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

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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.
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:
Received: 28 July 2015
Accepted: 24 September 2015
Subject Areas:
environmental science
neonicotinoid, honeybee, bumblebee,
pollinator, pest management, evidence
for policy
Authors for correspondence:
H. Charles J. Godfray
Angela R. McLean
Electronic supplementary material is available
at or
A restatement of recent advances in the
natural science evidence base concerning
neonicotinoid insecticides and insect
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
Oxford Martin School, c/o Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
Plant Research International, Wageningen University and Research, PO Box 16, 6700 AA Wageningen,
The Netherlands
Rothamsted Research, Harpenden, Herts AL5 2JQ, UK
NERC Centre for Ecology and Hydrology, Crowmarsh Gifford, Wallingford OX10 8BB, UK
School of Agriculture, Policy and Development, University of Reading, Reading, UK
School of Environmental Sciences, University of Guelph, Guelph, Ontario, Canada N1G 2W1
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, which permits unrestricted use, provided the original
author and source are credited.
on October 28, 2015 from
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. 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
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. Proc. R. Soc. B 282: 20151821
on October 28, 2015 from
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:
] A strong evidence base involving experimental
studies or field data collection, with appropriate detailed
statistical or other quantitative analysis.
] A consensus of expert opinion extrapolating
results from related ecological systems and well-estab-
lished ecological principles.
] Some supporting evidence but further work
would improve the evidence base substantially.
]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 26 ng g
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
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
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
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. 0.253 ng g
). 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
] 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
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
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
(d) Laboratory studies of lethal and sublethal effects of
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
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 Proc. R. Soc. B 282: 20151821
on October 28, 2015 from
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
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
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
], which
limits the degree to which honeybee data can be
extrapolated to other sentinel species. [E
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
(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
] Incidences of high neoni-
cotinoid residues that would almost certainly cause acute
toxic effects in honeybees and bumblebees do occur, but
not commonly. [E
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
(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
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
) 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
) con-
centrations. [D
] The authors concluded that their
results did not suggest that neonicotinoids were a sole
cause of colony collapse. [P
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
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
-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
) 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
] Evidence
was found that the insecticide affected the pollinators’
preference for different flowers as sources of pollen.
A22 Moffat et al. [8]. Bumblebee (B. terrestris) colonies were pro-
vided with syrup containing low doses (approx. 2 ng g
of imidacloprid and placed in the field in a non-intensive
agricultural location for 4348 days. By most measures,
the neonicotinoid had a significantly negative effect on
colony performance compared with controls. [D
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 Proc. R. Soc. B 282: 20151821
on October 28, 2015 from
exposure was not manipulated at the colony level, this
study should be considered as correlational rather than
experimental. [P
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
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
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
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
(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
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
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
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
A31 (§43) Evidence continues to accumulate on the drivers of
pollinator decline. Analyses of the extinction rates (since
1850) and changes (19211950 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
A32 (§44) Updates on overwintering honeybee colony loss in
Europe and North America (USA and Canada) have
been published. [D
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
] Proc. R. Soc. B 282: 20151821
on October 28, 2015 from
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.
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
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on October 28, 2015 from
... However, parasitoid insects are among the most important and well-studied enemies of caterpillars. Parasitoids are a special category of secondary consumers that complete their development on or in a single "host" individual (in this case, a caterpillar), killing it in the process (Godfray 1994). Parasitoid insects are distinguished from parasites such as lice and fleas, which may exploit resources from multiple "host" individuals and typically do not kill their hosts (although the line between parasitoid and parasite is sometimes difficult to discern). ...
... In addition, wood boring and subterranean caterpillars may be host to parasitoids that have evolved specialized strategies to locate and attack such hidden hosts (Chandra and Gupta 1977;Hinz and Short 1983;Zong et al. 2012). Parasitoids of most caterpillars develop internally as endoparasitoids; however, ectoparasitism, where the immature parasitoid develops outside the host body, is fairly common and widespread among the parasitic wasps (Quicke 1997(Quicke , 2015Gibson et al. 1997). In addition to being endo-or ectoparasitic, parasitoids are often categorized into two main groups based on their developmental strategies -idiobionts and koinobionts (Askew and Shaw 1986). ...
... It has been estimated that approximately 15% of all insects possess parasitoid lifestyles (Godfray 1994). This is likely a substantial underestimate, as recent studies suggest that the diversity of some parasitoid groups is considerably greater than current described species suggest (e.g., Quicke 2015;Stireman et al. 2017;Forbes et al. 2018;Burington et al. 2020). ...
... In modern agriculture, pesticides are used intensively to mitigate the direct impact of pests or weeds on crop yields (Jess et al., 2018;Krupke et al., 2012;Kudsk et al., 2018). Unfortunately, the current widespread use of pesticides may jeopardize the ecosystem services provided by insect pollinators by exposing bees to harmful chemicals (Godfray et al., , 2015Johnson, 2015;Krupke et al., 2012). More specifically, insecticides pose the highest risk for bee populations as they are designed to kill insects (Johnson, 2015;Sanchez-Bayo and Goka, 2014). ...
... One of the most widely considered routes of pesticide exposure for bees is through the ingestion of contaminated nectar, pollen, water, and chronic 10 day oral NOED (μg/bee) guttation fluids (Godfray et al., , 2015. Because they are considered safe for bees, fungicides can be sprayed on insect attractive crops during bloom when bees are likely foraging on them (Favaro et al., 2019;Gierer et al., 2019;Kopit & Pitts-Singer, 2018). ...
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Fungicides account for more than 35% of the global pesticide market and their use is predicted to increase in the future. While fungicides are commonly applied during bloom when bees are likely foraging on crops, whether real-world exposure to these chemicals – alone or in combination with other stressors – constitutes a threat to the health of bees is still the subject of great uncertainty. The first step in estimating the risks of exposure to fungicides for bees is to understand how and to what extent bees are exposed to these active ingredients. Here we review the current knowledge that exists about exposure to fungicides that bees experience in the field, and link quantitative data on exposure to acute and chronic risk of lethal endpoints for honey bees (Apis mellifera). From the 702 publications we screened, 76 studies contained quantitative data on residue detections in honey bee matrices, and a further 47 provided qualitative information about exposure for a range of bee taxa through various routes. We compiled data for 90 fungicides and metabolites that have been detected in honey, beebread, pollen, beeswax, and the bodies of honey bees. The risks posed to honey bees by fungicide residues was estimated through the EPA Risk Quotient (RQ) approach. Based on residue concentrations detected in honey and pollen/beebread, none of the reported fungicides exceeded the levels of concern (LOC) set by regulatory agencies for acute risk, while 3 and 12 fungicides exceeded the European Food Safety Authority (EFSA) chronic LOC for honey bees and wild bees, respectively. When considering exposure to all bees, fungicides of most concern include many broad-spectrum systemic fungicides, as well as the widely used broad-spectrum contact fungicide chlorothalonil. In addition to providing a detailed overview of the frequency and extent of fungicide residue detections in the bee environment, we identified important research gaps and suggest future directions to move towards a more comprehensive understanding and mitigation of the risks of exposure to fungicides for bees, including synergistic risks of co-exposure to fungicides and other pesticides or pathogens.
... Although Science of the Total Environment 850 (2022) 157822 these declines are caused by a combination of factors, evidence suggests that the use of pesticides is one of the main drivers . Among the various pesticide groups, neonicotinoid insecticides, which have been widely used to control insect pests since the 1990s, have raised particular concern (Godfray et al., 2015;Goulson, 2013;Maini et al., 2010;Sgolastra et al., 2020;Woodcock et al., 2017). As a result, the outdoors use of three neonicotinoids -clothianidin, imidacloprid, and thiamethoxam-has been banned in the EU and restricted in some areas of the US. ...
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The recent EU ban of the three most widely used neonicotinoids (imidacloprid, thiamethoxam and clothianidin) to all outdoors applications has stimulated the introduction of new insecticides into the market. Sulfoxaflor is a new systemic insecticide that, like neonicotinoids, acts as a modulator of nicotinic acetylcholine receptors. In agro-environments, bees can be exposed to this compound via contaminated pollen and nectar for long periods of time. Therefore, it is important to assess the potential effects of chronic exposure to sulfoxaflor, alone and in combination with fungicides, on pollinators. In this study, we tested the effects of chronic exposure to two field concentrations of sulfoxaflor (20 and 100 ppb) alone and in combination with four concentrations of the fungicide fluxapyroxad (7500, 15,000, 30,000 and 60,000 ppb) on syrup consumption and longevity in females of the solitary bee Osmia bicornis. Exposure to 20 ppb of sulfoxaflor, alone and in combination with the fungicide, stimulated syrup consumption, but did not affect longevity. In contrast, syrup consumption decreased in bees exposed to 100 ppb, all of which died after 2–6 days of exposure. We found no evidence of synergism between the two compounds at any of the two sulfoxaflor concentrations tested. Comparison of our findings with the literature, confirms that O. bicornis is more sensitive to sulfoxaflor than honey bees. Our results highlight the need to include different bee species in risk assessment schemes.
... Compared to traditional pesticides, they show stronger selectivity for insects on nAChRs than vertebrates and are thus considered to have reduced toxicity and to exhibit lower resistance in mammals (Jeschke et al. 2013). Since NEOs were first produced in the 1990s beginning with imidacloprid (IMI), other NEOs, including acetamiprid (ACE), clothianidin (CLO), thiamethoxam (TXM), thiacloprid (THI), nitenpyram (NIT), and dinotefuran (DIN), have been successively developed for the market (Godfray et al. 2015). In addition, imidaclothiz (IMZ) is a new NEO with more systemic activity developed by Nantong Jiangshan Agrochemical and Chemical Co. Ltd., China, and it was registered in 2006 by the Chinese Ministry of Agriculture (Shao et al. 2013). ...
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Neonicotinoids (NEOs) are a class of insecticides that have high insecticidal activity and are extensively used worldwide. However, increasing evidence suggests their long-term residues in the environment and toxic effects on nontarget organisms. NEO residues are frequently detected in water and consequently have created increasing levels of pollution and pose significant risks to humans. Many studies have focused on NEO concentrations in water; however, few studies have focused on global systematic reviews or meta-analyses of NEO concentrations in water. The purpose of this review is to conduct a meta-analysis on the concentration of NEOs in global waters based on published detections from several countries to extend knowledge on the application of NEOs. In the present study, 43 published papers from 10 countries were indexed for a meta-analysis of the global NEO distribution in water. Most of these studies focus on the intensive agricultural area, such as eastern Asia and North America. The order of mean concentrations is identified as imidacloprid (119.542 ± 15.656 ng L⁻¹) > nitenpyram (88.076 ± 27.144 ng L⁻¹) > thiamethoxam (59.752 ± 9.068 ng L⁻¹) > dinotefuran (31.086 ± 9.275 ng L⁻¹) > imidaclothiz (24.542 ± 2.906 ng L⁻¹) > acetamiprid (23.360 ± 4.015 ng L⁻¹) > thiacloprid (11.493 ± 5.095 ng L⁻¹). Moreover, the relationships between NEO concentrations and some environmental factors are analyzed. NEO concentrations increase with temperature, oxidation–reduction potential, and the percentage of cultivated crops but decrease with stream discharge, pH, dissolved oxygen, and precipitation. NEO concentrations show no significant relations to turbidity and conductivity.
... Verlust von geeignetem Lebensraum (Fahrig 2003;Olden et al. 2006;van Dyck et al. 2009;Kennedy et al. 2013), Pestizide (Godfray et al. 2015;Goulson et al. 2015), Parasiten und Pathogene (Fürst et al. 2014;Ravoet et al. 2014;Wilfert et al. 2016), invasive Arten (Stout & Morales 2009) sowie der Klimawandel (Giannini et al. 2012;Kerr et al. 2015;Schmidt et al. 2016) genannt. Der Verlust von geeignetem Lebensraum, in qualitativer sowie in quantitativer Hinsicht, stellt dabei aber höchstwahrscheinlich den gravierendsten aller genannten Einschnitte für die Bestäuberinsekten dar (Goulson et al. 2015;Sánchez-Bayo & Wyckhuys 2021). ...
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Aktuell ist weltweit eine zunehmende Ausdehnung der städtischen Gebiete zu beobachten, was ein Verlust von natürlichen Lebensräumen bedeutet. Soll die derzeitige Biodiversität jedoch erhalten bleiben, müssen vermehrt Anstrengungen unternommen werden, um heimischer Flora und Fauna auch im urbanen Gebiet Ersatzlebensräume bieten zu können. Hinsichtlich der Artenvielfalt und der Bewertung des Lebensraums „Stadt“ kommen wissenschaftliche Studien zu stark unterschiedlichen Ergebnissen, wenngleich sie jedoch alle betonen, dass urbane Grünflächen einen wertvollen Beitrag zur Förderung eines städtischen Artenreichtums leisten können. Während vielfach darauf hingewiesen wird, dass ausreichende und geeignete Nahrungsressourcen für die Bestäuberinsekten bereitgestellt werden müssen, wurde in den seltensten Fällen untersucht, ob Zierpflanzen von den urbanen Bestäubern überhaupt als Nahrungsquelle genutzt werden. Dies war für lange Zeit umstritten, wird aber inzwischen zunehmend durch Publikationen belegt, wobei die ökologische Bedeutung der Zierpflanzen nach wie vor kontrovers diskutiert wird. So gibt es offenbar große Attraktivitätsunterschiede innerhalb der Zierpflanzen und darüber hinaus können wohl nicht alle Bestäubergruppen gleichermaßen von den zumeist exotischen Zierpflanzen als Nahrungsressource profitieren. Da zum jetzigen Zeitpunkt nicht zu jeder Zierpflanze wissenschaftlich erhobene Daten vorliegen, war es zunächst ein Ziel dieser Arbeit, belastbare Daten hinsichtlich der Bestäuberfreundlichkeit bestimmter Zierpflanzen, insbesondere solche mit einem hohen Markanteil, zu gewinnen. Für solche Versuche sollten darüber hinaus entsprechende Erfassungsmethoden beurteilt und weiterentwickelt werden. Ein weiterer und bisher kaum untersuchter Schwerpunkt der Arbeit war die Frage, welche Faktoren sich in welcher Form auf die Zusammensetzung und Abundanz der urbanen Bestäuber auswirken. Um diese Fragestellungen bearbeiten zu können, wurden in den Jahren 2017 – 2019 in Freiland- und Semifreilandversuchen Zählungen, Beobachtungen sowie Kescherfänge zur Bestäuberattraktivität bestimmter Zierpflanzen durchgeführt. Im ersten Versuchsansatz wurde an 13 verschiedenen Standorten im Stadtgebiet Stuttgart jeweils ein Hochbeet aufgestellt, welches mit einer identischen Auswahl an Zierpflanzen bepflanzt wurde. In den Jahren 2017 und 2018 wurden alle Standorte während der Sommermonate wöchentlich besucht und die Hochbeete 20 Minuten lang beobachtet. In dieser Zeit wurde die Anzahl der Bestäuberinsekten sowie deren Zugehörigkeit zu bestimmten Insektengruppen erfasst. Es konnten im Rahmen dieser Erfassungen insgesamt 10.565 pollen- und/oder nektarsammelnde Blütenbesucher gezählt werden. Dies bestätigt zunächst einmal, dass unsere Auswahl an Zierpflanzen von Bestäuberinsekten als Nahrungsquelle genutzt wurde. Die Attraktivität der getesteten Zierpflanzen unterschied sich jedoch in erheblichem Maße innerhalb der Pflanzenarten und reichte von durchschnittlich 1,2 Blütenbesuche pro 20 Minuten bei Bracteantha bracteata (Garten-Strohblume) bis zu 5,3 Besuche bei Bidens (Goldmarie). Die Attraktivität variierte jedoch auch – und dies teilweise in stärkerem Maße – zwischen den Sorten einer Art. Statistische Modelle zeigten darüber hinaus signifikante Einflüsse von Untersuchungsjahr und Standort. Dies unterstreicht die Notwendigkeit einer kontinuierlichen Testung aller Zierpflanzen hinsichtlich der Bestäuberfreundlichkeit, wofür die hier beschriebenen Methoden sich als gut geeignet erwiesen haben. Bemerkenswert ist, dass sich nicht nur die Abundanz, sondern auch die Zusammensetzung der Bestäuber signifikant zwischen getesteten Zierpflanzen unterschied (Publikation I). Bei ihrer Nahrungssuche und zur Entscheidungsfindung, ob sich eine Ressource als Nahrungsquelle eignet, ziehen Bestäuberinsekten die charakteristischen und oftmals gattungs-, art- oder gar sortenspezifischen Merkmale der Blüten heran. Während diese bei vielen heimischen Blühpflanzen gut untersucht sind, ist sehr wenig über die Rolle der Blütenmerkmale wie Farbe, morphologische Ausprägungen oder Blütenduft bei den Zierpflanzen bekannt. Da die einzigen diesbezüglichen Untersuchungen bei Astern keine klaren Ergebnisse erbrachten, wurden in dieser Arbeit erstmals anhand der Beispielkultur Calibrachoa und dem Modellbestäuber Bombus terrestris untersucht, welche Blütenmerkmale mit der Attraktivität für Bestäuber korreliert sind. Wie im oben angeführten Stadtversuch zeigte sich, dass die Attraktivität zwischen den getesteten Calibrachoa Sorten stark variierte. Während der Blütenduft die beobachteten Attraktivitätsunterschiede nur in geringem Maße erklären konnte, hatte die Blütenfarbe einen signifikanten Einfluss auf die Attraktivität bei B. terrestris. Für die Frage, ob und welche spezifische Blütenmerkmale bei Calibrachoa und anderen Zierpflanzen die Attraktivität für Bestäuberinsekten beeinflussen, sind aber weitere Untersuchungen notwendig (Publikation II).
... In group-living species, such as honey bees and bumblebees, a diversity of behavioural phenotypes among individuals was also suggested to influence decisionmaking at the group level and to increase the flexibility of the group behaviour (Burns and Dyer 2008;Michelena et al. 2010). Unfortunately, bees often encounter pesticides over long time periods in the foraging environment, especially when colonies are located near treated crops, and in the hive due to the residues present in the honey and wax (Godfray et al. 2014(Godfray et al. , 2015Tsvetkov et al. 2017). The consequences of such a chronic exposure to pesticides are often not a priority in risk assessment procedures. ...
Honey bees are crucial pollinators. A plethora of environmental stressors, such as agrochemicals, have been identified as contributors to their global decline. Especially, these stressors impair cognitive processes involved in fundamental behaviours. So far however, virtually nothing is known about the impact of metal pollutants, despite their known toxicity to many organisms. Their worldwide emissions resulting from human activities have elevated their concentrations far above natural baselines in the air, soil, water and flora, exposing bees at all life stages. The aim of my thesis was to examine the effects of metallic pollution on honey bees using a multiscale approach, from brain to colonies, in laboratory and field conditions. I first observed that bees exposed to a range of concentrations of three common metals (arsenic, lead and zinc) in the laboratory were unable to perceive and avoid, low, yet harmful, field-realistic concentrations of those metals in their food. I then chronically exposed colonies to field-realistic concentrations of lead in food and demonstrated that consumption of this metal impaired bee cognition and morphological development, leading to smaller adult bees. As metal pollutants are often found in complex mixtures in the environment, I explored the effect of cocktails of metals, showing that exposure to lead, arsenic or copper alone was sufficient to slow down learning and disrupt memory retrieval, and that combinations of these metals induced additive negative effects on both cognitive processes. I finally investigated the impact of natural exposure to metal pollutants in a contaminated environment, by collecting bees in the vicinity of a former gold mine, and showed that individuals from populations most exposed to metals exhibited lower learning and memory abilities, and development impairments conducing to reduced brain size. A more systematic analysis of unexposed bees revealed a relationship between head size, brain morphometrics and learning performances in different behavioural tasks, suggesting that exposure to metal pollutants magnifies these natural variations. Hence, altogether, my results suggest that honey bees are unable to avoid exposure to field-realistic concentrations of metals that are detrimental to development and cognitive functions; and call for a revision of the environmental levels considered as ‘safe’. My thesis is the first integrated analysis of the impact of several metal pollutants on bee cognition, morphology and brain structure, and should encourage further studies on the contribution of metal pollution in the reported decline of honey bees, and more generally, of insects.
... Another related major driver for the development of new pesticides, is the need for thriving populations of pollinator species such as bees, which are currently being reduced by climate change (5), and Varroa with associated viral infections leading to colony loss (6,7). There is also a debate about whether the use of existing pesticides results in adverse impacts on populations of beneficial species, for example pollinators such as bees (8). ...
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Global agriculture loses over $100 billion of produce annually to crop pests such as insects. Many of these crop pests either have no current means of control or have developed resistance against chemical pesticides. Long dsRNAs are capable of inducing RNA interference (RNAi) in insects and are emerging as novel highly selective alternatives for sustainable insect management strategies. However, there are significant challenges associated with RNAi efficacy in insects. In this study, we synthesised a range of chemically modified long dsRNA in an approach to improve nuclease resistance and RNAi efficacy in insects. The results showed that dsRNA containing phosphorothioate modifications demonstrated increased resistance to southern green stink bug saliva nucleases. Phosphorothioate and 2'-fluoro modified dsRNA also demonstrated increased resistance to degradation by soil nucleases and increased RNAi efficacy in Drosophila melanogaster cell cultures. In live insects, chemically modified long dsRNA successfully resulted in mortality in both stink bug and corn rootworm. The results provide further mechanistic insight of RNAi efficacy dependence on modifications in the sense or antisense strand of the dsRNA in insects and demonstrate for the first time that RNAi can successfully be triggered by chemically modified long dsRNA in insect cells or live insects.
Global agriculture loses over $100 billion of produce annually to crop pests such as insects. Many of these crop pests either are not currently controlled by artificial means or have developed resistance against chemical pesticides. Long dsRNAs are capable of inducing RNA interference (RNAi) in insects and are emerging as novel, highly selective alternatives for sustainable insect management strategies. However, there are significant challenges associated with RNAi efficacy in insects. In this study, we synthesised a range of chemically-modified long dsRNAs in an approach to improve nuclease resistance and RNAi efficacy in insects. Our results showed that dsRNAs containing phosphorothioate modifications demonstrated increased resistance to southern green stink bug saliva nucleases. Phosphorothioate- and 2’-fluoro-modified dsRNA also demonstrated increased resistance to degradation by soil nucleases and increased RNAi efficacy in Drosophila melanogaster cell cultures. In live insects, we found chemically-modified long dsRNAs successfully resulted in mortality in both stink bug and corn rootworm. These results provide further mechanistic insight into the dependence of RNAi efficacy on nucleotide modifications in the sense or antisense strand of the dsRNA in insects and demonstrate for the first time that RNAi can successfully be triggered by chemically-modified long dsRNAs in insect cells or live insects.
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Hoverflies (Diptera: Syrphidae) and bees (Hymenoptera: Anthophila) are two key taxa for plant pollination. In the present research, the altitudinal distribution of these taxa was studied along two gradients (elevation range: 780–2130 m) in the Dolomiti Bellunesi National Park (Northeastern Italy). Pan traps were used as a sampling device to collect both hoverflies and bees. Other than altitude, the effect of landscape complexity and plant diversity were considered as potential predictors of hoverfly and bee richness and abundance along the two gradients. A total of 68 species of hoverflies and 67 of bees were collected during one sampling year, confirming the efficacy of pan traps as a sampling device to study these taxa. Altitude was the main variable affecting both hoverfly and bee distribution. The two taxa show different distribution patterns: hoverflies have a unimodal distribution (richness and abundance) with peak at middle altitude (1500 m), while bees have a monotonic decline (richness and abundance) with increasing altitude. Both hoverfly and bee populations change with the increasing altitude, but the change in hoverflies is more pronounced than in bees. Species turnover dominates the β-diversity both for hoverflies and bees; therefore, the hoverfly and bee communities at higher altitudes are not subsamples of species at lower altitude but are characterized by different species. This poses important conservation consequences. Some rare species, typical of an alpine habitat were recorded; the present research represents important baseline data to plan a monitoring scheme aimed at evaluating the effect of climate change on pollinators in these fragile habitats.
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The Common Eastern Bumblebee (Bombus impatiens) is native to North America with an expanding range across Eastern Canada and the USA. This species is commercially produced primarily for greenhouse crop pollination and is a common and abundant component of the wild bumblebee fauna in agricultural, suburban and urban landscapes. However, there is a dearth of pesticide toxicity information about North American bumblebees. The present study determined the acute oral lethal toxicity (48-h LD50) of: the butenolide, flupyradifurone (>1.7 μg/bee); the diamide, cyantraniliprole (>0.54 μg/bee); the neonicotinoid, thiamethoxam (0.0012 μg/bee); and the sulfoximine, sulfoxaflor (0.0177 μg/bee). Compared with published honey bee (Apis mellifera) LD50 values, the present study shows that sulfoxaflor and thiamethoxam are 8.3× and 3.3× more acutely toxic to B. impatiens, whereas flupyradifurone is more acutely toxic to A. mellifera. The current rule of thumb for toxicity extrapolation beyond the honey bee as a model species, termed 10× safety factor, may be sufficient for bumblebee acute oral toxicity. A comparison of five risk assessment equations suggested that the Standard Risk Approach (SRA) and Fixed Dose Risk Approach (FDRA) provide more nuanced levels of risk evaluation compared to the Exposure Toxicity Ratio (ETR), Hazard Quotient (HQ), and Risk Quotient (RQ), primarily because the SRA and FDRA take into account real world variability in pollen and nectar pesticide residues and the chances that bees may be exposed to them.
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1 Chronic exposure to neonicotinoid insecticides has been linked to reduced survival of pollinating insects at both the individual and colony level, but so far only experimentally. Analyses of large-scale datasets to investigate the real-world links between the use of neonicotinoids and pollinator mortality are lacking. Moreover, the impacts of neonicotinoid seed coatings in reducing subsequent applications of foliar insecticide sprays and increasing crop yield are not known, despite the supposed benefits of this practice driving widespread use. Here, we combine large-scale pesticide usage and yield observations from oilseed rape with those detailing honey bee colony losses over an 11 year period, and reveal a correlation between honey bee colony losses and national-scale imidacloprid (a neonicotinoid) usage patterns across England and Wales. We also provide the first evidence that farmers who use neonicotinoid seed coatings reduce the number of subsequent applications of foliar insecticide sprays and may derive an economic return. Our results inform the societal discussion on the pollinator costs and farming benefits of prophylactic neonicotinoid usage on a mass flowering crop.
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Endonuclease V (EndoV) is a ubiquitous protein present in all three kingdoms of life, responsible for the specific cleavages at the second phosphodiester bond 3' to inosine. E. coli EndoV (EcEndoV) is the first member discovered in the EndoV family. It is a small protein with a compact gene organization, yet with a wide spectrum of substrate specificities. However, the structural basis of its substrate recognition is not well understood. In this study, we determined the 2.4 Å crystal structure of EcEndoV. The enzyme preserves the general 'RNase H-like motif' structure. Two subunits are almost fully resolved in the asymmetric unit, but they are not related by any 2-fold axes. Rather, they establish "head-to-shoulder" contacts with loose interactions between each other. Mutational studies show that mutations that disrupt the association mode of the two subunits also decrease the cleavage efficiencies of the enzyme. Further biochemical studies suggest that EcEndoV is able to bind to single-stranded, undamaged DNA substrates without sequence specificity, and forms two types of complexes in a metal-independent manner, which may explain the wide spectrum of substrate specificities of EcEndoV.
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The causes of bee declines remain hotly debated, particularly the contribution of neonicotinoid insecticides. In 2013 the UK's Food & Environment Research Agency made public a study of the impacts of exposure of bumblebee colonies to neonicotinoids. The study concluded that there was no clear relationship between colony performance and pesticide exposure, and the study was subsequently cited by the UK government in a policy paper in support of their vote against a proposed moratorium on some uses of neonicotinoids. Here I present a simple re-analysis of this data set. It demonstrates that these data in fact do show a negative relationship between both colony growth and queen production and the levels of neonicotinoids in the food stores collected by the bees. Indeed, this is the first study describing substantial negative impacts of neonicotinoids on colony performance of any bee species with free-flying bees in a field realistic situation where pesticide exposure is provided only as part of normal farming practices. It strongly suggests that wild bumblebee colonies in farmland can be expected to be adversely affected by exposure to neonicotinoids.
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Here we present results of a three-year study to determine the fate of imidacloprid residues in hive matrices and to assess chronic sublethal effects on whole honey bee colonies fed supplemental pollen diet containing imidacloprid at 5, 20 and 100 μg/kg over multiple brood cycles. Various endpoints of colony performance and foraging behavior were measured during and after exposure, including winter survival. Imidacloprid residues became diluted or non-detectable within colonies due to the processing of beebread and honey and the rapid metabolism of the chemical. Imidacloprid exposure doses up to 100 μg/kg had no significant effects on foraging activity or other colony performance indicators during and shortly after exposure. Diseases and pest species did not affect colony health but infestations of Varroa mites were significantly higher in exposed colonies. Honey stores indicated that exposed colonies may have avoided the contaminated food. Imidacloprid dose effects was delayed later in the summer, when colonies exposed to 20 and 100 μg/kg experienced higher rates of queen failure and broodless periods, which led to weaker colonies going into the winter. Pooled over two years, winter survival of colonies averaged 85.7, 72.4, 61.2 and 59.2% in the control, 5, 20 and 100 μg/kg treatment groups, respectively. Analysis of colony survival data showed a significant dose effect, and all contrast tests comparing survival between control and treatment groups were significant, except for colonies exposed to 5 μg/kg. Given the weight of evidence, chronic exposure to imidacloprid at the higher range of field doses (20 to 100 μg/kg) in pollen of certain treated crops could cause negative impacts on honey bee colony health and reduced overwintering success, but the most likely encountered high range of field doses relevant for seed-treated crops (5 μg/kg) had negligible effects on colony health and are unlikely a sole cause of colony declines.
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The global decline in the abundance and diversity of insect pollinators could result from habitat loss, disease, and pesticide exposure. The contribution of the neonicotinoid insecticides (e.g., clothianidin and imidacloprid) to this decline is controversial, and key to understanding their risk is whether the astonishingly low levels found in the nectar and pollen of plants is sufficient to deliver neuroactive levels to their site of action: the bee brain. Here we show that bumblebees (Bombus terrestris audax) fed field levels [10 nM, 2.1 ppb (w/w)] of neonicotinoid accumulate between 4 and 10 nM in their brains within 3 days. Acute (minutes) exposure of cultured neurons to 10 nM clothianidin, but not imidacloprid, causes a nicotinic acetylcholine receptor-dependent rapid mitochondrial depolarization. However, a chronic (2 days) exposure to 1 nM imidacloprid leads to a receptor-dependent increased sensitivity to a normally innocuous level of acetylcholine, which now also causes rapid mitochondrial depolarization in neurons. Finally, colonies exposed to this level of imidacloprid show deficits in colony growth and nest condition compared with untreated colonies. These findings provide a mechanistic explanation for the poor navigation and foraging observed in neonicotinoid treated bumblebee colonies.-Moffat, C., Pacheco, J. G., Sharp, S., Samson, A. J., Bollan, K. A., Huang, J., Buckland, S. T., Connolly, C. N. Chronic exposure to neonicotinoids increases neuronal vulnerability to mitochondrial dysfunction in the bumblebee (Bombus terrestris). © FASEB.
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In summer 2012, we initiated a large-scale field experiment in southern Ontario, Canada, to determine whether exposure to clothianidin seed-treated canola (oil seed rape) has any adverse impacts on honey bees. Colonies were placed in clothianidin seed-treated or control canola fields during bloom, and thereafter were moved to an apiary with no surrounding crops grown from seeds treated with neonicotinoids. Colony weight gain, honey production, pest incidence, bee mortality, number of adults, and amount of sealed brood were assessed in each colony throughout summer and autumn. Samples of honey, beeswax, pollen, and nectar were regularly collected, and samples were analyzed for clothianidin residues. Several of these endpoints were also measured in spring 2013. Overall, colonies were vigorous during and after the exposure period, and we found no effects of exposure to clothianidin seed-treated canola on any endpoint measures. Bees foraged heavily on the test fields during peak bloom and residue analysis indicated that honey bees were exposed to low levels (0.5-2 ppb) of clothianidin in pollen. Low levels of clothianidin were detected in a few pollen samples collected toward the end of the bloom from control hives, illustrating the difficulty of conducting a perfectly controlled field study with free-ranging honey bees in agricultural landscapes. Overwintering success did not differ significantly between treatment and control hives, and was similar to overwintering colony loss rates reported for the winter of 2012-2013 for beekeepers in Ontario and Canada. Our results suggest that exposure to canola grown from seed treated with clothianidin poses low risk to honey bees.
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Neonicotinoid insecticides have been studied as possible contributors to bumble bee declines in North America and Europe. This has potential significance in corn agro-ecosystems since this crop is frequently treated with neonicotinoids and dominates much of the agricultural landscape in North America and Europe where bumble bees and other pollinators are commonplace. We conducted an experiment where commercial bumble bee (Bombus impatiens) hives were placed during pollen shed next to corn (Zea mays) fields that were grown from "conventional" seed that was treated with neonicotinoids, or "organic" seed that was not treated with pesticides. Samples of pollen were collected from corn plants for neonicotinoid residue analysis, pollen types carried by worker bees returning to hives were determined, and in autumn hives were dissected to measure various endpoints that serve as markers of colony vigor. Clothianidin was detected (0.1-0.8 ng/g) in pollen collected from all conventional fields, but was not detected in pollen from organic fields. Corn pollen was only rarely collected from bumble bee foragers and the vast majority of pollen was from wild plants around the corn fields. All hives appeared healthy and neonicotinoid seed treatments had no effect on any hive endpoints measured, except the number of workers, where significantly fewer workers were recovered from hives placed next to conventional fields (96 ± 15 workers per hive) compared to organic fields (127 ± 17 workers per hive). The results suggest that exposure during pollen shed to corn grown from neonicotinoid-treated shed poses low risk to B. impatiens.
Honey bee (Apis mellifera L.) colony collapse disorder (CCD) that appeared in 2005/2006 still lingers in many parts of the world. Here we show that sub-lethal exposure of neonicotinoids, imidacloprid or clothianidin, affected the winterization of healthy colonies that subsequently leads to CCD. We found honey bees in both control and neonicotinoid-treated groups progressed almost identically through the summer and fall seasons and observed no acute morbidity or mortality in either group until the end of winter. Bees from six of the twelve neonicotinoid-treated colonies had abandoned their hives, and were eventually dead with symptoms resembling CCD. However, we observed a complete opposite phenomenon in the control colonies in which instead of abandonment, they were re-populated quickly with new emerging bees. Only one of the six control colonies was lost due to Nosema-like infection. The observations from this study may help to elucidate the mechanisms by which sub-lethal neonicotinoids exposure caused honey bees to vanish from their hives.
Understanding the effects of neonicotinoid insecticides on bees is vital because of reported declines in bee diversity and distribution and the crucial role bees have as pollinators in ecosystems and agriculture. Neonicotinoids are suspected to pose an unacceptable risk to bees, partly because of their systemic uptake in plants, and the European Union has therefore introduced a moratorium on three neonicotinoids as seed coatings in flowering crops that attract bees. The moratorium has been criticized for being based on weak evidence, particularly because effects have mostly been measured on bees that have been artificially fed neonicotinoids. Thus, the key question is how neonicotinoids influence bees, and wild bees in particular, in real-world agricultural landscapes. Here we show that a commonly used insecticide seed coating in a flowering crop can have serious consequences for wild bees. In a study with replicated and matched landscapes, we found that seed coating with Elado, an insecticide containing a combination of the neonicotinoid clothianidin and the non-systemic pyrethroid β-cyfluthrin, applied to oilseed rape seeds, reduced wild bee density, solitary bee nesting, and bumblebee colony growth and reproduction under field conditions. Hence, such insecticidal use can pose a substantial risk to wild bees in agricultural landscapes, and the contribution of pesticides to the global decline of wild bees may have been underestimated. The lack of a significant response in honeybee colonies suggests that reported pesticide effects on honeybees cannot always be extrapolated to wild bees.
Neonicotinoids are the most widely used insecticides world-wide, but their fate in the environment remains unclear, as does their potential to influence non-target species and the roles they play in agroecosystems.We investigated in laboratory and field studies the influence of the neonicotinoid thiamethoxam, applied as a coating to soya bean seeds, on interactions among soya beans, non-target molluscan herbivores and their insect predators.In the laboratory, the pest slug Deroceras reticulatum was unaffected by thiamethoxam, but transmitted the toxin to predaceous beetles (Chlaenius tricolor), impairing or killing >60%.In the field, thiamethoxam-based seed treatments depressed activity–density of arthropod predators, thereby relaxing predation of slugs and reducing soya bean densities by 19% and yield by 5%.Neonicotinoid residue analyses revealed that insecticide concentrations declined through the food chain, but levels in field-collected slugs (up to 500 ng g−1) were still high enough to harm insect predators.Synthesis and applications. Our findings reveal a previously unconsidered ecological pathway through which neonicotinoid use can unintentionally reduce biological control and crop yield. Trophic transfer of neonicotinoids challenges the notion that seed-applied toxins precisely target herbivorous pests and highlights the need to consider predatory arthropods and soil communities in neonicotinoid risk assessment and stewardship.