Terrestrial Ectotherms Research Articles

The Semi-Natural Climate Chambers across Latitudes: A Broadly Applicable Husbandry and Experimental System for Terrestrial Ectotherms under Climate Change.

With limited resources and efforts, assessing species' vulnerabilities across various geographic regions before the conservation practice is essential for biodiversity conservation in the context of climate change. One pressing challenge has been establishing natural temperature-manipulated research systems across latitudes. To address this challenge, an innovative infrastructure is developed named the semi-natural climate chambers across latitudes (SCCAL), consisting of semi-natural climate chambers at three latitudes, spanning 27° and 3393km from tropical to temperate regions. Each latitude features eight medium-sized patches for temperature manipulation, organisms rearing, and ecological experiments. Independent of external water and electricity supplies, the SCCAL allows to simulate thermal environments under different climate change scenarios with natural soil moisture. Ecological experiments with Grass lizards successfully are conducted, demonstrating that the SCCAL effectively supports species rearing, responses determining, and the vulnerability assessing. The widespread adoption or development of similar infrastructures is encouraged, which can facilitate the assessment of latitudinal animal vulnerabilities under climate change.

The effect of moisture during development on phenotypes of egg-laying reptiles: a systematic review and meta-analysis.

The embryonic environment is critical for the development of many ectothermic vertebrates, which makes them highly vulnerable to environmental change. Changes in temperature and moisture, in particular, are known to influence embryo survival and offspring phenotypes. Although most papers concerning phenotypic development of terrestrial ectotherms focus on the role of temperature on eggs and embryos, the comparatively small number of studies on the effects of substrate moisture are well suited for quantitative analysis aimed at guiding future research. To accomplish this goal, we compiled data from 37 studies on 28 different reptile species and used a meta-analytic approach to quantify the effect of substrate moisture on several offspring outcomes: hatching success (survival), incubation duration, hatchling mass and length, and sex ratio. We found that substrate moisture had a small effect across most traits but significantly affected body size (i.e. length and mass), with wetter conditions producing longer and heavier hatchlings. Temperature also moderated the effect of moisture on hatching success, with higher temperatures resulting in lower success. Additionally, the effect of moisture on hatching success and hatchling mass was enhanced by larger differences in moisture concentration between treatments, yet the effect was small. Lastly, substrate moisture affected sex ratio in turtles, but not in other squamates. Overall, these analyses provide a foundation for further research investigating the effects of moisture on oviparous reptile development. Increasing the diversity of environmental variables for which we understand their impact on animal phenotype will be beneficial in an era with wide-ranging global change.

Insect size responses to climate change vary across elevations according to seasonal timing.

Body size declines are a common response to warming via both plasticity and evolution, but variable size responses have been observed for terrestrial ectotherms. We investigate how temperature-dependent development and growth rates in ectothermic organisms induce variation in size responses. Leveraging long-term data for six montane grasshopper species spanning 1,768-3 901 m, we detect size shifts since ~1960 that depend on elevation and species' seasonal timing. Size shifts have been concentrated at low elevations, with the early emerging species (those that overwinter as juveniles) increasing in size, while later season species are becoming smaller. Interannual temperature variation accounts for the size shifts. The earliest season species may be able to take advantage of warmer conditions accelerating growth during early spring development, whereas warm temperatures may adversely impact later season species via mechanisms such as increased rates of energy use or thermal stress. Grasshoppers tend to capitalize on warm conditions by both getting bigger and reaching adulthood earlier. Our analysis further reinforces the need to move beyond expectations of universal responses to climate change to consider how environmental exposure and sensitivity vary across elevations and life histories.

Novel method to investigate thermal exchange rates in small, terrestrial ectotherms: A proof-of-concept on the gecko Tarentola mauritanica.

Thermoregulating ectotherms may resort to different external heat sources to modulate their body temperature through an array of behavioural and physiological adaptations which modulate heat exchange with the environment and its distribution across the animal's body. Even small-bodied animals are capable of fine control over such rates and the subsequent re-allocation of heat across the body. Such thermal exchanges with the environment usually happen through two non-mutually exclusive modes: heliothermy (radiant heat gain from the sun) or thigmothermy (heat gained or lost via conduction). Classically, the study of these phenomena has relied on invasive methodologies which often disregard the effect of stress, behaviour and regional heterothermy on the rates and patterns of thermal exchange across the body of the animal. This study proposes a novel experimental methodology, capitalising on thermography, to provide an alternative method to less invasively obtain reliable body temperatures of thermoregulating ectotherms, while allowing behaviour and heating mode to be considered when quantifying thermal exchange rates. This methodology was tested in the gecko Tarentola mauritanica, where twenty males were allowed to heat up and cool down under a novel experimental set-up which isolates heliothermic and thigmothermic processes, while being recorded with a thermal camera. The study revealed differences in the heating and cooling rates of several body parts per treatment suggesting that thermal exchanges are complex even in small ectotherms. Ultimately, the described set-up provides the opportunity to revisit classical questions with a less invasive and more flexible experimental approach, enabling heliothermic and thigmothermic processes to be disentangled. The described methodology also better integrates behaviour and physiology while obtaining higher temporal and spatial resolution of body temperatures in a thermoregulating ectotherm.

Winter break? The effect of overwintering on immune gene expression in wood frogs

Winter break? The effect of overwintering on immune gene expression in wood frogs

Thermal adaptation affects the temperature-dependent toxicity of the insecticide imidacloprid to soil invertebrates

Thermal adaptation affects the temperature-dependent toxicity of the insecticide imidacloprid to soil invertebrates

Acclimation to moderate temperatures can have strong negative impacts on heat tolerance of arctic arthropods

Abstract The Arctic is impacted by some of the fastest temperature changes observed on Earth, but the impact on the terrestrial arthropod fauna is unclear. Acute physiological thermal limits of terrestrial ectotherms from high latitudes often exceed the local air temperatures, suggesting that they may be able to cope with increasing temperatures. However, knowledge on how Arctic terrestrial arthropods cope with elevated temperatures for longer periods is lacking. Here we investigate how acclimation temperature and exposure time affect the acute physiological heat tolerance of five terrestrial arthropod species (Neomolgus littoralis, Megaphorura arctica, Nysius groenlandicus, Psammotettix lividellus and Nabis flavomarginatus) immediately after collection in Arctic and sub‐Arctic habitats. We show that although acute heat tolerances are relatively high, even exposure to moderate (temperature span assessed ca. 3–29°C) acclimation temperatures for a 24 h period have strong negative effects on heat tolerance for four of the five species. Similarly, exposure time negatively affected heat tolerance, but depending on species and temperature. Together our results suggest that exposure to even moderately elevated temperatures for periods of 24 h or even shorter can lead to lower acute heat tolerance for cold adapted terrestrial arthropod species from sub‐Arctic and Arctic regions. Consequently, climate change leading to extended periods of mildly elevated temperatures may have strong negative effects on these species. We argue that this aspect is currently overlooked when assessing the ability of arthropods from Arctic and sub‐Artic regions to cope with climate changes as such predictions are typically based on acute heat tolerance estimates and with the assumption of beneficial acclimation responses. Read the free Plain Language Summary for this article on the Journal blog.

3D printed models are an accurate, cost-effective, and reproducible tool for quantifying terrestrial thermal environments

3D printed models are an accurate, cost-effective, and reproducible tool for quantifying terrestrial thermal environments

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

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

Negative effects of the spatial clumping of thermal resources on lizard thermoregulation in a fragmented habitat

Negative effects of the spatial clumping of thermal resources on lizard thermoregulation in a fragmented habitat

The role of body mass in limiting post heat-coma recovery ability in terrestrial ectotherms.

Under global warming, animal species show shrinking body size responses, cascading deep changes in community structure and ecosystem functions. Although the exact physiological mechanisms behind this phenomenon remain unsolved, smaller individuals may benefit from warming climate more than larger ones. Heat-coma, a physiological state with severe consequences on locomotion ability, is often considered as an "ecological death" scenario under which individuals are unable to escape and exposed to predation, further heat injury, and other hazards. Species are expected to increasingly encounter heat-coma temperature thresholds under warming climate, and body size may be an important trait for thermoregulation in particular for ectotherms. The relationship between heat-coma and shrinking body size remains, however, unclear. Yet, recovery after short-term heat-coma is possible, but little is known about its importance in thermal adaptation and how organismal size correlates with post heat-coma recovery. Here, using ants as a model system, we firstly examined the fate of heat-comatose individuals under field conditions to quantify the ecological benefits of post heat-coma recovery. Then, we quantified ants' recovery ability after heat-coma using a dynamic thermal assay in the laboratory and asked if thermal resilience varies between species with different body mass. Our results confirm that heat-coma represents an inherent ecological death where individuals failed to recover from coma suffer strong predation pressure. Additionally, following phylogenetic signals inclusion, organisms with small mass were more likely to recover, supporting the temperature-size rule in thermal adaptation and recent studies showing a decrease in body size composition of ectotherm community under warmer climatic conditions. Body size as a fundamental trait in ecology thus affects ectotherm survival under thermal stress, which may drive species body size adaptations and community composition under future warming scenarios.

Novel physiological data needed for progress in global change ecology

Studies examining the underlying causes of the distributions of species and their future trajectories under climate change have benefitted from the accumulation of measurements of thermal tolerance across the tree of life. However, gaps in the global coverage of heat-tolerance data for ectotherms persist on four critical fronts. First, most large-scale analyses treat heat tolerance as a fixed species trait despite that population-level variation can equal or exceed cross-species variation. Second, terrestrial non-arthropod invertebrates and aquatic ectotherms other than bony fish have been poorly sampled, particularly in boreal and tropical regions, the Indian Ocean and the mesopelagic-deep ocean. Third, the study of climate impacts on the heat tolerance of terrestrial ectotherms has often neglected the interaction of environmental temperatures with water availability. And fourth, the mechanisms driving the dependence of heat tolerance on oxygen supply-demand remain largely unknown. We contend that filling those data and knowledge gaps requires novel strategies for the ecophysiological sampling of the range of understudied populations and species that occupy the length of climatic gradients globally. Such developments are essential for comprehensively predicting species responses to climate change across aquatic and terrestrial biomes.

Physiological ecology and vulnerability to climate change of a microendemic, habitat-specialist lizard in a tropical dry forest of Mexico

Physiological ecology and vulnerability to climate change of a microendemic, habitat-specialist lizard in a tropical dry forest of Mexico

Tolerance of high temperature and associated effects on reproduction in euedaphic Collembola

Studies show that tropical and mid-latitude terrestrial ectotherms are more vulnerable to global warming than species from high latitudes. However, thermal tolerance studies from these regions still lack soil invertebrates. In the present study, we investigated six euedaphic species of Collembola (of the genera Onychiurus and Protaphorura) sampled across latitudes ranging from 31° N to 64° N and determined their upper thermal limit (UTL) by static assays. In another experiment, we submitted springtails to high temperatures for exposure times, causing 5% to 30% mortality within each species. Survivors from this series of increasing heat injuries were used to determine the time-to-first-oviposition and the number of eggs produced following heat exposure. Two hypotheses are tested in this study: 1) heat tolerance of species correlates positively with the environmental temperature of their habitat; 2) the most heat-tolerant species require less time to regain reproduction and produce more eggs than the least heat-tolerant species. Results showed that the UTL positively correlates to the soil temperature of the sampling site. The sequence of UTL60 (the temperature causing 50% mortality after 60 min of exposure) from highest to least was O. yodai > P. fimata > P. armata ≈ P. tricampata > P. macfadyeni > P. pseudovanderdrifti. Heat stress inflicted on springtails can delay reproduction in all species, and two species showed a reduced egg production rate after heat exposure. For heat stress causing up to 30% mortality, the most heat-tolerant species did not have advantages over the least heat-tolerant species for what concerns the recovery of reproduction. The relation between UTL and recovery from heat stress is not linear. Our study provides evidence for a potential long-term effect of high-temperature exposure on euedaphic species of Collembola and highlights the need for further studies on the effects of global warming on soil-living organisms.

Climate aridity and habitat drive geographical variation in morphology and thermo-hydroregulation strategies of a widespread lizard species

Abstract Thermo-hydroregulation strategies involve concurrent changes in functional traits related to energy, water balance and thermoregulation and play a key role in determining life-history traits and population demography of terrestrial ectotherms. Local thermal and hydric conditions should be important drivers of the geographical variation of thermo-hydroregulation strategies, but we lack studies that examine these changes across climatic gradients in different habitat types. Here, we investigated intraspecific variation of morphology and thermo-hydroregulation traits in the widespread European common lizard (Zootoca vivipara louislantzi) across a multidimensional environmental gradient involving independent variation in air temperature and rainfall and differences in habitat features (access to free-standing water and forest cover). We sampled adult males for morphology, resting metabolic rate, total and cutaneous evaporative water loss and thermal preferences in 15 populations from the rear to the leading edge of the distribution across an elevational gradient ranging from sea level to 1750 m. Besides a decrease in adult body size with increasing environmental temperatures, we found little effect of thermal conditions on thermo-hydroregulation strategies. In particular, relict lowland populations from the warm rear edge showed no specific ecophysiological adaptations. Instead, body mass, body condition and resting metabolic rate were positively associated with a rainfall gradient, while forest cover and water access in the habitat throughout the season also influenced cutaneous evaporative water loss. Our study emphasizes the importance of rainfall and habitat features rather than thermal conditions for geographical variation in lizard morphology and physiology.

Developmental plasticity in thermal tolerance: Ontogenetic variation, persistence, and future directions.

Understanding the factors affecting thermal tolerance is crucial for predicting the impact climate change will have on ectotherms. However, the role developmental plasticity plays in allowing populations to cope with thermal extremes is poorly understood. Here, we meta-analyse how thermal tolerance is initially and persistently impacted by early (embryonic and juvenile) thermal environments by using data from 150 experimental studies on 138 ectothermic species. Thermal tolerance only increased by 0.13°C per 1°C change in developmental temperature and substantial variation in plasticity (~36%) was the result of shared evolutionary history and species ecology. Aquatic ectotherms were more than three times as plastic as terrestrial ectotherms. Notably, embryos expressed weaker but more heterogenous plasticity than older life stages, with numerous responses appearing as non-adaptive. While developmental temperatures did not have persistent effects on thermal tolerance overall, persistent effects were vastly under-studied, and their direction and magnitude varied with ontogeny. Embryonic stages may represent a critical window of vulnerability to changing environments and we urge researchers to consider early life stages when assessing the climate vulnerability of ectotherms. Overall, our synthesis suggests that developmental changes in thermal tolerance rarely reach levels of perfect compensation and may provide limited benefit in changing environments.

Evolution of diel activity patterns in skinks (Squamata: Scincidae), the world's second-largest family of terrestrial vertebrates.

Many animals have strict diel activity patterns, with unique adaptations for either diurnal or nocturnal activity. Diel activity is phylogenetically conserved, yet evolutionary shifts in diel activity occur and lead to important changes in an organism's morphology, physiology, and behavior. We use phylogenetic comparative methods to examine the evolutionary history of diel activity in skinks, one of the largest families of terrestrial vertebrates. We examine how diel patterns are associated with microhabitat, ambient temperatures, and morphology. We found support for a nondiurnal ancestral skink. Strict diurnality in crown group skinks only evolved during the Paleogene. Nocturnal habits are associated with fossorial activity, limb reduction and loss, and warm temperatures. Our results shed light on the evolution of diel activity patterns in a large radiation of terrestrial ectotherms and reveal how both intrinsic biotic and extrinsic abiotic factors can shape the evolution of animal activity patterns.

Impact of developmental temperatures on thermal plasticity and repeatability of metabolic rate

Phenotypic plasticity is an important mechanism that allows populations to adjust to changing environments. Early life experiences can have lasting impacts on how individuals respond to environmental variation later in life (i.e., individual reaction norms), altering the capacity for populations to respond to selection. Here, we incubated lizard embryos (Lampropholis delicata) at two fluctuating developmental temperatures (cold = 23 ºC + / − 3 ºC, hot = 29 ºC + / − 3 ºC, ncold = 26, nhot = 25) to understand how it affected metabolic plasticity to temperature later in life. We repeatedly measured individual reaction norms across six temperatures 10 times over ~ 3.5 months (nobs = 3,818) to estimate the repeatability of average metabolic rate (intercept) and thermal plasticity (slope). The intercept and the slope of the population-level reaction norm was not affected by developmental temperature. Repeatability of average metabolic rate was, on average, 10% lower in hot incubated lizards but stable across all temperatures. The slope of the thermal reaction norm was overall moderately repeatable (R = 0.44, 95% CI = 0.035 – 0.93) suggesting that individual metabolic rate changed consistently with short-term changes in temperature, although credible intervals were quite broad. Importantly, reaction norm repeatability did not depend on early developmental temperature. Identifying factors affecting among-individual variation in thermal plasticity will be increasingly more important for terrestrial ectotherms living in changing climate. Our work implies that thermal metabolic plasticity is robust to early developmental temperatures and has the capacity to evolve, despite there being less consistent variation in metabolic rate under hot environments.

Rapid Adjustments in Thermal Tolerance and the Metabolome to Daily Environmental Changes - A Field Study on the Arctic Seed Bug Nysius groenlandicus.

Laboratory investigations on terrestrial model-species, typically of temperate origin, have demonstrated that terrestrial ectotherms can cope with daily temperature variations through rapid hardening responses. However, few studies have investigated this ability and its physiological basis in the field. Especially in polar regions, where the temporal and spatial temperature variations can be extreme, are hardening responses expected to be important. Here, we examined diurnal adjustments in heat and cold tolerance in the Greenlandic seed bug Nysius groenlandicus by collecting individuals for thermal assessment at different time points within and across days. We found a significant correlation between observed heat or cold tolerance and the ambient microhabitat temperatures at the time of capture, indicating that N. groenlandicus continuously and within short time-windows respond physiologically to thermal changes and/or other environmental variables in their microhabitats. Secondly, we assessed underlying metabolomic fingerprints using GC-MS metabolomics in a subset of individuals collected during days with either low or high temperature variation. Concentrations of metabolites, including sugars, polyols, and free amino acids varied significantly with time of collection. For instance, we detected elevated sugar levels in animals caught at the lowest daily field temperatures. Polyol concentrations were lower in individuals collected in the morning and evening and higher at midday and afternoon, possibly reflecting changes in temperature. Additionally, changes in concentrations of metabolites associated with energetic metabolism were observed across collection times. Our findings suggest that in these extreme polar environments hardening responses are marked and likely play a crucial role for coping with microhabitat temperature variation on a daily scale, and that metabolite levels are actively altered on a daily basis.

Influence of photoperiod on thermal responses in body size, growth and development in Lycaena phlaeas (Lepidoptera: Lycaenidae).

Influence of photoperiod on thermal responses in body size, growth and development in Lycaena phlaeas (Lepidoptera: Lycaenidae).