Literature DB >> 26511042

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

H Charles J Godfray1, Tjeerd Blacquière2, Linda M Field3, Rosemary S Hails4, Simon G Potts5, Nigel E Raine6, Adam J Vanbergen7, Angela R McLean8.   

Abstract

A summary is provided of recent advances in the natural science evidence base concerning the effects of neonicotinoid insecticides on insect pollinators in a format (a 'restatement') intended to be accessible to informed but not expert policymakers and stakeholders. Important new studies have been published since our recent review of this field (Godfray et al. 2014 Proc. R. Soc. B 281, 20140558. (doi:10.1098/rspb.2014.0558)) and the subject continues to be an area of very active research and high policy relevance.
© 2015 The Authors.

Entities:  

Keywords:  bumblebee; evidence for policy; honeybee; neonicotinoid; pest management; pollinator

Mesh:

Substances:

Year:  2015        PMID: 26511042      PMCID: PMC4650156          DOI: 10.1098/rspb.2015.1821

Source DB:  PubMed          Journal:  Proc Biol Sci        ISSN: 0962-8452            Impact factor:   5.349


Introduction

Neonicotinoid insecticides were introduced in the 1990s and their market share quickly expanded to approximately a third of the global insecticide total by value. They are used in different ways, but particularly as seed treatments where the chemical is absorbed by the growing plant and is distributed through all tissues at concentrations that can kill insect herbivores. However, neonicotinoids are also translocated to nectar and pollen where they can be consumed by pollinating insects. Numbers of pollinators have declined in agricultural landscapes and there is concern that the introduction and widespread use of neonicotinoids is partly responsible. In December 2013, the European Union (EU) instigated partial restrictions on the use of neonicotinoid insecticides on crops that might be used as food by pollinating insects. This move is strongly opposed by many in the farming community and there has been a vigorous debate focusing on the scientific evidence that neonicotinoids harm pollinators, as well as the environmental and economic costs and benefits of the restrictions. To try to assist the debate we produced a ‘restatement’ of the underlying natural science evidence base in a form that was intended to be accessible to informed but not expert policymakers and stakeholders [1]. Our avowed aim was to be as policy-neutral as possible while acknowledging that perfect neutrality is never achievable. The restatement was published as an appendix to a short paper in this journal accompanied by an extensive annotated bibliography as the electronic supplementary material. Since the restatement was published the debate about restricting neonicotinoid use has continued unabated. Farming organizations have successfully applied for ‘120-day derogations’ from the restrictions in several European countries (see electronic supplementary material, paragraph A.2) on the grounds of lack of alternative pest-management options, moves that have been criticized by environmental non-governmental organizations. The EU is committed to review the restrictions in 2015–2016 and through the independent European Food Safety Authority opened a call for evidence (closing 30 September 2015; http://www.efsa.europa.eu/en/data/call/150522). Much new research has been published on the topic (we review over 80 studies here) including the largest replicated field study to date [2]. Despite the relatively short time since the restatement was published we provide here an update in the same format. We do this (i) because of the significant advances in the science; (ii) because of the continuing need for policy-neutral evidence summaries in this highly contested area, especially in the run up to the review of the EU restrictions; and (iii) in response to a request to do so by the UK Government Chief Scientific Adviser.

Methods

The literature on pollinators and neonicotinoids published since our restatement was completed was reviewed and a first draft evidence summary produced by a subset of the authors. All authors reviewed and revised the document, and agreed on the categorizing of the different evidence components using the same scheme we adopted earlier, and which is explained in paragraph A2 of the restatement update (appendix A). The second draft was sent to a series of 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 from over 40 stakeholders (see acknowledgements). Though many groups were consulted, the project was conducted completely independent of any stakeholder and was funded by the Oxford Martin School (part of the University of Oxford).

Results

The update to the restatement 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 new evidence and evidence syntheses that have been published in the last 18 months (between February 2014 and August 2015) significantly advance our understanding of the effects of neonicotinoids on insect pollinators. Nevertheless, major gaps in our understanding remain, and different policy conclusions can be drawn depending on the weight one accords to important (but not definitive) science findings and the weightings given to the economic and other interests of different stakeholders. The natural science evidence base places constraints on policies that claim to be consistent with the science, but does not specify a single course of action. We also raise an issue here that arises from our original study but is not directly relevant to the evidence base on the effects of neonicotinoids on pollinators. In introducing the subject we wrote ‘Neonicotinoid insecticides are a highly effective tool to reduce crop yield losses due to insect pests’, and in the restatement itself listed a small number of papers in the scientific literature to support this statement [1]. It has been pointed out that some of these papers were funded by industry and that there are other studies that have recorded no benefits of neonicotinoid use (e.g. [3]). The efficacy of neonicotinoids is clearly an important issue, and we believe few would doubt that in some circumstances (combinations of crops, pests and locales) they are highly effective and in other circumstances they do not justify the costs of their purchase. We did not attempt to review this subject and should have been more careful to say we were not commenting on efficacy per se. Though a meta-analysis of efficacy would be very informative it would also be very difficult. Efficacy studies are largely conducted by industry, the sector that benefits most from the data, and are not the type of science usually funded by public organizations. Typically, the studies are not published in the peer-reviewed literature (though they are often made available to regulators) and some are kept confidential for commercial reasons. Efficacy trials are expensive and it seems unlikely that they will ever be publicly funded at scale. It is an interesting topic for debate whether industry would benefit in the long run from placing more of its data in the public domain as well as putting in place measures to increase public confidence in studies they fund themselves. The recent movement in the pharmaceutical sector to set up trial registries (see https://clinicaltrials.gov/ct2/home and https://www.clinicaltrialsregister.eu) provides a model for how the latter might be achieved.
  9 in total

1.  Seed coating with a neonicotinoid insecticide negatively affects wild bees.

Authors:  Maj Rundlöf; Georg K S Andersson; Riccardo Bommarco; Ingemar Fries; Veronica Hederström; Lina Herbertsson; Ove Jonsson; Björn K Klatt; Thorsten R Pedersen; Johanna Yourstone; Henrik G Smith
Journal:  Nature       Date:  2015-04-22       Impact factor: 49.962

2.  A field study examining the effects of exposure to neonicotinoid seed-treated corn on commercial bumble bee colonies.

Authors:  G Christopher Cutler; Cynthia D Scott-Dupree
Journal:  Ecotoxicology       Date:  2014-09-07       Impact factor: 2.823

3.  Evidence for pollinator cost and farming benefits of neonicotinoid seed coatings on oilseed rape.

Authors:  G E Budge; D Garthwaite; A Crowe; N D Boatman; K S Delaplane; M A Brown; H H Thygesen; S Pietravalle
Journal:  Sci Rep       Date:  2015-08-13       Impact factor: 4.379

4.  Chronic exposure to neonicotinoids increases neuronal vulnerability to mitochondrial dysfunction in the bumblebee (Bombus terrestris).

Authors:  Christopher Moffat; Joao Goncalves Pacheco; Sheila Sharp; Andrew J Samson; Karen A Bollan; Jeffrey Huang; Stephen T Buckland; Christopher N Connolly
Journal:  FASEB J       Date:  2015-01-29       Impact factor: 5.191

5.  Neonicotinoids impact bumblebee colony fitness in the field; a reanalysis of the UK's Food & Environment Research Agency 2012 experiment.

Authors:  Dave Goulson
Journal:  PeerJ       Date:  2015-03-24       Impact factor: 2.984

6.  Assessment of chronic sublethal effects of imidacloprid on honey bee colony health.

Authors:  Galen P Dively; Michael S Embrey; Alaa Kamel; David J Hawthorne; Jeffery S Pettis
Journal:  PLoS One       Date:  2015-03-18       Impact factor: 3.240

7.  A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success.

Authors:  G Christopher Cutler; Cynthia D Scott-Dupree; Maryam Sultan; Andrew D McFarlane; Larry Brewer
Journal:  PeerJ       Date:  2014-10-30       Impact factor: 2.984

Review 8.  A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators.

Authors:  H Charles J Godfray; Tjeerd Blacquière; Linda M Field; Rosemary S Hails; Gillian Petrokofsky; Simon G Potts; Nigel E Raine; Adam J Vanbergen; Angela R McLean
Journal:  Proc Biol Sci       Date:  2014-07-07       Impact factor: 5.349

9.  Combined pesticide exposure severely affects individual- and colony-level traits in bees.

Authors:  Richard J Gill; Oscar Ramos-Rodriguez; Nigel E Raine
Journal:  Nature       Date:  2012-10-21       Impact factor: 49.962

  9 in total
  49 in total

1.  Comparison of Pesticide Exposure in Honey Bees (Hymenoptera: Apidae) and Bumble Bees (Hymenoptera: Apidae): Implications for Risk Assessments.

Authors:  Angela E Gradish; Jozef van der Steen; Cynthia D Scott-Dupree; Ana R Cabrera; G Christopher Cutler; Dave Goulson; Olaf Klein; David M Lehmann; Johannes Lückmann; Bridget O'Neill; Nigel E Raine; Bibek Sharma; Helen Thompson
Journal:  Environ Entomol       Date:  2019-02-13       Impact factor: 2.377

Review 2.  Safeguarding pollinators and their values to human well-being.

Authors:  Simon G Potts; Vera Imperatriz-Fonseca; Hien T Ngo; Marcelo A Aizen; Jacobus C Biesmeijer; Thomas D Breeze; Lynn V Dicks; Lucas A Garibaldi; Rosemary Hill; Josef Settele; Adam J Vanbergen
Journal:  Nature       Date:  2016-11-28       Impact factor: 49.962

3.  Imidacloprid slows the development of preference for rewarding food sources in bumblebees (Bombus impatiens).

Authors:  Jordan D Phelps; Caroline G Strang; Malgorzata Gbylik-Sikorska; Tomasz Sniegocki; Andrzej Posyniak; David F Sherry
Journal:  Ecotoxicology       Date:  2017-12-22       Impact factor: 2.823

4.  The Adverse Outcome Pathway: A Multifaceted Framework Supporting 21st Century Toxicology.

Authors:  Gerald T Ankley; Stephen W Edwards
Journal:  Curr Opin Toxicol       Date:  2018-06-01

Review 5.  The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013.

Authors:  Thomas James Wood; Dave Goulson
Journal:  Environ Sci Pollut Res Int       Date:  2017-06-07       Impact factor: 4.223

6.  Neonicotinoid pesticides and nutritional stress synergistically reduce survival in honey bees.

Authors:  Simone Tosi; James C Nieh; Fabio Sgolastra; Riccardo Cabbri; Piotr Medrzycki
Journal:  Proc Biol Sci       Date:  2017-12-20       Impact factor: 5.349

Review 7.  Weight of evidence evaluation of a network of adverse outcome pathways linking activation of the nicotinic acetylcholine receptor in honey bees to colony death.

Authors:  Carlie A LaLone; Daniel L Villeneuve; Judy Wu-Smart; Rebecca Y Milsk; Keith Sappington; Kristina V Garber; Justin Housenger; Gerald T Ankley
Journal:  Sci Total Environ       Date:  2017-01-24       Impact factor: 7.963

8.  Imidacloprid alters ant sociobehavioral traits at environmentally relevant concentrations.

Authors:  James D Sappington
Journal:  Ecotoxicology       Date:  2018-09-05       Impact factor: 2.823

9.  Non-cultivated plants present a season-long route of pesticide exposure for honey bees.

Authors:  Elizabeth Y Long; Christian H Krupke
Journal:  Nat Commun       Date:  2016-05-31       Impact factor: 14.919

10.  A horizon scan of future threats and opportunities for pollinators and pollination.

Authors:  Mark J F Brown; Lynn V Dicks; Robert J Paxton; Katherine C R Baldock; Andrew B Barron; Marie-Pierre Chauzat; Breno M Freitas; Dave Goulson; Sarina Jepsen; Claire Kremen; Jilian Li; Peter Neumann; David E Pattemore; Simon G Potts; Oliver Schweiger; Colleen L Seymour; Jane C Stout
Journal:  PeerJ       Date:  2016-08-09       Impact factor: 2.984

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