Two’s company, three’s a crowd: co-occurring pollinators and parasite species in Breynia oblongifolia (Phyllanthaceae)

Abstract

BackgroundObligate pollination mutualisms (OPMs) are specialized interactions in which female pollinators transport pollen between the male and female flowers of a single plant species and then lay eggs into those same flowers. The pollinator offspring hatch and feed upon some or all of the developing ovules pollinated by their mothers. Strong trait matching between plants and their pollinators in OPMs is expected to result in reciprocal partner specificity i.e., a single pollinator species using a single plant species and vice versa, and strict co-speciation. These issues have been studied extensively in figs and fig wasps, but little in the more recently discovered co-diversification of Epicephala moths and their Phyllanthaceae hosts. OPMs involving Epicephala moths are believed occur in approximately 500 species of Phyllanthaceae, making it the second largest OPM group after the Ficus radiation (> 750 species). In this study, we used a mixture of DNA barcoding, genital morphology and behavioral observations to determine the number of Epicephala moth species inhabiting the fruits of Breynia oblongifolia, their geographic distribution, pollinating behavior and phylogenetic relationships.ResultsWe found that B. oblongifolia hosts two species of pollinator that co-occurred at all study sites, violating the assumption of reciprocal specificity. Male and female genital morphologies both differed considerably between the two moth species. In particular, females differed in the shape of their ovipositors, eggs and oviposition sites. Phylogenetic analyses indicated that the two Epicephala spp. on B. oblongifolia likely co-exist due to a host switch. In addition, we discovered that Breynia fruits are also often inhabited by a third moth, an undescribed species of Herpystis, which is a non-pollinating seed parasite.ConclusionsOur study reveals new complexity in interactions between Phyllantheae and Epicephala pollinators and highlights that host switching, co-speciation and non-pollinating seed parasites can shape species interactions in OPMs. Our finding that co-occurring Epicephala species have contrasting oviposition modes parallels other studies and suggests that such traits are important in Epicephala species coexistence.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1314-y) contains supplementary material, which is available to authorized users.

A non‐pollinating moth inflicts higher seed predation than two co‐pollinators in an obligate pollination mutualism

“…In 59 flower visits from Epicephala species A, 39/59 flowers contained eggs or scarring on the surface of the stigma consistent with oviposition by species A (Finch et al ., ). Of the remaining flowers observed to be visited by females of species A, 8/59 were found not to have an egg or evidence of oviposition (scarring on the stigma), despite apparently having been subjected to oviposition.…”

“…On average, fruits containing species B contained 0.5 more developed seeds than fruits containing species A, indicating that species B might be a slightly more effective pollinator. Previously, we detected no difference in the number of pollen grains deposited on female flowers by either species (Finch et al ., ) but differences in the number of seeds that develop may be accounted for by other behavioural differences. For example, it may be that pollen collection behaviour differs between pollinators such that the pollen deposited by species B is more likely to be compatible.…”

“…Breynia oblongifolia occurs primarily along the east coast of Australia, from the Cape York Peninsula to southern New South Wales (NSW). It is known to be pollinated by at least two closely related species of Epicephala moth (Finch et al, 2018b). Pollinators are active by night and the two species of Epicephala on B. oblongifolia co-occur across NSW.…”

“…Although otherwise very similar, they differ in their ovipositor morphology and oviposition strategy. Species A oviposits thin, whitish, fusiform eggs in the plant tissue above the ovules (internal oviposition), whereas species B deposits larger, yellowish, oblong-shaped eggs between the ovary and the sepal wall (external oviposition) (Finch et al, 2018b). A third species of moth, Herpystis sp.…”

“…A third species of moth, Herpystis sp. ANIC1 Meyrick (Tortricidae), co-occurs in B. oblongifolia fruits as a non-pollinating seed parasite, laying its eggs after fruit development has already begun (Finch et al, 2018b). In OPMs the primary cost of pollination to the host plant is the number of seeds consumed by pollinators.…”