Neonicotinoids, bee disorders and the sustainability of pollinator services

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Neonicotinoids, bee disorders and the sustainability of pollinator
§
services
Jeroen P van der Sluijs1, Noa Simon-Delso1, Dave Goulson2,

Laura Maxim3, Jean-Marc Bonmatin4 and Luc P Belzunces5

Inlessthan20years,neonicotinoidshavebecomethemost CurrentOpinioninEnvironmentalSustainability2013,5:xx–yy

widelyusedclassofinsecticideswithaglobalmarketshare
ThisreviewcomesfromathemedissueonOpenissue2013
of more than 25%. For pollinators, this has transformed the
EditedbyRikLeemansandWilliamDSolecki
agrochemical landscape. These chemicals mimic the

acetylcholine neurotransmitter and are highly neurotoxic to

insects. Their systemic mode of action inside plants means

phloemic and xylemic transport that results in translocation 1877-3435/$–seefrontmatter,#2013TheAuthors.Publishedby
to pollen and nectar. T heir wide app lication , p ersistence in ElsevierB.V. A llrig htsre served.

soilandwaterandpotentialforuptakebysucceedingcrops
http://dx.doi.org/10.1016/j.cosust.2013.05.007
and wild plants make neonicotinoids bioavailable to

pollinators at sublethal concentrations for most of the year.

This results in the frequent presence of neonicotinoids in
Introduction
honeybeehives.Atfieldrealisticdoses,neonicotinoidscause
a wide ran ge of ad vers e subleth al effe cts in honeybe e and The introduction to the market in the early 1990s of
b umble bee c olo nies, affe cting colo ny perf or mance thro ugh imid acloprid and thi aclop rid ope ned the neon icotino id
impairment of foragin g succes s, broo d and larval eraofinsectp estc ontrol[1].A ctingsys tem ically,thisnew

development, memory and learning, damage to the central class of neurotoxic insecticides is taken up by plants,

nervoussystem,susceptibilitytodiseases,hivehygieneetc. primarilythroughtheroots,andtranslocatestoallpartsof

Neonicotinoids exhibit a toxicity that can be amplified by the plant through xylemic and phloemic transport [2].

various other agrochemicals and they synergistically Thissystemicpropertycombinedwithveryhightoxicity

reinforce infectious agents such as Nosema ceranae which to insects enabled formulating neonicotinoids for soil

together can produce colony collapse. The limited available treatment and seed coating with typical doses from 10
datasug gest thatthey arelik elytoexh ibit s imilar t oxicityto to200gha (cid:2)1h ighen oughto prov idelong lastin gprot ec-

virtually all other wild insect pollinators. The worldwide tion of the whole plant from pest insects.

production of neonicotinoids is still increasing. Therefore a

transitiontopollinator-friendlyalternativestoneonicotinoids Neonicotinoids interact with the nicotinic acetylcholine

is urgently needed for the sake of the sustainability of receptors(nAChRs)oftheinsectcentralnervoussystem.

pollinator ecosystem services. They act mainly agonistically on nAChRs on the post-

synaptic membrane, mimicking the natural neurotrans-
Addresses

1EnvironmentalSciences,CopernicusInstitute,UtrechtUniversity, mitter acetylcholine by binding with high affinity [3–
Heidelberglaan 2,3584CS Utrecht,Th eNether lands 5,6(cid:3)(cid:3),7 (cid:3),8(cid:3)(cid:3)]. This in duc es a neu ronal hype r-excitat ion,
2SchoolofLife Sc ience s,U niversity ofS ussex,UK whichcanle adtot heinsec t’s deathwit hinminutes[6,9].
3Institut de sSc iencesde laCommu nic ation,CN RSUPS3088,Paris,
Some of the major metabolites of neonicotinoids are
France
4CentredeBiophysiqueMole´culaire,UPR4301CNRSaffiliatedto equally neurotoxic, acting on the same receptors [10–
Orle´ans Un iversityandto INSERM,4 5071 Orle´a nscede x02,Fra nce 12] the reby prolon ging th e e ffec tivene ss as syst emic
5INRA, UR406Ab eille s& Environn ement, Laborat oirede Tox icologie inse cticide. T he nAChR bin ding sites in th e v ertebrate

Environnementale,CS40509,Avignon,France
nervoussystemaredifferentfromthoseininsects,andin

general they have lower numbers of nicotinic receptors
Correspondingauthor:vanderSluijs,JeroenP([email protected])
withhig haffi nityto neon icotinoids ,w hichareth ereasons

that neonicotinoids show selective toxicity for insects

over vertebrates [9,13].

The main neonicotinoids presently on the market are
§This is an open-access article distributed under the terms of the imid aclopr id, thiamethox am, clothi anid in, thiaclop rid,

CreativeCommonsAttribution-NonCommercial-NoDerivativeWorks
dinotefuran, acetamiprid, nitenpyram and sulfoxaflor
License, which permits non-commercial use, distribution, and repro-
[12,14,15]. Since their introduction, neonicotinoids have
duction in any medium, provided the original author and source are
credited . grown to becom e th e most wide ly used and fa stest

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growing class of insecticides with a 2010 global market wild flowers results from systemic uptake from polluted

share of 26% of the insecticide market [16] and imida- soilandwaterorfromdirectcontaminationoftheflowers

clopridthesecondmostwidelyused(2008)agrochemical by contaminated dust from seed drilling.

in the world [17]. The worldwide production of neoni-

cotinoidsisstillincreasing[18].Large-scaleuseinEurope Attheirintroduction,neonicotinoidswereassumedtobe

and US started around 2004. Neonicotinoids are nowa- moreefficientthantheorganophosphatesandcarbamates

daysauthorisedinmorethan120countriesformorethan thattheyreplaced[37].Asaseedtreatment,theycouldbe

1000uses[19]forthetreatmentsofawiderangeofplants used in much lower quantities and they promised to be

including potato, rice, maize, sugar beets, cereals, oil less polluting to the environment. It is however not the

rapeseed, sunflower, fruit, vegetables, soy, ornamental quantity that is relevant but the potency to cause harm,

plants, tree nursery, seeds for export, and cotton. which results from toxicity,persistence and bioavailabil-

itytonon-targetspecies.Indeed,soonaftertheintroduc-

Whenusedasaseedcoating,only1.6–20%oftheamount tionofneonicotinoids,exposuretoitsresiduesinpollen,

of active substance applied actually enters the crop to nectar,sowingdustetc.,ofnon-targetpollinatinginsects

protectit[20],andtheremaining80–98.4%pollutesthe became clear. This led to various harmful effects
environ m ent with out any inten ded actio n to p lant [10,37,3 8,39(cid:3)(cid:3),4 0,41,4 2(cid:3)(cid:3),43 (cid:3)(cid:3)].

pests. Diffusion and transformation of pesticides in the
enviro nment le ad t o various envi ron mental co nc en- Ecosystem services of pollinators

trations and bioavailability, all strongly dependent on Amongst the wide diversity of pollinating species [44],

thepropertiesofthesubstance[21].Becauseoftheirhigh bees are the most important. Although bee research

leaching potential, neonicotinoids tend to contaminate mostly focuses on the domesticated Apis mellifera, over

surfacewaterandgroundwater[22–25].Owingtosorp- 25,000differentbeespecieshave been identified(FAO:

tiontoorganicmatter insoilandsediments[24,26],the Pollination; URL: http://www.fao.org/agriculture/crops/

equilibrium partitioning over soil and water varies with core-themes/theme/biodiversity/pollination/en/). Bees

soil type and is typically 1:3 (logP=0.57) [25]. In provide a vital ecosystem service, playing a key role in

countries where monitoring data are available, high the maintenance of biodiversity and in food and fibre
levels of neonico tinoid pollu tion in sur face water have pro duction [45–4 7,48 (cid:3)(cid:3),49–51]. P ollina tio n com pris es an

beenreported[27–30].IntheNetherlands,45%of9037 integrated system of interactions that links earth’s veg-

water samples taken from 801 different locations in a etation,wildlifeandhumanwelfare[52].Ofallflowering

nation-wide routine water quality monitoring scheme, plants on earth, 87.5% benefits from animal pollination

over the period 1998 and 2003–2009, exceeded the [53].Globally,87oftheleadingfoodcrops(accountingfor
13ng l(cid:2)1 imidac loprid wa ter quality standard, the 35% of the w orld f ood produc tion volum e) depend on
me dia nconcentrationb eing80 ngl(cid:2)1an dthemaxim um anim al polli nation [45]. Pollinator m ediated crops are of
concent ration found b eing 3 20 mg l(cid:2)1, wh ich is acutely key im portance in prov iding esse ntial nutr ients in t he
toxictohoney bees[2 7].In the US ,neo nicotin oi dswere hum an food sup ply [54(cid:3)].The historyo f apicultu re g oes

also found in surface water. In 108 water samples col- backtopre-agricultural times [55,56]and later co-devel-

lectedin2005fromplayawetlandsontheSouthernHigh oped with agriculture [57,58]. In addition, wild bees

Plains, thiamethoxam was found at an average concen- deliver a substantial and often unappreciated portion of
tration of 3.6mgl(cid:2)1 an d ac etamip rid at 2.2mgl (cid:2)1 [30]. pollinat io nservicest oagr icultur eandwildflowe rs[59,6 0].

Beesandapiaryproductshaveapharmacological[61,62],

Neonicotinoids and their metabolites are highly persist- scientific and technological [63], poetic [64], aesthetic

ent in soil, aquatic sediments and water. To give an (springs filled with buzzing bumblebees) culinary (e.g.,

example: Six years after a single soil drench application keeping alive traditional cuisine of patisseries with hon-
ofimidac lopr id,res iduel ev elsup to1 9mgkg (cid:2)1couldbe ey) and cultur al value.

recovered in Rhododendron shrub blossoms [31]. Clothia-
nidin has a h alf-life in soil betwe en 148–6 900 d ays [32], Global pollinator decline and emerging bee
and i mida c loprid 40 –9 97 d ays [33]. Conseque ntly, neo- disorde rs

nicotinoids exhibit a potential for accumulation in soil Long-term declines have been observed in wild bee

followingrepeatedapplications[23]andcanbetakenup populations around the world [47,65–70]. Over the past

by succeeding crops up to at least two years after appli- decades,aglobaltrendofincreasinghoneybeedisorders

cation[34].Imidaclopridhasbeendetectedin97%of33 andcolonylosseshasemerged[71–77].Wintermortality

soil samples from untreated fields on which treated corn ofentirehoneybeecolonieshasriseninmanypartsofthe
seed s were used 1 or 2 yea rs bef ore the sa mpling [34]. wo rld [7 2(cid:3),73,74,75 (cid:3)]. Whe n n eonic ot inoids were first

Concentrations in these soil samples ranged from 1.2 to used, beekeepers started describing different disorders
22mgkg(cid:2)1[34] .Se veral stud iesrecov eredneo nicot inoi ds and s igns ranging from: b ees not ret urning to the hive,
in wil d flowers n ear trea ted fiel ds [35,36(cid:3) (cid:3)]. However, it diso riente d bees, bees g ather ed c lose toget he r in small

remainsaknowledgegaptowhatextentthepresencein groups on the ground, abnormal foraging behaviour, the

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Neonicotinoids,beedisordersandpollinatorservicesvanderSluijsetal. 3

occurrenceofmassivebeelossesinspring,queenlosses, viaintakeoffood.Foodwithresiduescanbesubdivided

increasedsensitivitytodiseasesandcolonydisappearance into self-collected raw food (nectar, pollen, water, hon-

[38,40–43,77].Noneoftheseindividualsignsisaunique eydew,extrafloralnectar,guttationdroplets,variousother

effect of neonicotinoids, other causal factors or other edible substances available in the foraging area etc.), in-

agrochemicals could produce similar signs, which com- hive processed food (honey, beebread, royal jelly, wax

plicates the establishment of a causal link. etc.), and food supplied by bee keepers (high fructose

corn syrup, sugar water, sugar dough, bee candy, pollen,

Scientific research appears to indicate no single cause pollen substitutes based on soybean flower and other

explainingtheincreaseinwintercolonylosses.Allviruses vegetable protein supplements etc.).

and other pathogens that have been linked to colony

collapse have been found to be present year-round also Giventhelargenumbersofcropsinwhichneonicotinoids

in healthy colonies [78]. That colonies remain healthy are used and the large scale of use, there is a huge

despitethepresenceoftheseinfectiousagents,supports variability in space and time for each possible exposure

thetheorythatcolonycollapsemaybecausedbyfactors pathway as well as in their relative importance for the
wor kingin com binatio n.Farooq ui[7 9(cid:3)] hasan alys edthe overalle xpo sure ata gi venp laceand time.Thisis fur ther

differenthypothesesprovidedbysciencewhensearching complicated by the fact that the foraging area of a hon-

for an explanation of Colony Collapse Disorder (CCD). eybeecolonycanextendtoaradiusofupto9kmaround

Research points in the direction of a combination of the hive which is never a homogenous landscape [86].

reciprocallyenhancingcauses.Amongthose,theadvance Additionally, suburban areas have become a stronghold

of neonicotinoid insecticides has gained more weight forsomewildbeespeciesduetotheabundanceoffloral

in light of the latest independent scientific results resources in gardens and parks [87]. Thus, bees may be
[8 0,81(cid:3)(cid:3), 82(cid:3)(cid:3) ]. In the pr esent article, we synthe sise the exposed t o s ystemic inse cticide s wh ich are wide ly us ed

state of knowledge on the role of neonicotinoids in on garden flowers, vegetables, ornamental trees, and

pollinator decline and emerging bee disorders. lawns. The relative importance of exposure pathways

will also vary according to bee species as they have
Multiple ways of exposure diffe rent forag ing ranges , ph enol ogies, an d flight times

Neonicotinoidsareauthorisedforawiderangeofagricul- ina day. This can be exemplified by Osmia bees in corn

turalandhorticulturalplantsthatfloweratdifferenttimes growingareasforwhichintakeofguttationdropletsmay

of the year. The systemic properties of neonicotinoids be more important than for honeybees.

imply translocation to pollen, nectar, and guttation

droplets [34,37,83,84]. The persistency and potential Different categories of honeybees could be exposed in

contamination of wild plants and trees surrounding the differentways and to varying extents [42].For example,

treated crops [36] and the possibility for travelling far pollenforagers(whichdifferfromnectarforagers)donot

outside the fields via surface and ground water [27] and consume pollen, merely bringing it to the hive. The

the potential to contaminate wild plants and crops that pollen is consumed by nurse bees and to a lesser extent

takeuppollutedwater,meansthatpollinatinginsectsare by larvae which are thus the ones that are exposed to

likely to be exposed for much of the year to multiple residues of neonicotinoids and their metabolites [88].

sourcesofmultipleneonicotinoidsintheirforagingarea, The exposure of nectar foragers to residues of neonico-

but often at very low doses. tinoidsandmetabolitesinthenectartheygathercanvary

dependingontheresourcesavailableinthehiveenviron-

Honeybees’ exposure to neonicotinoids can occur ment.Inaddition,foragerstakesomehoneyfromthehive

through ingestion, contact and inhalation (aerosols). beforetheyleaveforforaging.Dependingonthedistance
Many po ssible expo sure pat hway s can exist [ 85(cid:3)]. Here, from t he h ive w her e they f orage, the hon eyb ees are

weaggregateexposurepathwaysinto:first,intakeoffood obliged to consume more or less of the nectar/honey

thatcontainresidues;second,nestingmaterial(resin,wax taken from the hive and/or of the nectar collected, for

etc.); third, direct contact with spray drift and dust drift energyforflyingandforaging.Theycanthereforeingest

during application; fourth, contact with contaminated more or less neonicotinoid residues, depending on the

plants, soil, water; fifth, use ofcoolingwater inthe hive; foragingenvironment[42].Oraluptakeisestimatedtobe

and sixth, inhalation of contaminated air. For bumble highest for forager honeybees, winter honeybees and

bees and other wild bees that nest in soil, contact with larvae [85].

contaminated soil is an additional pathway of concern.

Leafcutterbeesusecutleaffragmentstoformnestcells Littleisknownabouttherealexposuretocontaminated

andcanthusbeexposedtoresiduesinleaves.Thereare food for different categories of honeybees in a colony,

many other conceivable exposure routes, for instance, a eitherintermsofcontactwithpollenorcontactwith,and

bee hive could have been made from timber from trees possibleconsumptionof,nectarifneeded.Forwildbees

treated with neonicotinoids and may thus contain resi- veryfewdataexistonexposureinthefield.Theamount

dues.However,thebestresearchedexposurepathwayis thatwildbeesactuallyconsumeinthefieldhasnotbeen

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measured.EFSAestimatedthatworkerbees,queensand have high acute toxicity to all other bee species so far

larvae of bumblebees and adult females and larvae of tested, including various Bombus species, Osmia lignaria

solitarybeesarelikelytohavethehighestoraluptakeof and Megachile rotundata [99–102]. O. lignaria is more

residues [85]. sensitive to both clothianidin and imidacloprid than is

B. impatiens, with M. rotundata more sensitive still [100].

In2002,69%ofpollensamplescollectedbyhoneybeesat Inanacutetoxicitytestundersemifieldconditionsonthe

variousplacesinFrancecontainedresiduesofimidacloprid Indian honeybee Apis cerana indica, clothianidin showed

anditsmetabolites[89].Inasystematicsamplingscheme the highest toxicity, followed by imidacloprid and thia-

covering5locationsover3years,imidaclopridwasfoundin methoxam [103].

40.5% of the pollen samples and in 21.8% of the honey

samples [90,91]. On the basis of data from authorisation For mass-dying of bees in spring nearby and during

authorities,neonicotinoidresiduesinnectarandpollenof sowing of corn seeds coated with neonicotinoids there

treatedcropplantsareestimatedtobeintherangeofbelow nowisaonetooneprovencausallinkwithacuteintoxi-
analytic al de tectio n li mit (0.3m gk g(cid:2) 1) to 5.4mg k g(cid:2)1 in catio n th oug h cont act with the d ust cloud arou nd the

nectar,thehighestvaluecorrespondingtoclothianidinin pneumatic sowing machines during foraging flights to

oilseed rape nectar, and a range of below detection limit adjacent forests (providing honeydew) or nearby flower-
(0.3mg kg(cid:2)1 ) to 51 mgk g(cid:2) 1 in p ol len, the highest value ing field s [104 (cid:3)(cid:3),105–109] . Such ma ss colony losses

corresponding to thiamethoxam in alfalfa pollen [85]. A during corn sowing have also been documented in
recent review r eports wider r an ges fo r polle n: 0. 2– Italy, G erma ny, Aus tria a nd Sl ovenia [110,111,104 (cid:3)(cid:3)].
912mg kg(cid:2)1for imidaclo pridan d1.0–11 5mg kg(cid:2)1fo rthia- In res ponse to th e incide nts, the adher ence of the seed

cloprid [92]. Residues of imidacloprid, dinotefuran, and coating has been improved owing to better regulations,

thiamethoxam plus metabolites in pumpkin treated with andanimproved sowing-techniquehasrecentlybecome

United States label rates reach average levels up to compulsory throughout Europe, [112]. Despite the
122mg kg(cid:2)1 in polle n and 17.6m gkg(cid:2)1 i n necta r [9 3]. deployment of air deflec tors in th e drillin g machin es or
Up to 346mg l(cid:2)1 for imid aclop rid and 14 6mgl(cid:2) 1 for improved se ed co ating tech niq ues , emissi ons are s till
thia me thox ama nd102 mgl(cid:2)1clothia nidin and hav ebeen substantia l and the dus t cloud is st ill acutely tox ic to

foundinguttationdropsfromleavesofplantsgerminated bees [105,109,111,113–115]. Acute lethal effects of neo-

fromneonicotinoid-coatedseeds[84,94].Inmelon,gutta- nicotinoidsdispersedasparticulatematterintheairseem
tionl evelsupto4.1mgl(cid:2)1 imidac lopridw ere found 3days to be prom oted by h igh environm ental h um idit y w hich

afteratop(US)labelratesoilapplication[95].InaUSwide accelerates mortality [105]. Honeybees also bring the

survey of pesticide residues in beeswax, pollen and hon- toxic dust particles they gather on their body into the

eybeesduringthe2007–2008growingseasons,highlevels hive[106].Sunnyandwarmdaysalsoseemtofavourthe

ofneonicotinoidswerefoundinpollen(includedin[92]) dispersal of active substances [35].
bu timidaclopridw asal sofoun du pto13 .6mgkg(cid:2) 1in wax

[96]. In Spain, neonicotinoids were found in beeswax Lethal effects from chronic exposure refer to honeybee

samples from apiaries near fruit orchards: 11 out of 30 mortalitythatoccursafterprolongedexposure.Incontrast
samples tested positive in r anges from 11m gk g(cid:2)1 (ac et- toacutel ethal effect s,the rearenost andardise dp rotocols
amiprid) to153 mgkg(cid:2)1 (t hiaclop rid)[9 7]. fo r mea suring chron ic le thal e ffects. Ther efore, in

traditional risk assessment of pesticides they are usually

Little is known on the presence of neonicotinoids in expressedinthreeways:LD50:thedoseatwhich50%of

honeydew. Given differences in life span of aphids and theexposedhoneybeesdie(often,butnotalways,within

bees, concentrations in plant sap too low to kill aphids 10 days); NOEC (No Observed Effect Concentration):

could translocate to honeydew and could still produce the highest concentration of imidacloprid producing no

sublethal effects and chronic toxicity mortality in bees observed effect; and LOEC (Lowest Observed Effect

and bee colonies. Concentration):thelowestconcentrationofimidacloprid

producing an observed effect. However, for neonicoti-
Acute and chronic effects of lethal and noids and its neurotoxic metab olites, leth al t oxicity can
sublet hal e xposure increa se u p to 100,000 ti mes compare d to a cute toxi city

Pesticides can produce four types of effects on honey- when the exposure is extended in time [10]. There has

bees: lethal effects and sublethal effects from acute or been some controversy on the findings of that study,

chronic exposures. whichisdiscussedindetailbyMaximandVanderSluijs

[40,42]. However, the key finding that exposure time

Acute toxicity is expressed as the lethal dose (LD) at amplifiesthetoxicityofneonicotinoidsisconsistentwith

which50%oftheexposedhoneybeesdiewithin48hours: later findings. Micro-colonies of bumblebees fed with

abbreviated to ‘LD50 (48hours)’. Neonicotinoids are imidacloprid showed the same phenomenon [102]: at

highly toxic (in the range of ng/bee) to honeybees [98], one tenth of the concentration of the toxin in feed,

bothwhenadministeredorallyandbycontact.Theyalso it took twice as long to produce 100% mortality in a

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bumblebee microcolony. At a 100 times lower dose, it level, population level and community level impacts on

tookca.fourtimeslongertoproduce100%mortality.The pollinators.

measurable shortening of the life span ceases to occur
only when a dose w as adm inist ered, for w hic h the At field realistic concentrations (1mgl(cid:2)1) imidacloprid

(extrapolated)chronicintoxicationtimewouldbelonger repels pollinating beetles while at concentrations well
than the natur al life s pan of a wor ker b umble bee . This below theanalytic aldetect ionlim it( 0.01mgl(cid:2)1)itr epels

implies that the standard 10 day chronic toxicity test for pollinating flies [125]. This implies that imidacloprid

bees is far too short for testing neonicotinoids. Indeed, pollutionmaydisruptpollinationbothinpollutednature

honeybees fed with one tenth of the LC50 of thia- andinagriculturallands.Onhoneybees,imidaclopridhas

methoxam showed a 41.2% reduction of life span [116]. norepellingeffectatfieldrealisticconcentrations:itstarts
Recent stu dies hav e shown that chron ic toxi city o f neo- be ingrepell entat 50 0mg l(cid:2)1[126] .Insomeplant pr otec-

nicotinoidscanmoreadequatelybeexpressedbytimeto tion formulations, neonicotinoids are mixed with bee

50% mortality instead of by the 10 day LD50 [117– repellents. However, the persistence of neonicotinoids
120,1 21(cid:3),122].T hereis ali near rela tion betw eenlo gdaily exceedsth atofthere pelle nceandthe irs ystemicproper-
dose and log time t o 50 % mo rtality [ 118,120,1 21(cid:3) ]. In ties diffe r. B es ides , if bees ar e ef fectiv ely repel led and

experiments with honeybee colonies, similar long term avoid the contaminated flowers, pollination is disrupted

chronic effects have indeed been found with typical because plants are not visited by bees.

times of 14–23 weeks to collapse 25–100% of the

colonies exposed to imidacloprid-contaminated food at Sublethal doses of neonicotinoids impair the olfactory
20mgkg (cid:2)1 [123] and 80–120 days for 1mgkg(cid:2)1 dino te- memory a nd lea rni ng capacity of honeyb ees [127,128,
fur an and400mg kg(cid:2) 1clothia nidin [76 ]. No tethatthese 129(cid:3),130 ] an d the o rientation a nd foraging activity

studies used concentrations that are on the high end of [131]. The impact of sublethal exposure on the flying

the currently reported ranges of concentrations found in behaviour and navigation capacity has been shown

thefield.However,suchdataaresparseandlimitedtoa through homing flight tests [82,126,132,133]. Exposed
few crops , so it can not y et b e co nclude d w hether s uc h to a ver y low co ncentr ation (0.05mgkg(cid:2)1) imi dacloprid

concentrations are rare or common in the field. honeybees show an initial slight increase in travel dis-

tance.However,withincreasingconcentration,startingat
Atlowconcentrationsofneonicotinoids,sublethaleffects 0.5mg kg(cid:2)1imid aclop riddecreas esdistancetra velledan d

canoccur.Sublethaleffectsinvolvemodificationsofhon- interaction time between bees, while time in the food
eyb ee beh aviour and physi ology (e .g., immune s yst em). zone incre ases w ith conc entrati on [13 4(cid:3)]. I mi dacl oprid

Theydonotdirectlycausethedeathoftheindividualor disrupts honeybee waggle dancing and sucrose respon-
theco llap seo ftheco lonyb utm aybe co mel ethalintim e siveness at doses o f 0.21 an d 2.16n gbe e(cid:2)1 [135 ].

and/or may make the colony more sensitive (e.g., more

pronetodiseases),whichmaycontributetoitscollapse.For If honeybee brood is reared at suboptimal temperatures

instance,anindividualwithmemory,orientationorphys- (thenumberofadultbeesisnotsufficienttomaintainthe

iologicalimpairmentsmightfailtoreturntoitshive,dying optimal temperature level), the new workers will be

from hunger or cold. This would not be detected in characterised by reduced longevity and increased

standard pesticide tests, which focus on acute mortality. susceptibility to pesticides (bee-level effect) [136]. This

A distinction can be made between acute and chronic willagainresultinanumberofadultbeesinsufficientto

sublethal effects. Acute sublethal effects are assessed by maintain the brood at the optimal temperature, which

exposingbeesonlyoncetothesubstance(byingestionor maythenleadtochroniccolonyweakeninguntilcollapse

by contact), and observing them for some time (variable (colony-level effect).

from one laboratory to another, from several minutes to

fourdays).Chronicsublethaleffectsareassessedbyexpos- Sublethal effects seem to be detected more frequently

inghoneybeesmorethanoncetoneonicotinoidsduringan and at lower concentrations when bumblebees (Bombus

extendedperiodoftime(e.g.,every24hours,for10days). terrestris) have to travel to gather food, even when the

Bothacuteandchronicsublethaleffectsareexpressedas distancesaretiny.Noobservableimpactsofimidacloprid

NOEC and/or LOEC (No or Lowest Observable Effect at field realistic concentrations on micro-colonies of B.

Concentration,respectively)[42]. terrestris provided with food in the nest were found, but

when workers had to walk just 20cm down a tube to

In an extensive review Desneux et al. found that sub- gather food, they exhibited significant sublethal effects

lethaleffectsofneonicotinoidsexistonneurophysiology, on foraging activity, with a median sublethal effect con-
larval develo pm ent, moulting , adu lt l ongevity, immu- cen tration ( EC ) o f 3.7 m gkg(cid:2)1 [102]. In queen right
50

nology, fecundity, sex ratio, mobility, navigation and bumblebeecolonies foraging in aglasshousewhere food
orientat ion, feedin g be havio ur, ovipos ition behav iour, was3mawa yfromth eirnest, 20 m gkg(cid:2)1ofi midaclo prid

and learning [124]. All these effects have been reported caused significant worker mortality, with bees dying at

forpollinatorsandallhavethepotentialtoproducecolony the feeder. Significant mortality was also observed at

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10mgkg(cid:2)1, but not at 2mgkg(cid:2)1 [102]. Bumblebees performances of colonies after experimental exposure do

exhibit concentration-dependent sublethal responses not last long enough [85]. Major weaknesses of existing

(declining feeding rate) to imidacloprid starting at field studies are the small size of the colonies, the very
1mgl(cid:2)1 in syrup, w hile h one ybees seemed unaffec ted smal ldistanc ebe twe enthe hive sa ndth etreated field and

[137]. theverylowsurfaceofthetestfield.Asaconsequenceof

these weaknesses, the real exposures of the honey bees

Field-relevantconcentrationsofimidacloprid,usedalone during these field tests are highly uncertain and may in

or in mixture with l-cyhalothrin, were shown to impair reality be much smaller than what has been assumed in
po lle n foragin g effi ciency in bum blebee colon ies [138(cid:3)]. thesefi eld studi es.[85]

In an attempt to fulfill colony needs for pollen, more
wo rke rswerer ecr uitedt oforage instead of takingc areof In addition, the meta-analysis [146(cid:3)] demonstrates that

brood. This seemed to affect brood development result- field tests published until now on which European and
ing in redu ced wor ke r prod uction [138(cid:3)]. Bum blebee Nort h Am erican aut horiza tions are based , lack the sta-

colonies have been exposed to field realistic levels of tistical power required to detect the reduction in colony
imidaclo prid( 0.7mg kg(cid:2)1inn ec tar, 6 mgkg(cid:2)1 inpolle n) perform ance p redicted fro m the dos e–response re lation-

for two weeks in the laboratory. When subsequently ship derived from that meta-analysis. For this purpose,

placedbackinthefieldandallowedtodevelopnaturally the tests were wrongly designed, there were too few

for the following six weeks, treated colonies showed an colonies in each test group, and the follow up time

85% reduction in queen production and a significantly monitoring the long term colony level impacts were too
redu cedgrowth ra te[81(cid:3)(cid:3) ].Effectson bum b lebeerepro- short to de tect man y of the ef fects describe d abo ve.

duction occur at imidacloprid concentrations as low as Nonetheless, these field studies have been the basis
1mgl(cid:2)1 [139(cid:3) ] w hich is highly field-realistic. forgrantingth epres entm arketaut horiza tionsb yna tional

and European safety agencies. The meta-analyses com-

Ithasalsobeenshownthatpesticideslikeimidaclopridact bined data from 14 previous studies, and subsequently

on the hypopharyngeal glands of honeybee nurses by demonstrated that, at exposure to field realistic doses,
de gene rating the tissues [140,1 41,1 42(cid:3)(cid:3)], whi ch indu ces imidaclopridd oesh ave significan tsu bleth aleffect s,even

ashiftfromnesttofieldactivities.Inthenativestingless atauthorisedlevelsofuse,impairsperformanceandthus
b ee M elipo na q ua drifas ciata anth idi oide s, imid acloprid we akens hon eybee co lonie s [146(cid:3)] .

causes impairment of the mushroom bodies which are

involved in learning [143]. Imidacloprid and clothianidin Afurtherlimitationoffieldstudiesistheirlimitedrepro-

have been shown to be potent neuromodulators of the ducibility due to the high variability in environmental

honeybeebrain,causingmushroombodyneuronalinacti- conditions in the foraging area of honeybees, which

vationinhoneybees,whichaffecthoneybeecognitionand extendsuptoa9kmradiusaroundthehive.Observations

behaviouratconcentrationsthatareencounteredbyfora- made in a particular field experiment might not be

ginghoneybeesandwithinthehive[8].Sublethaldosesof representative of the range of effects that could occur

imidaclopridwerealsofoundtohavecytotoxicactivityin inrealconditions.Owingtothelargevariabilityoffactors

the Malpighian tubules in honeybees that make up the that cannot be controlled (e.g. other stressors, soil struc-

excretory and osmoregulatory system [144]. Exposure to ture, climate, combination of plants attractive to bees

thiamethoxam has also been shown to result in morpho- etc.), current field experiments only give information

logicalimpairmentofthebeebrainandbeemidgut[116]. about the particular situation in which they were done.

Exposure to neonicotinoid residues leads to a delayed The challenges of field studies became also clear in the

development of honeybee larvae, notably in the early debates over the highly contested field study recently

stages (day 4 to day 8) [145]. This can favour the de- conductedbytheFoodandEnvironmentResearchAgen-

velopment of the Varroa destructor parasitic mite within cy (FERA) which resorts under the UK Department for

thecolony.Likewise,thelifespanofadultbeesemerging Environment, Food and Rural Affairs (DEFRA). This

from the exposed brood proved to be shorter. studywassetupinresponsetotheSciencepublicationthat

showedthatashorttermexposureofbumblebeestofield

Short-termandmid-termsublethaleffectsonindividuals realistic imidacloprid concentrations causes a long term
oragegroup sre sultinlong -termeffe ctsatth ec olonylevel, 85%red uctioninque enproduction[ 81(cid:3)(cid:3)].A t three sites

whichfollowweekstomonthsaftertheexposure,suchas 20bumblebeecolonieswereexposedtocropsgrownfrom

honeybee colony depopulation and bumblebee colony untreated, clothianidin-treated or imidacloprid-treated
queen pro duction [76,81(cid:3)(cid:3),123,1 38(cid:3)] . As it has r ecently seeds. The agency concluded tha t ‘no clear consistent

beenacknowledged,thefieldtestsonwhichthemarketing relationships’ between pesticide levels and harm to the

authorisation of the use of neonicotinoids is essentially insects could be found [FERA: URL: http://www.fera.

based were not developed to detect sublethal nor long- defra.gov.uk/scienceResearch/scienceCapabilities/che-

termeffectsonthecolonylevel,andtheobservationofthe micalsEnvironment/documents/reportPS2371V4a.pdf].

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Neonicotinoids,beedisordersandpollinatorservicesvanderSluijsetal. 7

However, it turned out that the control colonies them- the subject of patents by agrochemical companies

selves were contaminated with the pesticides tested [152,153].

[147]. Further, thiamethoxam was detected in two out

of the three bee groups tested, even though it was not Synergy has also been demonstrated for neonicotinoids

used in the experiment. The major studies that have andinfectiousagents.Prolongedexposuretoanon-lethal

measured neonicotinoid residues in pollen collected by doseofneonicotinoidsrendersbeehivesmoresusceptible
honeybee sclearlyshow that neon ico tinoids are found in topa ras itessuchasNo semacera naeinfec tions [39(cid:3)(cid:3),154(cid:3)(cid:3),
pollenallo verthe yeara ndin allstudiedregi ons ,noton ly 15 5(cid:3),156].T hisc an beexpla inedei therbyan alterationof

afterthesowingorduringthefloweringperiod[89,91,96]. theimmunesystemorbyanimpairmentofgroomingand

With the present scale of use, it will be very difficult to allogrooming that leads to reduced hygiene at the indi-

find a control site where bees cannot come into contact vidual level and in the nest, which gives the pathogens

with neonicotinoids. more chances to infect the bees. The same mechanism,

where the balance between an insect and its natural

Given all the major limitations to the reliability of out- enemies is disturbed by sublethal exposures to neonico-

comesoffieldstudies,itisrecommendabletogivemore tinoids that impairs grooming, is well known and often

weightintheriskassessmenttoreproducibleresultsfrom used in pest management of target insects [157–161].

controlled lab studies and use the ratio between the
environme ntal concent ratio n an d th e no e ffect con cen- Conclusion and prospects

trationasthemainriskindicator[40,42].Itcouldperhaps In less than 20 years, neonicotinoids have become the

be linked to modelling to explore how, and to what the mostwidelyusedclassofinsecticides.Beingusedinmore

degree,thevariouswell-knownsublethaleffectsonindi- than120countriesinmorethan1000differentcropsand

vidual bees can weaken the colony [148]. applications,theynowaccountforatleastonequarterof

the world insecticide market. For pollinators, this has

A key aspect in honeybee biology is that the colony transformedtheagrochemicallandscape tooneinwhich

behavesasa‘superorganism’[149].Inacolony,sufficient mostfloweringcropsandanunknownproportionofwild

membership,sothatthenumberoforganismsinvolvedin flowers contain varying concentrations of neonicotinoids

the various tasks to maintain that colony, is critical, not intheirpollenandnectar.Mostneonicotinoidsarehighly

theindividualqualityofataskperformedbyanindividual persistentinsoil,waterandsedimentsandtheyaccumu-

bee. Varying between winter and summer, the 10,000– late in soil after repeated uses. Severe surface water

60,000honeybeesthattypicallyformacolonyfunctionas pollutionwithneonicotinoidsiscommon.Theirsystemic

a cooperative unit, maintaining intraorganismic homeo- modeofactioninsideplantsmeansphloemicandxylemic

stasisaswellasfoodstorage,nesthygienic,defenceofthe transportthatresultsintranslocationtopollenandnectar.

hive,rearingofbroodetc.Hence,sublethaleffectsaffect- Theirwideapplication,persistenceinsoilandwaterand

ingthenumberofindividualsthatperformspecificfunc- potentialforuptakebysucceedingcropsandwildplants

tions,caninfluencethefunctioningofthewholecolony. make neonicotinoids bioavailable to pollinators in sub-

In a simplified theoretical modelling approach, colony lethalconcentrationsformostoftheyear.Thisresultsin

failurecanbeunderstoodintermsofobservedprinciples the frequent presence of neonicotinoids in honeybee

of honeybee population dynamics [150]. A colony simu- hives.Neonicotinoidsarehighlyneurotoxictohoneybees

lation model predicts a critical threshold forager death and wild pollinators. Their capacity to cross the ion-

rate above which rapid population decline is predicted impermeable barrier surrounding the central nervous
and colony failure is ine vitable.Hig h forage rd eathrates system (BBB , blood– brain barrier) [7(cid:3)] and the ir strong

draw hive bees towards the foraging population at much bindingtonAChRinthebee’scentralnervoussystemare

youngeragesthannormal,whichactstoacceleratecolony responsible for a unique chronic and sublethal toxicity

failure [150]. profile. Neonicotinoid toxicity is reinforced by exposure
time. S ome studies indicate a non-mono ton ic [162(cid:3)]
Synergistic effects: pesticide–pesticide and dose– respon se curve at doses far below the LD50 . Mass
pesticide–in fectious agents bee dying even ts in spr ing fro m acute i ntox ication have

A synergy occurs when the effect of a combination of occurred in Germany, Italy, Slovenia and France during

stressors is higher than the sum of the effect of each pneumatic sowing of corn seeds coated with neonicoti-

stressor alone. When neonicotinoids are combined with noids.Beesthatforagenearcornfieldsduringsowingget

certainfungicides(azoles,suchasprochloraz,oranilides, exposedtoacutelethaldoseswhencrossingthetoxicdust

such as metalaxyl) or other agrochemicals that block cloud created by the sowing machine.

cytochrome P450 detoxification enzymes, their toxicity

increases by factor from 1.52 to 1141 depending on the Atfieldrealisticexposurelevels,neonicotinoidsproduce

combination[151,152].Thestrongestsynergismhasbeen a wide range of adverse sublethal effects in honeybee

foundfortriflumizolemakingthiacloprid1141timesmore colonies and bumblebee colonies, affecting colony per-

acutelytoxictohoneybees[151].Thissynergisticeffectis formancethroughimpairmentofforaging success,brood

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andlarvaldevelopment,memoryandlearning,damageto 6. BelzuncesLP,TchamitchianS,BrunetJL:Neuraleffectsof
(cid:3)(cid:3) insecticide sin thehoneyb ee .Apido logie 2012, 43:348-3 70.
the central nervous system, susceptibility to diseases, Excellent review o f neur al impa cts o f field expo sure of honeybees to
hive hygien eetc.Ne onicotino idssynergistic ally reinforce sublethal residue so fneuro toxicinse cti cides inpollena nd nectar.The se
impair:fir stlycogn itiv efunctions ,includingl ea rninga ndm emory ,habi-
infectiousagentssuchasN.ceranaeandexhibitsynergistic tuation , olfac tion and gustation, navigatio n and o rienta tion; sec ondly
toxicity w ith oth er ag ro che micals . Th e large impact of behavio ur,includi ngfo ragingand thirdlyphy siolog icalfunction s,includ-
ingthermo regulation andmus cle activity .Timeisake yfactorin insecti-
shorttermfieldrealisticexposureofbumblebeecolonies cid etoxicity.Combin ation toxicity ofjointe xpos ur et om ultiple pe sticides
on l ong term bumbl ebee que en productio n (85% urge ntlyrequ iresattention .

reduction)couldbeakeyfactorcontributingtotheglobal
7. TomizawaM:Chemicalbiologyofthenicotinicinsecticide
trendsofb umble be e decl ine.O nlyafewstud ie sas sessed (cid:3) receptor. Adv InsectPh ysiol201 3, 44:6 3-99.
Introduction in to th e mol ecular b asis o f binding site interaction and
the toxicity to other wild pollinators, but the available explanation of d iffere nt binding affinit y o f neonic otino ids with in sect
data suggest th atthey arel ikelytoexhi bits imila rtoxicity and vertebr ate nicotinic acetyl choline re ceptor. Another key factor
expl ainingtheh ighinsec ttoxicit yisitsc apacity(st emmingf rom hydro-
ntoe aolnl iwcoiltdin ionisdescti psoslltiinllationrcsr.e Tashien gw.oIrlndwviidewe porofdtuhcetiovnit oafl ipnhsoebcitcniteyr) v otou s pseynset termat.e t he ion-i mp er meable b arrier surr oundi ng the

importance of the service insect pollinators provide to
8. PalmerMJ,MoffatC,SaranzewaN,HarveyJ,WrightGA,
bothnatura lec osys temsan dfarmi ng,theyreq uireahi gh (cid:3)(cid:3) Connol lyCN :Chol ine rgicpestic ide scause m ushro ombody
neurona linac tivationinh oneybees. NatCo mmun2013, 4:1634
level of protection. Therefore a transition to pollinator- http://dx.d oi.org/10.10 38 /ncomms264 8.

friendlyalternativestoneonicotinoidsisurgentlyneeded UsingrecordingsfrommushroombodyKenyoncellsinacutelyisolated
for the s ake of the s us tainability of po ll inator eco system honey bee brain, it is shown that the n eonicoti noids im idaclop rid and
clothianidi n,and th eo rganop hosp hate miticidecouma phosoxon,c ause
services.TherecentdecisionbytheEuropeanCommis- adepolariza tion- bloc kofneuronalfirin gandin hibitnicotinic respo nses.
sion to temp orary b an the use of imidaclop rid, thia- T heseeffectsareobse rv edatcon centr ation sthat areenco unteredby
foragin ghone ybee sandwith in thehive,andar ead ditiv ewithcombin ed
methoxam and clothianidin in crops attractive to bees applicati on.Exposu reto multip lep estic ides tha ttargetc holin ergicsig-
is a first ste p in that directio n [ 163]. nallingwillc auseenha nc edtoxici tytopollin ators .

9. TomizawaM,CasidaJE:Neonicotinoidinsecticidetoxicology:
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2005,45:247 -26 8.
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Task ForceonS ystemicP esticid es duringitsp len ary meetin gsinBath 10. SuchailS,GuezD,BelzuncesLP:Discrepancybetweenacute
(2011 ),Cam bri dge(2012 ),Padua(2 012)an dL ouvain-l a-Neuve( 20 13).Part andch ron ictox ici tyinduced by imidacloprid andits
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j.cosus t.201 3.05 .007