skip to main content


Title: Wildfire alters the disturbance impacts of an emerging forest disease via changes to host occurrence and demographic structure
Abstract

Anthropogenic activities have altered historical disturbance regimes, and understanding the mechanisms by which these shifting perturbations interact is essential to predicting where they may erode ecosystem resilience. Emerging infectious plant diseases, caused by human translocation of nonnative pathogens, can generate ecologically damaging forms of novel biotic disturbance. Further, abiotic disturbances, such as wildfire, may influence the severity and extent of disease‐related perturbations via their effects on the occurrence of hosts, pathogens and microclimates; however, these interactions have rarely been examined.

The disease ‘sudden oak death’ (SOD), associated with the introduced pathogenPhytophthora ramorum, causes acute, landscape‐scale tree mortality in California's fire‐prone coastal forests. Here, we examined interactions between wildfire and the biotic disturbance impacts of this emerging infectious disease. Leveraging long‐term datasets that describe wildfire occurrence andP. ramorumdynamics across the Big Sur region, we modelled the influence of recent and historical fires on epidemiological parameters, including pathogen presence, infestation intensity, reinvasion, and host mortality.

Past wildfire altered disease dynamics and reduced SOD‐related mortality, indicating a negative interaction between these abiotic and biotic disturbances. Frequently burned forests were less likely to be invaded byP. ramorum, had lower incidence of host infection, and exhibited decreased disease‐related biotic disturbance, which was associated with reduced occurrence and density of epidemiologically significant hosts. Following a recent wildfire, survival of mature bay laurel, a key sporulating host, was the primary driver ofP. ramoruminfestation and reinvasion, but younger, rapidly regenerating host vegetation capable of sporulation did not measurably influence disease dynamics. Notably, the effect ofP. ramoruminfection on host mortality was reduced in recently burned areas, indicating that the loss of tall, mature host canopies may temporarily dampen pathogen transmission and ‘release’ susceptible species from significant inoculum pressure.

Synthesis. Cumulatively, our findings indicate that fire history has contributed to heterogeneous patterns of biotic disturbance and disease‐related decline across this landscape, via changes to the both the occurrence of available hosts and the demography of epidemiologically important host populations. These results highlight that human‐altered abiotic disturbances may play a foundational role in structuring infectious disease dynamics, contributing to future outbreak emergence and driving biotic disturbance regimes.

 
more » « less
Award ID(s):
1753965
NSF-PAR ID:
10453511
Author(s) / Creator(s):
 ;  ;  ;  ;
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Journal of Ecology
Volume:
109
Issue:
2
ISSN:
0022-0477
Page Range / eLocation ID:
p. 676-691
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Human‐altered disturbance regimes and changing climatic conditions can reduce seed availability and suitable microsites, limiting seedling regeneration in recovering forest systems. Thus, resprouting plants, which can persist in situ, are expected to expand in dominance in many disturbance‐prone forests. However, resprouters may also be challenged by changing regimes, and the mechanisms determining facultative seedling recruitment by resprouting species, which will determine both the future spread and current persistence of these populations, are poorly understood. In the resprouter‐dominated forests of coastal California, interactions between wildfire and an emerging disease, sudden oak death (SOD), alter disturbance severity and tree mortality, which may shift forest regeneration trajectories. We examine this set of compound disturbances to (1) assess the influence of seed limitation, biotic competition, and abiotic conditions on seedling regeneration in resprouting populations; (2) investigate whether disease‐fire interactions alter postfire seedling regeneration, which have implications for future disease dynamics and shifts in forest composition. Following a wildfire that impacted a preexisting plot network in SOD‐affected forests, we monitored seedling abundances and survival over eight years. With pre‐ and postfire data, we assessed relationships between regeneration dynamics and disturbance severity, biotic, and abiotic variables, using Bayesian generalized linear models and mixed models. Our results indicate that postfire seedling regeneration by resprouting species was shaped by contrasting mechanisms reflecting seed limitation and competitive release. Seedling abundances declined with decreasing postfire survival of mature, conspecific stems, while belowground survival of resprouting genets had no effect. However, where seed sources persisted, seedling abundances and survival generally increased with the prefire severity of disease impacts, suggesting that decreased competition with adults may enhance seedling recruitment in this resprouter‐dominated system. Species’ regeneration responses varied with their relative susceptibility to SOD and suggest compositional shifts, which will determine future disease management and forest restoration actions. These results additionally highlight that mechanisms related to biotic competition, seed limitation, and opportunities for seedling recruitment beneath mature canopies may determine possible shifts in the occurrence of resprouting traits. This result has broad applications to other systems impacted by human‐altered regimes where asexual persistence may be predicted to be a beneficial life history strategy.

     
    more » « less
  2. Human-altered disturbance regimes and changing climatic conditions can reduce seed availability and suitable microsites, limiting seedling regeneration in recovering forest systems. Thus, resprouting plants, which can persist in situ, are expected to expand in dominance in many disturbance-prone forests. However, resprouters may also be challenged by changing regimes, and the mechanisms determining facultative seedling recruitment by resprouting species, which will determine both the future spread and current persistence of these populations, are poorly understood. In the resprouter-dominated forests of coastal California, interactions between wildfire and an emerging disease, sudden oak death (SOD), alter disturbance severity and tree mortality, which may shift forest regeneration trajectories. We examine this set of compound disturbances to (1) assess the influence of seed limitation, biotic competition, and abiotic conditions on seedling regeneration in resprouting populations; (2) investigate whether disease-fire interactions alter postfire seedling regeneration, which have implications for future disease dynamics and shifts in forest composition. Following a wildfire that impacted a preexisting plot network in SOD-affected forests, we monitored seedling abundances and survival over eight years. With pre- and postfire data, we assessed relationships between regeneration dynamics and disturbance severity, biotic, and abiotic variables, using Bayesian generalized linear models and mixed models. Our results indicate that postfire seedling regeneration by resprouting species was shaped by contrasting mechanisms reflecting seed limitation and competitive release. Seedling abundances declined with decreasing postfire survival of mature, conspecific stems, while belowground survival of resprouting genets had no effect. However, where seed sources persisted, seedling abundances and survival generally increased with the prefire severity of disease impacts, suggesting that decreased competition with adults may enhance seedling recruitment in this resprouter-dominated system. Species’ regeneration responses varied with their relative susceptibility to SOD and suggest compositional shifts, which will determine future disease management and forest restoration actions. These results additionally highlight that mechanisms related to biotic competition, seed limitation, and opportunities for seedling recruitment beneath mature canopies may determine possible shifts in the occurrence of resprouting traits. This result has broad applications to other systems impacted by human-altered regimes where asexual persistence may be predicted to be a beneficial life history strategy. 
    more » « less
  3. Abstract

    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 inSODis 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 theSODsystem. 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.

     
    more » « less
  4. Sudden oak death (SOD), caused by the generalist pathogen Phytophthora ramorum, has profoundly impacted California coastal ecosystems. SOD has largely been treated as a two-host system, with Umbellularia californica as the most transmissive host, Notholithocarpus densiflorus less so, and remaining species as epidemiologically unimportant. However, this understanding of transmission potential primarily stems from observational field studies rather than direct measurements on the diverse assemblage of plant species. Here, we formally quantify the sporulation potential of common plant species inhabiting SOD-endemic ecosystems on the California coast in the Big Sur region. This study allows us to better understand the pathogen’s basic biology, trajectory of SOD in a changing environment, and how the entire host community contributes to disease risk. Leaves were inoculated in a controlled laboratory environment and assessed for production of sporangia and chlamydospores, the infectious and resistant propagules, respectively. P. ramorum was capable of infecting every species in our study and almost all species produced spores to some extent. Sporangia production was greatest in N. densiflorus and U. californica and the difference was insignificant. Even though other species produced much less, quantities were nonzero. Thus, additional species may play a previously unrecognized role in local transmission. Chlamydospore production was highest in Acer macrophyllum and Ceanothus oliganthus, raising questions about the role they play in pathogen persistence. Lesion size did not consistently correlate with the production of either sporangia or chlamydospores. Overall, we achieved an empirical foundation to better understand how community composition affects transmission of P. ramorum. 
    more » « less
  5. Abstract

    Pathogen spread rates are determined, in part, by the performance of pathogens under altered environmental conditions and their ability to persist while switching among hosts and vectors.

    To determine the effects of new conditions (host, vector, and nutrient) on pathogen spread rate, we introduced a vector‐borne viral plant pathogen, Barley Yellow Dwarf Virus PAV (BYDV‐PAV) into hosts, vectors, and host nutrient supplies that it had not encountered for thousands of viral generations. We quantified pathogen prevalence over the course of two serial inoculations under the new conditions. Using individual‐level transmission rates from this experiment, we parameterized a dynamical model of disease spread and projected spread across host populations through a growing season.

    A change in nutrient conditions (increased supply of phosphorus) reduced viral transmission whereas shifting to a new vector or host species had no effect on infection prevalence. However, the reduction in the new nutrient environment was only temporary; infection prevalence recovered after the second inoculation.

    Synthesis. These results highlight how robust the pathogen, BYDV‐PAV, is to changes in its biotic and abiotic environment. Our study also highlights the need to quantify longitudinal infection information beyond snapshot assessments to project disease risk for pathogens in new environments.

     
    more » « less