Coping with third parties in a nursery pollination mutualism: Hadena bicruris avoids oviposition on pathogen‐infected, less rewarding Silene latifolia

Summary•  In nursery pollination systems, pollinator offspring usually feed on pollinated fruits or seeds. Costs and benefits of the interaction for plant and pollinator, and hence its local outcome (antagonism–mutualism), can be affected by the presence of ‘third‐party’ species. Infection of Silene latifolia plants by the fungus Microbotryum violaceum halts the development of fruits that provide shelter and food for larvae of the pollinating moth Hadena bicruris. We investigated whether the moth secures its benefit by selective oviposition on uninfected flowers. •  Oviposition was recorded in eight natural populations as a function of plant infection status, local neighbourhood, plant and flower characteristics. •  Oviposition was six times lower on flowers from infected than on those from uninfected plants. Oviposition decreased with decreasing flower and ovary size. Moths could use the latter to discriminate against diseased flowers. •  Although moths show an adaptive oviposition response, they reduce the future potential of healthy hosts because they still visit infected plants for nectar, vectoring the disease, and they reduce any fitness advantage gained by disease‐resistant plants through selective predation of those plants.