Narrow safety margin in the phyllosphere during thermal extremes

Significance

The thermal limits of terrestrial ectotherms vary more locally than globally. Local microclimatic variations can explain this pattern, but the underlying mechanisms remain unclear. We show that cryptic microclimatic variations at the scale of a single leaf determine the thermal limit in a community of arthropod herbivores living on the same host plant. Herbivores triggering an increase in transpiration, thereby cooling the leaf, had a lower thermal limit than those decreasing leaf transpiration and causing the leaf to warm up. These subtle mechanisms have major consequences for the safety margin of these herbivores during thermal extremes. Our findings suggest that temperate species may be more vulnerable to heat waves than previously thought.

Abstract

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.