smaller but not larger organisms, decreases with thermal safety margin (upper lethal temperature minus maximum environmental temperatures), and is regularly underestimated because of experimental artefacts. We then demonstrate that our framework can predict the contribution of acclimation plasticity to the IUCN threat status of amphibians globally, suggesting that phenotypic plasticity is already buffering some species from climate change.

Behavioral and physiological polymorphism in males of the austral lizard Liolaemus sarmientoi.

Integrative behavioral studies show that the interplay between individual physiology and social behavior influences the ecology of the species, ultimately affecting individual fitness. Particularly in lizards, color polymorphism is associated with differential behaviors and reproductive strategies, which are evident in mature males during the mating season. Dominant males generally have greater endurance, higher body temperature, and larger bodies than submissive males, so they can acquire and defend larger territories and have greater access to females for mating. We studied whether the color morphs observed in males of one of the world's southernmost reptiles, Liolaemus sarmientoi, are related to behavioral variation during agonistic interactions, thermal physiology, morphology, and/or locomotor stamina. Liolaemus sarmientoi males exhibit three color morphs: red (RR), red-yellow (RY), and yellow (YY). These lizards exhibit subtle behavioral displays and we did not observe stamina differences among morphs. However, we found that RR males are more aggressive than YY males during agonistic encounters. In addition, greater body temperature change during trials, higher field body temperatures, and greater head sizes of RR males compared to RY or YY indicate that RR is a dominant morph, which may influence their ability to acquire and defend territory and tactics for achieving reproductive success.

Reduction in baseline corticosterone secretion correlates with climate warming and drying across wild lizard populations.

Climate change should lead to massive loss of biodiversity in most taxa, but the detailed physiological mechanisms underlying population extinction remain largely elusive so far. In vertebrates, baseline levels of hormones such as glucocorticoids (GCs) may be indicators of population state as their secretion to chronic stress can impair survival and reproduction. However, the relationship between GC secretion, climate change and population extinction risk remains unclear. In this study, we investigated whether levels of baseline corticosterone (the main GCs in reptiles) correlate with environmental conditions and associated extinction risk across wild populations of the common lizard Zootoca vivipara. First, we performed a cross-sectional comparison of baseline corticosterone levels along an altitudinal gradient among 14 populations. Then, we used a longitudinal study in eight populations to examine the changes in corticosterone levels following the exposure to a heatwave period. Unexpectedly, baseline corticosterone decreased with increasing thermal conditions at rest in females and was not correlated with extinction risk. In addition, baseline corticosterone levels decreased after exposure to an extreme heatwave period. This seasonal corticosterone decrease was more pronounced in populations without access to standing water. We suggest that low basal secretion of corticosterone may entail downregulating activity levels and limit exposure to adverse climatic conditions, especially to reduce water loss. These new insights suggest that rapid population decline might be preceded by a downregulation of the corticosterone secretion.

Extinction risks forced by climatic change and intraspecific variation in the thermal physiology of a tropical lizard.

Temperature increases can impact biodiversity and predicting their effects is one of the main challenges facing global climate-change research. Ectotherms are sensitive to temperature change and, although predictions indicate that tropical species are highly vulnerable to global warming, they remain one of the least studied groups with respect to the extent of physiological variation and local extinction risks. We model the extinction risks for a tropical heliothermic teiid lizard (Kentropyx calcarata) integrating previously obtained information on intraspecific phylogeographic structure, eco-physiological traits and contemporary species distributions in the Amazon rainforest and its ecotone to the Cerrado savannah. We also investigated how thermal-biology traits vary throughout the species' geographic range and the consequences of such variation for lineage vulnerability. We show substantial variation in thermal tolerance of individuals among thermally distinct sites. Thermal critical limits were highly correlated with operative environmental temperatures. Our physiological/climatic model predicted relative extinction risks for local populations within clades of K. calcarata for 2050 ranging between 26.1% and 70.8%, while for 2070, extinction risks ranged from 52.8% to 92.8%. Our results support the hypothesis that tropical-lizard taxa are at high risk of local extinction caused by increasing temperatures. However, the thermo-physiological differences found across the species' distribution suggest that local adaptation may allow persistence of this tropical ectotherm in global warming scenarios. These results will serve as basis to further research to investigate the strength of local adaptation to climate change. Persistence of Kentropyx calcarata also depends on forest preservation, but the Amazon rainforest is currently under high deforestation rates. We argue that higher conservation priority is necessary so the Amazon rainforest can fulfill its capacity to absorb the impacts of temperature increase on tropical ectotherms during climate change.

Climate and habitat interact to shape the thermal reaction norms of breeding phenology across lizard populations.

Substantial plastic variation in phenology in response to environmental heterogeneity through time in the same population has been uncovered in many species. However, our understanding of differences in reaction norms of phenology among populations from a given species remains limited. As the plasticity of phenological traits is often influenced by local thermal conditions, we expect local temperature to generate variation in the reaction norms between populations. Here, we explored temporal variation in parturition date across 11 populations of the common lizard (Zootoca vivipara) from four mountain chains as a function of air temperatures during mid-gestation. We characterized among-population variation to assess how local weather conditions (mean and variance of ambient temperatures during mid-gestation) and habitat openness (an index of anthropogenic disturbance) influence the thermal reaction norms of the parturition date. Our results provide evidence of interactive effects of anthropogenic disturbance and thermal conditions, with earlier parturition dates in warmer years on average especially in closed habitats. Variation in the reaction norms for parturition date was correlated with mean local thermal conditions at a broad geographical scale. However, populations exposed to variable thermal conditions had flatter thermal reaction norms. Assessing whether environmental heterogeneity drives differentiation among reaction norms is crucial to estimate the capacity of different populations to contend with projected climatic and anthropogenic challenges.

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.

Using motion-sensor camera technology to infer seasonal activity and thermal niche of the desert tortoise (Gopherus agassizii).

Understanding the relationships between environmental variables and wildlife activity is an important part of effective management. The desert tortoise (Gopherus agassizii), an imperiled species of arid environments in the southwest US, may have increasingly restricted windows for activity due to current warming trends. In summer 2013, we deployed 48 motion sensor cameras at the entrances of tortoise burrows to investigate the effects of temperature, sex, and day of the year on the activity of desert tortoises. Using generalized estimating equations, we found that the relative probability of activity was associated with temperature (linear and quadratic), sex, and day of the year. Sex effects showed that male tortoises are generally more active than female tortoises. Temperature had a quadratic effect, indicating that tortoise activity was heightened at a range of temperatures. In addition, we found significant support for interactions between sex and day of the year, and sex and temperature as predictors of the probability of activity. Using our models, we were able to estimate air temperatures and times (days and hours) that were associated with maximum activity during the study. Because tortoise activity is constrained by environmental conditions such as temperature, it is increasingly vital to conduct studies on how tortoises vary their activity throughout the Sonoran Desert to better understand the effects of a changing climate.

Frequency-dependent and correlational selection pressures have conflicting consequences for assortative mating in a color-polymorphic lizard, Uta stansburiana.

Genetically determined polymorphisms incorporating multiple traits can persist in nature under chronic, fluctuating, and sometimes conflicting selection pressures. Balancing selection among morphs preserves equilibrium frequencies, while correlational selection maintains favorable trait combinations within each morph. Under negative frequency-dependent selection, females should mate (often disassortatively) with rare male morphotypes to produce conditionally fit offspring. Conversely, under correlational selection, females should mate assortatively to preserve coadapted gene complexes and avoid ontogenetic conflict. Using controlled breeding designs, we evaluated consequences of assortative mating patterns in color-polymorphic side-blotched lizards (Uta stansburiana), to identify conflict between these sources of selection. Females who mated disassortatively, and to conditionally high-quality males in the context of frequency-dependent selection, experienced highest fertility rates. In contrast, assortatively mated females experienced higher fetal viability rates. The trade-off between fertility and egg viability resulted in no overall fitness benefit to either assortative or disassortative mating patterns. These results suggest that ongoing conflict between correlational and frequency dependent selection in polymorphic populations may generate a trade-off between rare-morph advantage and phenotypic integration and between assortative and disassortative mating decisions. More generally, interactions among multiple sources of diversity-promoting selection can alter adaptations and dynamics predicted to arise under any of these regimes alone.

Natural parasites in conjunction with behavioral and color traits explain male agonistic behaviors in a lizard.

Male competition conforms to a cost-benefit model, because while aggression may increase reproductive prospects, it can also increase the risk of injury. We hypothesize that an additional cost in aggressive males would be an increase in parasite load associated with a high energy investment into sexual competition. Some of these infections, in turn, may downmodulate the level of host aggression via energetic trade-offs. We staged dyadic male contests in the lab to investigate the relationships of multiple parasites with the agonistic behavior of lizard hosts, Sceloporus occidentalis. We also included both color and behavioral traits from opponents in the analyses because (1) color patches of lizards may serve as intraspecific signals used by conspecifics to assess the quality of opponents, and (2) contests between male lizards fit classical models of escalated aggression, where lizards increase aggression displays in response to an opponent's behavior. The results conform to our hypothesis because male lizards displayed more pushups when they had more ticks. Moreover, some parasites may modulate the levels of aggression because lizards infected by hematic coccidians performed fewer pushups. Interestingly, lizards also displayed fewer pushups when both the chroma and size of the opponent's blue patch were greater. The results thus also supported the role of the blue patch of S. occidentalis as a sexual armament, because it contributed to the deterrence of aggression from opponent lizards. We revealed that natural parasitic infections in lizard hosts can contribute to their agonistic behavior. We encourage future studies to account for parasites in behavioral tests with lizards.

Iridophores and not carotenoids account for chromatic variation of carotenoid-based coloration in common lizards (Lacerta vivipara).

Abstract Carotenoids typically need reflective background components to shine. Such components, iridophores, leucophores, and keratin- and collagen-derived structures, are generally assumed to show no or little environmental variability. Here, we investigate the origin of environmentally induced variation in the carotenoid-based ventral coloration of male common lizards (Lacerta vivipara) by investigating the effects of dietary carotenoids and corticosterone on both carotenoid- and background-related reflectance. We observed a general negative chromatic change that was prevented by ß-carotene supplementation. However, chromatic changes did not result from changes in carotenoid-related reflectance or skin carotenoid content but from changes in background-related reflectance that may have been mediated by vitamin A1. An in vitro experiment showed that the encountered chromatic changes most likely resulted from changes in iridophore reflectance. Our findings demonstrate that chromatic variation in carotenoid-based ornaments may not exclusively reflect differences in integumentary carotenoid content and, hence, in qualities linked to carotenoid deposition (e.g., foraging ability, immune response, or antioxidant capacity). Moreover, skin carotenoid content and carotenoid-related reflectance were related to male color polymorphism, suggesting that carotenoid-based coloration of male common lizards is a multicomponent signal, with iridophores reflecting environmental conditions and carotenoids reflecting genetically based color morphs.

Selective loss of polymorphic mating types is associated with rapid phenotypic evolution during morphic speciation.

Polymorphism may play an important role in speciation because new species could originate from the distinctive morphs observed in polymorphic populations. However, much remains to be understood about the process by which morphs found new species. To detail the steps of this mode of speciation, we studied the geographic variation and evolutionary history of a throat color polymorphism that distinguishes the "rock-paper-scissors" mating strategies of the side-blotched lizard, Uta stansburiana. We found that the polymorphism is geographically widespread and has been maintained for millions of years. However, there are many populations with reduced numbers of throat color morphs. Phylogenetic reconstruction showed that the polymorphism is ancestral, but it has been independently lost eight times, often giving rise to morphologically distinct subspecies/species. Changes to the polymorphism likely involved selection because the allele for one particular male strategy, the "sneaker" morph, has been lost in all cases. Polymorphism loss was associated with accelerated evolution of male size, female size, and sexual dimorphism, which suggests that polymorphism loss can promote rapid divergence among populations and aid species formation.

Plastic responses to warmer climates: a semi-natural experiment on lizard populations.

Facing warming environments, species can exhibit plastic or microevolutionary changes in their thermal physiology to adapt to novel climates. Here, using semi-natural mesocosms, we experimentally investigated over two successive years whether a 2°C-warmer climate produces selective and inter- and intragenerational plastic changes in the thermal traits (preferred temperature and dorsal coloration) of the lizard Zootoca vivipara. In a warmer climate, the dorsal darkness, dorsal contrast, and preferred temperature of adults plastically decreased and covariances between these traits were disrupted. While selection gradients were overall weak, selection gradients for darkness were slightly different between climates and in the opposite direction to plastic changes. Contrary to adults, male juveniles were darker in warmer climates either through plasticity or selection and this effect was strengthened by intergenerational plasticity when juveniles' mothers also experienced warmer climates. While the plastic changes in adult thermal traits alleviate the immediate overheating costs of warming, its opposite direction to selective gradients and to juveniles' phenotypic responses may slow down evolutionary shifts toward phenotypes that are better adapted to future climates. Our study demonstrates the importance of considering inter- and intragenerational plasticity along with selective processes to better understand adaptation and population dynamics in light of climate change.

Convergent evolution of kin-based sociality in a lizard.

Studies of social birds and mammals have produced extensive theory regarding the formation and dynamics of kin-based social groups in vertebrates. However, comparing kin dynamics in birds and mammals to social reptiles provides the opportunity to identify selective factors that promote independent origins of kin sociality across vertebrates. We combined a 5-year mark-recapture study with a DNA microsatellite analysis of relatedness in a social lizard (Xantusia vigilis) to examine the formation and stability of kin groups. We found that these lizards are highly sedentary and that groups often form through the delayed dispersal of offspring. Groups containing juveniles had higher relatedness than adult-only groups, as juveniles were commonly found in aggregations with at least one parent and/or sibling. Groups containing nuclear family members were more stable than groups of less-related lizards, as predicted by social theory. We conclude that X. vigilis aggregations conform to patterns of kin sociality observed in avian and mammalian systems and represent an example of convergent evolution in social systems. We suggest that kin-based sociality in this and other lizards may be a by-product of viviparity, which can promote delayed juvenile dispersal by allowing prolonged interaction between a neonate and its mother.