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

Abstract

Background and aims: Fungi are widely known for their pathological impact on flowers, but some play a beneficial role in pollination. The inner petal corrugation of Meiogyne hainanensis (Annonaceae) in Hainan, China was reported to be prone to fungal infection and hypothesized to be a potential brood site for insects. We therefore investigated whether a nursery pollination system occurs in this species and whether the fungi play a mutualistic role.

Methods: Floral phenology and pollinator activity were observed. Effective pollinators were identified by assessing the presence of pollen grains on floral visitors retrieved from pistillate-phase flowers. Floral odour was characterized using gas chromatography-mass spectrometry. To assess the fungal composition of post-anthetic flowers and the gut contents of pollinators, ITS2 metabarcoding was performed.

Key results: The flowers emit a fruity scent composed mostly of sesquiterpenes, aliphatic esters, aliphatic ketones and aliphatic alcohols, attracting the effective beetle pollinators Paraphloeostiba sp. (Staphylinidae) and Mimemodes sp. (Monotomidae). The pollinators mate and oviposit onto the adaxial corrugation of the inner petals. After the end of anthesis, filamentous fungi grow extensively on these corrugated tissues. The flower has an unusually long post-anthetic phase that lasts ≤2 months, during which the fungus-infected petals remain arboreal. Upon hatching, the Paraphloeostiba and Mimemodes larvae consume the fungal mycelia. ITS2 metabarcoding analysis reveals that the larval diet and the fungal community of the inner petal corrugation are composed primarily of ascomycete fungi, such as Fusarium, Penicillium and Cladosporium species, suggesting that the fungi provide a food reward for the pollinator's brood.

Conclusions: Meiogyne hainanensis exhibits brood-site pollination, in which filamentous fungi are an essential mutualistic partner. The fungal partners appear to consist of opportunistic fungi that are also fruit pathogens. These findings provide insights into the possible origin of the tripartite nursery pollination system.