A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators.

There is evidence that in Europe and North America many species of pollinators are in decline, both in abundance and distribution. Although there is a long list of potential causes of this decline, there is concern that neonicotinoid insecticides, in particular through their use as seed treatments are, at least in part, responsible. This paper describes a project that set out to summarize the natural science evidence base relevant to neonicotinoid insecticides and insect pollinators in as policy-neutral terms as possible. A series of evidence statements are listed and categorized according to the nature of the underlying information. The evidence summary forms the appendix to this paper and an annotated bibliography is provided in the electronic supplementary material.

Introduction

Neonicotinoid insecticides are a highly effective tool to reduce crop yield losses owing to insect pests. Since their introduction in the 1990s, their use has expanded so that today they comprise about 30% by value of the global insecticide market [1]. They are commonly applied to crops as seed treatments, with the insecticide taken up systemically by the growing plant, so that it can be present in all plant parts, including nectar and pollen that bees and other pollinating insects collect and consume. Pollinators can potentially be exposed to neonicotinoids in other ways, for example through plant exudates, dust from planting machines and contamination of soil and water.

There is evidence that in Europe and North America many species of pollinators are in decline; both in abundance and distribution. There is a long list of potential causes for these declines, including parasites, disease, adverse weather and loss of habitat [2,3]. However, there has been particular concern about the impact on pollinators of the relatively recently introduced neonicotinoids and the European Union (EU) imposed a partial restriction on their use in December 2013. This decision has been criticized on the grounds that the benefits of neonicotinoid use outweigh any detriment they might cause.

The tension between the agricultural and environmental consequences of neonicotinoid use, and the recent EU restriction, has made this topic one of the most controversial involving science and policy. Here, we describe a project that aimed to provide a ‘restatement’ of the relevant natural science evidence base expressed in a succinct way that is comprehensible to non-expert readers. We have tried to be policy-neutral though are aware that complete neutrality is impossible. The evidence restatement forms appendix A to this paper and is accompanied in the electronic supplementary material by a detailed annotated bibliography that provides an entry into the technical literature. The restatement is divided into six sections: after a description of the methodology and the importance of pollinators and insecticides, successive sections consider evidence for exposure paths, laboratory evidence for lethal and sublethal effects, the occurrence of residues in pollinators and their products in the environment, experiments conducted in the field, and consequences for pollinators at colony and population levels.

Experiments to establish the effect of defined doses of insecticides upon individual pollinators are required by regulatory authorities and can be carried out under laboratory conditions. These laboratory studies have the strength of allowing carefully controlled experiments to be performed on individual insects subjected to well-defined exposure. However, because they are conducted under artificial conditions, it is hard to assess a number of processes that may be relevant in the field. For example, neonicotinoids may affect the sensitivity of insects to other stressors; pollinators may actively avoid food contaminated by insecticide and responses at the colony or population level may mitigate or exacerbate the loss or impairment of individual insects. Nevertheless, such experiments provide important information about the range of concentrations where death or sublethal effects are to be expected.

Purely observational surveys in the field are used to establish the levels of exposure that occur under normal use. A number of large surveys in different countries have measured neonicotinoid residues in wild-foraging honeybees and unmanaged pollinators, as well as in nectar, pollen, honey and wax within bee colonies. These data are heavily weighted towards honeybees, and long time series are seldom available.

Experiments in the field are used to establish the impact of different doses of insecticide on pollinator behaviour, mortality and colony performance. They may be conducted as part of the registration process or for general research. One class of experiment involves bees artificially exposed to neonicotinoids and then observed to forage in the field. These are designed to discover whether neonicotinoids affect the performance of individual pollinators (and where appropriate their colonies) under field conditions. The critical issue here is whether the experimental exposure to insecticides is representative of what pollinators are actually likely to experience. The second class of experiment involves placing bee colonies in the environment in situations where they are exposed to crops treated with neonicotinoids, with suitable controls. These are large, difficult experiments where the unit of replication is typically the field site and where there are potentially many confounding factors to be taken into consideration. So far only one such study has been concluded successfully. The statistical power of this type of experiment is likely to be constrained by the expense and logistics of high levels of replication.

To understand the consequences of changing neonicotinoid use, it is important to consider pollinator colony- and population-level processes, the likely effect on pollination ecosystem services, as well as how farmers might change their agronomic practices in response to restrictions on neonicotinoid use. While all these areas are currently being researched, there is at present a relatively limited evidence base to guide policy-makers.

Material and methods

The literature on pollinators and neonicotinoids was reviewed and a first draft evidence summary produced by a subset of the authors. At a workshop, all authors met to discuss the different evidence components and to assign to each a description of the nature of the evidence using a restricted set of terms. We considered several options to describe the nature of the evidence we summarize including the GRADE [4] system widely used in the medical sciences, or the restricted vocabulary used by the International Panel on Climate Change [5]. However, none precisely matched our needs and instead we used a scoring system based on one previously developed for another ‘restatement’ project concerning bovine tuberculosis [6]. The categories we used are:

— [Data] a strong evidence base involving experimental studies or field data collection, with appropriate detailed statistical or other quantitative analysis;

— [Exp_op] a consensus of expert opinion extrapolating results from related ecological systems and well-established ecological principles;

— [Supp_ev] some supporting evidence but further work would improve the evidence base substantially; and

— [Projns] projections based on the available evidence for which substantial uncertainty often exists that could affect outcomes.

These categories are explicitly not in rank order.

A revised evidence summary was produced and further debated electronically to produce a consensus draft. This was sent out to 34 stakeholders or stakeholder groups including scientists involved in pollinator research, representatives of the farming and agrochemical industries, non-governmental organizations concerned with the environment and conservation, and UK government departments and statutory bodies responsible for pollinator policy. The document was revised in the light of much helpful feedback. Though many groups were consulted, the project was conducted completely independently of any stakeholder and was funded by the Oxford Martin School (part of the University of Oxford).

Results

The summary of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators is given in appendix A, with an annotated bibliography provided as the electronic supplementary material.

Discussion

The purpose of this project is not to conclude whether neonicotinoids are ‘safe’ or ‘dangerous’ but to try to help set out the existing evidence base. When neonicotinoids are used as seed dressing on crops visited by pollinators there is no doubt that these systemic insecticides are typically present in pollen and nectar and so bees and other pollinators can be exposed to them [7,8]. The concentrations in pollen and nectar are nearly always some way below those that would cause immediate death. The great problem is to understand whether the sublethal doses received by pollinators in the field lead to significant impairment in individual performance, and whether the cumulative effect on colonies and populations affects pollination in farmed and non-farmed landscapes and the viability of pollinator populations [3].

For this topic, the published literature is a small fraction of the evidence that has been collected. The process of registering a new insecticide requires the production of detailed environmental risk assessments (see http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2013:093:0001:0084:EN:PDF and http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2013:093:0085:0152:EN:PDF). These include substantial evidence on toxicity to non-target organisms (including honeybees) and a range of further studies that will, in some cases, escalate to full-scale field trials of toxicity. The data generated in such studies are not typically in the public domain, or only in a form summarized by the regulatory agencies, and hence we have not been able to include reference to them. There are understandable commercial reasons for the withholding of this information, though the chief reason is not that it contains proprietary intellectual property but that the information would be commercially advantageous to a competitor in registering the compound when it is out of licence. We wonder if registration rules might be amended to allow this type of data to be published, a clear public good, without disadvantaging companies that had invested in its collection.

If neonicotinoids are not available, then farmers will have to choose alternative pest-management strategies, alternative crops or accept greater losses. The impact upon pollinators of withdrawing neonicotinoids will be greatly influenced by such choices. Farmers' likely strategies when faced with restrictions on the use of neonicotinoids are being researched, but there is currently only limited evidence to guide policy-makers in what changes to expect. This is just one aspect of human behaviour, economics and other social science that may be relevant to questions about threats to pollinators. However, it was not the purpose of this review to summarize the social science literature in this area (the annotated bibliography provides an entry into this literature).

There is clear evidence of the great value of neonicotinoids in agriculture [1] as well as the importance of the ecosystem services provided to agriculture by managed and wild pollinators [9]. Pollinators also have intrinsic importance as components of natural biodiversity that cannot, or can only inexactly, be accorded economic value. In some cases, intelligent regulation of insecticide use can provide ‘win-wins’ that improve both agricultural and biodiversity outcomes but in other cases there will be trade-offs, both within and between different agricultural and environmental objectives. Different stakeholders will quite naturally differ in the weightings they attach to the variety of objectives affected by insecticide use, and there is no unique answer to the question of how best to regulate neonicotinoids, an issue that inevitably has both economic and political dimensions. But economic and political arguments need to be consistent with the natural science evidence base, even though the latter will always be less complete than desirable. We hope that our attempt to set out this evidence base in as policy-neutral a manner as possible will stimulate discussion within the science community about whether our assessments are fair and where investment most needs to be made to strengthen them. We hope it will also make the evidence base less contested and so help stakeholders from all perspectives develop coherant policy and policy recommendations.