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

BACKGROUND: Obligate 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. RESULTS: We 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. CONCLUSIONS: Our 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.

Cuckoo-hawk mimicry? An experimental test.

The similarity between many Old World parasitic cuckoos (Cuculinae) and Accipiter hawks, in size, shape and plumage, has been noted since ancient times. In particular, hawk-like underpart barring is more prevalent in parasitic than in non-parasitic cuckoos. Cuckoo-hawk resemblance may reflect convergent evolution of cryptic plumage that reduces detection by hosts and prey, or evolved mimicry of hawks by parasitic cuckoos, either for protection against hawk attacks or to facilitate brood parasitism by influencing host behaviour. Here, we provide the first evidence that some small birds respond to common cuckoos Cuculus canorus as if they were sparrowhawks Accipiter nisus. Great tits and blue tits were equally alarmed and reduced attendance at feeders during and after the presentation of mounted specimens of common cuckoos and sparrowhawks, but not in response to control presentations of collared doves or teal. Plumage manipulations revealed that the strong alarm response to cuckoos depended on their resemblance to hawks; cuckoos with barred underparts were treated like hawks, while those with unbarred underparts were treated like doves. However, barring was not the only feature inducing alarm because tits showed similarly strong alarm to barred and unbarred hawks, and little alarm to barred doves. These responses of tits, unsuitable as hosts and hence with no history of cuckoo parasitism, suggest that naive small birds can mistake cuckoos for hawks. Thus, any cuckoo-hawk discrimination by host species is likely to be an evolved response to brood parasitism.