Does the “Enemies Hypothesis” operate by enhancing natural enemy evenness?

Abstract

Root (1973) observed fewer pests in weedy Brassica oleracea plantings, and suggested this could be because greater plant diversity bolstered resources for natural enemies and strengthened herbivore suppression (i.e., the Enemies Hypothesis) and/or disrupted host-location by specialist herbivores (i.e., the Resource Concentration Hypothesis). These proposed mechanisms have been exceptionally influential in efforts to manage agroecosystems to promote conservation biological control, yet their relative importance remains unclear. Because direct (plant-driven) and indirect (enemy-mediated) drivers of herbivore pressure are difficult to isolate experimentally, we compiled a multi-year observational dataset tracking arthropod pest and predator densities in B. oleracea plantings on over 50 farms varying in weed cover within fields as well as in habitat diversity in surrounding landscapes. We then used structural equation models to evaluate direct and indirect interaction links consistent with the Enemies and Resource Concentration Hypotheses, while also considering landscape context and enemy community structure. We predicted that non-crop habitat would limit herbivores indirectly by supporting evenly distributed communities of natural enemies. Our results revealed that weedy vegetation indeed benefitted predator evenness and thus indirectly correlated with enhanced predator densities, but instead of limiting herbivores, natural enemies seemed to track both aphids and caterpillars. Landscape diversity had no effect on predator evenness, yet appeared to benefit predator density, while having contrasting direct effects on aphids (positive) and caterpillars (negative). We found no evidence for direct negative links between weed cover and herbivores that would indicate an important role for the Resource Concentration Hypothesis. Instead, we found indirect links between weedy plants and natural enemy evenness across our network of field sites, suggesting partial support for the Enemies Hypothesis. More generally, we suggest that greater consideration of predator-predator interactions and local biodiversity effects could help explain inconsistent relationships between landscape diversity and herbivore suppression.