Why fitness impacts of different herbivores may combine nonadditively, and why it matters to the ecology and evolution of plant-herbivore communities

Background and aims – The manner by which the effects of multiple antagonists combine is a fundamental issue in ecology. This issue has been especially important in plant-herbivore evolutionary ecology—particularly predicting whether the combined fitness impacts of multiple herbivores on a shared host plant can be inferred by simply adding the individual impacts that each herbivore has when feeding alone. Despite accumulating empirical data, relatively little theoretical progress has been made in explaining why impacts of herbivore damage often combine nonadditively, as well as predicting the conditions that lead to a greater-than-additive (synergistic) or to a less-than-additive (subadditive) pattern. Material and methods – Based on considerations of limiting resources and source-sink relationships, I proposed and tested two hypotheses: 1) The fitness impacts of two species of herbivores that affect the same resource (i.e. feed on the same tissue in a similar fashion) will combine in a synergistic pattern (if that resource is not limiting reproduction when plants do not experience herbivory), and 2) The fitness impacts of two herbivores that affect different resources (i.e. feed on different tissues) will combine in a subadditive pattern. I performed a field experiment in which horsenettle (Solanum carolinense) was exposed to a factorial combination of four levels of leaf herbivory and five levels of simulated floral herbivory. Key results – The results were consistent with both hypotheses: 1) The combined fitness impact of flower damage that was simulated as being caused by two florivorous species feeding on the same plants was greater than the sum of the same total amount of damage when the two species were simulated as feeding individually; and 2) The combined fitness impact of the leaf and floral damage was less than the sum of the same total amount of damage when the two species fed individually. Conclusions – The main ecoevolutionary implication of these results is that subadditive impacts of leaf- and flower-feeding herbivores could weaken selection for resistance in horsenettle (or any plant species that hosts multiple herbivores), and thus subadditive impacts may contribute to the maintenance of diverse herbivore communities sharing a species of host plant.