Small scale variability in soil moisture drives infection of vulnerable juniper populations by invasive forest pathogen

Abstract The oomycete plant pathogen, Phytophthora austrocedri, is an aggressive killer of cypress trees causing severe mortality of Chilean cedar (Austrocedrus chilensis) in Argentina since the 1940 s and now of common juniper (Juniperus communis s.l.) in the UK. Rapid mortality of key UK juniper populations was first observed in the early 2000 s. The causal agent of mortality was confirmed as P. austrocedri in 2012 and the pathogen has now been widely detected - but is not ubiquitous - in juniper populations across Scotland and England. Although juniper has a broad distribution across the northern hemisphere, the UK incidence of P. austrocedri remains the only confirmed infection of juniper populations globally. Juniper is an important species for biodiversity, so it is imperative to understand the abiotic and biotic drivers of emergent P. austrocedri infection to inform detection, containment and conservation strategies to manage juniper populations across the full extent of its range. As management of UK juniper populations is primarily conducted at a local level, we investigated field scale drivers of disease – in three, geographically separate populations with different infection histories. Variation in the proportion of juniper showing symptoms - discoloured or dead foliage – was measured using stratified sampling across along key environmental gradients within each 100-hectare population. Potential predictors of infection included altitude, slope, distance to nearest watercourse, soil moisture (mean percentage volumetric water content), area of red deer browsing damage and area of commonly associated vascular plant species. We assessed support in the data for alternative models explaining the spatial distribution of P. austrocedri symptoms using full subset covariate selection and Deviance Information Criteria (DIC). Despite differences in environmental gradients and infection histories between populations, area of juniper symptomatic for P. austrocedri increased with waterlogging, increasing with soil moisture in sites where soils had higher peat or clay contents, and decreasing with proximity to watercourses where sites had shallower, sandier soils. Furthermore, we identified common taxa in the associated plant community that correlated with increased area of symptoms and could be used by land managers as indicators to identify microsites at high risk of infection, enabling site-specific tailoring of disease management strategies. Such strategies could include prioritising detection inspections in microsites with high water tables and high grazing pressure (guided by indicator taxa), limiting soil disturbance in wet microsites and creating sites for natural regeneration in drier microsites, to minimise pathogen spread and maximise the resilience of existing juniper populations.