Plant water‐use strategies as mediators of herbivore drought response: Ecophysiology, host plant quality and functional traits

Abstract

Abstract The response of herbivorous insects to plant drought stress can range from positive to negative, and it has been challenging to understand the causes of this variation. We tested whether plant trait values associated with aridity gradients might underlie this variation and how such effects vary between two insect feeding guilds. Here, we propose that plants trait values associated with adaptation to arid environments would result in positive effects of experimental drought on herbivores, with such plant species adaptively shifting resources away from resistance to maintain performance under stress. In contrast, plants with trait values associated with adaptation to mesic environments would result in negative effects of drought because such species lose vigour and thus decrease their host quality. We tested these predictions using experimental manipulations in 13 milkweed species (genus Asclepias) adapted to a wide range of environmental conditions and the herbivore performance of a specialist leaf‐chewer (monarch butterfly; Danaus plexippus) and sap‐feeder (oleander aphid; Aphis nerii). We exposed plants to physiologically calibrated species‐specific watering regimes to maximize (100%) or reduce (50%) stomatal conductance and then monitored herbivore performance. The effects of drought stress on herbivore survival ranged from strongly positive (50% increase) to strongly negative (80% decrease) among milkweed species, but these effects were inconsistent between the two herbivores. Plant trait values associated with adaptation to aridity were correlated with monarch survival in the predicted manner, such that milkweed species with high water‐use efficiency (WUE) and low relative water content (RWC) increased monarch survival under drought. In contrast, aphid survival was unrelated to arid‐adapted trait values. Drought‐induced changes in plant quality were negatively associated with both herbivore survivals. Specifically, milkweed species that increased cardenolides concentration under drought conditions decreased monarch and aphid survival. Synthesis. We demonstrated that the indirect effects of drought on herbivores varied tremendously among closely related plant species and between co‐occurring insect herbivores. We in turn present evidence that some of this variation is explained by plant traits associated with adaptation to arid versus mesic environments for leaf‐chewers but not sap‐feeders and that such effects are mediated by drought‐induced changes in chemical defences.