Sylvain Pincebourde

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.

Lifetime gains of host‐feeding in a synovigenic parasitic wasp

Abstract.  Understanding behavioural decisions relative to host use for feeding or reproduction by foraging parasitoids requires not only the study of metabolic pathways followed by nutrients, but also the quantification of lifetime fitness gains of each alternative behaviour. By using a combination of observational and manipulative approaches, the lifetime host‐feeding gains are measured both in terms of fecundity and longevity in the parasitoid Eupelmus vuilletti. Host‐feeding increases both egg production and longevity. The increase in fecundity is mainly determined by the amount of lipids obtained whereas the lifespan extension is mainly determined by carbohydrates. Proteins obtained through host‐feeding have been implicated previously in egg production by parasitoids but protein intake has no effect on fecundity and longevity in E. vuilletti. The amount of nutrients gained through host‐feeding and invested in eggs is variable and changes over the lifetime of the animal. Therefore, lifetime feeding gains are best understood through the construction of dynamical budgets running over the entire lifespan of an insect.

Diel flight activity and ecological segregation within an assemblage of tropical forest dung and carrion beetles

Temporal variation in activity of dung and carrion beetles in tropical forest is considered as a mechanism of ecological segregation between potentially competing species. We describe the diel flight activity of Scarabaeidae collected with baited pitfall traps at Les Nouragues field station in French Guiana. A total of 2663 individuals of 63 species was recorded, from the subfamilies Coprinae, Scarabaeinae and Aphodinae. Temporal guilds of diurnal, nocturnal and crepuscular species were identified. Diurnal species were about twice as numerous and abundant as either nocturnal or crepuscular species. Two main activity patterns characterize the diurnal species while nocturnal and crepuscular species show overlapping activity. The association of activity rhythm with the other niche variables, food selection, functional group, body size and relative abundance, was analysed using multiple correspondence analysis. Small diurnal coprophagous species were opposed to large crepuscular necrophagous species. Species packing is suggested but further analysis showed that the variables were independent of one another. The temporal differentiation of species combined with separation along multiple niche dimensions and resource gradients may facilitate the coexistence of species assumed to be strongly affected by interspecific competition.

MULTITROPHIC BIOPHYSICAL BUDGETS: THERMAL ECOLOGY OF AN INTIMATE HERBIVORE INSECT-PLANT INTERACTION

Physiology of ectothermic organisms depends on microclimate temperature. In some insect–plant relationships, the herbivore physically manipulates its proximate environment (i.e., plant tissues). However, little is known about the effects of this manipulation on the insect microclimate. We studied the thermal environment of the leaf-mining insect Phyllonorycter blancardella (Lepidoptera: Gracillariidae). This herbivore modifies both morphology and physiology of attacked apple leaf tissues to construct a mine inside which the entire larval development occurs. Spectral measurements showed that absorbance of mined leaf tissues differed from that of intact leaf tissues. Gas exchange measurements in mined leaf tissues demonstrated that responses of stomata to changes in climatic parameters were modified compared to intact leaf tissues. We built an energy budget model to predict the temperature within a mine given climatic variables, and measured parameters related to radiative absorption properties and to the e...

Natural History Note 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.

Warming decreases thermal heterogeneity of leaf surfaces: implications for behavioural thermoregulation by arthropods

Summary 1. Ectotherms rely heavily on the spatial variance of environmental conditions to thermoregulate. Theoretically, their fitness is maximized when they can find suitable microhabitats by moving over short distances – this condition is met when spatial variance is high at fine spatial scales. Strikingly, despite the diversity of organisms living in leaf microhabitats, little is known about the impact of warming on the spatial variance of climatic conditions at the scale of individual leaf surfaces. 2. Here, we used experimental manipulation of ambient conditions to quantify the effects of environmental change on the thermal heterogeneity within individual leaf surfaces. We also explored the implications for behavioural thermoregulation by arthropods at a single leaf surface. 3. Using thermography, we characterized the apple leaf microclimate in terms of span and spatial aggregation of surface temperatures across a range of air temperatures and relative humidities. Then, we assessed how thermal heterogeneity within individual leaves affected behavioural thermoregulation by the two-spotted spider mite (Tetranychus urticae Koch) under both nearoptimal and sublethal conditions in this microhabitat. We measured the upper lethal temperature threshold of the mite to define sublethal exposure. 4. Thermal heterogeneity of individual leaves was driven mainly by ambient air temperature. Higher air temperatures gave both smaller ranges and higher spatial aggregation of temperatures at the leaf surface, such that the leaf microclimate was homogenized. 5. Tetranychus urticae used behavioural thermoregulation at moderate air temperature, when thermal heterogeneity was high at the leaf surface. At higher air temperature, however, heterogeneity declined and spider mites did not perform behavioural thermoregulation. 6. Warming decreases thermal heterogeneity of leaf surfaces with critical implications for arthropods – behavioural thermoregulation alone is not sufficient to escape the heat in the leaf microhabitat. Information on spatial variance of microclimatic conditions is critical for estimating how readily organisms can buffer global warming by moving.

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.

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.

On the canopy structure manipulation to buffer climate change effects on insect herbivore development

Insect pest development is often linearly related to air temperature, without taking into account the multiple interactions between the particular host plant and pest, the microclimatic conditions actually experienced by the insect, and the non-linear response of insect development rate to temperature. In this study, using an integrative biophysical model, we have investigated effects of both climatic and tree structure changes on the development of a phytophagous leaf mining moth (Phyllonorycter blancardella), taking into account the heterogeneous microclimatic conditions provided by its host plant, the domestic apple (Malus domestica), the larval body temperature rather than the ambient air temperature, and a non-linear development rate model. Hourly body temperature dynamics of larvae homogeneously dispersed in tree canopies were simulated from hourly meteorological conditions (medium IPCC climate change scenario) within the canopy of apple trees. To analyse the effect of tree architecture on leaf miner development, both pruned and unpruned trees, and one, two and three scaffold branched trees were used. Body temperature dynamics was used to compute larval development time and mortality following the non-linear developmental model for this insect. The results showed that tree pruning influences significantly larval development time and mortality. Nevertheless, the effects of manipulating tree structure on larval development and survival were relatively weak compared with the impact of chosen climate variations. This survey also showed that the variability in insect development time within a year and insect mortality change markedly with climatic variations, and highlights the importance of using non-linear rate curves and insect body temperatures instead of air temperature in forecasting models of climate-related insect pest outbreaks.