Herbivores disrupt clinal variation in plant responses to water limitation

Abstract

Abstract Plasticity in plant traits, including secondary metabolites, is critical to plant survival and competitiveness under stressful conditions. The ability of a plant to respond effectively to combined stressors can be impacted by crosstalk in biochemical pathways, resource availability and evolutionary history, but such responses remain underexplored. In particular, we know little about intraspecific variation in response to combined stressors or whether such variation is associated with the stress history of a given population. Here, we investigated the consequences of combined water and herbivory stress for plant traits, including relative growth rate, leaf morphology and various measures of phytochemistry, using a common garden of Asclepias fascicularis milkweeds. To examine how plant trait means and plasticities depend on the history of environmental stress, seeds for the experiment were collected from across a gradient of aridity in the Great Basin, United States. We then conducted a factorial experiment crossing water limitation with herbivory. Plants responded to water limitation alone by increasing the evenness of UV‐absorbent secondary metabolites and to herbivory alone by increasing the richness of metabolites. However, plants that experienced combined water and herbivory stress exhibited similar phytochemical diversity to well‐watered control plants. This lack of plasticity in phytochemical diversity in plants experiencing combined stressors was associated with a reduction in relative growth rates. Leaf chemistry means and plasticities exhibited clinal variation corresponding to seed source water deficits. The total concentration of UV‐absorbent metabolites decreased with increasing water availability among seed sources, driven by higher concentrations of flavonol glycosides, which are hypothesized to act as antioxidants, among plants from drier sites. Plants sourced from drier sites exhibited higher plasticity in flavonol glycoside concentrations in response to water limitation, which increased phytochemical evenness, but simultaneous herbivory dampened plant responses to water limitation irrespective of seed source. Synthesis. These results suggest that climatic history can affect intraspecific phytochemical plasticity, which may confer tolerance to water limitation, but that co‐occurring herbivory disrupts such patterns. Global change is increasing the frequency and intensity of stress combinations, such that understanding intraspecific responses to combined stressors is critical for predicting the persistence of plant populations.