Neonicotinoid Insecticides and Their Impacts on Bees: A Systematic Review of Research Approaches and Identification of Knowledge Gaps.

Ola Lundin,Ingemar Fries,Henrik G Smith,Maj Rundlöf,Riccardo Bommarco,Nigel E Raine

doi:10.1371/journal.pone.0136928

Abstract

It has been suggested that the widespread use of neonicotinoid insecticides threatens bees, but research on this topic has been surrounded by controversy. In order to synthesize which research approaches have been used to examine the effect of neonicotinoids on bees and to identify knowledge gaps, we systematically reviewed research on this subject that was available on the Web of Science and PubMed in June 2015. Most of the 216 primary research studies were conducted in Europe or North America (82%), involved the neonicotinoid imidacloprid (78%), and concerned the western honey bee Apis mellifera (75%). Thus, little seems to be known about neonicotinoids and bees in areas outside Europe and North America. Furthermore, because there is considerable variation in ecological traits among bee taxa, studies on honey bees are not likely to fully predict impacts of neonicotinoids on other species. Studies on crops were dominated by seed-treated maize, oilseed rape (canola) and sunflower, whereas less is known about potential side effects on bees from the use of other application methods on insect pollinated fruit and vegetable crops, or on lawns and ornamental plants. Laboratory approaches were most common, and we suggest that their capability to infer real-world consequences are improved when combined with information from field studies about realistic exposures to neonicotinoids. Studies using field approaches often examined only bee exposure to neonicotinoids and more field studies are needed that measure impacts of exposure. Most studies measured effects on individual bees. We suggest that effects on the individual bee should be linked to both mechanisms at the sub-individual level and also to the consequences for the colony and wider bee populations. As bees are increasingly facing multiple interacting pressures future research needs to clarify the role of neonicotinoids in relative to other drivers of bee declines.

Highlights

Animal pollination, mainly performed by bees, is an important ecosystem service with almost 90 percent of flowering plants and 75 percent of the world’s most common crops benefiting from animal flower visitation [1,2]
Concern for pollinators has led to a temporary restriction of three neonicotinoids as seed treatments for use on crops attractive to bees in the European Union [15] and a policy to reduce the use of the same three insecticides as seed treatments for maize and soy by 80 percent from 2014 levels in Ontario, Canada [16]
Based on our systematic literature review we conclude that despite considerable research efforts, there are still significant knowledge gaps concerning the impacts of neonicotinoids on bees

Summary

Introduction

Mainly performed by bees, is an important ecosystem service with almost 90 percent of flowering plants and 75 percent of the world’s most common crops benefiting from animal flower visitation [1,2]. Neonicotinoid compounds are used in more than 120 countries with at least 140 different crop uses (e.g. soil and foliar applications of the same compound in the same crop are defined as two different crop uses) [7] Since their commercial introduction in the early 1990s, neonicotinoids have quickly become the most commonly used class of insecticides in the world. Neonicotinoids have high selectivity towards invertebrate over vertebrate organisms [9] They are taken up systemically and can be present in all plant tissues, which makes them efficient against a wide range of pests over a protracted time period and when applied in small quantities, e.g. as seed treatments [7,8,9]. Significant knowledge gaps and controversy remain as to whether such restrictions are justified [17,18,19]

Objectives

Methods

Results

Discussion

Conclusion