Direct and indirect effects of forest microclimate on pathogen spillover.

Disease dynamics are governed by variation of individuals, species, and environmental conditions across space and time. In some cases, an alternate reservoir host amplifies pathogen loads and drives disease transmission to less competent hosts in a process called pathogen spillover. Spillover is frequently associated with multi-host disease systems where a single species is more tolerant of infection and more competent in pathogen transmission compared to other hosts. Pathogen spillover must be driven by biotic factors, including host and community characteristics, yet biotic factors interact with the abiotic environment (e.g., temperature) to create disease. Despite its fundamental role in disease dynamics, the influence of the abiotic environment on pathogen spillover has seldom been examined. Improving our understanding of disease processes such as pathogen spillover hinges on disentangling the effects of interrelated biotic and abiotic factors over space and time. We applied 10 yr of fine-scale microclimate, disease, and tree community data in a path analysis to investigate the relative influence of biotic and abiotic factors on pathogen spillover for the emerging infectious forest disease sudden oak death (SOD). Disease transmission in SOD is primarily driven by the reservoir host California bay laurel, which supports high foliar pathogen loads that spillover onto neighboring oak trees and create lethal canker infections. The foliar pathogen load and susceptibility of oaks is expected to be sensitive to forest microclimate conditions. We found that biotic factors of pathogen load and tree diversity had relatively stronger effects on pathogen spillover compared to abiotic microclimate factors, with pathogen load increasing oak infection and tree diversity reducing oak infection. Abiotic factors still had significant effects, with greater heat exposure during summer months reducing pathogen loads and optimal pathogen conditions during the wet season increasing oak infection. Our results offer clues to possible disease dynamics under future climate change where hotter and drier or warmer and wetter conditions could have opposing effects on pathogen spillover in the SOD system. Disentangling direct and indirect effects of biotic and abiotic factors affecting disease processes can provide key insights into disease dynamics including potential avenues for reducing disease spread and predicting future epidemics.

Effects of individual, community, and landscape drivers on the dynamics of a wildland forest epidemic.

The challenges posed by observing host-pathogen-environment interactions across large geographic extents and over meaningful time scales limit our ability to understand and manage wildland epidemics. We conducted a landscape-scale, longitudinal study designed to analyze the dynamics of sudden oak death (an emerging forest disease caused by Phytophthora ramorum) across hierarchical levels of ecological interactions, from individual hosts up to the community and across the broader landscape. From 2004 to 2011, we annually assessed disease status of 732 coast live oak, 271 black oak, and 122 canyon live oak trees in 202 plots across a 275-km2 landscape in central California. The number of infected oak stems steadily increased during the eight-year study period. A survival analysis modeling framework was used to examine which level of ecological heterogeneity best predicted infection risk of susceptible oak species, considering variability at the level of individuals (species identity, stem size), the community (host density, inoculum load, and species richness), and the landscape (seasonal climate variability, habitat connectivity, and topographic gradients). After accounting for unobserved risk shared among oaks in the same plot, survival models incorporating heterogeneity across all three levels better predicted oak infection than did models focusing on only one level. We show that larger oak trees (especially coast live oak) were more susceptible, and that interannual variability in inoculum production by the highly infectious reservoir host, California bay laurel, more strongly influenced disease risk than simply the density of this important host. Concurrently, warmer and wetter rainy-season conditions in consecutive years intensified infection risk, presumably by creating a longer period of inoculum build-up and increased probability of pathogen spillover from bay laurel to oaks. Despite the presence of many alternate host species, we found evidence of pathogen dilution, where less competent hosts in species-rich communities reduce pathogen transmission and overall risk of oak infection. These results identify key parameters driving the dynamics of emerging infectious disease in California woodlands, while demonstrating how multiple levels of ecological heterogeneity jointly determine epidemic trajectories in wildland settings.