Emerging Beetle-Pathogen Symbioses and Their Consequences for Forest Health: Lessons from Rapid 'Ohi'a Death in Hawai'i

Abstract

Invasive ambrosia beetles and fungal pathogens threaten forest ecosystems worldwide, exemplified in Hawaii by the widespread loss of keystone species [o]hia (Metrosideros polymorpha), due to Rapid [O]hia Death (ROD). A unique occurrence of five ambrosia beetle species (one native, four introduced) that vary in their symbiotic relationships with two introduced fungal pathogens provide an opportunity to test hypotheses of how opportunistic symbioses facilitate disease dynamics involving dominant forest trees. ROD is caused by two novel Ceratocystis fungal pathogens whose spores can spread via association with ambrosia beetles as they bore into [o]hia trees. We examined beetle-pathogen interactions of all five ambrosia beetle species in three ROD-affected regions on Hawaii Island, and used quantitative PCR (qPCR) to provide the first molecular confirmation of the two ROD pathogens associated with the exterior, mycangia, and gut of each beetle species. Results from generalized linear models and correlation networks show that pathogen acquisition and transport, including the potential for consumption and the presence of the pathogens, are determined by beetle invasion status and mycangia morphology. A niche construction framework suggests that both varying symbioses and opportunism facilitate disease spread, with the three invasive Xyleborus species emerging as key disease vectors. Identifying the beetle species that are more likely to contribute to disease spread, and understanding their biology as vectors, can inform targeted conservation strategies for [o]hia and for insect-pathogen threats in forests worldwide, and illustrates the potential ecosystem-level impacts of novel and opportunistic symbioses between globally distributed invasive vectors and pathogens.