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

Abstract

BackgroundSeed-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.MethodsTo 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.ResultsSeed-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 = 8.70, df = 1, P = 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 = 2.7% for no-insecticide controls; I2 = 0% for pyrethroid controls), suggesting little moderating influence of crop species, neonicotinoid active ingredients, or methodological choices.DiscussionOur 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.

Ecological impacts of pesticide seed treatments on arthropod communities in a grain crop rotation

“…The lack of impact on soil taxa is consistent with the low levels of insecticide residues we found in the soil, which were generally below the threshold for acute toxicity towards arthropods (Douglas & Tooker, 2016;Pisa et al, 2015). However, as mentioned earlier, chronic exposure to the low levels of insecticides that we detected could sub-lethally impact soil-dwelling organisms over time.…”

“…Additionally, it has been suggested that individual studies of pesticide non-target impacts lack the power to detect effects due to relatively small sample size and high variability in arthropod community datasets (Douglas & Tooker, 2016). A meta-analysis across 20 studies revealed small negative effects [effect size d = −0.30 ± 0.10 (95% confidence interval)] on natural enemy abundance associated with NSTs, with a trend towards soil taxa being more impacted than foliar taxa (Douglas & Tooker, 2016 we expected foliar communities to recover rapidly, as observed by Disque et al (2018) in maize. In contrast, PRC analysis for sticky cards showed increasing deviations from the control community over time in insecticide-treated winter wheat and for all pesticide treatments in maize, with no recovery over the sampling period.…”

Effects of Thiamethoxam-Treated Seed on Mexican Bean Beetle (Coleoptera: Coccinellidae), Nontarget Arthropods, and Crop Performance in Southwestern Virginia Snap Beans

“…Many studies have shown the potential for neonicotinoid seed-treatments to harm nontarget organisms such as arthropod pollinators and predators (Prabhaker et al 2011, Seagraves and Lundgren 2012, Lundin et al 2015, Douglas and Tooker 2016. Although neonicotinoid seed-treatments have shown efficacy against many snap bean pests (Nault et al 2004, Koch et al 2005, Reisig et al 2012, this method has not been tested for efficacy or nontarget effects in snap bean systems predominated by E. varivestis prior to this study.…”

Escalating insecticide resistance in Australian grain pests: contributing factors, industry trends and management opportunities

“…The use of broad‐spectrum insecticides disrupts biological control through direct toxicity to beneficial species and indirectly by changing arthropod communities. While insecticide seed dressings are now widely used in grains and have less pervasive effects on beneficial organisms than conventional high‐volume sprays, they can still adversely impact arthropod predator and parasitoid communities . This is an important issue given the scale at which these insecticides are now being applied.…”

“…While insecticide seed dressings are now widely used in grains and have less pervasive effects on beneficial organisms than conventional high-volume sprays, they can still adversely impact arthropod predator and parasitoid communities. 54,55 This is an important issue given the scale at which these insecticides are now being applied. Outside of beneficial arthropods, a lack of economic thresholds for key pests is a major constraint to the adoption of IPM in Australian grain crops and elsewhere.…”