Three novel Ambrosia Fusarium Clade species producing clavate macroconidia known (F. floridanum and F. obliquiseptatum) or predicted (F. tuaranense) to be farmed by Euwallacea spp. (Coleoptera: Scolytinae) on woody hosts

Authors: AOKI, TAKAYUKI - National Agriculture And Food Research Organization (NARO), Agricultrual Research Center; SMITH, JASON - University Of Florida; KASSON, MATTHEW - West Virginia University; FREEMAN, STANLEY - Volcani Center (ARO); GEISER, DAVID - Pennsylvania State University; GEERING, ANDREW - University Of Queensland; O Donnell, Kerry

Submitted to: Mycologia
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/20/2019
Publication Date: 9/27/2019
Citation: Aoki, T., Smith, J.A., Kasson, M.T., Freeman, S., Geiser, D.M., Geering, A.D.W., O'Donnell, K. 2019. Three novel Ambrosia Fusarium Clade species producing clavate macroconidia known (F. floridanum and F. obliquiseptatum) or predicted (F. tuaranense) to be farmed by Euwallacea spp. (Coleoptera: Scolytinae) on woody hosts. Mycologia. 111(6):919-935. https://doi.org/10.1080/00275514.2019.1647074.
DOI: https://doi.org/10.1080/00275514.2019.1647074

Interpretive Summary: The recent and rapid global spread of wood-boring Euwallacea ambrosia beetles from Asia is of significant concern because they can cause considerable damage to economically important hosts including avocado, cacao, rubber trees, citrus and Chinese tea. They also pose a serious threat to forest ecosystems and urban landscapes. Female Euwallacea ambrosia beetles farm 1-2 different Fusarium fungi as a source of nutrition for themselves and their offspring in tunnels they construct in their woody hosts. When beetles tunnel into the tree’s vascular tissue, fungal growth can block transport of nutrients and water from the roots, which can cause wilting of branches and leaves, branch dieback and even tree death. In the present study, we describe three of the plant pathogenic Fusarium species cultivated by the ambrosia beetles and determined how to distinguish them genetically and microscopically. These species are formally recognized as Fusarium floridanum farmed by E. interjectus isolated from box elder (Acer negundo) in Gainesville, Florida; Fusarium tuaranense isolated from beetle damaged rubber trees (Hevea brasiliense) in North Borneo; and F. obliquiseptatum farmed by an unnamed Euwallacea ambrosia beetle on avocado (Persea americana) in Queensland, Australia. Results of the present study provide detailed information on the genetic diversity, host range and geographic distribution of these important plant pathogens and will enable quarantine officials and others to prevent these economically destructive foreign insect pests and fungal pathogens from entering the U.S. and the countries of our trading partners.

Technical Abstract: The Ambrosia Fusarium Clade (AFC) comprises at least 16 genealogically exclusive species level lineages within Clade 3 of the Fusarium solani species complex. These fusaria are either known or predicted to be farmed as a source of nutrition by exotic Asian Euwallacea ambrosia beetles (Coleoptera: Curculionidae: Scolytinae) in the tribe Xyleborini. Although the Euwallacea-Fusarium mutualism is thought to be obligate, and it was estimated to have evolved ~21 Mya near the Oligocene-Miocene boundary, cophylogenetic analyses indicate that speciation in this clade has been driven by repeated host shifts rather than strict coevolution. To date only four of the 16 AFC have been described formally. In the absence of Latin binomials for most of the AFC, an ad hoc nomenclature was developed to distinguish the 16 species lineages as AF-1 to AF-16. Herein, AFC Fusarium spp. AF-3, AF-5 and AF-7 were formally described as F. floridanum, F. tuaranense, and F. obliquiseptatum, respectively. Fusarium floridanum farmed by E. interjectus on box elder (Acer negundo) in Gainesville, Florida was distinguished morphologically by the production of sporodochial conidia that were highly variable in size and shape together with greenish pigmented chlamydospores. Fusarium tuaranense was isolated from a beetle damaged Para rubber tree (Hevea brasiliense) in North Borneo, Malaysia and was diagnosed by production of the smallest sporodochial conidia of any species within the AFC. Lastly, F. obliquiseptatum was farmed by an unnamed ambrosia beetle designated Euwallacea sp. #3 (E. fornicatus species complex) on avocado (Persea americana) in Queensland, Australia. It uniquely produces some clavate sporodochial conidia with oblique septa. Multilocus maximum likelihood analyses resolved these three novel AFC taxa as phylogenetically distinct species based on genealogical concordance. These exotic mutualists pose a serious threat to the avocado industry, native forests and urban landscapes in diverse regions throughout the world.