Parasites and mutualism function: measuring enemy‐free space in a fig–pollinator symbiosis

Abstract

Mutualisms involve cooperation between species and underpin several ecosystem functions. However, there is also conflict between mutualists, because their interests are not perfectly aligned. In addition, most mutualisms are exploited by parasites. Here, we study the interplay between cooperation, conflict and parasitism in the mutualism between fig trees and their pollinator wasps. Conflict occurs because each fig ovary can nurture either one seed or one pollinator offspring and, while fig trees benefit directly from seeds and pollinator offspring (pollen vectors), pollinators only benefit directly from pollinator offspring. The mechanism(s) of conflict resolution is debated, but must explain the widespread observation that pollinators develop in inner, and seeds in outer, layers of fig flowers. We recently suggested a role for non‐pollinating figs wasps (NPFWs) that are natural enemies or competitors of the pollinators and lay their eggs through the fig wall. Most NPFW offspring develop in outer and middle layer flowers, suggesting that inner flowers provide enemy‐free space for pollinator offspring. Here, we test the hypothesis that NPFWs cannot reach inner flowers, by measuring wasp and fig morphology at the species‐specific times of NPFW attack in the field. We found that three species of Sycoscapter and Philotrypesis wasps that parasitise pollinators could reach 34–73%, 75–92% and 82–97% of fig ovaries, respectively. Meanwhile, Eukobelea and Pseudidarnes gall‐formers, despite having shorter ovipositors, can access almost all fig flowers (93–99% and 100%), because they attack smaller (younger) fig fruits. Our mechanistic results from ovipositing wasps support spatial patterns of wasp offspring segregation within figs to suggest that inner ovules provide enemy‐free‐space for pollinators. This may contribute to mutualism stability by helping select for pollinators to avoid laying eggs where they are likely to be parasitised. These outer flowers then remain free to develop as seeds, promoting mutualism persistence.

The dominant exploiters of the fig/pollinator mutualism vary across continents, but their costs fall consistently on the male reproductive function of figs

“…They have limited impact on seed production, even though far more seeds than pollinators are accessible to sycoryctine wasps laying eggs through the syconium wall in the closely related fig F. rubiginosa (Al-Beidh et al, 2012). Our new results therefore provide evidence that the sycoryctines associated with F. obliqua are indeed likely to be inquilines or parasitoids of the pollinators.…”

Parasites exert conflicting selection pressures to affect reproductive asynchrony of their host plant in an obligate pollination mutualism

“…; Al‐Beidh et al . ), could be contributing to stabilizing and maintaining the system through their effects on within‐ and between‐tree reproductive phenology. Since many developing wasps are herbivores, it is also possible that the phenotypic plasticity seen in syconium development is mediated by changes in ethylene (Galil ) as a result of herbivory (Von Dahl & Baldwin ).…”

Plantas, polinizadores e algumas articulações da biologia da polinização com a teoria ecológica

“…Estudando as vespas do figo, Al-Beidh et al (2012) trazem um bom exemplo da teoria de espaço livre de inimigos aplicada no contexto de biologia da polinização. Nesse estudo, eles identificaram três camadas de flores com diferentes níveis de parasitismo dentro dos sicônios.…”

“…Nesse sistema, a diferenciação de nicho espacial de espécies competidoras devido às diferenças na acessibilidade permite a coexistência de polinizadores e não polinizadores. A camada mais interna, à qual as vespas não polinizadoras e parasitoides tem pouco acesso, é muito mais intensamente ocupada pelas vespas polinizadoras que se desenvolvem então em um espaço livre de inimigos (Al-Beidh et al 2012).…”