Fungus-infected Meiogyne flowers offer a brood site for beetle pollinators in a tripartite nursery pollination system

Fungi are widely known for their pathological impact on flowers, but some play a beneficial role in pollination. We report a case of tripartite pollination system in the flowering plant Meiogyne hainanensis (Annonaceae) in Hainan, China. The flowers emit a fruity scent composed of a mixture of mostly sesquiterpenes and aliphatic esters, attracting the primary beetle pollinators Paraphloeostiba sp. (Staphylinidae) and Mimemodes sp. (Monotomidae). The pollinators utilise the floral chamber as a mating ground and oviposit onto the adaxial corrugations of the inner petals. After the end of anthesis, extensive growth of filamentous fungi was observed to be restricted on these corrugated tissues. Upon hatching, the Paraphloeostiba and Mimemodes larvae consumed the fungal mycelia. ITS2 metabarcoding analysis reveals that the diet of the larvae consists of similar fungal taxa as those found on the inner petals. Both were primarily composed of ascomycete fungi such as Fusarium, Penicillium and Cladosporium species. The flower has an unusually long post-anthetic phase that lasts at least 21 days and up to 2 months, during which the fungus-infested petals remain arboreal, offering suitable microclimate and shelter for the broods. This is the second reported angiosperm genus that exhibits tripartite brood-site pollination in which filamentous fungi are an essential mutualistic partner.