Modelling thermal reaction norms for development and viability in Drosophila suzukii under constant, fluctuating and field conditions.

Phenological models for insect pests often rely on knowledge of thermal reaction norms. These may differ in shape depending on developmental thermal conditions (e.g. constant vs. fluctuating) and other factors such as life-stages. Here, we conducted an extensive comparative study of the thermal reaction norms for development and viability in the invasive fly, Drosophila suzukii, under constant and fluctuating thermal regimes. Flies, were submitted to 15 different constant temperatures (CT) ranging from 8 to 35 °C. We compared responses under CT with patterns observed under 15 different fluctuating temperature (FT) regimes. We tested several equations for thermal performance curves and compared various models to obtain thermal limits and degree-day estimations. To validate the model's predictions, the phenology was monitored in two artificial field-like conditions and two natural conditions in outdoor cages during spring and winter. Thermal reaction norm for viability from egg to pupa was broader than that from egg to adult. FT conditions yielded a broader thermal breadth for viability than CT, with a performance extended towards the colder side, consistent with our field observations in winter. Models resulting from both CT and FT conditions made accurate predictions of degree-day as long as the temperature remained within the linear part of the developmental rate curve. Under cold artificial and natural winter conditions, a model based on FT data made more accurate predictions. Model based on CT failed to predict adult's emergence in winter. We also document the first record of development and adult emergence throughout winter in D. suzukii. Population dynamics models in D. suzukii are all based on summer phenotype and CT. Accounting for variations between seasonal phenotypes, stages, and thermal conditions (CT vs. FT) could improve the predictive power of the models.

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.

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.

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.

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.

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.

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.

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.

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.

Warming tolerance across insect ontogeny: influence of joint shifts in microclimates and thermal limits.

The impact of warming on the persistence and distribution of ectotherms is often forecasted from their warming tolerance, inferred as the difference between their upper thermal limit and macroclimate temperature. Ectotherms, however, are thermally adapted to their microclimates, which can deviate substantially from macroscale conditions. Ignoring microclimates can therefore bias estimates of warming tolerance. We compared warming tolerance of an insect across its ontogeny when calculated from macro- and microclimate temperatures. We used a heat balance model to predict experienced microclimate temperatures from macroclimate, and we measured thermal limits for several life stages. The model shows a concomitant increase in microclimate temperatures and thermal limits across insect ontogeny, despite the fact that they all share the same macroclimate. Consequently, warming tolerance; as estimated from microclimate temperature, remained constant across ontogeny. When calculated from macroclimate temperature, however, warming tolerance was overestimated by 7-10 degrees C, depending on the life stage. Therefore, errors are expected when predicting persistence and distribution shifts of ectotherms in changing climates using macroclimate rather than microclimate.

The roles of microclimatic diversity and of behavior in mediating the responses of ectotherms to climate change.

We analyze the effects of changing patterns of thermal availability, in space and time, on the performance of small ectotherms. We approach this problem by breaking it into a series of smaller steps, focusing on: (1) how macroclimates interact with living and nonliving objects in the environment to produce a mosaic of thermal microclimates and (2) how mobile ectotherms filter those microclimates into realized body temperatures by moving around in them. Although the first step (generation of mosaics) is conceptually straightforward, there still exists no general framework for predicting spatial and temporal patterns of microclimatic variation. We organize potential variation along three axes-the nature of the objects producing the microclimates (abiotic versus biotic), how microclimates translate macroclimatic variation (amplify versus buffer), and the temporal and spatial scales over which microclimatic conditions vary (long versus short). From this organization, we propose several general rules about patterns of microclimatic diversity. To examine the second step (behavioral sampling of locally available microclimates), we construct a set of models that simulate ectotherms moving on a thermal landscape according to simple sets of diffusion-based rules. The models explore the effects of both changes in body size (which affect the time scale over which organisms integrate operative body temperatures) and increases in the mean and variance of temperature on the thermal landscape. Collectively, the models indicate that both simple behavioral rules and interactions between body size and spatial patterns of thermal variation can profoundly affect the distribution of realized body temperatures experienced by ectotherms. These analyses emphasize the rich set of problems still to solve before arriving at a general, predictive theory of the biological consequences of climate change.

Microclimatic challenges in global change biology.

Despite decades of work on climate change biology, the scientific community remains uncertain about where and when most species distributions will respond to altered climates. A major barrier is the spatial mismatch between the size of organisms and the scale at which climate data are collected and modeled. Using a meta-analysis of published literature, we show that grid lengths in species distribution models are, on average, ca. 10 000-fold larger than the animals they study, and ca. 1000-fold larger than the plants they study. And the gap is even worse than these ratios indicate, as most work has focused on organisms that are significantly biased toward large size. This mismatch is problematic because organisms do not experience climate on coarse scales. Rather, they live in microclimates, which can be highly heterogeneous and strongly divergent from surrounding macroclimates. Bridging the spatial gap should be a high priority for research and will require gathering climate data at finer scales, developing better methods for downscaling environmental data to microclimates, and improving our statistical understanding of variation at finer scales. Interdisciplinary collaborations (including ecologists, engineers, climatologists, meteorologists, statisticians, and geographers) will be key to bridging the gap, and ultimately to providing scientifically grounded data and recommendations to conservation biologists and policy makers.

Survival and arm abscission are linked to regional heterothermy in an intertidal sea star.

Body temperature is a more pertinent variable to physiological stress than ambient air temperature. Modeling and empirical studies on the impacts of climate change on ectotherms usually assume that body temperature within organisms is uniform. However, many ectotherms show significant within-body temperature heterogeneity. The relationship between regional heterothermy and the response of ectotherms to sublethal and lethal conditions remains underexplored. We quantified within-body thermal heterogeneity in an intertidal sea star (Pisaster ochraceus) during aerial exposure at low tide to examine the lethal and sublethal effects of temperatures of different body regions. In manipulative experiments, we measured the temperature of the arms and central disc, as well as survival and arm abscission under extreme aerial conditions. Survival was related strongly to central disc temperature. Arms were generally warmer than the central disc in individuals that survived aerial heating, but we found the reverse in those that died. When the central disc reached sublethal temperatures of 31-35°C, arms reached temperatures of 33-39°C, inducing arm abscission. The absolute temperature of individual arms was a poor predictor of arm abscission, but the arms lost were consistently the hottest at the within-individual scale. Therefore, the vital region of this sea star may remain below the lethal threshold under extreme conditions, possibly through water movement from the arms to the central disc and/or evaporative cooling, but at the cost of increased risk of arm abscission. Initiation of arm abscission seems to reflect a whole-organism response while death occurs as a result of stress acting directly on central disc tissues.

Temporal coincidence of environmental stress events modulates predation rates.

Climate warming experiments generally test the ecological effects of constant treatments while neglecting the influence of more realistic patterns of environmental fluctuations. Thus, little is known regarding how the temporal interaction between multiple episodes of thermal stress influences biotic interactions. We measured the sensitivity of predation rate in an intertidal sea star to changing levels of temporal coincidence of underwater and aerial thermal stress events. In laboratory trials, we controlled for intensity, variance and temporal patterning of both underwater and aerial body temperature. Predation rate decreased as underwater and aerial thermal stress episodes became temporally non-coincident, despite a similar intensity and variance among treatments. Experiments under constant conditions were a poor predictor of more complex environmental scenarios because of these strong temporal interactions. Such temporal interactions may be widespread in various ecosystems, suggesting a strong need for empirical studies and models that link environmental complexity, physiology, behaviour and species interactions.

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.

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.

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.

An intertidal sea star adjusts thermal inertia to avoid extreme body temperatures.

The body temperature of ectotherms is influenced by the interaction of abiotic conditions, morphology, and behavior. Although organisms living in different thermal habitats may exhibit morphological plasticity or move from unfavorable locations, there are few examples of animals adjusting their thermal properties in response to short-term changes in local conditions. Here, we show that the intertidal sea star Pisaster ochraceus modulates its thermal inertia in response to prior thermal exposure. After exposure to high body temperature at low tide, sea stars increase the amount of colder-than-air fluid in their coelomic cavity when submerged during high tide, resulting in a lower body temperature during the subsequent low tide. Moreover, this buffering capacity is more effective when seawater is cold during the previous high tide. This ability to modify the volume of coelomic fluid provides sea stars with a novel thermoregulatory "backup" when faced with prolonged exposure to elevated aerial temperatures.

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.