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PESTICIDES AND BEE HEALTH | JANUARY 2019
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Greenpeace Research Laboratories Technical Report (Review)January 2019
PESTICIDES AND BEE HEALTH
An evaluation of the application of the 2013 European Food Safety Authority Bee Guidance document as a mechanism to protect bees from agricultural pesticides.
TAKE-HOME MESSAGES 3 1.0 INTRODUCTION 5
1.1 AN ASSESSMENT OF THE EUROPEAN FOOD SAFETY AUTHORITY BEE GUIDANCE DOCUMENT 5
1.2 MANY YEARS LATER, STILL NO CONSISTENT APPLICATION 8
1. 3 BEE DECLINE 9
1.4 KNOWLEDGE GAPS 9
2.0 PEER REVIEWED LITERATURE ON THE EIGHT PESTICIDES UNDER INVESTIGATION IN THIS REPORT: CLOTHIANIDIN, IMIDACLOPRID, THIAMETHOXAM, ACETAMIPRID, THIACLOPRID, SULFOXAFLOR, CYANTRANILIPROLE AND FLUPYRADIFURONE. 10
3.0 THE USE OF THE BEE GUIDANCE DOCUMENT IN PESTICIDE RISK ASSESSMENTS. 13
3.1 KEY POINTS MENTIONED IN THE EUROPEAN FOOD SAFETY AUTHORITY ASSESSMENTS 19
4.0 PESTICIDES APPROVED FOR USE: ACETAMIPRID, THIACLOPRID, SULFOXAFLOR, CYANTRANILIPROLE AND FLUPYRADIFURONE 21
5.0 MAJOR KNOWLEDGE GAPS FROM USE OF THE BEE GUIDANCE DOCUMENT AND THE EFSA REVIEW DOCUMENTS 22
REFERENCES 23
APPENDICES 26
CONTENTS
PESTICIDES AND BEE HEALTH. AN EVALUATION OF THE APPLICATION OF THE 2013 EUROPEAN FOOD
SAFETY AUTHORITY BEE GUIDANCE DOCUMENT AS A MECHANISM TO
PROTECT BEES FROM AGRICULTURAL PESTICIDES.
Kathryn A. Miller, Kirsten F. Thompson, Franziska Achterberg and David Santillo Greenpeace Research Laboratories Technical Report (Review) 01-2019
Suggested citation: Miller, K. A., Thompson, K. F., Achterberg, F. & Santillo, D. Pesticides and bee health. An
evaluation of the application of the 2013 European Food Safety Authority Bee Guidance document as a mechanism to protect bees from agricultural pesticides. Greenpeace Research Laboratories Technical Report (Review) 01-2019
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• Pesticide testing guidance on bees. The European Food Safety Authority’s Bee Guidance document (EFSA, 2013a) is the most comprehensive – though by no means perfect – testing regime to assess the potential risks to bees arising from the use of pesticides. It covers wild bee species (bumble bees and solitary bees) in addition to honey bees. It takes into account risks from chronic or repeat exposure to pesticides, and potential risks to larvae. It also considers various routes of exposure, including from spray deposits or dust particles, from contaminated pollen and nectar and from contaminated water (guttation fluid, surface water and puddles). The guidance indicates that it is not acceptable for a honey bee colony to shrink by more than 7% as a result of exposure to pesticides.
• Only three neonicotinoids fully tested in accordance with the guidance. The European Food Safety Authority (EFSA) used the Bee Guidance document in the assessment of four neonicotinoid insecticides – clothianidin, imidacloprid, thiamethoxam and acetamiprid (Appendix Table 1). However, only the assessments of clothianidin, imidacloprid and thiamethoxam covered impacts to honey bees, bumble bees and solitary bees. The assessment of acetamiprid was limited to honey bees. No updated risk assessment is available for thiacloprid, another neonicotinoid approved for use in the European Union (EU).
• A high risk to bees from some pesticides could not be excluded. The assessments of clothianidin, imidacloprid and thiamethoxam concluded that most uses of these pesticides
presented a high risk to bees, or that a high risk could not be excluded. As a result, the EU banned all outdoor uses of clothianidin, imidacloprid and thiamethoxam. In the case of acetamiprid, EFSA concluded that it posed a low risk to honey bees, although it judged the available data insufficient “to draw any firm conclusion on the risk to honey bees, particularly to exclude any potential chronic effect or effect on brood development”. The EU renewed the approval for acetamiprid until 2033, without any restrictions on use that would protect bees from exposure to the active ingredient
• Other pesticides were not tested in accordance with the Bee Guidance document. EFSA’s assessments of three other insecticides that were suspected of being harmful to bees (sulfoxaflor, cyantraniliprole and flupyradifurone) were not based on the 2013 Bee Guidance document but on previous, outdated guidance. None of the three aforementioned assessments covers any wild bee species. In the case of sulfoxaflor, EFSA concluded that a high risk to honey bees could not be excluded for open field uses. EFSA is currently undertaking an additional assessment on this insecticide. In the case of cyantraniliprole, experts considered that the risk to honey bees could be mitigated for some uses if certain conditions are respected. For other uses the risk assessments could not be finalised because there were data gaps. The risk to honey bees from exposure to flupyradifurone was considered low. The EU allowed use all three insecticides for a period of ten years, without any restrictions that would protect bees from exposure to the active ingredients.
TAKE-HOME MESSAGES
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• Chemical alternatives to banned neonicotinoids could be just as harmful to bee health. In recognition of the above-mentioned limitations, the risk assessments for acetamiprid, sulfoxaflor, flupyradifurone and cyantraniliprole do not provide reassurance that these pesticides pose a low risk to managed honey bees or wild bees. Moreover, further data have become available on some of the pesticides within peer-reviewed publications since the assessments were published. The newly published evidence should also be taken into consideration by EFSA in relation to the assessment of pesticides. An updated, state-of-the-art risk assessment of hould be performed to ensure that they cannot be used as alternatives to the banned neonicotinoids, causing potentially similar harm to bees.
• Peer-reviewed literature search. This report details the findings from a systematic search of peer-reviewed literature was performed in relation to the eight pesticides and different bee types (honey bee, bumble bee and solitary bee). The majority of the literature on all eight pesticides is biased toward research on honey bees (661 papers), with fewer papers on bumble bees (78 papers) and only 12 papers that mention solitary bees in the abstract. The literature search also found that between 1994 and 2018, most literature focused on clothianidin, imidacloprid and thiamethoxam (those that are now banned from outdoor use in the EU). Very few publications have so far assessed the risks to bee health from sulfoxaflor, flupyradifurone and cyantraniliprole, although at least some of those that are available indicate cause for concern.
• Sulfoxaflor. Subsequent to the publication of its review for sulfoxaflor, the EU requested additional data to help determine the risk to honey bees and other bees. EFSA’s initial conclusion was that “a low risk could not be demonstrated for honey bees and non-Apis (wild) bees”. In the meantime, a new peer-reviewed study has appeared in the journal Nature suggesting that bumble bees that are exposed to sulfoxaflor may suffer population-level impacts due to reduced reproductive success (Siviter et al., 2018). EFSA is expected to publish a new set of conclusions in March 2019, taking into account the new evidence.
• Knowledge gaps. The Bee Guidance document identifies a number of knowledge gaps: it does not mention other pollinators, beneficial insects or arthropods; the same stringent field tests are not required for metabolites (that is, breakdown products) because they are only intended for active ingredients (yet metabolites can be as toxic as the active compound); risk mitigation strategies are only useful if they are understood and interpreted correctly.
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The objective of this report is to provide insight into the current state of the implementation of the European Union (EU) Bee Guidance Document (EFSA, 2013). The report investigates the differences between the way the Bee Guidance document was applied in the EU assessments of a number of systemic insecticides, including those that have been banned for open field uses and others that are permitted for use in the EU.
The eight pesticides included in the analysis are five neonicotinoids – clothianidin, imidacloprid, thiamethoxam, acetamiprid and thiacloprid – and three other systemic pesticides – sulfoxaflor, cyantraniliprole and flupyradifurone. The classification of neonicotinoids is under discussion (Sparks & Nauen, 2015; EFSA, 2017; IRAC, 2018). A report by the Pesticide Action Network Europe suggests that both sulfoxaflor and flupyradifurone should be classed as neonicotinoids because both compounds bind to insect nicotinic acetylcholine receptors and their action is systemic (PAN, 2016). Giorio et al, 2017 suggest that sulfoxaflor and flupyradifurone are fourth-generation neonicotinoid compounds. Cyantraniliprole has been described as an “anthranilic diamide” (Selby et al., 2016) that could replace neonicotinoid seed treatments 1, 2.
1.1 AN ASSESSMENT OF THE EUROPEAN FOOD SAFETY AUTHORITY BEE GUIDANCE DOCUMENT Under EU law, pesticides can only be approved if their use has “no unacceptable effects on the environment”, including potential effects on “non-target species” as well as “biodiversity and the ecosystem” (Regulation (EC) No 1107/2009, Article 4).
In addition, pesticides can only be approved if their use does not lead to unacceptable effects on honey bees. It has to be “established following an appropriate risk assessment on the basis of Community or internationally agreed test guidelines” that their use will either “result in negligible exposure of honey bees” or that it has “has no unacceptable acute or chronic effects on colony survival and development, taking into account effects on honeybee larvae or honeybee behaviour” (Regulation (EC) No 1107/2009, ANNEX II, Point 3.8.3).
EU pesticides law requires that the risk assessment, which forms the basis for regulatory decisions, be “independent, objective and transparent” and carried out “in the light of current scientific and technical knowledge” (Regulation (EC) No 1107/2009, Articles 11 and 36).
In March 2011, the European Commission asked EFSA to review the existing scheme for the assessment of risks posed by pesticides to bees. It considered that the scheme was outdated in that it covered only the acute mortality of adult bees due to pesticide exposure, and did not cover risks from sub-lethal effects, from exposure to contaminated water and from seed treatment.
1 https://entomologytoday.org/2016/10/19/anthranilic-diamides-can-potentially-replace-neonicotinoid-seed-treatments-in-vegetable-crops/
2 https://www.npr.org/sections/thesalt/2016/08/31/491962115/minnesota-cracks-down-on-neonic-pesticides-promising-aid-to-bees
1.0 INTRODUCTION
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In response to the Commission’s request, EFSA published a Scientific Opinion (EFSA, 2012) that showed how the existing risk assessment guidance failed to capture all relevant aspects of bee risk assessment. It advised that the risk of long-term exposure (chronic toxicity) should be assessed, that different life stages (adult and larvae) should be considered and that the risk to bumble bees and solitary bees should be assessed separately, in addition to the risk to honey bees.
EXPOSURE IS RELATED TO BEE SPECIES AND CASTES WITHIN SPECIES.EFSA (2012) reviewed the science behind the development of a risk assessment of plant protection products on bees. A number of key points relating to exposure risk to all bee species were discussed. Some of the main points are highlighted below.
Different bees (species, castes within the hive and life stages) have different exposure opportunities. The Scientific Opinion document suggests that there is need for a separate risk assessment for bumble bees and solitary bees, in comparison to honey bees.
Exposure through oral intake is highest for bees that are active in winter, forager bees and larvae.
Nurse bees are exposed through pollen and nectar.
Larvae of all bee species may be exposed by contact to wax within the hive.
Foragers, drones, queens and swarms of all bee types may be exposed to droplets and vapour by contact and inhalation.
Worker bees, queens and larvae of bumble bees and adult females and larvae of solitary bees were considered to be the categories that are most exposed through oral uptake.
Larvae of solitary bees may be more exposed to residues in pollen than the larvae of honey bees because solitary bee larvae consume large mass provisions with unprocessed pollen.
Bumble bees and solitary bees may have greater exposure through contact with nesting material (soil or plants) compared to honey bees.
The scientific opinion noted that conventional regulatory tests that assess acute toxicity over short periods (48–96 hours) may not be accurate to assess the risks of long-term exposure. Specific chronic toxicity tests are recommended for each bee type.
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The EU also updated its data requirements for pesticide active substances and formulated products in line with the new Bee Guidance document (Commission Regulations (EU) No 283/2013, No 284/2013). Manufacturers are now required to also submit tests on chronic toxicity as well as a bee brood study. In addition, tests investigating sub-lethal effects, such as behavioural and reproductive effects, on bees and colonies “may be required”. The updated data requirements have been valid for application dossiers submitted since 1 January 2014, both for renewals of EU approvals and for new EU approvals.
EFSA used the 2013 Bee Guidance document to assess the additional data submitted by Bayer for imidacloprid and clothianidin (EFSA, 2016a, EFSA 2016b). EFSA has also used the Bee Guidance document for its wider review of the risks posed to bees from all three neonicotinoids, including Syngenta’s thiamethoxam, published in February 2018 (EFSA 2018a, EFSA 2018b, EFSA 2018c). Based on these assessments, the EU imposed a near-total ban on the three neonicotinoids in May 2018, permitting their use only in permanent greenhouses. For further information on the use of neonicotinoids in greenhouses please see a Greenpeace report published in 2017 (Thompson, 2017)
When the Commission asked EFSA to assess the risk to bees from the use of three neonicotinoid insecticides (imidacloprid, clothianidin, thiamethoxam) and fipronil, EFSA relied on the Scientific Opinion (EFSA, 2012) to perform the evaluation. EFSA could not use the existing guidance since it was asked to consider “the acute and chronic effects on colony survival and development, taking into account effects on bee larvae and bee behaviour, and the effects of sublethal doses on bee survival and behaviour” (EFSA 2013b). Based on the EFSA assessments, presented in January 2013, the EU imposed a number of restrictions on the use of these insecticides (Commission Implementing Regulations (EU) No 485/2013 and No 781/2013).
Since EFSA found that there were insufficient data to perform a full assessment in line with the Scientific Opinion, the EU required the manufacturers to submit, by end of 2014, additional data on a number of issues including “the risk to pollinators other than honey bees”, “the risk to honey bees foraging in nectar or pollen in succeeding crops”, “the acute and long term risk to colony survival and development and the risk to bee brood for honey bees from ingestion of contaminated nectar and pollen” (Commission Implementing Regulations (EU) No 485/2013 and No 781/2013).
In July 2013, EFSA published an updated risk assessment guidance (EFSA, 2013a) that takes into account the findings of its 2012 Scientific Opinion.
The 2013 EFSA Bee Guidance document (EFSA, 2013a) contains a risk assessment scheme for the chronic risk to adult honey bees and honey bee larvae as well as for the risk to bumble bees and solitary bees. It considers different routes of exposure to pesticides, including from spray deposits or dust particles, from the consumption of contaminated pollen and nectar and from the consumption of contaminated water (guttation fluid, surface water and puddles).
The Bee Guidance document also details what “no unacceptable effects” means (that is, the protection goal that the EU aims to achieve). It suggests that it is not acceptable for a honey bee colony to shrink by more than 7% as a result of exposure to pesticides at any time.
Despite some weaknesses, the Bee Guidance document represents the most comprehensive methodology for assessing the risks posed by pesticides to bees.
WHAT IS NEW IN THE UPDATED RISK ASSESSMENT SCHEME?
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Pesticide manufacturers have argued against the application of the 2013 EFSA Bee Guidance document. Syngenta (2018) claimed that “the Bee Risk Guidance document is so conservative and so far removed from the reality of agriculture that its application would see most, if not all agricultural chemicals banned”.
In a blog from Bayer Crop Science head of seed growth, Martin Gruss (Gruss, 2017) said that a consistent application of the Bee Guidance document “would result in a denial of registration for most pesticides, even those used in organic agriculture!”
Bayer (Bayer, 2018) also said that the Bee Guidance document should not have been used in the assessment of its products. In response to the EFSA reviews of February 2018, the company said: “Unfortunately, EFSA chose to base its assessment on an unworkable guidance doctument that makes it impossible to field a study that would not find risk, despite repeated requests by Member States for a review of this guidance. EFSA’s conclusions can therefore not be used as a measuring stick to justify further neonicotinoid restrictions.”
INDUSTRY POSITION
1.2 MANY YEARS LATER, STILL NO CONSISTENT APPLICATIONThe 2013 the European Commission proposed that the Bee Guidance document should come into force on 1 January 2015. However, the Bee Guidance document is still not consistently applied across all EU pesticide risk assessments. The reason for this is that national governments have not yet endorsed it. Many governments have refused to agree to a step-by-step introduction of its different parts. This is despite the fact that relevant Organisation for Economic Co-operation and Development (OECD) test protocols have been defined (for example, for chronic toxicity tests for honey bees, for acute toxicity tests for bumble bees), and many companies have already submitted relevant tests for their products.
At least one EU country, Belgium, has decided unilaterally to apply large parts of the Bee Guidance Document in the risk assessment of formulated products. In the EU, formulations are authorised at the national level, not at the EU level. Belgian authorities are saying that, “from a scientific point of view, it is not acceptable to ignore available robust toxicity data on vulnerable non-target species simply because there is no generally accepted risk assessment guideline” (FPS Health, Food Chain Safety and Environment, 2018).
In June 2018, the European Commission announced that it would “adopt an implementation plan for the EFSA Guidance Document on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees) in order to enhance the risk assessment of pesticides on pollinators” (EC, 2018). The indicated timeline was the end of 2018.
Since 2018, the European Commission services have proposed several draft implementation plans by which an increasingly smaller part of the Bee Guidance document would be applied. They have also suggested that EFSA should be mandated to review key elements of the Bee Guidance document. Under the Commission’s plan, even tests that are part of existing EU data requirements, and for which OECD test protocols exist, would not be considered in pesticide risk assessments. Pesticides that fail these tests could be approved in the EU even when it has not been shown that the risk may be acceptable under field conditions. In that sense, the Commission’s latest proposals amount to a plan for non-implementation of the Bee Guidance document, and a free pass for the approval of bee-harming pesticides in the EU.
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1. 3 BEE DECLINEBees are crucially important in maintaining healthy ecosystems and help to sustain biodiversity by providing essential pollination for a wide range of crops and wild plants. Failure of pollination can lead to crop failure and, subsequently, lead to problems with food security. Various statistics have been published to support the importance of pollinators, including that 75% of crops are pollinated by insects (Klein et al., 2003) and that 57 species (mainly bees and only two vertebrate species) are key pollinators for 107 global crops that are of direct human use (Klein et al., 2006).
Globally, it is estimated that there are in the region of 25,000 species of bee. The number of species of bees, and other pollinators, has declined over the past 50 years. It is thought that many bee species are in decline because of multiple stressors including land use change that has caused habitat loss, bee parasites and diseases, and pesticide use (which can be directly toxic to bees but can also kill the wildflowers on which they live). Data from wild bees indicate declines in North American species Bombus terricola and B. occidentalis; B. dahlbomii in South America; and B. distinguendus in the United Kingdom, among many others (Goulson et al., 2015).
An estimated 2,000 or so bee species live in Europe. For 1,048 species (55.6%) there is too little scientific information to evaluate their population status, according to the IUCN Red List of Threatened Species for European bees (Nieto et al., 2014).
Approximately 15% of bee species inhabiting Europe (at EU-27 level) are known to be either Threatened or Near-Threatened. According to Nieto et al., (2014), around 30% of all the species threatened (Critically Endangered, Endangered, or Vulnerable) within the geographic area of Europe are endemic.
Bumble bees are the best studied group of wild bees, with less than 10% of data-deficient species. Their status is considerably worse than for bees in general – more than 45% of bumble bee species have a declining population trend and almost 24% are facing extinction (Nieto et al., 2014).
Many EU countres have published national lists of threatened species based on IUCN Red List criteria. They show that more than 50% of wild bee species are threatened with extinction in the Netherlands (Reemer, 2018), and almost one third in Ireland (Fitzpatrick et al., 2006).
1.4 KNOWLEDGE GAPSThe EFSA Bee Guidance Document represents the most comprehensive methodology for assessing the risk posed by pesticides to bees. However, there are a number of significant knowledge gaps associated with assessing the risks to bees, particularly the population-level impacts on wild bees and the sub-lethal impacts of exposure. For further details, see Section 5.
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The EFSA pesticide risk assessments were based upon available peer-review (open literature) and unpublished industry studies at the time of submission of the manufacturers application dossier. The majority of these data consisted of unpublished studies. In the absence of access to unpublished studies, an assessment was made of the published literature for each pesticide and each bee type (honey bee, bumble bee and solitary bee). This serves to illustrate the relative amount of research that has been undertaken on each substance, especially for comparing those that have and have not been banned, and what information may be available since the time of publication for each review document.
In this report, a systematic search of the Web of Science Core Collection3 was used to gain an understanding of previous peer-reviewed publications on all eight pesticides4 in this report and the three bee types (honey bees, bumble bees and solitary bees) The search terms used were, “pesticide” AND either “honey bee”, “bumble bee”, “solitary bee”, “bee”. The search provides information on how many publications mentioned these terms in the title, abstract and keywords and, therefore, there may be overlap in the total number of publications when a publication refers to more than one term. Note that this search did not include analyses of the publications themselves or the context of how the search terms were described within them.
The search found 1,693 peer-reviewed publications dating from 1994 and to 2018, published up until the search date5. From the systematic search of the literature it is clear that the main body of peer-reviewed publications has focused on the three banned pesticides (clothianidin, imidacloprid and thiamethoxam) (Figure 1a).
3 http://apps.webofknowledge.com
4 Banned neonicotinoids, clothianidin, imidacloprid, thiamethoxam. Approved neonicotinoids, acetamiprid and thiacloprid. The three other approved pesticides, sulfoxaflor, cyantraniliprole and flupyradifurone.
5 Search date was January 5, 2019.
2.0 PEER REVIEWED LITERATURE ON THE EIGHT PESTICIDES UNDER INVESTIGATION IN THIS REPORT:
0
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Pesticide
Num
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Bumble beeHoney beeSolitary bee
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Pesticide
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a) Number of publications per pesticide b) Number of publications per bee type
banned
Clothia
nidin
Imida
clopri
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Thiameth
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Cyantr
anilip
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600ClothianidinImidaclopridThiamethoxamAcetamiprid
CyantraniliproleFlupyradifuroneSulfolxaflorThiacloprid
0
CLOTHIANIDIN, IMIDACLOPRID, THIAMETHOXAM, ACETAMIPRID, THIACLOPRID, SULFOXAFLOR, CYANTRANILIPROLE AND FLUPYRADIFURONE.
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Figure 2. Yearly trends in publications that mention the eight pesticides and three bee types in title, keywords and abstract according to a systematic search of peer-reviewed literature. a) yearly number of publications per bee type, and b) number of publications that mention “bee” and the eight pesticides. For details on the literature related to pesticides other than the three neonicotinoids whose uses have been restricted due to potentially unacceptable risks to bees, please refer to Appendix 2
a) Number of publications per bee type per year (1992–2018)
Bumble beeHoney beeSolitary bee
Bee type
Year
Num
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150
100
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2000 2010
b) Number of publications that mention bee per year (1992–2018) per pesticide
Pesticide
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Year
AcetamipridClothianidinCyantraniliproleFlupyradifuroneImidaclopridSulfoxaflorThiaclopridThiamethoxam
2000 2010
0
20
40
60
The largest number of peer-reviewed papers considering “bees” AND “pesticide” were for imidacloprid (385 papers) followed by thiamethoxam (204 papers), clothianidin (203 papers), thiacloprid (67 papers), acetamiprid (65 papers), sulfoxaflor (8 papers), flupyradifurone (6 papers), cyantraniliprole (4 papers). The majority of peer reviewed papers mentioned honey bees (661 papers) and fewer considered bumble bees (78 papers) or solitary bees (12 papers) (Fig. 1b and Fig. 2a). Much of the peer-reviewed research was published after 2009, with the greatest numbers of papers considering “bees” and the three banned pesticides, presumably due to the focus on funding for research (Fig. 2b).
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Although these findings must be viewed separately from our evaluation of the risk assessment documents themselves, they illustrate, nonetheless, that understanding of the environmental fates and effects of those additional five pesticides remains extremely limited. In turn this serves to highlight the dangers in continuing to authorize their use while publicly available, peer-reviewed data remain so completely insufficient to support a thorough, transparent assessment of their risks to bees. Despite those limitations, at least some of the studies that are available for those pesticides already indicate significant cause for concern, indicating that, against a background of very substantial gaps in data and research, the ‘benefit of the doubt’ cannot safely be conferred to their ongoing use. For further details of this outline overview of available peer-reviewed literature, see Appendix 2.
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3.0 THE USE OF THE BEE GUIDANCE DOCUMENT IN PESTICIDE RISK ASSESSMENTS.Analyses of the pesticide assessments in this report show that the Bee Guidance document is only referenced in the EFSA’s ‘Conclusion on the pesticides peer review’ for four pesticides: clothianidin, imidacloprid, thiamethoxam and acetamiprid. In the case of acetamiprid, there is little evidence to indicate how it was applied in practice (Appendix Table 1). There is currently no updated assessment document for thiacloprid. The current EU approval is based on an assessment report that dates back to 2003. The extent to which the protocols described in the Bee Guidance document were used to review each pesticide vary. The application of the Bee Guidance document was complicated by the fact that it was being prepared at the same time as some of the pesticide risk assessments were being prepared. In addition, the updated data requirements were not yet in force when the application dossiers were submitted. Appendix Table 1 indicates the number of times, and in what context, the Bee Guidance document was cited in the recent EFSA reports.
It is vital that acetamiprid, thiacloprid, sulfoxaflor, cyantraniliprole and flupyradifurone should be subject to thorough assessments for their risk to bees of all types, taking into consideration the available peer-reviewed literature, including those studies that have become available in the period since the initial risk assessments for these pesticides were carried out..
The section below (section 3.1) presents a bullet list of key points mentioned in the EFSA documents.
When reference is made to the Bee Guidance document in the pesticide assessments, the context is primarily related to the methodology adopted, rather than in the context of conclusions drawn. For example, the wording in the conclusion on pesticides peer review assessment for clothianidin (EFSA, 2018a) in relation to the tier-1 risk assessment 6states:
“The Tier-1 risk assessment was carried out using default exposure values in accordance
with EFSA (2013c)”
An analysis was carried out of the statements within the review documents that refer to risk of exposure to bees (honey bees, bumble bees and solitary bees) from nectar, pollen, dust drift, guttation fluid, surface water and any particular statements on toxicity studies and endpoints. This overview of the documents is summarised in Table 1.
6 Tier-1 risk assessment. The Bee Guidance document suggests taking a tiered approach to assessing risk of the active substance to bees. Tier-1 is a simple and cost-effective first level; higher tiers are more complex and take place under field conditions. The appendices in the Bee Guidance document (EFSA, 2013a) give more detail on the laboratory and field studies in the tiered assessment scheme.
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An overview of the latest review documents found that those that included in-depth analyses of the scientific evidence relating to clothianidin, imidacloprid and thiamethoxam suggest a high risk to bees through several exposure routes, with the exception of thiamethoxam and certain routes of exposure (nectar, pollen and dust drift). For imidacloprid the review document stated that there was a low risk for honey bees through exposure from surface water. The risks were identified using the protocols outlined in the Bee Guidance document (Appendix Table 1).
The five pesticides whose EU approval has not been restricted contrast to the three neonicotinoids that have been banned for open field uses in that no full assessments have been made to evaluate the impact to bees of different routes of exposure or toxicity. Only the three updated pesticide risk assessments (for clothianidin in EFSA, 2018a; for imidacloprid in EFSA, 2018b; and for thiamethoxam in EFSA 2018b) followed the methodologies in the Bee Guidance document.
For the EFSA conclusion relating to acetamiprid (EFSA, 2016), reference is made to the Bee Guidance document (EFSA, 2013a) having been used in the ecotoxicology risk assessment, though no specific indications as to how it was applied can be found in the accompanying annex. For the conclusions relating to both cyantraniliprole (EFSA, 2014a) and flupyradifurone (EFSA, 2015), there are no mentions of the Bee Guidance document within the text and the document is not within the reference list. Please see Appendix Table 1.
For the conclusion relating to sulfoxaflor (EFSA, 2014b), the Bee Guidance document was not used. However,, additional confirmatory data (further studies) were requested to specifically investigate (see Appendix table 1):
A. the risk to honey bees from the different routes of exposure, in particular nectar, pollen, guttation fluid and dust;
B. risk to honey bees foraging in nectar or pollen in succeeding crops and flowering weeds;
C. the risk to pollinators other than honey bees;
D. the risk to bee brood.
According to the request, these data were requested for submission by August 18, 2017.
The additional investigations resulted in an Addendum to the original sulfoxaflor risk assessment document (i.e. the Draft Assessment Report) that describes and evaluates the newly available laboratory data and higher tier studies. The tier-1 assessment remained unchanged compared to the previous conclusion of the peer review document. However, the higher tier studies for sulfoxaflor included the latest knowledge. According to EFSA (2018d), there were divergent views expressed by Member States during the commenting phase of the review of sulfoxaflor, particularly in relation to:
“....the interpretation and the use of the available higher tier studies and as regards the consideration of risk mitigation measures for the use of sulfoxaflor.”
EFSA (2018d) states that:
Based on the data assessed, a low risk could not be demonstrated for honeybees and non-Apis bees as a result of the current assessments (points a –d).
Field-based studies on bumble bees from chronic exposure consistent with post-spray levels of sulfoxaflor during early growth phase suggest that there are significant sub-lethal population-level effects to this species (Siviter et al., 2018). Colonies exposed to sulfoxaflor produced fewer reproductive offspring. The study stated that direct and indirect effects on these bumblebees may have cumulative effects on colonies and the authors urged caution in using this pesticide in field conditions.
The Commission asked EFSA to consider this study in its upcoming conclusions on the potential risks posed to bees by sulfoxaflor.
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Route of exposure or toxicity
Imidacloprid
Application as a seed treatment or as a granule, apart from potato tubers, which are sprayed.
Thiamethoxam
Application as a seed treatment only.
Clothianidin
Application as a seed dressing or as a granule
Nectar Seed treatment
H - for honey and bumble (dietary route; acute, chronic, larvae). Low risk not demonstrated for solitary (p23).
Granules
H – for honey and bumble (dietary route of exposure; acute, chronic, larvae). Low risk not demonstrated for solitary (p38).
Succeeding crop scenario
H - to honey bees and solitary bees (using surrogate data) at Tier-1 and Tier-2. (No bumble bee data).
L - to honey bees; H - to bumble bees (no solitary bee data) at Tier-3. (p42)
Seed treatment
H - for honey and bumble (oral exposure; acute, larvae. No data available for chronic). L- not demonstrated for solitary (p21).
Seed treatment
H - for honey and bumble bees. L - for solitary bees not shown in the screening tests acute, chronic, larva). (p24).
Granules
H - for honey and bumble bees for certain crops (Maize, Potatoes, Sorghum, Sweet maize) (acute, chronic, honey bee larvae).
L - not demonstrated for solitary bees during screening. (p67).
Pollen Seed treatment
H - for honey and bumble (dietary route; acute, chronic, larvae). L - not demonstrated for solitary (p23).
Granules
H – for honey and bumble (dietary route of exposure; acute, chronic, larvae). L - not demonstrated for solitary (p38).
Seed treatment
H - for honey and bumble (oral exposure; acute, larvae. No data available for chronic). L- not demonstrated for solitary (p21).
Seed treatment
H - for honey and bumble bees. L - for solitary bees not shown in the screening tests (acute, chronic, larva). (p24).
Granules
H - for honey and bumble bees for certain crops (Maize, Potatoes, Sorghum, Sweet maize) (acute, chronic, honeybee larvae).
L - not demonstrated for solitary bees during screening. (p67).
Table 1: Findings from the tier-1 stage (and higher stages as indicated) of the risk assessments to evaluate risk to honey bees, bumble bees and solitary bees from the different application methods of eight pesticides based on the EFSA review documents. H denotes high risk, L denotes low risk as concluded by EFSA. H–L denotes high risk for some applications / routes of exposure / bee types, but low risk for others. The table contents consider outdoor application only (not greenhouse use).
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Route of exposure or toxicity
Imidacloprid
Application as a seed treatment or as a granule, apart from potato tubers, which are sprayed.
Thiamethoxam
Application as a seed treatment only.
Clothianidin
Application as a seed dressing or as a granule
Dust drift Seed treatment
H - L for honey and bumble bees; risk depends on the crop (crops not listed here) and whether a deflector was used; (contact and exposure routes; acute, chronic, larvae). L - to all bees from spray application to potato crop. L- not demonstrated for solitary (p33).
Granules
H – for honey and bumble (contact & dietary routes; acute, chronic, larvae). L- not demonstrated for solitary (p39).
Seed treatment
H – L for h oney and bumble bees. Risk depends on the crop. L for all three bee types for use on sugar beet. Contact and dietary routes. But data deficient for chronic dietary exposure. L- not demonstrated for solitary bees (p45).
Seed treatment Contact exposure
H -for contact route of exposure to honey and bumble bees for certain crops alfalfa, carrot, winter cereals, spring cereals, chicory, clover, maize, mustard, sunflower)
L–H for contact route of exposure honey bees and bumble bees for certain crops (winter rape, spring rape, sugar beet, fodder beet, poppy).
L- not demonstrated for contact exposure for solitary bees (p59).
Oral exposure
H -for oral route of exposure to honey and bumble bees for certain crops (Alfalfa, carrot, winter cereals, spring cereals, chicory, clover, maize, mustard, sunflower, winter rape, spring rape, poppy)
L–H for oral route of exposure honey bees and bumble bees for certain crops (sugar beet, fodder beet).
L- for oral route of exposure not demonstrated for solitary bees (p59).
Granules
H - honey and bumble bees for contact and oral exposure to certain crops (maize, potatoes, sorghum, sweet maize) (acute, chronic and honey bee larvae).
L - to solitary bees not demonstrated. (p69).
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Route of exposure or toxicity
Imidacloprid
Application as a seed treatment or as a granule, apart from potato tubers, which are sprayed.
Thiamethoxam
Application as a seed treatment only.
Clothianidin
Application as a seed dressing or as a granule
Dust drift Seed treatment
H - L for honey and bumble bees; risk depends on the crop (crops not listed here) and whether a deflector was used; (contact and exposure routes; acute, chronic, larvae). L - to all bees from spray application to potato crop. L- not demonstrated for solitary (p33).
Granules
H – for honey and bumble (contact & dietary routes; acute, chronic, larvae). L- not demonstrated for solitary (p39).
Seed treatment
H – L for honey and bumble bees. Risk depends on the crop. L for all three bee types for use on sugar beet. Contact and dietary routes. But data deficient for chronic dietary exposure. L- not demonstrated for solitary bees (p45).
Seed treatment
Contact exposure
H -for contact route of exposure to honey and bumble bees for certain crops alfalfa, carrot, winter cereals, spring cereals, chicory, clover, maize, mustard, sunflower)
L–H for contact route of exposure honey bees and bumble bees for certain crops (winter rape, spring rape, sugar beet, fodder beet, poppy).
L- not demonstrated for contact exposure for solitary bees (p59).
Oral exposure
H -for oral route of exposure to honey and bumble bees for certain crops (Alfalfa, carrot, winter cereals, spring cereals, chicory, clover, maize, mustard, sunflower, winter rape, spring rape, poppy)
L–H for oral route of exposure honey bees and bumble bees for certain crops (sugar beet, fodder beet).
L- for oral route of exposure not demonstrated for solitary bees (p59).
Granules
H - honey and bumble bees for contact and oral exposure to certain crops (maize, potatoes, sorghum, sweet maize) (acute, chronic and honey bee larvae).
L - to solitary bees not demonstrated. (p69).
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Route of exposure or toxicity
Imidacloprid
Application as a seed treatment or as a granule, apart from potato tubers, which are sprayed.
Thiamethoxam
Application as a seed treatment only.
Clothianidin
Application as a seed dressing or as a granule
Guttation Seed treatment
No risk assessment was carried out (p36).
Granules
Risk not stated.
Seed treatment
L - honey bees. Data deficient for other bees.
No risk assessment carried out.
Seed treatment
No risk assessment from exposure to contaminated guttation fluids was carried out at Tier-1.
H - to honey bees at Tier-2 level. Data deficient for other bee types.
Granules
No Tier-1, Tier-2, or Tier-3 risk assessments of exposure to guttation fluids were carried. L risk to honey bees (no other bees mentioned) was demonstrated. Data gaps acknowledged out (p70).
Puddles Seed treatment
L - to honey bees (p37) (data gaps for other species).
Granules
L - to honey bees (p40) (data gaps for other species)
Seed treatment
No assessment carried out (because “always negligible when seeds are drilled below the soil surface”) (p.49).
Seed treatment
Risk was considered negligible to for honey bees (no mention of other bees) and so no assessment was carried out.
Granules
No assessment carried out. Surface runoff was considered negligible.
Surface water
Seed treatment
L–honey bees (p37) (data gaps for other species).
Granules
L - to honey bees (p40) (data gaps for other species)
Seed treatment
Risk for honey bees from exposure to surface water could not be performed.
Seed treatment
Risk for honey bees from exposure to surface water not assessed. No mention of other bees.
Granules
Risk for honey bees from exposure to surface water not assessed. No mention of other bees.
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3.1 KEY POINTS MENTIONED IN THE EUROPEAN FOOD SAFETY AUTHORITY ASSESSMENTS
For more excerpts from the EFSA documents, see Appendix 1.
The European Food Safety Authority has published updated risk assessments in relation to the effect on bees for three neonicotinoids: clothianidin (EFSA, 2018a), imidacloprid (2018b) and thiamethoxam (2018c). Some key points from the three updated risk assessments of neonicotinoids in the three ‘Conclusion on pesticide peer review documents’ are bulleted below:
Imidacloprid
• Exposure to imidacloprid from pesticide residues from dust drift was found to pose a high risk for all bee groups (that is, honey bees, bumble bees and solitary bees).
• With regards to tier-1 risk assessments to assess exposure to the active compound, there were no toxicity data for bumble bees and solitary bees so the data were extrapolated from honey bee studies.
• In accordance with the EFSA Bee Guidance document (EFSA, 2013a), when data are missing, surrogate endpoints for different bee species can can be calculated using toxicity data for honey bees.
Thiamethoxam
• Dust drift was found to pose a low risk to bees if used in indoor greenhouses but a high risk for all other uses.
• No agreed methodology is available on how to use or interpret data to estimate exposure to field margin vegetation or adjacent crops when measured at the individual trial sites.
• There are data deficiencies when trying to assess the impact of acute versus chronic exposure. For example, with regards to studies involving honey bees there were five reliable acute contact endpoints, three reliable acute oral endpoints but there were no reliable data available to derive a chronic lethal dietary dose. For bumble bees, there was only one reliable acute oral toxicity study and one acute contact toxicity study. There were no reliable toxicity data available for solitary bees.
• Several routes of exposures are not covered by the risk assessment scheme, for example insect honeydew and exposure through the soil.
Clothianidin
• The report found a low risk to honey bees when the active substance was used on sugar and fodder beet, but a high risk from other outdoor uses. The report also noted that there was a high risk to honey bees and bumble bees, but more data are needed to fully assess the effect on solitary bees.
In addition to the three pesticides with EU-wide restrictions on use, there are other pesticides that are licenced for use in the EU that are of concern because of potential toxicity to bees. These include:
Acetamiprid (not banned in EU apart from in France)
• Several data gaps were identified in relation to the ecotoxicology of the active compound and the report suggests that further information would be needed to address the risk assessment for birds, mammals, aquatic organisms, bees and non-target arthropods.
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• Based on tier-1 studies, a “low risk to honeybees (acute, chronic and larvae) and to bumble bees (acute) was concluded for all scenarios for the representative uses on pome fruit (post-flowering application) and potatoes”.
• However, EFSA concluded that available higher tier studies were insufficient ”to draw any firm conclusion on the risk to honeybees, particularly to exclude any potential chronic effect or effect on brood development”.
• EFSA also concluded that: “No data were available to perform a complete risk assessment for bumble bees or solitary bees. Information was available in the RAR from public literature data indicating that bumble bees may be more sensitive than honeybees.”
• EFSA noted data gaps on “sublethal effects on bees (i.e. HPG)” and on “the risk to honeybees via exposure to residue in guttation fluids”.
Cyantraniliprole
• The conclusion of the peer review (EFSA, 2014a) does not refer to the Bee Guidance document (EFSA, 2013).
• The crop on which the pesticide is used can have an impact on its toxicity to bees. For example, it was found in the tier-1 risk assessment that there was a high risk for the active substance for all the representative uses, but a there was a low risk for honey bees when the formulated product was used on potatoes and mandarins. The risk to honey bees for use on lettuce was judged to be low because lettuce is not attractive to honey bees (it is not a flowering crop).
• In some cases, there were not sufficient data to be able to conclude a high or a low risk to bees. For example, when using the active compound as a spray application on apples, pears, nectarines, peaches or apricots, plums, citrus, mandarins, olives, grapes, a high risk could not be excluded with the available data.
• No risk assessment was performed for wild bees.
• Ecotoxicology data gaps were identified to further
address the risk to mammals, bees and non-target arthropods.
Flupyradifurone
• The conclusion of the peer review (EFSA, 2015) does not refer to the Bee Guidance document (EFSA, 2013a).
• The risk to honey bees was considered to be low for the representative uses of flupyradifurone.
• No risk assessment was performed for wild bees.
• No data gaps were identified.
Sulfoxaflor
• The conclusion of the peer review (EFSA, 2014b) does not refer to the Bee Guidance document (EFSA, 2013).
• The rapporteur Member State (Ireland) did not provide a transparent evaluation.
• The myriad uses for this pesticide include tomatoes, aubergine, cucumber, water melon, winter cereals and cotton.
• Tier-1 risk assessments found a high risk to honey bees.
• Because of data gaps, more studies are needed to address the risk to honey bees for the field uses.
• With the available assessments a high risk to bees was not excluded for field uses.
• No risk assessment was performed for wild bees.
Thiacloprid
• Recent assessment not available yet.
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4.0 PESTICIDES APPROVED FOR USE:
The overview of the five pesticides that are still approved for use in the EU (with the exception of France) uses both the EFSA (European Food Safety Authority) review documents and the Pesticide Properties Database of the University of Hertfordshire8 (PPD) (Appendix 3). For thiacloprid, only the PPD was reviewed in the absence of an EFSA review document. To assess the risks in using these substances a list of mitigation measures, as suggested in the EFSA review documents, are noted in Appendix 3.
The mitigation measures put forward by EFSA within the review documents are claimed to reduce the risks to bees of the relevant pesticide. In practice, many of these measures are focused on protection of aquatic habitats (and are not focused on bees or non-target arthropods). While some of the mitigation measures do focus on non-target arthropods, they could only ever reduce this risk, but not eliminate the risk to bees. For completeness, a compilation of the mitigation measures suggested by EFSA are included in Appendix Table 3. For example, for sulfoxaflor a high risk to bees was concluded by the experts at the EFSA meeting to discuss toxicological risks. Some risk mitigation steps were proposed at the review meeting, but ‘the experts at the meeting did not consider that the data and the assessments that were available were sufficient to demonstrate a low risk to bees for the field uses even with the proposed measures’. A data gap was agreed to further address the risk to bees in field situations. Risks were also highlighted for pollinators in situations in which sulfoxaflor is used in greenhouses and it was suggested that colonies be covered or removed until residues on leaves and surfaces within the greenhouse have dried.
8 https://sitem.herts.ac.uk/aeru/ppdb/en/atoz.htm#A
ACETAMIPRID, THIACLOPRID, SULFOXAFLOR,
CYANTRANILIPROLE AND FLUPYRADIFURONE
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5.0 MAJOR KNOWLEDGE GAPS FROM USE OF THE BEE GUIDANCE DOCUMENTAND THE EFSA REVIEW DOCUMENTS
This chapter notes a number of key knowledge gaps within both the Bee Guidance document and the review documents. Any knowledge gaps that are mentioned in the Bee Guidance document are highlighted and to address uncertainties, the authors of the Bee Guidance document have attempted to give a qualitative indication of the level of conservatism for the risk assessment scheme9.
The following knowledge gaps also relate to the reading of the Bee Guidance document and EFSA reviews:• Conservatism. While some conservatism is built into the Bee Guidance document document, there
are certain areas where key knowledge gaps could have significant impact on pollinators and other species. For example, the assessment is field-based and not landscape-based and, therefore, there is no assessment of realistic scenarios where multiple plant protection products are used. Assessments also assume healthy bees and there are no assessments of sub-lethal effects.
• Sub-lethal doses. It is not possible to determine the risk of sub-lethal doses for reasons that include the lack of tier-1 studies that are relevant at the colony level (therefore representing a knowledge gap).
• Guttation water. More studies are needed to assess the extent to which crops produce guttation water and the extent to which bees consume/take back to hive, and whether it is used in brood food. Residues of pesticide in guttation droplets varied and depended on the crop type. More research is also needed to assess the best distance from the field to provide a permanent water supply for bees. Bees prefer permanent water supplies to guttation water and an assessment of suitable mitigation options for the replacement of guttation water is necessary.
• Honeydew. Risk assessment for exposure from honeydew was not included in the Bee Guidance document because there is a lack of information on the issue.
• Metabolites. The same stringent field tests are not required for metabolites as they are for active ingredients. Metabolites can be just as toxic as the active compound.
• Mitigation methods. There are uncertainties relating to some proposed mitigation methods. Risk mitigation strategies are only useful if they are read and interpreted correctly by the relevant agricultural worker.
• Toxicology of mixtures. A chemical-by-chemical approach to risk assessment is too simplistic because often mixtures contain several active ingredients.
• Multiple, simultaneous exposure routes. More studies are needed on multiple exposures by nurse bees, and also exposure through water consumption and exposure by inhalation of vapour from fields/spraying crops.
• Dust. Application of the Bee Guidance could lead to underestimation of the exposure of bees to contaminated dust during seed sowing. The Bee Guidance document assumes that the wind blows from one direction only, and applies a dilution factor of 3 when estimating exposure concentrations for bees flying through the dust cloud,, which could in some circumstances lead to an underestimation of the true exposure.
9 See Table 1 on page 9, EFSA (European Food Safety Authority), 2013a.
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Siviter, H., Brown, M., Leadbeater, E. Sulfoxaflor exposure reduces bumblebee reproductive success Nature 561, 109–112 (2018). doi: 10.1038/s41586-018-0430-6
Sparks, T.C. & Nauen, R. IRAC: Mode of action classification and insecticide resistance management. Pesticide Biochemistry and Physiology 121, 122–128 (2015). doi: 10.1016/j.pestbp.2014.11.014
Syngenta, 2018. Press release, April 27, 2018: ‘Syngenta: Neonicotinoid Decision Takes European Farming in the Wrong Direction’. Syngenta, Basel, Switzerland. Available at https://www.businesswire.com/news/home/20180427005296/en/Syngenta-Neonicotinoid-Decision-Takes-European-Farming-Wrong [Accessed January 16, 2019.]
Thompson, K. Will the use of neonicotinoids in greenhouses continue to present a risk for bees and other organisms? Greenpeace Research Laboratories Technical Report (Review) 09-2017: 14 pp (2017).
GRL-TR(R)-01-2019
26
PESTICIDES AND BEE HEALTH | JANUARY 2019
Subs
tanc
eRe
fere
nce
Wha
t top
ic d
oes
the
Bee
Gui
danc
e
rela
te to
.O
utco
mes
and
oth
er c
omm
ents
Imid
aclo
prid
Pee
r re
view
of t
he
pes
ticid
e ris
k as
sess
men
t fo
r b
ees
for
the
activ
e su
bst
ance
imid
aclo
prid
co
nsid
erin
g th
e us
es
as s
eed
tre
atm
ents
and
gr
anul
es (E
FSA
, 201
8b).
The
Sum
mar
y sp
ecifi
es t
hat:
“R
isk
asse
ssm
ents
wer
e p
erfo
rmed
for
hone
ybee
s, b
umb
leb
ees
and
sol
itary
b
ees
acco
rdin
g to
the
EFS
A g
uid
ance
d
ocum
ent
on t
he r
isk
asse
ssm
ent
of
pla
nt p
rote
ctio
n p
rod
ucts
on
bee
s.”
Say
s in
the
Sum
mar
y th
at: “
For
exp
osur
e vi
a re
sid
ues
in p
olle
n an
d
nect
ar…
whe
n al
l the
bee
gro
ups
(hon
eyb
ees,
bum
ble
bee
s an
d s
olita
ry
bee
s) a
re c
onsi
der
ed, a
hig
h ris
k w
as
conc
lud
ed o
r it
was
con
clud
ed t
hat
a lo
w r
isk
was
not
dem
onst
rate
d fo
r al
l the
us
es a
sses
sed
.”
Exp
osur
e vi
a re
sid
ues
from
dus
t d
rift:
hi
gh r
isk
for
all b
ee g
roup
s.
Exp
osur
e vi
a w
ater
con
sum
ptio
n: lo
w
risk
from
gut
tatio
n w
ater
or
pud
dle
s,
high
ris
k fo
r so
me
othe
r us
es.
Rea
din
g th
e P
eer
Rev
iew
Ass
essm
ent
doc
umen
t, t
he E
FSA
Bee
Gui
dan
ce
doc
umen
t (re
ferr
ed t
o as
EFS
A
2013
c) w
as r
efer
red
to
and
cite
d
thro
ugho
ut. B
ut a
mor
e th
orou
gh
read
ing
and
rea
din
g th
e m
etho
ds
and
ap
pen
dic
es w
ill b
e ne
cess
ary
to m
ore
fully
und
erst
and
the
ris
k as
sess
men
t p
roce
sses
and
dat
a us
ed.
This
doc
umen
t re
fers
to
the
Bee
Gui
dan
ce d
ocum
ent
62 t
imes
-
coun
ted
usi
ng a
‘sea
rch
and
find
’ met
hod
- p
rob
ably
incl
udes
the
re
fere
nce.
Sec
tion
3.2.
In r
elat
ion
to T
ier-
1 ris
k as
sess
men
ts t
o as
sess
ex
pos
ure
to t
he a
ctiv
e co
mp
ound
: In
the
abse
nce
of t
oxic
ity d
ata
for
bum
ble
bee
s an
d s
olita
ry b
ees,
dat
a w
ere
extr
apol
ated
from
ho
neyb
ees
assu
min
g th
e en
dp
oint
is a
fact
or o
f 10
low
er.
Tier
-1 r
isk
asse
ssm
ent
carr
ied
out
in a
ccor
dan
ce w
ith t
he B
ee
Gui
dan
ce d
ocum
ent.
Sec
tion
3.3
says
tha
t “n
o st
epw
ise
app
roac
h is
offe
red
for
high
er
tier
risk
asse
ssm
ent”
.
Sec
tion
3.3.
1.1.
Res
idue
s in
nec
tar
and
pol
len.
The
Bee
Gui
dan
ce
doc
umen
t w
as d
iscu
ssed
in r
elat
ion
to A
pp
end
ix R
, ab
out
exp
osur
e in
the
fiel
d.
3.3.
1.2
Use
of t
he B
ee G
uid
ance
doc
umen
t fo
r va
lues
to
use
in
shor
tcut
val
ues.
3.3.
2 us
ed t
he B
ee G
uid
ance
doc
umen
t r
e d
ust
drif
t, w
eed
s (3
.3.2
), w
ater
sou
rces
(3.3
.4)
3.3.
4, p
15. S
ays
that
: “fo
llow
ing
EFS
A (2
013c
), a
refin
emen
t of
th
e ex
pos
ure
can
only
be
per
form
ed if
at
leas
t fiv
e fie
ld s
tud
ies
are
avai
lab
le fo
r th
e sa
me
crop
” th
en g
oes
on t
o sa
y “R
esid
ues
from
five
fiel
d s
tud
ies
wer
e no
t av
aila
ble
for
any
of t
he c
rop
s b
eing
as
sess
ed h
ere.
” A
nd t
hen
that
“N
o ex
pos
ure
refin
emen
t w
as
nece
ssar
y fo
r as
sess
ing
resi
due
s in
pud
dle
s as
usi
ng t
he T
ier-
1 ex
pos
ure
asse
ssm
ent
ind
icat
ed lo
w r
isk”
AP
PE
ND
ICE
SA
ppen
dix
Tab
le 1.
A su
mm
ary
of th
e E
FSA
ass
essm
ents
rela
ting
to e
ight
pla
nt p
rote
ctio
n pr
oduc
ts li
cens
ed fo
r use
in th
e E
U.
Ban
ned
from
out
door
use
in E
U fr
om D
ec 2
018
(apa
rt fr
om F
ranc
e, w
hich
ban
ned
all fi
ve n
eoni
cs fr
om S
ept 1
, 201
8)
PESTICIDES AND BEE HEALTH | JANUARY 2019
GRL-TR(R)-01-2019
27
Subs
tanc
eRe
fere
nce
Wha
t top
ic d
oes
the
Bee
Gui
danc
e
rela
te to
.O
utco
mes
and
oth
er c
omm
ents
Imid
aclo
prid
Sec
tion
3.4,
p15
. Dis
cuss
es t
he B
ee G
uid
ance
doc
umen
t in
re
latio
n to
refi
nem
ent
with
hig
her
tier
exp
erim
ents
.
Pag
e 16
, re
leve
ls o
f exp
osur
e: “
The
dai
ly c
onsu
mp
tion
valu
es,
for
pol
len
and
nec
tar,
for
each
bee
cas
te w
ere
take
n fr
om E
FSA
(2
013c
).”
Pag
e 20
: “In
acc
ord
ance
with
EFS
A (E
FSA
, 201
3c),
whe
re d
ata
are
mis
sing
, sur
roga
te e
ndp
oint
s ca
n b
e ca
lcul
ated
usi
ng t
oxic
ity d
ata
for
hone
ybee
s d
ivid
ed b
y 10
..” S
o th
ey u
sed
sur
roga
te d
ata
in t
he
risk
asse
ssm
ent.
P23
. Th
e B
ee G
uid
ance
doc
umen
t w
as u
sed
for
exp
osur
e as
sess
men
t d
ata
in T
ier-
1
P25
. “Ti
er-2
ris
k as
sess
men
ts p
erfo
rmed
by
usin
g th
e E
FSA’
s B
eeTo
ol (v
.3.)
(Ap
pen
dix
Y o
f EFS
A (2
013c
)) fo
r ho
neyb
ees.
”
Thia
met
hoxa
m
Pee
r re
view
of t
he p
estic
ide
risk
asse
ssm
ent
for
bee
s fo
r th
e ac
tive
sub
stan
ce
thia
met
hoxa
m c
onsi
der
ing
the
uses
as
seed
tre
atm
ents
an
d g
ranu
les
(EFS
A, 2
018c
).
Info
from
the
Sum
mar
y: P
olle
n an
d
nect
ar: l
ow r
isk
of e
xpos
ure
in s
ome
case
s b
ut a
hig
h ris
k in
oth
ers.
Whe
n Ti
er-3
ass
essm
ent
was
car
ried
out
, the
d
ata
did
not
dem
onst
rate
low
ris
k b
ut
neith
er d
id it
ind
icat
e a
clea
r hi
gh r
isk.
Dus
t d
rift:
low
ris
k fr
om in
doo
r gr
eenh
ouse
s; h
igh
risk
for
othe
r us
es.
Wat
er c
onsu
mp
tion:
low
ris
k to
hon
ey
bee
s fr
om p
udd
les
and
sug
ar b
eet
gutt
atio
n flu
id. H
igh
risk
to h
oney
bee
s fr
om o
ther
pla
nts’
gut
tatio
n flu
id.
This
ass
essm
ent
follo
ws
the
reco
mm
end
atio
ns in
the
Bee
G
uid
ance
doc
umen
t (m
entio
ned
in t
he d
ocum
ent
45 t
imes
).
Say
s: “
The
bas
is o
f the
ris
k as
sess
men
t ac
cord
ing
to E
FSA
(2
013c
) is
to e
nsur
e th
at t
he s
pec
ific
pro
tect
ion
goal
s (S
PG
) for
ho
neyb
ees,
bum
ble
bee
s an
d s
olita
ry b
ees
are
met
.”
Ther
e ar
e nu
mer
ous
refe
renc
es t
o th
e B
ee G
uid
ance
.
Ap
pen
dix
C is
a T
ier-
1 as
sess
men
t b
ased
on
the
Bee
Gui
dan
ce
doc
umen
t.
Sec
tion
3.2
Tier
-1 a
sses
smen
t ca
rrie
d o
ut a
ccor
din
g to
the
Bee
G
uid
ance
.
3.2.
1: “
The
end
poi
nt w
as c
onsi
der
ed a
s re
leva
nt fo
r a
risk
asse
ssm
ent
acco
rdin
g to
EFS
A (2
013c
)”
Res
idue
s in
pol
len
and
nec
tar:
stu
die
s us
ed “
pro
toco
l pro
pos
ed in
A
pp
end
ix G
of E
FSA
(201
3c).”
GRL-TR(R)-01-2019
28
PESTICIDES AND BEE HEALTH | JANUARY 2019
Subs
tanc
eRe
fere
nce
Wha
t top
ic d
oes
the
Bee
Gui
danc
e
rela
te to
.O
utco
mes
and
oth
er c
omm
ents
Thia
met
hoxa
m
3.3.
2: D
ust
drif
t: “
Acc
ord
ing
to t
he E
FSA
(201
3c),
exp
osur
e to
dus
t d
rift
in t
he fi
eld
mar
gin
or in
ad
jace
nt c
rop
s ar
e co
nsid
ered
rel
evan
t fo
r se
ed t
reat
men
t us
es a
nd g
ranu
lar
form
ulat
ions
.” A
lso
des
crib
es
wha
t th
e as
sess
ors
thou
ght
to b
e a
relia
ble
stu
dy.
Als
o m
entio
ns
that
the
y re
ad a
bou
t “d
ust
drif
t ou
tsid
e th
e b
ound
ary
of t
he t
reat
ed
field
was
als
o m
easu
red
usi
ng v
ertic
al g
auze
net
ting.
” b
ut t
hat
“The
se v
ertic
al g
auze
res
ults
wer
e no
t us
ed fu
rthe
r, as
it w
as n
ot
clea
r ho
w t
he r
esul
ts r
epor
ted
as
g a.
s./h
a w
ere
der
ived
and
wha
t th
ey r
epre
sent
. Als
o, a
n ag
reed
met
hod
olog
y is
not
ava
ilab
le
on h
ow t
o us
e or
inte
rpre
t su
ch v
alue
s th
at m
ay h
ave
utili
ty in
es
timat
ing
exp
osur
e to
fiel
d m
argi
n ve
geta
tion
or a
dja
cent
cro
ps
whe
n m
easu
red
at
the
ind
ivid
ual t
rial s
ites.
”
The
asse
ssm
ent
follo
wed
the
EFS
A B
ee G
uid
ance
to
refin
e th
e as
sess
men
ts in
hig
her
tiers
.
P14
, exp
osur
e th
roug
h p
olle
n an
d n
ecta
r: “
The
dai
ly c
onsu
mp
tion
valu
es, f
or p
olle
n an
d n
ecta
r, fo
r ea
ch b
ee c
aste
wer
e ta
ken
from
E
FSA
(201
3c).”
P18
, sec
tion
4. R
elev
ant
info
: “Fi
ve r
elia
ble
acu
te c
onta
ct
end
poi
nts
wer
e av
aila
ble
for
hone
ybee
s” “
Thre
e re
liab
le a
cute
or
al e
ndp
oint
s w
ere
avai
lab
le fo
r ho
neyb
ees”
”No
relia
ble
dat
a w
ere
avai
lab
le t
o d
eriv
e a
chro
nic
leth
al d
ieta
ry d
ose
(LD
D50
) for
ho
neyb
ees.
”
“For
bum
ble
bee
s, o
nly
one
relia
ble
acu
te o
ral..
and
one
acu
te
cont
act
[stu
dy
avai
lab
le]”
“N
o re
liab
le t
oxic
ity d
ata
wer
e av
aila
ble
fo
r so
litar
y b
ees.
”.
5.1.
1.2.
Tre
ated
cro
p s
cena
rio t
estin
g. B
ee G
uid
ance
say
s “i
t is
pre
fera
ble
to
have
mea
sure
d r
esid
ues
in p
olle
n an
d n
ecta
r co
llect
ed fr
om b
ees
in o
pen
fiel
d c
ond
ition
s.”
Res
idue
s in
pol
len
and
nec
tar
colle
cted
dire
ctly
from
hon
eyb
ees
was
ava
ilab
le in
so
me
stud
ies.
Res
idue
s fr
om p
olle
n an
d n
ecta
r co
llect
ed d
irect
ly
from
oth
er b
ee s
pec
ies
wer
e no
t av
aila
ble
.
P35
. A m
etab
olite
of t
hiam
etho
xam
is c
loth
iani
din
, whi
ch is
als
o to
xic.
PESTICIDES AND BEE HEALTH | JANUARY 2019
GRL-TR(R)-01-2019
29
Clo
thia
nidi
nP
eer
revi
ew o
f the
p
estic
ide
risk
asse
ssm
ent
for
bee
s fo
r th
e ac
tive
sub
stan
ce c
loth
iani
din
co
nsid
erin
g th
e us
es
as s
eed
tre
atm
ents
and
gr
anul
es (E
FSA
, 201
8a).
In t
he S
umm
ary:
“R
isk
asse
ssm
ents
w
ere
per
form
ed a
ccor
din
g to
EFS
A
(201
3c) -
the
Bee
Gui
dan
ce -
for
hone
ybee
s, b
umb
leb
ees
and
sol
itary
b
ees.
”
In s
umm
ary:
“...
resi
due
s in
pol
len
and
nec
tar
a lo
w r
isk
was
con
clud
ed
for
som
e b
ee g
roup
s/us
e/sc
enar
io
com
bin
atio
ns, w
hile
a h
igh
risk
was
co
nclu
ded
in o
ther
cas
es.”
In S
umm
ary:
Re
dus
t d
rift:
“lo
w r
isk
to h
oney
bee
s fo
r th
e us
e to
sug
ar
and
fod
der
bee
t” b
ut a
hig
h ris
k fr
om o
ther
out
doo
r us
es”
and
“hi
gh
risk
to h
oney
bee
s an
d b
umb
leb
ees”
b
ut a
low
ris
k to
sol
itary
bee
s w
as
not
dem
onst
rate
d.
In S
umm
ary:
Wat
er c
onsu
mp
tion:
lo
w r
isk
to h
oney
bee
s fr
om p
udd
les,
an
d lo
w r
isk
to h
oney
bee
s fr
om
gutt
atio
n flu
id fr
om “
win
ter
cere
als,
su
gar
bee
t an
d p
otat
oes.
A h
igh
risk
was
con
clud
ed fo
r al
l oth
er u
ses.
A
risk
asse
ssm
ent
for
hone
ybee
s fr
om
exp
osur
e vi
a su
rfac
e w
ater
cou
ld
not
be
per
form
ed.”
The
Bee
Gui
dan
ce d
ocum
ent
is r
efer
red
to
in t
his
asse
ssm
ent
54 t
imes
.
P8
in t
he B
ackg
roun
d in
fo: S
tate
s cl
early
tha
t: “
The
EFS
A
guid
ance
doc
umen
t on
the
ris
k as
sess
men
t of
pla
nt
pro
tect
ion
pro
duc
ts o
n b
ees
(EFS
A, 2
013c
) was
use
d fo
r th
e cu
rren
t ev
alua
tion.
”
Sec
tion
4.1,
tox
icity
end
poi
nts:
“Th
ere
was
no
relia
ble
to
xici
ty d
ata
avai
lab
le fo
r so
litar
y b
ees.
No
dat
a gi
ving
the
ch
roni
c or
al t
oxic
ity t
o b
umb
leb
ees
or t
oxic
ity t
o b
umb
leb
ee
larv
ae w
ere
avai
lab
le. I
n ac
cord
ance
with
EFS
A (2
013c
), w
here
dat
a ar
e m
issi
ng, s
urro
gate
end
poi
nts
can
be
calc
ulat
ed u
sing
tox
icity
dat
a fo
r ho
neyb
ees
div
ided
by
10.
Sur
roga
te e
ndp
oint
s w
ere
ther
efor
e ca
lcul
ated
for
the
acut
e co
ntac
t an
d o
ral t
oxic
ity t
o so
litar
y b
ees
and
for
the
chro
nic
oral
tox
icity
to
bum
ble
bee
s an
d s
olita
ry b
ees.
”
In g
ener
al, t
here
are
sev
eral
inst
ance
s th
at m
entio
n la
ck o
f d
ata
rela
ting
to t
he s
ubst
ance
und
er q
uest
ion
and
the
bee
sp
ecie
s.
Subs
tanc
eRe
fere
nce
Wha
t top
ic d
oes
the
Bee
Gui
danc
e
rela
te to
.O
utco
mes
and
oth
er c
omm
ents
Thia
met
hoxa
m
P55
: “as
ack
now
led
ged
in E
FSA
, 201
3c, t
here
are
sev
eral
ro
utes
of e
xpos
ures
whi
ch a
re n
ot c
over
ed b
y th
e ris
k as
sess
men
t sc
hem
e. (e
.g. i
nsec
t ho
neyd
ew, e
xpos
ure
via
soil)
.”
GRL-TR(R)-01-2019
30
PESTICIDES AND BEE HEALTH | JANUARY 2019
Acet
amip
ridPe
er re
view
of t
he
pest
icid
e ris
k as
sess
men
t of
the
activ
e su
bsta
nce
acet
amip
rid (E
FSA,
201
6).
This
doc
umen
t re
fers
to
a re
que
st fo
r m
ore
info
on
acet
amip
rid in
pol
len
/ b
ee p
rod
ucts
as
bee
s ar
e at
trac
ted
to
pot
atoe
s.
It is
a g
ener
al r
isk
asse
ssm
ent,
not
onl
y ad
dre
ssin
g ris
ks t
o b
ees/
pol
linat
ors
but
als
o aq
uatic
and
mam
mal
ian
toxi
city
.
It st
ates
tha
t B
ee G
uid
ance
doc
umen
t w
as
used
in e
coto
xico
logy
ris
k as
sess
men
t.
It al
so s
tate
s: “
A lo
w r
isk
to h
oney
bee
s (a
cute
, chr
onic
and
larv
ae) a
nd t
o b
umb
le
bee
s (a
cute
) was
con
clud
ed fo
r al
l sce
nario
s fo
r th
e re
pre
sent
ativ
e us
es o
n p
ome
frui
t (p
ost-
flow
erin
g ap
plic
atio
n) a
nd p
otat
oes.
”
P4:
“S
ever
al d
ata
gap
s w
ere
iden
tified
in t
he
area
of e
coto
xico
logy
, i.e
. to
furt
her
add
ress
the
ris
k as
sess
men
t fo
r b
irds,
mam
mal
s, a
qua
tic
orga
nism
s, b
ees
and
non
-tar
get
arth
rop
ods.
”
A s
epar
ate
onlin
e E
U s
tate
men
t ve
rifies
tha
t E
FSA
dee
med
tha
t th
is p
estic
ide
was
con
clud
ed
to b
e of
low
ris
k to
bee
s.
Cya
ntra
nilip
role
Con
clus
ion
on t
he p
eer
revi
ew o
f the
pes
ticid
e ris
k as
sess
men
t of
the
act
ive
sub
stan
ce c
yant
rani
lipro
le
(EFS
A, 2
014a
).
This
doc
umen
t d
oes
not
refe
r to
the
Bee
G
uid
ance
doc
umen
t
It is
a g
ener
al r
isk
asse
ssm
ent,
not
onl
y ad
dre
ssin
g ris
ks t
o b
ees/
pol
linat
ors
but
als
o aq
uatic
and
mam
mal
ian
toxi
city
.
In t
he S
umm
ary:
“A
dat
a ga
p w
as
iden
tified
for
a se
arch
of t
he s
cien
tific
pee
r-re
view
ed o
pen
lite
ratu
re o
n th
e ac
tive
sub
stan
ce a
nd it
s re
leva
nt
met
abol
ites.
”
Som
e p
oint
s fr
om t
he d
ocum
ent.
P13
: “Th
e ap
plic
ant’s
dos
sier
did
not
incl
ude
any
info
rmat
ion
to a
dd
ress
the
effe
ct o
f wat
er
trea
tmen
ts p
roce
sses
on
the
natu
re o
f the
re
sid
ues
that
mig
ht b
e p
rese
nt in
sur
face
w
ater
and
gro
und
wat
er, w
hen
surf
ace
wat
er o
r gr
ound
wat
er a
re a
bst
ract
ed fo
r d
rinki
ng w
ater
.”
This
was
iden
tified
by
the
pan
el a
s a
dat
a ga
p.
P14
, sec
tion
5. E
coto
xico
logy
.
p14
: Lon
g-te
rm r
isk
to m
amm
als
was
dee
med
hi
gh r
isk
until
rea
naly
sis
of t
he d
ata
conc
lud
ed
low
ris
k.
Ap
pro
ved
for
use
in E
U (a
ll fiv
e ne
onic
s ar
e b
anne
d in
Fra
nce)
Subs
tanc
eRe
fere
nce
Wha
t top
ic d
oes
the
Bee
Gui
danc
e
rela
te to
.O
utco
mes
and
oth
er c
omm
ents
PESTICIDES AND BEE HEALTH | JANUARY 2019
GRL-TR(R)-01-2019
31
Cya
ntra
nilip
role
P15
: hon
ey b
ees.
“Th
e fir
st-t
ier
risk
asse
ssm
ent
bas
ed
on t
he o
ral a
nd c
onta
ct H
Q a
pp
roac
h in
dic
ated
a h
igh
risk
for
the
activ
e su
bst
ance
for
all t
he r
epre
sent
ativ
e us
es.”
But
a lo
w r
isk
for
hone
y b
ees
whe
n th
e fo
rmul
ated
pro
duc
t is
use
d o
n p
otat
oes
and
man
dar
ins.
P16
. Det
ail o
n fie
ld t
rials
to
asse
ss t
oxic
ity t
o ho
ney
bee
s. S
pra
y ap
plic
atio
n to
fiel
d v
eget
able
s: “
risk
to
hone
ybee
s co
uld
be
cons
ider
ed a
s lo
w o
nly
if th
e fir
st a
pp
licat
ion
is c
arrie
d o
ut b
efor
e th
e flo
wer
ing
per
iod
and
the
sec
ond
ap
plic
atio
n is
car
ried
out
dur
ing
the
flow
erin
g p
erio
d b
ut a
fter
dai
ly b
ee fl
ight
”The
p
anel
ad
ded
tha
t fu
rthe
r d
ata
is n
eed
ed t
o ad
dre
ss
unce
rtai
ntie
s.
“The
ris
k to
hon
eyb
ees
for
the
rep
rese
ntat
ive
use
in
lett
uce
(sp
ray)
was
con
sid
ered
as
low
bec
ause
it is
not
at
trac
tive
to h
oney
bee
s (i.
e. it
is n
ot a
flow
erin
g cr
op).”
P17
: “re
pre
sent
ativ
e us
es a
s sp
ray
app
licat
ion
on
app
les,
pea
rs, n
ecta
rines
pea
ches
and
ap
ricot
s p
lum
s ci
trus
, man
dar
ins,
oliv
es, g
rap
es a
hig
h ris
k co
uld
not
be
excl
uded
with
the
ava
ilab
le d
ata.
”
Re
mam
mal
ian
toxi
colo
gy, t
here
is n
o cr
itica
l are
a of
con
cern
. Dat
a ga
ps
wer
e id
entifi
ed fo
r fu
rthe
r as
sess
men
t of
som
e m
etab
olite
s. I
n th
e ar
ea o
f ec
otox
icol
ogy
dat
a ga
ps
wer
e id
entifi
ed t
o fu
rthe
r ad
dre
ss t
he r
isk
to m
amm
als,
bee
s an
d n
on-t
arge
t ar
thro
pod
s. T
he r
isk
asse
ssm
ent
coul
d n
ot b
e fin
alis
ed
for
all n
on t
arge
t or
gani
sms
“
P17
(in
this
col
umn
due
to
spac
e): “
By
taki
ng in
to
acco
unt
that
the
se c
rop
s [a
pp
les,
pea
rs, n
ecta
rines
p
each
es a
nd a
pric
ots
plu
ms
citr
us, m
and
arin
s,
oliv
es, g
rap
es] m
ay b
e hi
ghly
att
ract
ive
to h
oney
bee
s,
over
all,
EFS
A c
onsi
der
ed t
hat
the
risk
asse
ssm
ent
for
cyan
tran
ilip
role
and
its
met
abol
ites
for
thes
e re
pre
sent
ativ
e us
es s
houl
d b
e fu
rthe
r ad
dre
ssed
(dat
a ga
p).
Subs
tanc
eRe
fere
nce
Wha
t top
ic d
oes
the
Bee
Gui
danc
e
rela
te to
.O
utco
mes
and
oth
er c
omm
ents
GRL-TR(R)-01-2019
32
PESTICIDES AND BEE HEALTH | JANUARY 2019
Cya
ntra
nilip
role
How
ever
, for
the
rep
rese
ntat
ive
uses
ap
plie
d o
nly
afte
r th
e flo
wer
ing
per
iod
, the
ris
k ca
n b
e co
nsid
ered
as
low
, p
rovi
ded
tha
t ris
k m
itiga
tion
mea
sure
s ar
e ta
ken
to
avoi
d d
irect
exp
osur
e of
the
bee
s fo
ragi
ng o
n flo
wer
ing
wee
ds.
”
P17
:” o
n th
e b
asis
of t
he r
esid
ue d
ata
pro
vid
ed, E
FSA
no
ted
tha
t it
was
not
pos
sib
le t
o ob
serv
e a
clea
r tr
end
fo
r th
e re
sid
ue d
eclin
e.”
P17
: ass
essm
ents
for
all t
he fi
eld
use
s re
fer
to h
oney
b
ees
and
oth
er p
ollin
ator
s su
ch a
s w
ild b
ees
are
not
cove
red
.”
P17
: “d
ata
on m
elon
s ca
nnot
be
extr
apol
ated
to
the
rep
rese
ntat
ive
uses
in t
omat
o an
d p
epp
er d
ue
to d
iffer
ent
attr
activ
enes
s to
bee
s an
d t
he in
trin
sic
diff
eren
ces
bet
wee
n th
e p
lant
s in
ter
ms
of r
esid
ue
tran
sloc
atio
n.”
P17
: “fu
rthe
r d
ata
wou
ld b
e ne
eded
to
add
ress
the
ris
k to
bee
s fo
r th
e re
pre
sent
ativ
e us
es a
s fie
ld d
rip ir
rigat
ion
for
exam
ple
to
acco
unt
for
the
resi
due
inta
kes
with
the
co
nsum
ptio
n of
con
tam
inat
ed n
ecta
r an
d p
olle
n.”
P23
-24:
A n
umb
er o
f dat
a ga
ps
are
liste
d (t
oo m
any
to
cove
r he
re).
Subs
tanc
eRe
fere
nce
Wha
t top
ic d
oes
the
Bee
Gui
danc
e
rela
te to
.O
utco
mes
and
oth
er c
omm
ents
PESTICIDES AND BEE HEALTH | JANUARY 2019
GRL-TR(R)-01-2019
33
Subs
tanc
eRe
fere
nce
Wha
t top
ic d
oes
the
Bee
Gui
danc
e
rela
te to
.O
utco
mes
and
oth
er c
omm
ents
Flup
yrad
ifuro
neC
oncl
usio
n on
the
peer
re
view
of t
he p
estic
ide
risk
asse
ssm
ent o
f th
e ac
tive
subs
tanc
e flu
pyra
difu
rone
(EFS
A,
2015
).
This
doc
umen
t doe
s no
t ref
er to
the
Bee
Gui
danc
e do
cum
ent.
It is
a g
ener
al ri
sk a
sses
smen
t, no
t onl
y ad
dres
sing
risk
s to
bee
s/po
llina
tors
but
als
o aq
uatic
and
m
amm
alia
n to
xici
ty.
Som
e p
oint
s fr
om t
he d
ocum
ent.
“On
the
bas
is o
f the
ava
ilab
le d
ata
and
ass
essm
ents
, a
low
ris
k to
bird
s (a
cute
and
long
-ter
m) a
nd m
amm
als
(acu
te) w
as in
dic
ated
for
all r
epre
sent
ativ
e us
es.”
“a lo
w lo
ng-t
erm
ris
k fo
r m
amm
als
was
ind
icat
ed
for
the
rep
rese
ntat
ive
use
on h
ops,
how
ever
for
the
rep
rese
ntat
ive
use
on le
ttuc
e a
high
ris
k fo
r sm
all
herb
ivor
ous
mam
mal
was
stil
l ind
icat
ed. T
here
fore
, a d
ata
gap
was
iden
tified
”
“low
ris
k fo
r fis
h (a
cute
for
par
ent
and
met
abol
ites
and
ch
roni
c fo
r th
e p
aren
t), a
low
ris
k fo
r al
gae
and
a lo
w r
isk
for
aqua
tic p
lant
s”
P14
. Hon
eyb
ees.
“ch
roni
c to
xici
ty s
tud
ies
(10-
day
feed
ing
test
) wer
e av
aila
ble
for
the
activ
e su
bst
ance
and
for
the
met
abol
ites
difl
uoro
acet
ic a
cid
(DFA
), d
ifluo
roet
hyl-
amin
o-fu
rano
ne (D
FEA
F), 6
-chl
oron
icot
inic
aci
d (6
-CN
A),
6-ch
loro
-pic
olyl
alco
hol a
nd B
YI0
2960
-hyd
roxy
” Th
ey
note
d “
it is
like
ly t
hat
the
...m
etab
olite
s ar
e le
ss t
oxic
to
bee
s th
an fl
upyr
adifu
rone
.”
“the
ris
k to
hon
ey b
ees
was
con
sid
ered
as
low
for
the
rep
rese
ntat
ive
uses
of fl
upyr
adifu
rone
.”
Onl
y on
e st
udy
avai
lab
le fo
r b
umb
leb
ees
ther
efor
e no
t su
ffici
ent
to m
ake
a ju
dge
men
t.
“the
ris
k to
ear
thw
orm
s an
d n
on-t
arge
t so
il m
acro
and
m
icro
orga
nism
s w
as a
sses
sed
as
low
”
In t
he S
umm
ary:
“A
dat
a ga
p w
as id
entifi
ed in
rel
atio
n to
th
e se
arch
of t
he s
cien
tific
pee
r-re
view
ed o
pen
lite
ratu
re
on t
he a
ctiv
e su
bst
ance
and
its
rele
vant
met
abol
ites.
”
GRL-TR(R)-01-2019
34
PESTICIDES AND BEE HEALTH | JANUARY 2019
Subs
tanc
eRe
fere
nce
Wha
t top
ic d
oes
the
Bee
Gui
danc
e
rela
te to
.O
utco
mes
and
oth
er c
omm
ents
Flup
yrad
ifuro
ne“t
he a
ctiv
e su
bst
ance
flup
yrad
ifuro
ne h
as a
hig
h p
oten
tial
to e
xcee
d t
he p
aram
etric
drin
king
wat
er li
mit
of 0
.1μg
/L in
gr
ound
wat
er”
“Dat
a ga
ps
wer
e id
entifi
ed in
the
eco
toxi
colo
gy s
ectio
n…
[incl
udin
g] lo
ng-t
erm
ris
k to
sm
all h
erb
ivor
ous
mam
mal
s fr
om d
ieta
ry r
oute
s in
lett
uce
and
to
furt
her
add
ress
the
ch
roni
c ris
k to
aq
uatic
inve
rteb
rate
s fo
r th
e re
pre
sent
ativ
e fie
ld u
ses
in le
ttuc
e.”
Sulfo
xaflo
r C
oncl
usio
n on
the
peer
re
view
of t
he p
estic
ide
risk
asse
ssm
ent o
f th
e ac
tive
subs
tanc
e su
lfoxa
flor (
EFSA
, 20
14b)
This
doc
umen
t doe
s no
t ref
er to
the
Bee
Gui
danc
e do
cum
ent.
It is
a g
ener
al ri
sk a
sses
smen
t, no
t onl
y ad
dres
sing
risk
s to
bee
s/po
llina
tors
but
als
o aq
uatic
and
m
amm
alia
n to
xici
ty.
In th
e Su
mm
ary:
“D
ata
gaps
w
ere
iden
tified
in th
e Se
ctio
n on
ec
otox
icol
ogy.
With
the
avai
labl
e as
sess
men
ts a
hig
h ris
k to
bee
s w
as n
ot e
xclu
ded
for fi
eld
uses
. A
high
long
-ter
m ri
sk w
as in
dica
ted
for t
he s
mal
l her
bivo
rous
mam
mal
sc
enar
io fo
r fiel
d us
es in
veg
etab
les
and
in c
otto
n.”
Ther
e ar
e m
any
uses
for
this
pes
ticid
e: “
rep
ort
wer
e re
ache
d o
n th
e b
asis
of t
he e
valu
atio
n of
the
re
pre
sent
ativ
e us
es o
f sul
foxa
flor
as a
n in
sect
icid
e on
frui
ting
vege
tab
les
(fiel
d u
se a
nd g
lass
hous
e ap
plic
atio
n; t
omat
o, c
herr
y to
mat
o, p
epp
er (b
ell a
nd n
on
bel
l), a
uber
gine
), cu
curb
its (fi
eld
use
and
gla
ssho
use
app
licat
ion;
cuc
umb
er, w
ater
mel
on, c
ourg
ette
), sp
ring
and
win
ter
cere
als
(whe
at, r
ye, b
arle
y, o
ats,
trit
ical
e)
and
cot
ton
as p
rop
osed
by
the
app
lican
t. M
RLs
wer
e as
sess
ed in
alm
ond
s, p
ecan
s, a
pp
les,
pea
rs, c
herr
y,
pea
ch in
clud
ing
nect
arin
es a
nd a
pric
ots,
plu
m, w
heat
gr
ain,
bar
ley
grai
n, b
rocc
oli,
caul
iflow
er, m
usta
rd g
reen
s,
cab
bag
e, le
af a
nd h
ead
lett
uce,
sp
inac
h, c
eler
y, c
otto
n se
ed, o
ilsee
d r
ape
seed
, gra
pef
ruit,
lem
on, o
rang
es,
mel
on, s
qua
sh (w
inte
r an
d s
umm
er),
cucu
mb
er, p
otat
oes,
su
gar
bee
t, c
arro
t, s
oya
bea
n, b
eans
(pul
ses)
, fre
sh b
eans
w
ith a
nd w
ithou
t p
ods,
str
awb
erry
, tom
ato,
pep
per
s, w
ine
grap
es a
nd t
able
gra
pes
, and
in a
nim
al c
omm
oditi
es s
uch
as m
ilk, e
ggs,
mus
cle,
fat,
live
r an
d k
idne
y.”
P18
: dat
a ga
ps
liste
d, i
nclu
din
g: “
Info
rmat
ion
to fu
rthe
r ad
dre
ss t
he r
isk
to h
oney
bee
s fo
r th
e fie
ld u
ses”
PESTICIDES AND BEE HEALTH | JANUARY 2019
GRL-TR(R)-01-2019
35
Subs
tanc
eRe
fere
nce
Wha
t top
ic d
oes
the
Bee
Gui
danc
e
rela
te to
.O
utco
mes
and
oth
er c
omm
ents
Sulfo
xaflo
r P
7: “
The
app
lican
t ca
rrie
d o
ut a
nd s
ubm
itted
a r
epor
t of
th
eir
sear
ch o
f the
sci
entifi
c p
eer-
revi
ewed
op
en li
tera
ture
on
the
act
ive
sub
stan
ce a
nd it
s re
leva
nt m
etab
olite
s.
The
RM
S [t
he r
app
orte
ur M
emb
er S
tate
, Ire
land
] did
not
p
rovi
de
a tr
ansp
aren
t ev
alua
tion
of t
his
rep
ort,
or
of t
he
per
tinen
t ar
ticle
s th
at w
ere
foun
d. T
here
fore
a d
ata
gap
ha
s b
een
iden
tified
for
a se
arch
of t
he s
cien
tific
pee
r-re
view
ed o
pen
lite
ratu
re o
n th
e ac
tive
sub
stan
ce a
nd it
s re
leva
nt m
etab
olite
s, d
ealin
g w
ith s
ide-
effe
cts
on h
ealth
, th
e en
viro
nmen
t an
d n
on-t
arge
t sp
ecie
s an
d p
ublis
hed
w
ithin
the
last
10
year
s b
efor
e th
e d
ate
of s
ubm
issi
on
of d
ossi
er, t
o b
e co
nduc
ted
and
rep
orte
d in
acc
ord
ance
w
ith t
he G
uid
ance
of E
FSA
on
the
sub
mis
sion
of s
cien
tific
pee
r-re
view
ed o
pen
lite
ratu
re fo
r th
e ap
pro
val o
f pes
ticid
e ac
tive
sub
stan
ces
und
er R
egul
atio
n (E
C) N
o 11
07/2
009
(EFS
A, 2
011)
.”
P15
, eco
toxi
colo
gy: “
Firs
t-tie
r ris
k as
sess
men
ts ..
. in
dic
ated
hig
h ris
k to
hon
ey b
ees.
” an
d “
incr
ease
d
mor
talit
y w
as o
bse
rved
in t
he t
unne
l tes
ts w
hen
sulfo
xaflo
r w
as a
pp
lied
on
flow
erin
g P
hace
lia d
urin
g b
ee
fligh
t, a
nd a
lso
whe
n th
e ap
plic
atio
n w
as in
the
pre
viou
s ev
enin
g (a
fter
bee
flig
ht).
The
incr
ease
in m
orta
lity
was
on
ly a
pp
aren
t on
the
day
of t
he a
pp
licat
ion
or o
n th
e fo
llow
ing
day
. Pot
entia
l ad
vers
e ef
fect
s on
bee
bro
od
coul
d a
lso
not
be
excl
uded
from
the
ava
ilab
le d
ata
and
as
sess
men
ts. h
igh
risk
to b
ees
was
con
clud
ed fr
om t
hese
d
ata
by
the
exp
erts
at
the
mee
ting.
In o
rder
to
man
age
the
risk
to b
ees,
som
e ris
k m
itiga
tion
mea
sure
s w
ere
pro
pos
ed b
y th
e R
MS
for
the
field
use
s. H
owev
er t
he
exp
erts
at
the
mee
ting
did
not
con
sid
er t
hat
the
dat
a an
d
the
asse
ssm
ents
tha
t w
ere
avai
lab
le w
ere
suffi
cien
t to
d
emon
stra
te a
low
ris
k to
bee
s fo
r th
e fie
ld u
ses
even
with
th
e p
rop
osed
mea
sure
s (i.
e. a
pp
licat
ion
only
whe
n b
ees
are
not
pre
sent
in t
he c
rop
).
GRL-TR(R)-01-2019
36
PESTICIDES AND BEE HEALTH | JANUARY 2019
Subs
tanc
eRe
fere
nce
Wha
t top
ic d
oes
the
Bee
Gui
danc
e
rela
te to
.O
utco
mes
and
oth
er c
omm
ents
Sulfo
xaflo
r P
15: “
A lo
w r
isk
was
con
clud
ed fo
r ea
rthw
orm
s an
d o
ther
so
il m
acro
orga
nism
s, s
oil m
icro
orga
nism
s, n
on-
targ
et
terr
estr
ial p
lant
s an
d o
rgan
ism
s”
Thia
clop
ridR
ecen
t as
sess
men
t no
t av
aila
ble
yet
.
Sulfo
xaflo
r E
FSA
(Eur
opea
n Fo
od
Saf
ety
Aut
horit
y),
2018
. Tec
hnic
al r
epor
t on
the
out
com
e of
th
e co
nsul
tatio
n w
ith
Mem
ber
Sta
tes,
the
ap
plic
ant
and
EFS
A
on t
he p
estic
ide
risk
asse
ssm
ent
for
sulfo
xaflo
r in
ligh
t of
co
nfirm
ator
y d
ata.
E
FSA
sup
por
ting
pub
licat
ion
2018
(EFS
A,
2018
d).
This
tec
hnic
al r
epor
t d
etai
ls t
he
outc
ome
of fu
rthe
r co
nsul
tatio
n on
ce
rtai
n as
pec
ts o
f ris
k as
sess
men
t of
ex
pos
ure
to s
ulfo
xaflo
r, in
par
ticul
ar:
(a) t
he r
isk
to h
oney
bee
s vi
a th
e d
iffer
ent
rout
es o
f exp
osur
e, in
p
artic
ular
nec
tar,
pol
len,
gut
tatio
n flu
id a
nd d
ust
(b) r
isk
to h
oney
bee
s fo
ragi
ng in
ne
ctar
or
pol
len
in s
ucce
edin
g cr
ops
and
flow
erin
g w
eed
s;
(c) t
he r
isk
to p
ollin
ator
s ot
her
than
ho
ney
bee
s;
(d) t
he r
isk
to b
ee b
rood
.
Acc
ord
ing
to t
he s
umm
ary:
“The
ris
k as
sess
men
t fo
r b
ees
has
bee
n am
end
ed
cons
ider
ing
the
new
ly a
vaila
ble
lab
orat
ory
and
hig
her
tier
stud
ies.
Fol
low
ing
the
reco
mm
end
atio
ns o
f the
P
estic
ide
Pee
r R
evie
w M
eetin
g 13
3(E
FSA
201
5), t
he
co-R
MS
eva
luat
ed t
he h
ighe
r tie
r st
udie
s in
ligh
t of
the
is
sues
rai
sed
in E
FSA
PP
R P
anel
(201
2) a
nd E
FSA
(201
3).
It is
not
ed t
hat
the
tier
1 ris
k as
sess
men
t ac
cord
ing
to
the
SA
NC
O g
uid
ance
rem
ains
unc
hang
ed c
omp
ared
to
the
pre
viou
s co
nclu
sion
s re
ache
d d
urin
g th
e p
eer
revi
ew o
f the
ris
k as
sess
men
t of
sul
foxa
flor
in 2
014.
Th
e as
sess
men
t of
the
hig
her
tier
stud
ies
mad
euse
of
the
late
st s
tate
of t
he k
now
led
ge o
n th
e to
pic
, with
out
div
ergi
ng fr
om t
he S
AN
CO
gui
dan
ce r
ecom
men
dat
ions
.
The
risk
asse
ssm
ent
incl
uded
som
e no
vel r
efine
men
t st
eps
on w
hich
div
erge
nt v
iew
s w
ere
exp
ress
ed
by
Mem
ber
Sta
tes
dur
ing
the
com
men
ting
pha
se.
Diff
eren
t op
inio
ns w
ere
also
exp
ress
ed in
rel
atio
n to
the
in
terp
reta
tion
and
the
use
of t
he a
vaila
ble
hig
her
tier
stud
ies
and
as r
egar
ds
the
cons
ider
atio
n of
ris
k m
itiga
tion
mea
sure
s fo
r th
e us
e of
sul
foxa
flor.
Bas
ed o
n th
e d
ata
asse
ssed
, a lo
w r
isk
coul
d n
ot b
e d
emon
stra
ted
for
hone
ybee
s an
d n
on-A
pis
bee
s as
a r
esul
t of
the
cur
rent
as
sess
men
ts (p
oint
s a
–d).”
PESTICIDES AND BEE HEALTH | JANUARY 2019
GRL-TR(R)-01-2019
37
Appendix Table 2. The number of peer reviewed papers published up to the date on which the search was conducted, on January 14, 2019. The number of papers is included in brackets and is based on a search of Web of Science7 on January 14, 2019 using “substance” AND “bee” AND “[route of exposure]” to indicate the extent to which research has taken place. NADA denotes ‘not assessed but literature available’ (numbers of published peer-reviewed papers identified in searches are shown in parentheses) and NAND denotes ‘not assessed and no literature available’.
7 http://apps.webofknowledge.com
Route of exposure or
toxicity
Acetamiprid Sulfoxaflor Cyantraniliprole Flupyradifurone Thiacloprid
Nectar NADA (3) (i) NAND NAND NADA (2) (v) NADA (2) (vii)
Pollen NADA (18) (ii)
NADA (3) (iv) NAND NADA (2) (vi) NADA (22) (vii)
Dust drift NAND NAND NAND NAND NADA (1) (ix)
GuttationNAND, risk
could not be excluded
NAND NAND NAND NAND
Puddles NAND NAND NAND NAND NAND
Surface water NADA (6) (iii) NAND NAND NAND NADA (4) (x)
Citations for the peer-review papers found in the Web of Science searches and indicated in Table 2:
(i) (1) Baines, D. et al. Neonicotinoids act like endocrine disrupting chemicals in newly-emerged bees and winter bees. Sci. Rep. 7, 10979 (2017).
(2) Purdy, J. R. Monitoring in-hive residues of neonicotinoids in relation to bee health status. Conference: 12th International Symposium of the ICP-PR Bee Protection Group - Hazards of Pesticides to Bees Location: Ghent Univ, Fac Bioscience Engn, Ghent, Belgium. Sept. 15-17, 2014. HAZARDS OF PESTICIDES TO BEES: 12TH INTERNATIONAL SYMPOSIUM OF THE ICP-PR BEE PROTECTION GROUP Book Series: Julius-Kuhn-Archiv Volume: 450 Pages: 276-283 (2015).
(3) Pohorecka, K. et al. Residues of neonicotinoid insecticides in bee collected plant materials from oilseed rape crops and their effect on bee colonies. J. Api. Sci. 56, 115–134 (2012).
GRL-TR(R)-01-2019
38
PESTICIDES AND BEE HEALTH | JANUARY 2019
(ii) (1) Calatayud-Vernich, P. et al. Pesticide residues in honey bees, pollen and beeswax: Assessing beehive exposure. Environ. Poll. 241, 106–114 (2018).
(2) Balsebre, A. et al. Matrix solid-phase dispersion associated to gas chromatography for the assessment in honey bee of a group of pesticides of concern in the apicultural field. J. Chromatog. A. 1567, 47-54 (2018).
(3) Valverde, S. et al. Development and validation of UHPLC MS/MS methods for determination of neonicotinoid insecticides in royal jelly-based products. J. Food Compos Anal. 70, 105-113 (2018).
(4) Bridi, R. et al. LC-MS/MS analysis of neonicotinoid insecticides: Residue findings in Chilean honeys. Ciênc. Agrotec. 42, 51-57 (2018).
(5) Mitchell, E.I.D. et al. A worldwide survey of neonicotinoids in honey. Science 358, 109-111 ( 2017).
(6) Baines, D. et al. Neonicotinoids act like endocrine disrupting chemicals in newly-emerged bees and winter bees. Sci. Rep. 7, 10979 (2017).
(7) Pohorecka, K. et al. THE EXPOSURE OF HONEY BEES TO PESTICIDE RESIDUES IN THE HIVE ENVIRONMENT WITH REGARD TO WINTER COLONY LOSSES. J. Apic. Sci. 61, 105-125 (2017).
(8) Silvina, N. et al. Neonicotinoids transference from the field to the hive by honey bees: Towards a pesticide residues biomonitor. Sci. Total Environ. 581, 25-31 (2017).
(9) Valverde, S. et al. Fast determination of neonicotinoid insecticides in bee pollen using QuEChERS and ultra-high performance liquid chromatography coupled to quadrupole time-of-flight mass spectrometry. ELECTROPHORESIS 37, 19 Special Issue, 2470-2477 (2016).
(10) Sanchez-Hernandez, L. et al. Simultaneous determination of neonicotinoid insecticides in sunflower-treated seeds (hull and kernel) by LC-MS/MS. FOOD ADDITIVES AND CONTAMINANTS PART A-CHEMISTRY ANALYSIS CONTROL EXPOSURE & RISK ASSESSMENT 33, 442-451 (2016).
(11) Laaniste, A. et al. Determination of neonicotinoids in Estonian honey by liquid chromatography-electrospray mass spectrometry. J. Environ. Sci. Health B 51, 455-464 (2016).
(12) Hao, C. et al. Liquid chromatography/tandem mass spectrometry analysis of neonicotinoids in environmental water. Rapid Comm. Mass Spectr. 29, 2225-2232 (2015).
(13) Lopez-Fernandez, O. et al. High-throughput HPLC-MS/MS determination of the persistence of neonicotinoid insecticide residues of regulatory interest in dietary bee pollen. Analytical & bioanalytical Chem. 407, 7101-7110 (2015).
(14) van der Zee, R. et al. An Observational Study of Honey Bee Colony Winter Losses and Their Association with Varroa destructor, Neonicotinoids and Other Risk Factors. PLoS ONE 7, e0131611 (2015).
(15) Purdy, J. R. Monitoring in-hive residues of neonicotinoids in relation to bee health status. Conference: 12th International Symposium of the ICP-PR Bee Protection Group - Hazards of Pesticides to Bees Location: Ghent Univ, Fac Bioscience Engn, Ghent, Belgium. Sept. 15-17, 2014. HAZARDS OF PESTICIDES TO BEES: 12TH INTERNATIONAL SYMPOSIUM OF THE ICP-PR BEE PROTECTION GROUP Book Series: Julius-Kuhn-Archiv Volume: 450 Pages: 276-283 (2015).
(16) Johnson, S. et al. Evaluation of pesticide toxicity at their field recommended doses to honeybees, Apis cerana and A-mellifera through laboratory, semi-field and field studies. Chemosphere 119, 668-674 (2015).
(17) Yanez, K.P. et al. Trace Analysis of Seven Neonicotinoid Insecticides in Bee Pollen by Solid-Liquid Extraction and Liquid Chromatography Coupled to Electrospray Ionization Mass Spectrometry. Food Analy. Methods 7, 490-499 (2014).
(18) Pohorecka, K. et al. Residues of neonicotinoid insecticides in bee collected plant materials from oilseed rape crops and their effect on bee colonies. J. Api. Sci. 56, 115–134 (2012).
(iii) (1) Murano, H. et al. Influence of humic substances and iron and aluminum ions on the sorption of acetamiprid to an arable soil. Sci. Total. Environ. 615, 1478-1484 (2018).
PESTICIDES AND BEE HEALTH | JANUARY 2019
GRL-TR(R)-01-2019
39
(2) Hao, C. et al. Liquid chromatography/tandem mass spectrometry analysis of neonicotinoids in environmental water. Rapid Comm. Mass Spectrom. 29, 2225-2232 (2015).
(3) Vehovszky, A. et al. Neonicotinoid insecticides inhibit cholinergic neurotransmission in a molluscan (Lymnaea stagnalis) nervous system. Aquatic Toxicol. 167, 172-179 (2015).
(4) Lu, Z. et al. Quantum Yields for Direct Photolysis of Neonicotinoid Insecticides in Water: Implications for Exposure to Nontarget Aquatic Organisms. Environ. Sci. Tech. Lett. , 188-192 (2015).
(5) Wijaya, W. et al. Rapid Detection of Acetamiprid in Foods using Surface-Enhanced Raman Spectroscopy (SERS). J. Food Sci. 79, T743-T747 (2014).
(6) Miranda, G.R.B. et al. Environmental Fate of Neonicotinoids and Classification of Their Potential Risks to Hypogean, Epygean, and Surface Water Ecosystems in Brazil. Human Ecol. Risk Assess. 17, 981-995 (2011).
(iv) (1) Cheng, Y. et al. A semi-field study to evaluate effects of sulfoxaflor on honey bee (Apis mellifera). Bull. Insectol. 71, 225-233 (2018).
(2) Zhu, Y. et al. Feeding toxicity and impact of imidacloprid formulation and mixtures with six representative pesticides at residue concentrations on honey bee physiology (Apis mellifera). PLoS ONE 12, e0178421 (2017).
(3) Siviter, H., Brown, M., Leadbeater, E. Sulfoxaflor exposure reduces bumblebee reproductive success Nature 561, 109–112 (2018). doi: 10.1038/s41586-018-0430-6
(v) (1) Hesselbach, H. et al. Effects of the novel pesticide flupyradifurone (Sivanto) on honeybee taste and cognition. Sci. Rep. 8, 4954 (2018).
(2) Campbell, J. W. et al. An Evaluation of the Honey Bee (Hymenoptera: Apidae) Safety Profile of a New Systemic Insecticide, Flupyradifurone, Under Field Conditions in Florida. J. Econ. Entemol. 109, 1967-1972 (2016).
(vi) (1) Hesselbach, H. et al. Effects of the novel pesticide flupyradifurone (Sivanto) on honeybee taste and cognition. Sci. Rep. 8, 4954 (2018).
(2) Campbell, J. W. et al. An Evaluation of the Honey Bee (Hymenoptera: Apidae) Safety Profile of a New Systemic Insecticide, Flupyradifurone, Under Field Conditions in Florida. J. Econ. Entemol. 109, 1967-1972 (2016).
(vii) (1) Ellis, C. et al. The Neonicotinoid Insecticide Thiacloprid Impacts upon Bumblebee Colony Development under Field Conditions. Environ. Sci. Tech. 51, 1727-1732 (2017).
(2) Pohorecka, K. et al. Residues of neonicotinoid insecticides in bee collected plant materials from oilseed rape crops and their effect on bee colonies. J. Api. Sci. 56, 115–134 (2012).
(viii) (1) Shi, T. et al. Metabolomic analysis of honey bee, Apis mellifera L. response to thiacloprid. Pest. Biochem. Physiol. 152, 17-23 (2018).
(2) Beyer, M. et al. Pesticide residue profiles in bee bread and pollen samples and the survival of honeybee coloniesa case study from Luxembourg. Environ. Sci. Pol. Res. 25, 32163-32177 (2018).
(3) Valverde, S. et al. Development and validation of UHPLC MS/MS methods for determination of neonicotinoid insecticides in royal jelly-based products. J. Food Compos Anal. 70, 105-113 (2018).
(4) Bridi, R. et al. LC-MS/MS analysis of neonicotinoid insecticides: Residue findings in Chilean honeys. Ciênc. Agrotec. 42, 51-57 (2018).
(5) Mitchell, E.I.D. et al. A worldwide survey of neonicotinoids in honey. Science 358, 109-111 ( 2017).
(6) Pohorecka, K. et al. THE EXPOSURE OF HONEY BEES TO PESTICIDE RESIDUES IN THE HIVE ENVIRONMENT WITH REGARD TO WINTER COLONY LOSSES. J. Apic. Sci. 61, 105-125 (2017).
(7) Ellis, C. et al. The Neonicotinoid Insecticide Thiacloprid Impacts upon Bumblebee Colony Development under Field Conditions. Environ. Sci.
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PESTICIDES AND BEE HEALTH | JANUARY 2019
Technol. 51, 1727-1732 (2017).
(8) Roszko, M.L. et al. Levels of Selected Persistent Organic Pollutants (PCB, PBDE) and Pesticides in Honey Bee Pollen Sampled in Poland. PLoS ONE 11, e0167487 (2016).
(9) Valverde, S. et al. Fast determination of neonicotinoid insecticides in bee pollen using QuEChERS and ultra-high performance liquid chromatography coupled to quadrupole time-of-flight mass spectrometry. ELECTROPHORESIS 37, 19 Special Issue, 2470-2477 (2016).
(10) Sanchez-Hernandez, L. et al. Simultaneous determination of neonicotinoid insecticides in sunflower-treated seeds (hull and kernel) by LC-MS/MS. FOOD ADDITIVES AND CONTAMINANTS PART A-CHEMISTRY ANALYSIS CONTROL EXPOSURE & RISK ASSESSMENT 33, 442-451 (2016).
(11) David, A. et al. Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environ. Int. 88, 169-178 (2016).
(12) Kiljanek, T. et al. Multi-residue method for the determination of pesticides and pesticide metabolites in honeybees by liquid and gas chromatography coupled with tandem mass spectrometry-Honeybee poisoning incidents. J. Chromatog. A 1435, 100-114 (2016).
(13) Laaniste, A. Determination of neonicotinoids in Estonian honey by liquid chromatography-electrospray mass spectrometry. J. Environ. Health B 51, 455-464 (2016).
(14) Hao, C. et al. Liquid chromatography/tandem mass spectrometry analysis of neonicotinoids in environmental water. Rapid Comm. Mass Spectrom. 29, 2225-2232 (2015).
(15) David, A. et al. Sensitive determination of mixtures of neonicotinoid and fungicide residues in pollen and single bumblebees using a scaled down QuEChERS method for exposure assessment. Anal. Bioanal. Chem. 407, 8151-8162 (2015).
(16) Lopez-Fernandez, O. et al. High-throughput HPLC-MS/MS determination of the persistence of
neonicotinoid insecticide residues of regulatory interest in dietary bee pollen. Anal. Bioanal. Chem. 407, 7101-7110 (2015).
(17) van der Zee, R. et al. An Observational Study of Honey Bee Colony Winter Losses and Their Association with Varroa destructor, Neonicotinoids and Other Risk Factors. PLoS ONE 7, e0131611 (2015).
(18) Niell, S. et al. QuEChERS Adaptability for the Analysis of Pesticide Residues in Beehive Products Seeking the Development of an Agroecosystem Sustainability Monitor. J. Agri. Food Chem. 63, 4484-4492 (2015).
(19) Yanez, K.P. Trace Analysis of Seven Neonicotinoid Insecticides in Bee Pollen by Solid-Liquid Extraction and Liquid Chromatography Coupled to Electrospray Ionization Mass Spectrometry. Food Anal. Methods 7, 490-499 (2014).
(20) Pohorecka, K. et al. Residues of neonicotinoid insecticides in bee collected plant materials from oilseed rape crops and their effect on bee colonies. J. Api. Sci. 56, 115–134 (2012).
(21) Mommaerts, V. et al. Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. 19, 207-215 (2010).
(22) Skerl, M.I.S. et al. Residues of Pesticides in Honeybee (Apis mellifera carnica) Bee Bread and in Pollen Loads from Treated Apple Orchards. Bull. Environ. Contamin. Toxicol. 83, 374-377 (2009).
(ix) (1) Pochi, D. et al. Sowing of seed dressed with thiacloprid using a pneumatic drill modified for reducing abrasion dust emissions. Bull. Insectol. 68, 273-279 (2015).
(x) (1) Hao, C. et al. Liquid chromatography/tandem mass spectrometry analysis of neonicotinoids in environmental water. Rapid Comm. Mass Spectrom. 29, 2225-2232 (2015).
(2) Vehovszky, A. et al. Neonicotinoid insecticides inhibit cholinergic neurotransmission in a molluscan
PESTICIDES AND BEE HEALTH | JANUARY 2019
GRL-TR(R)-01-2019
41
(Lymnaea stagnalis) nervous system. Aquat. Toxicol. 167, 172-179 (2015).
(3) Lu, Z. et al. Quantum Yields for Direct Photolysis of Neonicotinoid Insecticides in Water: Implications for Exposure to Nontarget Aquatic Organisms. Environ. Sci. Tech. Lett. , 188-192 (2015).
(4) Miranda, G.R.B. et al. Environmental Fate of Neonicotinoids and Classification of Their Potential Risks to Hypogean, Epygean, and Surface Water Ecosystems in Brazil. Human Ecol. Risk Assess. 17, 981-995 (2011).
PEER-REVIEW STUDIES THAT ASSESS EXPOSURE. CASE EXAMPLES FROM TABLE 2.The examples below provide an overview of the sorts of studies available. Note the funding sources.
Case study 1 (from the Web of Science search “acetamiprid” + “bee” + “pollen”)
Pohorecka, K. et al. (2012) looked at the concentration of neonicotinoid insecticides in pollen, nectar, honey and bee bread (bee-collected pollen). The results showed that acetamiprid, thiamethoxam and thiacloprid were the most prevalent insecticides present in pollen and nectar that had been collected by honey bees. The researchers state that bee colonies are at high risk from pesticide exposure in areas where there is intensive cultivation of oilseed rape. The study did not see any adverse short- or long-term effects following seed treatment and spraying of winter and spring oilseed rape. They conclude that additional research into the toxicological impact of neonicotinoid exposure on bees is warranted. [Funding from an industry source was not indicated.]
Case study 2 (from the Web of Science search “flupyradifurone” + “bee” + “pollen”)
Campbell, J. W. et al. (2016) studied whether flupyradifurone applied to a bee-attractive crop (buckwheat) would affect a neighbouring bee colony over a study period of three weeks (ie short-term exposure). The study took place in Florida, US, in June
2015 and involved 24 study colonies. The researchers found that the honey bees they observed did not seem to actively avoid the buckwheat plants that had been sprayed with flupyradifurone (control fields of buckwheat had been sprayed with water). The study found a significantly higher level of flupyradifurone in bee-collected pollen in comparison to bee-collected nectar, but did not find that when flupyradifurone had been applied as directed by the manufacturer that there was an adverse effect on bee colonies. [Note that Bayer, Crop Science Division provided funding for the research.]
Case study 3 (from the Web of Science search “thiacloprid” + “bee” + “pollen”)
Ellis, C. et al. (2017) conducted a field study to look at the effects of the neonicotinoid thiacloprid on bumble bee colonies. In particular, the study looked into whether proximity to a non-treated and good food source mitigated the bees’ exposure to the pesticide if the colonies were moved to a location far from the treated crop. Thiacloprid has a lower toxicity to bees than imidacloprid, thiamethoxam or clothianidin, but it has been shown to cause a higher level of mortality in honey bees. The study took place on nine raspberry farms in central Scotland. In the study (summer 2013), nine test bee colonies were placed adjacent to a sprayed raspberry crop (spraying according to the manufacturer’s recommendation) and, in a separate location, control bee colonies were placed adjacent to a non-sprayed raspberry crop. Bees foraged at their farm for two weeks. The results found that bee colonies exposed to thiacloprid were more likely to fail. The exposed colonies that survived had a lower weight and had fewer reproductives in comparison to the control colonies. They found that some colonies were exposed to very high levels of thiacloprid (up to 771 ppb in pollen), which they state is around two orders of magnitude higher than concentrations of neonicotinoids in nectar and pollen of seed-treated crops. It would seem that spraying crops exposes the bees to slightly higher levels of the pesticide than seed-treated crops. They also note that the crop is significant when determining exposure; bees are highly attracted to raspberry flowers (as they are to oilseed rape, although they are not as attracted to
GRL-TR(R)-01-2019
42
PESTICIDES AND BEE HEALTH | JANUARY 2019
corn). The study did not investigate the mechanisms by which bumble bees are affected by thiacloprid. The researchers say that there is a small chance that the control bees were exposed to pesticides, either by long-distance foraging to nearby farms or because much of the farmed landscape is contaminated with pesticide residues. In conclusion, thiacloprid used at the manufacturer-suggested concentration can harm bumble bee colonies. Further research on the long-term impact to bees (and other pollinators) is warranted. [Funding from UK research grants including the BBSRC.]
Case study 4 (from the Web of Science search “thiacloprid” + “bee” + “surface water”)
Lu, Z. et al. (2015) studied the persistence of neonicotinoid pesticides (thiamethoxam, clothianidin, imidacloprid, acetamiprid, and thiacloprid) in water in the laboratory under environmentally relevant conditions. The study found that in water, the half-life of thiamethoxam was 0.2-1.5 days, depending on the season (and the sunlight available to degrade the active substance) The researchers conclude that other neonicotinoids are likely to behave similarly. [Funding from the Natural Sciences and Engineering Research Council of Canada, a University of Manitoba Graduate Fellowship, and the Canada Research Chairs Program.]
Case study 5 (from the Web of Science search “thiacloprid” + “bee” + “dust drift”)
Pochi, D. et al. (2015) looked at the potential exposure of honey bees to dust from maize seeds that had been treated with thiacloprid and which were being sown in a field. The study was designed to investigate a new drilling prototype that mitigates dust drift, which it compared with conventional drilling. Using a number of Petri dishes and air sampling devices, the researchers assessed the amount of dust drift from conventional and modified seed sowing. The study found that the prototype reduced dust drift by 93.4% in comparison to conventional seed sowing. In both conventional and prototype seed sowing, the amount of dust drift to the field edges was similar at a 5m and at 20 m from the field edge, which the researchers suggest could be because of wind velocity at distances
further from the field. The results show that exposure to thiacloprid from dust drift to a bee flying through a field in which conventional sowing is taking place could be in the range 2.0-49.9 ng bee-1. By contrast, the figures are reduced to 0.3-7.4 ng bee-1 when the prototype dust-mitigation sowing was used. [Funded by the Italian Ministry of Agriculture, Food and Forestry Policies.]
PESTICIDES AND BEE HEALTH | JANUARY 2019
GRL-TR(R)-01-2019
43
Pest
icid
eM
ode
of u
seM
ain
targ
et p
est /
cr
ops
Miti
gatio
n su
gges
ted
by E
FSA
revi
ew d
ocum
ent.
Acet
amip
idS
olub
le g
ranu
les
for
spra
y ap
plic
atio
nM
ultip
le p
ests
(p
artic
ular
ly a
phi
ds)
of
tom
ato,
pot
ato
and
p
ome
frui
t, e
valu
ated
b
y E
FSA
. Oth
er
uses
incl
ude:
leaf
y ve
geta
ble
s; fr
uitin
g ve
geta
ble
s; fr
uit
incl
udin
g ci
trus
, ap
ple
s,
pea
rs, g
rap
es; c
otto
n;
orna
men
tal p
lant
s an
d
flow
ers.
P20
. ‘M
itiga
tion
mea
sure
s co
mp
arab
le t
o 20
m n
o-sp
ray
buf
fer
zone
an
d 2
0 m
veg
etat
ed s
trip
wer
e ne
eded
to
achi
eve
a lo
w r
isk
to a
qua
tic
orga
nism
s fo
r th
e us
e in
pom
e fr
uit
(see
Sec
tion
5). M
itiga
tion
mea
sure
s co
mp
arab
le t
o 10
m n
o-sp
ray
buf
fer
zone
wer
e ne
eded
to
achi
eve
a lo
w
risk
to n
on-t
arge
t ar
thro
pod
s fo
r th
e us
e in
pot
atoe
s (s
ee S
ectio
n 5)
.’
Cya
ntra
n-ili
prol
eA
pp
lied
dire
ctly
to
soil
but
may
als
o b
e us
ed a
s a
seed
tre
atm
ent
or fo
liar
spra
y.
Bro
ad s
pec
trum
in
sect
icid
e fo
r a
wid
e ra
nge
of c
rop
s th
at
is e
ffect
ive
agai
nst
man
y ke
y ch
ewin
g an
d
suck
ing
pes
ts.
Pes
ticid
es P
rop
ertie
s D
atab
ase
stat
es t
hat
this
pes
ticid
e is
hig
hly
toxi
c to
hon
ey b
ees.
From
the
EFS
A r
evie
w,
rep
rese
ntat
ive
field
us
es a
re fo
r le
ttuc
e,
tom
ato,
gre
en b
ean,
p
epp
er a
nd p
otat
oes.
P24
. ‘M
itiga
tion
mea
sure
s su
ch a
s no
-sp
ray
buf
fer
zone
and
/or
vege
tate
d b
uffe
r st
rips
shou
ld b
e ap
plie
d t
o m
anag
e th
e ris
k to
aq
uatic
or
gani
sms
for
the
field
rep
rese
ntat
ive
uses
.’
P24
. ‘Fo
r th
e re
pre
sent
ativ
e us
es a
s sp
ray
app
licat
ion
on fi
eld
ve
geta
ble
s w
ith 2
ap
plic
atio
ns a
t 90
g a
.s./
ha (i
.e. fi
eld
tom
ato,
gre
en
bea
n, a
nd fi
eld
pep
per
), th
e ris
k to
hon
eyb
ees
coul
d b
e co
nsid
ered
as
low
onl
y if
the
first
ap
plic
atio
n is
car
ried
out
bef
ore
the
flow
erin
g p
erio
d
and
the
sec
ond
ap
plic
atio
n is
car
ried
out
dur
ing
the
flow
erin
g p
erio
d b
ut
afte
r d
aily
bee
flig
ht F
or t
he r
epre
sent
ativ
e fie
ld u
se in
lett
uce
(sp
ray)
an
d fo
r th
e re
pre
sent
ativ
e sp
ray
uses
in o
rcha
rds
and
gra
pes
ap
plie
d
only
aft
er t
he fl
ower
ing
per
iod
s, a
pp
licat
ions
dur
ing
the
bee
flig
ht s
houl
d
be
avoi
ded
to
pre
vent
pot
entia
l exp
osur
e vi
a flo
wer
ing
wee
ds.
’
NO
TE: P
25 d
escr
ibes
six
issu
es t
hat
coul
d n
ot b
e fin
alis
ed in
the
rev
iew
. In
clud
ed in
the
se is
sues
was
the
ris
k to
bee
s fo
r th
e re
pre
sent
ativ
e us
es
as fi
eld
drip
irrig
atio
n on
tom
ato
and
pep
per
.
App
endi
x T
able
3. A
n ov
ervi
ew o
f the
five
pes
tici
des i
nclu
ded
in o
ur st
udy
who
se E
U a
ppro
vals
hav
e no
t bee
n re
stri
cted
due
to p
oten
tial
ri
sks t
o be
es. I
nfor
mat
ion
is b
ased
on
the
EFS
A re
view
doc
umen
ts fo
r eac
h pe
stic
ide
and
the
Pest
icid
es P
rope
rtie
s Dat
abas
e of
Uni
vers
ity
of
Her
tfor
dshi
re (P
PD).
Info
rmat
ion
on th
iacl
opri
d fr
om P
PD o
nly
as n
o E
FSA
doc
umen
t is a
vaila
ble.
Ple
ase
note
that
mit
igat
ion
mea
sure
are
di
rect
ly q
uote
d fr
om re
view
doc
umen
ts a
nd d
o no
t ref
lect
a G
reen
peac
e po
siti
on.
GRL-TR(R)-01-2019
44
PESTICIDES AND BEE HEALTH | JANUARY 2019
Pest
icid
eM
ode
of u
seM
ain
targ
et p
est /
cro
psM
itiga
tion
sugg
este
d by
EFS
A re
view
doc
umen
t.
Flup
yrad
ifuro
neFo
liar
and
d
renc
h/d
rip u
se
and
a s
eed
tr
eatm
ent.
For
the
cont
rol o
f Pho
rod
on
hum
uli i
n ho
ps
in N
orth
ern
Eur
ope
and
Nas
onov
ia
ribis
nigr
i in
lett
uce
in t
he
EU
.
P19
. ‘M
itiga
tion
mea
sure
s co
mp
arab
le t
o a
tota
l red
uctio
n of
95
%
(i.e.
sp
ray
drif
t an
d r
unof
f) w
ere
need
ed t
o ad
dre
ss t
he r
isk
for
aqua
tic
orga
nism
s fo
r th
e re
pre
sent
ativ
e us
e in
hop
s (s
ee S
ectio
n 5)
.’
‘Miti
gatio
n m
easu
res
com
par
able
to
the
effe
cts
of a
30-
met
res
non-
spra
y b
uffe
r zo
ne fo
r ho
ps
or 5
- m
etre
s no
n-sp
ray
buf
fer
zone
for
field
use
s le
ttuc
e w
ere
need
ed t
o ad
dre
ss t
he r
isk
for
non-
targ
et a
rthr
opod
s (s
ee
Sec
tion
5).’
NO
TE: P
20 d
escr
ibes
five
issu
es t
hat
coul
d n
ot b
e fin
alis
ed in
the
rev
iew
. O
ne o
f the
se w
as t
he p
oten
tial f
or a
ccum
ulat
ion
in g
roun
dw
ater
.
Sulfo
xaflo
rFo
liar
spra
y ap
plic
atio
nsFo
r th
e co
ntro
l sap
fe
edin
g in
sect
s on
fr
uitin
g ve
geta
ble
s (to
mat
oes;
pep
per
s;
aub
ergi
nes;
cuc
umb
ers;
m
elon
s; c
ourg
ette
s),
sprin
g an
d w
inte
r ce
real
s (w
heat
, rye
, bar
ley,
oat
s,
triti
cale
) and
cot
ton.
PP
D s
tate
s th
at s
ulfo
xaflo
r ha
s a
high
pot
entia
l to
bio
accu
mul
ate,
gen
eral
ly
mod
erat
ely
toxi
c to
bird
s an
d m
amm
als
and
has
a lo
w t
oxic
ity t
o m
ost
aqua
tic s
pec
ies.
It is
tox
ic t
o ho
ney
bee
s an
d e
arth
wor
ms.
P15
. ‘A
hig
h ris
k to
bee
s w
as c
oncl
uded
from
the
se d
ata
by
the
exp
erts
at
the
mee
ting.
In o
rder
to
man
age
the
risk
to b
ees,
som
e ris
k m
itiga
tion
mea
sure
s w
ere
pro
pos
ed b
y th
e R
MS
for
the
field
use
s. H
owev
er t
he
exp
erts
at
the
mee
ting
did
not
con
sid
er t
hat
the
dat
a an
d t
he a
sses
smen
ts
that
wer
e av
aila
ble
wer
e su
ffici
ent
to d
emon
stra
te a
low
ris
k to
bee
s fo
r th
e fie
ld u
ses
even
with
the
pro
pos
ed m
easu
res
(i.e.
ap
plic
atio
n on
ly w
hen
bee
s ar
e no
t p
rese
nt in
the
cro
p).
Ther
efor
e, a
dat
a ga
p w
as a
gree
d t
o fu
rthe
r ad
dre
ss t
he r
isk
to h
oney
bee
s fo
r th
e fie
ld u
ses.
It is
furt
her
note
d t
hat
the
avai
lab
le a
sses
smen
ts fo
r th
e fie
ld u
ses
refe
r to
hon
ey b
ees
and
oth
er p
ollin
ator
s su
ch a
s w
ild b
ees
are
not
cove
red
. A h
igh
risk
to p
ollin
ator
s in
trod
uced
in g
lass
hous
es w
here
su
lfoxa
flor
is u
sed
cou
ld a
lso
not
be
excl
uded
. The
refo
re r
isk
miti
gatio
n m
easu
res
such
us
cove
ring
or r
emov
ing
bum
ble
bee
col
onie
s fo
r th
e ap
plic
atio
n un
til t
he fo
liar
resi
due
s ha
ve d
ried
wer
e p
rop
osed
for
thes
e si
tuat
ions
.’
P19
. The
rev
iew
doc
umen
t st
ates
tha
t th
ere
are
no is
sues
tha
t ca
nnot
be
final
ised
.
Greenpeace is an independent global campaigning organisation that acts to change attitudes and behaviour, to protect and conserve the environment and to promote peace.
Written by: Kirsten Thompson
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Layout design: Juliana Devis / julianadevis.com
Published in January 2019 by Greenpeace Research LaboratoriesSchool of BiosciencesInnovation Centre Phase 2Rennes DriveUniversity of ExeterExeter EX4 4RNUnited Kingdom
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