An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 2: impacts on organisms and ecosystems

Lennard Pisa,Dave Goulson,Chiara Giorio,Chris J K Macquarrie,Jean-Marc Bonmatin,En-Cheng Yang,Edward Mitchell,Melanie Mcfield,Alexandre Aebi,Elizabeth Yim Long,David Gibbons,Maarten Bijleveld Van Lexmond,Francisco Sánchez-Bayo,Jeroen Van Der Sluijs

doi:10.1007/s11356-017-0341-3

Abstract

New information on the lethal and sublethal effects of neonicotinoids and fipronil on organisms is presented in this review, complementing the previous Worldwide Integrated Assessment (WIA) in 2015. The high toxicity of these systemic insecticides to invertebrates has been confirmed and expanded to include more species and compounds. Most of the recent research has focused on bees and the sublethal and ecological impacts these insecticides have on pollinators. Toxic effects on other invertebrate taxa also covered predatory and parasitoid natural enemies and aquatic arthropods. Little new information has been gathered on soil organisms. The impact on marine and coastal ecosystems is still largely uncharted. The chronic lethality of neonicotinoids to insects and crustaceans, and the strengthened evidence that these chemicals also impair the immune system and reproduction, highlights the dangers of this particular insecticidal class (neonicotinoids and fipronil), with the potential to greatly decrease populations of arthropods in both terrestrial and aquatic environments. Sublethal effects on fish, reptiles, frogs, birds, and mammals are also reported, showing a better understanding of the mechanisms of toxicity of these insecticides in vertebrates and their deleterious impacts on growth, reproduction, and neurobehaviour of most of the species tested. This review concludes with a summary of impacts on the ecosystem services and functioning, particularly on pollination, soil biota, and aquatic invertebrate communities, thus reinforcing the previous WIA conclusions (van der Sluijs et al. 2015).

Highlights

Since the publication of the first Worldwide Integrated Assessment (WIA) review (Bijleveld van Lexmond et al 2015) on the impact of neonicotinoids and fipronil systemic insecticides on invertebrates (Pisa et al 2015), vertebrates (Gibbons et al 2015), ecosystem services (Chagnon et al 2015), and its conclusions, there has been a surge in publications related to this important issue
The impact of neonicotinoids on pollination has primarily been studied for oil seed rape agro-ecosystems. This crop is especially relevant at least in the European context because, as stated by Budge et al (2015): BNowhere is this tension more evident than in the system we describe here with the world’s most widely used insecticide, the world’s most widely used managed pollinator and Europe’s most widely grown mass flowering crop.^ These authors used combined data on large-scale pesticide use, yields of oliseed rape and honeybee colony losses over an 11 year period in England and Wales to study the impact of the three major neonicotioids used in that crop
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

Summary

Introduction

Since the publication of the first Worldwide Integrated Assessment (WIA) review (Bijleveld van Lexmond et al 2015) on the impact of neonicotinoids and fipronil systemic insecticides on invertebrates (Pisa et al 2015), vertebrates (Gibbons et al 2015), ecosystem services (Chagnon et al 2015), and its conclusions (van der Sluijs et al 2015), there has been a surge in publications related to this important issue. The first review paper of the updated WIA (Giorio et al 2017, this special issue) deals with the mode of action of neonicotinoids and fipronil, their metabolism, synergies with other pesticides or stressors, degradation products, and the contamination of the environment by neonicotinoids and fipronil, including new insecticides introduced on the market. For this second review paper, a broad-scaled literature search was performed using the Web of ScienceTM and Scopus® as reported by Gibbons et al (2015) and restricted to the years 2014-early 2017. It summarizes the current regulations in Europe and other countries concerning these widely used systemic insecticides

Part A: invertebrates

Part B: vertebrates

Summary of impacts on vertebrates

Part C: Ecosystem services

Findings

Conclusions