Preferred temperature in the warmth of cities: Body size, sex and development stage matter more than urban climate in a ground-dwelling spider.

Most ectotherms rely on behavioural thermoregulation to maintain body temperatures close to their physiological optimum. Hence, ectotherms can drastically limit their exposure to thermal extremes by selecting a narrower range of temperatures, which includes their preferred temperature (Tpref). Despite evidence that behavioural thermoregulation can be adjusted by phenotypic plasticity or constrained by natural selection, intraspecific Tpref variations across environmental gradients remain overlooked as compared to other thermal traits like thermal tolerance. Here, we analyzed Tpref variation of spider populations found along a gradient of urban heat island (UHI) which displays large thermal variations over small distances. We measured two components of the thermal preference, namely the mean Tpref and the Tpref range (i.e., standard deviation) in 557 field-collected individuals of a common ground-dwelling spider (Pardosa saltans, Lycosidae) using a laboratory thermal gradient. We determined if Tpref values differed among ten populations from contrasting thermal zones. We showed that endogenous factors such as body size or sex primarily determine both mean Tpref and Tpref range. The Tpref range was also linked to the UHI intensity to a lesser extent, yet only in juveniles. The absence of relationship between Tpref metrics and UHI in adult spiders suggests a Bogert effect according to which the ability of individuals to detect and exploit optimal microclimates weakens the selection pressure of temperatures (here driven by UHI) on their thermal physiology. Alternatively, this lack of relationship could also indicate that temperature patterns occurring at the scale of the spiders' micro-habitat differ from measured ones. This study shows the importance of considering both inter-individual and inter-population variations of the Tpref range when conducting Tpref experiments, and supports Tpref range as being a relevant measure to inform on the strength of behavioural thermoregulation in a given population.

Mechanistic forecasts of species responses to climate change: The promise of biophysical ecology.

A core challenge in global change biology is to predict how species will respond to future environmental change and to manage these responses. To make such predictions and management actions robust to novel futures, we need to accurately characterize how organisms experience their environments and the biological mechanisms by which they respond. All organisms are thermodynamically connected to their environments through the exchange of heat and water at fine spatial and temporal scales and this exchange can be captured with biophysical models. Although mechanistic models based on biophysical ecology have a long history of development and application, their use in global change biology remains limited despite their enormous promise and increasingly accessible software. We contend that greater understanding and training in the theory and methods of biophysical ecology is vital to expand their application. Our review shows how biophysical models can be implemented to understand and predict climate change impacts on species' behavior, phenology, survival, distribution, and abundance. It also illustrates the types of outputs that can be generated, and the data inputs required for different implementations. Examples range from simple calculations of body temperature at a particular site and time, to more complex analyses of species' distribution limits based on projected energy and water balances, accounting for behavior and phenology. We outline challenges that currently limit the widespread application of biophysical models relating to data availability, training, and the lack of common software ecosystems. We also discuss progress and future developments that could allow these models to be applied to many species across large spatial extents and timeframes. Finally, we highlight how biophysical models are uniquely suited to solve global change biology problems that involve predicting and interpreting responses to environmental variability and extremes, multiple or shifting constraints, and novel abiotic or biotic environments.

Thermal tolerance of two Diptera that pollinate thermogenic plants.

Pollinating insects can be exposed to temperatures far from ambient air when visiting flowers, reducing their warming tolerance. Typically, such scenario occurs when flowers are exposed to solar radiation. The case of thermogenic flowers is particular because they warm up even when they are not exposed to solar energy. The flowers of Arum attract their pollinators with a deceptive method and trap them for a whole day, thereby imposing elevated temperature to visiting insects. Therefore, we predict a relatively high basal thermal tolerance in those insects. The aim of this study was to assess the thermal tolerance and warming tolerance of females of two fly species (genus Psychoda) pollinating Arum sp. (thermogenic plant). We measured their critical temperature (CTmax) and its response to rate of temperature increase as well as acclimation period to moderate temperature of 25 °C. We found relatively low CTmax (33.7 °C on average) for both species, and a weak response to acclimation period and ramping rate. In general, the thermal tolerance increased with a rapid ramping in temperature. To evaluate the warming tolerance, we compared thermal tolerance limits to flower temperatures measured in the field. We highlighted that the temperature of the thermogenic floral organ could reach values close to the thermal tolerance threshold of pollinators. This discovery raises questions about the sustainability of the interaction between these thermogenic plants and their pollinators.

The Impact of Phloem Feeding Insects on Leaf Ecophysiology Varies With Leaf Age.

Herbivore insects have strong impacts on leaf gas exchange when feeding on the plant. Leaf age also drives leaf gas exchanges but the interaction of leaf age and phloem herbivory has been largely underexplored. We investigated the amplitude and direction of herbivore impact on leaf gas exchange across a wide range of leaf age in the apple tree-apple green aphid (Aphis pomi) system. We measured the gas exchange (assimilation and transpiration rates, stomatal conductance and internal CO2 concentration) of leaves infested versus non-infested by the aphid across leaf age. For very young leaves up to 15 days-old, the gas exchange rates of infested leaves were similar to those of non-infested leaves. After few days, photosynthesis, stomatal conductance and transpiration rate increased in infested leaves up to about the age of 30 days, and gradually decreased after that age. By contrast, gas exchanges in non-infested leaves gradually decreased across leaf age such that they were always lower than in infested leaves. Aphids were observed on relatively young leaves up to 25 days and despite the positive effect on leaf photosynthesis and leaf performance, their presence negatively affected the growth rate of apple seedlings. Indeed, aphids decreased leaf dry mass, leaf surface, and leaf carbon content except in old leaves. By contrast, aphids induced an increase in leaf nitrogen content and the deviation relative to non-infested leaves increased with leaf age. Overall, the impacts of aphids at multiple levels of plant performance depend on leaf age. While aphids cause an increase in some leaf traits (gas exchanges and nitrogen content), they also depress others (plant growth rate and carbon content). The balance between those effects, as modulated by leaf age, may be the key for herbivory mitigation in plants.

Extended phenotypes: buffers or amplifiers of climate change?

Historic approaches to understanding biological responses to climate change have viewed climate as something external that happens to organisms. Organisms, however, at least partially influence their own climate experience by moving within local mosaics of microclimates. Such behaviors are increasingly being incorporated into models of species distributions and climate sensitivity. Less attention has focused on how organisms alter microclimates via extended phenotypes: phenotypes that extend beyond the organismal surface, including structures that are induced or built. We argue that predicting the consequences of climate change for organismal performance and fitness will depend on understanding the expression and consequences of extended phenotypes, the microclimatic niches they generate, and the power of plasticity and evolution to shape those niches.

When insect pests build their own thermal niche: The hot nest of the pine processionary moth.

Temperature strongly drives physiological and ecological processes in ectotherms. While many species rely on behavioural thermoregulation to avoid thermal extremes, others build structures (nests) that confer a shelter against climate variability and extremes. However, the microclimate inside nests remains unknown for most insects. We investigated the thermal environment inside the nest of a temperate winter-developing insect species, the pine processionary moth (PPM), Thaumetopoea pityocampa. Gregarious larvae collectively build a silken nest at the beginning of the cold season. We tested the hypothesis that it provides a warmer microenvironment to larvae. First, we monitored temperature inside different types of nests varying in the number of larvae inside. Overall, nest temperature was positively correlated to global radiation and air temperature. At noon, when global radiation was maximal, nest temperature exceeded air temperature by up to 11.2-16.5 °C depending on nest type. In addition, thermal gradients of amplitude from 6.85 to 15.5 °C were observed within nests, the upper part being the warmest. Second, we developed a biophysical model to predict temperature inside PPM nests based on heat transfer equations and to explain this important temperature excess. A simple model version accurately predicted experimental measurements, confirming that nest temperature is driven mainly by radiation load. Finally, the model showed that nest temperature increases at the same rate as air temperature change. We conclude that some pest insects already live in warm microclimates by building their own sheltering nest. This effect should be considered when studying the impact of climate change on phenology and distribution.

Survive a Warming Climate: Insect Responses to Extreme High Temperatures.

Global change includes a substantial increase in the frequency and intensity of extreme high temperatures (EHTs), which influence insects at almost all levels. The number of studies showing the ecological importance of EHTs has risen in recent years, but the knowledge is rather dispersed in the contemporary literature. In this article, we review the biological and ecological effects of EHTs actually experienced in the field, i.e., when coupled to fluctuating thermal regimes. First, we characterize EHTs in the field. Then, we summarize the impacts of EHTs on insects at various levels and the processes allowing insects to buffer EHTs. Finally, we argue that the mechanisms leading to positive or negative impacts of EHTs on insects can only be resolved from integrative approaches considering natural thermal regimes. Thermal extremes, perhaps more than the gradual increase in mean temperature, drive insect responses to climate change, with crucial impacts on pest management and biodiversity conservation.

There is plenty of room at the bottom: microclimates drive insect vulnerability to climate change.

Climate warming impacts biological systems profoundly. Climatologists deliver predictions about warming amplitude at coarse scales. Nevertheless, insects are small, and it remains unclear how much of the warming at coarse scales appears in the microclimates where they live. We propose a simple method for determining the pertinent spatial scale of insect microclimates. Recent studies have quantified the ability of forest understory to buffer thermal extremes, but these microclimates typically are characterized at spatial scales much larger than those determined by our method. Indeed, recent evidence supports the idea that insects can be thermally adapted even to fine scale microclimatic patterns, which can be highly variable. Finally, we discuss how microhabitat surfaces may buffer or magnify the amplitude of climate warming.

On the importance of getting fine-scale temperature records near any surface.

The SoilTemp database will identify the microhabitats that best buffer the amplitude of warming. The temperature heterogeneity at spatial scales below the meter also requires attention. A worldwide database of temperatures near any surface is still lacking. This article is a Commentary on Lembrechts et al., 26, 6616-6629.

Enhanced heat tolerance of viral-infected aphids leads to niche expansion and reduced interspecific competition.

Vector-borne pathogens are known to alter the phenotypes of their primary hosts and vectors, with implications for disease transmission as well as ecology. Here we show that a plant virus, barley yellow dwarf virus, increases the surface temperature of infected host plants (by an average of 2 °C), while also significantly enhancing the thermal tolerance of its aphid vector Rhopalosiphum padi (by 8 °C). This enhanced thermal tolerance, which was associated with differential upregulation of three heat-shock protein genes, allowed aphids to occupy higher and warmer regions of infected host plants when displaced from cooler regions by competition with a larger aphid species, R. maidis. Infection thereby led to an expansion of the fundamental niche of the vector. These findings show that virus effects on the thermal biology of hosts and vectors can influence their interactions with one another and with other, non-vector organisms.

Narrow safety margin in the phyllosphere during thermal extremes.

The thermal limit of ectotherms provides an estimate of vulnerability to climate change. It differs between contrasting microhabitats, consistent with thermal ecology predictions that a species' temperature sensitivity matches the microclimate it experiences. However, observed thermal limits may differ between ectotherms from the same environment, challenging this theory. We resolved this apparent paradox by showing that ectotherm activity generates microclimatic deviations large enough to account for differences in thermal limits between species from the same microhabitat. We studied upper lethal temperature, effect of feeding mode on plant gas exchange, and temperature of attacked leaves in a community of six arthropod species feeding on apple leaves. Thermal limits differed by up to 8 °C among the species. Species that caused an increase in leaf transpiration (+182%), thus cooling the leaf, had a lower thermal limit than those that decreased leaf transpiration (-75%), causing the leaf to warm up. Therefore, cryptic microclimatic variations at the scale of a single leaf determine the thermal limit in this community of herbivores. We investigated the consequences of these changes in plant transpiration induced by plant-insect feedbacks for species vulnerability to thermal extremes. Warming tolerance was similar between species, at ±2 °C, providing little margin for resisting increasingly frequent and intense heat waves. The thermal safety margin (the difference between thermal limit and temperature) was greatly overestimated when air temperature or intact leaf temperature was erroneously used. We conclude that feedback processes define the vulnerability of species in the phyllosphere, and beyond, to thermal extremes.

Structure is more important than physiology for estimating intracanopy distributions of leaf temperatures.

Estimating leaf temperature distributions (LTDs) in canopies is crucial in forest ecology. Leaf temperature affects the exchange of heat, water, and gases, and it alters the performance of leaf-dwelling species such as arthropods, including pests and invaders. LTDs provide spatial variation that may allow arthropods to thermoregulate in the face of long-term changes in mean temperature or incidence of extreme temperatures. Yet, recording LTDs for entire canopies remains challenging. Here, we use an energy-exchange model (RATP) to examine the relative roles of climatic, structural, and physiological factors in influencing three-dimensional LTDs in tree canopies. A Morris sensitivity analysis of 13 parameters showed, not surprisingly, that climatic factors had the greatest overall effect on LTDs. In addition, however, structural parameters had greater effects on LTDs than did leaf physiological parameters. Our results suggest that it is possible to infer forest canopy LTDs from the LTDs measured or simulated just at the surface of the canopy cover over a reasonable range of parameter values. This conclusion suggests that remote sensing data can be used to estimate 3D patterns of temperature variation from 2D images of vegetation surface temperatures. Synthesis and applications. Estimating the effects of LTDs on natural plant-insect communities will require extending canopy models beyond their current focus on individual species or crops. These models, however, contain many parameters, and applying the models to new species or to mixed natural canopies depends on identifying the parameters that matter most. Our results suggest that canopy structural parameters are more important determinants of LTDs than are the physiological parameters that tend to receive the most empirical attention.

Temperature effects on ballistic prey capture by a dragonfly larva.

Understanding the effects of temperature on prey-predator interactions is a key issue to predict the response of natural communities to climate change. Higher temperatures are expected to induce an increase in predation rates. However, little is known on how temperature influences close-range encounter of prey-predator interactions, such as predator's attack velocities. Based on the speed-accuracy trade-off concept, we hypothesized that the increase in predator attack velocity by increasing temperature reduces the accuracy of the attack, leading to a lower probability of capture. We tested this hypothesis on the dragonfly larvae Anax imperator and the zooplankton prey Daphnia magna. The prey-predator encounters were video-recorded at high speed, and at three different temperatures. Overall, we found that (1) temperature had a strong effect on predator's attack velocities, (2) prey did not have the opportunity to move and/or escape due to the high velocity of the predator during the attack, and (3) neither velocity nor temperature had significant effects on the capture success. By contrast, the capture success mainly depended on the accuracy of the predator in capturing the prey. We found that (4) some 40% of mistakes were undershooting and some 60% aimed below or above the target. No lateral mistake was observed. These results did not support the speed-accuracy trade-off hypothesis. Further studies on dragonfly larvae with different morphological labial masks and speeds of attacks, as well as on prey with different escape strategies, would provide new insights into the response to environmental changes in prey-predator interactions.

Do Aphids Alter Leaf Surface Temperature Patterns During Early Infestation?

Arthropods at the surface of plants live in particular microclimatic conditions that can differ from atmospheric conditions. The temperature of plant leaves can deviate from air temperature, and leaf temperature influences the eco-physiology of small insects. The activity of insects feeding on leaf tissues, may, however, induce changes in leaf surface temperatures, but this effect was only rarely demonstrated. Using thermography analysis of leaf surfaces under controlled environmental conditions, we quantified the impact of presence of apple green aphids on the temperature distribution of apple leaves during early infestation. Aphids induced a slight change in leaf surface temperature patterns after only three days of infestation, mostly due to the effect of aphids on the maximal temperature that can be found at the leaf surface. Aphids may induce stomatal closure, leading to a lower transpiration rate. This effect was local since aphids modified the configuration of the temperature distribution over leaf surfaces. Aphids were positioned at temperatures near the maximal leaf surface temperatures, thus potentially experiencing the thermal changes. The feedback effect of feeding activity by insects on their host plant can be important and should be quantified to better predict the response of phytophagous insects to environmental changes.

Temperature heterogeneity over leaf surfaces: the contribution of the lamina microtopography.

Temperature is spatially heterogeneous over leaf surfaces, yet the underlying mechanisms are not fully resolved. We hypothesized that the 3D leaf microtopography determines locally the amount of incoming irradiation flux at leaf surface, thereby driving the temperature gradient over the leaf surface. This hypothesis was tested by developing a model of leaf temperature heterogeneity that includes the development of the leaf boundary layer, the microtopography of the leaf surface and the physiological response of the leaf. Temperature distributions under various irradiation loads (1) over apple leaves based on their 3D microtopography, (2) over simulated flat (2D) apple leaves and (3) over 3D leaves with a transpiration rate distributed as in 2D leaves were simulated. Accuracy of the predictions was quantified by comparing model outputs and thermographic measurements of leaf surface temperature under controlled conditions. Only the model with 3D leaves predicted accurately the spatial heterogeneity of surface temperature over single leaves, whereas the mean temperature was well predicted by both 2D and 3D leaves. We suggest that in these conditions, the 3D leaf microtopography is the primary driver of leaf surface heterogeneity in temperature when the leaf is exposed to a light/heat source.

The Vulnerability of Tropical Ectotherms to Warming Is Modulated by the Microclimatic Heterogeneity.

Most tropical ectotherms live near their physiological limits for temperature. Substantial ecological effects of global change are predicted in the tropics despite the low amplitude of temperature change. These predictions assume that tropical ectotherms experience air temperature as measured by weather stations or predicted by global circulation models. The body temperature of ectotherms, however, can deviate from ambient air when the organism samples the mosaic of microclimates at fine scales. The thermal heterogeneity of tropical landscapes has been quantified only rarely in comparison to temperate habitats, limiting our ability to infer the vulnerability to warming of tropical ectotherms. Here, we used thermal imaging to quantify the heterogeneity in surface temperatures across spatial scales, from the micro- up to landscape scale, at the top of an Inselberg in French Guiana. We measured the thermal heterogeneity at the scale of Clusia nemorosa leaves, by categorizing leaves in full sun versus leaves in the shade to quantify the microclimatic variance available to phytophagous insects. Then, we measured the thermal heterogeneity at the scales of the single shrub and the landscape, for several sites differing in their orientation toward the sun to quantify the microclimatic heterogeneity available for larger ectotherms. All measurements were made three times per day over four consecutive days. There was a high level of thermal heterogeneity at all spatial scales. The thermal variance varied between scales, increasing from the within-leaf surface to the landscape scale. It also shifted across the day in different ways depending on the spatial scale. Then, using a set of published data, we compared the critical temperature (CTmax) of neo-tropical ectotherms and temperature distributions. The portion of space above the CTmax varied substantially depending on spatial scale and taxa. Insects were particularly at risk at the surface of leaves exposed to solar radiation but not on shaded leaves. By contrast, ants tolerated elevated surface temperatures and can survive almost anywhere in the habitat. We suggest that the fine scale mosaic of microclimates in the tropics modulates the vulnerability of ectotherms to warming. By moving just a few meters, or even a few centimeters, small tropical ectotherms can radically change their microclimatic temperature and escape overheating.

Life in the Frequency Domain: the Biological Impacts of Changes in Climate Variability at Multiple Time Scales.

Over the last few decades, biologists have made substantial progress in understanding relationships between changing climates and organism performance. Much of this work has focused on temperature because it is the best kept of climatic records, in many locations it is predicted to keep rising into the future, and it has profound effects on the physiology, performance, and ecology of organisms, especially ectothermic organisms which make up the vast majority of life on Earth. Nevertheless, much of the existing literature on temperature-organism interactions relies on mean temperatures. In reality, most organisms do not directly experience mean temperatures; rather, they experience variation in temperature over many time scales, from seconds to years. We propose to shift the focus more directly on patterns of temperature variation, rather than on means per se, and present a framework both for analyzing temporal patterns of temperature variation and for incorporating those patterns into predictions about organismal biology. In particular, we advocate using the Fourier transform to decompose temperature time series into their component sinusoids, thus allowing transformations between the time and frequency domains. This approach provides (1) standardized ways of visualizing the contributions that different frequencies make to total temporal variation; (2) the ability to assess how patterns of temperature variation have changed over the past half century and may change into the future; and (3) clear approaches to manipulating temporal time series to ask "what if" questions about the potential effects of future climates. We first summarize global patterns of change in temperature variation over the past 40 years; we find meaningful changes in variation at the half day to yearly times scales. We then demonstrate the utility of the Fourier framework by exploring how power added to different frequencies alters the overall incidence of long-term waves of high and low temperatures, and find that power added to the lowest frequencies greatly increases the probability of long-term heat and cold waves. Finally, we review what is known about the time scales over which organismal thermal performance curves change in response to variation in the thermal environment. We conclude that integrating information characterizing both the frequency spectra of temperature time series and the time scales of resulting physiological change offers a powerful new avenue for relating climate, and climate change, to the future performance of ectothermic organisms.

Fine-Scale Microclimatic Variation Can Shape the Responses of Organisms to Global Change in Both Natural and Urban Environments.

When predicting the response of organisms to global change, models use measures of climate at a coarse resolution from general circulation models or from downscaled regional models. Organisms, however, do not experience climate at such large scales. The climate heterogeneity over a landscape and how much of that landscape an organism can sample will determine ultimately the microclimates experienced by organisms. This past few decades has seen an important increase in the number of studies reporting microclimatic patterns at small scales. This synthesis intends to unify studies reporting microclimatic heterogeneity (mostly temperature) at various spatial scales, to infer any emerging trends, and to discuss the causes and consequences of such heterogeneity for organismal performance and with respect to changing land use patterns and climate. First, we identify the environmental drivers of heterogeneity across the various spatial scales that are pertinent to ectotherms. The thermal heterogeneity at the local and micro-scales is mostly generated by the architecture or the geometrical features of the microhabitat. Then, the thermal heterogeneity experienced by individuals is modulated by behavior. Second, we survey the literature to quantify thermal heterogeneity from the micro-scale up to the scale of a landscape in natural habitats. Despite difficulties in compiling studies that differ much in their design and aims, we found that there is as much thermal heterogeneity across micro-, local and landscape scales, and that the temperature range is large in general (>9 °C on average, and up to 26 °C). Third, we examine the extent to which urban habitats can be used to infer the microclimatic patterns of the future. Urban areas generate globally drier and warmer microclimatic patterns and recent evidence suggest that thermal traits of ectotherms are adapted to them. Fourth, we explore the interplay between microclimate heterogeneity and the behavioral thermoregulatory abilities of ectotherms in setting their overall performance. We used a random walk framework to show that the thermal heterogeneity allows a more precise behavioral thermoregulation and a narrower temperature distribution of the ectotherm compared to less heterogeneous microhabitats. Finally, we discuss the potential impacts of global change on the fine scale mosaics of microclimates. The amplitude of change may differ between spatial scales. In heterogeneous microhabitats, the amplitude of change at micro-scale, caused by atmospheric warming, can be substantial while it can be limited at the local and landscape scales. We suggest that the warming signal will influence species performance and biotic interactions by modulating the mosaic of microclimates.

Hypoxia and hypercarbia in endophagous insects: Larval position in the plant gas exchange network is key.

Gas composition is an important component of any micro-environment. Insects, as the vast majority of living organisms, depend on O2 and CO2 concentrations in the air they breathe. Low O2 (hypoxia), and high CO2 (hypercarbia) levels can have a dramatic effect. For phytophagous insects that live within plant tissues (endophagous lifestyle), gas is exchanged between ambient air and the atmosphere within the insect habitat. The insect larva contributes to the modification of this environment by expiring CO2. Yet, knowledge on the gas exchange network in endophagous insects remains sparse. Our study identified mechanisms that modulate gas composition in the habitat of endophagous insects. Our aim was to show that the mere position of the insect larva within plant tissues could be used as a proxy for estimating risk of occurrence of hypoxia and hypercarbia, despite the widely diverse life history traits of these organisms. We developed a conceptual framework for a gas diffusion network determining gas composition in endophagous insect habitats. We applied this framework to mines, galls and insect tunnels (borers) by integrating the numerous obstacles along O2 and CO2 pathways. The nature and the direction of gas transfers depended on the physical structure of the insect habitat, the photosynthesis activity as well as stomatal behavior in plant tissues. We identified the insect larva position within the gas diffusion network as a predictor of risk exposure to hypoxia and hypercarbia. We ranked endophagous insect habitats in terms of risk of exposure to hypoxia and/or hypercarbia, from the more to the less risky as cambium mines>borer tunnels≫galls>bark mines>mines in aquatic plants>upper and lower surface mines. Furthermore, we showed that the photosynthetically active tissues likely assimilate larval CO2 produced. In addition, temperature of the microhabitat and atmospheric CO2 alter gas composition in the insect habitat. We predict that (i) hypoxia indirectly favors the evolution of cold-tolerant gallers, which do not perform well at high temperatures, and (ii) normoxia (ambient O2 level) in mines allows miners to develop at high temperatures. Little is known, however, about physiological and morphological adaptations to hypoxia and hypercarbia in endophagous insects. Endophagy strongly constrains the diffusion processes with cascading consequences on the evolutionary ecology of endophagous insects.