1049 1 17 − – 15 This is not 15 , 14 13 – 9 a* L., is a flagship species whose popularity Apis mellifera Correspondence to:mologia, Raul Universidade Narciso FederalE-mail: [email protected] de C Viçosa, Guedes, Viçosa, Departamento MGDepartamento de 36570-900, Entomologia, de Universidade Federal Brazil. de Viçosa, Ento- Viçosa, Brazil Department of CropUniversity, Ghent, Protection, Belgium Faculty of Bioscience Engineering, Ghent The concern surrounding the potential impact of pesticides, par- ∗ a b ticularly insecticides, on the honey beelogical and services its is products justifiable, and not eco- of only such because products of and the servicesdemand importance but for also pollinators because of in the current increased agricultural production. High-yield agricultural systems and middle-to-high-income coun- tries continue theoveruse reflected heavy in average pesticide use amounts: above 2.0 of kg ha pesticides, with evidence of results of the ongoing effort to settle this debateof show some congruence, points which includeof the honey following: bee (1) decline the inevery different recognition area areas of and every countries,phenomenon; but (3) country; the not apparent (2) lack in of the a primary,between multifactorial direct honey association bee nature decline and of neonicotinoid use. the to say that pesticides, particularly neonicotinoidimportance insecticides, in lack this debate, as theyponents are in most likely this important scenario, com- potentiatingwhere there colony is decline a high in demand a for period pollination services. and Raul Narciso C Guedes b The The end 8 ). However, – 6 The reasons for this are 2 , Guy Smagghe Zeus and the Ant 1 This is exemplified by Aesop’s a,b 1 ). Therefore, it comes as no surprise Suchaheateddebateprovedtobe 5 – 3 : 1049–1053 www.soci.org © 2015 Society of Chemical Industry 71 Again, Aesop comes to mind with his fable Aesop’s Fables ( 2 , 1 L., being one of them. 2015; bioinsecticides; biorational insecticides; insecticidal stress; Meliponini; wild pollinators

The earlier suspicion that the involvement of pesticides was lead- Bear and the Bees that there is stillhas moved beyond a beekeepers, academia, industry raging and regulatory debateagencies, over extending to honey non-governmental bee organisationsmass decline media, (NGOs), fiction that writers and the general public. ing to the reportedadded further fuel honey to the bee debate, which colonynomenon shifted (detected from mainly collapse in the the CCD United disorder phe- States between (CCD) 20062008) and to honey bee colony decline, particularly in theand United States the European Union. Pest Manag Sci Invertebrates are generallyWestern not society, with particularly a few liked exceptions,Apis the or mellifera European honey praised bee, in 1 PUBLICDECLINE PERCEPTION AND OF PEST HONEY CONTROL BEE Abstract Although invertebrates generally have a low public profile, the honey bee, and perspectives Wagner F Barbosa, bees and pantropical stingless bees: pitfalls (wileyonlinelibrary.com) DOI 10.1002/ps.4025 Pesticides and reduced-risk insecticides, native Perspective Received: 22 December 2014 Revised: 6 February 2015 Accepted article published: 17 April 2015 Published online in Wiley Online Library: 18 May 2015 Keywords: likely derives from the products itbee provides and decline its has perceived ecological surpassed services. Therefore,non-governmental the the agencies, realm raging debate of media, regarding honey beekeepers, fictioncolony academia, writers collapse industry disorder and (CCD) and the soon regulatory shifted generalof agencies to pesticides public. the and in bigger The now issue such early also of aparticularly encompasses pollinator interest phenomenon. the decline, neonicotinoid and Pesticides with insecticides were a concern owing previously to focus aboutthe their on recognised potential widespread honey the pivotal as and role potential bee peculiar the of involvement use these potential neonicotinoids in in culprits agriculture.of honey However, the bee of the decline evidence the multifactorial remains for a reported nature matter of declines, ofuse. debate, The with the an focus problem increased on recognition the and decline the ofmatter honey lack of bee concern, of populations particularly subsequently a in spread Europe direct toregions and other association of the species, between the United and world, States. bumblebees the remain Other became noted the bee another objectis species, decline of ones also and little that in neonicotinoid concern are (unjustifiably particularly need so). important ofaddress Furthermore, in the revision, both other continuous shortcomings. as focus the on neonicotinoids current© evidence 2015 suggests Society that of Chemical a Industry broad spectrum of compounds deserve attention. Here we invaluable in identifying knowledge gapssation of and resources led for to scientific theamplitude research mobili- focusing and on causes the of spread, honey bee colony decline. deeply ingrained and intuitive. ‘Bugs’subject (i.e. to insects) in dominionisticperception general and are that negativistic they are views pests. owing to the honey bees areviews, the extending target even to ofare aesthetics considered. more if their naturalistic social and characteristics utilitarian view of ants as ‘thieves’ in his fables ( 48 – The The 46 35 33 , There- , 42 34 but the – 32 30 39 29 : 1049–1053 71 Wild pollinators Furthermore, wild Such concern and 45 2015; – 44 46 , 43 43 the more frequently used con- 31 Pest Manag Sci In this context, biopesticides and/or reduced-risk 38 bees, and a tenfold range of variation in pesticide but they are also potentially affected by pesticide – 45 36 Apis The concept of biopesticides, which may also be considered sparked byhoney Western bee society, declinefor and illustrates organically produced this food the items (i.e. fact.ticides where neonicotinoid only The are natural insec- allowed) increased risk also demand (bio)pesticides, reinforces to the which demand forconventional are reduced-risk pesticides. Curiously generally though, currentventional) perceived levels of pesticide (con- as residues on saferof foodstuffs significance do than to not human appearfrequently health, to and detected be pesticide residues on are organically also produced food, use, and, again, thecotinoids primary and concern their potentially has higher been toxicity with to the wild neoni- bees. The honey bee is routinelypesticide risk used assessments, as but a recent surrogate meta-analysisneed bee indicates for the pollinator more in comparative informationand between non- the honey bee sensitivity exists between both bee groups. 3 NATIVE BEES:PESTICIDES EXTENDED CONCERNS WITH The significant declineUnited in States honey and bee in partslinator colonies of communities observed Europe and drew in their attention the importance. to wild pol- insecticides may exhibit significant lethal and/or sublethalto toxicity the honey bee and other pollinator bees,as even showing high lethality as that attributedis to usually the neglected neonicotinoids, in a spite possibility of some that available evidence. can perform equally wellpollinators or in even some better crops than and the wild honey plants. bee as pollinators are important in maintaining plantlandscapes, diversity in natural problem with this is the(or common biological assumption pesticides, that or biopesticides than natural synthetic pesticides) insecticides, pose which ation is lower aligned and risk with the public supporters percep- as Global of Good respectful Agricultural Production production (GlobalGAP)grated and systems, the such Production Inte- (IP)Organisation initiative for Biological launched and Integrated by Controldeception (IOBC). the lies in International theessarily fact that true the because statednot assumption the is a origin not determinant (either nec- ofcal natural toxicity, structure which or and is synthetic) the acompound. derived is function physicochemical of properties the of chemi- the popularity of organically produced foodsurpassing items the is residue a concern. complex The US issue Agency Environmental defines Protection reduced-risk pesticides as those exhibitingone at least trait of thepesticides: following (1) six low advantageous impactnon-target organisms; traits on (3) over human low potential existing health; forination; groundwater (2) (4) contam- low lower use toxicitycompatibility rates; to with (5) integrated low pest pest resistance management potential; (IPM). (6) fore, the concept isthe not majority particularly of insecticides stringent developedeven and and if is used they since likely are the to not 1970s, pollinators. fit safe for non-target organisms, such as plant to be reduced-risk pesticides,with is public another perception. potential Although pitfall some‘biopesticide’ playing authors for living reserve organisms, the term cept gives a broader definition ofticides), biopesticides (or encompassing biological all pes- molecules of biological origin. 23 – The 21 25 , 24 Although The plant 28 28 This scenario – – However, they © 2015 Society of Chemical Industry 26 26 , 25 , 25 14 , 24 , www.soci.org WF Barbosa, G Smagghe, RNC Guedes 24 , the general concern 18 20 , 28 19 Nonetheless, there are still 20 , 19 , 17 The challenge remains, as always, the effective in countries such as Brazil and China, among 18 , 1 17 − Among agricultural pesticides, insecticides are also 18 – 16 The recent expansion and incentives towards the development Current pesticides exhibit greater potency against the target The myriad of pesticide groups currently available and the wileyonlinelibrary.com/journal/ps in spite ofregarding the their progressive use, change promptingwith in the better attitudes search toxicological for and new and behaviour compounds ecotoxicological profiles. 2 PESTICIDES,AND REDUCED-RISK THE INSECTICIDES HONEY BEE Pesticide use hasdecades. remained High the efficacybesides basis competitive against costs, leading of to pestity improved crop and production species yield qual- protection with and attractive for commonly associated economic with fast returns, pesticide use are that action, characteristics favour itsas prevalence a pest management method. in the United States, Canada andover several 10 European countries, kg and ha recognised risks and controversies surrounding pesticides, others. management of pest insects with minimal non-target impacts. without a noticeable reduction in use, withincrease some in having an use, actual evenmodified under crops. the intense adoption of genetically systemicity of neonicotinoids and the broad scale ofhigh their lethal use, with and pronounced sublethalthe toxicity to key honey reasons bees, are forinsecticides, the a group concern that and stilluse attention exhibits against the agricultural to arthropod potential this pest for species. increased group of and use ofbiopesticides, are the reactions to the so-called environmental safety reduced-risk concerns pesticides, particularly a few other insecticidesorganophosphates, pyrethroids and fipronil, are also considered, including the old is largely focused on neonicotinoid insecticides. usually require more frequentfield applications owing persistence to compared theira with lower higher older rate compounds,duction of leading in consumption, to middle-to-high-income particularly countries. for agricultural pro- end-result is the current prevalence of acidal broader compounds, diversity some of pesti- of whichand/or are reduced-risk recognised pesticides. as biopesticides pests, requiring lower field application rateslevels and of affording safety higher for non-target organisms. has allowed thecoining burgeoning alternative of references neologisms tolacious pesticides, and ones, including pleonasms which some in include fal- vary ‘agricultural greatly protectants’, ‘plant from protectiontosanitary country products’, agents’, ‘agrochemicals’, ‘phy- to ‘agrotoxics’, ‘biological country pes- ticides’, and ‘biopesticides’, ‘biorational pesticides’pesticides’, among and others. This ‘reduced-risk colourful semantic exuberancequently fre- exhibits little scientific or technicalconveys value subliminal and, worst and of equivocated all, notionscally such higher as (or lower) the level intrinsi- of safety of a pesticidal compound. present societal perceptions ofchallenges, pesticides create as new new regulatory toxicologicalessary. tests The and honey endpoints bee seemthis provides nec- species an is interesting needed paradox throughoutcal the assessments because aimed world at pesticide for registration for basic agriculturalbut toxicologi- use, it is reported to be sufferingin from different pesticide-influenced decline countries, with callsright for ban the of some restriction compounds, or notably neonicotinoid evenand insecticides down- particularly in Europe and the United States.

1050 1051 6 a 64 , 62 63 and Until – Again, 63 60 , 65 61 62 , , – 60 46 60 , 46 , 42 67 , 66 wileyonlinelibrary.com/journal/ps but such information is based mainly 62 , 46 The sparse information currently available indi- 65 , 63 The large-scale agricultural use of pesticides and the resource The commercial importance of honey bee products is easy to competition imposed by the Africanised honeynative bee bees are threats in to Neotropicalthan America, the decline potentially of more (Africanised) important honey bees in the region, recognise, as is theeven potential in economic the impact tropics.services of However, the their (namely concern decline, about pollination)bees the in provided ecosystem the by tropics,disputable mainly (Africanised) because in wild honey Neotropical stingless America,tant bees seems seem for to to both be be wild more and impor- cultivated plants in the region 5The CONCLUDING REMARKS apparent paradox of theused worldwide colony as decline the of surrogate the pollinatorcological main species studies for for species basic the toxi- useis registration of not agriculture pesticides difficultthat to are likely understand created precisely by inThe such stated regulatory light requirements. requirements are of basedthus the on dose–mortality focusing knowledge on bioassays, gaps lethalular acute species effects – the ofemerge: (1) pesticides honey the on bee. creation ainsecticide of In partic- knowledge effects; doing gaps exploring (2) so,to sublethal two the pursue shortcomings the non-provisionplace potential of under indirect necessary pesticide effectsing exposure stimuli that on in a are a single likely (model)importance, given species to as environment that is take well focus- perceivedtant as as species being ignoring of in other key certaindeters potentially scenarios. initiatives more This of impor- second studiescal shortcoming exploring impact, also higher including impacts levelslevels. at of the hierarchi- population and community Among these wild beeally species, active the eusocial ratherpass diverse stingless and bees a perenni- (Apidae: varietyand Meliponini) of cultivated encom- plant pollinators species thatperformance. where honey are bees very exhibit marginal important for wild cates that pantropical stingless bees are more susceptiblecides than to the pesti- honey bee, on dose–response (acute) toxicity bioassays, withscant only information recent on and the sublethal effects of pesticides. neonicotinoids, in addition to fipronil and awere few the focus older of insecticides, attention, and no informationing is available the regard- potential impact ofagricultural the pesticides over 150 in active use ingredients indose–mortality of the the tropics lethal today, acute with bioassays only inuse basic registration honey before bees marketing. required for recently, a representative ofthe the red stingless list beesfor was of included the endangered in Conservation species2013; of of http://www.iucnredlist.org, the Nature Internationaland accessed and Union it Natural 2 remainsof Resources October recognised (IUCN Environment as 2013), (Normativehttp://www.mma.gov.br/biodiversidade/espécies-ameaçadas-de- such Instruction by No.extinção/fauna-ameaçada). the 3, Attention Brazilian to 27necessary Ministry the and May long group overdue. is 2003; therefore are vulnerable not only tohigh pesticide susceptibility use owing but to alsotition their to apparent from habitat the destruction invasive and Africanised compe- honey bee. status that largely remains unconfirmed. It is notics, only the but Neotrop- the wholewild bee pantropical species that region are that vulnerable to houses agricultural pesticides. hundreds of 1 − How- .These 55 , Bumble- 54 , 52 51 A call for the – 50 56 , 17 57 , 47 Bumblebee decline has 53 Neonicotinoids have again A. mellifera scutellata 50 , 49 : 1049–1053 © 2015 Society of Chemical Industry 42 In Latin America, European honey bees were 71 – 59 , 39 58 2015; and some progress has been achieved. 48 , 47 Another important issue to consider is that the honey bee Higher insecticide use compromises pollinator diversity, and dif- subspecies and hybridsica prevailing in are Europe distinctexhibit and North different from Amer- habits thoseand pathogens and prevailing and seem likely inbee distinct subspecies. susceptibility even the among to European tropics, honey pesticides which Pest Manag Sci and an intensive use of neonicotinoid insecticides. The tropics deal with afrom scenario and the challenges that United areregarding States different honey bee decline and and neonicotinoid use Europe, do exist.for although Brazil, instance, similar is the concerns world’sin second agriculture, largest with consumer an of average pesticides yearly consumption of 10 kg ha 4 PESTICIDESBEYOND AND HONEY BEES BEES IN AND THE BUMBLEBEES TROPICS: Pesticides and reduced-risk insecticides, native bees and pantropical stingless beesneed have also beenstudies, expressed in different global surveys and www.soci.org bees prevail in the Northerndo Hemisphere, although exist some in species Southimportant in America, agriculture and as pollinators they ofgreenhouse cultivated have tomatoes crops, become such and as increasingly strawberry. also been reported,tant and component pesticide of use thisthe is decline, bee’s vulnerability apparently with to an neonicotinoids accumulated in impor- evidence particular. on ever, little information is available regardingof the reduced-risk insecticides potential to impact wild bees andbut the even few to studies bumblebees, available indicate the potentialtial for the substan- impact of somefurther such attention. pesticidal compounds, which deserves ferences between the insecticide susceptibility of honeywild bees bees and have been recognised. been the focusincrease of in studies attention, with but solitarytors, bumblebees bees although have and been the there other centre wild of has attention. bee pollina- been an injunctive suspension of the aerial applicationissued of in insecticides 2012 was byRenewable the Natural Brazilian Resources (IBAMA), Institute from of theof Brazilian the the Ministry Environment Environment, and and was subsequently reviewedadditional with a studies call for on the honey2012, bee Ofício (DOU Circular/12/CGASQ/DIQUA No. 192DOU of of No. November 3 3 of 2012 October 4no and January records 2013). of An honey important beeor shortcoming decline elsewhere. is exist that There in arewhere Brazil a nearly or few 30% Latin of exceptions, America, colony suchto a losses as social were parasite, South suggesting registered a as Africa, differentexperienced being set in of the due causes Northern than Hemisphere. those Africanised honey bees provedtheir European to counterparts in be Latin dominant, Americaing and outcompeting throughout quickly spread- the regionbee and genotype becoming in one the ofcurrently prevailing the recorded. honey most While successful some biologicalin typical invasions Africanised traits honey thatness, bees, are such foraging prevalent as behaviour,their a colony likelihood high hygiene, level ofbees etc., of decline in may aggressive- the as minimise Unitedassessed. observed States and with parts European of honey Europe, it remains to be introduced and flourished forspecies several were years. subsequently The replacedhoney European by bee sub- hybrids breeding from effort athe after Brazilian African the honey escape bee of some subspecies swarms of Science Hum Ecol Crop Prot Annu Rev PLoS ONE ). 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The financial support provided bycil the of National Scientific Coun- and Technological Development (CNPq), theFoundations CAPES (Brazilian Ministry of Education), thecil Research of Coun- Ghent University (BOF-UGent) andAgency the for Flemish Innovation Government by Science andis also Technology (IWT, greatly Belgium) appreciated. ity (EFSA) and the US Environmentallatter Protection Agency in (EPA), the aRegulatory joint Agency effort and withRegulation, the Health refer to California tiered Canada’s assessments on Department other Pest importanttors pollina- of Management such Pesticide as bumblebees and solitary bees. eral of the existing gaps in knowledgebeen regarding scrutinised, and honey the bees level have of knowledgeing has some improved, allow- congruence in guidingprocess. the Even regulatory the decision-making initial andinsecticides extensive has improved, focus and attention on has been a shifting, single encom- passing group other groups of of insecticides, fungicides and pesticidetures, mix- which seems paramount inrisk the whole assessment pollinator–pesticide scenario. 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