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1171 or honey A. mellifera 60% AI) was 15–20 = than other insects, are 21 ll, Cornell University, Ithaca, NY, USA rtment of Entomology, Comstock Hall, 2010 Society of Chemical Industry c owing to their ‘extreme susceptibility’, and other insects to determine the relative sensitivity to compared with other insect species has 8,15 f the six classes of insecticides (, nicotinoids, included. or technical-grade material (minimum purity ay 2010 Published online in Wiley Online Library: 29 July 2010 icides, they are not a highly sensitive species to insecticides Correspondence to: Jeffrey G Scott, Depa Cornell University, Ithaca, NY 14853-0901, USA. E-mail: [email protected] Department of Entomology, Comstock Ha to insecticides, although no comparative toxicology study To date, no comprehensive review of the susceptibility of ∗ ∗ ure review was conducted, using data in which adult insects bees being particularly sensitive to insecticides becauselower they total have numbers of cytochrome P450s indicators 2 MATERIALSThe AND guidelines METHODS used toinsecticides were assess as how follows: sensitive honey bees are1. to Only literature in which adult topical assays using analytical- A. mellifera been reported. Therefore, the goal of thistoxicity paper was data to summarize of insecticidesA. mellifera in a comparativeof manner honey between bees toliterature were insecticides. reviewed, the relative Toxicity sensitivities of data62 honey bees insecticides obtained to from from six the classesof these were findings compared were and examined. implications often made with no citations given. cticides on honey bees have been frequently noted. It has been 1 view was to summarize toxicity data between The 11,12 14 In spite of the number of bees and/or honey contamination. 9,10 L.) are among the most important pollinators in natural and agricultural settings. more sensitive to insecticides ethroids and miscellaneous) examined. in the United States, and Bee poisoning observations 5 8,13 or in pollen loads. Apis mellifera 8 L.) are invaluable to the operation : 1171–1180 www.soci.org in the United Kingdom. Honey bee declines 66 7 to $14 560 million 6 Apis mellifera 2010; 6 comparative toxicology; ; ; ; The economic value of honey bees as pollinators ranges

2–5 Apis mellifera

2010 Society of Chemical Industry Honey bee exposure to insecticides has primarily been While honey bees are unquestionably exposed to various c have been recorded since the late nineteenth century. can have a direct impactcommodity on foods. the food market and on the price of measured by worker mortality in theof field, residues as from well as the by bee detection body , statements about honey bees serving as environmental economic impact of honeyof bee the kills Bee resultedmandates/requires the in Indemnity USDA the to Act legislation have pay of ‘occurred beekeepers for 1970 aswhich losses had that (Pub. a been registered result L. andGovernment’. approved of 91–524) for use the by which the use Federal of economic poisons Pest Manag Sci interpretation of insecticide residue levelshas on bees created and some indirect pollen debate cause of honey regarding bee deaths. whether exposure is the of commercial agriculture, to thepollination and propagation to human of society plants by producing through Overall, various products. the directagriculture are and estimated at indirect $10–33 benefitsStates. billion annually in provided the United by bees to 1INTRODUCTION Honey bees ( than other insects? Abstract BACKGROUND: Honey bees ( Melissa C Hardstone and Jeffrey G Scott (wileyonlinelibrary.com) DOI 10.1002/ps.2001 Is Review Received: 17 February 2010 Revised: 26 May 2010 Accepted: 27 M lies at £190 million evidence that foraging beesand may are be exposed exposed to during field applications residues of pesticides, from $80 million They commonly encounter insecticides, and the effects of inse suggested that honey bees may be (as a species) uniquely sensitive has been undertaken to examinewere topically this treated claim. with An insecticides. The extensive goal literat of this re Keywords: and other insects to determine the relative sensitivity of honey beesRESULTS: to It insecticides. was found that, inexamined. general, In honey addition, bees honey were beesorganochlorines, no , more were pyr sensitive not than more other sensitive insect species to across any the o 62CONCLUSIONS: insecticides While honey bees can be sensitive to individualoverall, insect or even toexposure, specific so classes as of to minimize insecticides. possible However, declines all in pesticides should be used inSupporting information a may way be found that in minimizes the online honey version bee of this article. for the A. florae 50 ranked in A. mellifera : 1171–1180 compared with 66 for the honey values available to 50 50 2010; for the other insects for the honey bee to Fabricius and 50 50 range of the honey bee Aphis mellifera Apis mellifera A. mellifera 50 A. indica range of the other insect species Pest Manag Sci 50 (Table 2). , whereas the average LD 1 1 − − gg gg µ µ means and ranges, but the averages were 4 . species such as , while the average LD 50 1 − (Table 2). The average LD Apis 1 gg tended to be of average or less sensitivity overall − µ gg µ Therelativesensitivityrankingof 83 . other insect speciesare to divided carbamate into and the total neonicotinoid number insecticides. of insect Bars species LD larger, indicating that,sensitive (Table overall, 1). The the honey bee ranked othersensitivity in the middle to species for species wereof and not these as insecticides, the (Fig. 1). average For LD both for that insecticide.compared Shaded with the boxes other insect indicate species. the position of was 1 was 236 Figure 1. with honey bee LD other insects was 11 the middle for sensitivity to three organochlorines:and , . Of the other insects examined for susceptibility to (Table 1). Other bee was 120 overlapped with the average LD Fabricius rank as more sensitive than and equally sensitive tospecies thiamethoxam of (Table the 1). other Themore insects or individual less tested sensitive showed to no (Table 1). pattern of being 3.4 Organochlorines Apis mellifera to organochlorines when compared with the(Fig. other 2). species tested There were fourandmethoxychlor,wherethehoneybeerankedinthebottom50% insecticides, , DDT, of sensitive species. In fact,species the to honey endosulfan (out bee of three was species) and the methoxychlorof least (out four sensitive species). For endosulfan, the average LD 1 is ´ e) − was gg 62) for of 2.64 ranges of 24.3 µ Bouch 50 = 50 50 n www.soci.org MC Hardstone, JG Scott was ranked 2010 Society of Chemical Industry A. mellifera c 50 Apis mellifera was the most sensitive to insecticides ( was about equally sensitive Ctenocephalides felis value was included. (most likely to reflect the value of a A. mellifera 50 50 values, the average for that species derived from the other three species A. mellifera compared with an average LD Apis mellifera values were reported on a per insect 50 1 1 values of the other insect species (if one − − 50 values from three or more insect species. 50 gg gg µ 50 equivalents were calculated using published L.) and cat flea ( µ 1 − was among the most sensitive species for three of gg µ . values from all insect species were converted to tions, only the lowest LD susceptible strain) was included. or resistance level determinationsthe of susceptible strain field LD populations, only 50 In cases where LD Musca domestica 3.3 Neonicotinoids Apis mellifera tended to be the least sensitiveconsistently species. most No sensitive particular (Table species 1). was the five neonicotinoids, compared with(Table the S2). other Honey species bees tested any of were the not neonicotinoids. thebee The most to sensitivity , sensitive rankings imidacloprid of species and50%. the nicotine to For were honey these all three in neonicotinoid the insecticides, top the LD in relation to the LD (Table 1 and Table S1). Of the( other insects examined, the housefly was used) in order toA. mellifera obtain the sensitivity percentile ranking of species had multiple LD (range 1.00–4.28) body weights ofand references the in specificapproach, the an species extensive supporting search of or the information).honey literature for In bees insect toxicity was data the on conducted, type following present literature the (details was above guidelines. then The using searched for insecticides toxicity forThe data which insecticides on that other honeythat insects were bee contained included data LD in were this review available. were those wileyonlinelibrary.com/journal/ps 3.2 Carbamates In the case of carbamates, highly sensitive to insecticides relative to other insects.25, There 10 were and 27 cases wherethe the honey middle bee or was the in theThere top bottom were 50% 50%, five of cases thespecies, where sensitive and nine species cases respectively. where it was the least sensitive species. the most sensitive species to , with a mean LD 3RESULTS 3.1 Overall observations The relative sensitivity of which there were available data is shownS1 in Figs to 1, S6 2 and in 3classes (Tables the of insecticides supporting there information). was Overall, no across evidence the that six measurements based on the average weight of thatFor insect species. each insecticide, the average honey bee LD 2. If data were obtained from multiple field-collected popula- basis, the associated with the other species examined often overlapped (range 8.09–52.2) LD 3. If data were obtained from a study on resistance mechanisms overall compared with the other species tested (Fig.three 1). There (, were methomylcarbaryl) and ), and two threecases ( (bendiocarb, where and the honey bee and wasthe in maxacarbate) top the 50% of bottom the 50%, sensitive the species respectively. middle or

1172 1173 ; ; ; ; , but Apis 22 Nabis ;A.tri, ;C.bal, ;L.hes, Bombus Tribolium H.arm, ,N.per, Oncopeltus ;A.ind, (plain font); ;N.ame, B.ter, M.dom b,c,d ;B.luc, L.dec, N.per, ;T.cas, C.fel, M.per, Phymata fasicata M.cro ;O.fas, Galleria mellonella B.ter, O.fas, O.fas, L.dec, , A.ste, C.qui, D.vir, L.dec, M.dom, , ) Coleomegilla maculate A. mellifera 1 Crioceris asparagi ;P.fas, Melanoplus differentialis − , B.vag, B.ger, D.vir, L.dec, A.aeg, C.qui Anastepha suspense of , M.dom C.fel ;G.mel, , ,A.ind,A.flo, gg 50 Diabrotica undecimpunctata µ ( A.aeg, V.pen, A.ery, M.rot, O.fas, B.ter, C.fel, M.dom M.dom, D.vir N.per, T.nig, M.dom P.aus, P.ame, B.asa, P.ful, A.aeg M.dom, C.fel A.qua, L.dec, N.mel, T.irr, H.con, A.erv, A.aeg, C.vir, C.qui, M.rot, B.ger, M.dom B.ger, P.ame, P.jap, T.mol C.vir, T.irr LD Anopheles gambiae Vespula pensylvanica ;C.mac, ;M.dif, 50 Leptinotarsa decemlineata ;A.sus, T.aur, A.pis, A.ind, A.flo A.ste, A.aeg V.pen, B.dor, S.fru, M.bee, M.dom T.aur B.ger, B.asa, C.fel L.hes, A.qua L.hes, B.ori, A.ste, I.ver, P.bru, A.gam L.dec = Crysopa rufilabris/oculata/carnea Blattella germanica ; H.par, Hippodamia parenthesis; Toxoptera aurantii Megachile rotundata spp.; C.asp, ;D.und, wileyonlinelibrary.com/journal/ps ;V.pen, Neolygus quercalbae ;A.gam, ;L.dec, ;B.ger, ;T.aur, ;M.rot, ; C.r/o/c, Bombus Formica sanguine Periplaneta brunnea ;N.que, of other species Apis florae ;Bom, Ctencephalides felis Crotalus viridis .10–85.0 A.ery, M.rot, O.fas, ;P.bru, Microplitis croceipes 50 Anopheles stephensi Hippodamia glacialis spp.; F.san, Ichnura vericalis ); LD ;A.flo, was the least sensitive species to bromophos (four ;C.fel, ;C.vir, Bactrocera dorsalis Macrosiphum pisi ;A.ste, ;M.cro, ;H.gla, Spodopterafrugiperda Blattella vaga Tetraopes tetrophthalmus Culex quinquefasciatus italic font spp.; I.ver, ; B.dor, ( ;M.pis, ;S.fru, Mean Range Species There are multiple types of organophosphate insecticides, ;T.tet, ;B.vag, ;C.qui, they can generally be classified as those(e.g. that phosphorothionates) and require those bioactivation that do not (e.g. phosphates). 11, four and 12 cases where the honeythe bee was middle in the or bottom 50%, theApis top mellifera 50% of thespecies), mipafox sensitive (four species), species (three respectively. species) and sulprofos (four species). Honey bees were theorganophosphates, most sensitive azinphos-methyl species (four to two species)(four species). and Colias eurytheme Enellagma/Ishnura Andrena erythronii Periplaneta australasiae Nannotrigona perilampoides Melipora beecheii A. mellifera Coccinella trifasciata Hydrophilus of a Myzus persicae ;A.ery, Blatella asahinai n ;P.aus, 50 ;Co.eur, Trigona nigra ;N.per, ;Ene/Ish, ;C.tri, LD ; M.bee, Anopheles quadrimaculatus Hippodamia convergens < Bombus terrestris ) Other species LD ;M.per, ;B.asa, 1 2010 Society of Chemical Industry ;T.nig, − c Phthorimaea operculella gg Aphidius ervi ;A.qua, ). ;H.con, µ ;Bo.ter, ( 50 Coriscus eurinus ;P.ope, Nomia melanderi LD ;A.erv, )tendedtobethemost Chauliognathus pennsylvanicus Melanoplus differentialis of other species Locusta migratoria Periplaneta americana bold font ( ; Hep, Heptageniidae; Hyd, Bombus agrorum 50 ;C.eur, Tenebrio molitor Epicauta pennsylvanica ;N.mel, and other species to carbamate and neonicotinoid insecticides Dallas) tended to be the least ;C.pen, Bombus terricola ;L.mig, Coccinella transversoguttata ;P.ame, ;B.agr, Heliothis armigera ;T.mol, ;E.pen, Melanoplus femur-rubrum Apis mellifera Acyrthosiphon pisum Popillajaponica M.domestica A. mellifera ;B.ter, ;C.tra, Adalia bipunctata of 50 ;A.pis, ;P.jap, ;H.arm, to insecticides www.soci.org Apis mellifera ;M.fem, Ceratonia catalpa LD : 1171–1180 ;A.bip, > Lygus lineolaris Nemobius fasciatus 66 Acalymma vittata determinations. ;C.cat, Oulema melanopus Trigona irridipenis values of 50 Oncopeltus fasciatus Diabrotica virgifera ; L.lin, Blatta orientalis 50 2010; A. mellifera Conotrachelus nenuphar Agrotis ipsilon ;N.fas, ;A.vit, LD ; T.irr, ;O.mel, Aedes aegypti Musca domestica ;D.vir, ;B.ori, Geocrois punctipes values listed in increasing order. LD Cercopis sanguinolenta ;A.ips, Hippodamia tredecimpunctata tibialis Periplanetafuliginosa of other species ;C.nen, 50 50 References are provided in the supporting information. A.aeg, Number of LD LD castaneum americoferus M.dom, Lygus hesperus fasciatus H.tre, P.ful, G.pun, lengi C.san, howardi Collops balteatus lucorum Anasa tristis indica LD c d a b Carbamates AldicarbAminocarb 2.36 4.40 1.52–2.85 0.850–11.2 3 3 21.4 3.61 1 1.71–5.50 L.dec, Insecticide Mean Range Table 1. BendiocarbCarbaryl 2.64 7.87Mexacarbate 1.00–4.28 0.53–18.4 1.77 2 15Imidacloprid 24.3 0.477–3.08 132 8.09–52.2 6 0.403 0.35–900 17.7 0.128–0.750 12 0.986–66.3 A.ery, 8.23 M.rot, 0.001–133 CarbofuranMethomyl 1.55 14.0 1.49–1.60 12.9–15.1 2 2 3.18 27.81 0.920–5.36 0.900–162 PropoxurNeonicotinoids Dinotefuran 11.4 7.21–13.5 0.220 3 n/a 36.7 1 0.320–478 5.42 0.180–13.8 Nicotine 173 30.0–315 2 777 150–3200 O.fas, A.tri, NitenpyramThiamethoxam 1.10 0.202 0.067–0.299 0.810–1.38 3 2 0.431 0.970 0.001–1.34 0.230–1.70 Sensitivity of Pest Manag Sci organochlorines,thehousefly( 3.5 Organophosphates Honey bee sensitivitytended to to rank in the organophosphates middle for sensitivity was(Fig. relative 2). to other variable, Out species of but the 27 organophosphate insecticides, there were sensitive species and theThomas) grasshopper was ( similar inmilkweed bug sensitivity ( to thesensitive (Table honey 2). bee, while the C.fel, G.pun, H.con, : 1171–1180 O.fas, D.vir 66 G.pun, N.ame, B.asa, S.cal, A.aeg, A.qua, A.pis, M.rot, A.qua, P.ame, M.dom, B.ter, 2010; N.mel, B.asa, B.ger, b,c,d N.ame, M.cro , I.ver, V.pen, A.ste, , V.pen, G.mel, O.fas, D.vir B.agr, B.luc, Bo.ter, C.fel ) ,Ene/Ish, , M.dom, , 1 D.vir , − B.dor, M.cro, T.cas, M.dom, M.rot B.ger gg , M.cro ,P.ame, µ , C.r/o/c, M.dom, H.con, , , M.dom, ( , C.bal, C.r/o/c, H.con, M.dom, B.ger, H.con, P.ame, C.pen, Pest Manag Sci , 50 D.vir, O.fas T.cas M.rot , M.dif, B.ger, V.pen, A.qua, , M.dif, P.ame, A.ste, B.agr, B.luc, Bo.ter, M.dom M.dom A.aeg, D.vir, L.lin , M.dom, , M.rot, M.fem, M.dom, L.mig, P.ame, , , ,B.dor,G.pun,N.ame,M.dom, , A.qua, A.aeg, H.arm, C.fel, O.fas, B.ger M.rot, M.dom, P.ope O.fas, M.dif O.fas O.fas H.arm, B.ger, G.pun, B.ger, O.fas H.arm, V.pen, M.bee, C.qui, H.con, D.vir, N.per, T.nig, C.fel L.hes, B.dor, B.ger, P.ame C.bal, N.ame M.dom, B.ori, P.aus, Hep, P.bru, B.ger, Bo.ter, P.ful, C.nen, M.cro, D.vir, H.con, Hyd, C.san, L.lin A.ery, V.pen, C.r/o/c, M.rot, C.bal, B.ter M.dom D.und, F.san, C.eur, N.que, Co.eur, M.fem, P.fas, T.tet, E.pen C.bal B.ger, D.vir, M.pis M.per M.dom, L.dec, M.cro L.hes, M.pis, A.sus, A.sol L.hes, M.per M.dom P.ame, L.dec, B.vag N.mel A.erv, A.qua, A.aeg M.rot, N.mel M.dom, M.dif L.dec, H.arm B.agr, B.luc, L.dec I.ver, B.dor, M.dom B.dor N.mel, M.rot N.mel, L.hes, B.ger, A.aeg, A.ste, P.ame, A.qua, M.dom M.dom, V.pen, A.qua M.dom, A.aeg, A.ste L.hes N.mel M.dom, B.agr, B.luc L.hes M.pis, M.dom C.asp, A.vit, Bom, O.fas, L.mig, M.pis, N.fas, M.dom, B.ger, M.pis H.arm, M.cro 10–29.6 A.aeg, M.rot, A.ste, A.ery, 010–106 M.rot, N.mel, C.r/o/c, H.con, nd organophosphate insecticides Mean Range Species a n www.soci.org MC Hardstone, JG Scott 2010 Society of Chemical Industry ) Other species LD 1 c − gg µ ( 50 LD and other species to organochlorine a Apis mellifera Apis mellifera values of 50 LD As per Table 1. 4.19 1.10–7.26 6 22.5 0.130–111 a,b,c,d InsecticideOrganochlorines Aldrin Mean Range 3.26 1.49–4.50 4 232 1.38–1140 Table 2. Chlordane 40.1 14.0–88.0 5 273 6.04–1660 Methyl 1.76 0.610–3.24 8 1.86 0.490–5.28 1.79 n/a 1 2.27 1.12–3.41 DFPDiazinonDimethoate 2.10 30.0 1.37–3.72 1.62 n/a 5 1.00–2.47 1 8.19 11 59.0 0.300–27.0 23.2 5.00–160 0.260–78.0 DDTDieldrinEndosulfanLindane 73.0MethoxychlorOrganophosphates 1.59 120Azinphos-methyl 7.00–164Bromophos 236Chlorpyrifos 1.33–2.20 2.50 11 70.0–218 1.99 0.350–5.62 6 687 39.6 0.550–4.28 5 n/a 0.847 8 4.25 7 0.090–9380 0.590–1.14 1.83 n/a 1 8.55 1.04–15.0 9.33 5 0.510–3.14 11.4 0.963–32.5 1 8.79–10.2 9.00 M.dom, A.ste, 6.20–18.9 M.dif, A.aeg, 6.91 0.280–66.7 2.32–10.3 DisulfotonFenitrothion 42.7 1.66 14.6–61.2 0.180–3.83Mevinophos 7 7 217 7.03 1.82 0.250–3.60 1. 8.00–607 5 2.16 0.025–4.85 DichlorvosDicrotophos 2.73 1.72Fenthion 0.290–5.01 0.410–3.05 4 5 3.14 13.5 41.2 3.08–3.19 2.08–25.0 0.010–124 2 M.dom, 4.15 1.30–11.3 -S-methyl 4.98 2.60–9.37 5 9.55 0.285–16.7 Demeton 17.3 11.1–26.0 4 52.1 0.300–147 TEPPTrichlorfon 24.0 0.410 5.81–36.7 0.010–1.20 4 3 472 0.814 0.037–1.59 0.430–3290 N.mel, MipafoxNaledParaoxonParathion 57.3Phorate 0.600 2.93Phosphamidon n/a 1.00–4.85 n/a 1.36 4.89 2 2.45 1 0.100–3.50 0.020–14.5 1 0.910–3.20 16.0 1.46 7 3 1.21 4 1.08–1.84 6.62 7.89–20.0 22.8 0.030–4.50 6.27 M.dom, 0.020–47.0 B.dor 0. 4.27–8.26 SulprofosTemephos 72.0 14.8 14.0–15.5 n/a 2 1 288 34.1 0.110–478 13.4–54.7 wileyonlinelibrary.com/journal/ps

1174 1175 L., )are L. were was about C. felis Aphis mellifera Aedes aegypti A. mellifera Culex quinquefasciatus Say) and cat flea ( wileyonlinelibrary.com/journal/ps Say and Leptinotarsa decemlineata values. Thus, for insecticides with a smaller number of 50 to (seven species)allethrin (seven and species) the and least cyhalothrinFor (nine sensitive the species) species (Table for to 3). beetle which ( data concerning Coloradoavailable, potato the sensitivity ranking ofthan these that species of tends the to honey bee be (Table less 3). 3.7 Miscellaneous insecticides In the case ofone miscellaneous of the insecticides classes (thoseequally previously not sensitive referenced), fitting overall compared into with(Fig. the 3). other There species were tested two,sensitivity zero ranked and three in50% cases the of where the bottom honey sensitive species bee 50%,most respectively. The sensitive the honey species bee middle to wassensitivetorotenone(fivespecies)(Table3).Analysisoftheother the or (eight the species) top andinsects tested the showed least that the mosquitoAnopheles species quadrimaculatus all generally less sensitive than the honey beeinsecticide to the compounds miscellaneous (Table 3). 4A DISCUSSION limitation to thisthere type is of analysis notLD is that a for large every insecticide number of species that have reported values available for that insecticide. Shaded boxes indicate the position of 2010 Society of Chemical Industry 50 compared with other insect species to organochlorine and organophosphate insecticides. Apis mellifera c Apis mellifera was the most sensitive species was the least sensitive species to two of to insecticides www.soci.org : 1171–1180 Apis mellifera 66 2010; A. mellifera was about equally sensitive to a variety of pyrethroids Apis mellifera Therelativesensitivityrankingof For organophosphates that require activation, honey bees were Sensitivity of Bars are divided into the total number of insect species LD compared with the other insect species. Pest Manag Sci For those organophosphates for which activationhoney is bees not required, were notfive, uniquely two sensitive and overall,bottom 50%, as five the there middle cases were orrespectively. the where top 50% the of the honey sensitive species bee was in the Figure 2. compared with the otherwas species in tested (Fig. the 3). bottomtwo The 50% honey pyrethroids bee for and fivethree pyrethroids. pyrethroids, in in the the middle top for 50% sensitivity ranking for 3.6 Pyrethroids Apismellifera was the least sensitive species to(bromophos-methyl two and of these sulprofos), organophosphates andspecies was to two the of most thesephorate). organophosphates sensitive (azinphos-methyl Examination and ofpattern the of an other individual insectssensitive species to these tested being organophosphates consistently (Table showed 2). more no or less these organophosphates (mipafox and naled). Examination ofother the insects tested showedbeing no consistently pattern of more an or(Table individual 2). less species sensitive to organophosphates not uniquely sensitive overall,cases as where there the were honey seven,or bee two the was top and in 50% six of the the bottom sensitive 50%, species respectively. the middle ) Bombus Bombus put forth : 1171–1180 26 and 66 L. and Bombus agrorum Apis 2010; B. lucorum L., Pest Manag Sci B. terrestris ) such that they can be used around bees are generally as sensitive to insecticides as 1 − Kirby, 23,25 noted that the low toxicity of pyrethroids to wild gbee µ A. florae 27 0 (Table 1). Conversely, bumble bees ( . B. terricola this does not reflect a greater sensitivity to insecticides. and 11 21 > 50 Inglesfield To gain a greater understanding of the relative sensitivity of Based on the available literature using adult topical bioassay spp.) tended to becompounds less sensitive across than the theeconomic insecticide honey and bee agricultural classes impact to of (Tables various bees) 1 honey bees is to (and enormous. other 3). wild sensitive While The to they insecticides as doshould a not be species, used all appear in pesticides a toas are way to be toxic that minimize and minimizes uniquely declines honey incontamination. bee the exposure, number so of foragers and/or honey with minimal harm. the interesting hypothesis that pesticides thatkill the are foraging fast bees acting quickly and provide aand means the by rest which of the brood the colonyof will exposure. not However, be foragers exposed with tocuticle insecticide the and residues toxic in on effects their their pollenpollen load may contain do naturally return occurring toxic to allelochemicals. Thus, thethe hive. idea In that addition, honey beesa are uniquely way sensitive to to insecticides preventappear as to be from likely. reaching hive members does not honey bees, it wouldand/or be bioassay desirable endpoints to otherinsufficient evaluate than other information mortality. life Unfortunately, stages susceptibility is of larval honey bees available to other insect species.insects, to For social insecticides that evaluate have sublethal effectspresent the on problems behavior could to relative thethese colony, effects are although sparse and comparative do not data permitsensitivity an analysis for relative of to honey bee other species. Atkins and Kellum ACKNOWLEDGEMENTS The authors thank the Cornell Universityassistance. library This staff for work technical wasInsect supported Physiology and by Toxicology. the Sarkaria Institute of SUPPORTING INFORMATION Supporting information may be found in thearticle. online version of this data, it was foundsensitive that, to in insecticides general,true than honey that other bees honey bees were insectinsecticides, can no species. it be more is While particularlysensitive sensitive not it to species the is individual case tothough that honey all they bees insecticides. have aregenes, This a among lower suggests the number most that, of cytochrome even P450 bee populations in the fieldlevels was not of comparable toxicity with the observedanalyses. higher to These the types sameassessment of chemicals of finding in laboratory can beeimportance create of sensitivity comparing equivalent uncertainty to toxicity data in within insecticides,to a the species multiple highlighting insecticides. the The toxicities associated with other bee species ( were also compared. Although the data are extremely limitedtwo (only neonicotinoid insecticides, imidacloprid and thiamethoxam), A. indica A. mellifera Fabricius, conducted properly. Pesticides in group 3(LD are relatively non-toxic and 23 ., in which A. mellifera www.soci.org MC Hardstone, JG Scott et al 12 2010 Society of Chemical Industry compared with values available c values (Tables 1 50 to an insecticide 50 Apis mellifera Group 1 pesticides are highly A. mellifera ), causing severe bee losses 24 1 − (Figs 1 to 3) rather than considering ) compounds are moderately toxic and gbee 1 µ − 99 . A. mellifera gbee µ 001–1 . 99 . 0 50 Therelativesensitivityrankingof 0–10 . 2 50 Many previous reports on honey bee sensitivity have not the number of timesusing a it direct was comparison the of most/least the averaged sensitive LD species or to 3). incorporated the comparative aspectbecause often addressed the in susceptibility this of review, has been describedraw using data. a The hazard hazard indicator scale rather was than used with by Johansen, toxic (LD insecticides were categorizedclasses’. The into classes general were further ‘poisoning defined hazard by Atkins for that insecticide.compared Shaded with the boxes other insect indicate species. the position of if applied when(LD bees are present at treatment time, Group 2 wileyonlinelibrary.com/journal/ps species in which(owing comparisons to are a possible, randomappear sampling there uniquely error) sensitive is thatfor or a the insensitive. the chance honey This bee presentto may could analysis, be be the because thenine case most the of these or honey (bendiocarb, leastmethyl, endosulfan, bee bromophos, sensitive methoxychlor, mipafox, was azinphos- naled, species phorate found were and in suprofos) less there 14 than cases,conclusions five and were species in drawn, compared.relative ranking greater of For weight this was reason, when allotted to the Figure 3. other insect speciesare to divided pyrethroid into and the total miscellaneous number insecticides. of Bars insect species LD the following definitionsEnvironmental Protection were Agency. adopted by the United States can be used in a location where bees are present if application is

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The Health of Livestock an - 0.400 0.300–0.500 2 1.15 0.280–2.40 B.ger, 1 Allen-Wardell G, Bernhardt P, Bitner R, Burquez A, Buchmann S, 4 Southwick EE and Southwick L, Estimating the economic value of 2 Losey JE and Vaughan M, The economic value of ecological services 3 Pimentel D, Acquay H, Biltonen M, Rice P, Silva M, Nelson J, 5 Morse RA and Calderone NW, The value of honey bees as pollinators 6 Pimentel D, Andow D, Dyson-Hudson R, Gallahan D, Jacobson S, 9 Chauzat M-P, Faucon J-P, Martel A-C, Lachaize J, Cougoule N and 7 8 Greig-Smith PW, Thompson HM, Hardy AR, Bew MH, Findlay E and CyhalothrinCypermethrin 0.270 1.18 0.200–3.70 n/a 4 1 1.13 0.045 0.003–6.10 0.011–0.079 DNOC A.bip, C.mac, M.dom, O.fas, H.tre,RH-7988 H.par, D.lon, O.mel, 31.7 26.2 n/a n/a 1 1 25.0 81.3 10.0–35.0 0.520–203 360 120–600 2 22.1 2.00–42.5 Cyfluthrin 0.677 n/a 1Pyrethrins 1.10Other SpinosadDiafenthiuron 0.290–2.69 1.28 15.0 0.402 0.460–2.10 0.025–0.780 2 n/a 3 25.9 3.20 1 7.00–50.0 27.03 0.580–13.4 M.rot, 11.12–48.0 N.mel, DeltamethrinFenvalerate 0.440Permethrin 2.45 0.370–0.510 0.800–4.08 2 1.18 4 0.600 0.173–2.02 23.6 0.018–2.38 5 0.022–376 15.8 0.100–318 α 0.100 n/a 1 1.35 0.077–6.50 a,b,c,d Pyrethroids Allethrin 47.0 34.0–60.0 2 13.7 1.60–46.0 Insecticide Mean Range Table 3. 11 Koch H and Weißer P, Exposure of honey bees during pesticide 10 Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, van Sensitivity of Pest Manag Sci REFERENCES ) J J J Pestic Pestic Musca JEcon adults. 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