The cost of mutualism: interactions between Trollius europaeus and its pollinating parasites

Summary

Pollination by seed parasites is unusual, and previously studied case involve plant species (figs, yuccas) that are pollinated mostly by one host-specific pollinator. Trollius europaeus (Ranunculaceae), however, is pollinated by four Chiastocheta species (Diptera: Anthomyiidae) that mate in the flowers, eat pollen and nectar, and complete larval development in the seeds. Strict resource partitioning is present between the fly species, in that different parts of the infructescence are used by larvae of each species, and fly species oviposit at different times in the life of a flower. The flies were shown to be the exclusive pollinators. Because the numbers of ovules fertilized per visit was a fixed proportion of remaining non-fertilized ovules, fly species differed in mean pollinator efficacy, with the last species contributing the fewest pollinations. Therefore, with larval consumption of seeds being fixed and seed initiation decreasing per visit, larvae from later ovipositions consumed more seeds than their mothers pollinated. The point at which costs and benefits were equal was found to be around 4–5 eggs; observed population means of eggs per flower varied between 2.3–7.25 during three years of study. The system is rather insensitive to variation in pollinator density, remaining mutualistic over a wide range. Small changes in pollinator efficacy, however, can tilt the equilibrium to a negative net effect for the plant. These data on Trollius/ Chiastocheta interactions provide the first extensive cost/ benefit analyses for mutualism based on seed parasites as pollinators.