Abstract
Leafflowers (Phyllanthus; Phyllanthaceae) are engaged in obligate mutualisms with leafflower moths (Epicephala) that actively pollinate leafflowers and consume the developing seeds as larvae. Among the >1,000 species of leafflowers worldwide, however, the mutualism is considered to be present in only roughly half of the species. Knowledge on pollination biology of the remaining species is critical for understanding the origin of the mutualism, but such information is thus far limited. We studied the pollination biology of two Phyllanthus species in Japan (P. flexuosus and P. liukiuensis) and one species in New Caledonia (P. baladensis); the three species belong to three distantly related subgenera but share a characteristic dark red floral display. A bagging experiment showed that P. flexuosus is self-incompatible and wind hardly plays a role in pollination. In P. flexuosus, gall midges of the genera Clinodiplosis and Macrolabis were the most consistent and abundant flower visitors. They fed on nectar at the spongy floral disc of male flowers and laid eggs in male flower buds, picking up pollen and contacting the styles of nearby female flowers in the process. Infested buds developed into sterile galls, within which midge larvae completed their development. These results indicate that P. flexuosus is pollinated by gall midges that use male flower buds as larval brood sites. Because Macrolabis larvae infested galls at a later stage than did Clinodiplosis, Macrolabis is likely an inquiline in the gall induced by Clinodiplosis. Association with gall midges was also observed in P. liukiuensis and P. baladensis flowers, suggesting that pollination by gall midges likely occurs in at least three subgenera of Phyllanthus, two of which contain species pollinated by specialized leafflower moths.
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