Temporal synchrony mediates the outcome of indirect effects between prey via a shared predator

摘要

The role of generalist predators in suppressing herbivores in complex food webs is controversial because alternative prey can modulate predation on focal prey through various indirect interactions, e.g. by distracting or enhancing predation (i.e. apparent mutualism and apparent competition, respectively). We predict that temporal synchrony (i.e., whether the two prey items co-occur at the same time) mechanistically shifts the indirect predator-mediated effect from mutualism in the short-term to competition in the long-term. The impact of alternative prey on population growth of soybean aphid (Aphis glycines), a key invasive pest in Northern American soybean fields, was tested over two years in 520 replicated open field plots. Specifically, we tested short- and long-term predator-mediated indirect interactions, respectively, by quantifying these relationships instantaneously vs. implementing a time lag with alternative prey preceding aphid trials by two weeks. This allowed us to statistically disentangle behavioral effects of prey preferences from population-level effects mediated by numerical responses of natural enemies. The predator, Orius insidiosus, constituted >90% of the aphidophagous predator community and was thus considered the driver of indirect interactions between pests. Of the alternative prey, soybean thrips, Neohydatothrips variabilis, was the dominant species and predicted variation in aphid population growth rates in three of four analyses. Notably, thrips increased aphid growth when co-occurring in the short-term, presumably by satiating O. insidiosus, but negatively affected aphids when tested with a time lag (i.e., asynchronous dynamics). Mites also weakened aphid suppression in the short-term during one of two years. These data suggest that indirect effects in food webs are not static, but fluctuate between positive and negative depending on the time scale over which interactions are tracked. Consequently, alternative foods can be simultaneously beneficial and detrimental to prey suppression with the net effect likely driven by the degree of phenological synchrony exhibited by the co-occurring herbivores.