Weather and distance to fire refugia limit landscape‐level occurrence of fungal disease in an exotic annual grass

Abstract

The enemy release hypothesis proposes that invasion by exotic plant species is driven by their release from natural enemies (i.e. herbivores and pathogens) in their introduced ranges. However, in many cases, natural enemies, which may be introduced or managed to regulate invasive species, may fail to impact target host populations. Landscape heterogeneity, which can affect both the population dynamics of the pathogen and the susceptibility and the density of hosts, may contribute to why pathogens fail to control hosts despite established negative disease impacts. We explored patterns of post‐fire infection of the fungal head‐smut pathogen Ustilago bullata on the invasive annual cheatgrass Bromus tectorum, which has caused the notorious grass‐fire cycle and ecosystem degradation across Western North America. We asked whether infection level was a driver of host density or vice‐versa, and how weather affected infection and how spatial patterns of infection varied with time since fire, using a combination of structural equation modelling (SEM), proportional odds modelling and entropy‐based local indicator of spatial association (ELSA) on data from >700 plots spanning >100,000 ha remeasured annually for 4 years. Observed infection levels increased with greater prior‐year cheatgrass cover, and disease severity did not suppress cheatgrass populations. Warm, humid fall/winters and proximity to fire refugia (unburned patches) were associated with more infections. Infection clustering was most evident 2–3 years following fire with warm‐wet fall–winter conditions and decreased after two drier, colder winters. Synthesis. Severity of fungal disease did not result in measurable reductions of populations of a non‐native, invasive host species, cheatgrass, which suggests that natural enemies may not strongly regulate cheatgrass in its introduced range. Landscape heterogeneity associated with disturbance and weather limited population‐level infection of hosts by the fungal pathogen. Disturbance (specifically wildfire) and variable weather are key components of this and similar invasion systems, and likely need to be considered when evaluating disease dynamics and potential for natural enemies to influence invasion potential.

Systematic reduction of natural enemies and competition across variable precipitation approximates buffelgrass invasiveness (Cenchrus ciliaris) in its native range

“…Smuts that are often asymptomatic, living endophytically or in soils may have little year‐to‐year impact on grass productivity and reproduction (Zuo et al., 2019), yet when an outbreak occurs, their impact on the population and future generations are likely exponentially significant to future population dynamics (Farrell et al., 2002). Similarly, smut outbreaks of Ustilago bullata on Bromus tectorum followed weather patterns and landscape characteristics following fires that shifted disease incidence (Applestein et al., 2021). Our study showed similar associations with shifts from wet to dry periods.…”

Smut fungus (Langdonia walkerae) incidence is lower in two bunchgrass species (Aristida stricta and A. beyrichiana) after fires early in the year

“…Specifically, fires at the very end and beginning of the year (i.e., winter) were associated with lower smut incidence in plants than prescribed fires that were implemented as the year progressed (through summer). This pattern could have resulted from variation in fire intensity or interactions between weather conditions and plant or pathogen phenology (Mims and Mims, 2004; Applestein et al, 2021), which vary between seasons. For example, it is possible that after prescribed fires early in the year, plants began to form stigma (the suspected location of penetration) while soil temperatures or environmental conditions were not conducive for teliospore germination.…”

“…Disturbances have been shown to alter the relationship between fungi and their host plants. Fires, in particular, can alter or reorganize microbial communities as a result of nutrient releases into the soil or changes in vegetation composition or structure (Semenova‐Nelsen et al, 2019; Applestein et al, 2021; Bowd et al, 2021, Vermeire et al, 2021; Hopkins et al, 2023). In addition, research has also shown that fires can cause spores to be released and dispersed long distances via smoke (e.g., Fox et al, 2022).…”