Forest fragmentation reduces parasitism via species loss at multiple trophic levels

Although there is accumulating evidence from artificially assembled communities that reductions of species diversity result in diminished ecosystem functioning, it is not yet clear how real-world changes in diversity affect the flow of energy between trophic levels in multi-trophic contexts. In central Argentina, forest fragmentation has led to species loss of plants, herbivore and parasitoid insects, decline in trophic processes (herbivory and parasitism), and food web contraction. Here we examine if and how loss of parasitoid species following fragmentation causes decreased parasitism rates, by analyzing food webs of leaf miners and parasitoids from 19 forest fragments of decreasing size. We asked three questions: Do reductions in parasitoid richness following fragmentation directly or indirectly affect parasitism rate? Are changes in community parasitism rate driven by changes in the parasitism rate of individual leaf miner species, or changes in leaf miner composition, or both? Which traits of species determine the effects of food web change on parasitism rates? We found that habitat loss initiated a bottom-up cascade of extinctions from plants to leaf miners to parasitoids, with reductions in parasitoid richness ultimately driving decreases in parasitism rates. This relationship between parasitoid richness and parasitism depended on changes in the relative abundance (but not occurrence) of leaf miners such that parasitoid-rich fragments were dominated by leaf miner species that supported high rates of parasitism. Surprisingly, we found that only a small subset of species in the food web could account for much of the increase in parasitism with parasitoid richness: lepidopteran miners that attained exceptionally high densities in some fragments and their largely specialist parasitoids. How specialized a parasitoid is, and the relative abundance of leaf miners, had important effects on the diversity-parasitism rate relationship, but not other leaf miner traits including trophic breadth, body size, and mine shape. Our results show that a full understanding of the functional consequences of perturbations and species loss requires both a multi-trophic perspective and a trait-based approach, which together capture some of the biological complexity of natural systems.