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Review
Cite this article: Godfray HCJ, Blacquie
`re T,
Field LM, Hails RS, Potts SG, Raine NE, Van-
bergen AJ, McLean AR. 2015 A restatement of
recent advances in the natural science evidence
base concerning neonicotinoid insecticides and
insect pollinators. Proc. R. Soc. B 282:
20151821.
http://dx.doi.org/10.1098/rspb.2015.1821
Received: 28 July 2015
Accepted: 24 September 2015
Subject Areas:
environmental science
Keywords:
neonicotinoid, honeybee, bumblebee,
pollinator, pest management, evidence
for policy
Authors for correspondence:
H. Charles J. Godfray
e-mail: charles.godfray@zoo.ox.ac.uk
Angela R. McLean
e-mail: angela.mclean@zoo.ox.ac.uk
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2015.1821 or
via http://rspb.royalsocietypublishing.org.
A restatement of recent advances in the
natural science evidence base concerning
neonicotinoid insecticides and insect
pollinators
H. Charles J. Godfray1, Tjeerd Blacquie
`re2, Linda M. Field3, Rosemary S. Hails4,
Simon G. Potts5, Nigel E. Raine6, Adam J. Vanbergen7and Angela R. McLean1
1
Oxford Martin School, c/o Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
2
Plant Research International, Wageningen University and Research, PO Box 16, 6700 AA Wageningen,
The Netherlands
3
Rothamsted Research, Harpenden, Herts AL5 2JQ, UK
4
NERC Centre for Ecology and Hydrology, Crowmarsh Gifford, Wallingford OX10 8BB, UK
5
School of Agriculture, Policy and Development, University of Reading, Reading, UK
6
School of Environmental Sciences, University of Guelph, Guelph, Ontario, Canada N1G 2W1
7
NERC Centre for Ecology and Hydrology, Bush Estate, Penicuik, Edinburgh EH26 0QB, UK
NER, 0000-0001-6343-2829
A summary is provided of recent advances in the natural science evidence base
concerning the effects of neonicotinoid insecticides on insect pollinators in a
format (a ‘restatement’) intended to be accessible to informed but not expert
policymakers and stakeholders. Important new studies have been published
since our recent review of this field (Godfray et al. 2014 Proc. R. Soc. B 281,
20140558. (doi:10.1098/rspb.2014.0558)) and the subject continues to be an
area of very active research and high policy relevance.
1. Introduction
Neonicotinoid insecticides were introduced in the 1990s and their market share
quickly expanded to approximately a third of the global insecticide total by
value. They are used in different ways, but particularly as seed treatments
where the chemical is absorbed by the growing plant and is distributed through
all tissues at concentrations that can kill insect herbivores. However, neonicoti-
noids are also translocated to nectar and pollen where they can be consumed by
pollinating insects. Numbers of pollinators have declined in agricultural land-
scapes and there is concern that the introduction and widespread use of
neonicotinoids is partly responsible.
In December 2013, the European Union (EU) instigated partial restrictions
on the use of neonicotinoid insecticides on crops that might be used as food
by pollinating insects. This move is strongly opposed by many in the farming
community and there has been a vigorous debate focusing on the scientific evi-
dence that neonicotinoids harm pollinators, as well as the environmental and
economic costs and benefits of the restrictions.
To try to assist thedebate we produced a ‘restatement’ of the underlying natu-
ral science evidence base in a form that was intended to be accessible to informed
but not expert policymakers and stakeholders [1]. Our avowed aim was to be as
policy-neutral as possible while acknowledging that perfect neutrality is never
achievable. The restatement was published as an appendix to a short paper in
this journal accompanied by an extensive annotated bibliography as the electronic
supplementary material.
Since the restatement was published the debate about restricting neonicoti-
noid use has continued unabated. Farming organizations have successfully
&2015 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution
License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original
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applied for ‘120-day derogations’ from the restrictions in
several European countries (see electronic supplementary
material, paragraph A.2) on the grounds of lack of alternative
pest-management options, moves that have been criticized by
environmental non-governmental organizations. The EU is
committed to review the restrictions in 2015– 2016 and through
the independent European Food Safety Authorityopened a call
for evidence (closing 30 September 2015; http://www.efsa.
europa.eu/en/data/call/150522). Much new research has
been published on the topic (we review over 80 studies here)
including the largest replicated field study to date [2].
Despite the relatively short time since the restatement
was published we provide here an update in the same
format. We do this (i) because of the significant advances in
the science; (ii) because of the continuing need for policy-
neutral evidence summaries in this highly contested area,
especially in the run up to the review of the EU restrictions;
and (iii) in response to a request to do so by the UK
Government Chief Scientific Adviser.
2. Methods
The literature on pollinators and neonicotinoids published since
our restatement was completed was reviewed and a first draft
evidence summary produced by a subset of the authors. All
authors reviewed and revised the document, and agreed on the
categorizing of the different evidence components using the
same scheme we adopted earlier, and which is explained in
paragraph A2 of the restatement update (appendix A). The
second draft was sent to a series of stakeholders or stakeholder
groups including scientists involved in pollinator research,
representatives of the farming and agrochemical industries,
non-governmental organizations concerned with the environ-
ment and conservation, and UK government departments and
statutory bodies responsible for pollinator policy. The document
was revised in the light of much helpful feedback from over 40
stakeholders (see acknowledgements). Though many groups
were consulted, the project was conducted completely indepen-
dent of any stakeholder and was funded by the Oxford Martin
School (part of the University of Oxford).
3. Results
The update to the restatement of the natural science evidence
base concerning neonicotinoid insecticides and insect pollina-
tors is given in appendix A, with an annotated bibliography
provided as the electronic supplementary material.
4. Discussion
The new evidence and evidence syntheses that have
been published in the last 18 months (between February
2014 and August 2015) significantly advance our understand-
ing of the effects of neonicotinoids on insect pollinators.
Nevertheless, major gaps in our understanding remain, and
different policy conclusions can be drawn depending on the
weight one accords to important (but not definitive) science
findings and the weightings given to the economic and
other interests of different stakeholders. The natural science
evidence base places constraints on policies that claim to be
consistent with the science, but does not specify a single
course of action.
We also raise an issue here that arises from our original
study but is not directly relevant to the evidence base on the
effects of neonicotinoids on pollinators. In introducing the sub-
ject we wrote ‘Neonicotinoid insecticides are a highly effective
tool to reduce crop yield losses due to insect pests’, and in the
restatement itself listed a small number of papers in the scien-
tific literature to support this statement [1]. It has been pointed
out that some of these papers were funded by industry and
that there are other studies that have recorded no benefits of
neonicotinoid use (e.g. [3]).
The efficacy of neonicotinoids is clearly an important
issue, and we believe few would doubt that in some circum-
stances (combinations of crops, pests and locales) they are
highly effective and in other circumstances they do not justify
the costs of their purchase. We did not attempt to review this
subject and should have been more careful to say we were not
commenting on efficacy per se.
Though a meta-analysis of efficacy would be very infor-
mative it would also be very difficult. Efficacy studies are
largely conducted by industry, the sector that benefits most
from the data, and are not the type of science usually
funded by public organizations. Typically, the studies are
not published in the peer-reviewed literature (though they
are often made available to regulators) and some are kept
confidential for commercial reasons. Efficacy trials are
expensive and it seems unlikely that they will ever be pub-
licly funded at scale. It is an interesting topic for debate
whether industry would benefit in the long run from placing
more of its data in the public domain as well as putting in
place measures to increase public confidence in studies they
fund themselves. The recent movement in the pharmaceuti-
cal sector to set up trial registries (see https://clinicaltrials.
gov/ct2/home and https://www.clinicaltrialsregister.eu)
provides a model for how the latter might be achieved.
Competing interests. H.C.J.G. chairs and A.R.M. has been a member of the
Science Advisory Council of the UK’s Department of Food & Rural
Affairs (Defra). H.C.J.G. has been a vice-president of Buglife. H.C.J.G.,
R.S.H., L.F., S.G.P. and A.J.V. were members of Defra’s Pollinator
Expert Advisory Group. Some projects in T.B.’s laboratory have been
funded by Bayer Animal Health and co-funded by the Dutch Govern-
ment and Nefyto (the trade association of the Dutch agrochemical
industry). Some projects in L.F.’s laboratory have been funded by
Bayer CropScience, Bayer Animal Health and Syngenta Crop Protection,
and in S.G.P.’s laboratory by Syngenta and Friends of the Earth. R.S.H. is
the director at CEH (where A.J.V. also works)responsiblefor an indepen-
dent field trial on the effect of neonicotinoid seed treatments on
pollinators that is co-funded by Syngenta and Bayer. S.G.P. co-chairs,
A.J.V. is a lead author and N.E.R. is a review editor for the Intergovern-
mental science-policy Platform on Biodiversity and Ecosystem Services
(IPBES) thematic assessment of pollinators, pollination and food
production. N.E.R. is supported as the Rebanks Family Chair in
Pollinator Conservation by The W. Garfield Weston Foundation.
Funding. The Oxford Martin School funded the project.
Acknowledgements. We are very grateful for extremely valuable comment
and criticism from David Aston, Peter Campbell, Norman Carreck,
Christopher Connolly, Darryl Cox, Adrian Dixon, Dave Goulson,
Connie Hart (and colleagues), Chris Hartfield, Emma Hockridge
Reed Johnson, Rebecca Lawrence, Paul Leonard, Tom Macmillan, Ste-
phen Martin, Christian Maus, Jane Memmott, John Mumford, Andy
Musgrove, Ralf Nauen, Jeff Ollerton, Robert Paxton, Louise Payton,
Deborah Procter, Francis Ratnieks, Stuart Roberts, Lucy Rothstein,
Maj Rundlo
¨f, Keith Sappington, Cynthia Scott-Dupree, Matt Shardlow,
Steve Sunderland, David Williams (and colleagues), Ben Woodcock
(and colleagues), Geraldine Wright and Paul de Zylva. Their insights
have strongly shaped the final document, but not all their helpful sug-
gestions were or could be included and the final version is the
responsibility of the authors alone.
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Appendix A. ‘A restatement of recent advances
in the natural science evidence base concerning
neonicotinoid insecticides and insect pollinators’
For an annotated bibliography of the evidence supporting
each statement (hereafter ‘Annotated Bibliography’) see the
electronic supplementary material.
(a) Introduction and aims
A1 This document is an update to our previous ‘restatement’
of the natural science evidence base concerning neonicoti-
noid insecticides and insect pollinators. It does not repeat
evidence presented earlier and concentrates on material
published between February 2014 and August 2015. It is
arranged in the same six sections (a– g). Paragraphs are
numbered A1, A2, etc. and the symbol § (e.g. §16) is
used to indicate the paragraph number in the original
document [1], where the same subject was treated.
A2 (§1) The restrictions on the use of certain neonicotinoids
as seed coatings on crops attractive to pollinating bees
will have been in place for two years in December
2015. The Commission has now mandated the European
Food Safety Authority to collate relevant data as the first
step in the review of these measures. Industry groups in a
number of EU countries have successfully applied for
‘120-day’ derogations to use restricted neonicotinoids in
defined geographical areas on the grounds of the absence
of viable alternatives (see also A33). The province of
Ontario in Canada is introducing restrictions on neonico-
tinoid use on maize (corn) and soy from July 2015. We
are not aware of other equivalent measures that have
been introduced elsewhere in the world.
A3 (§2) As before the authors provide a consensus judgement
on the nature of the different evidence components. We use
the following descriptions, which explicitly are not a rank-
ing, indicated by abbreviated codes. Statements are
considered to be supported by:
[D
ata
] A strong evidence base involving experimental
studies or field data collection, with appropriate detailed
statistical or other quantitative analysis.
[E
xp_op
] A consensus of expert opinion extrapolating
results from related ecological systems and well-estab-
lished ecological principles.
[S
upp_ev
] Some supporting evidence but further work
would improve the evidence base substantially.
[P
rojns
]Projections based on the available evidence for
which substantial uncertainty often exists that could
affect outcomes.
(b) Pollinators and neonicotinoid insecticides
A4 (§§4– 11) In the Annotated Bibliography we list new refer-
ences relevant to the introductory material in this section.
(c) Exposure of pollinators to neonicotinoid insecticides
A5 (§§13 – 14) As in the first version of the restatement
we consider concentrations of neonicotinoids in pollen
and nectar of the order of 2–6 ng g
21
to be typical of
those that a pollinator might encounter when foraging
on seed-treated crops. Statements about low or high
concentrations are made relative to this benchmark,
though we acknowledge there will be variation around
these figures and that this benchmark involves an
element of expert judgment. A wide-ranging review of
how neonicotinoids, introduced as seed coatings, may
move through and persist in the environment has been
published. [E
xp_op
]
A6 (§15) There is evidence that contaminated dust expelled
into the environment from drilling machines during the
planting of seeds treated with neonicotinoids can con-
tinue to pose threats to honeybees. [D
ata
]
A7 (§16) There continues to be intensive study of movement
of neonicotinoids through the environment and their
effect on non-pollinating organisms. This topic is out-
side the scope of this restatement though in the
Annotated Bibliography we provide an entry into this
literature. [E
xp_op
]
A8 (§18) A laboratory study of honeybee and bumblebee
(Bombus terrestris) behaviour showed that foraging-age
insects do not avoid food sources containing imidaclo-
prid, thiamethoxam or clothianidin at field relevant
concentrations (approx. 0.25–3 ng g
21
). The bees do
not seem able to ‘taste’ these compounds though there
is evidence that the first two stimulate feeding. The
response is affected by insect age: newly emerged hon-
eybees and bumblebees largely avoid imidacloprid-
contaminated sugar solution. [D
ata
] These results
suggest that it may be less likely that individual
flower-visiting bees will reduce their pesticide exposure
by avoiding flowers in the field contaminated by insec-
ticides, but this needs to be tested in the field. [E
xp_op
]
A9 (§20) Honeybee colonies placed in or beside fields of
flowering oilseed rape (canola) forage extensively on
the crop, though those situated further away may use
it much less, even in landscapes where it is the domi-
nant bee-attractive crop. There is limited evidence for
similar patterns in other bee species. [D
ata
]
A10 (§21) Summary. Some information is available on the
extent to which pollinators are exposed to neonicoti-
noids through different pathways in the environment.
Most exposure will be at sublethal levels from foraging
on seed-treated plants, the most important exception
being contamination from dust at the time of planting,
especially when regulations and best practice are not fol-
lowed. Better quantitative data on typical concentrations
in nectar and pollen of non-crop plants in agricultural
landscapes and the extent of exposure through planting
dust and other sources is desirable, as is improved data
on how different species of pollinating bees collect food
in different landscapes. [E
xp_op
]
(d) Laboratory studies of lethal and sublethal effects of
neonicotinoids
A11 (§§22 – 27) New reviews of the literature on lethal and
sublethal effects of neonicotinoids on pollinators, and
a large literature survey, have been published. [E
xp_op
]
A12 (§25) Further studies have shown the potential of neoni-
cotinoids to cause detrimental sublethal effects in
different species of flower-visiting bees, as well as the
complexity of the physiological response of larval and
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adult honeybees to acute and chronic sublethal neonico-
tinoid exposure. How sublethal doses of neonicotinoids
affect behavioural processes such as homing ability in
honeybees is strongly context-dependent (affected by,
for example, temperature and landscape structure)
complicating the design of standard assays of sublethal
effects. Recent studies have associated chronic low doses
of neonicotinoids with neuronal dysfunction in the
brain of bumblebees and increased vulnerability to
other neural stressors. [D
ata
]
A13 (§26) There is some new evidence that biological and
non-biological stresses can exacerbate sublethal effects
of neonicotinoids, though such effects are not universal
and are difficult to predict. [S
upp_ev
]
A14 (§27a) A new survey of toxicity data shows that the rela-
tive sensitivity to different pesticides of honeybees and
other pollinating bees is highly variable [D
ata
], which
limits the degree to which honeybee data can be
extrapolated to other sentinel species. [E
xp_op
]
A15 (§28) Summary. Data continue to accumulate showing
that sublethal neonicotinoid exposure can affect many
aspects of pollinator behaviour and physiology
(though most studies involve honeybees or bumble-
bees). Sublethal effects at field-realistic doses are now
established, but their consequences for pollinator popu-
lations and pollination are still unclear. Responses to
neonicotinoids vary across bee species and are affected
by type of exposure (for example, acute versus chronic
or oral versus contact), which makes generalisations
difficult. [E
xp_op
]
(e) Neonicotinoid residues observed in pollen, nectar
and wax in the field
A16 (§§29 –31) New data, data compilations and reanalyses of
earlier data continue to show that neonicotinoid residues
can be detected in pollen and nectar collected by pollinat-
ing bees. However, these data are highly variable, making
general inference hard. [S
upp_ev
] Incidences of high neoni-
cotinoid residues that would almost certainly cause acute
toxic effects in honeybees and bumblebees do occur, but
not commonly. [E
xp_op
]
A17 (§32) Summary (unchanged from earlier restatement). Neo-
nicotinoids can be detected in wild pollinators as well
as honeybee and bumblebee colonies but data are rela-
tively few and restricted to a limited number of
species. Studies to date have found low levels of resi-
dues in surveys of honeybees and honeybee products.
Observed residues in pollinating bees and the products
they collect will depend critically on details of spatial
and temporal sampling relative to crop treatment and
flowering. [E
xp_op
]
(f) Experiments conducted in the field
A18 (§33) As before, we give separate, detailed treatment to
‘semi-field’ studies where insects are exposed by the
experimenter to a known dose of insecticide and then
allowed to forage in the environment, and ‘true field’
studies involving exposure to neonicotinoids as applied
in actual farm landscapes. There is continuing debate
about the relevance of the doses and application
methods used in semi-field studies, and about the
relevance of methodologies used in true field
experiments. [E
xp_op
]
A19 Dively et al. [4] provided replicate colonies of honeybees
over a 12-week period with supplemental pollen paste
diets containing imidacloprid at three concentrations (5,
20 and 100 ng g
21
) with a fourth control treatment. Exper-
iments were conducted in 2009 (10 replicates per
treatment) and 2010 (seven replicates). They found no
effect on foraging performance or colony health in the
short term but over a longer period, colonies exposed to
neonicotinoids were more likely to lose queens, suffer
higher overwintering mortality and have greater Varroa
infestations, though these effects were only statistically
significant at the high (20) and very high (100 ng g
21
) con-
centrations. [D
ata
] The authors concluded that their
results did not suggest that neonicotinoids were a sole
cause of colony collapse. [P
rojns
]
A20 Lu et al. [5].Honeybee colonies were fed with syrup
containing high concentrations of imidacloprid or
clothianidin, or with no added insecticide, for a 13-
week period from July to September (in Massachusetts,
USA). A detrimental effect of neonicotinoids on success-
ful overwintering was reported though we have
concerns (see Annotated Bibliography) about how this
conclusion was reached. [E
xp_op
]
A21 (§37) Gill & Raine [6] reported how the day-to-day fora-
ging patterns of 259 bumblebee (B. terrestris) workers
from 40 colonies were affected by individual or com-
bined exposure to the neonicotinoid imidacloprid and
the pyrethroid
l
-cyhalothrin. These data, and results
presented by Gill et al. [7], were collected in the same
experiment conducted in 2011 (see §37). Exposure to
imidacloprid concentrations (10 ng g
21
) towards the
high end of what is typically observed in the field led
to acute and chronic effects on individual foraging be-
haviour (although actual imidacloprid consumption by
individual workers will have been diluted by foraging
from untreated floral sources in the field; see §37).
Whereas individual bumblebee foraging efficiency nor-
mally improves with experience, this did not occur in
individuals exposed to imidacloprid. [D
ata
] Evidence
was found that the insecticide affected the pollinators’
preference for different flowers as sources of pollen.
[S
upp_ev
]
A22 Moffat et al. [8]. Bumblebee (B. terrestris) colonies were pro-
vided with syrup containing low doses (approx. 2 ng g
21
)
of imidacloprid and placed in the field in a non-intensive
agricultural location for 43–48 days. By most measures,
the neonicotinoid had a significantly negative effect on
colony performance compared with controls. [D
ata
]
A23 (§38) A true field experiment by Thompson et al. [9]
was originally interpreted as showing no effects of
two neonicotinoids on bumblebee (B. terrestris) colony
performance. The experiment placed multiple colonies
adjacent to oilseed rape fields that had received different
insecticide treatments (but with no replication at the
field level). A colony-level reanalysis of the data by
Goulson [10] showed a significant relationship between
neonicotinoid concentration and performance: colonies
with higher concentrations of thiamethoxam or clothia-
nidin in nectar, or thiamethoxam in pollen stores,
produced significantly fewer new queens. Because
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exposure was not manipulated at the colony level, this
study should be considered as correlational rather than
experimental. [P
rojns
]
A24 Cutler et al. [11]. Ten 2-hectare plots in Southern Ontario,
Canada, were planted with oilseed rape, half of which
were planted with seed treated with the neonicotinoid
clothianidin with the other half controls. During peak
flowering, four honeybee hives were placed in the
centre of each field for two weeks before being moved
to a site away from insecticide treated crops. Pollen
from hives in treated fields had higher concentrations of
clothianidin (which were non-zero in controls) but
no effects of the insecticide were found for a variety of
honeybee colony growth or overwintering metrics. [D
ata
]
A25 Cutler & Scott-Dupree [12].Bumblebee (Bombus impatiens)
colonies were placed beside four fields planted with
organic maize and four with maize grown from neonico-
tinoid-coated seeds in Southern Ontario, Canada. The
study took place on commercial farms and organic and
non-organic maize produced pollen at different times.
No differences were found in ten measures of colony
health, except that colonies by treated fields had signifi-
cantly fewer workers (which the authors attributed to
an effect of crop development time). Analysis of collec-
ted pollen showed maize was a very small component
(0–2%) of these bumblebees’ diets. [D
ata
]
A26 Rundlo
¨f et al. [2]. In southern Sweden eight pairs of
spring-sown oilseed rape fields were chosen with one
of each pair grown from clothianidin coated seeds and
the other from non-coated seeds. The seed treatment
used, as recommended by the manufacturer, led to
higher concentrations of clothianidin in pollen than is
normally observed in this crop. Treated fields had
lower densities of solitary bees and bumblebees, and
poorer bumblebee (B. terrestris) colony growth and
queen production (all comparisons statistically signifi-
cant). Solitary bees (Osmia bicornis) placed adjacent to
treated fields all disappeared while a small but signifi-
cantly higher number nested beside control fields. The
experiment detected no significant effects on measures
of honeybee colony strength. Wildflowers, to which
pollinators may also be exposed, had higher levels
of clothianidin when growing in uncultivated land
around treated compared to untreated crops. [D
ata
]
A27 (§40) Summary. Evidence continues to accumulate from
semi-field experiments that sublethal exposure to neoni-
cotinoid insecticides, chiefly but not exclusively at the
high end of what is likely to be experienced in the
environment, can affect foraging and other behaviours
in the field. Several true field studies have reported no
effect of exposure to neonicotinoid-treated crops on hon-
eybee colony performance, but the first large-scale study
of the exposure of bumblebees (see A26) found strong
evidence of harmful effects. There is very little infor-
mation about the effects of neonicotinoids on non-bee
pollinators. [E
xp_op
]
(g) Consequences of neonicotinoid use
A28 (§41) A new, open access computer model of honeybee
colony performance has been developed that could help
integrate the effects of different stressors (including
insecticide exposure on colony performance). Models
of the effects of sublethal stress, including insecticide
exposure, on bumblebee colony dynamics and failure
rates have also been developed. [E
xp_op
]
A29 Budge et al. [13] collected data on honeybee colony
in-season loss and neonicotinoid use from nine regions
of the UK every other year from 2000 to 2010. Controlling
for region (but not year) they find a weak but significant
correlation between colony loss and imidacloprid use,
but not total neonicotinoid use. We found that this
effect was due to a correlation between annual average
colony loss and imidacloprid use. Imidacloprid use
peaked mid-decade (after which it was replaced by thia-
mexotham and clothianidin) and there was a tendency
for honeybee losses to be higher at this time. Because
other factors not included in the analysis may show simi-
lar annual patterns, and because of statistical issues with
the analysis (see Annotated Bibliography), the correlation
of honeybee colony losses with imidacloprid use, and the
lack of correlation with total neonicotinoid use, should be
treated with great caution. [E
xp_op
]
A30 (§42) A meta-analysis suggests that 80% of the pollination
of global crops for which wild bees are responsible can be
attributed to the activities of just 2% of species. These also
tend to be species that are most responsive to interventions
designed to increase bee densities. [E
xp_op
]Themost
important species of wild bees in Europe and North
America are common species of bumblebee (Bombus
spp.) underlying the importance of understanding their
interaction with insecticides. [E
xp_op
]
A31 (§43) Evidence continues to accumulate on the drivers of
pollinator decline. Analyses of the extinction rates (since
1850) and changes (1921–1950 versus 1983– 2012) in
species richness and composition of bees and wasps in
the UK suggests land use and management changes
are the most important historical drivers with major
faunal losses occurring early in the twentieth century.
Any effects of changes in pesticide use over recent dec-
ades are unlikely to be picked up by these analyses. An
analysis of the historical shifts in the ranges of European
and North American bumblebees showed that they
have failed to track climate warming at their northern
range limits, while southern range limits have con-
tracted. These shifts were independent of changes in
land use (both continents) and pesticides application,
including neonicotinoids (in North America only; pesti-
cide data was unavailable for Europe). This study only
assessed changes in species range distributions, and so
any impacts of pesticides on population density or
diversity at finer habitat or landscape scales would not
be identified. [S
upp_ev
]
A32 (§44) Updates on overwintering honeybee colony loss in
Europe and North America (USA and Canada) have
been published. [D
ata
]
A33 (§45) There are still few data examining the effects of the
neonicotinoid restrictions on pest numbers and conse-
quently on crop yields and income, on farmers’
decisions about whether to grow crops subject to restric-
tion, or on alternative pest-management strategies used
by farmers. A recently published study suggests farmers
that use neonicotinoid seed treatments on oilseed rape
in the UK use fewer subsequent foliar insecticide appli-
cations in the autumn but with no overall effect on
applications at flowering time. [E
xp_op
]
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A34 (§46) Summary. There still remain major gaps in our
understanding of how pollinator colony-level (for
social bees) and population processes may dampen or
amplify the lethal or sublethal effects of neonicotinoid
exposure and their effects on pollination services; as
well as how farmers might change their agronomic prac-
tices in response to restrictions on neonicotinoid use and
the resulting positive or negative effects on pollinators
and pollination. While these areas continue to be
researched there is still a limited evidence base to
guide policymakers on how pollinator populations
will be affected by neonicotinoid use or how agricul-
ture will respond to neonicotinoid usage restrictions.
[E
xp_op
]
References
1. Godfray HCJ, Blacquie
`re T, Field LM, Hails RS,
Petrokofsky G, Potts SG, Raine NE, Vanbergen AJ,
McLean AR. 2014 A restatement of the natural
science evidence base concerning neonicotinoid
insecticides and insect pollinators. Proc. R. Soc. B
281, 20140558. (doi:10.1098/rspb.2014.0558)
2. Rundlo
¨fMet al. 2015 Seed coating with a
neonicotinoid insecticide negatively affects wild
bees. Nature 521, 77– 80. (doi:10.1038/
nature14420)
3. Douglas MR, Rohr JR, Tooker JF. 2015 Neonicotinoid
insecticide travels through a soil food chain,
disrupting biological control of non-target pests
and decreasing soya bean yield. J. Appl. Ecol. 52,
250–260. (doi:10.1111/1365-2664.12372)
4. Dively GP, Embrey MS, Kamel A, Hawthorne DJ,
Pettis JS. 2015 Assessment of chronic sublethal
effects of imidacloprid on honey bee colony health.
PLoS One 10, e0118748. (doi:10.1371/journal.pone.
0118748)
5. Lu CS, Warchol KM, Callahan RA. 2014 Sub-lethal
exposure to neonicotinoids impaired honey bees
winterization before proceeding to colony collapse
disorder. B. Insectol. 67, 125–130.
6. Gill RJ, Raine NE. 2014 Chronic impairment of
bumblebee natural foraging behaviour induced
by sublethal pesticide exposure. Funct. Ecol. 28,
1459–1471. (doi:10.1111/1365-2435.12292)
7. Gill RJ, Ramos-Rodriguez O, Raine NE. 2012
Combined pesticide exposure severely affects
individual- and colony-level traits in bees. Nature
491, 105–108. (doi:10.1038/nature11585)
8. Moffat C, Pacheco JG, Sharp S, Samson AJ, Bollan
KA, Huang J, Buckland ST, Connolly CN. 2015
Chronic exposure to neonicotinoids increases
neuronal vulnerability to mitochondrial dysfunction
in the bumblebee (Bombus terrestris). FASEB J. 29,
2112–2119. (doi:10.1096/fj.14-267179)
9. Thompson H, Harrington P, Wilkins W, Pietravalle S,
Sweet D, Jones A. 2013 Effects of neonicotinoid
seed treatments on bumble bee colonies under field
conditions. See http://fera.co.uk/ccss/documents/
defraBumbleBeeReportPS2371V4a.pdf (accessed
October 2015).
10. Goulson D. 2015 Neonicotinoids impact
bumblebee colony fitness in the field; a
reanalysis of the UK’s Food & Environment Research
Agency 2012 experiment. PeerJ 3, e854. (doi:10.
7717/peerj.854)
11. Cutler GC, Scott-Dupree CD, Sultan M, McFarlane
AD, Brewer L. 2014 A large-scale field study
examining effects of exposure to clothianidin seed-
treated canola on honey bee colony health,
development, and overwintering success. PeerJ,
e652. (doi:10.7717/peerj.652)
12. Cutler GC, Scott-Dupree CD. 2014 A field study
examining the effects of exposure to neonicotinoid
seed-treated corn on commercial bumble bee
colonies. Ecotoxicology 23, 1755–1763. (doi:10.
1007/s10646-014-1340-5)
13. Budge GE, Garthwaite D, Crowe A, Boatman ND,
Delaplane KS, Brown MA, Thygesen HH, Pietravalle
S. 2015 Evidence for pollinator cost and farming
benefits of neonicotinoid seed coatings on
oilseed rape. Sci. Rep. 5, 12754. (doi:10.1038/
srep12574)
rspb.royalsocietypublishing.org Proc. R. Soc. B 282: 20151821
6
on October 28, 2015http://rspb.royalsocietypublishing.org/Downloaded from
