Density‐dependent fitness effects stabilize parasitic hitchhiking within a mutualism

Abstract Mutualisms are often subject to perturbations by parasitism arising from third‐party interactions. How third‐party perturbations are dampened is a fundamental question pertaining to mutualism stability. Phoretic organisms that turn parasitic within a mutualism may destabilize it. If the fitness cost of such phoresy is high, then density‐dependent effects could be one mechanism to stabilize these interactions. We experimentally examined the fitness effects of a phoretic nematode community on a brood‐site pollination mutualism involving a pollinating fig wasp (the vehicle) and its associated fig species (the host for wasp and nematode development). We comprehensively investigated fitness impacts of phoresy on wasp lifespan, lifetime reproductive success, dispersal ability and predation risk as well as on host brood‐site volume and seed number. We employed a range of hitchhiker densities that encompassed natural and overloading levels for two nematode taxa (one plant‐ and one animal‐parasitic type). None of the plant host and vehicle fitness parameters were affected by wasps with low nematode transportation loads for either type of nematode. Furthermore, wasps arriving at their destinations carried lower densities of both animal‐ and plant‐parasitic nematodes compared to dispersing wasps, suggesting that there is selection on hitchhiker numbers during the dispersal process and that wasps loaded with a greater density of nematodes do not successfully disperse. Overloaded wasps had shorter flight durations, suggesting limited dispersal ability; on arrival at their destination, they suffered greater predation risk. Such overloaded wasps delivered impaired pollination services and produced fewer offspring resulting in lower lifetime fitness. Therefore, the direct and indirect effects of nematodes on their vehicles are strong. These effects also translated into impacts on host plant fitness, with the overloaded pollinators promoting the development of smaller brood sites with fewer seeds, thus reducing fig tree reproductive success. The effects of the animal parasites were greater than that of the plant parasite in this study. The third‐party interaction is therefore self‐limited and exhibits density dependence. The strong negative effects of overloading likely explain the low number of nematodes found in nature on dispersing and arriving fig wasps. Consequently, parasitic hitchhikers are unlikely to destabilize the mutualism. A free Plain Language Summary can be found within the Supporting Information of this article.