A systematic review of the direct and indirect effects of herbivory on plant reproduction mediated by pollination

Background: Plant reproduction is influenced by the net outcome of plant-herbivore and plant-pollinator interactions. While both herbivore impacts and pollinator impacts on plant reproduction have been widely studied, few studies examine them in concert. Methodology: Here, we review the contemporary literature that examines the net outcomes of herbivory and pollination on plant reproduction and the impacts of herbivores on pollination through damage to shared host plants using systematic review tools. The direct or indirect effects of herbivores on floral tissue and reported mechanisms were compiled including the taxonomic breadth of herbivores, plants and pollinators. Results: A total of 4,304 studies were examined producing 59 relevant studies for synthesis that reported both pollinator and herbivore measures. A total of 49% of studies examined the impact of direct damage to floral tissue through partial florivory while 36% of studies also examined the impact of vegetative damage on pollination through folivory, root herbivory, and stem damage. Only three studies examined the effects of both direct and indirect damage to pollination outcomes within the same study. Conclusions: It is not unreasonable to assume that plants often sustain simultaneous forms of damage to different tissues and that the net effects can be assessed through differences in reproductive output. Further research that controls for other relative drivers of reproductive output but examines more than one pathway of damage simultaneously will inform our understanding of the mechanistic relevance of herbivore impacts on pollination and also highlight interactions between herbivores and pollinators through plants. It is clear that herbivory can impact plant fitness through pollination; however, the relative importance of direct and indirect damage to floral tissue on plant reproduction is still largely unknown.