Parasitoids Turn Herbivores into Mutualists in a Nursery System Involving Active Pollination

Nursery pollination involves pollinators that lay eggs on the flowers they pollinate and have their brood fed on flower parts or developing ovules [1-4]. Active pollination, a ritualistic behavioral sequence shown by nursery pollinators when transferring pollen from anthers to stigmas, is known in only four plant lineages [5-8], including the classical examples of fig trees-fig wasps and yuccas-yucca moths [5, 6]. We report in detail a system in which weevils actively pollinate orchids prior to having their larvae fed on the developing fruits. Sampling over five years revealed that although weevils trigger fruit set, this interaction is negative for the plant as weevil larvae often consume all contents of infested fruits. However, part of weevil-infested fruits is often rescued'' by parasitoid wasps, which kill the weevil larvae before all fruit content is consumed (Figure 1). Rescued'' fruits present high seed viability and biomass similar to that of non-infested fruits, much higher than that of fruits with weevils only. Hence, parasitoids mediate the fitness consequences of the interaction between the plant and its parasitic pollinator. Weevils constitute a meg-adiverse group of herbivores commonly reported as florivores [9] but are also appreciated as flower-ovipositing pollinators of cycads and palms [4, 10-13] and were previously recorded carrying orchid pollinaria [14-16]. The orchid-weevil system presented here shows that plant-floral visitor interaction outcome can be mediated by a third party (parasitoids) and illustrates a way by which the biological context may allow the emergence and persistence of active nursery pollination behavior in nature.