organisms explained above, which is the real cause of concern for the long-term impacts on this ecosystem.

Aquatic vertebrates such as fish, however, may not be affected directly by residues of neonicotinoids in water. Treatment of oyster beds with imidacloprid to avoid burrowing shrimps after harvest did not appear to threaten populations of the endangered green sturgeon (*Acipenser medirostris*) in the west coast of the USA (Frew and Grue 2015; Frew et al. 2015). Nevertheless, the authors only compared the residual concentrations of imidacloprid in the water column (28 ppb) and shrimp (31 ppb) to the acute and chronic toxicity of this insecticide to a surrogate fish species (rainbow trout), since the actual toxicity to the sturgeon is unknown. It is likely that the risks of such contamination to a large fish like the sturgeon are negligible, even though sublethal effects cannot be ruled out (see Section B). Impacts on fish species, if any, would occur through indirect starvation after the invertebrate food source is depleted.

## Conclusions

In the past 3 years, we have gained a greater description about the exposure to neonicotinoids and fipronil and a greater understanding about their effects in arthropods and other species, as a result of a large research effort made worldwide. Fipronil has been studied to a lesser extent. A summary of our worldwide integrated assessment for taxonomic groups is synthesized in Fig. 3, with the exposure data to these systemic insecticides (Giorio et al., 2017, this special issue), their ecotoxicological effects and the related ecosystem services.

Research on bees has revealed new aspects of sublethal effects, including the reduced fecundity of queen bees, impairment of sperm in drones, negative interactions with parasites and the immune system. Our knowledge of acute toxicity has also broadened to include some wild bee species, while the mixture toxicity in combination with other pesticides or infectious agents has reported some synergisms that are more pronounced than simply additive. Impacts of neonicotinoids and fipronil at the population level of bumblebees were known to some extent, but have now been compared among countries with different environments. The impacts on other wild bees were unknown and recent studies have shown that they are more sensitive to neonicotinoids than the honey bee. These impacts on pollinators are a real cause for concern, with a few studies showing a correlation between the use of neonicotinoids and the declines in wild bees and butterflies in Europe and America. Their presence in hedgerows or field margins may expose pollinators to drift or uptake of active molecule by growing plants.

It was known that neonicotinoids were very toxic to natural enemies of agricultural pests and caused secondary poisoning. The new information gathered in this area has only contributed to enlarge the range of species tested, whether predatory or

parasitoids, thus confirming the unsuitability of neonicotinoids for integrated pest control programs.

Little progress has been made, however, in evaluating the effects of these insecticides on soil organisms, with the exception of a study showing the possible bioaccumulation of fipronil in earthworms. Some field studies on indirect impacts on non-target termites and other arthropods have reported ambiguous findings.

New studies on aquatic invertebrates have focused on acute and chronic toxicity of clothianidin, thiamethoxam, and a few new compounds to a wider range of taxa, since the data available until recently referred almost exclusively to imidacloprid. There is now sufficient data to set protective limits for aquatic invertebrate communities in the legislation. Some studies have shown how the current contamination of surface waters in many countries are effectively damaging the underlying insect communities that provide a rich food source not only to fish but also birds and other insectivorous vertebrates. The chronic exposure to low levels of neonicotinoid residues in water are causing a long-term lethality in most aquatic species, which eliminates entire populations from the affected areas.

Fipronil and the neonicotinoids imidacloprid and clothianidin exert a wide range of deleterious sublethal neurological effects in terrestrial vertebrates, such as rats and bats. Ingestion of treated seeds by birds can cause sublethal effects on immunity and can be lethal at times. Aquatic vertebrates, however, are very unlikely to be exposed to lethal or sublethal concentrations of neonicotinoids in their natural environment, whereas environmental concentrations of fipronil may be sufficiently high to harm fish.

Overall, the negative impacts of neonicotinoids and fipronil on terrestrial and aquatic invertebrates are translated in indirect impact for the entire ecosystems. Invertebrates constitute the main food source for an innumerable number of insectivorous vertebrates and fulfill an essential role in recycling organic matter in the soil as well as in water. The consequences of losing the invertebrate fauna due to continuous exposure to ubiquitous residues of neonicotinoids and fipronil are thus far reaching and cannot be ignored any longer.

**Acknowledgments** The work has been funded by the Triodos Foundation's Support Fund for Independent Research on Bee Decline and Systemic Pesticides. This Support Fund received donations from the Act Beyond Trust (Japan), Stichting Triodos Foundation (The Netherlands), M.A.O.C. Gravin van Bylandt Stichting (The Netherlands), Zukunft Stiftung Land-wirtschaft (Germany), Hartmut Spaeter Umweltstiftung (Germany) and citizens. The authors also thank the Lune de Miel Foundation (France), the David Suzuki Foundation (Canada), the SumOfUs community (Germany), the Rovaltain Foundation (France), the Aurelia Foundation (Germany) and IUCN for their help in dissemination of these updated WIA findings. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors declare no competing conflict of interest. The authors thank C. Pacteau, E. Lumawig, N. Pezant, T. Brooks, and A.-L. Thomann for fruitful discussions and their help in this project.
**Open Access** This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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