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

Abstract

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 megadiverse 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.

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

“…Likewise, in the related plant genus Phyllanthus, almost 60% of developing Epicephala larvae were killed by braconid wasps, which resulted in increased net seed production (Kawakita & Kato, 2004a). Furthermore, the killing of pollinator larvae by parasitoids in several other non-Epicephala OPMs is also known to promote plant reproductive fitness (Dunn et al, 2008;Nunes et al, 2018). It may be that some of the parasitoid species that attack Epicephala on B. oblongifolia are koinobionts, i.e.…”

“…In addition to pollinators, the fruits of plants involved in OPMs may host various non-pollinating seed predators, parasitoids and hyperparasitoids. Parasitoids can play a direct role in reducing seed herbivory and promoting plant reproductive fitness by killing developing pollinators (Kawakita & Kato, 2004a;Kawakita & Kato, 2004b;Dunn et al, 2008;Nunes et al, 2018). Furthermore, seeds may be consumed by other, non-pollinating seed predators, which are unrelated to pollinators.…”

Friend or foe? A parasitic wasp shifts the cost/benefit ratio in a nursery pollination system impacting plant fitness

“…Dufaÿ and Anstett (2003) reviewed nursery pollination systems and described a total of 13 documented cases, although since then other systems have been discovered (see Kawakita & Kato, 2004; Nunes, Maruyama, Azevedo‐Silva, & Sazima, 2018; Song et al, 2014). Within these systems, there are some which are obligate mutualisms, such as the interaction between Ficus trees and fig wasps, Yucca and yucca moths, or senita cacti and senita moths (Anstett, Bronstein, & Hossaert‐McKey, 1996; Dufaÿ & Anstett, 2003; Holland & Fleming, 1999; Pellmyr et al, 1996).…”

“…In an empirical case study, though not of a nursery pollination system, van Loon, Boer, and Dicke (2000) found that parasitization of the herbivore Pieris rapae significantly reduced seed loss of its host plant Arabidopsis thaliana , suggesting that parasitism of herbivores potentially increased plant fitness. In that line, a study by Nunes et al (2018) described a new nursery pollination system formed by a weevil and its orchid host plant, in which parasitoid wasps mediated the outcome of the interaction by killing the weevil larvae and therefore changing the cost/benefit ratio of the partnership. Moreover, very recently Stucchi, Giménez‐Benavides, and Galeano (2019) developed a population dynamics model demonstrating how the Silene–Hadena system might be more stable in the presence of parasitoids.…”

Active pollination drives selection for reduced pollen‐ovule ratios

“…Active pollination has evolved in yucca moths (Riley, ; Pellmyr, ), fig wasps (Ramirez, ; Weiblen, ; Herre et al., ), leafflower moths (Kato et al., ; Kawakita and Kato, ), and senita moths (Fleming and Holland, ; Holland and Fleming, ). Recently, active pollination has also been discovered in weevils that pollinate orchid species (Nunes et al., ) and in heliozelid moths that pollinate Boronia (Rutaceae) in Australia (Milla, ). In all of these species, females actively collect pollen from flowers via specialized behaviors and morphologies.…”