Distinct thermal responses of a host plant and an invertebrate herbivore affect ecosystem productivity and disease dynamics in a coastal marine ecosystem

Abstract

Biological rates, like growth, tend to have unimodal (hump-shaped) responses to temperature, and these relationships can vary among species and biological processes. In most systems, full thermal performance relationships are rarely characterized for interacting species (e.g., consumer-resource or host-pathogen pairs), making it challenging to predict how their interactions, and subsequently, how communities, will shift with climate change. We investigated how the thermal responses of eelgrass (Zostera marina, an important marine foundation species in the N. hemisphere) and an isopod grazer (Pentidotea resecata), which putatively acts as an indirect vector of eelgrass wasting disease, interact to affect eelgrass productivity and wasting disease dynamics. In a laboratory experiment crossing five temperatures, two grazing, and two disease exposure treatments, across various metrics, eelgrass growth responded unimodally to temperature in the absence of grazers. Grazers depressed plant growth and flattened its thermal performance curves. Thermal performance curves for isopods indicated that increases in grazing and survival at intermediate temperatures negated concurrent gains in plant growth at these temperatures, while decreased isopod survival at high temperatures reduced their top-down effect on eelgrass. Isopods had negligible effects on plant disease responses, but warming reduced the time to disease onset and increased final disease severity. Overall, whole-plant disease severity remained low and did not substantially affect eelgrass leaf elongation, net growth, or rhizome dry mass. However, disease-treatment plants grew more new leaves at intermediate temperatures, possibly to combat losses in photosynthetic capacity in diseased leaf tissue. These results indicate that climate change-associated warming will likely increase eelgrass vulnerability to wasting disease. However, in sublethal outbreaks, disease could have less of an impact on eelgrass productivity than warming-induced increases in grazing. Thus, ignoring grazer responses to temperature could result in unreliable predictions of eelgrass productivity under climate change.