EvaluationofHoneybeeDeclinesinNorthAmericaandEurope

MatthewYoung

EnvironmentalStudies190

May17,2017

2

TableofContents

4 Abstract

5 Introduction

6 BiologyoftheWesternHoneybee

8 HistoryofColonyCollapseDisorder

8 SymptomsofColonyCollapseDisorder

10 ContributingFactors:Mites

10 Varroadestructor

12 Acarapiswoodii

13 Fungi

13 Nosemaapis

14 Acosphaeraapis

15 Aspergillus

15 LossofHabitatDuetoAnthropogenicDevelopment

16 BeekeepingPractices

17 ClimateChange

18 Pesticides

20 GovernmentAction

24 Recommendations

27 Conclusion

29 Figure1

30 Figure2

3

31 Figure3

32 Figure4

33 Figure5

34 Table1

35 Table2

36 WorksCited

4

Abstract

ThenumberofhoneybeecoloniesinNorthAmericaandEuropehasbeensteadily

decliningsincethelate1940’s.In2006,beekeepersnotedasignificantincreaseinthe

numberofhivesthatdidnotsurvivethepollinatingseason.Thisphenomenonwasnamed

colonycollapsedisorder,andcaseshavebeencontinuingtooccurtothepresentday.

Thecollapseofahoneybeecolonyhasbeenattributedtothesynergisticeffectsof

multipleenvironmentalfactorsworkinginconjunctiontodecreasethe

immunosuppressionofaffectedhives.Damagingfactorsincludemultiplespeciesof

parasiticmitesandfungi,lossofforagehabitatduetoanthropogenicdevelopment,

changingbeekeepingpractices,achangingclimate,andpesticides.

ThegovernmentsofmultiplecountriesinbothNorthAmericaandEuropehave

enactedlegislationwithvaryingdegreesofsuccesstoreducetheamountofdamage

occurringtohoneybeecolonies.However,thelegislationthathasbeenenactedisnot

enoughtosignificantlyreducethenumberofcasesofcolonycollapse,andmorefunding

andresearchisneededtolearnmoreabouttheissue.

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Introduction

TheWesternHoneybee(Apismellifera)isthemostcommonhoneybeespecies

worldwide,andisresponsibleforthevastmajorityofcommercialpollinationoccurringin

NorthAmericaandEurope(UNEP,2010).Beginningin2006,NorthAmericanand

Europeancommercialandhobbyistbeekeepersnotedasubstantialincreaseinhoneybee

hivelosses(Kaplan,2012).

Hivelossoccurswhentheworkerbeesdisappear,leavingbehindthequeen,nurse

bees,andplentyoffoodstillpresentinthehives.Withoutworkers,thequeendiesandthe

hiveislost.Hivelossisanaturalprocess,buttherateatwhichithasbeenoccurringis

unprecedented(Goulson&Hughes,2015).Iftheselossescontinue,agriculturalproduction

andnaturalpollinationprocesseswillbeseverelyaffected.Thephenomenonwasnamed

“colonycollapsedisorder”,andreportedcaseshavebeencontinuingtooccuratan

alarmingrate(UNEP,2010).

TheUnitedStatesDepartmentofAgriculturehasattributedcolonycollapsedisorder

tothesynergisticeffectofmultiplefactors(USDA,2012).Mitesandfungiinfecthivesand

causeimmunodeficiencyinthebees,lossofforageflowerhabitatcausedbyanthropogenic

overdevelopmentpreventsbeesfromgettingadequatenutrition,commercialbeekeeping

practicesresultinincreasedstresslevels,andevensmalldosesofpesticidesusedin

agricultureaffectbeememoryandflight(Henryetal.,2012).

DespitetheUnitedStatesgovernment’snumerousstudiesandreports,itisstilla

mysteryastowhatmixandpotencyoffactorscausecoloniestocollapse(USDA,2012).

TheUnitedStatesgovernmentandtheEuropeanUnionhavebothrecognizedtheproblem,

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andlegislativeactionhasbeentaken,butincidencesarestilloccurringandthestepsbeing

takenarenotenough.

Thispaperwillorganizeandcompileinformationpertainingtothedeclinein

populationofNorthAmericanandEuropeanhoneybeesbysearchingthroughgovernment

documents,andpeerreviewedarticles.Allofthepertinentdataisorganizedintoasingle

report,whichsynthesizestheavailableinformationandidentifiesstepsthatcanbetaken

toreduceoccurrencesofcolonycollapsedisorder.

BiologyoftheWesternHoneybee

TheWesternHoneybee(Apismellifera)isacolonialinsectpresentonevery

continentwiththeexceptionofAntarctica.ItisnativetoEurope,westernAsia,andAfrica.

Itisthemostcommonofallhoneybeespeciesworldwideandisusedfortheproductionof

honey,beeswax,andforagriculturalpollination(UNEP,2010).Honeybeesliveinhives

withasinglefertilequeenproducingeggs,asmallnumberofmaledronesusedfor

fertilization,andhundredsorthousandsofsterilefemaleworkersthatgatherfoodand

performotherdutiessuchascleaningthehiveandcaringforthebrood(Williamsetal.,

2010).

Theaveragelifespanforaqueenisapproximatelyfouryears,whileworkerbees’

lifespansvaryconsiderablydependingonwhatseasontheywerebornin.Duringthe

springandsummertime,aworker’slifeaveragesafewweeksduetothehardworkit

performs.Duringthewintermonthswhenbeesremaininthehive,workerscansurvive

forseveralmonths.Onaveragethroughouttheyear,approximatelyonepercentofthe

hive’sthousandsofworkerbeesnaturallydieeachday(Kaplan,J&K,2012).

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Beescommunicatethroughdanceandpheromones(Williamsonetal.,2013).With

theirdances,theycanrelayinformationaboutthedistanceanddirectionoffoodtoother

workerbees,andusingpheromones,theycancommunicateaboutregulatinghive

activities,mating,raisingthealarm,friendorfoerecognition,anddefenseofthehive

(Santosetal.,2016).

Honeybeesstayinsidetheirhivesduringthewintertime.Inpreparationfor

springtime,thequeenbeginslayingeggsinmidtolatewinter.Theeggshatchintolarvae,

whicharecaredforandfedbyspecializedworkersknownasnursebees(Seeley&Smith,

2015).Alllarvaeeatroyaljellyforthefirstthreedaysoftheirlarvalstage,whichis

secretedfromglandsintheworkerbees’hypopharynx.Afterthreedaysofroyaljelly,

workersareswitchedtoadietofpollenandnectar.Larvaedestinedtobecomenew

queenscontinuetobefedroyaljellyfortheremainderoftheirlarvalstage.Thehivemust

bekeptataconstant93degreesFahrenheittoensureproperdevelopment.Theheatis

generatedbythebeesthemselves.Thelarvaearesealedintheircellsafteraweekand

entertheirpupalstage.Inanotherweek,theygrowintoadultbees.

Thenewlytransformedadultbeesstayinsidethehiveandhelpfeedthelarvaefor

theirfirsttendays.Afterthat,theybeginbuildingcombcells,andondayssixteenthrough

twentyofadulthood,theyworkatstoringnectarandpollenforthehive.Afterdaytwenty,

thematureworkerbeeexitsthehiveandspendstherestofitslifeforagingforpollenand

nectar.

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HistoryofColonyCollapseDisorder

Commercialandhobbyisthoneybeehiveshavebeendeclininginnumbersincethe

late1940’s.In1947,theUnitedStateshad5.6millionhives.By1980thatnumberhad

decreasedto4.3million,andin2007,thenumberofhivespresentintheUnitedStateshad

plummetedto2.4million(Figure1);(VanEngelsdorpetal.,2008).HivelossintheUnited

Statesvariessignificantlybystatewithuptofiftysixpercentoftotalcolonieslost(Figure

2);(Vanengensdorpetal.,2008).Thelossofhiveshashadmanynamesovertheyears

includingdisappearingdisease,springdwindle,Maydisease,autumndisease,falldwindle

disease,spontaneoushivecollapse,andMaryCelestesyndrome(UNEP,2010).Thenames

ofhivelosseswereallbroughtunderonemonikerin2006afteradrasticriseinthe

numberofincidences.Hivelosseswerenotedtobemoresignificantinthewintertime

(Figure3);(VanEngelsdorpetal.,2008)andwerenottheresultofasinglediseaseorfactor.

ThesuddendeathofahivewasnamedColonyCollapseDisorder.

SymptomsofColonyCollapseDisorder

IncasesofColonyCollapseDisorder,thequeenisleftbehindinthehivealongwith

immatureworkersandnursebees(USDA,2012).Ifthequeenisnotpresent,thehive’s

deathoccurredduetolackofaqueen,anditisnotconsideredacaseofcolonycollapse

disorder.Incasesofcolonycollapsedisorder,thecappedbrood,whichincludesembryos,

eggs,larvae,andpupae,areallstillpresentinthehive,alongwithampleamountsofhoney

andpollen.Thematureworkerbees;however,areallgoneandthereisanoticeable

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absenceofbeecorpsesinsideorneartheentrancetothehive.Withoutherworkers,the

queeninevitablydies,andthehivecollapses(Williamsetal.,2010).

Someothertelltalesymptomsthatmayoccurbeforeacolonycollapseincludean

inadequatenumberofworkerstomaintainthebroodpresentinthehive,andamajorityof

youngbeesintheworkforce.Human-tendedbeesalsobecomehesitanttoeatprovided

foodsuchassugarsyrup,orproteinsupplements(Goulson&Nicholls,2016).Another

symptomariseswhenanaffectedhiveiscomparedtoahealthyhive’sinhabitants.Higher

loadsofpathogenshavebeenfoundinthegutsofbeesfromhivessufferingfromcolony

collapsedisorder(Schwarzetal.,2016).

Colonycollapsedisordershouldnotbemistakenforswarming,anaturaland

expectedphenomenoninthehoneybeehive’slifecycle(Williamsetal.,2010).Swarmsare

triggeredwhenthecellsinthehivearefilledwithhoney,whichleaveslittleroomforeggs.

Theoldqueenwillflyaway,bringingapproximatelyhalfofherworkerbeestofindanew

locationtostartahive(Williamsetal.,2010).Theotherhalfoftheworkersremainwith

theoldhive,andraiseanewqueen.Duringaswarm,thebeesfindasafeplacetorestsuch

asonthebranchesofatreeorintheroofofabarn.Mostofthecolonystayswiththe

queen,andworkersaresentouttoscoutforpotentialnewhivelocations.Onceasuitable

locationisfoundforthenewhive,allofthebeestaketotheskiesatthesametimeand

maketheirwaytothenewarea,whichbecomesthehomeoftheirnewhive.

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Contributingfactors:

Mites

Therearetwospeciesofmites:Varroadestructor,andAcarapiswoodithatare

causingsevereproblemstohoneybeesinNorthAmericaandEurope(Levinetal.,2016).

Theirspreadisnotwellcontrolled,anditiseasyforfarmerstoinadvertentlyintroduce

themtootherhives(Seeley&Smith,2015).Thesetwospeciesofmitesarelikelytobea

significantcontributingfactortocolonycollapsedisorder.

Varroadestructor

Outofallofthehoneybeepathogens,Varroadestructorhashadthelargest

economicimpactonbeekeepersworldwide.Theyarethesinglemostdestructivepeststo

honeybees,especiallyinthewinter-time(Giacobinoetal.,2016).Thehoneybeehasno

naturaldefenseagainstVarroamites,andasevereinfestationcanleadtothedeathofa

hive(Kurzeetal.,2016).VarroamitesoriginatedinSoutheastAsia,arrivedinFrancein

1982andspreadfromthere.TheymovedtoSwitzerland,SpainandItalyin1984,the

UnitedStatesandPortugalin1987,andtheUnitedKingdomin1992(Seeley&Smith,

2016).Varroamitesareoneofthecommonfactorsthateverycountryexperiencingcolony

collapsedisordershares,butitisimportanttonotethatnotallhivessufferingfromcolony

collapsedisordercontainedVarroamites(UNEP,2010).Australia,SouthAmerica,Africa,

andmostofAsia,withtheexceptionofJapanhavehadnocasesofVarroamitesandno

colonycollapseproblems(Figure4);(UNEP,2010).Inthesecontinents,Africanizedbees

havesuccessfullybredwithlocalhoneybeepopulations,resultinginanincreased

resistancetomiteinfection(deMattosetal.,2016).

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Varroamitesaretinyexternalparasitesthatsticktothebodyofhoneybeesand

consumetheirhemolymph,ablood-likefluidpresentinmostinvertebrates(Seeley&

Smith,2016).Theirbitesleaveopenwoundsontheirhosts,whichfacilitatethetransferof

varoosis,thediseasecausedbyvarroamites,andleavethehoneybeessusceptibleto

infectionfromotherpathogensaswell.Acutebeeparalysisvirus,deformedwingvirus,

Kashmirbeevirus,andblackqueencellvirusarealsotransferablebyvarroamites(Levin

etal.,2016).Theyalsoinhibitaninfectedqueen’sabilitytoreproduce,alterbehavior,and

affectflightinworkerbees(Santosetal.,2016).Colonyageisasignificantfactorin

determiningwhetherthehivewillsurvivetheinfestation.Inolderhives,effectsof

infectionscompound(Bettietal.,2016).

Varroamitesonlyreproduceinhoneybeecolonies.Apregnantfemalemitelaysher

eggsonabeelarvainitscell(Seeley&Smith,2016).Thebeethenhatchesfromthecell

andspreadsthemitestootherbeesandlarvae.Crowdinghasasignificanteffectonahive’s

susceptibilitytoaVarroamiteinfestation,asthemiteshaveaten-dayreproductioncycle

andspreadquicklyinhiveswithahighpopulation(Seeley&Smith,2015).

Earlydetectionoflow-levelinfestationisthekeytocombattingaVarroainfestation

inahive,butwhenthemitepopulationreacheshighlevels,chemicalandheatcontrolis

required.VarroosisiscommonlytreatedwithFluvalinate;apyrethroidinsecticideinthe

formofstrips.Fluvalinateis95%effective,butthesurvivingVarroamitesbecomeimmune

tothetreatment,whichmakestheircompleteeradicationchallenging(Adjilaneetal.,

2016).Organophosphateinsecticidestripscanalsobeused,butbeekeepersmustbe

cautiousaboutthedosagetheyadministerastheinsecticiderisksharmingthebees

themselves(Ghasemietal.,2016).

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NaturalchemicalscanbeintroducedintoinfectedhivestohelpcontrolaVarroa

outbreak.Formicacidvaporcanhelpagainstmiteinfection,andpowderedsugarortalc

canbesprinkledonbeestomakeitharderfortheVarroamitestoattachthemselves.

Essentialoilssuchaslemonoil,mint,orthymeoilhavevaryingeffectivenessonthemites

(Ghasemietal.,2016),andoxalicacidinvapororliquidformhasalsoproveneffectivein

controllingVarroainfestations(Figure5);(Adjilaneetal.,2016).Finally,physicallyheating

thehiveto104degreesFahrenheitfortwohourswillcausethemitestodropfromthe

bees,butdoesnotresultintheirdeath,whichcanleadtore-infestation(Ghasemietal.,

2016).

Acarapiswoodii

Acarapiswoodii,alsoknownastrachealmites,havehadlessofasignificantimpact

onhoneybeecoloniesbutcouldstillbeacontributingfactorincasesofcolonycollapse

disorder(USDA,2012).Acarapiswoodiwerefirstidentifiedin1921inGreatBritainand

arenowpresentoneverycontinentbutAustraliaandAntarctica.Theyareaninternal

parasitethatinfectsbeesuptotwoweeksold(VanEngelsdorpetal.,2008).

Trachealmitesliveandbreedinsidethebee’strachea,feedingonhemolymph

throughtheirtracheawalls.Theyclogthebees’tracheas,physicallyblockingoxygenflow

andshorteningtheirlifespan(Goulson&Hughes,2015).Theyaffectbeeflight,anda

telltalesymptomoftrachealmiteinfestationisalargenumberofbeesoutsidethehivethat

cannotfly.Incaseswheremorethanthirtypercentofbeeswereinfected,therewasa

notabledecreaseinhoneyandbroodproduction,whichaffectsahive’sresilienceto

wintertime,whenfoodisscarce(VanEngelsdorpetal.,2008).Thepresenceoftracheal

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mitesishardtoconfirm,andthehighestlikelihoodofdetectingthemisinthefallorwinter.

Theycanonlybediagnosedwithamicroscopicexaminationofthebees’trachea.

Chemicaltreatmentsagainsttrachealmitesarenoteffective,sothebestcontrolis

administeringmentholpelletsinsidethehivewhentheweatheriswarm.Thewarmair

causesthepelletsvaporize,thebeesbreathethementhol,andthemitesdie(Maeda&

Sakamoto,2016).

Fungi

Anumberofdifferentfungispeciesarealsolikelyacontributingfactortothe

problemofcolonycollapsedisorder(USDA,2012).Infectionisspreadeasilyashivesare

transportedincloseproximitytoeachotheracrossborderstofulfilltheirpollination

contracts(Goulson&Hughes,2015).

Nosemaapis

Nosemaapis,alsoknownasNosema,isamicrosporidianthatcauses“nosemosis”,

themostcommondiseaseintheWesternHoneybee.Nosemasporesareresistantto

extremesintemperatureanddehydration,whichmakesthemveryhardtotreat.Whena

beeisinfected,itleavesthecolonyandistooweaktoreturn,dyingfarawayfromitshive.

AseverehiveinfectionofNosemacanleaveacolonywithdangerouslylowamountsof

workerbees,whichcanresultincolonycollapse(Hold&Grozinger,2016).

AhoneybeeinfectedwithNosemasuffersfromimpairedflight,impaireddigestion,

andseveredysentery,whichaidsinthespreadoffungalspores(Dosselietal.,2016).

Workersaremostcommonlyinfectedbecausetheycleanthehive,ingestingspore-laden

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fecesastheydoso.Onceinfected,cellscanreleasethirtytofiftymillionsporeswhenthey

burst.

Treatmentisperformedbyadministeringtheantibiotic“FumidilB”,whichstops

sporereproduction,butdoesnotkillthesporesthemselves.Thewholehiveandalltools

usedbythebeekeepermustbecompletelydisinfectedinordertogetridoftheremaining

spores.

Acosphaeraapis

Acosphaeraapisisaninsectpathogenfoundworldwide.Itwasdiscoveredinthe

UnitedStatesin1968.Ifbrooddensityandhumidityishighandtemperaturesarecool,

threetofourdayoldhoneybeelarvaecaningestthefungalspores,whichgerminateinside

theirdigestivetract.ThereisnotreatmentforAcosphaeraapis,andonceeradicated,

reinfectioncanoccurviastoredfoodsupplies.Theonlywaytocontrolthefungusisto

keepthehivewarmanddry(Goulson&Hughes,2015),whichisachallengeincold,wet

wintermonths.

Acosphaeraapiscausesthedisease“Chalkbrood”.Infectedlarvaebecomecovered

infungalmycelium,whicheventuallyfillstheentirecellandleavesbehindwhite,chalky

lookingcorpsesthatarehighlyinfectivetootherbees.Seriousnessoftheinfection

dependslargelyonthehygieneofworkerbeesinthehive,whoremoveanddisposeof

infectedcorpses.Onitsown,Acosphaeraapisdoesnotusuallyresultinhivecollapse,but

cancontributetoitifmultipleotherpathogensarepresent(USDA,2012).

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Aspergillus

Aspergillusfumigatus,Aspergillusflavus,andAspergillusniger,closerelativesof

Acosphaeraapis,areothermicrosporidiansthatinfectWesternHoneybees.Theyare

predominatelyfoundinsoilandarecommoninsoilinsects.Honeybeeadults,larvae,and

pupaeabsorbthesporesthroughtheircuticle,whichhatchintheirstomachandproduce

aflatoxins,whichresultsindeath.Theycausethediseasestonebrood,namedafterthe

powderyfungalsporesthatcoverlarvaecorpses.stonebroodhasarelativelylowvirulence

inhivesbutcouldbealsoacontributingfactorincolonycollapsedisorderwhencombined

withotherfactors.

LossofForageHabitatduetoAnthropogenicDevelopment

Ashumandevelopmentcontinuesusinguplargeswathsofland,honeybeesareleft

withfewerlocationstoforageforfood.Theremaybeplentyoffarmlandinwhichtogather

pollen,buthoneybeesrequireavariedarrayflowerstomaintainoptimumhealth.Fields

areoftentemporarilyplantedwithasinglespeciesofcrop,andwhilethismonoculturecan

providebeesthesustenancetheyneed,differentvarietiesofpollenarebetterfor

strengtheningthehoneybees’immunesystems.Weedcontrolinforests,agriculture,andin

residentialareasisalsoacontributingfactorinthereducedamountofforageflowers

availabletobees(Smartetal.,2016).

Coloniesthathaveaccesstothebestpollen,whichhasmorethan25%protein,and

essentialaminoacids,aremoreresistanttodisease,andadiversearrayofflowersprovide

that(Smartetal.,2016).Beekeepershaveanever-increasingneedofmorehivestomeet

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pollinationdemands,buthoneybeecolonynumbershavedecreased;atelltalesignofthe

environment’sdeclininghealth(Goulson&Nicholls,2016).

BeekeepingPractices

CommercialbeekeepingisabigbusinessandintheUnitedStatesitaccountsfor$15

billioninaddedcroprevenue.AlmondcropsinCaliforniarequirethemajorityofhives

available--over1.6million(Williamsetal.,2010).Duetothisoverwhelmingdemand,

hivesmustbeimportedfromotherstatestopollinateCalifornia’salmondorchards.

Beehivesarestackedontoflatbedtrucksanddrivenhundredsorthousandsofmilesto

Californiawherethebeeswillprovidetheirpollinationservicesduringtheflowering

season.Twodetrimentscomewiththisjourney:closeproximity,andstress.

Theextremelycloseproximityofhivesduringtransportfacilitatesthetransferof

mites,fungi,andotherpathogens.Theireffectscompound,whichcanresultincolony

collapse.Hivesfrommanydifferentlocationscanbeadjacenttoeachotherfordaysata

time,givingampleopportunityforinfection(Goulson&Hughes,2015).Stressalsoresults

fromthehivesbeingtransported.Increasedstresslevelsinbeesincreases

immunodeficiencyandmakestransferofdisease,mites,andfungimuchmorelikely

(Asensioetal.,2016).

Withpathogens,fungiandparasitesthreateningtheirhives,commercialand

hobbyistbeekeepersareunderincreasingpressuretousevariouschemicaltreatmentsto

combatinfection.Usingthesetreatmentscanhavebothbeneficialanddetrimentaleffects;

theymayfixthehive’smiteproblem,buttheymayalsoincreasethebees’susceptibilityto

otherdiseasesorevenkillthebeestheyweretryingtoprotect.

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ClimateChange

Climatechangeishavingasignificanteffectonhoneybeepopulations.Rising

temperaturesdisruptthetimingofflowerbloomsinthespringtime.Flowersbloomearlier

anddieearlierbeforethebeeshavebredenoughworkerstogatherfoodforthehivefor

thewintermonths(Calatayud-Vernichetal.,2016).Beeshaveashortertimespaninwhich

tofindfood,whichalsoresultsinincreasedinterspecificandintraspecificcompetitionfor

nectarandpollen.Honeybeesarehighlyadaptable,andhavelearnedtoliveinmany

differentclimatesaroundtheworld,buttherateofwarmingistoofastforthemtoadapt.

Astheweathershifts,beebehaviorchanges.Insomeareastheamountofrainwill

increase,whichwashesawaythepollenbeeseatandcausesthemtostayintheirhives,

reducingvaluabletimeneededtoforage.Inareaswherethetemperatureisincreasing,

therewillbemorepressuretogatherwaterforthehive,andintimesofdroughttherewill

befewerflowersforbeestoforageon(Smartetal.,2016).Thehotter,drierweatheralso

resultsinmorewildfires,primarilyinthewesternUnitedStates,whichsendmassive

amountsofparticulatematterintotheairandaffectsbeerespiration.

Asclimatechangecontinuestotakehold,climatebeltswillshiftnorthward.Areas

thatcurrentlyhavetheidealtemperatureandprecipitationforbeeswillsoonbecomedrier

andcolder,andareasnorthofthatwillreceivemorefavorableweather.Wildhoneybees

arenotshiftingnorthwiththeclimate;theirrangestaysthesameinthenorth,and

compressesinthesouthasitgetscolder,whichresultsinlesshabitat(Smartetal.,2016).

Itisnotknownwhythebeesdonotmovenorthwiththechangingclimate,butshifting

climatebeltswillchangethedistributionofwildhoneybeesdrastically.

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Pesticides

Pesticideshavebeenthemostcontroversialissueinvolvingcolonycollapse

disorder.Manystudieshavebeenperformedattemptingtoassociatepesticideusewith

declinesinhoneybeepopulations,buttheyhavenotbeenabletoconclusivelylinkreal-

worldpesticideapplicationconcentrationsasthemainfactorincolonycollapses(USDA,

2009).

Therearetwotypesofpesticides:contact,andsystemic.Contactpesticidesare

sprayeddirectlyontheplant’sleaves,andareconsideredmoredangeroustohoneybee

populationsbecausethebeescancomeindirectcontactwiththepoison.Systemic

pesticidesarewater-solubleandinthecaseofneonicotinoids,areusedasseedandsoil

treatments.Soiltreatmentreducesaccidentalwind-driftwhencomparedtosprayed-on

contactpesticides;however,honeybeesarestilllikelytobeexposedtosoil-borne

pesticides(Table1);(Krupkeetal.,2012).Systemicpesticidesarestillpresentastheplant

growsandresiduesinthenectarandpollenofflowersarestilldetectable(Table

2);(Pohoreckaetal.,2007).

Theprimaryfamilyofpesticideunderscrutinybybeekeepersand

environmentalistsareneonicotinoids,atypeofofsystemicpesticidethatattacksinsects’

nervoussystems.DevelopedbytheShellandBayercorporationsinthe1980’sand1990’s,

theyarechemicallysimilartonicotine.Thenameneonicotinoidliterallymeans“new

nicotine-likepesticide”.Comparedtotheorganophosphatestheyreplaced,neonicotinoids

arelesstoxictobirds,animals,andhumans,andwereconsideredagroundbreakingstep

forwardforpestcontrolinagriculturalapplications(Yamamoto&Casida,1999).

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ImidaclopridwasthefirstneonicotinoidpatentedbyBayerin1988,followedbysix

othersintheyearsfollowing.Therearesevendifferentneonicotinoidscurrentlyinuse

aroundtheworld.Clothianidin,andThialloprid,alsomanufacturedbyBayer,areonthe

marketaswellasThiamethoxam,manufacturedbySyngenta,Acetamiprid,madeby

NipponSoda,Pinotefuran,manufacturedbyMitsuiChemicals,andNitenpyram,

manufacturedbySumitomoChemical.

Neonicotinoidsaccountfor24%oftheglobalinsecticidemarketandareusedin

over120countriestocontrolpests(Jeschkeetal.,2011).IntheUnitedStates,virtuallyall

ofthecorncrops,andonehalfofallsoybeansalongwithavastmajorityoffruits,

vegetables,andcerealgrainsaretreatedwithneonicotinoids.Theyarealsousedin

residentiallandscaping,asananti-fleatreatmentfordomesticlivestockandpets,andare

availabletothegeneralpublicforhomeusebyveterinarians.

Theleveloftoxicityofthepesticide,andexposuretimearethebiggestfactors

regardingchancesoffatalityinbees(Kiljaneketal.,2016).Unlikecontactpesticides,which

haveahightoxicitylevel,areeasytocomeincontactwith,andusuallyresultinarelatively

quickdeath,systemicpesticideslikeneonicotinoidsoftenresultincompoundingsub-lethal

effects(Meikleetal.,2016).Repeatedexposurethroughcontaminatedpollenandnectar

candisorient,compromiseimmunity,delaydevelopment,reduceforagingbehavior,inhibit

memoryandlearning,andchangethecommunicationhabitsofhoneybees(Williamsonet

al.,2016).Theyhavebeenfoundtomakebeesmoresusceptibletothegutpathogen

nosema,impairodorencoding,andcausereducedimmunodeficiency(Andrioneetal.,

2016).Repeatedacuteexposureofneonicotinoidsislikelytocausecumulativeeffects

resultinginparalysisandeventualdeath(Samuelsonetal.,2016).

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Inastudyperformedin2012,whencomingintocontactwithlowlevelsof

neonicotinoidpesticidesataconcentrationmuchsmallerthanalethaldose,onethirdof

honeybeesbecomedisoriented,andneverreturnedtotheirhive(Henryetal.,2012).

Binarymixturesofneonicotinoidsalsorepresentasignificantdangertohoneybees.When

comparedtoasingleneonicotinoid,twocombinedmadeasignificantdifferencein

honeybeemortality(Christenetal.,2017).

Opponentstoneonicotinoidbansincludefarmersandpesticidemanufacturersthat

citethattheyaresafertobees,mammals,andbirdsthanorganophosphates(Yamamoto&

Casida,1999).Theystatethatneonicotinoidsarenotthesolecauseofcolonycollapse

disorder,andthatmorestudiesareneededtodiscovertheirtrueenvironmentalimpact.

Theyarguethatthestudiesthathavebeenperformedhaveproducedmixedevidence,and

thatmanytestedunrealisticallyhighlevelsofthepesticidethatahoneybeewouldnever

encounterintherealworld(USDA,2012).

Whileneonicotinoidshavenotconclusivelybeenfoundtobethesolecauseof

colonycollapsedisorder,theyarelikelyasignificantcontributingfactor(Fairbrotheretal.,

2014).Morestudiesareneededtodiscoverthetruedamageneonicotinoidsarecausingto

honeybeecolonies,anduntilthen,morelegislationisneededtoregulatetheirvirtually

unrestricteduse.

GovernmentAction

Mostofthelegislativeactionoccurringpertainingtohoneybeeprotectionisrelated

toneonicotinoiduse,butfarmersandpesticidemanufacturersmakeitdifficulttopassany

21

bansorrestrictions.ItistheEnvironmentalProtectionAgency’stasktoapproveall

pesticidesintheUnitedStatesofAmerica.

In2003,theEPAconditionallyapprovedtheuseofClothianidin.Theneonicotinoid

metthestandardsforregistration,butstudieswerestillneeded.Thismeantthatitcould

beusedbyfarmerseventhoughitsfulleffectsontheenvironmentwerenotknown.In

2013,USbeekeepersandenvironmentalistsfiledajointlawsuitagainsttheEPAfor

allowingtheuseofneonicotinoids.

TheEPAblamedcolonycollapseonVarroamites,andstatedthattherewasnot

enoughevidencetoceaseusingneonicotinoids(USDA,2009).Despitetheirclaims,they

institutednewwarninglabelingforneonicotinoidpesticidecontainers,whichcautioned

againsttheirusenearbees.Thelabelswarnagainstapplyingthepesticideswherebeesare

foraging,andadvisenottoapplythemuntilfloweringisoverandallofthepetalshave

fallenfromtheplant.

RepresentativeJohnConyerscreatedthe“SaveAmericanPollinatorsAct”,which

washeardintheHouseofRepresentativesin2015.Theactrequestedthesuspensionof

fourneonicotinoidsuntilreviewswerecompletedbytheEPA,butitdidnotleavethe

congressionalcommittee.

TheEnvironmentalProtectionAgencyhasafifteen-yearregistrationcycleforall

pesticides,whichmeansthatClothianidinwillhavetoundergoanotherapprovalin2018.

Theyupdatedtheirstandardsin2014toincludeacutecontacttoxicitypesticides,but

neonicotinoidsaresystemic,anddonotapplyinthisupdate.Thenewstandardsalsodo

notaccountforsub-lethaleffectsonhoneybeebroodorlarvae.Therearestillnocurrent

guidelinesforchronicoracuteoraltoxicityofsystemicpesticidesbuttheEPAhopesto

22

completethereviewofsixdifferentneonicotinoidsby2018.Inanefforttoreducethe

amountofneonicotinoidsbeingutilizedintheUnitedStates,thereviewofThiaclopridwas

voluntarilycancelledbytheEPAin2014(EPA,2014).

In2015,theEPAproposedtostoptheapplicationofcertainneonicotinoids

includingallproductsconsistingofliquidordustthatareusedoncropswithahightoxicity

tobeesduringpollinationperiods;however,inanemergency,suchaswithmosquito

controlmeasures,therulescanbeignored.Theyimplementedapolicyin2017toprotect

beesfromagriculturalpesticideswhilethebeeswereprovidingtheircommercial

pollinationservices,whichiswhenmanyexposuresoccur(Calatayud-vernichetal.,2016).

Therehasalsobeenindividualstateandprovinciallegislationconcerningtheuseof

neonicotinoids.OntarioCanadawasthefirstinNorthAmericatopassrulesinvolvingthe

useofneonicotinoids.In2015,theystipulatedthatfor2016,farmerswouldonlybeableto

useneonicotinoidsin50%oftheirseeds.In2017,theywouldneedtoprovethattheyhave

peststobeabletocontinuetheiruse.

In2015,afterMarylandhadlost61%ofitshives,thestateenactedSB0198,the

“MarylandPollinatorProtectionActof2016”makingitthefirstUSstatetointroduce

neonicotinoidlegislature.Thelawbannedtheconsumeruseofneonicotinoidswiththe

exceptionofspeciallytrained“certifiedapplicators”suchasfarmersorveterinarians.They

wouldnotbeavailabletobesoldonorafterJanuary1st,2018.

In2016,CaliforniafollowedinMaryland’sfootstepsandintroducedSB1282.The

billwouldalsomakethesaleofneonicotinoidsexclusivelyavailableto“certified

applicators”suchastrainedfarmersandveterinarians,andcalledforthelabelingofall

retailplantsandseedstreatedwithneonicotinoids.Thelabelwouldwarnagainsttheiruse

23

andinformthebuyerthattheproductharmshoneybees.Thebillpassedacommittee,but

diedoninactivefileinNovemberof2016.

TheEuropeanUnionisinchargeoftheregulationofallpesticidesinEurope,and

hashadmoreluckinregulatingtheuseofneonicotinoidsinEurope.In2013,fifteen

Europeancountriesvotedinfavorofbanningthreeneonicotinoids:Clothianidin,

Imidacloprid,andThiametoxam.TheEUbannedtheiruseoncropspollinatedbybeesfor

twoyears,andriskevaluationisscheduledtofinishin2017.Onestipulationisthata

countrycanauthorizetheiruseinemergenciesfor120days,whichtheUnitedKingdomdid

in2015for5%oftheirrapeseedcrop.IfacountrydecidestoleavetheEuropeanUnion,as

GreatBritaindidin2016,thatgovernmentcoulddecidetoreinstatetheiruse.

Legislationforthegeneralhealthandstudyofhoneybeeshasalsobeenintroduced

inNorthAmericaandEurope.In2007,theUSDepartmentofAgriculturereleasedthe

“ColonyCollapseDisorderActionPlan”.Itsgoalsincludedanincreasednumberof

honeybeesurveysanddatacollection,analysisofthesamplescollected,research,

mitigation,andpreventativeaction(USDA,2007).Thefirstreportresultingfromthe

actionplanwasreleasedin2009,whichconcludedthatcolonycollapsedisorderwaslikely

tobecausedbytheinteractionofmanydifferentfactorsincombination.Thereportstates

thatofthesixty-onevariablesquantified,nosinglevariablewasfoundtosuggestasingle

causalagent.Italsonotedthatthesub-lethaleffectsofpesticidesandfungicidescould

hinderthebees’immunesystems,andmakethemmorevulnerabletoviruses(USDA,

2009).

In2013,theEnvironmentalProtectionAgencyandtheUnitedStatesDepartmentof

Agricultureformedacommitteetocreateanationalpollinatorhealthstrategy.

24

In2015,usingtheinformationgainedbytheEPA/USDAtaskforce,PresidentObama

implementedthe“NationalStrategyforImprovingtheHealthofBeesandOther

Pollinators”.Thisstrategyplannedtorestoresevenmillionacresofbeehabitatwitha

assortmentofnativeplantsthatbeesutilize,andproposedspending$82.5millionfor

honeybeeresearch.Italsostipulatedthatgovernmentagenciesmustincludebeefriendly

landscapingontheirpropertytoincreasetheamountandvarietyofforageflowers,and

encouragedpollinatorfriendlyhabitatconsiderationinlandcleanupprogramssuchas

superfundsites.ThestrategyinstitutedmorestudiesconductedbytheEPAonthe

neonicotinoidsthattheEUhadalreadytemporarilybannedinEuropeandalsopromised

nottoapproveanynewneonicotinoidsuntilthestudiesarecompleted.Itplannedtospend

moremoneyonresearch,anduselesspesticideoverall.Italsorecommendedthat

individualstatesandIndiantribesdevelopactionplansandbestmanagementpractices,or

“managedpollinatorprotectionplans”fortheirownareas.

Recommendations

Thereareanumberofthingsthatcanbedonetohelplessentheimpactofcolony

collapsedisorder,butitwilltakealotofwork,funding,andsocialawareness.Thethreatof

miteinfestationandfungispreadmustbetakenmuchmoreseriouslythanitisbeingtaken

now.Mitesandfungiareverylikelytobetwofactorsthatcontributetocolonycollapse

disorder(USDA,2009),yettheyarenotbeingcontrolledascloselyastheyshouldbe.More

legislationmustbeputinplacethatstopstheirdispersalacrossbothstateandnational

bordersbytestingformitesandfungiandstoppinghivetransportifeitherarefoundtobe

25

present.Governmentfundingisalsoneededtopayforresearchonhowtocombatthem

andstoptheirspread.

Anthropogenicdevelopmentistakingawayhoneybees’foraginghabitatresultingin

amonocultureofflowersthattheycanutilize(Smartetal.,2016).Awidervarietyof

flowersmustbeplantedbybothcommercialfarmersandprivateresidentstohelpbees

receivethenutritiontheyrequiretomaintainahealthyimmunesystem.Small,local,

diversifiedfarmsshouldbeestablishedthatwillhelphoneybeehealthandencourage

peopletogetinvolvedtoremedytheproblem.Commercialfarmersshouldplantawider

varietyofcrops,whichwouldbothhelpthehoneybeesgetawidervarietyofnutrition,and

helpthefarmerwithamorediversearrayofproducetosellintheeventofmarketchanges.

Morelandmustbesetasidetoactasforagehabitatforhoneybees.When

developinghouses,orbusinessinfrastructure,developersmustberequiredtoleavea

certainamountoflandundeveloped,andplantedwithavarietyofflowersspecificallyfor

honeybeeuse.Theaveragepersonshouldalsobeencouragedtoplantadiversearrayof

nativeflowersintheirowngardenstohelphoneybees.

Travellinghundredsorthousandsofmilesputsalotofstressonhoneybeehives,

andclosequarterstransportfacilitatesthespreadofmites,fungi,anddiseases(Seeley&

Smith,2015).Inordertolessenstressandreducethespreadofpathogens,local

honeybeesshouldbeusedasoftenaspossibletopollinatefarmer’sfields.Theaverage

citizenshouldalsobeencouragedtostarttheirownhivestopropupthepopulationof

availablelocalbees.

Climatechangeisoneofthebiggestissuesofthe21stcenturyandisaffecting

countlessirreplaceablespeciesincludingthehoneybee.Worldgovernmentsmustdo

26

everythingintheirpowertospreadawarenessabouttheissue,reduceemissionsand

sequesterthecarbonthatisalreadyintheatmosphere.

Pesticideshaveproventobeanecessaryevilwhenitcomestoproducingfoodfor

theworld,butstepscanbetakentomakethemmorehoneybee-friendly.Neonicotinoids

havenotbeenconclusivelyfoundtosingle-handedlycausecolonycollapsedisorder,and

aresaferthanorganophosphatesformammalsandbirds(USDA,2009),sotheiruseshould

stillbepermittedbyprofessionalfarmersthathavebeentrainedinthecorrectdosageand

applicationtechniquesuntilmoreconclusivestudieshavebeenconducted.However,

neonicotinoidusebyuntrainedprivateandresidentialpartiesshouldbehalted

immediatelyastheiruseisnotabsolutelynecessaryintheprivatesetting,andapplication

ofpesticidesbyuntrainedindividualsisoftenoverzealous.

Moregovernment-funded,independentjointresearchfrombothNorthAmerican

andEuropeancountriesisrequiredtoconclusivelydeterminewhetherornot

neonicotinoidsareasbee-safeastheirmanufacturersandfarmersclaim.Thisresearch

mustbeginimmediatelyandonceconclusiveevidenceisfoundeitherfororagainst

neonicotinoiduse,decisionsmustbemaderapidlyaboutwhattodo.

Thetwomostimportantfactorsneededincombattingthedeclineofhoneybeesare

moreawareness,andmorefunding.Additionalfundsmustbeallocatedforfurther

researchintocolonycollapsedisorderanditscauses,aswellasforthedevelopmentof

saferfungicidesandmiticides,andsaferpesticidestobeusedinagriculturalapplications.

Withoutgreaterpublicawarenessandsupport,thefundswillnotbeappropriatedforthese

causesandtheproblemofcolonycollapsedisorderwillcontinue.

27

Inordertocreatepublicawareness,fundsmustalsobeappropriatedtomakepublic

serviceannouncementsontelevisionandtheradio.Theaveragepersonneedstobemade

awareofhowseriousaproblemcolonycollapsedisorderis,whateffectsitcanhaveon

themselvesandfuturegenerations,andwhattheycandotohelp.Theymustbe

encouragedtodosomethingaboutitbyplantingwildflowersinyardsandunusedfields,

ceasingtheiruseofdamagingpesticides,propositioningtheirlocalleadersforchange,and

managingtheirownhives.

Conclusion

Colonycollapsedisorderwillcontinuetogetworseifnothingisdoneaboutit.Itis

causedbyanumberofcontributingfactorsincludingvariousmitesthatspreaddiseaseand

inhibitimmunosuppression,andfungithatinfectandkillthebrood.Lossofforagehabitat

resultsingreaterimmunodeficiency,andchangingbeekeepingpracticesfacilitatethe

spreadofdiseaseandincreasestresslevels.Globalwarmingchangeshoneybeebehavior,

distributions,andhabitats,andpesticidescauseharmfuleffectssuchasdisorientationand

memorylossafterrepeatedlow-doseexposures.

LegislationhasjustbeguninmanydifferentcountriesinNorthAmericaandEurope,

andwillhopefullycontinuetobeimplementedastheproblemgetsworse.However,more

fundingandpublicawarenessisneededabouttheissuebecauseifthepublicisignorant

aboutthelong-termeffectsofaworldwithoutbees,verylittlewillbedoneaboutthe

causes.Thespreadofdamagingmitesmustbestopped,pesticidesmustberesearched

morethoroughly,moreforagehabitatisneeded,transportofhivesmustbekepttoa

minimum,andmorebee-friendlylegislationisneededifthereistobeanyhopeofkeeping

28

thesupplyofbeeshealthytopollinatecropsandfeedtheworld.Theactioncurrentlybeing

takenisslowandisnotenoughtohaveadiscernibleeffect.Despitethestepsbeingtaken,

colonycollapsedisorderisstilloccurringandmoreresearchandsupport,bothfinancial

andsocial,isneededtofindasolutiontotheproblem.

29

Figure1.NumberofhoneyproducingbeecoloniesintheUnitedStatesfrom1945to

2007(FigurefromUNEP,2010).

30

Figure2.Totalcolonylossbystatein2008(FigurefromVanEngelsdorpetal.,2008).

31

Figure3.ColonylossesinPennsylvaniaasafunctionofaverageambienttemperaturebetweenSeptember2007andMarch2008(FromVanEngelsdorpetal.,2008).

32

Figure4.YearlyaverageofmanagedhoneybeecolonylossesduetoVarroamites

(FigurefromUNEP,2010).

33

Figure5.LethalityofOxalicAcidtreatmentsonVarroamites(FigurefromAdjilane

etal.,2016).

34

Table1.Concentrationsofpesticidesinpartsperbilliontakenfromsoilsamples

nearagriculturalfieldsinIndiana(TablefromKrupkeetal.,2012).

35

Table2.NeonicotinoidpresenceandconcentrationlevelinsamplesfromPoland’swinterandspringoilseedrapecropin2010and2012(TablefromPohoreckaetal.,2007).

36

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