Ecological responses of squamate reptiles to nocturnal warming.

Nocturnal temperatures are increasing at a pace exceeding diurnal temperatures in most parts of the world. The role of warmer nocturnal temperatures in animal ecology has received scant attention and most studies focus on diurnal or daily descriptors of thermal environments' temporal trends. Yet, available evidence from plant and insect studies suggests that organisms can exhibit contrasting physiological responses to diurnal and nocturnal warming. Limiting studies to diurnal trends can thus result in incomplete and misleading interpretations of the ability of species to cope with global warming. Although they are expected to be impacted by warmer nocturnal temperatures, insufficient data are available regarding the night-time ecology of vertebrate ectotherms. Here, we illustrate the complex effects of nocturnal warming on squamate reptiles, a keystone group of vertebrate ectotherms. Our review includes discussion of diurnal and nocturnal ectotherms, but we mainly focus on diurnal species for which nocturnal warming affects a period dedicated to physiological recovery, and thus may perturb activity patterns and energy balance. We first summarise the physical consequences of nocturnal warming on habitats used by squamate reptiles. Second, we describe how such changes can alter the energy balance of diurnal species. We illustrate this with empirical data from the asp viper (Vipera aspis) and common wall lizard (Podarcis muralis), two diurnal species found throughout western Europe. Third, we make use of a mechanistic approach based on an energy-balance model to draw general conclusions about the effects of nocturnal temperatures. Fourth, we examine how warmer nights may affect squamates over their lifetime, with potential consequences on individual fitness and population dynamics. We review quantitative evidence for such lifetime effects using recent data derived from a range of studies on the European common lizard (Zootoca vivipara). Finally, we consider the broader eco-evolutionary ramifications of nocturnal warming and highlight several research questions that require future attention. Our work emphasises the importance of considering the joint influence of diurnal and nocturnal warming on the responses of vertebrate ectotherms to climate warming.

Prey consumption does not restore hydration state but mitigates the energetic costs of water deprivation in an insectivorous lizard.

To cope with limited availability of drinking water in their environment, terrestrial animals have developed numerous behavioral and physiological strategies including maintaining an optimal hydration state through dietary water intake. Recent studies performed in snakes, which are generalist carnivorous reptiles, suggest that the benefits of dietary water intake are negated by hydric costs of digestion. Most lizards are generalist insectivores that can shift their prey types, but firm experimental demonstration of dietary water intake is currently missing in these organisms. Here, we performed an experimental study in the common lizard Zootoca vivipara, a keystone mesopredator from temperate climates exhibiting a great diversity of prey in its mesic habitats, in order to investigate the effects of food consumption and prey type on physiological responses to water deprivation. Our results indicate that common lizards cannot improve their hydration state through prey consumption, irrespective of prey type, suggesting that they are primarily dependent upon drinking water. Yet, high-quality prey consumption reduced the energetic costs of water deprivation, potentially helping lizards to conserve a better body condition during periods of limited water availability. These findings have important implications for understanding the physiological responses of ectotherms to water stress, and highlight the complex interactions between hydration status, energy metabolism and feeding behavior in insectivorous lizards.

Behavioural hydroregulation protects against acute effects of drought in a dry-skinned ectotherm.

During extreme climate events, behavioural thermoregulation may buffer ectotherms from thermal stress and overheating. However, heatwaves are also combined with dry spells and limited water availability, and how much individuals can behaviourally mitigate dehydration risks through microclimate selection remains largely unknown. Herein, we investigated the behavioural and physiological responses to changes in air and microhabitat humidity in a terrestrial ectotherm, the asp viper (Vipera aspis). We exposed individuals to a simulated heatwave together with water deprivation for 3 weeks, and manipulated air water vapour density (wet air vs. dry air) and microclimate (wet shelter vs. dry shelter) in a two-by-two factorial design. Dry air conditions led to substantial physiological dehydration and muscle wasting. Vipers exposed to dry air used more often a shelter that offered a moist microclimate, which reduced dehydration and muscle wasting at the individual level. These results provide the first experimental evidence that active behavioural hydroregulation can mitigate specific physiological stress responses caused by a dry spell in an ectotherm. Future studies investigating organismal responses to climate change should consider moisture gradient in the habitat and integrate both hydroregulation and thermoregulation behaviours.

Lizards from warm and declining populations are born with extremely short telomeres.

Aging is the price to pay for acquiring and processing energy through cellular activity and life history productivity. Climate warming can exacerbate the inherent pace of aging, as illustrated by a faster erosion of protective telomere DNA sequences. This biomarker integrates individual pace of life and parental effects through the germline, but whether intra- and intergenerational telomere dynamics underlies population trends remains an open question. Here, we investigated the covariation between life history, telomere length (TL), and extinction risk among three age classes in a cold-adapted ectotherm (Zootoca vivipara) facing warming-induced extirpations in its distribution limits. TL followed the same threshold relationships with population extinction risk at birth, maturity, and adulthood, suggesting intergenerational accumulation of accelerated aging rate in declining populations. In dwindling populations, most neonates inherited already short telomeres, suggesting they were born physiologically old and unlikely to reach recruitment. At adulthood, TL further explained females' reproductive performance, switching from an index of individual quality in stable populations to a biomarker of reproductive costs in those close to extirpation. We compiled these results to propose the aging loop hypothesis and conceptualize how climate-driven telomere shortening in ectotherms may accumulate across generations and generate tipping points before local extirpation.

Mitochondrial oxidative phosphorylation response overrides glucocorticoid-induced stress in a reptile.

Stress hormones and their impacts on whole organism metabolic rates are usually considered as appropriate proxies for animal energy budget that is the foundation of numerous concepts and models aiming at predicting individual and population responses to environmental stress. However, the dynamics of energy re-allocation under stress make the link between metabolism and corticosterone complex and still unclear. Using ectopic application of corticosterone for 3, 11 and 21 days, we estimated a time effect of stress in a lizard (Zootoca vivipara). We then investigated whole organism metabolism, muscle cellular O2 consumption and liver mitochondrial oxidative phosphorylation processes (O2 consumption and ATP production) and ROS production. The data showed that while skeletal muscle is not impacted, stress regulates the liver mitochondrial functionality in a time-dependent manner with opposing pictures between the different time expositions to corticosterone. While 3 days exposition is characterized by lower ATP synthesis rate and high H2O2 release with no change in the rate of oxygen consumption, the 11 days exposition reduced all three fluxes of about 50%. Oxidative phosphorylation capacities in liver mitochondria of lizard treated with corticosterone for 21 days was similar to the hepatic mitochondrial capacities in lizards that received no corticosterone treatment but with 40% decrease in H2O2 production. This new mitochondrial functioning allows a better capacity to respond to the energetic demands imposed by the environment but do not influence whole organism metabolism. In conclusion, global mitochondrial functioning has to be considered to better understand the proximal causes of the energy budget under stressful periods.

Environmental conditions and male quality traits simultaneously explain variation of multiple colour signals in male lizards.

Male lizards often display multiple pigment-based and structural colour signals which may reflect various quality traits (e.g. performance, parasitism), with testosterone (T) often mediating these relationships. Furthermore, environmental conditions can explain colour signal variation by affecting processes such as signal efficacy, thermoregulation and camouflage. The relationships between colour signals, male quality traits and environmental factors have often been analysed in isolation, but simultaneous analyses are rare. Thus, the response of multiple colour signals to variation in all these factors in an integrative analysis remains to be investigated. Here, we investigated how multiple colour signals relate to their information content, examined the role of T as a potential mediator of these relationships and how environmental factors explain colour signal variation. We performed an integrative study to examine the covariation between three colour signals (melanin-based black, carotenoid-based yellow-orange and structural UV), physiological performance, parasitism, T levels and environmental factors (microclimate, forest cover) in male common lizards Zootoca vivipara from 13 populations. We found that the three colour signals conveyed information on different aspects of male condition, supporting a multiple message hypothesis. T influenced only parasitism, suggesting that T does not directly mediate the relationships between colour signals and their information content. Moreover, colour signals became more saturated in forested habitats, suggesting an adaptation to degraded light conditions, and became generally brighter in mesic conditions, in contradiction with the thermal melanism hypothesis. We show that distinct individual quality traits and environmental factors simultaneously explain variations of multiple colour signals with different production modes. Our study therefore highlights the complexity of colour signal evolution, involving various sets of selective pressures acting at the same time, but in different ways depending on colour production mechanism.

Les lézards mâles arborent souvent plusieurs signaux colorés de nature pigmentaire et structurale qui reflètent de multiples traits de qualité (e.g. performance, parasitisme), et la testostérone (T) joue souvent un rôle de médiateur dans ces relations. En outre, les conditions environnementales peuvent également expliquer les variations des signaux colorés en influençant des aspects tels que l'efficacité des signaux, la thermorégulation ou le camouflage. Les relations entre signaux colorés, traits de qualité individuelle et facteurs environnementaux ont souvent été analysées séparément, mais rarement de manière simultanée. Ainsi, la réponse de ces multiples signaux colorés aux variations de tous ces facteurs reste à explorer dans le contexte d'une étude intégrative. Ici, nous explorons la relation entre ces multiples signaux colorés et leur contenu informatif, nous examinons le rôle de T comme médiateur potentiel de ces relations et nous recherchons si les conditions environnementales expliquent la variation de ces signaux colorés. Nous avons mené une étude intégrative afin d'examiner la covariation entre trois types de signaux colorés (noir produit par la mélanine, jaune-orange produit par les caroténoïdes et UV produit par des éléments structuraux), la performance physiologique, le parasitisme, les niveaux de T et les conditions environnementales (e.g. microclimat, couverture forestière) chez des mâles du lézard vivipare (Zootoca vivipara) provenant de 13 populations. Nos résultats indiquent que les trois signaux colorés transmettent des informations sur différents aspects de la condition des mâles, en accord avec l'hypothèse de « messages multiples ¼. T influence uniquement le parasitisme, suggérant que T n'agit pas en tant que médiateur des relations entre ces signaux colorés et leur contenu informatif. De plus, les signaux colorés sont plus saturés dans les habitats les plus forestiers, ce qui suggère une adaptation à des conditions lumineuses dégradées. Enfin, les signaux colorés sont plus intenses lorsque les conditions sont mésiques, en contradiction avec l'hypothèse du mélanisme thermal. Nous démontrons que différents traits de qualité individuelle et facteurs environnementaux expliquent de manière simultanée les variations de multiples signaux colorés impliquant différents modes de production. Notre étude souligne ainsi la complexité de l'évolution des signaux colorés, qui implique plusieurs types de pressions de sélection agissant en même temps mais dans des directions différentes selon le mode de production.

Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity.

Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.

Two stressors are worse than one: combined heatwave and drought affect hydration state and glucocorticoid levels in a temperate ectotherm.

Heatwaves and droughts are becoming more intense and frequent with climate change. These extreme weather events often occur simultaneously and may alter organismal physiology, yet their combined impacts remain largely unknown. Here, we experimentally investigated physiological responses of a temperate ectotherm, the asp viper (Vipera aspis), to a simulated heatwave and drought. We applied a two-by-two factorial design by manipulating the daily temperature cycle (control versus heatwave) and the water availability (water available versus water deprived) over a month followed by exposure to standard thermal conditions with ad libitum access to water. Simulated heatwave and water deprivation additively increased mass loss, while water deprivation led to greater plasma osmolality (dehydration). Mass gain from drinking after the treatment period was higher in vipers from the heatwave and water-deprived group, suggesting that thirst was synergistically influenced by thermal and water constraints. Heatwave conditions and water deprivation also additively increased baseline corticosterone levels but did not influence basal metabolic rate and plasma markers of oxidative stress. Our results demonstrate that a short-term exposure to combined heatwave and drought can exacerbate physiological stress through additive effects, and interactively impact behavioral responses to dehydration. Considering combined effects of temperature and water availability is thus crucial to assess organismal responses to climate change.

Water deprivation compromises maternal physiology and reproductive success in a cold and wet adapted snake Vipera berus.

Droughts are becoming more intense and frequent with climate change. These extreme weather events can lead to mass mortality and reproduction failure, and therefore cause population declines. Understanding how the reproductive physiology of organisms is affected by water shortages will help clarify whether females can adjust their reproductive strategy to dry conditions or may fail to reproduce and survive. In this study, we investigated the consequences of a short period of water deprivation (2 weeks) during early pregnancy on the physiology and behaviour of a cold- and wet-adapted ectotherm (Vipera berus). We also examined water allocation to developing embryos and embryonic survival. Water-deprived females exhibited significant dehydration, physiological stress and loss of muscle mass. These effects of water deprivation on water balance and muscle loss were correlated with the number of developing embryos. While water-deprived females maintained water transfer to embryos at the expense of their own maintenance, water deprivation also led to embryonic mortality. Overall, water deprivation amplifies the reproductive costs of water allocation to support embryonic development. The deleterious impacts of water deprivation on female current reproductive performance and on potential survival and future reproduction could lead to severe population declines in this species.

Intense nocturnal warming alters growth strategies, colouration and parasite load in a diurnal lizard.

In the past decades, nocturnal temperatures have been playing a disproportionate role in the global warming of the planet. Yet, they remain a neglected factor in studies assessing the impact of global warming on natural populations. Here, we question whether an intense augmentation of nocturnal temperatures is beneficial or deleterious to ectotherms. Physiological performance is influenced by thermal conditions in ectotherms and an increase in temperature by only 2°C is sufficient to induce a disproportionate increase in metabolic expenditure. Warmer nights may expand ectotherms' species thermal niche and open new opportunities for prolonged activities and improve foraging efficiency. However, increased activity may also have deleterious effects on energy balance if exposure to warmer nights reduces resting periods and elevates resting metabolic rate. We assessed whether warmer nights affected an individual's growth, dorsal skin colouration, thermoregulation behaviour, oxidative stress status and parasite load by exposing yearling common lizards (Zootoca vivipara) from four populations to either ambient or high nocturnal temperatures for approximately 5 weeks. Warmer nocturnal temperatures increased the prevalence of ectoparasitic infestation and altered allocation of resources towards structural growth rather than storage. We found no change in markers for oxidative stress. The thermal treatment did not influence thermal preferences, but influenced dorsal skin brightness and luminance, in line with a predicted acclimation response in colder environments to enhance heat gain from solar radiation. Altogether, our results highlight the importance of considering nocturnal warming as an independent factor affecting ectotherms' life history in the context of global climate change. ​.

Short-term changes in air humidity and water availability weakly constrain thermoregulation in a dry-skinned ectotherm.

Thermoregulation is critical for ectotherms as it allows them to maintain their body temperature close to an optimum for ecological performance. Thermoregulation includes a range of behaviors that aim at regulating body temperature within a range centered around the thermal preference. Thermal preference is typically measured in a thermal gradient in fully-hydrated and post-absorptive animals. Short-term effects of the hydric environment on thermal preferences in such set-ups have been rarely quantified in dry-skinned ectotherms, despite accumulating evidence that dehydration might trade-off with behavioral thermoregulation. Using experiments performed under controlled conditions in climatic chambers, we demonstrate that thermal preferences of a ground-dwelling, actively foraging lizard (Zootoca vivipara) are weakly decreased by a daily restriction in free-standing water availability (less than 0.5°C contrast). The influence of air humidity during the day on thermal preferences depends on time of the day and sex of the lizard, and is generally weaker than those of of free-standing water (less than 1°C contrast). This shows that short-term dehydration can influence, albeit weakly, thermal preferences under some circumstances in this species. Environmental humidity conditions are important methodological factors to consider in the analysis of thermal preferences.

Ecotrons: Powerful and versatile ecosystem analysers for ecology, agronomy and environmental science.

Ecosystems integrity and services are threatened by anthropogenic global changes. Mitigating and adapting to these changes require knowledge of ecosystem functioning in the expected novel environments, informed in large part through experimentation and modelling. This paper describes 13 advanced controlled environment facilities for experimental ecosystem studies, herein termed ecotrons, open to the international community. Ecotrons enable simulation of a wide range of natural environmental conditions in replicated and independent experimental units while measuring various ecosystem processes. This capacity to realistically control ecosystem environments is used to emulate a variety of climatic scenarios and soil conditions, in natural sunlight or through broad-spectrum lighting. The use of large ecosystem samples, intact or reconstructed, minimizes border effects and increases biological and physical complexity. Measurements of concentrations of greenhouse trace gases as well as their net exchange between the ecosystem and the atmosphere are performed in most ecotrons, often quasi continuously. The flow of matter is often tracked with the use of stable isotope tracers of carbon and other elements. Equipment is available for measurements of soil water status as well as root and canopy growth. The experiments ran so far emphasize the diversity of the hosted research. Half of them concern global changes, often with a manipulation of more than one driver. About a quarter deal with the impact of biodiversity loss on ecosystem functioning and one quarter with ecosystem or plant physiology. We discuss how the methodology for environmental simulation and process measurements, especially in soil, can be improved and stress the need to establish stronger links with modelling in future projects. These developments will enable further improvements in mechanistic understanding and predictive capacity of ecotron research which will play, in complementarity with field experimentation and monitoring, a crucial role in exploring the ecosystem consequences of environmental changes.

Additive effects of temperature and water availability on pregnancy in a viviparous lizard.

One of the greatest current threats to biodiversity is climate change. However, understanding of organismal responses to fluctuations in temperature and water availability is currently lacking, especially during fundamental life-history stages such as reproduction. To further explore how temperature and water availability impact maternal physiology and reproductive output, we used the viviparous form of the European common lizard (Zootoca vivipara) in a two-by-two factorial design manipulating both hydric and thermal conditions, for the first time. We collected blood samples and morphological measurements during early pregnancy and post-parturition to investigate how water availability, temperature and a combination of the two influence maternal phenology, morphology, physiology and reproductive output. We observed that dehydration during gestation negatively affects maternal physiological condition (lower mass gain, higher tail reserve mobilization) but has little effect on reproductive output. These effects are mainly additive to temperature regimes, with a proportional increase in maternal costs in warmer environments. Our study demonstrates the importance of considering combined effects of water and temperature when investigating organismal responses to climate changes, especially during periods crucial for species survival such as reproduction.

Micro-geographic shift between negligible and actuarial senescence in a wild snake.

While it has long been known that species have contrasted life expectancy (pace of mortality) and generation time (pace of reproduction), recent studies have also uncovered that the shape of adult age trajectories of mortality and reproduction can vary remarkably among species along a continuum of senescence ranging from strong deterioration (senescence), insignificant deterioration (negligible senescence) to improvement with advancing age (negative senescence). As for many long-lived ectotherms with asymptotic growth and increasing reproductive output with age, snakes are good candidates for negligible senescence to occur. Yet, intraspecific variation in the pace and shape of actuarial and reproductive senescence across wild populations of these species remains to be explored. Here, we used 37 years of mark-recapture data in two nearby habitats inside a meadow viper Vipera ursinii population to quantify life expectancies, generation times and the shape of actuarial and reproductive senescence. Female vipers maintained stable reproductive performances at old ages, even when accounting for the predicted increase of fertility with body size, providing evidence for negligible reproductive senescence in both habitats. Males had a higher adult mortality and a shorter life expectancy on average than females and actuarial senescence shifted from negligible senescence in the optimal habitat to strong senescence in the sub-optimal habitat. Overall, these results demonstrate that micro-geographic environmental variation can generate qualitative shifts in actuarial senescence patterns. This highlights that taking into account the within-species plasticity of age-dependent trajectories could prove useful in better understanding what determines the evolution of life-history age trajectories.

La longévité et la manière de vieillir varient grandement entre espèces. Chez certaines espèces, la survie et la reproduction déclinent avec l'âge : les individus souffrent de sénescence. Chez d'autres, les vieux individus maintiennent des performances reproductives et de survie similaires à celles des jeunes : la sénescence est alors dite négligeable. Enfin, la sénescence peut être négative quand la survie des adultes ou leur reproduction s'améliorent avec l'âge. Les formes des trajectoires de mortalité et de reproduction avec l'âge sont encore mal connues chez les serpents, mais la théorie évolutive prédit une sénescence négligeable chez les espèces qui, comme les serpents, continuent à grandir à l'âge adulte et dont les femelles produisent des portées dont l'effectif augmente avec la taille corporelle de la mère. Nous avons exploité ici 37 années de données de capture-marquage-recapture de vipères d'Orsini, Vipera ursinii ursinii, dans deux habitats voisins d'une petite population isolée du Sud-Est de la France pour quantifier l'espérance de vie, les temps de génération et les formes de la sénescence de survie et de la sénescence reproductrice. Nous montrons que les vipères femelles parviennent à maintenir de bonnes performances reproductives même à des âges avancés, illustrant une sénescence reproductrice négligeable dans cette population. Nous montrons aussi que la forme de la sénescence de survie varie fortement à une très petite échelle géographique : dans l'habitat optimal, la survie adulte des vipères demeure stable quel que soit leur âge alors qu'à quelques centaines de mètres, dans un habitat moins favorable, les vipères subissent une forte sénescence de survie. Ces résultats démontrent que de forts changements qualitatifs dans les profils de sénescence peuvent être observés à une échelle spatiale réduite. Cette plasticité intra-spécifique de la sénescence offre de nouvelles perspectives pour mieux comprendre ce qui détermine l'évolution de la sénescence.

Short-term change in water availability influences thermoregulation behaviours in a dry-skinned ectotherm.

Mechanistic models of terrestrial ectotherms predict that climate warming will induce activity restriction due to heat stress and loss of shade, leading to the extinction of numerous populations. Such models rely on the assumption that activity patterns are dictated by simple temperature thresholds independent of changes in water availability. However, changes in water availability may further influence thermoregulation behaviour of ectotherms through dehydration risk perception, changes in water balance or changes in microclimatic conditions. Here, we experimentally assess the interactive effects of thermal conditions and water availability on activity patterns, shade selection and thermoregulation efficiency in a model ectothermic species. Thermoregulation behaviour of adult common lizards Zootoca vivipara was monitored in outdoor mesocosms as we manipulated water availability, providing water as mist in the morning and free-standing water during the daytime. We recorded operative temperatures and micro-meteorological conditions to infer thermal constraints and dehydration risk. Activity and shade selection were better predicted by continuous changes in thermal conditions and dehydration risk, respectively, than by threshold functions. In addition, water supplementation increased activity in males and reduced shade selection in both sexes, most probably as a behavioural response to the perception of a stronger dehydration risk. Water supplementation also influenced the thermal quality of the environment, which in turn altered daily activity patterns and thermoregulation statistics. This demonstrates that dual effects of heat and water stress on activity patterns may lead to stronger activity restriction as a result of climate change than currently predicted.

Chronic water restriction triggers sex-specific oxidative stress and telomere shortening in lizards.

Animals use a variety of strategies to avoid acute dehydration and death. Yet, how chronic exposure to sub-lethal dehydration may entail physiological and fitness costs remains elusive. In this study, we experimentally tested if water restriction causes increased oxidative stress (OS) and telomere length (TL) shortening, two well-described mediators of environment-fitness relationships. We exposed 100 yearling female and male common lizards (Zootoca vivipara) either to a 51-day period of water restriction or to water ad libitum, followed by 45 days in common garden outdoor conditions. We measured the kinetic changes in OS and TL and found that water-restricted males had enhanced antioxidant defences and decreased oxidative damage at day 36, whereas females did not immediately respond. A month and a half after water restriction, both sexes experienced a drop in antioxidant capacity but only males exhibited significant TL shortening. In the following 3 years, we found that lizards with longer initial TL and those who maintained stronger antioxidant defences experienced higher longevity, irrespective of sex and water restriction. Together, these results unravelled sex-specific responses to water restriction, with potential applications in better understanding the physiological costs of increasing summer droughts as a result of global climate change.

Acclimation to Water Restriction Implies Different Paces for Behavioral and Physiological Responses in a Lizard Species.

Chronic changes in climate conditions may select for acclimation responses in terrestrial animals living in fluctuating environments, and beneficial acclimation responses may be key to the resilience of these species to global changes. Despite evidence that climate warming induces changes in water availability, acclimation responses to water restriction are understudied compared with thermal acclimation. In addition, acclimation responses may involve different modes, paces, and trade-offs between physiological and behavioral traits. Here, we tested the dynamical acclimation responses of a dry-skinned terrestrial ectotherm to chronic water restriction. Yearling common lizards (Zootoca vivipara) were exposed to sublethal water restriction during 2 mo of the summer season in laboratory conditions, then released in outdoor conditions for 10 additional months. Candidate behavioral (exploration, basking, and thermal preferences) and physiological (metabolism at rest and standard water loss rate) traits potentially involved in the acclimation response were measured repeatedly during and after water restriction. We observed a sequential acclimation response in water-restricted animals (yearlings spent less time basking during the first weeks of water deprivation) that was followed by delayed sex-specific physiological consequences of the water restriction during the following months (thermal depression in males and lower standard evaporative water loss rates in females). Despite short-term negative effects of water restriction on body growth, annual growth, survival, and reproduction were not significantly different between water-restricted and control yearlings. This demonstrates that beneficial acclimation responses to water restriction involve both short-term flexible behavioral responses and delayed changes in thermal and water biology traits.

Chronic elevation of glucorticoids late in life generates long lasting changes in physiological state without a life history switch.

Chronic stressors have profound impacts on phenotypes and life history strategies on the short term, but delayed effects of stress experienced late in life remain poorly investigated in wild populations. Here, we used a combined laboratory and field experiment to test if chronic stress late in life has immediate and delayed effects on physiological and demographic traits in the common lizard, Zootoca vivipara. We increased plasma corticosterone levels in adults and yearlings during three weeks of the post-reproductive season. We quantified immediate responses in the laboratory, delayed intra-generational effects in field enclosures one month and one year later during the next reproductive season, and delayed inter-generational effects in the first generation of offspring. Our phenotypic assays included metabolism, immune capacities, lipid metabolism and oxidative stress. Relative to placebos, lizards treated with corticosterone had higher body condition and lower oxidative damages but an increased skin swelling response directly after the manipulation. Delayed responses in field enclosures were of three types. First, we found catch-up growth for body mass such the placebos had similar body conditions one month after the laboratory manipulation. Second, we found persistent differences in oxidative damages during one month but not one year later. Third, during the next reproductive season, corticosterone-treated females had higher levels of plasma triglycerides, whereas corticosterone-treated individuals had a higher skin swelling response. We found no delayed inter-generational effects on demographic traits of offspring. Our study demonstrates the potential for long-lasting physiological consequences of chronic corticosterone enhancement despite no obvious changes in life history.

When water interacts with temperature: Ecological and evolutionary implications of thermo-hydroregulation in terrestrial ectotherms.

The regulation of body temperature (thermoregulation) and of water balance (defined here as hydroregulation) are key processes underlying ecological and evolutionary responses to climate fluctuations in wild animal populations. In terrestrial (or semiterrestrial) ectotherms, thermoregulation and hydroregulation closely interact and combined temperature and water constraints should directly influence individual performances. Although comparative physiologists traditionally investigate jointly water and temperature regulation, the ecological and evolutionary implications of these coupled processes have so far mostly been studied independently. Here, we revisit the concept of thermo-hydroregulation to address the functional integration of body temperature and water balance regulation in terrestrial ectotherms. We demonstrate how thermo-hydroregulation provides a framework to investigate functional adaptations to joint environmental variation in temperature and water availability, and potential physiological and/or behavioral conflicts between thermoregulation and hydroregulation. We extend the classical cost-benefit model of thermoregulation in ectotherms to highlight the adaptive evolution of optimal thermo-hydroregulation strategies. Critical gaps in the parameterization of this conceptual optimality model and guidelines for future empirical research are discussed. We show that studies of thermo-hydroregulation refine our mechanistic understanding of physiological and behavioral plasticity, and of the fundamental niche of the species. This is illustrated with relevant and recent examples of space use and dispersal, resource-based trade-offs, and life-history tactics in insects, amphibians, and nonavian reptiles.

Some like it dry: Water restriction overrides heterogametic sex determination in two reptiles.

ABSTRACT: The evolution of sex determination is complex and yet crucial in our understanding of population stability. In ectotherms, sex determination involves a variety of mechanisms including genetic determination (GSD), environment determination (ESD), but also interactions between the two via sex reversal. In this study, we investigated whether water deprivation during pregnancy could override GSD in two heterogametic squamate reptiles. We demonstrated that water restriction in early gestation induced a male-biased secondary sex ratio in both species, which could be explained by water sex reversal as the more likely mechanism. We further monitored some long-term fitness estimates of offspring, which suggested that water sex determination (WSD) represented a compensatory strategy producing the rarest sex according to Fisher's assumptions of frequency-dependent selection models. This study provides new insights into sex determination modes and calls for a general investigation of mechanisms behind WSD and to examine the evolutionary implications. OPEN RESEARCH BADGES: This article has earned an Open Data Badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.mv06pv1.