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

Abstract

Japanese encephalitis virus (JEV), a zoonotic, mosquito-borne virus, has broad circulation across the Central Indo-Pacific biogeographical region (CIPBR), which recently expanded dramatically within this region across southeastern Australia over the summer of 2021-2022. Preliminary investigation of the landscape epidemiology of the outbreaks of JEV in Australian piggeries found associations with particular landscape structure as well as ardeid species richness. The ways in which waterbird species from diverse taxonomic pools with substantial functional variation might couple with JEV-associated landscape structure was not explored, and therefore, key questions regarding the landscape epidemiology and infection ecology of JEV remain unanswered. Moreover, given the established presence of JEV within the CIBPR, the extent to which waterbird species pools in JEV-associated landscapes in Australia reflect broader regional patterns in functional biogeography presents a further knowledge gap particularly with respect to potential virus dispersal via maintenance hosts. The current study investigated waterbird species presence, ecological traits, and functional diversity distribution at landscape scale, and how these aligned with confirmed JEV detections in eastern Australia and the wider CIPBR. The results showed that waterbird habitat associated with JEV detection in Australia in 2022 and more widely across the CIPBR over the last 20 years reflects a range of species representing 8 families in 4 orders (ardeids, anatids, rallids, phalacrocoracids, threskiornithids, gruids, and pelecanids). Increasing waterbird functional diversity (trait-based mean pairwise dissimilarity) was associated with landscapes delineating JEV occurrence, while only one individual trait, high hand-wing index, was consistently associated with species presence in these JEV-associated landscapes in both Australia and the broader CIPBR. This suggests that dispersal capacity among the waterbird species pools that dominate JEV-associated landscapes might be important. By taking an agnostic approach to JEV maintenance host status, this study indicates a relatively large, CIPBR-wide pool of waterbird families associated with JEV landscapes, challenging the narrow view that JEV maintenance is limited to ardeid birds. In addition, these findings highlight the potential for leveraging functional biogeography in high-risk landscapes across broad geographic extent to guide landscape-specific selection of species for JEV surveillance.