Sensitivity of amphibian embryos to timing and magnitude of present and future thermal extremes.

Ongoing climate change is increasing the frequency and intensity of extreme temperature events. Unlike the gradual increase on average environmental temperatures, these short-term and unpredictable temperature extremes impact population dynamics of ectotherms through their effect on individual survival. While previous research has predominantly focused on the survival rate of terrestrial embryos under acute heat stress, less attention has been dedicated to the nonlethal effects of ecologically realistic timing and magnitude of temperature extremes on aquatic embryos. In this study, we investigated the influence of the timing and magnitude of current and projected temperature extremes on embryonic life history traits and hatchling behavior in the alpine newt, Ichthyosaura alpestris. Using a factorial experiment under controlled laboratory conditions, we exposed 3- or 10-day-old embryos to different regimes of extreme temperatures for 3 days. Our results show that exposure to different extreme temperature regimes led to a shortened embryonic development time and an increase in hatchling length, while not significantly affecting embryonic survival. The duration of development was sensitive to the timing of temperature extremes, as early exposure accelerated embryo development. Exposure to temperature extremes during embryonic development heightened the exploratory activity of hatched larvae. We conclude that the timing and magnitude of ecologically realistic temperature extremes during embryogenesis have nonlethal effects on life history and behavioral traits. This suggests that species' vulnerability to climate change might be determined by other ecophysiological traits beyond embryonic thermal tolerance in temperate pond-breeding amphibians.

Impacts of behaviour and acclimation of metabolic rate on energetics in sheltered ectotherms: a climate change perspective.

Many ectothermic organisms counter harsh abiotic conditions by seeking refuge in underground retreats. Variations in soil hydrothermal properties within these retreats may impact their energy budget, survival and population dynamics. This makes retreat site choice a critical yet understudied component of their strategies for coping with climate change. We used a mechanistic modelling approach to explore the implications of behavioural adjustments and seasonal acclimation of metabolic rate on retreat depth and the energy budget of ectotherms, considering both current and future climate conditions. We used a temperate amphibian, the alpine newt (Ichthyosaura alpestris), as a model species. Our simulations predict an interactive influence of different thermo- and hydroregulatory strategies on the vertical positioning of individuals in underground refuges. The adoption of a particular strategy largely determines the impact of climate change on retreat site choice. Additionally, we found that, given the behavioural thermoregulation/hydroregulation and metabolic acclimation patterns considered, behaviour within the retreat has a greater impact on ectotherm energetics than acclimation of metabolic rate under different climate change scenarios. We conclude that further empirical research aimed at determining ectotherm behavioural strategies during both surface activity and inactivity is needed to understand their population dynamics and species viability under climate change.

Individual variation in thermally induced plasticity of metabolic rates: ecological and evolutionary implications for a warming world.

Energy metabolism is a fundamental property of life providing the energy for all processes and functions within an organism. As it is temperature-dependent, it mediates the effects of changing climate on ectotherm fitness and population dynamics. Though resting metabolic rate is a highly labile trait, part of its variation is individually consistent. Recent findings show that resting metabolic rate contains consistent variation not only in the elevations (intercepts) but also in the slopes of individual thermal dependence curves, challenging the thermal dependence assumption for this trait in several ectotherm taxa. I argue that among-individual variation in thermal metabolic curves represents a previously undetected component of ectotherm response to climate change, potentially affecting their adaptive capacity and population resilience under increasing stochasticity of thermal environment. Future studies need to examine not only the amount of among-individual variation in thermal metabolic curves across phylogenetic contexts but also other aspects concerning its mechanisms and adaptive significance to improve predictions about the impact of climate change on ectotherm population dynamics. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Terrestrial amphibians respond to rapidly changing temperatures with individual plasticity of exploratory behaviour.

Terrestrial ectotherms react to acute changes in environmental temperatures by adjusting their behaviour. Evaluating the adaptive potential of these behavioural adjustments requires information on their repeatability and plasticity. We examined behavioural response (exploration) to acute temperature change in two amphibian taxa, alpine (Ichthyosaura alpestris) and smooth (Lissotriton vulgaris) newts. These responses were investigated at both population and individual levels under multiple thermal contexts (dimensions), represented by the direction and range of changing temperature and rearing thermal regimes. Population-level analyses showed species-specific, non-additive effects of direction and range of temperature change on acute thermal reaction norms for exploration, but explained only a low amount (7-23%) of total variation in exploration. In contrast, within- and among-individual variation in acute thermal reaction norm parameters explained 42-50% of total variation in the examined trait. Although immediate thermal responses varied among individuals (repeatability = 0.07 to 0.53), they were largely shaped by environmental contexts during repeated trials. We conclude that these amphibians respond to acute temperature change through individual plasticity of behavioural traits. A repeated-measures approach under multiple thermal contexts will be needed to identify the selective and plastic potential of behavioural responses used by juvenile newts and perhaps other ectotherm taxa to cope with rapidly changing environmental temperatures.

Ontogeny, phylogeny and mechanisms of adaptive changes in evaporative water loss in geckos.

Body size dependence of metabolic rate, body surface and scale morphology complicate disentangling the contribution of these characteristics to adaptive changes in total evaporative water loss (TEWL) of reptiles. To separate adaptive changes from size-related dependence, we compared intra- and interspecific scaling of several candidate traits in eyelid geckos (Eublepharidae), a group exhibiting large variation in body size and TEWL. The intraspecific allometry of TEWL of a eublepharid species fits the geometric surface-mass relationship. However, evolutionary shifts to both higher and lower evaporation were strongly correlated with habitat aridity and cannot be explained by shifts in body size alone. The intraspecific allometry of standard metabolic rate is nearly the same as the interspecific allometry. Unlike for mammals and birds, this pattern rules out respiratory water loss as a driver of the adaptive changes in TEWL among eublepharids. Scale morphology was independent of TEWL variation as well, but the correlation between cutaneous water loss and TEWL suggests a crucial role of skin permeability in adaptation to habitat aridity. Our analyses demonstrate how powerful a comparison between intra- and interspecific allometries can be for detecting body size-dependent mechanisms of adaptive changes in ecophysiological traits correlated with body size.

Thermal dependence and individual variation in tonic immobility varies between sympatric amphibians.

Tonic immobility (TI) is an important antipredator response employed by prey in the last stages of a predation sequence. Evolution by natural selection assumes consistent individual variation (repeatability) in this trait. In ectotherms, which experience variable body temperatures, TI should be repeatable over a thermal gradient to be targeted by natural selection; however, information on thermal repeatability of this trait is missing. We examined thermal repeatability of TI in juveniles of two sympatric amphibians, smooth (Lissotriton vulgaris) and alpine (Ichthyosaura alpestris) newts. Both species showed disparate TI responses to body temperature variation (13-28 °C). While the proportion of TI response was repeatable in both taxa, it increased with body temperature in alpine newts but was temperature independent in smooth newts. Duration of TI decreased with body temperature in both taxa but was only repeatable in smooth newts. Our results suggest that a warming climate may affect population dynamics of sympatric ectotherms through asymmetry in thermal reaction norms for antipredator responses.

Repeatability and heritability of resting metabolic rate in a long-lived amphibian.

Resting metabolic rate (RMR), i.e. spent energy necessary to maintain basic life functions, is a basic component of energy budget in ectotherms. The evolution of RMR through natural selection rests on the premise of its non-zero repeatability and heritability, i.e. consistent variation within individual lifetimes and resemblance between parents and their offspring, respectively. Joint estimates of RMR repeatability and heritability are missing in ectotherms, however, which precludes estimations of the evolutionary potential of this trait. We examined RMR repeatability and heritability in a long-lived ectotherm, the alpine newt (Ichthyosaura alpestris). Individual RMR was repeatable over both six-month (0.28 ±â€¯0.09 [SE]) and five-year (0.16 ±â€¯0.07) periods. While there was no resemblance between parent and offspring RMR (0.21 ±â€¯0.34), the trait showed similarity among offspring within families (broad-sense heritability; 0.25 ±â€¯0.09). Similar repeatability and broad-sense heritability values in parental and offspring generations, respectively, and non-conclusive narrow-sense heritability suggest the contribution of non-additive genetic factors to total phenotypic variance in this trait. We conclude that RMR evolutionary trajectories are shaped by other processes than natural selection in this long-lived ectotherm.

Impacts of predator-induced behavioural plasticity on the temperature dependence of predator-prey activity and population dynamics.

Predation is a key ecological interaction affecting populations and communities. Climate warming can modify this interaction both directly by the kinetic effects of temperature on biological rates and indirectly through integrated behavioural and physiological responses of the predators and prey. Temperature dependence of predation rates can further be altered by predator-induced plasticity of prey locomotor activity, but empirical data about this effect are lacking. We propose a general framework to understand the influence of predator-induced developmental plasticity on behavioural thermal reaction norms in prey and their consequences for predator-prey dynamics. Using a mesocosm experiment with dragonfly larvae (predator) and newt larvae (prey), we tested if the predator-induced plasticity alters the elevation or the slope of the thermal reaction norms for locomotor activity metrics in prey. We also estimated the joint predator-prey thermal response in mean locomotor speed, which determines prey encounter rate, and modelled the effect of both phenomena on predator-prey population dynamics. Thermal reaction norms for locomotor activity in prey were affected by predation risk cues but with minor influence on the joint predator-prey behavioural response. We found that predation risk cues significantly decreased the intercept of thermal reaction norm for total activity rate (i.e. all body movements) but not the other locomotor activity metrics in the prey, and that prey locomotor activity rate and locomotor speed increased with prey density. Temperature had opposite effects on the mean relative speed of predator and prey as individual speed increased with temperature in predators but decreased in prey. This led to a negligible effect of body temperature on predicted prey encounter rates and predator-prey dynamics. The behavioural component of predator-prey interaction varied much more between individuals than with temperature and the presence of predation risk cues in our system. We conclude that within-population variation in locomotor activity can buffer the influence of body temperature and predation risk cues on predator-prey interactions, and further research should focus on the magnitude and sources of behavioural variation in interacting species to predict the impact of climate change on predator-prey interactions and food web dynamics.

Underwater sound production varies within not between species in sympatric newts.

Sound production is a widespread phenomenon among animals. Effective sound use for mate or species recognition requires some acoustic differentiation at an individual or species level. Several species of caudate amphibians produce underwater sounds, but information about intra- and interspecific variation in their acoustic production is missing. We examined individual, sex, and species variation in underwater sound production in adults of two sympatric newt taxa, Ichthyosaura alpestris and Lissotriton vulgaris. Individual newts produced simple low- (peak frequency = 7-8 kHz) and mid-high frequency (14-17 kHz) clicks, which greatly overlap between sexes and species. Individual differences explained about 40-50% of total variation in sound parameters. These results provide foundations for further studies on the mechanisms and eco-evolutionary consequences of underwater acoustics in newts.

Repeatability of thermal reaction norms for spontaneous locomotor activity in juvenile newts.

Locomotor activity is a major attribute of animals. Although this trait determines important ecological processes, such as dispersal and species interactions, the sources of its variation are not fully understood. We examined the influence of body temperature (13, 18, 23, and 28 °C) and individual identity on spontaneous locomotor activity in juvenile alpine newts, Ichthyosaura alpestris, over three consecutive weeks. Locomotor activity was characterized by four parameters: distance covered, mean velocity, frequency of movements, and total activity rate (all directional and non-directional movements). Apart from total activity rate, thermal reaction norms for locomotor parameters had convex or concave curvilinear shapes. During the first trial series, i.e. across the four body temperatures that were tested, individual identity explained less variation in thermal reaction norms than during the second series. Individual means, i.e. the vertical positions of individual thermal reaction norms, were repeatable between trial series in all locomotor activity parameters but the frequency of movements. We conclude that spontaneous locomotor activity is a complex trait, which can be characterized by several parameters with varying individual repeatability and thermal dependency. This information should be considered for planning further locomotor activity experiments, conservation strategies, and modeling ectotherm responses to climate change.

Limited differentiation of fundamental thermal niches within the killifish assemblage from shallow temporary waters.

The coexistence of ectothermic species is enabled among other factors by the differentiation of their thermal niches. While this phenomenon is well described from deep temperate lakes, it is unclear whether the same pattern applies to temporary pools. In this study, we examined fundamental thermal niches in three coexisting annual killifish species Nothobranchius furzeri, N. orthonotus and N. pienaari from temporary pools in southern Mozambique. We hypothesized that the disparate thermal requirements of the three congeneric species are a candidate niche component that facilitates their local coexistence. We estimated species' thermal requirements as preferred body temperatures (Tpref) in a horizontal thermal gradient. Under thermal gradient conditions, sympatric killifish maintained their body temperatures within similar Tpref ranges despite some variation in mean Tpref. The daily variation in water temperature in their native habitats enables killifish to thermoregulate at least for part of the diurnal cycle. We conclude that the coexistence of African annual killifish species is possible without the differentiation of their fundamental thermal niches.

No trade-offs in interspecific interference ability and predation susceptibility in newt larvae.

Coexistence of species with similar requirements is allowed, among others, through trade-offs between competitive ability and other ecological traits. Although interspecific competition is based on two mechanisms, exploitation of resources and physical interference, trade-off studies largely consider only species' ability to exploit resources. Using a mesocosm experiment, we examined the trade-off between interference competition ability and susceptibility to predation in larvae of two newt species, Ichthyosaura alpestris and Lissotriton vulgaris. In the presence of heterospecifics, L. vulgaris larvae slowed somatic growth and developmental rates, and experienced a higher frequency of injuries than in conspecific environments which suggests asymmetrical interspecific interference. During short-term predation trials, L. vulgaris larvae suffered higher mortality than I. alpestris. Larvae of the smaller species, L. vulgaris, had both lower interference and antipredator performance than the larger I. alpestris, which suggests a lack of trade-off between interference competition ability and predator susceptibility. We conclude that interference competition may produce a positive rather than negative relationship with predation susceptibility, which may contribute to the elimination of subordinate species from common habitats.

Costly neighbours: Heterospecific competitive interactions increase metabolic rates in dominant species.

The energy costs of self-maintenance (standard metabolic rate, SMR) vary substantially among individuals within a population. Despite the importance of SMR for understanding life history strategies, ecological sources of SMR variation remain only partially understood. Stress-mediated increases in SMR are common in subordinate individuals within a population, while the direction and magnitude of the SMR shift induced by interspecific competitive interactions is largely unknown. Using laboratory experiments, we examined the influence of con- and heterospecific pairing on SMR, spontaneous activity, and somatic growth rates in the sympatrically living juvenile newts Ichthyosaura alpestris and Lissotriton vulgaris. The experimental pairing had little influence on SMR and growth rates in the smaller species, L. vulgaris. Individuals exposed to con- and heterospecific interactions were more active than individually reared newts. In the larger species, I. alpestris, heterospecific interactions induced SMR to increase beyond values of individually reared counterparts. Individuals from heterospecific pairs and larger conspecifics grew faster than did newts in other groups. The plastic shift in SMR was independent of the variation in growth rate and activity level. These results reveal a new source of individual SMR variation and potential costs of co-occurrence in ecologically similar taxa.

An energetic perspective on tissue regeneration: The costs of tail autotomy in growing geckos.

Tail autotomy is a crucial antipredatory lizard response, which greatly increases individual survival, but at the same time also compromises locomotor performance, sacrifices energy stores and induces a higher burden due to the ensuing response of regenerating the lost body part. The potential costs of tail autotomy include shifts in energy allocation and metabolic rates, especially in juveniles, which invest their energy primarily in somatic growth. We compared the metabolic rates and followed the growth of juvenile males with and without regenerating tails in the Madagascar ground gecko (Paroedura picta), a nocturnal ground-dwelling lizard. Geckos with intact tails and those that were regrowing them grew in snout-vent-length at similar rates for 22weeks after autotomy. Tail regeneration had a negligible influence on body mass-corrected metabolic rate measured at regular intervals throughout the regenerative process. We conclude that fast-growing juveniles under the conditions of unrestricted food can largely compensate for costs of tail loss and regeneration in their somatic growth without a significant impact on the total individual body mass-corrected metabolic rate.

Economic thermoregulatory response explains mismatch between thermal physiology and behaviour in newts.

Temperature is an important factor determining distribution and abundance of organisms. Predicting the impact of warming climate on ectotherm populations requires information about species' thermal requirements, i.e. their so-called 'thermal niche'. The characterization of thermal niche remains a complicated task. We compared the applicability of two indirect approaches, based on reaction norm (aerobic scope curve) and optimality (preferred body temperature) concepts, for indirect estimation of thermal niche while using newts, Ichthyosaura alpestris, as a study system. If the two approaches are linked, then digesting newts should keep their body temperatures close to values maximizing aerobic scope for digestion. After feeding, newts maintained their body temperatures within a narrower range than did hungry individuals. The range of preferred body temperatures was well below the temperature maximizing aerobic scope for digestion. Optimal temperatures for factorial aerobic scope fell within the preferred body temperature range of digesting individuals. We conclude that digesting newts prefer body temperatures that are optimal for the maximum aerobic performance but relative to the maintenance costs. What might be termed the 'economic' thermoregulatory response explains the mismatch between thermal physiology and behaviour in this system.

Variation in winter metabolic reduction between sympatric amphibians.

Distribution and abundance of temperate ectotherms is determined, in part, by the depletion of their limited caloric reserves during wintering. The magnitude of winter energy drain depends on the species-specific capacity to seasonally modify the minimal maintenance costs. We examined seasonal variation of minimum oxygen consumption between two newt species, Ichthyosaura alpestris and Lissotriton vulgaris. Oxygen consumption was measured in both species during their active season (daily temperature range=12-22°C) and wintering period (4°C) at 4°C and 8°C. The seasonal reduction in metabolic rates differed between species and experimental temperatures. Wintering newts reduced their metabolic rates at 4°C and 8°C in I. alpestris, but only at 8°C in L. vulgaris. Both species reduced the thermal sensitivity of oxygen consumption during wintering. Theoretical calculations of winter depletion of caloric reserves under various thermal conditions revealed that seasonal metabolic reduction is more effective in I. alpestris than in L. vulgaris, and its effectiveness will increase with the proportion of warmer days during wintering period. The variation in winter metabolic reduction between sympatric newt species potentially contributes to their distribution patterns and population dynamics under climate change.

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 (Tp) between reproductive (egg-laying) and non-reproductive female newts, Ichthyosaura alpestris. Next, we exposed reproductive females to temperatures mimicking Tp 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.

Body size, swimming speed, or thermal sensitivity? Predator-imposed selection on amphibian larvae.

BACKGROUND: Many animals rely on their escape performance during predator encounters. Because of its dependence on body size and temperature, escape velocity is fully characterized by three measures, absolute value, size-corrected value, and its response to temperature (thermal sensitivity). The primary target of the selection imposed by predators is poorly understood. We examined predator (dragonfly larva)-imposed selection on prey (newt larvae) body size and characteristics of escape velocity using replicated and controlled predation experiments under seminatural conditions. Specifically, because these species experience a wide range of temperatures throughout their larval phases, we predict that larvae achieving high swimming velocities across temperatures will have a selective advantage over more thermally sensitive individuals. RESULTS: Nonzero selection differentials indicated that predators selected for prey body size and both absolute and size-corrected maximum swimming velocity. Comparison of selection differentials with control confirmed selection only on body size, i.e., dragonfly larvae preferably preyed on small newt larvae. Maximum swimming velocity and its thermal sensitivity showed low group repeatability, which contributed to non-detectable selection on both characteristics of escape performance. CONCLUSIONS: In the newt-dragonfly larvae interaction, body size plays a more important role than maximum values and thermal sensitivity of swimming velocity during predator escape. This corroborates the general importance of body size in predator-prey interactions. The absence of an appropriate control in predation experiments may lead to potentially misleading conclusions about the primary target of predator-imposed selection. Insights from predation experiments contribute to our understanding of the link between performance and fitness, and further improve mechanistic models of predator-prey interactions and food web dynamics.

Thermoregulatory strategies in an aquatic ectotherm from thermally-constrained habitats: An evaluation of current approaches.

Many ectotherms employ diverse behavioral adjustments to effectively buffer the spatio-temporal variation in environmental temperatures, whereas others remain passive to thermal heterogeneity. Thermoregulatory studies are frequently performed on species living in thermally benign habitats, which complicate understanding of the thermoregulation-thermoconformity continuum. The need for new empirical data from ectotherms exposed to thermally challenging conditions requires the evaluation of available methods for quantifying thermoregulatory strategies. We evaluated the applicability of various thermoregulatory indices using fire salamander larvae, Salamandra salamandra, in two aquatic habitats, a forest pool and well, as examples of disparate thermally-constrained environments. Water temperatures in the well were lower and less variable than in the pool. Thermal conditions prevented larvae from reaching their preferred body temperature range in both water bodies. In contrast to their thermoregulatory abilities examined in a laboratory thermal gradient, field body temperatures only matched the mean and range of operative temperatures, showing thermal passivity of larvae in both habitats. Despite apparent thermoconformity, thermoregulatory indices indicated various strategies from active thermoregulation, to thermoconformity, and even thermal evasion, which revealed their limited applicability under thermally-constrained conditions. Salamander larvae abandoned behavioral thermoregulation despite varying opportunities to increase their body temperature above average water temperatures. Thermoconformity represents a favored strategy in these ectotherms living in more thermally-constrained environments than those examined in previous thermoregulatory studies. To understand thermal ecology and its impact on population dynamics, the quantification of thermoregulatory strategies of ectotherms in thermally-constrained habitats requires the careful choice of an appropriate method to avoid misleading results.