Landscapes associated with Japanese encephalitis virus reflect the functional biogeography of waterbird species across Australia and the Central Indo-Pacific region

Abstract

The geographic extent of Japanese encephalitis virus (JEV), a zoonotic, mosquito-borne virus, increased dramatically in south-eastern Australia over the summer of 2021-2022 resulting in outbreaks in piggeries, 45 cases of human disease, and simultaneous detection of JEV by mosquito and arbovirus surveillance programs. Preliminary investigation of the landscape epidemiology of the piggery outbreaks showed that they were associated with particular landscape structure as well as intermediate ardeid species richness. However, no exploration of the ways in which individual species or species composition may couple with JEV-associated landscape composition and configuration has been undertaken and, therefore, key questions regarding the landscape epidemiology and infection ecology of JEV in Australia remain unanswered. The current study sought to interrogate how individual species presence and their functional traits were distributed across the landscape, and how these distributions aligned with the landscape structure of JEV occurrence. Inhomogeneous Poisson point process models and multivariate hierarchical models were used to investigate the landscape-level ardeid species pools and the distribution of their pool-weighted traits with respect to JEV outbreaks. The distributions of six species were strongly associated with the distribution of JEV outbreaks reported in 2022: Casmerodius albus (Ardea alba), Ardea pacifica, Botaurus poiciloptilus, Egretta novaehollandiae, Ixobrychus minutus (Ixobrychus dubius), and Nycticorax caledonicus. Some JEV-delimiting landscape features, including transient wetlands and proximity to waterways, were associated with the presence of nearly all ardeid species, while others, such as crop cultivation, habitat fragmentation, and water flow accumulation were associated with only a subset of these species. In addition, hand-wing index was associated with species presence in landscapes associated with JEV outbreaks, which may suggest the importance of dispersal capacity in ardeid community assembly in landscapes that share environmental features with JEV occurrence. This study provides a preliminary selection of target species for the development of wild waterbird JEV surveillance, while uniquely accounting for sympatry and the potential for functional modulation of environmental filtering in high-risk landscapes, despite the broad landscape scale that necessarily constrained the analysis. Nevertheless, while the results provide an actionable One Health framework with which to develop wildlife surveillance, it must be noted that they do not describe community assembly rules, nor do they provide a description of community composition at local scale. The findings advance the current understanding of the landscape epidemiology of JEV in Australia by connecting landscapes with individual species from a family of established maintenance hosts and, given the large geographic extent of the potential circulation of JEV in maintenance hosts, provides valuable evidence-based information for targeted surveillance strategies.