Permafrost‐driven differences in habitat quality determine plant response to gall‐inducing mite herbivory

Abstract

Summary Canada's northern boreal forests are undergoing rapid change associated with warming trends, with permafrost thaw leading to increased forest stress and compositional changes in plant communities. Within this context, the influence of commonly occurring, resident natural enemies on plant species remains poorly understood. One of the dominant deciduous shrub genera, Betula, is abundant in northern forest–wetland landscapes, and is highly susceptible to leaf galling by mites, but the impacts of these specialist arthropod herbivores on plant‐level physiology remain unknown. We examined the impacts of mite galling on a suite of ecophysiological traits in Betula glandulosa, a shrubby species commonly found on permafrost plateaus, bogs and fens in a boreal wetland–forest mosaic, and on two congeners, B. occidentalis and B. neoalaskana, found only on plateaus. B. glandulosa leaves on plateaus showed marked declines in photosynthetic capacity [Amax], stomatal conductance [gs], and transpiration [E] in response to galling. However, B. glandulosa leaves in bogs and fens did not respond similarly, implying strong habitat‐related differences in response to galling herbivory. The impacts on plateaus were reinforced by similar responses of B. occidentalis and B. neoalaskana leaves to galling, and confirmed that on plateaus, galling appears to have significant negative effects on photosynthetic uptake. Moreover, carbon uptake in infested leaves showed photosynthetic declines even at low galling intensity. Interestingly, neighbouring nongalled leaves adjacent to galled ones showed similar declines in gas‐exchange rates in all the three species found on plateaus. However, reduced stomatal conductance and transpiration in galled and neighbour leaves did not affect whole plant water status, as we found no differences in either midday or diurnal stem water potentials between galled and gall‐free stems in any of the species. Synthesis: Based on these findings, we suggest that the impacts of mite galling are variable, and are likely to be most pronounced in habitats and on individuals that are already exposed to abiotic stresses such as the cooler, but more variable soil temperatures experienced by individuals on permafrost plateaus. Furthermore, galling can potentially contribute to localized thaw processes in these environments via impacts on plant functioning.