Meta-analysis reveals that seed-applied neonicotinoids and pyrethroids have similar negative effects on abundance of arthropod natural enemies

Background. Seed-applied neonicotinoids are widely used in agriculture, yet their effects on non-target species remain incompletely understood. One important group of non-target species is arthropod natural enemies (predators and parasitoids), which contribute considerably to suppression of crop pests. We hypothesized that seed- applied neonicotinoids reduce natural-enemy abundance, but not as strongly as alternative insecticide options such as soil- and foliar-applied pyrethroids. Furthermore we hypothesized that seed-applied neonicotinoids affect natural enemies through a combination of toxin exposure and prey scarcity. Methods. To test our hypotheses, we compiled datasets comprising observations from randomized field studies in North America and Europe that compared natural-enemy abundance in plots that were planted with seed-applied neonicotinoids to control plots that were either (1) managed without insecticides (20 studies, 56 site-years, 607 observations) or (2) managed with pyrethroid insecticides (eight studies, 15 site-years, 384 observations). Using the effect size Hedge's d as the response variable, we used meta-regression to estimate the overall effect of seed-applied neonicotinoids on natural- enemy abundance and to test the influence of potential moderating factors. Results. Seed-applied neonicotinoids reduced the abundance of arthropod natural enemies compared to untreated controls (d =-0.30±0.10 [95% confidence interval]), and as predicted under toxin exposure this effect was stronger for insect than for non- insect taxa (QM D 8.70, df D 1, P D 0.003). Moreover, seed-applied neonicotinoids affected the abundance of arthropod natural enemies similarly to soil- or foliar- applied pyrethroids (d=0.16 ± 0.42 or -0.02 ± 0.12; with or without one outlying study). Effect sizes were surprisingly consistent across both datasets (I₂ D 2:7% for no-insecticide controls; I₂ D0% for pyrethroid controls), suggesting little moderating influence of crop species, neonicotinoid active ingredients, or methodological choices. Discussion. Our meta-analysis of nearly 1,000 observations from North American and European field studies revealed that seed-applied neonicotinoids reduced the abundance of arthropod natural enemies similarly to broadcast applications of pyrethroid insecticides. These findings suggest that substituting pyrethroids for seed- applied neonicotinoids, or vice versa, will have little net affect on natural enemy abundance. Consistent with previous lab work, our results also suggest that seed-applied neonicotinoids are less toxic to spiders and mites, which can contribute substantially to biological control in many agricultural systems. Finally, our ability to interpret the negative effect of neonicotinoids on natural enemies is constrained by difficulty relating natural-enemy abundance to biological control function; this is an important area for future study.