EDITOR'S CHOICE: Neonicotinoid insecticide travels through a soil food chain, disrupting biological control of non‐target pests and decreasing soya bean yield

Abstract

Summary1. Neonicotinoids are the most widely used insecticides world-wide, but their fate in the environment remains unclear, as does their potential to influence non-target species and the roles they play in agroecosystems. 2. We investigated in laboratory and field studies the influence of the neonicotinoid thiamethoxam, applied as a coating to soya bean seeds, on interactions among soya beans, nontarget molluscan herbivores and their insect predators. 3. In the laboratory, the pest slug Deroceras reticulatum was unaffected by thiamethoxam, but transmitted the toxin to predaceous beetles (Chlaenius tricolor), impairing or killing >60%. 4. In the field, thiamethoxam-based seed treatments depressed activity-density of arthropod predators, thereby relaxing predation of slugs and reducing soya bean densities by 19% and yield by 5%. 5. Neonicotinoid residue analyses revealed that insecticide concentrations declined through the food chain, but levels in field-collected slugs (up to 500 ng g À1 ) were still high enough to harm insect predators. 6. Synthesis and applications. Our findings reveal a previously unconsidered ecological pathway through which neonicotinoid use can unintentionally reduce biological control and crop yield. Trophic transfer of neonicotinoids challenges the notion that seed-applied toxins precisely target herbivorous pests and highlights the need to consider predatory arthropods and soil communities in neonicotinoid risk assessment and stewardship.

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

“…Aphids and thrips are listed on the neonicotinoid label for soybeans and so could be considered ‘target pests,’ though in practice soybean aphids are often not controlled sufficiently with seed-applied neonicotinoids (Myers & Hill, 2014). Slugs are non-target pests because they are generally not susceptible to neonicotinoids (Douglas, Rohr & Tooker, 2015; Simms, Ester & Wilson, 2006). …”

“…Both effect sizes suggest that synthetic insecticides can undermine natural-enemy populations, but the consequences of these reductions for ecosystem services are hard to predict given a lack of research relating predator abundance to biological control function and its economic value (Naranjo, Ellsworth & Frisvold, 2015). The one study in our dataset that explicitly related predator abundance to crop yield was our previous study in a no-till soybean system (Douglas, Rohr & Tooker, 2015). In that study, a 31% reduction in early season abundance of slug predators in neonicotinoid-treated plots corresponded to a 67% increase in slug abundance and an eventual 5% reduction in soybean yield.…”

The pros and cons of ecological risk assessment based on data from different levels of biological organization

“…For instance, for some species, outdoor community-level mesocosm studies can capture positive and negative density-dependence at the population level (for those species that can reproduce in the mesocosms during the experiment), recovery from contaminants based on detoxification, reproduction, and dispersal (e.g., flying insects, some zooplankton, some algae, some microbes), and species interactions that can alter effects of contaminants (Douglas et al 2015, Staley et al 2010, Staley et al 2014). Additionally, outdoor mesocosm studies can do a good job of capturing cause-effect relationships between a contaminant and species densities.…”

Evidence for the effects of neonicotinoids used in arable crop production on non-target organisms and concentrations of residues in relevant matrices: a systematic map protocol

“…and indirect (e.g. reduction in prey or through soil, plant and water matrices) adverse effects of NNIs on non-target organisms other than bees, for example: beneficial predatory invertebrates via the consumption of crop pests [29,30] and parasitic wasps through nectar feeding [31], birds through the consumption of treated seed [32][33][34] or reduction in insect food [35], aquatic invertebrates via leaching of NNIs into water bodies [36][37][38][39][40], and non-target soil organisms via NNI treated seed or soil drenches [28]. A number of studies have also investigated the potential risk to non-target organisms, including pollinators, from the breakdown products (metabolites) of NNIs [15,37,41].…”