Thermal Sensitivity Of Locomotor Performance Research Articles

Intra and interspecific variation in thermal performance and critical limits in anurans from southern Chile

The relationship between temperature and performance can be illustrated through a thermal performance curve (TPC), which has proven useful in describing various aspects of ectotherms' thermal ecology and evolution. The parameters of the TPC can vary geographically due to large-scale variations in environmental conditions. However, only some studies have attempted to quantify how thermal performance varies over relatively small spatial scales, even in the same location or consistently among individuals within a species. Here, we quantified individual and species variation in thermal sensitivity of locomotor performance in five amphibia Eupsophus species found in the temperate rainforests of southern Chile and compared their estimates against co-occurring species that exhibit a substantially more extensive distributional range. We measured critical thermal limits and jumping performance under five different temperatures. Our results suggest that thermal responses are relatively conserved along the phylogeny, as the locomotor performance and thermal windows for activity remained narrow in Eupsophus species when compared against results observed for Batrachyla taeniata and Rhinella spinulosa. Additionally, we found significant individual differences in locomotor performance within most species, with individual consistency in performance observed across varied temperatures. Further analyses explored the influence of body size on locomotor performance and critical thermal limits within and between species. Our results suggest a trade-off scenario between thermal tolerance breadth and locomotor performance, where species exhibiting broader thermal ranges might have compromised performance. Interestingly, these traits seem partly mediated by body size variations, raising questions about potential ecological implications.

Physiological thermal responses of three Mexican snakes with distinct lifestyles.

The impact of temperature on reptile physiology has been examined through two main parameters: locomotor performance and metabolic rates. Among reptiles, different species may respond to environmental temperatures in distinct ways, depending on their thermal sensitivity. Such variation can be linked to the ecological lifestyle of the species and needs to be taken into consideration when assessing the thermal influence on physiology. This is particularly relevant for snakes, which are a very functionally diverse group. In this study, our aim was to analyze the thermal sensitivity of locomotor performance and resting metabolic rate (RMR) in three snake species from central Mexico (Crotalus polystictus, Conopsis lineata, and Thamnophis melanogaster), highlighting how it is influenced by their distinctive behavioral and ecological traits. We tested both physiological parameters in five thermal treatments: 15 °C, 25 °C, 30 °C, 33 °C, and 36 °C. Using the performance data, we developed thermal performance curves (TPCs) for each species and analyzed the RMR data using generalized linear mixed models. The optimal temperature for locomotion of C. polystictus falls near its critical thermal maximum, suggesting that it can maintain performance at high temperatures but with a narrow thermal safety margin. T. melanogaster exhibited the fastest swimming speeds and the highest mass-adjusted RMR. This aligns with our expectations since it is an active forager, a high energy demand mode. The three species have a wide performance breadth, which suggests that they are thermal generalists that can maintain performance over a wide interval of temperatures. This can be beneficial to C. lineata in its cold habitat, since such a characteristic has been found to allow some species to maintain adequate performance levels in suboptimal temperatures. RMR increased along with temperature, but the proportional surge was not uniform since thermal sensitivity measured through Q10 increased at the low and high thermal treatments. High Q10 at low temperatures could be an adaptation to maintain favorable performance in suboptimal temperatures, whereas high Q10 at high temperatures could facilitate physiological responses to heat stress. Overall, our results show different physiological adaptations of the three species to the environments they inhabit. Their different activity patterns and foraging habits are closely linked to these adaptations. Further studies of other populations with different climatic conditions would provide valuable information to complement our current understanding of the effect of environmental properties on snake physiology.

Comparative thermal sensitivity of locomotor performance and vulnerability to global warming of two sympatric Phymaturus lizards from cold environments of Patagonia (Argentina)

Abstract Sister species that live in sympatry provide the possibility to analyse the level of divergence in their ecological, physiological and life-history traits and how they can coexist without out-competing each other. We studied the thermal sensitivity of locomotor performance in the sympatric lizards Phymaturus querque and Phymaturus zapalensis from Patagonia, Argentina. We measured morphological traits relevant to locomotor performance and the running speed at different body temperatures, and we estimated the critical thermal minimum (CTmin) and maximum (CTmax) at which running performance equals zero. We obtained the maximum speeds, the temperature at which the performance is maximized (optimal temperature, To) and the temperature range over which an individual performs 50% and 80% of their maximal performance (B50 and B80). Also, we recorded the availability of thermal microenvironments for thermoregulation (operative temperatures) and calculated two indices of vulnerability to global warming. Phymaturus zapalensis and P. querque exhibited differences in most of the morphological traits relevant to locomotor performance. Both species presented similar values of To, CTmin and CTmax, but B50 and B80 were broader in P. zapalensis. During the warmest month, the environmental temperatures are already higher than the physiological optimal temperature, indicating that populations could currently be facing challenges in the context of global warming.

Experimental manipulation of microbiota reduces host thermal tolerance and fitness under heat stress in a vertebrate ectotherm

Identifying factors that influence how ectothermic animals respond physiologically to changing temperatures is of high importance given current threats of global climate change. Host-associated microbial communities impact animal physiology and have been shown to influence host thermal tolerance in invertebrate systems. However, the role of commensal microbiota in the thermal tolerance of ectothermic vertebrates is unknown. Here we show that experimentally manipulating the tadpole microbiome through environmental water sterilization reduces the host's acute thermal tolerance to both heat and cold, alters the thermal sensitivity of locomotor performance, and reduces animal survival under prolonged heat stress. We show that these tadpoles have reduced activities of mitochondrial enzymes and altered metabolic rates compared with tadpoles colonized with unmanipulated microbiota, which could underlie differences in thermal phenotypes. These results demonstrate a strong link between the microbiota of an ectothermic vertebrate and the host's thermal tolerance, performance and fitness. It may therefore be important to consider host-associated microbial communities when predicting species' responses to climate change.

Divergent incubation temperature effects on thermal sensitivity of hatchling performance in two different latitudinal populations of an invasive turtle.

The incubation temperature for embryonic development affects several aspects of hatchling performance, but its impact on the thermal sensitivity of performance attributes remains poorly investigated. In the present study, Trachemys scripta elegans hatchlings from two different latitudinal populations were collected to assess the effects of different incubation temperatures on the locomotor (swimming speed) and physiological (heart rate) performances, and the thermal sensitivity of these two attributes. The incubation temperature significantly affected the examined physiological traits. Hatchling turtles produced at low incubation temperature exhibited relatively higher cold tolerance (lower body temperatures at which the animals lose the ability to escape from the lethal conditions), and reduced heart rate and swimming speed. Furthermore, the effect of incubation temperature on the thermal sensitivity of swimming speed differed between the low- and high-latitude populations. At relatively high incubation temperatures, the high-latitude hatchling turtles exhibited reduced thermal sensitivities of swimming speed than those of the low-latitude ones. Reduced thermal sensitivity of locomotor performance together with high cold tolerance, exhibited by the high-latitude hatchling turtles potentially reflected local adaptation to relatively colder and more thermally-variable environments.

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

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

Potential benefits from global warming to the thermal biology and locomotor performance of an endangered Patagonian lizard.

Global warming can significantly affect many aspects of the biology of animal species, including their thermal physiology and physiological performance. Thermal performance curves provide a heuristic model to evaluate the impacts of temperature on the ecophysiology of ectotherms. When integrated with other thermal biology parameters, they can be used to predict the impacts of climate change on individual fitness and population viability. In this study, we combine holistic measures of thermal physiology and the thermal sensitivity of locomotor performance with environmental temperatures measured at fine scale to estimate the vulnerability to global warming of the endangered Patagonian lizard Phymaturus tenebrosus. Our results indicate that this lizard exhibits its preferred temperatures and maximum locomotor performance at higher temperatures than the mean temperature it currently experiences in its habitat. In addition, it exhibits a low effectiveness of thermoregulation, being a poor thermoregulator. In view of the results obtained, we suggest that the climatic conditions of Patagonia may be advantageous for P. tenebrosus to survive future global warming, since its thermal physiology and locomotor performance may improve under increasing in environmental temperatures in its habitat.

Variation in thermal biology of three closely related lizard species along an elevation gradient

The critical thermal limits of organisms and the thermal sensitivity of their performance tend to vary predictably across latitudinal gradients. There has been comparatively less investigation into variation in thermal biology with elevation, despite similar gradients in environmental temperatures. To redress this, we examined critical thermal limits (CTmin and CTmax), thermal sensitivity of locomotor performance, and shelter site attributes, in three lizard species that replace one another along a contiguous elevation gradient in south-eastern Australia. The species examined consisted of a highland specialist, Liopholis guthega, mid-elevation species, Liopholis montana, and lowland species, Liopholis whitii. We found similar habitat attributes between the species, but L. guthega predominantly occurred in open habitat, which might reflect a strategy for maximizing exposure to insolation. We found intraspecific variation in lizard thermal traits, most notably in cold tolerance of L. guthega and in both heat and cold tolerance of L. whitii, suggesting population-specific variables acting on thermal physiology rather than a species distribution maintained by distinct thermal tolerances. This study represents one of the few examinations of thermal trait variability within and between species with elevation in a temperate system and provides evidence for thermal physiology driven by adaptation and/or physiological plasticity to local conditions.

Altitude influences thermal ecology and thermal sensitivity of locomotor performance in a toad-headed lizard

Population differentiation in ectotherm physiological performance may be driven by adapting to different thermal environments. In this study, we measured locomotor performance in two different altitude populations of the Qinghai toad-headed lizards (Phrynocephalus vlangalii) at different test temperatures to assess between-population differences in thermal sensitivity of sprint speed. Low-elevation lizards ran faster than high-elevation lizards at most test temperatures. Sprint speed varied with test temperature similarly between populations, but the thermal sensitivity (performance breadth) differed significantly. Low-elevation lizards had a lower optimal temperature (Topt) for sprint speed and narrower performance breadth than high-elevation lizards as inferred from the thermal performance curves constructed for each individual. We also measured the body temperature of active lizards (Tb) in the field and selected temperature (Tsel) in the laboratory. Low-elevation lizards had a lower Tsel, and less variable Tb than high-elevation lizards. In both populations, Tsel was lower than Topt for sprint speed, which was inconsistent with the prediction for a match between thermal preference and Topt. Our results suggest that lower thermal sensitivity and weaker locomotor ability for high-elevation lizards may be an adaptive response to the local environmental conditions (e.g., greater thermal variability, higher food availability, and lower predator pressure).

Food, temperature and endurance: effects of food deprivation on the thermal sensitivity of physiological performance

Summary Studies of thermal ecology and physiology (e.g. the change in performance with temperature) provide critical data for predicting the potential responses of ectothermic organisms to climate change. Projected modification of current ambient temperature in the future is expected to result in shifts in whole‐organismal performance, which could lead to a diminishment in individual fitness, resulting in demographic collapse. The anticipated responses of ectothermic organisms to climate change focus on the direct effects of temperature and neglect other potential concomitant changes to the environment. Climate models forecast dramatic alteration in precipitation patterns, which in some regions will lead to prolonged drought. Rising temperatures coupled with decreased rainfall will disrupt patterns of net primary productivity and as a consequence alter the prey base and seasonal food availability. Individuals exposed to lower food availability are expected to adjust thermoregulatory behaviour to reduce their daily energetic expenditures. The consequences of fasting in lizards have received scant attention; consequently, we examined the effects of alteration in food availability on both preferred body temperatures in a thermal gradient and the thermal sensitivity of locomotor performance in the lizard Urosaurus ornatus. We experimentally manipulated food access to two groups of lizards and compared thermal preference and thermal performance curves. We found distinct shifts in preferred body temperature and locomotor performance when food availability is restricted. Fasted lizards exhibited reduced preferred body temperatures compared to fed lizards. The position and shape of thermal performance curves differed between fasted and fed lizards. Fasted lizards had lower optimal temperatures of performance and wider thermal performance breadths than fed lizards. Restricted access to food resources leads to thermal biological patterns favouring lower temperatures. Lizards with low food access may be restricted to shaded regions of their habitat, unable to cope with the stressful situation of activity at warmer temperatures, and thus be at a selective disadvantage for procuring energetic or reproductive opportunities. By characterizing the interaction between thermal physiology and food availability, our study provides more clarification regarding the bioenergetic pressures likely to affect lizards in warmer environments. A lay summary is available for this article.

Quantification of correlational selection on thermal physiology, thermoregulatory behavior, and energy metabolism in lizards.

Phenotypic selection is widely accepted as the primary cause of adaptive evolution in natural populations, but selection on complex functional properties linking physiology, behavior, and morphology has been rarely quantified. In ectotherms, correlational selection on thermal physiology, thermoregulatory behavior, and energy metabolism is of special interest because of their potential coadaptation. We quantified phenotypic selection on thermal sensitivity of locomotor performance (sprint speed), thermal preferences, and resting metabolic rate in captive populations of an ectothermic vertebrate, the common lizard, Zootoca vivipara. No correlational selection between thermal sensitivity of performance, thermoregulatory behavior, and energy metabolism was found. A combination of high body mass and resting metabolic rate was positively correlated with survival and negatively correlated with fecundity. Thus, different mechanisms underlie selection on metabolism in lizards with small body mass than in lizards with high body mass. In addition, lizards that selected the near average preferred body temperature grew faster that their congeners. This is one of the few studies that quantifies significant correlational selection on a proxy of energy expenditure and stabilizing selection on thermoregulatory behavior.

Abiotic constraints on the activity of tropical lizards

Summary Many tropical ectotherms are considered vulnerable to anthropogenic climate change because they have evolved to become thermal specialists. Indeed, several recent studies have suggested that even small increases in mean operative temperature may lead to a reduction in activity and the subsequent extinction of populations. Within the tropics, lizards are considered particularly vulnerable due to the potential for climate change to directly impact physiology and alter community interactions. However, models usually focus on the effects of mean operative temperature at the expense of other climate variables that may also affect lizard physiology. We used daily variation in operative temperature, humidity and wind speed to examine how changes in climate influence activity in two species of lizards from the island of Cayo Menor, Honduras. Anolis lemurinus is a forest species, whereas A. allisoni is an open‐habitat species. We conducted daily surveys for active lizards in habitat typical to each species, while simultaneously measuring operative thermal environments with physical models. The effects of the thermal environment were considered in the context of the thermal sensitivity of locomotor performance for each species and compared with the effects of the hydric (humidity) and convective (wind) environments. When all surveys were combined into a single analysis, the activity of the forest species Anolis lemurinus was positively correlated with wind speed, the spatial heterogeneity of operative temperature, and the mismatch between mean operative temperature and the optimal temperature for sprint performance. Mean operative temperature did significantly affect Anolis lemurinus activity, but only when it was above their thermal optimum. Activity of the open‐habitat species A. allisoni was negatively correlated with wind speed, but was not related to any other climate variable. Whereas the mismatch between mean operative temperature and the thermal optimum for performance predicted the activity level of the forest species in ways partially consistent with its use in models for the response of lizards to climate change, the effects of the abiotic environment were habitat dependent. Our results suggest that successfully predicting the biological impacts of climate change will require holistic models that account for more than changes in mean temperature alone.

Isopods failed to acclimate their thermal sensitivity of locomotor performance during predictable or stochastic cooling.

Most organisms experience environments that vary continuously over time, yet researchers generally study phenotypic responses to abrupt and sustained changes in environmental conditions. Gradual environmental changes, whether predictable or stochastic, might affect organisms differently than do abrupt changes. To explore this possibility, we exposed terrestrial isopods (Porcellio scaber) collected from a highly seasonal environment to four thermal treatments: (1) a constant 20°C; (2) a constant 10°C; (3) a steady decline from 20° to 10°C; and (4) a stochastic decline from 20° to 10°C that mimicked natural conditions during autumn. After 45 days, we measured thermal sensitivities of running speed and thermal tolerances (critical thermal maximum and chill-coma recovery time). Contrary to our expectation, thermal treatments did not affect the thermal sensitivity of locomotion; isopods from all treatments ran fastest at 33° to 34°C and achieved more than 80% of their maximal speed over a range of 10° to 11°C. Isopods exposed to a stochastic decline in temperature tolerated cold the best, and isopods exposed to a constant temperature of 20°C tolerated cold the worst. No significant variation in heat tolerance was observed among groups. Therefore, thermal sensitivity and heat tolerance failed to acclimate to any type of thermal change, whereas cold tolerance acclimated more during stochastic change than it did during abrupt change.

Modeling the consequences of thermal trait variation for the cane toad invasion of Australia

Mechanistic species distribution models (SDMs) are ideally suited for predicting the nonnative distributions of invasive species, but require accurate parameterization of key functional traits. Importantly, any ability of the invader to acclimate or adapt rapidly to local conditions must be incorporated. Our field and laboratory studies measured phenotypic variation and tested for plasticity in the thermal sensitivity of locomotor performance and low-temperature tolerance of adult cane toads Bufo marinus in eastern Australia. We used a biophysical model to explore the adaptive significance of this variation and how it affected distribution predictions. Laboratory trials showed that geographic differences in low-temperature tolerance (i.e., the critical thermal minimum; CTMin) of field-caught toads reflect thermal acclimation, whereas populations differed in the thermal dependence of locomotor performance even after acclimation. Incorporating low-temperature tolerance as a dimension of the fundamental niche reduced the predicted southern distribution. To test whether these factors predicted to be range limiting were consistent with reduced performance for individuals, we used the biophysical model and daily climate data to conduct "virtual transplants." These models predicted that acclimation reduced cold stress by 32-100% for toads sheltering near the ground surface; toads inside burrows could remain above their CTMin, but the required burrow depth increased with latitude. Low-temperature tolerance of the adult phase may constrain the southern range limit of the cane toad in Australia, and plasticity in this trait may have facilitated the southward range expansion.

Putting ourselves in a striped snake's shoes: thermal sensitivity of locomotor performance in a melanistic/striped colour‐dimorphic snake

AbstractIntermorph differences of thermoregulatory abilities in colour‐polymorphic (dimorphic) species have been demonstrated in many ectotherms. Usually, these studies reported slower body warming in pale‐coloured morphs than in dark‐coloured morphs. Under this circumstance, one way in which pale‐coloured individuals can manage their slower body warming is to perform better at lower temperatures than dark‐coloured individuals. If this is the case, the former need not necessarily raise their body temperature to the same level as the latter. Based on this scenario, intermorph differences in thermal sensitivity of performance were examined using the melanistic/striped colour‐dimorphic snake Elaphe quadrivirgata as a model species. As an indication of performance capability, the crawling speed was measured at several temperatures. Although striped individuals exhibited slower body warming than melanistic individuals under experimental conditions, the former did not exhibit faster crawling speed than the latter at lower temperatures. Shape and position of the performance curve were almost identical between melanistic and striped individuals, indicating a highly static nature in thermal sensitivity of crawling. Coupled with the results of field studies, it is suggested that striped individuals manage their slower body warming by efforts of behavioural thermoregulation. The possible significance of ecological performance in the wild was discussed.

The fast and the fractalous: speed and tortuosity trade off in running ants

Summary 1. The thermal sensitivity of locomotor performance has often been described in terms of speed, but the trajectory of locomotion may play an equally important role in capturing prey or escaping predators. Hypotheses based on physical constraints or behavioural plasticity predict relationships between the speed and the tortuosity of running, which should affect the thermal sensitivity of locomotion. 2. We measured the speed and tortuosity of running by leaf-cutter ants over a range of temperatures from 10 ° C to 40 ° C. Tortuosity was estimated by the fractal dimension of each path. 3. As we expected, ants ran faster at higher temperatures, but they also followed straighter (less tortuous) paths. A negative relationship between speed and tortuosity was observed both within and among thermal environments. 4. Both biomechanical and behavioural mechanisms might have caused the observed relationship. Turning at high speeds should be more difficult because of the force needed to overcome inertia, and turning at low speeds could help ants evade a predator. Staged encounters with predators should help to define the ecological significance of the trade-off between speed and tortuosity.

Consequences of Metamorphosis for the Locomotor Performance and Thermal Physiology of the NewtTriturus cristatus

During metamorphosis, most amphibians undergo rapid shifts in their morphology that allow them to move from an aquatic to a more terrestrial existence. Two important challenges associated with this shift in habitat are the necessity to switch from an aquatic to terrestrial mode of locomotion and changes in the thermal environment. In this study, I investigated the consequences of metamorphosis to the burst swimming and running performance of the European newt Triturus cristatus to determine the nature and magnitude of any locomotor trade-offs that occur across life-history stages. In addition, I investigated whether there were any shifts in the thermal dependence of performance between life-history stages of T. cristatus to compensate for changes in their thermal environment during metamorphosis. A trade-off between swimming and running performance was detected across life-history stages, with metamorphosis resulting in a simultaneous decrease in swimming and increase in running performance. Although the terrestrial habitat of postmetamorphic stages of the newt T. cristatus experienced greater daily fluctuations in temperature than the aquatic habitat of the larval stage, no differences in thermal sensitivity of locomotor performance were detected between the larval aquatic and postmetamorphic stages. The absence of variation across life-history stages of T. cristatus may indicate that thermal sensitivity may be a conservative trait across ontogenetic stages in amphibians, but further studies are required to investigate this assertion.

A QUANTITATIVE GENETIC ANALYSIS OF THERMAL SENSITIVITY IN THE LOCOMOTOR PERFORMANCE CURVE OF APHIDIUS ERVI.

The thermal sensitivity of locomotor performance in Aphidius ervi, a parasitic hymenopteran, conforms to the "jack-of-all-trades is master of none" model of specialist-generalist trade-offs. Performance breadth and maximal performance at the phenotypic level are negatively correlated in both sexes. A strong, negative genetic correlation was found for males, but not for females. In males, the broad-sense heritability of performance breadth was about 0.16, and that of maximum walking velocity was about 0.29. Neither heritability was significantly different from zero in females. The broad-sense heritability of body mass was about 0.3 in females and 0.6 in males, with a strong negative genetic correlation between size and maximum velocity in males only. These data provide the first quantitative genetic analysis of performance curves in eukaryotic animals, and one of the few demonstrations of the specialist-generalist trade-off that underlies much theory in evolutionary ecology.