TheImpactoftheNation smost WidelyUsedInsecticidesonBirds

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1 TheImpctoftheNtion smost WidelyUsedInsecticidesonBirds

2 Neonicotinoid Insecticides nd Birds The Impct of the Ntion s Most Widely Used Insecticides on Birds Americn Bird Conservncy, Mrch 2013 Grsshopper Sprrow by Luke Seitz Cover photos: orned Lrk nd chicks by Middleton Evns; Corn field, stock.xchng, sxc.hu; Clico Pennnt drgonfly by Dvid Cppert, Michign Stte University, Bugwood.org 1

3 Neonicotinoid Insecticides nd Birds Americn Bird Conservncy would like to thnk the Turner Foundtion, Wllce Genetic Foundtion, Jeff nd Connie Woodmn, Cornell Dougls Foundtion nd A.W. Berry Foundtion for their ongoing support for Americn Bird Conservncy s Pesticides Progrm. Written by Dr. Pierre Mineu nd Cynthi Plmer Designed by Stephnie von Blckwood About the Authors Dr. Pierre Mineu begn his long nd distinguished scientific creer studying the effects of persistent orgnochlorine compounds, like DDT nd PCBs, on fish-eting birds. e then becme responsible for the Cndin ssessment of new nd existing pesticides to determine their dverse impcts on wildlife. In 1994 he trnsitioned from regultory reviews to full-time reserch on the environmentl impcts of pesticides, chieving the rnk of Senior Reserch Scientist t Environment Cnd. Working with interntionl collbortors nd grdute students, he works on ssessing globlly the environmentl footprint of pesticides. e lso studies how birds re exposed to pesticides nd how bird popultions respond to pesticide use nd griculturl prctices. is work includes defining the ecologicl vlues of birds in croplnd s well s estimting the incidentl tke of birds from vrious other humn ctivities. e hs written more thn 100 peer-reviewed publictions nd hs uthored some 200 presenttions. e officilly retired from public service in 2012 nd now holds n Emeritus position with the Cndin government, serves s n djunct reserch professor t Crleton University in Ottw nd t the University of Ssktchewn in Ssktoon, nd consults privtely. Cynthi Plmer hs worked in the environmentl ren in the US nd interntionlly - in the executive nd legisltive brnches of government, in non-profit orgniztions, nd in the news medi. She hs been involved in pesticide issues for mny yers. She co-uthored report on pest control for the Congressionl Office of Technology Assessment, dvocted for sfer lterntives with the World Wildlife Fund, nd helped plce pesticide issues in the ntionl spotlight s senior editor of the dily news service, Environmentl elth News. er other work hs delt with chemicl contmintion, griculture nd food sfety issues, worker helth nd sfety, ir nd wter pollution, nd climte nd energy policy. Cynthi received her AB from rvrd College in 1988 mjoring in environmentl nd public helth policy, her JD from rvrd Lw School in 1993 with n emphsis on environmentl lw, nd her MP from the rvrd School of Public elth in 1994 concentrting in environmentl nd occuptionl helth. Acknowledgments We wish to thnk John Struger, Christy Morrissey nd their respective collegues for ccess to unpublished residue informtion. Jim Devries nd Peter Jenkins were relentless in their zel to ferret out the ltest publictions. We re grteful to Frncisco Snchez-Byo nd enk Tennekes for meeting nd shring their insights into the neonicotinoids nd other systemic insecticides. A huge thnk-you to Theo Colborn nd Lynn Crroll t The Endocrine Disruption Exchnge for offering their dt nd helping us sort through the implictions. Robert Miller, Shron McBride nd others t EPA helped fcilitte our ccess to EPA dt. Scott offmn Blck nd Lriss Wlker offered vluble guidnce. 2

4 Neonicotinoid Insecticides nd Birds SYNOPSIS First introduced in the 1990s in response to widespred pest resistnce s well s helth objections to older pesticides, the neonicotinoid insecticides quickly siled to the top slot in globl pesticide mrkets. Now the most widely-used insecticides in the world, it is difficult to find pest control commodities tht do not contin one or severl of the neonicotinoid insecticides. Cliforni lone hs registered nerly 300 neonicotinoid products. Neonicotinoids toxicity to bees nd other insects hs brought them the most ttention so fr nd hs dominted recent concerns of regultory institutions worldwide. In the United Sttes, the Environmentl Protection Agency s registrtion review of the neonicotinoids is focused on the thret to insect pollintors. The seriousness of this issue should not be underestimted, s one-third of the U.S. diet depends on these insect pollintors. But much more is t stke. The environmentl persistence of the neonicotinoids, their propensity for runoff nd for groundwter infiltrtion, nd their cumultive nd lrgely irreversible mode of ction in invertebrtes rise environmentl concerns tht go well beyond bees. This report reviews the effects on vin species nd concludes tht neonicotinoids re lethl to birds s well s to the qutic systems on which they depend. A single corn kernel coted with neonicotinoid cn kill songbird. Even tiny grin of whet or cnol treted with the oldest neonicotinoid, imidcloprid, cn poison bird. As little s 1/10 th of corn seed per dy during egg-lying seson is ll tht is needed to ffect reproduction with ny of the neonicotinoids registered to dte. Birds depend hevily on the qutic systems t the bottom of the food chin. But neonicotinoid contmintion levels in surfce nd groundwter in the US nd round the world re strikingly high, lredy beyond the threshold found to kill mny qutic invertebrtes. EPA risk ssessments hve gretly underestimted this risk, using scientificlly unsound, outdted methodology tht hs more to do with gme of chnce thn with rigorous scientific process. Mjor risk concerns rised by scientists both inside nd outside the gency pper to hve gone unheeded in gency registrtion decisions. The older insecticides tht the neonicotinoids lrgely replced including orgnophosphtes such s dizinon nd chlorpyrifos, nd crbmtes such s crbofurn nd methomyl were highly dmging to people nd wildlife. Wht is so disturbing is tht in their rush to register 3

5 Neonicotinoid Insecticides nd Birds lterntives, regultors hve pproved more nd more neonicotinoid products for n ever-growing number of uses without regrd to the red flgs rised by their experts concerning this persistent, cumultive, irreversibly-cting new clss of pesticides. Neonicotinoids re currently under registrtion review by EPA. The Agency s decision to pprove, restrict, suspend, or cncel these powerful insecticides will hve profound environmentl nd economic impct. We hve smll window of opportunity in which to ct; EPA s next review of this clss of pesticides will not occur for t lest 15 yers, nd the dmge done in those intervening yers will be irreversible. The results of this study nd others hve led Americn Bird Conservncy nd prtners in the Ntionl Pesticide Reform Colition to urge the EPA to tke the following ctions: - Suspend ll pplictions of neonicotinoids pending independent review of these products effects on birds, terrestril nd qutic invertebrtes, nd other wildlife. - Expnd its re-registrtion review of neonicotinoids beyond bees to include birds, qutic invertebrtes, nd other wildlife. - Bn the use of neonicotinoids s seed tretments. - Require tht registrnts of cutely toxic pesticides develop the tools necessry to dignose poisoned birds nd other wildlife. Sunflower field, stock.xchng, sxc.hu 4

6 EXECUTIVE SUMMARY Neonicotinoid Insecticides nd Birds The neonicotinoids represent reltively new group of insecticides. They were introduced in the erly 1990s to counter widespred resistnce in insect pests nd incresing helth nd sfety objections to the orgnophosphorous insecticides. Although of lower cute toxicity to vertebrtes thn the ltter, the neonicotinoids longer persistence, high wter solubility, runoff nd leching potentil s well s their very high toxicity to pollintors re plcing them under incresing public nd politicl scrutiny, especilly now tht they hve become the most widely used pesticides in the world. Their toxicity to pollintors hs brought them the most ttention so fr nd hs dominted the recent concerns of regultory institutions worldwide. The intent of this report is to review the risk tht neonicotinoids pose to birds. Birds hve borne more thn their fir shre of impcts from pesticides from the erly issues of eggshell thinning with DDT to the extensive mortlity cused by the orgnophosphorous nd crbmte insecticides tht followed. Some reserchers hve suggested tht birds my lredy be ffected by neonicotinoids nd tht, t lest in Europe, bird popultion declines cn be blmed on these populr insecticides. The min products reviewed here re cetmiprid, imidcloprid, thicloprid, clothinidin nd thimethoxm. Minor compounds include dinotefurn, nitenpyrm nd nithizine. For the ske of comprison, this report will discuss, where pproprite, number of older insecticides tht the neonicotinoids hve replced. This includes the orgnophosphorous insecticides dizinon, chlorpyrifos, mlthion, terbufos nd methmidophos, the crbmte insecticides crbofurn, methomyl, the pyrethroids tefluthrin nd deltmethrin s well s the seed tretment insecticide crbthiin. The report will emphsize US regultory history lthough it will mke reference to Cndin nd EU regultory reviews where relevnt. For ese of consulttion, summry points mde here re detiled in the body of the report under the sme section heding: 1. The history of neonicotinoid registrtions highlights mny of the criticl filings of our current pesticide registrtion system. Regultory gencies in both the US nd Cnd (nd to some extent in Europe s well) exhibited conflicted pproch to the neonicotinoid clss of compounds on the one hnd expressing serious concerns bout the persistence, mobility nd toxicity of the products on the other hnd, grnting registrtions in n ever-widening rnge of crops nd non-griculturl use sites. There is evidence the neonicotinoids got very soft ride through registrtion. Bsed on the existing record, registrtion decisions concerning the neonicotinoid insecticides were overwhelmingly positive despite consistent record of cutionry wrnings from the scientists involved in the ssessment process. Incresed concerns in the scientific nd populr literture over imidcloprid, clothinidin nd other neonicotinoid insecticides did not deter pesticide mnufcturers, who ppered to be in rce to register s mny uses s possible. It looks s if the USEPA nd other regultory gencies consistently pproved registrtions despite their own scientists repeted nd ever-growing concerns. It is relevnt to sk why we conduct scientific evlutions of products if those evlutions hve little or no bering on the registrtion decisions tht re mde, nd when stff scientists wrning of mjor risk concerns pper to be ignored. Even though severl erly reviews of the first neonicotinoid, imidcloprid, correctly identified 5

7 Neonicotinoid Insecticides nd Birds issues of bird nd mmml toxicity, persistence, runoff/leching nd qutic toxicity, regultors filed to pply some of the lessons lerned in the 1990s with imidcloprid to more recently developed compounds such s clothinidin nd thimethoxm. They lso filed (nd continue to fil) to consider the impct of combined neonicotinoid residues in the environment. Regultors hve tended to plce inordinte fith in precutionry lbelling to mitigte very serious terrestril nd qutic risks. 2. The cute toxicity of neonicotinoids to birds is lower thn the cute toxicity of mny of the insecticides they hve replced, notbly the orgnophosphorous nd crbmte insecticides. owever, EPA nd other regultory gencies worldwide hve underestimted the toxicity of these compounds to birds. This undervlution is prtly becuse the risk ssessment methods fil to ccount sufficiently for interspecies vrition in toxicity. Depending on the specific insecticide, we hve found tht EPA underestimtes toxicity by fold if the intent of the exercise is to protect most potentilly exposed bird species, nd not merely mllrds nd bobwhites, the two test species. In ddition, there is some evidence tht the neonicotinoid insecticides will debilitte birds t much reduced frction of lethl dose compred to other pesticides nd this debilittion will be longer-lsting. Smll non-lethl doses re likely to cuse prtil prlysis nd other sub-lethl effects in birds. These effects slip under the rdr screen in regultory ssessments bsed entirely on lethl levels. 3. The chronic/reproductive toxicity of neonicotinoids to birds is high. This ws recognised very erly on in the regultory reviews of the vrious ctive ingredients. Yet high reproductive toxicity in birds is typiclly ignored in the pesticide review process whether for neonicotinoids or for other pesticides. Mny pesticides fil the current reproduction screen, nd mny uncertinties exist surrounding the extrpoltion of lbortory dt to ctul field conditions. These problems re not new but regultory gencies hve filed to ddress the sitution. Becuse the neonicotinoids re systemic nd persistent in soils, nd becuse severl re used s seed tretment chemicls, they re vilble to birds in chronic fshion, mking their potentil to ffect reproduction n even greter concern. The stndrd tests crried out by mnufcturers plce reproductive effects t dosing levels rnging from 2 to 13 mg/kg/dy depending on the product. This level of exposure is esily chieved with seed tretment chemicls. owever, very recent toxicologicl informtion from Jpn suggests tht testiculr function in mle birds s well s embryonic development in the offspring of exposed mles is ffected t levels much lower thn indicted from these stndrd reproduction tests. 4. Of prticulr concern to birds re those compounds tht re used s seed tretments, primrily imidcloprid, clothinidin, thimethoxm nd cetmiprid. Regrdless of the exct lbel directions nd requirements, seed-tretment chemicls re widely vilble to birds. Seeds re never fully covered with soil, mking them esy to find by forging birds. Spills re commonplce with current mchinery. And mny species hve the bility to scrpe nd dig for plnted seed. Seed tretments, by definition, will result in high exposure sitution for birds (s well s for smll mmml species not discussed in this report). Both the EPA in the US nd Pest 6

8 Neonicotinoid Insecticides nd Birds Mngement Regultory Agency (PMRA) in Cnd hve filed t times to consider this high exposure potentil in their ssessments. 5. The mount of insecticide dhering to the verge corn (mize) seed cn result in cute intoxictions in birds with ll three registered products imidcloprid, clothinidin nd thimethoxm. With imidcloprid, single seed my prove lethl for n verge-sized bird (e.g. blue jy-sized) likely to be picking up whole corn seed from seeded fields. A few seeds only re required in the cse of clothinidin or thimethoxm. Indeed, we believe tht imidcloprid is too cutely toxic to be used s seed tretment insecticide on ny seed type bsed on our ssessment of its use in cerels nd oilseeds. Acute intoxictions in whet or cnol re less likely with clothinidin or thimethoxm becuse these neonicotinoids re less cutely toxic to birds. The birds would need to ingest greter number of the treted seeds to receive lethl dose. owever, bsed on chronic/reproduction endpoints, ll seed tretments re predicted to cuse effects given the very smll number of seeds (s low s 1/10 of seed per dy during egg lying seson) needing to be ingested to push birds into criticl rnge where reproductive effects re expected. The min uncertinty here is how long the seeds will be vilble to birds nd how long dosing is necessry before the type of effects seen in the lbortory will be seen in the wild. There re huge uncertinties for instnce wht types of effects might be seen in ltricil species (those in which the newly-htched young re born reltively helpless, such s most psserines, or perching birds) nd how this differs from effects seen in precocil species (in which the newly htched young re reltively mture, such s ducks nd geese, grouse nd phesnts). Bsed on our current understnding nd risk ssessment procedures in plce, the neonicotinoids s group hve high potentil to ffect vin reproduction. This is due in lrge prt to the very high exposure potentil tht seed tretment chemicls represent nd the persistent nture of the neonicotinoids. A publiction currently in press dvnces the hypothesis tht the neonicotinoids re contributory fctor to mny wildlife diseses through immune suppression. The uthors mke this clim on the bsis of geogrphic nd temporl ssocitions. The sheer scle nd seriousness of the issue demnds tht this hypothesis be investigted more fully. Despite industry clims, the neonicotinoids re not repellnt to birds. Any demonstrted voidnce cn be explined by hesittion before new food source or post-ingestion intoxiction nd illness. Neither is sufficient to spre birds from either cute or chronic effects. There re prllels with the cholinesterse-inhibiting insecticides where repellency ws similrly thought to reduce in-field risks. For exmple, the orgnophosphorous insecticide dizinon is extremely well voided in the lbortory. Yet, thousnds of geese nd other species hve grzed their wy to n erly deth on dizinon-treted turf. 6. The link between impcts on the insect food of birds nd declines of bird species is difficult to estblish unequivoclly, sve for the evidence linking the grey prtridge to pesticide use in the UK. A review of the existing literture suggests tht it is difficult to predict the reltive importnce of food supply during the breeding seson (i.e. when n insect food bse is criticl) compred to other risks such s hbitt loss, food supply during migrtion nd during winter, predtion or 7

9 Neonicotinoid Insecticides nd Birds even direct losses from poisoning or disturbnces such s mowing or tillge. Ech species responds to different set of stressors nd it is likely tht mny of the declines hve multiple cuses. Nevertheless, it would be foolhrdy to rgue tht drmtic losses of insect biomss from ecosystems is not going to hve potentil consequences on the integrity of those ecosystems nd on the species tht depend to vrying degrees on the spring-summer flush of insect food. The impcts on terrestril food chins from neonicotinoid (nd other systemic) insecticides my be much longer-lived nd pernicious thn those we hve seen with non-systemic products. Generlly speking, n over-efficient removl of insects in crop fields is seldom seen s mtter of serious concern by regultors especilly in North Americ. The indirect impcts of pesticides re not considered in registrtion reviews whether in the US or nywhere else in the world. In his book, Dutch toxicologist enk Tennekes (2010) mkes the cse tht the contmintion of surfce wter by neonicotinoids is so widespred in the Netherlnds (nd possibly elsewhere in Europe), tht loss of insect biomss on continentl scle is behind mny of the widespred declines tht re being seen, be they of mrsh birds, heth or medow birds or even costl species. This suggests tht we should be looking t possible links between neonicotinoid insecticides nd birds, not on frm scle, but in the context of whole wtersheds nd regions. Impcts from the neonicotinoids my very well be further field thn the rble re on which they re used, nd mny of those impcts my be medited through the qutic environment. Becuse qutic impcts re considered during product registrtion reviews, it is resonble to sk whether the potentil impct of neonicotinoids to qutic life hs been ssessed correctly. 7. Unfortuntely, North Americn regultors hve gretly underestimted the toxicity of imidcloprid nd other neonicotinoids to qutic invertebrtes. Reference doses re set using outdted methodology which hs more to do with gme of chnce thn with rigorous scientific process. A complete disregrd for the peer-reviewed literture is constnt fctor throughout the history of neonicotinoid ssessments. For imidcloprid, we believe tht scientificlly defensible reference level ( wter concentrtion t which undesirble effects re likely to be seen in resonbly sensitive species) for cute invertebrte effects (following short term exposure) is pproximtely 0.2 ug/l. Europen regultors cknowledge tht cute effects re likely t levels exceeding 0.5 ug/l. In contrst, the EPA s regultory nd non-regultory reference levels re set t 35 ug/l. Similrly, resonble reference level for effects following chronic exposure is t lest n order of mgnitude lower, or between 0.01 nd 0.03 ug/l rther thn the 0.5 ug/l used in the U.S.. EPA s pproch to the ssessment of qutic risk is scientificlly unsound nd plces qutic environments t risk. In ddition, there is evidence tht risk mngers t EPA hve ignored qutic risk rtios tht exceeded the usul level of concern, notwithstnding the fct tht those risk rtios were grossly underestimted in the first plce. Bsed on the reltive sensitivity of qutic insects tested with severl of the neonicotinoid insecticides, we suggest tht these reference levels should lso pply to the other neonicotinoid insecticides, notbly cetmiprid, thicloprid, clothinidin nd thimethoxm. In fct, becuse of their similrity in mode of ction, the bove reference levels should pply to the sum of ll residues for ll prent neonicotinoid compounds s well s some of the degrdtes. 8

10 Neonicotinoid Insecticides nd Birds Neonicotinoid insecticides my be totlly unprecedented in the history of pesticide registrtion in tht mesured groundwter contmintion levels hve been high enough to cuse qutic impcts. Dt on surfce wter contmintion from surveys to dte, notbly from Cliforni nd from the Cndin Priries, indicte tht concentrtions of severl of the neonicotinoid insecticides re high enough to be cusing impcts in qutic food chins. Dt from other jurisdictions (e.g. the Netherlnds) show even higher levels of contmintion. It is cler tht neonicotinoids hve often replced other insecticides of higher short-term toxicity to qutic life especilly fish. owever, the mode of ction of neonicotinoids, which entils cumultive irreversible ction nd delyed effects in invertebrtes, s well s their persistence in the environment, mkes them prticulrly worrisome. It is cler tht we re witnessing contmintion of the qutic environment t levels tht will ffect qutic food chins. This hs potentil to ffect consumers of those qutic resources, be they birds, fish or mphibins. In conclusion, policymkers nd the public should be very concerned bout the impct of neonicotinoid insecticides on birds nd on the broder environment. Specificlly, we should be concerned tht: regultory procedures re scientificlly deficient nd prone to the vgries of chnce risk mngers pper to plce miniml weight on concerns rised by environmentl scientists who crry out the scientific evlutions of the products despite ll the red flgs, regultors re dding to the list of permissible uses neonicotinoids the most hevily used insecticides in the world re systemic products tht re extremely persistent nd very much prone to runoff nd groundwter infiltrtion some neonicotinoids re cpble of cusing lethl intoxictions nd ll re predicted to cuse reproductive dysfunction in birds where we hve looked, we hve found brod-scle qutic contmintion t levels expected to cuse impcts on qutic food chins. ny future re-evlution of these products ppers to focus solely on pollintor toxicity. The seriousness of pollintor losses should not be underestimted, but there is much more t stke. A mortorium on ny further use expnsion is currently being discussed in the EU nd Member Sttes. Some countries hve moved forwrd on limited cncelltions. The North Americn regultory system needs to ct rther thn continue to ignore evidence of widespred environmentl dmge. There is evidence tht US regultors wited fr too long to impose needed restrictions on the toxic insecticides responsible for millions of bird deths per yer (Mineu 2004) nd tht this is one of the more plusible resons for the decline of grsslnd/frmlnd birds in North Americ (Mineu nd Whiteside, 2013). The neonicotinoids hve lrgely replced tht older genertion of chemicls. We re urging regultors to tke seriously the red flgs rised by this persistent, cumultive, irreversibly-cting new clss of pesticides. 9

11 Neonicotinoid Insecticides nd Birds Tble of Contents 1. The soft ride of neonicotinoids through registrtion Imidcloprid Clothinidin Thimethoxm ow cutely toxic to birds re the neonicotinoids? Wht is the chronic or reproductive toxicity of neonicotinoids to birds? A proposl for more rigorous considertion of endpoints from the vin reproductive study A short primer on seed vilbility nd bird exposure fter seeding Wht is the cute nd chronic risk to birds from the ingestion of treted seed? Incidents The issue of repellency Imidcloprid Clothinidin Could neonicotinoid insecticides be disrupting food chins nd ffecting birds indirectly? ve reductions in the vilble food supply been shown to ffect birds? ow toxic re the neonecotinoids to qutic life? s the toxicity of imidcloprid to qutic life been properly ssessed? Towrds more scientific pproch of ssessing toxicity informtion A quick note on test vribility nd repetbility Other fctors influencing sensitivity of orgnisms Deriving C5 vlues for imidcloprid Acute dt Chronic dt Deriving criticl wter concentrtions with other neonicotinoid insecticides Degrdtes or metbolites Concerns tht stndrd pproches to risk ssessment re not dequte for neonicotinoid insecticides A quick comprison of the toxicity of neonicotinoids nd older insecticides to qutic ecosystems Sublethl nd delyed effects of neonicotinoids Will exposure levels be high enough to cuse problems in qutic environments? The regultory view

12 Neonicotinoid Insecticides nd Birds Empiricl dt to dte Putting it together: Next steps Priority reserch directions Needed chnges to the regultory system References Cited Open literture Industry studies obtined through the US Freedom of Informtion process nd reviewed for the current report ANNEX 1 Toxicity of imidcloprid to qutic invertebrtes Soyben plnts by owrd F. Schwrtz, Colordo Stte University, Bugwood.org 11

13 DETAILED DISCUSSION Neonicotinoid Insecticides nd Birds For ese of consulttion, the numbering of the sections below is consistent with the min points mde in the executive summry. The neonicotinoid insecticides represent reltively new group of insecticides. They were introduced in the erly 1990s to counter widespred pest resistnce nd incresing helth nd environmentl objections to the orgnophosphorous insecticides. Although of lower cute toxicity to vertebrtes thn the orgnophosphtes, neonicotinoids longer persistence, high wter solubility nd runoff potentil s well s their very high toxicity to pollintors re bringing them incresed scrutiny, especilly now tht they hve become the world s most widely used insecticides. Their toxicity to pollintors hs brought them the most ttention so fr nd hs dominted the recent concerns of regultory bodies worldwide. The intent of this report is to review the risk tht neonicotinoids pose to birds. Birds hve borne more thn their fir shre of impcts from pesticides from the erly issues of eggshell thinning with DDT to the extensive mortlity cused by the orgnophosphorous nd crbmte insecticides tht followed. The min products reviewed here re cetmiprid, imidcloprid, thicloprid, clothinidin nd thimethoxm. Minor members of the neonicotinoid fmily include dinotefurn, nitenpyrm nd nithizine. For the ske of comprison, this report will discuss, where pproprite, number of older insecticides tht the neonicotinoids hve replced in key mrkets where they now dominte. This includes the orgnophosphorous insecticides dizinon, chlorpyrifos, mlthion, terbufos nd methmidophos, the crbmte insecticides crbofurn, methomyl, the pyrethroids tefluthrin nd deltmethrin s well s the seed tretment insecticide crbthiin. The report will emphsize US regultory history lthough it will mke reference to Cndin nd EU documents where relevnt. 1. The soft ride of neonicotinoids through registrtion A look t the regultory history of the three min neonicotinoids (imidcloprid, clothinidin nd thimethoxm) shows the extent to which registrtion decisions hve ignored repeted wrnings bout possible environmentl impcts Imidcloprid The oldest neonicotinoid, imidcloprid, ws registered in 1994 in pottoes, cotton nd pples. At the time, EPA 1 scientists cutioned tht both the cute nd the chronic qutic risk triggers hd been exceeded (USEPA 1994, b) for both non-endngered nd endngered species. A 200 ft. buffer round qutic hbitts frequented by endngered species ws suggested in consulttion with the 1 The cronyms EPA, USEPA nd US EPA re used interchngebly in this report. They ll refer to the U.S. Environmentl Protection Agency, the body responsible for federl pesticide regultion in the U.S. 12

14 Neonicotinoid Insecticides nd Birds registrnt. Detiled geogrphicl ssessments for endngered species were to continue. In its initil review, EPA identified tht imidcloprid ws both persistent nd mobile nd ws likely to give rise to groundwter contmintion. The reviewers went s fr s to sy tht there ws no need to conduct long term field dissiption studies becuse: the studies would probbly only provide informtion tht would confirm tht (imidcloprid) is both persistent nd mobile, which we lredy know (USEPA 1994b). Jumping forwrd to more recent times, not much seems to hve chnged. The re-registrtion document of 2007 sttes tht the ecologicl risk ssessments to dte hve filed to properly ssess the risks to endngered species. In this 2007 review, imidcloprid ws sid to crry n cute nd chronic risk to both freshwter nd esturine/mrine invertebrtes in greement with the 1994 conclusions, but it ws lso sid to hve the potentil to cuse chronic risk to vin species nd smll mmmls s well. Under mjor risk concerns the EPA scientist stted: Regrding effects to nontrget terrestril nd qutic orgnisms, the structure ctivity reltionship between imidcloprid, chloronicotinyl compound, nd its nlog nicotine, suggests potentil concern. Studies in the published literture show tht nicotine cn cuse developmentl toxicity, including functionl deficits, in nimls nd/or humns tht re exposed in utero. This suggests stff scientist who ws concerned bout the product but forced to follow n indequte ssessment prdigm when it cme time to ssess chronic or reproductive toxicity. Unfortuntely, there is no evidence tht wrnings of mjor risk concerns such s this one hve hd ny effect on registrtion decisions. In Cnd, imidcloprid ws first registered in 1995 for pottoes. Mny other uses were registered in the yers tht followed (PMRA , 2001), including lettuce, turf, s well s seed tretments in cnol nd corn. Becuse of concerns over wter contmintion nd pollintors, the PMRA stted in 2001 tht only new uses with low environmentl risk situtions or criticl uses in the context of sustinble pest mngement progrms where mitigtive mesures cn be incorported into product lbelling would be considered. Seed dressings were considered to represent use ptterns with low environmentl risk despite n cknowledgment tht imidcloprid ws persistent with soil DT50 3 vlues in the rnge of 1-2 yers. Such slow brekdown mens tht the pesticide hs the potentil to grdully increse in concentrtion in the soils if used on repeted bsis. Also, the compound is extremely wter soluble nd therefore mobile. In September of 2001, the PMRA cknowledged tht imidcloprid hd the potentil to contminte ground wter nd tht once contminted, no prcticl remedil ction ws possible. This dmission cme close on the heel of the registrtion of imidcloprid s seed tretment in field corn (My 2001). This rises obvious questions bout the wisdom of the use expnsion to corn when serious concerns bout the product were known Clothinidin Clothinidin, like thimethoxm, is used principlly s seed tretment though severl other uses hve been registered lso. This ctive ingredient my provide the best exmple of the pprent disconnect between registrtion decisions nd the scientific review of the dt. 2 Pest Mngement Regultory Agency. Under the responsibility of elth Cnd, the gency responsible for pesticide regultion in Cnd. 3 DT50 is the time required for hlf of the prent mteril to brek down. Units re typiclly dys. 13

15 Neonicotinoid Insecticides nd Birds In 2003, EPA first reviewed the ecologicl risk from clothinidin initilly for corn nd cnol 4 seed tretments, two mjor uses on continentl level (USEPA 2003, b). The Agency concluded tht exposure to treted seed through ingestion might result in chronic risk to birds nd mmmls, especilly mmmls where consumption of 1-2 seeds only could push them to n exposure level t which reproductive effects re expected. The detiled ssessment of clothinidin s reproductive toxicity in mmmls certinly provides cuse for concern: These chronic effects in mmmls cn include decresed body weight gins nd delyed sexul mturtion (mles only); decresed bsolute thymus weight in F1 pups (both sexes), nd incresed stillbirths (F1 nd F2 litters). Reproductive effects were noted for dult rts tht included decresed sperm motility nd incresed number of sperm with detched heds. These effects could especilly result in toxic risk to those species tht hve limited reproductive cpcity (e.g., few litters or broods, those nimls tht reproduce only once per yer, nd Endngered Species). Although effects on sperm mobility my not effect (sic) the number of offspring in some cses, there cn be n impct on the rtio of gender composition (e.g., more mles produced s opposed to femles) which cn result in popultion reductions. Over time, developmentl effects were noted in rbbits t 75 mglkgldy, nd included premture deliveries, decresed grvid uterine weights, nd incresed litter incidence of missing lung lobe in the fetus. The possibility of chronic risk suggests Restricted Use compound, Endocrine Disruption cndidte, s well s Endngered Species concern for mmmls, birds, nd invertebrtes. The EPA mde criticl error, however, in stting tht the prescribed griculturl prctice of drilling seeds t plnting should reduce exposure to these nimls. A quick review of the scientific literture (see section 2) would hve shown tht this ws nïve nd incorrect ssumption. In the sme 2003 ssessment, EPA described the chemicl s persistent nd mobile, with potentil to lech to ground wter s well s runoff to surfce wters (USEPA 2003). The high toxicity to bees ws identified s well, but this is outside the scope of the current review. With this level of concern, one might hve expected regultors to move slowly on new uses, especilly mjor ones. owever, plethor of registered uses for clothinidin followed in quick succession: Tobcco, turf, pples, pers nd ornmentls (USEPA 2004); pottoes, grpes, sorghum nd cotton (USEPA 2005); sugr beets (USEPA 2006, 2007); tuberous, corm nd bulb vegetbles, lefy greens, cole crops, cucurbits nd other miscellneous vegetbles, crnberry nd other low growing berries, tree nuts, cerels, figs, pomegrntes, more cotton, soyben, peches, nd more potto uses (USEPA 2009); incresed ppliction rtes to vegetbles nd tree trunk sprying (USEPA 2010); mustrd nd cotton seed (USEPA 2011). By 2005, EPA scientists hd significnt concerns bout pollintors; they hd lso incresed concerns bout both direct nd indirect effects on terrestril ecosystems. Now tht more dt hd been gthered on cute nd chronic qutic toxicity, they hd lso strted rising concerns bout possible qutic impcts. 4 Cnol is the term developed in Cnd for specific vrietls of oilseed rpe. These re vrietls of rpe modified to hve low glucosinolte nd erucic cid content nd therefore fir for humn consumption (e.g. 00 oilseed rpe in Europe). 14

16 Neonicotinoid Insecticides nd Birds As is the cse with mny other hzrdous products, the mnufcturers nd regultory uthorities pper to be stisfied with product lbelling tht shifts the responsibility of protecting the environment to the end user. A lbel sttement on clothinidin product such s Do not pply where runoff is likely to occur (Aren 50 WDG Reg ) my seem resonble enough t first blush. owever, hve the regultory uthorities ssessed wht proportion of their country s griculturl re cn be treted without risk of runoff? If this is deemed to be smll proportion of the totl, is it still resonble to plce this product in the hnds of ll growers? The sme lbel goes on to specify: The properties of this chemicl suggest it my lech into ground wter if used in res where soils re permeble nd where the wter tble is very shllow. This sttement is sid to pply specificlly to the Stte of Florid. Apprently, users elsewhere need not worry bout groundwter contmintion! 1.3. Thimethoxm Thimethoxm s first registrtion dtes bck to Bsed on EPA s 2011 re-registrtion review document (USEPA 2011b), thimethoxm is registered for severl griculturl nd non-griculturl commodities s well s for turf, ornmentls nd s n ntimicrobil on wood. The most recent ecologicl reviews re from 2010 when the Agency pproved the uses in lflf, onions, penuts, corn nd lefy vegetbles. Yet, s erly s 2008, the Agency hd stted, in their risk ssessment for citrus fruits nd tree nuts, tht thimethoxm posed potentil for direct dverse effects on freshwter invertebrtes, birds nd mmmls (USEPA 2008b). They hd lso predicted structurl nd functionl chnges of both the qutic nd terrestril ecosystems. As ws the cse with clothinidin, it would pper tht these wrnings from EPA scientists went unheeded. Also, s of 2011, the Agency ws still missing key pieces of dt in order to support current uses of thimethoxm. This included soil metbolism studies, terrestril field dissiption studies s well s vrious qutic toxicity requirements nd new studies mde necessry by emerging dt on pollintor toxicity (USEPA 2011b). Thimethoxm is considered by the Agency to be slightly toxic to birds on n cute nd sub-cute bsis. No mention is mde of its reproductive toxicity in the 2011 re-registrtion summry document. Interestingly, the sme 2011 re-registrtion document stted tht: the Agency does not hve dt to indicte tht thiomethoxm shres common mechnism of toxicity with other chemicl substnces nd therefore does not see need for cumultive risk ssessment. This is strnge sttement indeed, if only becuse the mjor degrdtion product for thimethoxm is clothinidin. Furthermore, ll neonicotinoid insecticides registered to dte re considered to hve the sme mode of ction for resistnce development purposes (nachr gonists, Group 4A) (Jeschke et l. 2011). The Agency proposes to complete reregistrtion review by In 2001, Cnd s PMRA registered thimethoxm for use s seed tretment in cnol, replcing the stndrd lindne seed tretment or lindne/grnulr terbufos combintion. Despite its demonstrted wter solubility nd soil persistence, the gency did not ssess ny environmentl toxicology except potentil impcts on birds. It seems to hve ssumed tht ny possibility for impcts on qutic systems ws negligible. The ecologicl review of thimethoxm cme in 2007 (PMRA 2007) in order to register the product for use on pottoes nd on number of tree fruit crops. The Agency concluded tht, other thn requiring lbeling for pollintors nd buffer zones round qutic bodies, the compound presents negligible risk to wild mmmls, birds, erthworms, fish, crustcens, mphibins, lge nd qutic plnts. We believe tht the evidence reviewed below shows otherwise. 15

17 Neonicotinoid Insecticides nd Birds Incresing concerns rised in the scientific nd populr literture in the lst decde over imidcloprid, clothinidin nd other neonicotinoid insecticides did not seem to deter pesticide mnufcturers, who ppered to be in rce to register s mny uses s possible in complete disregrd of ny environmentl consequences. It looks s if the USEPA nd other regultory bodies were rushing to oblige despite their own scientists repeted nd ever-growing concerns, rised in internl reviews. In Cliforni lone, the Cliforni Deprtment of Pesticide Regultion, s of July 2012, stted tht the re-evlution of neonicotinoids of concern viz. pollintor exposure (excluding pet uses nd the like) would involve 293 pesticide products from 57 registrnts nd tht s more products becme registered (suggesting tht registrtions re on-going), DPR would roll them into the re-evlution (CADPR 2012). It is now to the point tht it hs become difficult to find commodities tht do not hve registrtion of one or severl of the neonicotinoid insecticides. Bsed on informtion from Byer, one of the min registrnts (Jeschke et l. 2011), neonicotinoids hve overtken ll other insecticide clsses world-wide. 2. ow cutely toxic to birds re the neonicotinoids? The stndrd wy in which the toxicity of pesticides to birds is mesured is through n cute study. Birds re given the product by gvge (forced feeding) in vrying mounts nd the quntity of pesticide cusing the deth of hlf of the test birds is recorded nd expressed s proportion of bodyweight (i.e. the LD50 expressed s mg of pesticide per kg of bodyweight). One of the serious filings of current risk ssessment is the underestimtion of interspecies vrition in pesticide susceptibility. Typiclly, one or two species only re tested (Mllrd nd Bobwhite re the usul mndted species) nd the risk ssessment is crried out with the more sensitive of the two. Even with the ppliction of the customry sfety fctors, it hs been shown tht sensitive bird species re under-protected (Luttik et l. 2011). When more species re tested (s hppens through cdemic or government reserch with older products) inconsistencies develop mong regultors s to how these dt should be used. Sometimes, regultors will use the dt if the supplementry species re shown to be more sensitive thn the usul ones; t other times the dt re ignored, especilly if they were obtined in wys tht differ from the usul test protocols. The end result is often rbitrry nd the toxicity of different pesticides rnked bsed on luck of the drw. This prevents ny rigorous comprison of different chemicl options. Species sensitivity distributions were designed in prt to provide n unbised comprison mong chemicls. They will be used here. The method uses ll vilble toxicity dt nd fits those dt to frequency distribution often log norml distribution. This process hs been modified (in the cse of birds) by incorporting body weight scling (Mineu et l. 2001). This is becuse it hs been shown tht smll birds tend to be more sensitive to cutely toxic pesticides (Mineu et l. 1996), most likely becuse they succumb more esily to the rigours of debilittion nd the resulting strvtion. Scling for body weight in birds hs been ccepted in principle by the US EPA in their risk ssessment process (e.g. their internl TREX softwre). owever, the use of species sensitivity distributions or the use of smll smple methods tht pproximte these distributions re not yet commonplce in regultory circles. 16

18 Neonicotinoid Insecticides nd Birds The min cute toxicity endpoint presented here is vlue clled the D5 ( zrdous Dose t the 5% til of the species distribution ). It represents the mount of pesticide in mg of chemicl per kg of body weight estimted to led to 50% mortlity in species more sensitive thn 95% of ll bird species, clculted with 50 percent probbility of over- or underestimtion. The D5 cn be clculted from fitted distribution where severl toxicity vlues exist, or pproximtions cn be used for smller dt sets. The 5% threshold is totlly rbitrry lthough it hs gined gret del of use in the published literture. It does seem to fulfill the criterion tht, for resons of ecologicl integrity, we might not wish to see more thn 5% of species being seriously ffected in ny system. The 5% til will therefore be used throughout this report with the view tht this should protect most exposed species. The first pproch used here is the ETX 2.0 progrm (Vn Vlrdingen et l. 2004) developed by the Dutch Government to clculte the hzrdous concentrtions nd frction of species ffected by given exposure levels. It ssumes log-normlly distributed toxicity dt. Distribution-fitting ws crried out for ll dtsets with more thn 5 dt points in this cse, imidcloprid only. For the other compounds with only one or two toxicity vlues, smll smple method ws used (Aldenberg nd Luttik 2002). This consists of estimting the D5 on the bsis of men LD50 nd pooled vrince estimte clculted for lrge group of pesticides t lrge (Luttik nd Aldenberg 1997). The medin estimte of the D5 is clculted here in order not to bis for dt vilbility. We recognise tht this does not gurntee tht ny of the estimted vlues chieve the 95% level of protection. The second pproch estimtes body weight scled vlue following Mineu et l. (2001). The pproch ensures tht species t one or the other end of weight rnge spnning 10 to 1000g re dequtely covered. The vilble dt re tbulted in tble 2.1. The derived D5 vlues re given in tble 2.2. In the cse of neonicotinoids, the exct method does not mtter very much; similr vlues were estimted by both methods. owever, it is cler tht regultory risk quotients use much less protective vlues s their point of deprture. Depending on the specific insecticide, EPA underestimtes toxicity by 1.5 to 10 fold if the intent of the exercise is to protect most species, not merely mllrds nd bobwhites. This will result in non-conservtive (i.e. nonprotective) ssessments, especilly since the endpoint is lethlity to hlf of the tested popultion. Tble 2.1. Acute toxicity of the min neonicotinyl insecticides to birds bsed primrily on industry studies tbulted by regultory uthorities (principlly EPA & EU sources). Originl references obtined through the US Freedom of Informtion Act nd consulted for this report re indicted with n sterix. Active ingredient Species LD50 (mg/kg bw) Probit slope 5 when Dose vehicle Reference to originl industry study Notes 5 The LD50 is mesured using sttisticl construct clled the probit. The probit is normlised proportion of birds dying from the dose dministered. The slope of the probit is n indiction of the reltionship between dose nd mortlity nd is used to predict the dose t which certin proportions of birds (e.g. 1% or 5% rther thn 50% s in the LD50) re expected to die. The higher the slope, the fster the proportion of birds t risk will increse with slight increses in exposure. 17

19 Neonicotinoid Insecticides nd Birds provided when vilble cetmiprid bobwhite 180 Europen Commission 2004 mllrd sodium crboxyme thyl cellulose Johnson 1994* zebr finch Serious clinicl signs seen t lowest dose level of 52 mg/kg wter ubbrd 2011* NOEL for clinicl signs of 1.8 mg/kg. Onset of serious debilittion between 2.5 nd 3.6 mg/kg. clothinidin bobwhite >2000 corn oil Johnson 1998* NOEL for clinicl signs of 500 mg/kg. Serious clinicl signs nd 20% mortlity t 1000 mg/kg Jpnese quil 430 corn oil Gllgher nd Bevers 2000* mllrd >752 Europen Commission 2005 thicloprid bobwhite Geltin cpsules Gru 1995* thimethoxm bobwhite methyl cellulose mllrd methyl cellulose imidcloprid bobwhite Geltin cpsules Johnson 1996* Johnson 1996* Toll 1990* cnry 35 (25-50) Cremopho r EL in wter Gru 1986* gry 15 Grolleu 1990 prtridge Jpnese quil Gum Arbic in wter mllrd Geltin cpsules NOEL for clinicl signs of 12.5 mg/kg. Light signs t 25 mg/kg. More serious incpcittion t 100 mg/kg. Clinicl signs NOEL of 152. Severe signs onset t 551 mg/kg. NOEL for clinicl signs of 500 mg/kg. Emesis observed t ll dose levels. NOEL for clinicl signs of 137 mg/kg. EFSA (2008) gives vlue s 503 which is in error. NOEL for clinicl signs of 25 mg/kg. Onset of serious incpcittion between 50 nd 100 mg/kg. Serious incpcittion t lowest dose of 10 mg/kg. in EC dtbse Gru 1988* Severe clinicl signs t 5 mg/kg. NOEL for clinicl signs t 3.1 mg/kg (2.5 mg/kg nominl). ncock* 1996 Rock 25** Geltin Gru 1987* dove cpsule ouse 41 Stfford 1991 Severe signs t lowest dose tested 25 mg/kg; mortlities up to 8 dys post dose. Severe signs t lowest dose tested 12.5 mg/kg 18

20 Neonicotinoid Insecticides nd Birds sprrow in CCME 2007 ** Femle vlue. Mle pproximte LD50: Tble 2.2. Derived D5 vlues for the mjor neonicotinoid insecticides. This is the mount of pesticide in mg of chemicl per kg of body weight estimted to led to 50% mortlity in species more sensitive thn 95% of ll bird species, clculted with 50 percent probbility of over- or underestimtion. The vlue used by the USEPA to generte risk quotients is given for comprison. Active ingredient Unscled D5 (ETx softwre) Scled D5 (bsed on Mineu et l. 2001) Acute vlue used by USEPA in risk ssessment to which 0.5 fctor hs been pplied to reflect current Levels of Concern ppliction fctor Notes cetmiprid * 49 clothinidin ** thicloprid imidcloprid (20.5***) Dietry LC50 vlues were fvored initilly for clculting risk quotients****. These were 1536 ppm for bobwhite/mllrd; 143 ppm for songbirds bsed on the house sprrow. thimethoxm * The higher vlue reflects the lck of smll smple extrpoltion fctor for the zebr finch in Mineu et l ** Corresponds to the lower vlue of 430 for Jpnese quil. The USEPA routinely reruns probit nlyses nd reports slightly different vlues from the cited studies. *** This lower vlue is cknowledged nd used in the ssessment of grnulr product. **** Toxicity endpoints hve chnged over the yers. Dietry toxicity ws initilly fvored for risk ssessment by the USEPA but ttention hs now shifted to cute toxicity s more relible mesure. The dietry toxicity test hs severl problems ssocited with it tht cn mke interprettion difficult (Mineu et l. 1994). The neonicotinoid insecticides hve replced number of insecticides of high cute toxicity to birds notbly orgnophosphorous nd crbmte compounds. Tble 2.3 provides scled D5 vlues for severl of those lterntives in order to compre with the neonicotinoids. Tble 2.3. Comprison of vin toxicity of neonicotinoid insecticides (in bold) nd severl of the insecticides they hve replced, ordered from most to lest toxic to birds bsed on vin scled D5 vlues. (Dt from multiple sources Tble 3.2 bove nd see Mineu et l. 2001). Active ingredient Avin D5 [mg/kg bw] (Most re No. species tested 19

21 Neonicotinoid Insecticides nd Birds scled vlues) terbufos crbofurn dizinon methmidophos Crbthiin (crboxin) chlorpyrifos dimethote cetmiprid 8.0* 3 imidcloprid methomyl deltmethrin 97 5 thimethoxm 98 2 clothinidin mlthion tefluthrin thicloprid * unscled D5 The toxicity of imidcloprid nd cetmiprid, the most cutely toxic of the neonicotinoids, compres with the crbmte methomyl. owever, the toxicity of thimethoxm nd clothinidin, both extensively used s seed tretments, is much lower nd comprble to the lest toxic orgnophosphorous insecticides such s mlthion or the synthetic pyrethroids. We do need to keep in mind tht these dt only refer to lethlity. Different fmilies of pesticides elicit sub-lethl effects t different frctions of the lethl dose. Cllghn nd Mineu s (2008) review of 166 studies in birds found tht very few compounds (< 5%) cuse observble sub-lethl effects t doses s low s 1/10 of the lethl dose. But in the cse of the neonicotinoids, s seen in tble 2.1 bove, severe signs of debilittion (e.g. txi) were observed with imidcloprid full order of mgnitude below lethl doses. Thicloprid my behve similrly nd, bsed on similr mode of ction, other neonicotinoids my elicit similr effects s well. There is lso some indiction tht these symptoms persist for long time post dose, t lest reltive to cholinesterseinhibiting insecticides. 3. Wht is the chronic or reproductive toxicity of neonicotinoids to birds? As mentioned in section 1, the US EPA hs often commented on possible risks to vin reproduction. Only one mesure of chronic risk is vilble for birds reproductive test tht is typiclly conducted on either the bobwhite or the mllrd. It is truncted test which consists of feeding constnt concentrtion of the pesticide nd then collecting the eggs nd incubting them rtificilly. There is therefore no test of the bility of the birds to incubte, htch or rise their young. The test is hybrid between chronic toxicity nd true reproductive effects nd hs been the subject of criticism over the yers (Mineu et l. 1994, 1996, Mineu 2005). One of those criticisms is tht, becuse of the long durtion of the test, nd the occsionl pir tht fils to get long, spurious vrince is introduced in number of prmeters which decreses the power of the test to see reproductive deficits. On the other hnd, becuse the birds re offered contminted diet only with no other food choice, the test my overestimte likely exposure. owever, it remins the only test vilble with which to model non-cute risk. 20

22 Neonicotinoid Insecticides nd Birds Chronic toxicity endpoints re provided in tble 3.1. Tble 3.1. Chronic toxicity endpoints for the min neonicotinoid insecticides. The vlues re given in ppm in msh given to the birds for the durtion of the test. All studies obtined from US EPA FOIA process nd reviewed for this report. Conclusions my differ from reported informtion in regultory summries. Active ingredient Species NOEL 6 (ppm) LOEL (ppm) Dose levels cetmiprid bobwhite , 500, 1000 bobwhite , 200, 400, 800 mllrd , 125, 250, 500 mllrd , 125, 250, 500 clothinidin bobwhite 525 (500 NA 0, 80, nominl) 200, 500 mllrd (500 0, 80, nominl) 200, 500 imidcloprid bobwhite , 30, 60, 120, 240 mllrd , 60, 120, 240 thicloprid bobwhite , 153, 466 Reference Tliferro et l Temple et l Tliferro nd Miller 1999 Stfford 2004 Gllgher et l Gllgher et l. 2000b Toll 1991 Toll 1991b Schmuck 1997 mllrd NA 48 48, 140, 418 ncock 1997 mllrd , 28, 55 ncock 1998 thimethoxm bobwhite , 300, Tliferro 900 nd Miller 1998 mllrd , 300, 900 Brewer et l Effect Difficult study to interpret. Outlier pir should hve been removed from controls. Chick survivl per hen shows cler dose-response. Eggs lid lso. Chick survivl, eggs lid Tenttive. Difficult to interpret becuse of poor dose response with worst performnce in 62.5 ppm dose group. Eggs lid, fertility Severl smll non-sig deficits in mny prmeters Difficult to interpret. Vrible results, berrnt controls. Effect on mle weight only. No true reproductive effects. Study continued longer thn norml leding to high vribility. tching, egg lying clerly ffected t higher dose Agree with uthor tht slight decrese in feeding rte t ll concentrtions is not biologiclly relevnt Prentl effects, fertility or erly embryonic deth t high dose Erly embryonic deth, non-sig egg brekge Non sig. but lrge diff. in eggs lid Prentl effects, non-sig effects in severl prmeters. As with cute toxicity testing, ssessing risk to ll potentilly exposed bird species from the lower of two bird species tested is not very relistic. This pproch seriously underestimtes the likely difference in sensitivity between species nd the possibility tht bird species other thn mllrds or 6 NOEL (No Observble Effect Level) is highest dose level t which no effects were seen. It is more properly termed NOAEL to specify Adverse effects. The LOEL (or LOAEL) is the lowest level producing effects in the study. 21

23 Neonicotinoid Insecticides nd Birds bobwhites will be ffected t much lower levels of exposure. It hs been rgued tht chronic toxicity is no less vrible mong species thn cute toxicity nd tht the vrince in inter-species chronic toxicity endpoints could (nd should) be used s proxy for the vrince in reproductive toxicity (Mineu et l. 2001b, Luttik et l. 2005). This my give more relible estimte of the dose t which chronic toxicity effects re expected in those species tht hppen to be more sensitive to the pesticide thn the stndrd bobwhite or mllrd. Yet, EPA llows for rtio between exposure nd effect of 1 in their risk ssessment before they consider tht their Level of Concern hs been exceeded. This mens tht birds could be exposed to level s high s the lower NOEL of either bobwhite or mllrd without exceeding their level of concern. Given tht EPA s reproductive LOCs for birds re routinely exceeded with the neonicotinoids (section 1), this mens tht even insensitive species re likely to be ffected reproductively A proposl for more rigorous considertion of endpoints from the vin reproductive study. Following mjor interntionl review hosted by the British Government in 2004, recommendtions were mde by the pnel of ssembled scientists to improve the ssessment of long term or reproductive toxicity in birds. As first step, it ws recommended tht the vrious endpoints in the studies be seprted rther thn bsing risk ssessment on single NOEL (Bennett et l. 2005, Shore et l. 2005). This followed on nlyses (Mineu et l. 1994) showing tht three mjor effects were t ply in the current vin reproduction studies: prentl effects, eggshell effects nd effects on the reproductive & embryonic development process proper. Mineu nd collegues (1994) suggested tht we should be most interested in those true reproductive effects tht re mnifest t concentrtions lower thn those tht elicit prentl toxicity becuse these more pernicious effects will be hrder to detect in simple feeding studies. Unfortuntely, this proposl hs not been endorsed by regultors lthough the US EPA is currently investigting risk models tht would help with sounder interprettion of reproductive test results (R. Bennett, pers. comm.). In the mentime, we offer the following solution, developed by Mineu nd collegues (2006) for the Cndin Government. It still uses single NOEC (No Observble Effect Concentrtion) or LOEC vlue (s do ll regultory bodies currently) but does pply n extrpoltion fctor to ccount for inter-species differences in susceptibility s recommended previously. For ll the neonicotinoid insecticides being reviewed here (tble 3.1) NOEC vlues were determined. Where this is not the cse (i.e. when the lowest dose tested produced n effect; this occurred in some of the other seed tretment chemicls to which we compred the neonicotinoids below) Mineu et l. (2006) compiled vilble NOECs nd LOECs from the USEPA one liner dtbse (B. Montgue pers. comm.) nd clculted tht the medin spcing between the log NOEC nd log LOEC ws 1.23 bsed on smple of 272 studies. This rtio ws therefore used to obtin NOEC where the lowest level tested produced n effect. The NOEC (or more correctly stted, NOAEC No Observble Adverse Effect Concentrtion) hs been criticised s toxicologicl endpoint becuse of very vlid resons hving to do with sttisticl power, especilly in the context of qutic toxicity testing, nd we fully gree with this criticism. owever, it is currently not fesible to extrct n ECx type of vlue (the concentrtion producing pre-defined level of reproductive deficit) from the current vin reproduction test designs. 22

24 Neonicotinoid Insecticides nd Birds Mnipultions of the test endpoints re crried out s follows in order to rrive t resonble estimte of the dose of pesticide bird would need to ingest dily to dversely ffect reproduction. In the usul reproduction study, bobwhites (weight 210 g; unpublished industry studies) hve pek food consumption of pproximtely 10% of their bodyweight in food per dy; mesured food intkes for the mllrd (pprox. 1000g) re highly vrible nd pek bove 20% of bodyweight (unpublished industry studies). This is counter to expected llometric reltionships where, the smller the bird, the lrger its proportionl food intke. Mllrds in the lbortory tend to spill lot of food nd it is therefore difficult to estimte their true consumption. As verifiction, the llometric eqution of Ngy (1987) for non-psserine birds ws used to estimte food consumption even though it is recognised tht Ngy s lgorithms pply to birds in the wild. One expects wild birds to hve higher mintennce requirements thn birds kept in the lbortory. On the other hnd, the birds in the lbortory re induced to ly n unresonble clutch size which is likely to increse their food intke compred to n equivlent bird lying norml clutch in the wild. Dry food intke = * bw(g) Lbortory diet ws estimted to hve 11% moisture content bsed on personl communiction from Jonn Bevers with Wildlife Interntionl, one of the mjor testing lbortories. Therefore, for the bobwhite intke of lb diet (ctul weight) should be: Intke = (0.302 * )/0.89 (propn. dry wt.) = ~ 19 g. which is pproximtely 90% of the observed 10% of bodyweight. For the mllrd, the sme formul returns vlue of 61 g/dy or little over 6% of its bodyweight per dy rther thn the observed 20%. Becuse of the spillge problem mentioned previously, nd ssuming the figure of 21 g per dy (10% of bodyweight) in the bobwhite to be correct, we djusted the result of the Ngy clcultion by the sme proportionte mount rising the pproximte food intke in the Mllrd to 67 g/dy. The estimted food intkes of 21 g/dy or 67 g/dy for the bobwhite nd mllrd respectively were used to convert ll NOAEC vlues to NOAELs (criticl pesticide intke levels) expressed s mg.i. of pesticide / kg bird / dy. We believe this correction to be dequte where there is no lrge demonstrted effect of the chemicl on food intke. This is the cse for the neonicotinoids reviewed here. Therefore : NOAEL mllrd (mg.i./kg bw/dy) = (NOAEC mllrd (mg/kg food) * kg food/dy) / 1 kg bw NOAEL bobwhite (mg.i./kg bw/dy) = (NOAEC bobwhite (mg/kg food) * kg food/dy) / kg bw 23

25 Neonicotinoid Insecticides nd Birds A geometric men of NOAEL mllrd nd NOAEL bobwhite ws clculted s the best vilble verge for ll bird species. In order to use the compound-specific interspecies vrition in cute toxicity, we derived stndrd devitions (SDs) for cute dt in the following wy: o A single geometric men log LD50 vlue ws obtined for ech species-pesticide combintion s outlined in Mineu et l. (2001). o Where the number of species tested ws 4 or more, we derived stndrd devition. This ws possible here for the ctive ingredient imidcloprid. For ll other ctive ingredients, pooled SD of (fter Aldenberg nd Luttik 2002) ws used. The extrpoltion fctor ( fctor to be pplied multiplictively to the men untrnsformed NOAEL) ws defined s follows fter Aldenberg nd Luttik 2002): EF medin = (10 σ ) Kp where Kp is the z score of 1.64 in the cse of the 5% til of normlly-distributed species sensitivity distribution. This is equivlent to: EF medin = σ or to n extrpoltion fctor of 5.8 for the pooled vrince estimte of bird cute dt. The medin extrpoltion fctor (EF) ws then pplied to the geometric men NOAEL in order to obtin the criticl toxic effect level for sensitive bird t 5% of the puttive distribution of reproductive toxicities. The resulting vlue (the clculted criticl dose for bird t the 5% til of sensitivity) is tbulted in tble 3.2 for the min neonicotinoids insecticides nd some other common seed tretment pesticides (insecticides or fungicides). For the neonicotinoid insecticides, criticl intke vlue bsed on study LOAELs is lso given. Assuming the current vin reproduction studies cn be relied upon, effects from chronic intke should strt occurring t some exposure levels between those two vlues. Tble 3.2. Clculted criticl chronic dose intkes (NOAEL nd LOAEL) for sensitive bird species (t the 5% til of sensitivity) for the min neonicotinoids insecticides nd some other common seed tretment pesticides. Avin Chronic - Criticl intke level (NOAEL - mg/kg/dy) for sensitive bird t 5% til of cute sensitivity distribution Avin Chronic - Criticl intke level (LOAEL - mg/kg/dy) for sensitive bird t 5% til of cute sensitivity distribution Active ingredient Acetmiprid Clothinidin Imidcloprid Thicloprid Thimethoxm

26 Neonicotinoid Insecticides nd Birds Cptn 4.95 Crboxin 1.30 Dizinon 0.12 Difenoconzole 1.76 Fludioxonil 4.16 Iprodione 4.22 Metlxyl 2.44 Tebuconzole 2.01 Tridimenol 1.15 Triticonzole A short primer on seed vilbility nd bird exposure fter seeding Of prticulr concern to birds re those neonicotinoid compounds tht re used s seed tretments. istoriclly, seed tretments hve been ssocited with extensive exposure to nd impcts on birds. These were well documented for mercury-bsed seed tretments nd for cotings with the cyclodiene insecticides ldrin nd dieldrin. Any contmintion of vin food items from spry pplictions to field crops s well s non-dietry exposure is likely smll in comprison to the potentil for very hevy exposure from seed tretments 7. The min point to be mde here is tht, s fr s birds re concerned, seeds re vilble d libitum on fields. The type of mchinery nd plnting techniques drmticlly influence incorportion of treted seeds. All seed drills use the sme bsic principles. Seeds re dropped from row of individul dispensing units behind the trctor. In front of ech dispenser furrow is mde by soil openers (disks, hoes or knives). The seed is dropped, either by grvity, by trin-driven uger system or through pneumtic system (ir seeder). Air seeders provide better control of ppliction rte. Side-firming discs (closure wheels) push soil lterlly ginst the seed. Alterntively, press wheels roll over the whole furrow re to compress the soil ginst the seeds. In North Americ, the term plnter is usully reserved for crops tht need wide spcing between rows (i.e. mize/corn) nd the seed dispensing units re plced fr prt; the term drill (s in hoe drill or press drill) is used for crops tht cn be plnted t higher densities (i.e. cerels) so the dispensing units re close together. In Europe, the term seed drill is used for ll crop types. Additionl implements my be dded to id incorportion of the seeds, such s hrrows 8 plced in front of the seed dispenser to help cler debris (lso known s trsh) for more successful seed incorportion. Mny vritions on seeding exist depending on the specifics of the mchinery, nd lso on how the drill is configured. Specific implements nd mchinery re recommended for ech type of crop; however, this is usully left to the preference of ech individul grower. Growers my not lwys be using the best equipment for ny given crop becuse the sme drill is often used for severl crops in rottion. A good exmple of this is the use of ir seeders to dispense cnol on the soil surfce fter which it is crudely hrrowed in. Air seeders re designed for precision seeding of cerels (usully 4-5cm in depth). owever, growers find it difficult to get good results when ir 7 For this reson, this report will not conduct n ssessment of vin toxicity resulting from the contmintion of vin foods such s insects or weed seeds from spry pplictions. It is not tht this risk is necessrily negligible, but it ples in comprison to the risk from treted seed. 8 A hrrow is n griculturl implement tht loosens nd levels the surfce of the field. rrowing is typiclly crried out before or during plnting opertions. 25

27 Neonicotinoid Insecticides nd Birds seeding t very shllow depths s with cnol (1-3cm). They cn get round this problem by running the furrow openers bove the soil surfce nd crudely hrrowing in the seeds. The following fctors hve been tested experimentlly nd lso significntly ffect the proportion of plnted seed tht re ctully buried under the surfce (i.e. plced where they will hve the best chnce of germinting): Soil condition mesured s clump weight of the soil (Leeuw et l., 1995). Field trsh which impedes the ction of the incorportion. Surfce counts of seeds were significntly lower in summer fllow fields thn in stubble fields (Mze et l., 1991). Rin which mkes incorportion during plnting difficult (Dvis, 1974; Leeuw et l.,1995) Seed size nd plnting depth: lrger seeds re typiclly plnted deeper nd t lower densities (Tmis et l., 1994). Conversely, smll seeds such s cnol re plnted very shllow with much higher risk of lrge numbers left on the soil surfce. Deeper plntings typiclly result in fewer surfce seeds (Pscul et l. 1999) Trvel speed during plnting: the insertion of seeds t intended depths using drills is ensured only t certin speeds nd frmers will chnge speed during plnting. This hs been shown with grnulr insecticides (Ellis, 1982) which re subject to the sme limittions s seeds. The soil disturbnce ssocited with plnting typiclly increses vin hzrd by exposing soil invertebrtes on the field surfce which ttrcts invertebrte-eting birds with higher probbility tht treted seed will lso be ingested. Some crops re seeded from n ircrft (e.g. rice). This my be very high risk fctor given tht rice grins re likely to be widely distributed on levees nd other dry res in nd round pddies. igh densities of treted seed occur on certin res of the field, nmely t row ends where the plnters re lifted out of the furrows to permit turns (termed hedlnds in the Europen literture) (Pscul et l. 2009b), t irregulrities in field contour resulting in the plnter shoe rising out of the soil, nd where the frmer lods the mchine with the treted seed. These res my increse risk to vin species becuse spills re more visible; they present profitble feeding opportunity (Leeuw et l., 1995). igh densities cn lso occur midfield by mens of errtic ppliction from dispensing units resulting from incorrect clibrtion, clogging or obstructions such s stones. While environmentl conditions cn cuse high vin risk in loclized prts of the field, growers hve drmtic influence on the overll number of treted seeds left on the soil surfce fter plnting. Therefore, densities vilble to vin species re highly unpredictble, s illustrted by ctul field counts. Furthermore, exposure cn still occur if seeds re fully incorported in the soil. Geese dig for seed in upper surfce lyers of soil (Lorenzen & Mdsen, 1986). Western medowlrks nd mny blckbirds will probe for seed by pushing their bill into the ground or beneth n object nd then the buried food items re mde ccessible by spreding their mndibles wide (gping) (Lnyon, 1994). In Europe, skylrks will bring grin to the surfce by uprooting seedlings (Green, 1978), technique fvored by crnes nd geese in North Americ. This will expose them to systemic residues, residues still crried on the seed or grnules cught in the root hirs of the seedlings. Mourning doves will move light ground litter using their bill to find food (Mirrchi & Bskett, 1994). In light of these feeding ptterns nd the inefficiency of ll currently used incorporting devices, we cn conclude tht vin exposure to high numbers of treted seeds cnnot be prevented even if the product is pplied t recommended rtes using proper equipment. 26

28 Neonicotinoid Insecticides nd Birds Birds lso hve preferences for certin seed types. This is species dependent. For exmple, it hs been suggested tht some species dislike cnol seed. Pwlin nd Proulx (1996) showed tht the dily consumption of cnol by house sprrows ws fr less thn tht of millet or sunflower seeds even when no other food source ws vilble. owever, closely-relted mustrd seeds hve long been used in the pet bird trde, nd cnol ws found to be preferred seed for house finches nd ws used successfully s lethl bit (lced with strychnine) (Plmer, 1972). A mixture contining rpeseed s well s millet nd cnry seed is given s stndrd diet for Jpnese quil (Brfknecht 1998). Smith (2006) looked t the ttrctiveness of whet, corn, brley, ot nd soyben to subset of common frmlnd species. e found tht soyben ws the lest preferred. owever, Smith s review did not include some of the lrger frmlnd species more likely to be ttrcted to lrger seed: wterfowl, grouse nd phesnts, turkeys etc. In conclusion, given the high vribility nd lck of control regultors nd mnufcturers hve on the methods of ppliction t plnting (field conditions, equipment, clibrtion, etc.), it should be ssumed tht unlimited quntities of treted seed will be vilble to forging birds. Therefore, we believe tht regultors re clerly mistken in believing tht exposure to treted seed cn be minimized by lbel sttements or dherence to good griculturl prctice. The only fctors tht should be considered in vin risk ssessments of seed tretment chemicls re: 1) the mximum consumption rtes (preferbly under food stress relistic of field conditions) of frmlnd forging birds, nd 2) the mount of ctive ingredient per seed. For the purpose of this report, we will express risk s the number of seeds needing to be ingested for given biologicl effect. An initil ssumption will be tht seeds contin the lbeled mount of ctive ingredient. It hs been shown however, tht ctul concentrtions of ctive ingredients re lower t plnting thn the initil in the bg concentrtion (McKy et l. 1999). This loss of ctive ingredient my be to the dvntge of forging birds but hs proven to be problem with the neonicotinoids, resulting in lrge kills of bees from dust exhusted from pneumtic seeders. 5. Wht is the cute nd chronic risk to birds from the ingestion of treted seed? Working out the typicl loding of ctive ingredient per seed is not simple tsk given the mny lbels, formultions nd inconsistent wys of reporting tretment concentrtions. Only few representtive exmples re given here for the min field crop seeds likely to be consumed by birds whet (s representtive of cerel crops), corn nd cnol. Representtive seed weights were obtined from compiltion of the PMRA bsed on number of different sources (Chris Frser, PMRA, pers. comm.) s well s EPA review documents. Seed weight vlues used here re s follows: cnol = 2.9 mg, cerels = 35 mg nd corn = 377 mg. For imidcloprid, we consulted the Gucho 75ST lbel (EPA Reg. No ). This is one of the lbels for commercil seed tretments. Whet is lbeled t 2 oz. product per hundredweight (Cwt lb of seed) which works out to mg/seed. A direct figure of 1.34 mg.i./kernel is given for corn. The highest tretment rte for cnol is 21.3 oz of product per hundredweight. This works out to 0.03 mg of imidcloprid per seed. For clothinidin (USEPA 2003; s well s the following lbel: Poncho TM 600; Reg. No ; updted 22 April 2010), loding of 1.25 mg.i./kernel is given directly for corn. The mximum rte 27

29 Neonicotinoid Insecticides nd Birds on cnol/rpeseed is oz. product per Cwt which works out to pproximtely mg/kg seed. For whet nd other cerels not included on this prticulr lbel, USEPA (2010) gives 70 g.i/100 kg seed. For whet specificlly, this would work out to n pproximte loding of mg/seed. For thimethoxm, we looked t vrious Cruiser lbels (e.g. EPA Reg. No , , ). The following direct loding rtes were given: 0.8 mg/corn kernel, 0.03 mg/rice seed, mg/cotton seed, 0.25 nd 0.29 mg/kg for sunflower nd penut respectively. The higher rtes for whet nd cnol work out to nd mg/seed. Bsed on US EPA 2002 memorndum, cetmiprid ws registered for cnol tretment t 0.25 lb.i./100 lbs of seed. owever, the specific lbel with those use instructions (Adjust 70WP Reg. No ) is currently inctive nd we do not know whether it hs been superseded yet by new lbel with the sme uses (e.g. Vult TM insecticide registered in Cnd). Tht concentrtion of cetmiprid would work out to mg/seed. We re not wre of seed tretment use for thicloprid. The chosen risk mesure for the current ssessment is the number of seeds tht 15 g bird could ingest before reching either medin lethl dose (Tble 5.1) or the estimted reproductive NOAEL or LOAEL (Tble 5.2). At this point, we ssume no ctive voidnce of ny of the seed by birds (see discussion below) nd concentrtion on the seeds reflecting the usul lbel rte. A consistent bird weight of 15g ws chosen in line with previous clcultions by Mineu nd collegues (2006). It is cknowledged however tht sprrow-sized birds my be little smll to ingest whole corn seed in ny quntity. Tble 5.1. Estimted no. of seeds needing to be ingested by 15g bird to chieve 50% chnce of lethlity given sensitivity t the 5% til of the bird distribution. Active ingredient Seed type mg/seed Criticl endpoint Endpoint vlue (mg/kg) No. seeds to endpoint imidcloprid Corn 1.34 D5* cnol/rpeseed D5* Whet D5* clothinidin Corn 1.25 D5* cnol/rpeseed D5* Whet D5* thimethoxm Corn 0.8 D5* cnol/rpeseed D5* Whet D5* cetmiprid cnol/rpeseed D5* * Unscled LD50 for birds t the 5% til of species sensitivity 28

30 Neonicotinoid Insecticides nd Birds Tble 5.2. Estimted no. of seeds needing to be ingested by 15g bird to chieve estimted reproductive effects. Active ingredient Seed type mg/seed Criticl endpoint Endpoint vlue (mg/kg) No. seeds to endpoint imidcloprid Corn 1.34 LOAEL cnol/rpeseed LOAEL Whet LOAEL clothinidin Corn 1.25 LOAEL cnol/rpeseed LOAEL Whet LOAEL thimethoxm Corn 0.8 LOAEL cnol/rpeseed LOAEL Whet LOAEL cetmiprid cnol/rpeseed LOAEL It is cler tht the loding of ll neonicotinoid insecticides on corn is such tht cute intoxictions re possible with the three registered products. With imidcloprid, the number of seeds needing to be consumed is less thn 1 even for lrger (e.g. blue jy-sized) bird more likely to be picking up whole corn seed from seeded fields. Acute intoxictions in whet or cnol re not likely with clothinidin or thimethoxm becuse of the number of seeds needing to be ingested. owever, bsed on chronic/reproduction endpoints, ll seed tretments re predicted to cuse effects given the very smll number of seeds needing to be ingested to push birds into criticl rnge. Indeed, recent work on clothinidin in Jpnese quil (Tokumoto et l see below) suggests tht effects on bird fertility nd embryonic development re occurring t dose levels lower thn the criticl levels indicted by the stndrd reproduction study. The min uncertinty here is how long the seeds will be vilble to birds nd how long dosing is necessry before the type of effects observed in the lbortory will be seen in the wild. There re huge uncertinties such s wht types of effects might be seen in ltricil 9 species. owever, bsed on our current understnding nd risk ssessment procedures in plce, the neonicotinoids s group hve high potentil to ffect vin reproduction. This is due in lrge prt to the very high exposure potentil tht seed tretment chemicls represent. Recently, Lopez-Anti nd collegues (2012) tested the effect of imidcloprid seed tretments on cptive red prtridges. They pplied the mteril to whet t the intended lbeled rte of 0.7 g.i./g of seed nd twice tht rte 10. Actul mesured concentrtions were 74% nd 62% of nominl for the 9 Altricil species re those where the young re born nked nd blind nd need prolonged period of prentl cre to fledge. Mllrd nd bobwhite, the two test species, re both precocil species with young being mobile nd ble to feed themselves within few hours of htching. 10 This works out to nd mg/seed. The mximum llowed in the US flls between those two concentrtions. Given the reported mesured concentrtions, the high rte used in the experiment is lmost exctly the high rte llowed in the US. 29

31 Neonicotinoid Insecticides nd Birds low nd high dose rtes respectively, mening tht the high rte ws only slightly higher thn lbeled rte. Exposure lsted for 10 dys. Exposure strted 15 Mrch nd, bsed on personl communiction from one of the co-uthors (Rfel Mteo, pers. comm.) egg-lying begn 16 April nd ws concluded 28 My. Severl of the birds died during tretment, reducing the number of pirs vilble for breeding. Unfortuntely, food consumption ws not mesured, preventing n ssessment of ny voidnce. owever, birds in both imidcloprid groups showed reduced body condition suggesting reduction in food intke. (This ws confirmed in the personl communiction described bove. owever, in prllel tril, it ws found tht birds te norml mount of seed when treted nd untreted seed were mixed.) Cellulr immune function is reported to hve declined in mles t the high dose rte. Both mles nd femles showed reduced eye ring pigmenttion n interesting finding but one of unknown significnce t this point. Dt on reproductive success re difficult to interpret. Becuse of the smll number of birds tht survived, dt were nlysed using ech egg lid s n independent sttisticl unit. This ignores tht eggs within clutch re not sttisticlly independent nd therefore limits the inferences tht cn be mde from the reserch. The experiment does not dd criticl reproduction informtion beyond wht is known from the regultory studies. It does rise some questions s to new nd unexpected effects not typiclly mesured in the stndrd studies. Tokumoto nd collegues (2013), gve mle Jpnese quil dily doses of formulted clothinidin (Dntotsu TM 16% formultion of clothinidin mnufctured by the Sumitomo Chemicl co.) t rtes of 0.02, 1 nd 50 mg/kg over 30 dy period. These mles, long with the usul control individuls, were then mted to unexposed femles nd the eggs collected nd checked for fertility nd embryonic development. Testes, livers nd spleens were collected for exmintion. Their working hypothesis ws tht sperm production would be ffected though oxidtive stress s seen in mmmlin systems. They were most concerned bout the welfre of the crested Ibis (Nipponi nippon), criticlly endngered species being relesed into the wild from cptive breeding fcilities nd known to frequent rice fields nd other res where neonicotinoid insecticides re being used. The 50 mg/kg dose in quil cused one mortlity nd signs of toxicity in severl individuls. Interestingly, dosing cused n increse in bodyweight which the uthors ttributed to impired liver function. (The uthors reviewed similr reports of impired liver function with imidcloprid nd thicloprid in chickens.) There ws dose-relted increse in testiculr bnormlities nd DNA brekge in germ cells even though eventul fertility ws not ffected. Embryo length ws reduced in dose-dependent fshion with significnt effects seen in the 1mg/kg group. Embryo weight ws lso ffected. Some of the dosed embryos stopped developing ltogether but smple sizes re too smll to ssess whether this ws significnt issue. Finlly, rther sweeping proposl ws recently mde by Mson nd collegues (2013). They postulte tht mny of the severe epizootic diseses tht seem to rise with lrming frequency (chytrid fungus in mphibins, white nose syndrome in bts, mycoplsml nd other recently discovered pthogens in finches nd other bird species in North Americ nd Europe) my be the result of immune suppression resulting from low level exposure to neonicotinoids. They bse their hypothesis on reports of immune suppression in bees, fish nd rts following neonicotinoid exposure s well s on time nd plce correltions between neonicotinoid uses nd disese outbreks. Additionl reserch is needed, given the serious potentil consequences of this hypothesis. It is relevnt to sk how the neonicotinoid insecticides compre to other registered seed tretments. It is beyond our scope to conduct complete review of ll US-registered seed tretments. owever, 30

32 Neonicotinoid Insecticides nd Birds review of seed tretments ws crried out in Cnd by Mineu nd collegues (2006) nd hs been modified for this report. The comprison of cute lethl toxicity (Tble 5.3) uses scled D5 vlues with the exception of cetmiprid where the new informtion vilble for the zebr finch is considered criticl piece of informtion. Appliction rtes were djusted for the neonicotinoids in order to reflect US conditions described in this report. This could not be done for ll other ctive ingredients (primrily fungicides) but differences between seed tretment rtes in Cnd nd in the US re thought to be slight. As discussed bove, 15g bird is not likely to be feeding on whole corn seed; vin body weight ws incresed to 50g for tht seed type weight somewhere between tht of lrge sprrow nd blue jy. Tble 5.3. A comprison of the cute lethl toxicity of seeds treted with neonicotinoid insecticides (in bold) nd other common seed tretment chemicls. Seed tretment rtes for neonicotinoids re s lbeled in the US; those for other ctive ingredients re s lbeled in Cnd. Type of seed treted Averge weight of individul seed (g) Mximum rte AI per prticle (mg/seed) Risk s no. seed needed to rech D5 Scled bird AI Accepted Nme D5 weight (g) Imidcloprid Cnol Acetmiprid Cnol Thirm Cnol Crbthiin Cnol Thimethoxm Cnol Clothinidin Cnol Iprodione Cnol Metlxyl Cnol Metlxyl-m (mefenoxm) Cnol Difenoconzole Cnol Fludioxonil Cnol Crbthiin Cerel Imidcloprid Cerel Thirm Cerel Clothinidin Cerel Mneb Cerel Thimethoxm Cerel Tebuconzole Cerel Metlxyl Cerel Difenoconzole Cerel Metlxyl-m (mefenoxm) Cerel Tridimenol Cerel Fludioxonil Cerel Triticonzole Cerel Dizinon Corn Imidcloprid Corn Cptn Corn Crbthiin Corn

33 Neonicotinoid Insecticides nd Birds Thirm Corn Clothinidin Corn Metlxyl Corn Thimethoxm Corn Mncozeb Corn Thiophnte-methyl Corn Difenoconzole Corn Metlxyl-m (mefenoxm) Corn Fludioxonil Corn Agin, it is cler tht imidcloprid seed tretments crry higher risk of lethl intoxiction thn most other seed tretments. Two exceptions re dizinon on corn seed nd crbthiin on cerel, both of which hve been replced by or in the cse of whet, is in the process of being replced by the neonicotinoids. For the comprison of chronic toxicity (Tble 5.4), endpoints were modified to reflect the review of reproductive endpoints crried out in this report (Tble 3.1). For other ctive ingredients, NOAEL vlues were obtined from EPA summry dt (One liner dtbse - B. Montgue, pers. comm.). Tble 5.4. Comprison of the chronic/reproductive toxicity of neonicotinoids nd other registered seed tretment chemicls. Active ingredient Type of seed treted Bobwhite NOAEL (ppm) Mllrd NOAEL (ppm) Criticl intke level (mg/kg/dy) for sensitive bird t 5% til Prticle lod (mg/seed) Risk (no. seeds to criticl intke)* Imidcloprid Cnol Thirm Cnol Acetmiprid Cnol Thimethoxm Cnol Clothinidin Cnol ** Crbthiin Cnol Iprodione Cnol Metlxyl Cnol Difenoconzole Cnol Fludioxonil Cnol Crbthiin Cerel Mneb Cerel Tebuconzole Cerel Imidcloprid Cerel Thirm Cerel Tridimenol Cerel Metlxyl Cerel Clothinidin cerel

34 Neonicotinoid Insecticides nd Birds Difenoconzole Cerel Thimethoxm Cerel Triticonzole Cerel Fludioxonil Cerel Dizinon Corn Imidcloprid Corn Thirm Corn Cptn Corn Mncozeb Corn Crbthiin Corn Metlxyl Corn Clothinidin Corn Thimethoxm Corn Thiophntemethyl Corn Difenoconzole Corn Fludioxonil Corn * For 15g bird in the cse of cerels or cnol; 50g bird for corn. ** It is noteworthy tht Tokumoto nd collegues (2013) found tht doses s low s 1mg/kg clothinidin dily cused testiculr nomlies nd incresed DNA breks in mles s well s reductions of embryonic length when those mles were mted to undosed femles. These endpoints hve not been specificlly studied with other pesticides nd they re therefore not used here. This comprison highlights one of the current problems in pesticide risk ssessment. Severl ctive ingredients currently registered hve the potentil to cuse reproductive effects t lest bsed on the vilble lbortory studies. The need to verify some of these problems in the field ws brought up lmost two decdes go (Mineu et l. 1994) but persists to this dy. Indeed, extrpoltion from the contrived lbortory study with two precocil gmebird species to the intriccies of reproductive behvior in the field tkes veritble lep of fith. The lck of relism of the current study protocol s well s the existing difference between the two tested species (mking extrpoltion to third species even more tenuous) hs been well documented (Mineu et l. 1994, Mineu 2005, Luttik et l. 2005, Fernndez-Pere et l. 2009). Wht is missing is solution to this conundrum. Fernndez- Pere et l. (2009) believe tht the solution lies in the ppliction of lrge sfety fctors in the risk ssessment process. owever, this is not the cse now nor is it likely to hppen given tht lrge number of pesticides currently fil the test even before sfety fctors re pplied. Nevertheless, on comprtive bsis, the use of imidcloprid on corn or cnol ppers to be ill-dvised given tht consumption of 1 seed per dy is expected to bring birds over the limit where reproductive effects might be seen. Even if prt of the seed coting is lost t seeding or some of the pesticide is discrded when the seeds re hulled by the birds, criticl dosing is likely to be exceeded Incidents 33

35 Neonicotinoid Insecticides nd Birds The monitoring nd reporting of bird kills in the US hs been very limited in recent yers due to 1997 mendments to federl pesticide lws 11. There hve been reltively few reports involving neonicotinoids. This is in prt becuse the cute toxicity of these insecticides is lower thn tht of the orgnophosphorous nd crbmte insecticides tht they replced. Moreover, methods for dignosing kills either do not exist, or re not widely used. There is no esy biomrker s there is for cholinesterse inhibitors, lthough we believe tht one should be developed. There is strong cse to be mde tht, where cute intoxictions re possible, registrnts should be compelled to develop the dignostic tools necessry. In the cse of neonicotinoids, it should be reltively esy to work out binding ssy for the neurl receptor which is ffected by this clss of insecticides. Acute intoxictions with seed tretments hve been seen in Frnce (Berny et l. 1999). In its 2008 re-ssessment of imidcloprid, the USEPA reported n incident where grubs surfcing fter lwn tretment pper to hve poisoned young robins (USEPA 2008). More detils re vilble from the Americn Bird Conservncy s AIMS dtbse of kills (unfortuntely, government funding for this dtbse ended in 2006). A totl of seven birds were found ded or dying in this incident, which occurred on n re of residentil turf in Pennsylvni in In nother cse, 4 Cnd geese were found ded or dying on New Jersey golf course in June A mixture of chlorpyrifos nd imidcloprid hd been used on the course but the lck of cholinesterse inhibition suggested imidcloprid might hve been responsible. On South Crolin residentil property treted with imidcloprid in 2002, 6 mllrds were found ded or dying but no further informtion ws provided. In the spring of 2012, lrge number of bee deths were reported in SW Ontrio following the seeding of corn fields with clothinidin. In one such bee kill, ded robin ws reported midst ded nd dying bees thirteen dys fter seeding in ensll, Ontrio. About week lter, flyctcher ws lso found in the sme yrd. The incident is currently being investigted by the PMRA The issue of repellency Imidcloprid Bsed on erly reserch with imidcloprid-treted rice seed (Avery et l nd follow-up study, 1993b/1994) the registrnts of imidcloprid hve tried to mke the cse tht the ctive ingredient repels birds nd, therefore, is less of risk to birds thn clculted. Some of the tests reported employed two cup design (e.g. Avery et l. 1993b). This design mkes it esy for birds to recognise nd void treted seed when untreted seed is fed longside. In ddition, exposure to the treted seed ws brief nd the birds received their norml rtion before nd immeditely fter exposure to the treted seed nd untreted lterntive. The birds were therefore not subjected to ny form of food stress. Birds given treted seed only in single cup exhibited mrked reduction in feeding t ll dosing levels. Work on seed tretments (e.g. CSL 2002) hs shown tht, for lbortory tests to hve ny bering on the wild sitution, hunger stress nd motivtion to et novel seed must be mnipulted crefully. 11 Under its revised clssifiction criteri, EPA designtes s minor (nd thus brely reportble, side from ctloguing s WB ) ny pesticide incident tht kills fewer thn 200 individuls of flocking species, 50 individuls of songbird species, or 5 rptors. 34

36 Neonicotinoid Insecticides nd Birds A more interesting design involved brodcsting treted nd untreted seed on smll plots within n viry, mimicking (lbeit on smll scle) field sitution where one seeded field might be treted but neighbouring one not. This ws done t the highest seed tretment rte tested (2500 ppm). (In compring this with the seed rtes registered, the loding per seed is similr to the higher loding on corn seed 12 ). More seed ws removed from the control plots thn from the treted seed plot. owever, birds feeding on the treted plots did not rect s if the seeds were diststeful or unpltble. Birds feeding on the treted plots ingested seeds t rte of 5.4 seeds per minute versus 6.9 seeds per min. on control plots. The experimenters estimted from nother experiment tht 84-87% of the totl insecticide lod ws not consumed but left behind on the hulls. In lter work, however, the sme Byer-sponsored reserch tem (Avery et l. 1997) found tht house finches (Crpodcus mexicnus), red-winged blckbirds (Agelius phoeniceus) nd bot-tiled grckles (Quisclus mjor) only discrded between 15-41% of imidcloprid on treted millet, rice, sunflower or sorghum when shelling the seeds, nd tht there were severl species-seed type combintions where seeds were eten whole nd ll residues ingested. In their 2007 regultory review (EPA 2007), the EPA scientists quite rightly expressed misgivings bout relying on ny repellency to mitigte the high hzrd suggested by the toxicology. owever, to wht extent risk would be mitigted is still n uncertinty. Both studies suggested tht voidnce of birds to imidcloprid treted seed is lerned response medited by postingestionl distress. The treted seed ws not sensory repellent or irritnt to the birds. Although the birds did et the treted seed nd exhibited tretment relted effects (txi nd retching), effects were deemed s trnsitory. These effects, lthough deemed s trnsitory under lbortory conditions, my mke the ffected birds more susceptible to predtion in the wild. owever, to wht extent this is possibility is unknown. Indeed, when voidnce is due to post-ingestionl illness, the bility of birds to void the chemicl is directly relted to their bility to ssocite the contminted feed with the illness. Wheres this my be reltively esy for them to do in lbortory sitution, it becomes much more difficult in the wild when hbitul food sources hve become contminted. There re cler prllels with the cholinesterse-inhibiting insecticides where repellency ws similrly thought to reduce infield risks. For exmple, the orgnophosphorous insecticide dizinon is extremely well voided in the lbortory. Yet, thousnds of geese nd other species grzed their wy to n erly deth on dizinon-treted turf (Frnk et l. 1991, Mineu et l. 1994). Given tht shelling is very species nd seed specific, it is resonble to ssume tht some species will incur the full toxicologicl risk by ingesting seeds without shelling them. Mortlity of prtridges nd pigeons with imidcloprid-treted seed hs been seen in Frnce (Berny et l. 1999), one of the few countries with n ctive investigtion system for pesticide poisonings. Reports cme in of birds ppering wek nd reluctnt to move. They subsequently tested positive for residues. Regrdless of the exct conditions surrounding the kills (seed concentrtion etc.) they do suggest tht ny voidnce/repellency is not operting well enough under ctul field conditions to prevent exposure nd cute intoxiction. 12 A 2500 ppm concentrtion would work out to pproximtely mg/whet seed or 0.95 mg/corn seed. On rice, this cme to mg/seed. 35

37 Neonicotinoid Insecticides nd Birds Clothinidin Industry studies on voidnce were submitted for clothinidin. These followed the Germn BBA (Ministry of Agriculture) Test Guideline. The first (Brfknecht 1998) tested Jpnese quil exposed to treted cnol (rpeseed). The birds were hbituted to seed diet consisting of 50% rpeseed, 10% millet nd 60% cnry seed (sic - yes this dds up to more thn 100%). A week before exposure, the birds were given choice of 1:1 of their usul seed mixture nd the untreted trget seed type, in this cse rpeseed scttered on the ground. At the beginning of exposure, the birds (4 mles nd 4 femles) were fsted for 16 hours nd then exposed to mixture of their stndrd diet nd clothinidin-coted rpeseed. The ltter hd violet ppernce. The mount of regulr seed provided ws clculted to represent 25% of their usul dily intke only, while treted seed mde up the rest. Exposure lsted for 8 hours fter which the birds were returned to stndrd diet nd observed for further 14 dys. The entire design ws repeted four times. According to the uthor, the birds showed high rte of food intke during the first hour of exposure. e climed tht, with the exception of one bird, the stndrd diet only ws consumed while the treted seed ws left untouched. Without further informtion, we find this clim difficult to support. It is difficult to see how single observer could observe 8 birds simultneously nd determine wht the birds were ctully pecking t since the stndrd diet nd treted seed were sid to be spred uniformly on the floor. Following the first hour, birds were only observed t hourly intervls. No feeding ctivity ws observed t ny point between the first nd 8 th hour post dose. It is possible tht the viry floors were sieved nd the remining seed counted but this ws not pprent from the methods. No signs of intoxiction or mortlity were observed but two individuls (of 32) showed enlrged spleens t necropsy. This ws judged to be within norml vrition. In second study (Brfknecht 1998b), domestic rock doves were exposed to treted corn (mize) seed t 50 g.i./ seeds. The usul diet in this cse ws composed of 30% mize, 21% pes, 20% brley, 18% whet, 8% milo, 2% dri nd 1% vetch. Procedures were the sme s described bove except tht exposure ws repeted on three consecutive dys (8 hours/exposure period). As with the quil bove, the uthor reported tht the birds fed hevily during the first hour. owever, only one bird (of 10) showed reserved interest on treted seeds but spt out the red-coloured treted seeds immeditely fter picking them up. We believe this to be one off observtion without much ctul relevnce given tht the mechnism of voidnce of neo-nicotinoids is understood to be post-ingestionl illness. No signs of intoxiction or mortlity were observed. owever, 2 of 10 birds showed enlrged spleen t necropsy, nd 4 of the 10 showed reduced gond size scribed to the fct tht breeding condition hd not been induced in those birds 13 (the study ws run in My/June). Unfortuntely, there were no control birds with which to compre this popultion nd the uthor did not scribe ny importnce to those findings. In third study (Brfknecht 2000), rock doves were exposed to treted corn gin but t hlf of the concentrtion s the previous experiment (25 g.i./ seeds). This time, birds were either given untreted seed only or treted seed only. Food consumption ws mesured from 3 dys preexposure to three dys post exposure. On the dy of exposure, food intke (s proportion of body weight) ws sid to be 5.14% of body weight for control birds nd 2.32% for the treted seed. In 13 Bird species tested here re typiclly brought into breeding rediness by photoperiod (the rtio of the dily light to drk period). Filure to do so my be n indiction of some interference with the endocrine system. 36

38 Neonicotinoid Insecticides nd Birds terms of food weight, this ment tht individul birds feeding on treted seed consumed between 0 nd 20.5g of seed on exposure dy (men = 11.7g) compred to 20.4 to 34.8 (men = 26.1 g) for the control birds. This led the uthor to conclude tht the seeds were prtilly voided. On the whole, we support the US EPA view tht voidnce of treted seed hs not been sufficiently well demonstrted in relistic field context to believe tht this will mitigte ny high toxicologicl risk. 6. Could neonicotinoid insecticides be disrupting food chins nd ffecting birds indirectly? It hs been suggested by the Dutch toxicologist enk Tennekes (2010) tht the neonicotinoid insecticides nd other systemic products represent disster in the mking becuse of their potentil to ffect birds through reductions of their food supply. This mtter hs severl sub-questions relted to it. The first is whether it is indeed fesible to ffect bird popultions though reduction of their food supply. A smll review of the subject is clled for here ve reductions in the vilble food supply been shown to ffect birds? Food supply (i.e. bundnce nd vilbility) cn ffect hbitt selection, reproductive success nd survivl in birds (Simons nd Mrtin 1990, Mrtin 1987, Johnsson nd Blomqvist 1996, Brickle et l. 2000, Moller 2001, ole et l. 2002, Ngy nd olmes 2004, Strong et l. 2004, Botmn et l. 2004, Morris et l. 2005, Ngy nd olmes 2005, Britschgi et l. 2006, rt et l. 2006, Znette et l. 2006, Golwski et l. 2008, Sels et l 2008, Dunn et l. 2010, Poulin et l. 2010). In cses where food vilbility hs not been to found to ffect life history it is either considered to be superbundnt (Powell 1984, Greer nd Anderson 1989, Miller et l. 1994, Ruter et l. 2000), or in the cse of reproductive success, dults re considered to compenste for low food vilbility by trvelling further to find food, or spending more time forging (Adms et l. 1994, owe et l. 2000, Mrtin et l. 2000, Brdbury et l. 2003, Zlick nd Strong 2008). Given tht reproductive success nd survivl re key components of popultion growth nd stbility, one might be tempted to ssume tht bird popultions will redily show response to the food supply. There certinly re exmples of bird species whose popultions trck irruptive pests e.g. wood wrblers nd spruce budworm in estern North Americ. Showing this link in n griculturl context is hrder. Most of the detiled work on the effects of food supply on frmlnd birds hs been crried out in the UK. Evidence tht food supply cn ffect reproductive success of frmlnd birds in the UK is firly strong, but links with popultion declines re weker. The best documented exmple of food supply ffecting frmlnd birds is the exmple of the gry prtridge (Perdix perdix). erbicide use reduces the bundnce of invertebrtes in frm fields, including the bundnce of preferred invertebrte prey items criticl to the growth nd survivl of gry prtridge chicks. Simultion modelling shows tht declines in gry prtridge popultions cn be wholly explined by herbicide use in frmlnd (reviewed by Potts 1986). Insecticide use leding to reduced invertebrte food bundnce hs been linked to reductions in reproductive success of t lest four frmlnd psserines in the UK: corn bunting (Miliri 37

39 Neonicotinoid Insecticides nd Birds clndr), yellowhmmer (Emberiz citrinell), whincht (Sxicol rubetr) nd reed bunting (Emberiz schoeniclus) (Brickle et l. 2000, Brickle nd Pech 2004, Morris et l. 2005, rt et l. 2006, Dunn et l but see Brdbury et l. 2000, Brdbury et l. 2003). owever, in contrst to the gry prtridge, chnges in invertebrte bundnce lone do not fully explin popultion declines for these species. In fct, reproductive success for these species incresed during time periods when popultions were declining (Siriwrden et l. 2000). Popultion declines hve insted been linked to reduced over-winter survivl, linked to reduced seed vilbility (Pech et l. 1999, Siriwrden et l. 2000, Butler et l. 2010). The gry prtridge therefore remins the only cler exmple of pesticide-induced insect food reductions ffecting bird popultion directly. An exmple of pesticide-induced effects possibly more relevnt to brod contmintion of the qutic environment by neonicotinoid insecticides is the work crried out in the Cmrgue region of Frnce following the use of the biologicl insecticide Bti (Bcillus thuringiensis isrelensis) for the control of mosquitoes (Poulin et l. 2010, Poulin 2012, Poulin et l. 2012). Despite the very selective nture of Bti (being toxic to mosquitoes nd some midges only), the reserch tem documented cler impcts on the broder vin food web, especilly spiders nd other predtor species, s well s breeding success reductions in house mrtins (Delichon urbicum) nesting nerby. owever, it is importnt to note tht the bility of bird popultion to mintin itself is dependent on rte of re-nesting ttempts nd post-fledgling survivl s well s success of single nesting ttempts (Setchfield et l, 2012). Rte of re-nesting ttempts hs been shown to be ffected by food supply (Ngy nd olmes 2005), nd cn hve mjor effect on nnul reproductive success (Ngy nd oles 2005, Setchfield et l. 2012). Post-fledgling survivl is lso thought to be closely tied to food vilbility (Sullivn 1989, Simons nd Mrtin 1990, Yckel Adms et l. 2006), lthough very little is known bout this stge since juveniles re very difficult to follow or study. Survivl rtes of gry prtridges include this vulnerble stge, since these birds re precocil nd leve the nest very soon fter htching. Although invertebrte food supply hs been suggested s mechnism for incresed bundnce nd species richness of birds on orgnic frmlnd in North Americ (Freemrk nd Kirk 2001, Beecher et l. 2002), nd for reductions in the reproductive success of tree swllows (Tchycinet bicolor) s the proportion of intensive griculture in the lndscpe increses (Ghilin nd Bélisle 2008), very little reserch hs been conducted on diet, forging hbitt or food supply of frmlnd birds in North Americ. Frmlnd breeding birds in North Americ re known to use crop fields, hy fields nd boundry fetures, such s hedgerows, for forging (Best et l. 1990, Boutin et l. 1999; Puckett et l. 2009). Boutin et l. (1999) surveyed birds in corn, soyben, pple orchrds nd vineyrds in southern Ontrio nd found tht of 14 species regulrly observed within field centers nd in edges djcent to crop fields, most species were observed in edges more thn expected bsed on hbitt vilbility. Vesper sprrows (Pooecetes grmineus) nesting in corn nd soyben fields forge most often within 1 m of weedy or unplnted res, nd prefer fields with crop residue over bre fields, presumbly due to incresed food supply (Rodenhouse nd Best 1994). Song sprrows (Melospiz melodi) nesting in hedgerows djcent to hy, corn nd soyben in estern Ontrio were found to obtin pproximtely 40% of invertebrte nestling food from crop fields nd 60% from hedgerows nd hyfields (Girrd et l. 2012). owever, Zlick nd Strong (2008) exmined food supply for svnnh sprrows (Psserculus sndwichensis) in mown nd unmown hyfields nd found no effect of food reductions on reproductive success. In estern Ontrio, orgnic soyben fields were found to support greter biomss of soil-dwelling invertebrtes importnt for feeding nestlings thn conventionl soyben fields, but reproductive success of song 38

40 Neonicotinoid Insecticides nd Birds sprrows nesting in hedgerows in this region ws not ffected by locl invertebrte food vilbility (Girrd 2012). There hs been smll mount of experimentl mnipultive work on the food supply of breeding birds in North Americ, but this work hs occurred in forests or ntive grsslnds, rther thn in intensively mnged pstures or croplnd. In grsslnds, the effects of experimentl reductions in food supply due to insecticide ppliction hve hd little or no effects of reproductive success of birds (Powell 1984, Adms et l. 1994, Mrtin et l. 1998, Mrtin et l. 2000). Girrd (2012) found tht differences in soil-dwelling invertebrte biomss between orgnic nd conventionl fields ws gretest in the fields themselves, rther thn in the field edges or hedgerows, suggesting tht birds tht most depend on the fields will be most ffected by invertebrte food reductions. For forest species, s mentioned bove, the rise nd fll of wrbler species in response to budworm outbreks remins one of the best indictions of the impct of food supply on popultions. In summry, the link between impcts on the insect food of birds nd popultion declines of frmlnd bird species is difficult to estblish unequivoclly, sve for the evidence linking the grey prtridge to both insecticide nd herbicide use. Studies linking reductions in house mrtin breeding success nd mosquito control re directly relevnt to the issue of brod qutic contmintion from the neonicotinoid insecticides. Nevertheless, existing literture suggests tht it is difficult to predict the reltive importnce of food supply during the breeding seson compred to other risks such s hbitt loss, food supply during migrtion nd during winter, predtion or even direct losses from poisoning or disturbnces such s mowing or tillge. Ech species responds to different set of stressors nd it is likely tht resons behind mny of frm bird declines re multi-fctoril. Frmlnd species re lredy well dpted to use multiple, irregulr food sources tht my collpse overnight s result of griculturl opertions, whether tillge, mowing or insecticide use; these species lredy tke lrge proportion of their food outside of ctively cropped (nd pesticide-treted) res. Insecticides registered for griculture before the dvent of neonicotinoids, whether orgnochlorines, cholinesterse inhibitors or synthetic pyrethroids, were ll rther indiscriminte in the type of insects they killed nd sudden drops in food vilbility following insecticide tretment were undoubtedly commonplce before the neonicotinoids becme so dominnt in insect control. On the other hnd, systemic insecticides such s the neonicotinoids might be gme-chngers (Frncisco-Byo et l. 2013). Becuse of their persistence in plnt tissue, there is some evidence tht they my ffect terrestril insect popultions to greter extent thn non-systemic products. Systemic insecticides cn be returned to the soil nd remobilised in succession crops. The impcts on terrestril food chins my therefore be much longer-lived nd pernicious thn those we hve seen with other types of insecticides. Not only cn these questions not be nswered with the informtion mde vilble through the registrtion process but the questions themselves hve not even been considered (sve few comment by EPA scientists on structurl nd functionl chnges to ecosystems see section 1.3). Generlly speking, n over-efficient removl of insects in crop fields is seldom seen s mtter of serious concern by regultors especilly in North Americ. The indirect impcts of pesticides re not considered in registrtion reviews whether the US or nywhere else in the world. In his book, the Dutch toxicologist enk Tennekes (2010) mkes the cse tht the contmintion of surfce wter by neonicotinoids is so widespred in the Netherlnds (nd possibly elsewhere in Europe), tht loss of insect biomss on continentl scle is behind mny of the widespred declines tht re being seen, be they of mrsh birds, heth or medow birds or even costl species. This suggests tht we should be looking t possible links between neonicotinoid 39

41 Neonicotinoid Insecticides nd Birds insecticides nd birds, not on frm scle, but in the context of whole wtersheds nd regions. Impcts from the neonicotinoids my very well be further field thn the rble re on which they re used nd mny of those impcts my be medited through the qutic environment. Becuse qutic impcts re considered during product registrtion reviews, it is resonble to sk whether the potentil impct of neonicotinoids to qutic life hs been ssessed correctly. 7. ow toxic re the neonecotinoids to qutic life? In terms of scle of use, clothinidin nd the other more recently- registered neonicotinoid insecticides thimethoxm, cetmiprid nd thicloprid hve probbly overtken imidcloprid. Yet, much more is known bout imidcloprid, nd lot of the toxicity informtion being published now fetures tht ctive ingredient lmost exclusively. By necessity, much of this review will emphsize imidcloprid. We suggest (see 7.4) tht the other neonicotinoids cn be ssessed through comprison with imidcloprid s the toxicity of imidcloprid to qutic life been properly ssessed? In crrying out risk ssessment, it is customry for regultors to pick criticl toxicity vlue (or reference level) ginst which to compre exposure estimtes or empiricl wter residue mesurements. Vrious methods re used, some more scientificlly rigorous thn others. In sking whether the USEPA properly ssessed the qutic risks posed by imidcloprid, it my be unfir to go bck to the very first registrtion reviews becuse, clerly, we know much more bout the product now thn we did when it ws first registered in the mid-1990s. A more recent evlution of the ctive ingredient cme in 2007 when EPA ws considering requests to expnd the use of this ctive ingredient, notbly for soybens, penuts, kv, millet, ots, rtichoke, wild rspberry, nd cne berries (USEPA 2007). At the time, imidcloprid ws lredy registered for vriety of lefy nd fruiting vegetbles, pome fruits, cotton, pottoes, hops, pecns, cucurbits, citrus, nd tobcco, nd hd been studied extensively. In this 2007 risk ssessment, the EPA stted tht imidcloprid is ctegorized s very highly toxic ( ppm) to freshwter invertebrtes on n cute bsis. This ws bsed on two freshwter species tested by the registrnt in the erly 1990s; the lower vlue ws used to compute risk rtios with predicted exposure levels. By 2007, there were lredy host of studies in the open literture showing cute toxicity levels s low s ppm (see nnex 1). Despite the fct tht Dphni hd been shown to be very insensitive species compred to other qutic invertebrtes, this ws the only chronic dt exmined or required by EPA; on tht bsis, EPA concluded tht imidcloprid exposure to freshwter invertebrtes cn potentilly result in growth effects t 3.6 ppm. The NOEC for tht sme study ws given s 1.6 ppm full 23 times higher thn cute toxicity levels. Fortuntely, when it cme time to compute finl risk rtios, the EPA scientists bndoned this vlue in fvour of vlue of ppm obtined through n cute toxicity vlue nd n cute/chronic extrpoltion fctor. As luck would hve it, 14 the mrine invertebrte species tht hppened to be tested proved to be more sensitive to the pesticide nd reference levels were deemed to be lower in the mrine 14 In relying on hndful of test species, it is cler tht current regultory ssessments hve more to do with gme of chnce thn with good science. 40

42 Neonicotinoid Insecticides nd Birds environment. The 2007 EPA review stted: Imidcloprid is very highly toxic to esturine/mrine invertebrtes (mysid shrimp) on n cute bsis (0.037 ppm) nd chronic exposure of imidcloprid to esturine/mrine invertebrtes cn result in growth nd survivl effects ( ppm). In fct, ll of these reference levels re t lest n order of mgnitude too high (see below) nd totlly fil to protect the qutic environment. This exmple highlights the problems of blindly dhering to strict review protocols tht ignore much of the ccumulted scientific evidence nd scientific insights vilble from the open literture in fvour of few outdted studies crried out by the registrnt. By the time risk quotients re clculted by EPA scientists, it is difficult to know how much the selection of specific reference levels hs bering on registrtion decisions. Despite the incomplete use of vilble dt by EPA in 2007 nd the inherent underestimtion of risk, clculted risk quotients for ll proposed new uses exceeded EPA s chronic level of concern. Yet, it ppers tht ll new uses were pproved for registrtion. In December of 2008 (EPA 2008), the EPA lunched re-evlution of imidcloprid. It is cler from the re-evlution notice tht the emphsis is to be on honeybees. Despite n cknowledgment of imidcloprid s high qutic toxicity, no requirements re set out for better chrcteristion of qutic risk. The EU (EFSA 2008) bsed its finl 2008 risk ssessment of imidcloprid on the most sensitive of two species tested (Dphni mgn nd Chironomus riprius) s well s on mesocosm study. The use of mesocosm results sets the EU process prt from tht used by EPA. The Europen regultory body proceeded to clculte their risk rtios with the following: Acute risk: 24 h EC50 of 55.2 ug/l Chronic risk: EC5 (emergence) for 28 d exposure of 1.9 ug/l Community risk: NOEC of 0.6 ug/l given DT50 of d in the system studied. The LOEC ws 1.5 ug/l but, t this concentrtion, no recovery ws seen t the conclusion of the experiment. The Agency suggested tht sfety fctor of 1-3 would be pproprite long with the NOEC vlue cited bove, giving n pproximte vlue of 0.2 ug/l on which to compre clculted or empiricl wter concentrtions. In Cnd, the CCME 15 developed non-regultory wter qulity guidelines for imidcloprid in For freshwter bodies, they used the sme Chironomus emergence study but retined the EC15 (emergence) of 2.25 ug/l to which they pplied n rbitrry sfety fctor of 10. They therefore proposed n interim freshwter protection level of 0.23 ug/l. For the mrine environment, they only hd cute studies. They retined 48h LC50 of 13 ug/l for the slt mrsh mosquito to which they pplied sfety fctor of 20 on the grounds tht imidcloprid is non-persistent in wter 16. The interim proposed guideline for sltwter environments ws therefore set t 0.65 ug/l. It is more difficult to ssess the dequcy of the PMRA s ssessment of qutic risk from imidcloprid. Tht Agency often does not mke its ssessments public nd the two documents vilble for imidcloprid (PMRA 1997, 2001) not provide ny detils. 15 Cndin Council of Ministers of the Environment. A federl/provincil entity which, mong other things, sets proposed (i.e. non-binding nd non-regultory) ction levels for concentrtions of vrious chemicls in wter in order to protect both humn helth nd the environment. 16 owever, s the min degrdtion pthwy is photolytic, this my not be sfe ssumption in ll bodies of wter; e.g. turbid ones. 41

43 Neonicotinoid Insecticides nd Birds It is pproprite to question the continued seprtion of freshwter nd mrine endpoints in ssessing qutic toxicity. Mltby et l. (2005) explored the differences between toxicity estimtes from distributions generted with dt for freshwter nd sltwter crustcens for 10 well chrcterized insecticides. No significnt differences were seen between estimtes from these hbitts. Even though sltwter species tended to be more sensitive, this ws scribed to the mkeup of tx most represented in the two hbitts rther thn ny fundmentl (toxicologiclly-driven) slt vs. freshwter difference Towrds more scientific pproch of ssessing toxicity informtion A criticl filure of existing regultory evlution protocols is tht they typiclly look t dt generted from very smll number of species. For exmple, submitted crustcen dt my be for Dphni only. By relying on single indictor species, interspecies differences in susceptibility re not dequtely ddressed nd, s rgued bove, much is left to chnce. This is especilly true in the cse of pesticides with trgeted (receptor-bsed) modes of ction, such s the neonicotinoids. For this review, we opted to consider the ever-growing body of dt from the published literture in ddition to the few species mndted by regultory uthorities. The disdvntge of using these dt is tht they my be of vrying qulity nd protocols my not be s stndrdised s those dt mndted by regultory gencies. (owever, most of these studies re published nd hve therefore gone through peer-review process which my indeed be more rigorous thn regultory scrutiny.) The dvntge is tht the published studies more fully represent the rnge of species likely to be exposed, thus providing mesure of the differences in sensitivity of qutic orgnisms t lrge. Once these dt re ssembled, the most credible wy of determining criticl toxicity endpoint is through species sensitivity distribution (see section 2 for n introduction to this topic). Species sensitivity distributions were generted seprtely for qutic insects nd crustce nd we derived C5 (hzrdous concentrtion) vlues, using the ETX 2.0 softwre (vn Vlrgingen et l. 2004). Dt were obtined from regultory documents s well s the primry literture. It ws not lwys possible to obtin the source informtion so the study detils were not lwys vilble. owever, even stndrdised tests cn show wide vritions in results. This rgues for being inclusive when it comes to test results. In ssembling dt, priority ws given to 96h test durtion, the lowest of EC50 or LC50 if both were mesured, nd technicl versus formulted mteril in tht order. Geometric mens were computed where severl eqully cceptble vlues were vilble. To derive wter qulity criteri, the U.S EPA (Stephn et l. 1985) recommended the use of EC50 mesures bsed on deth or immobiliztion 17 to better reflect the totl severe cute dverse impct of the test mteril on the test species. Snchez Byo nd Gok (2006) reported tht the effective dose (EC50 immobilistion) ws X lower thn the LC50 (true deth) with imidcloprid specificlly. They recommended tht EC50 vlues should be used in risk ssessment nd suggested tht the gp between EC50 nd LC50 might be greter with neonicotinoids thn with other clsses of pesticides. Beketov nd Liess (2008) found tht with neonicotinoids nd other neurotoxic 17 The distinction cn be difficult to mke with some orgnisms. If n orgnism is sufficiently incpcitted nd fils responding when gently prodded, it is to be clssified s ded whether or not it is cliniclly ded. 42

44 Neonicotinoid Insecticides nd Birds insecticides, drift of invertebrtes 18 ws lredy considerble t wter concentrtions 1/10 of the LC50. For resons outlined in the previous section, mrine nd freshwter species were considered together A quick note on test vribility nd repetbility There is tendency in regultory circles to become overly preoccupied with the ccurcy nd precision of ny given toxicity test vlue. This fixtion is driven by vrious fctors: risk quotients re derived from very few tests, they my need to be defended in the courts, internl gency guidelines insist on stringent test conditions nd therefore expect perfect repetbility etc. In relity, whether deling with qutic invertebrtes or wrm-blooded vertebrtes, experience shows us tht there could be significnt test-to-test vrition, even when those tests re conducted under crefully stndrdised conditions. As n exmple, Tble 7.1 illustrtes the vrious test results obtined for 48h sttic or sttic renewl cute tests with imidcloprid nd Dphni mgn, the best known nd best chrcterised qutic test species. Tble 7.1. Toxicity test results for 48h EC50 nd LC50 vlues for Dphni mgn exposed to imidcloprid. refers to technicl mteril; FORM to formulted end product. All toxicity vlues re given in ug/l of ctive substnce. Form of the.i. Mesure Toxicity (ug/l) CL LC50 10,440 6,970-17,710 Probit slope 1.86 Originl publiction Source Reference Comments Song et l Test t 27 degrees C LC50 17,360 12,510-30, Originl publiction Song et l Test t 20 degrees C FORM LC50 30,000 28,000-44,000 Originl publiction Tisler et l FORM EC50 (immobility) 43,265 34,302-53,592 LC50 56,600 34,400-77,200 Originl publiction Originl publiction LC50 64,873 Originl publiction ysk et l Tisler et l Snchez-Byo Defined s the orgnisms being sufficiently impired to detch from the substrte nd be crried downstrem by the current. The removl of qutic life from stretches of strem represents n ecologiclly undesirble effect. 43

45 Neonicotinoid Insecticides nd Birds EC50 (immobility) 85,200 75, , One liner 2004, 2007; Pesticide Mnul, EPA 2007 ssessment Young 1990 (Byer) EC50 >32,000 Agritox Byer Frnce Bsed on these dt, 10X differences within species should not be surprising. This level of vrition lso underscores the importnce of obtining multiple tests on multiple species in order to derive credible criticl toxicity threshold for environmentl protection Other fctors influencing sensitivity of orgnisms Life stge Yokoym nd collegues (2009) showed tht sensitivity could vry gretly between different lrvl instrs 19 of the sme species with younger instrs tending to be more sensitive, possibly becuse of greter surfce to mss rtios. For exmple, sensitivity of the cddis fly Cheumtopsyche brevilinet to imidcloprid dropped by fold s the lrve mtured from first to fifth instr. Interestingly, these uthors showed tht for n orgnophosphorous nd crbmte insecticide, individuls from clener urbn strems were much more sensitive thn those tken from griculturl res. This did not hold true for imidcloprid however. Technicl vs. formulted insecticide The technicl product is the pure form of pesticide synthesised by the registrnt. Becuse it is synthesized under industril conditions, its level of purity typiclly pproches 95-99%. The pesticide purchsed by the consumer contins the ctive ingredient to which hs been dded: solvents, emulsifiers, chemicls to help the droplets stick to or penetrte plnt surfces, etc. This finl (formulted) product typiclly contins 40-80% ctive ingredient but this cn sometimes be much lower. The formulnts re often clled inerts but they re often nothing of the sort toxicologiclly. There re enough comprble test dt with imidcloprid to provide comprison of technicl vs. formulted mteril (Tble 7.2). Tble 7.2. A comprison of cute toxicity vlues for technicl nd formulted imidcloprid. All vlues corrected to ug/l in ctive ingredient. Species Endpoint Vlue for technicl mteril (ug/l) Americmysis Vlue for formulted mteril (ug/l) Reference 96h LC EPA One liner bhi Dphni mgn 24h LC50 97,900 38,000 Tisler et l Dphni mgn 48h LC50 56,600 30,000 Tisler et l ylell ztec 96h LC /17.4 Stoughton et l Chironomus tentns 96h LC Stoughton et l An insect s period of postembryonic growth between molts. 44

46 Neonicotinoid Insecticides nd Birds On tht bsis, we feel justified in pooling dt from both technicl nd formulted mteril in the sme distributions (see below). Temperture Song nd collegues obtined lmost identicl vlues for 48h LC50 vlues with Aedes egypti t either 20 or 27 degrees C. This does not rgue for strong temperture-dependence s is the cse for pyrethroid insecticides for exmple. On the other hnd, Mohr nd collegues (2012) obtined more pronounced effects on n ssemblge of benthic species from imidcloprid pulses in their summer pplictions which they ttributed to higher wter tempertures. Light Becuse photolysis is the min mode of degrdtion for imidcloprid, the mount of illumintion provided during testing is expected to be criticl to the results. Becuse wter clrity is vrible in nture, the extrpoltion from lb to field will be very difficult s result. Light levels re seldom reported in the test dt. For this reson, the Dutch government (RIVM 2008) in its ssessment of imidcloprid toxicity rejected ll tests conducted in the light unless concentrtions were empiriclly verified. Snchez-Byo nd Gok (2006) found tht vlues obtined in the drk could be two-fold lower thn vlues obtined in the light. This is not tht gret difference given some of the informtion shown bove on repet testing. Therefore, we chose not to restrict dt in the sme wy. Becuse we were not s strict with the test dt, some of the studies my hve underestimted the toxicity of imidcloprid compred to wht it could be in turbid or strongly coloured wter. Seson Seson ws found to be one of the most importnt fctors ffecting the toxicity of imidcloprid to the mphipod Gmmrus roselli (Bottger et l. 2012). Depending on test conditions, the 96h EC50 vried from 1.9 to 129 ug/l. Smll hungry individuls in the spring were found to be the most sensitive nd tests mnipulted to mimic those conditions gve results tht best pproximted wht ws observed in the field Deriving C5 vlues for imidcloprid The ETx softwre ws used to determine the C5 or hzrdous concentrtion bsed on vilble cute nd chronic toxicity dt Acute dt All qutic toxicity dt re given in ppendix 1. The following tbles summrise the dt entered into the clcultion of D5 vlues. Tble 7.2. Imidcloprid. Summry of cute toxicity vlues in ug/l for crustcen species. Study Time (h) FORM Mesure Toxicity SD_ppb Txonomic_SD Ceriodphni dubi* 48 FORM LC Cypridopsis vidu 48 EC

47 Neonicotinoid Insecticides nd Birds Ilyocypris dentifer 48 EC50 3 Cyprett seurti 48 EC50 16 Gmmrus roselli 96 UNKNOWN EC50 29 Americmysis bhi 96 FORM LC50 36 ylell ztec 96 LC50 65 Gmmrus pulex 96 LC Plemonetes pugio 96 LC Ceriodphni dubi* 48 FORM EC Gmmrus fossrum 48 FORM LC Chydorus sphericus 48 EC Ceriodphni reticult 48 FORM EC Asellus quticus 48 FORM LC Dphni mgn 48 EC50/LC Dphni pulex 48 FORM EC Moin mcrocop 48 FORM EC Artemi sp. 48 LC *Both vlues for Ceriodphni were kept becuse of their wide divergence nd the pprent vlidity of both independent tests performed on different continents. The wide inter-species rnge in recorded toxicity with imidcloprid is notble. Myer nd Ellerseck (1986) looked t in-house cute toxicity tests for 82 pesticides nd chemicls. In ll test species confounded, the verge rtio between the lowest nd highest LC/EC50 ws 256X (868X for insecticides only). The highest recorded spred ws 166,000X for n insecticide. The rtio for imidcloprid vlues is greter thn 174,000X. Also remrkble is the low sensitivity of the cldocern Dphni mgn. This is the most common test species on which much of the qutic risk ssessment is usully bsed. There is evidence tht cldocer s group re insensitive to neonicotinoid insecticides (ysk et l. 2012) lthough there is n lternte study which found the cldocern Ceriodphni dubi to be mong the most sensitive species tested (Chen et l. 2009). Tble 7.3. Imidcloprid. Summry of cute toxicity vlues in ug/l for qutic insect species. FORM_SD FORM FORM FORM Txonomic_SD Study Time (Vlue) Study time (Unit) Mesure Toxicity SD_ppb Epeorus longimnus 96 h LC Chironomus dilutus 96 h EC eptgeniid myfly 96 h LC

48 Neonicotinoid Insecticides nd Birds Simulium ltigonium 96 h LC Cheumtopsyche brevilinet 48 h LC Chironomus tentns 96 h LC Simulium vitttum 48 h LC Betis rhodni 48 h LC FORM Chironomus riprius 96 h EC Aedes teniorhynchus 48 h LC50 13 Aedes egypti 48 h LC50 44 A species sensitivity distribution bsed on the normlly distributed cute dt returns n C5 of 1.01 ug/l for crustce ( ) nd n lmost identicl 1.02 ug/l for qutic insects ( ). Despite the overlp, the insects pper to hve much lower sensitivity vrince i.e. more similrity in response. A pulse of imidcloprid in the ug/l rnge would therefore be expected to ffect lrger proportion of the insect community. Drgonfly on whet by Jim Occi, BugPics, Bugwood.org The following figure illustrtes the species sensitivity distribution for imidcloprid nd crustcen species. 47

49 Neonicotinoid Insecticides nd Birds For the combined dtset of qutic insects nd crustce, the clculted C5 is 0.22 ( ). owever, the dt do not fulfill the condition of normlity; forcing norml distribution 20 my not be the best wy to proceed. Using slightly different methods which involve collpsing dt within gener before pplying species sensitivity distribution, Ngi nd collegues (2012) rrived t similr vlue with n C5 of 0.43 ug/l Chronic dt There re enough chronic toxicity dt for imidcloprid to run species sensitivity distribution (Tble 7.4). Although they ddress slightly different endpoints, most del with survivl nd reproduction over dy period. The C5 for NOEC vlues is clculted to be ( ). Tble 7.4. Imidcloprid. Avilble chronic dt for qutic invertebrte species. Form of the pesticide Txon Species Study Time (d) Exposure type* Mesure Vlue ug/l Source Reference Crustce Mysidopsis bhi 28 EC50 (body length) 0.3 Stoughton et l Cox 2001 nd Felsot & Ruppert A norml distribution is continuous probbility density function symmetricl round men of 0 nd with stndrd devition of 1. It is the stndrd bell curve often used to chrcterise vrible subject to rndom influences. 48

50 Neonicotinoid Insecticides nd Birds Crustce Americmysis bhi microcosm Chironomide nd Btide Insect Chironomus tentns Insect Chironomus riprius NOEC (growth nd survivl) 0.6 EPA 2007 ssessment S, S NOEC 0.6 EFSA 2008 Scientific report 28 EC50 (emergence) 28 S EC50 (emergence) 0.91 Originl publiction 3.11 EFSA 2008 Scientific report FORM Crustce ylell ztec 28 SR LC Originl publiction Crustce Gmmrus pulex Crustce Dphni mgn 28 S NOEC (swimming behvior) 64 Drft ssessment report from Germny (Rpporteur Stte) SR NOEC (repro) 1800 EPA 2007 ssessment EFSA 2008 Scientific Report Wrd 1990 (Byer) Stoughton et l Stoughton et l Young 1990 (Byer) * S = Sttic; SR = Sttic with renewl; S,S = 2 pplictions t 21 d intervl. Another wy to pproch the problem is to consider the cute-chronic rtio for the compound nd pply this to the pproprite cute toxicity endpoint. This is scientificlly much more credible thn ccepting chronic toxicity endpoint tht is much higher thn most cute toxicity endpoints merely becuse it ws determined for species tht hppened to be insensitive. There re four species for which we cn derive n cute-chronic rtio. This rtio is lower in the crustce in ylell nd 5.5 in Gmmrus but much higher in the two Chironomus species studied to dte 17.7 nd The ltter vlues, pplied to the most sensitive insect species tested to dte (Epeorus) would return chronic toxicity vlue of ug/l (using fctor of 75.8) to ug/l (using fctor of 17.7). It is cler tht more credible considertion of ll the species toxicity informtion collected to dte suggests tht the toxicity of imidcloprid to qutic invertebrtes hs been gretly underestimted by EPA (summry in tbles 7.5 nd 7.6). Effects on qutic invertebrtes re likely to be substntil indeed t sub ppb levels of wter contmintion. Snchez-Byo nd Gok (2006) reported tht, in rice mesocosms, ll zooplnkton species were eliminted s long s wter concentrtions remined bove 1 ug/l. Tble 7.5. A summry of reference concentrtions (in chronologicl order) for cute (pek) exposure of imidcloprid in freshwter environments. Source Reference level ginst which exposure concentrtions re to be Justifiction 49

51 Neonicotinoid Insecticides nd Birds compred for freshwter environments (ug/l) EPA (2007) (US) 35 Lowest of three tests exmined to which fctor of 2 hs been pplied in keeping with the 0.5 LOC (Level of Concern) for risk quotient EFSA (2008) (Europe) 0.55 Lower of two species tested to which fctor of 100 hs been pplied in keeping with Annex VI triggers for the Toxicity/Exposure Rtio. RIVM (2008) (Netherlnds non regultory) 0.2 Mximum cceptble concentrtion from short term exposure or exposure peks bsed on mesocosm study nd 3X sfety fctor Ngi et l C5 but with SSD methodology which combines species within the sme genus lso with 50% confidence 35 Aqutic life benchmrk presumbly sme methodology s regultory review EPA (2012)* (US non regultory) This report 1.01 C5 (with 50% confidence) for cute exposure in crustce This report 1.02 C5 (with 50% confidence) for cute exposure in insects This report 0.22 C5 (with 50% confidence) for cute exposure in ll qutic invertebrtes (ignoring lck of normlity) * tm. Accessed December Tble 7.6. A summry of criticl toxicity levels for qutic invertebrtes exposed to chronic (3-4 week) exposures to imidcloprid. Source Reference level ginst Justifiction which verged exposure concentrtions re to be compred for freshwter environments (ug/l) EPA (2007) (US) 0.5 Obtined with n cute/chronic rtio nd pplying fctor of 2 for the usul LOC. (Using the usul chronic NOAEC for Dphni would hve CCME (2007) (Cnd non regultory) EFSA (2008) (Europe) RIVM (2008) (Netherlnds non regultory) EPA (2012)* (US ment ccepting vlue of 800 much higher thn the cute vlue) 0.23 EC15 for the most sensitive of two freshwter species tested chroniclly to which fctor of 10 hs been pplied NOEC from microcosm study (sme study used for deriving n cute criterion in the Netherlnds) to which 1-3 sfety fctor hs been pplied bsed on expert delibertions Mximum permissible concentrtion for long term exposure derived from lowest NOAEC vlue nd fctor of 10. This replces n older vlue of ug/l Aqutic life benchmrk methodology uncertin non regultory) This report Distribution nlysis of NOECs for chronic studies on 7 single species nd one species ssemblge. This report The higher of two empiriclly-determined cute-chronic rtios for insects pplied to the most sensitive insect species of 8 tested to dte * tm. Accessed December

52 Neonicotinoid Insecticides nd Birds Bsed on our ssessment s well s tht of vrious jurisdictions round the world, it is cler tht the US EPA hs underestimted the toxicity of imidcloprid to qutic invertebrtes by over n order of mgnitude. Severe impcts to qutic environments re expected from short term (pulse) exposures s low s 0.2 ug/l (ppb) nd chronic exposures to concentrtions t lest 10 times lower Deriving criticl wter concentrtions with other neonicotinoid insecticides Only two other neonicotinoid insecticides hve sufficient mount of dt to fit to distribution (nnex 1) but then only by pooling ll invertebrtes (crustce nd insect). Tbles 7.7 nd 7.8 provide the dt entered into ETx to derive n C5 vlue. Thimethoxm is t the limit of credibility given the smll smple size nd the fct tht one of the vlues is limit vlue. Nevertheless, we believe tht this is more resonble pproch thn simply bsing criticl concentrtion on one or two stndrd species s is currently the cse (especilly when the min test species is known to be insensitive). Tble 7.7. Thimethoxm cute toxicity dt for qutic invertebrtes. = technicl mteril. See nnex 1 for detils. Txon Species Study Time (h) Form Mesure Toxicity (ug/l) Crustce Dphni mgn 48 EC50 >106000* Crustce Crustce Choborus sp. Americmysis bhi 48 EC EC Insect Cloeon sp. 48 EC50 14 Insect Chironomus riprius 96(?) EC50 35 * Vlue entered s such regrdless of > Tble 7.8. Thicloprid cute toxicity dt for qutic invertebrtes. FORM = formulted mteril; ANALYTICAL = nlyticl grde mteril. See nnex 1 for detils. Txon Species Study Time (h) Form Mesure Toxicity (ug/l) Crustce Dphni mgn 24 FORM LC Crustce Asellus 24 FORM LC quticus Crustce Gmmrus 24 FORM LC

53 Neonicotinoid Insecticides nd Birds Insect pulex Sympetrum strioltum 24 FORM LC Insect Notidobi 24 FORM LC ciliris Insect Simulium 24 FORM LC ltigonium Insect Culex pipiens 24 FORM LC Crustce Gmmrus 96 ANALYTICAL LC pulex Insect Betis rhodni 96 ANALYTICAL LC C5 (with 50% confidence) vlues re estimted s 0.74 nd 0.80 ug/l for thimethoxm nd thicloprid respectively. With their own dt (7 species tested), Beketov nd Liess (2008b) hd determined n C5 vlue of 0.72 ug/l. Given the smll number of species tested, this certinly plces these compounds in the sme generl rnge s imidcloprid. Rther thn ttempt to derive unique vlues for the other compounds tht re bsed on very little dt, we propose comprtive pproch; i.e. how do the vrious neonicotinoids compre to imidcloprid where comprble dt exist. Tble 7.9 provides dt where species, formultion nd test durtion were resonble mtch. Tble 7.9. Comprison of neonicotinoid cute toxicity to qutic invertebrtes. Crustce in norml type, insect species re in bold. All dt derived with technicl mteril unless otherwise stted. All times s indicted in tble unless otherwise specified. IMI = Imidcloprid, ACE = Acetmiprid, TC = Thicloprid, CLO = Clothinidin, TM = Thimethoxm, DIN = Dinotefurn. Species Stud y Tim e (h) Endpoint IMI (ug/l) ACE (ug/l) TC (ug/l) CLO (ug/l) TM (ug/l) DIN (ug/l) Dphni mgn Americmysi s bhi Gmmrus pulex Asellus quticus ylell ztec Chironomus riprius Simulium ltigonium 48 EC50 35,539 49,800 43, ,523 >106, LC LC LC * 153* ** 96 LC EC50 20* LC * ** 1,000,000 52

54 Neonicotinoid Insecticides nd Birds Betis rhodni 48 LC *** * formulted ** 24h *** 96h The tble highlights more similrities thn differences between the ctive ingredients. Wheres clothinidin nd thimethoxm pper t first blush to be less toxic to crustce, the Chironomus dt suggest tht they re eqully toxic to nontrget qutic insects. Acetmiprid nd thicloprid pper to be very similr to imidcloprid. There isn t enough informtion for dinotefurn to sy one wy or the other. From the point of view of protecting qutic communities, we suggest tht the criticl vlues derived in section 7.3 for the protection of qutic ecosystems ginst imidcloprid could esily pply to ll other neonicotinoids. Indeed, becuse of the similrity in mode of ction, we suggest tht the criticl concentrtion vlues derived for imidcloprid should be pplied to the sum of ll neonicotinoid residues. We believe tht the bove is more credible pproch thn relying on few berrnt dt points s the EPA hs done repetedly. For exmple, in their 2003 ssessment of clothinidin for corn nd cnol seed tretments (US EPA 2003) the gency used n NOAEC of 42 ug/l bsed on the chronic life cycle test in dphni for the protection of fresh wter environments. This is despite the fct tht by the time of the 2003 review, Dphni hd been shown to be comprtively insensitive to both imidcloprid nd clothinidin; we now know this insensitivity extends to ll neonicotinoids. The 42 ug/l vlue for chronic exposure retined by EPA in 2003 is ctully higher thn the 22 ug/l vlue tht ws retined for cute effects. If nothing else, chronic reference level tht is twice s high s the cute reference level in the sme receiving wters should hve rung few lrm bells. Once gin, this leds one to conclude tht EPA s pproch to the ssessment of qutic risk is scientificlly unsound nd plces qutic environments t risk. In the Netherlnds, Vn Dijk (2010) reports tht chronic reference vlues were set independently by the government for ech of the neonicotinoids: ug/l for thicloprid, 1 ug/l for thimethoxm, 14 ug/l for clothinidin nd, the older vlue of ug/l for imidcloprid set in 2007 but reviewed upwrds in 2008 (tble 7.6). We question whether the dt re sufficient to scribe different qutic toxicity to ech of these ctive ingredients Degrdtes or metbolites Most of the neonicotinoid insecticides hve complex degrdtion pthwys in soil or in receiving wters. There re few cses where this degrdtion needs to be tken into ccount when ssessing the full toxicity of the ctive ingredient in the environment. The most obvious exmple is the production of clothinidin s mjor degrdtion product of thimethoxm. The higher qutic toxicity of the TZNG metbolite of clothinidin lso needs to be considered 21 s well s tht of the NOA metbolite of thimethoxm (Annex 1). Even when of equl or lesser toxicity thn the prent mteril, metbolites must be considered becuse they my prolong the toxicity profile of the insecticide. 21 Acute toxicity to Dphni mgn is given s 640 ug/l reltive to pprox. 110,000 ug/l for the prent mteril. 53

55 Neonicotinoid Insecticides nd Birds 7.5. Concerns tht stndrd pproches to risk ssessment re not dequte for neonicotinoid insecticides. As seen bove, the US EPA nd, to lesser extent, other regultory bodies hve grossly underestimted the toxicity of neonicotinoids to qutic environments. Criticl concentrtions t which effects re expected re much lower thn currently ssumed by regultors. owever, there is even more reson to be concerned bout these compounds in the qutic environment. Snchez-Byo nd Gok (2007) nd Snchez-Byo (2009) rgued, s hve some before them 22 tht the conventionl method of ssessing toxicity t fixed exposure times mkes it difficult to extrpolte to exposures of different durtion whether shorter pulse exposures or prolonged exposures resulting from compound persistence. Using imidcloprid specificlly, Snchez-Byo showed tht 48h LC50 of 390 ug/l for the ostrcod Cypridopsis dropped 100 fold to 4 ug/l fter 5 dy exposure period. This time dependence is not unique to neonicotinoids. owever, the more toxicity is shown to be function of time (keeping concentrtion equl), the more it cn be rgued tht the compound is hving n irreversible mode of ction. This rgument ws mde by Tennekes (2010) who likened the toxicity of neonicotinoid insecticides to one hit model of chemicl crcinogenesis. Tennekes went on to describe how neonicotinoids closely follow ber s rule which sttes tht the product of exposure concentrtion nd durtion is constnt. In theory, this mens tht n infinitesimlly smll dose cn result in toxic effect provided durtion of exposure is sufficient. e rgued tht the toxicity of neonicotinoids to both bees nd qutic orgnisms showed this chrcteristic. These insecticides bind lmost irreversibly to invertebrte cholinergic receptors which incidentlly mkes them very powerful insecticides nd helps explin why their use hs incresed so drmticlly over time. Despite Byer Corportion s protesttions tht the mode of ction of imidcloprid is not irreversible (Mus nd Nuen 2011), Tennekes (2011) counter-rgued successfully tht evidence to dte shows otherwise (despite minor devitions, the insecticide is dngerously close to showing irreversible ctivity) nd even used some of Byer Corportions erlier reports on imidcloprid s mode of ction to mke his point. Of course, wht is of interest is the internl (i.e. t the receptor level) exposure rther thn the externl (i.e. test medium) exposure. Possibly the most troublesome piece of evidence on neonicotinoid insecticides to dte is tht of Beketov nd Liess (2008b) studying the toxicity of thicloprid to severl qutic invertebrte species. Wht they reported is tht the pprent LC50 to vrious test species dropped drmticlly merely by extending the post-exposure observtion period. The most extreme exmple of delyed mortlity ws for Gmmrus pulex where the clculted LC50 ws 50X lower fter observing the exposed individuls for 17d even though exposure in ll cses ws for 24h only. Similrly, Stoughton et l. (2008) compred 96h pulse of imidcloprid with prolonged observtion period in clen wter with continuous 28d exposure. The 96h pulse ws intended to mimic relistic runoff scenrio. The clculted NOAEC ws identicl under both exposure scenrios in one of the two species tested (the mphipod yell ztec); continuous exposure proved more dmging for the midge Chriromus tentns. These types of observtion do lend credence to Tennekes s comment on irreversibility of ction nd increse our concern with exposure to the neonicotinoids even if those re pulse exposures. There 22 These uthors provide good review of time-dependent pproches to toxicity estimtion nd references going bck to the 1930s. 54

56 Neonicotinoid Insecticides nd Birds hs been t lest nother effort to look t the effect of pulsed neonicotinoid exposure. Mohr nd collegues (2012) exposed strem mesocosms to weekly imidcloprid pulses of 12 ug/l. The most sensitive species in the system ws ffected following the first pulse wheres effects on other tx were more grdul nd incresingly evident fter 2 or 3 pulses. Pond mesocosms hve effect levels tht re much lower thn this but the uthors rgued tht effect concentrtions re not tht dissimilr once time weighted concentrtion pproch is used in the cse of the pulse exposure. Tennekes nd Snchez-Byo finlly collborted in 2011 to reiterte the points mde bove nd rgued tht neonicotinoids re fr more dngerous thn other insecticides of higher toxicity. This is key point becuse the neonicotinoids hve replced insecticides (such s synthetic pyrethroids) of very high qutic toxicity (see section ) A quick comprison of the toxicity of neonicotinoids nd older insecticides to qutic ecosystems Whiteside nd collegues (2008) compred the toxicity of ll insecticides registered t the time in Cnd to qutic environments. They rn ll products through simplified runoff model ssuming mximum lbel rtes nd stndrd ppliction scenrio, nd ssessed the cute risk of registered products to fish, crustce, insects nd plnts through weighted community score. They weighted fish more hevily thn invertebrtes nd invertebrtes more hevily thn lge reflecting the ese with which these ecosystem components could be replced if lost. Becuse the toxicity of neonicotinoids to fish is quite low compred to either pyrethroid or orgnophosphorous insecticides, the neonicotinoids fred quite well when compred to number of older insecticides they hve replced (Tble 7.10). Tble Comprison of qutic toxicity nd reltive qutic community risk (fter Whiteside et l. 2008) of neonicotinoid insecticides nd severl of the insecticides they hve replced. Active ingredient Fish C5 Crustce C5 Aqutic insect C5 tefluthrin dimethote methmidophos dizinon chlorpyrifos crbofurn terbufos deltmethrin imidcloprid (1.01*) 1.40 (1.02*) 4.4 mlthion methomyl cetmiprid clothinidin crbthiin thimethoxm thicloprid NA * Updted vlue bsed on this report Weighted community risk score 55

57 Neonicotinoid Insecticides nd Birds Agin, this comprison my be misleding if the chronic risk of neonicotinoids is different, whether for resons invoked by Tennekes nd Snchez-Byo bove or becuse of exposure chrcteristics. Exposure will be reviewed briefly below. Cre must therefore be exercised before concluding (s hve some uthors e.g. Brbee nd Stout 2009) tht the neonicotinoids re n improvement over older clsses of insecticides. Wheres neonicotinoids re clerly less cutely toxic to fish thn mny other insecticides, we might expect fish to be ffected indirectly though efficient nd prolonged removl of qutic invertebrtes Sublethl nd delyed effects of neonicotinoids All pesticides hve the potentil to cuse effects t doses tht re not immeditely lethl. owever, there is some evidence tht neonicotinoids re more of n issue here thn other registered pesticides. The issue of disorienttion of honeybees t extremely low exposure levels suggests tht their mode of ction (i.e. the qusi-irreversible binding of neonicotinic synpses) cuses behviourl effects. Alexnder et l. (2007) showed tht short (12h) exposure pulses of 1 ug/l nd higher cused feeding inhibition in myflies. Even pulse exposures s low s 0.1 ug/l ffected the size of the dults t emergence (Alexnder et l. 2008). Englert nd collegues found tht predtor-prey interctions nd lef litter brekdown were ffected t concentrtions of thicloprid between 0.5 nd 1 ug/l in simple lbortory ecosystem. Pestno et l. (2009) found effects on respirtion in chironomids n order of mgnitude below lethl levels Will exposure levels be high enough to cuse problems in qutic environments? The regultory view In its erliest review of imidcloprid (USEPA 1994b), the Agency reviewers lredy hd concluded tht the chemicl s mobility, solubility nd persistence were concern for groundwter contmintion nd qutic systems. This concern ws echoed in most if not ll reviews crried out since tht time; e.g. EFED hs concluded tht the vilble dt on imidcloprid shows tht the compound is mobile nd persistent, hs potentil to lech to ground wter, nd lso presents concerns for trnsport to surfce wter vi runoff. In ddition to the persistence issue, EFED lso hs concern for imidcloprid residul crry-over to other crops fter the previous yer s ppliction. (USEPA 2007) In Cnd, imidcloprid ws first registered in 1995 lthough number of dt gps existed t the time. The PMRA updted its review in 2001 (PMRA 2001). Their review determined tht imidcloprid is clssified s persistent under griculturl field crop conditions ccording to the clssifiction scheme of Goring et l. (1975), with DT50 in soil in the order of 1-2 yers. They went on to compre imidcloprid to trzine, problemtic well known qutic contminnt, the ltter hving much shorter officil DT50 of 120 dys. The PMRA lso cknowledged the high probbility of both surfce nd groundwter contmintion with imidcloprid. Given some of the dt presented below, it ppers tht regultory gencies in Cnd, the US, nd EU were bsolutely correct in their erly ssessment. Yet they proceeded to llow multitude of lbeled registrtions under vried gronomic conditions. In 2001, the PMRA stted tht they were willing to entertin lbel extensions provided these new uses were in low environmentl risk situtions or criticl need uses in the context of sustinble pest mngement progrms nd where 56

58 Neonicotinoid Insecticides nd Birds mitigtive mesures cn be incorported into product lbelling. Unfortuntely, imidcloprid is still registered for wide rnge of field, horticulturl nd orchrd crops. In their ltest re-evlution of imidcloprid (EFSA 2008), Europen Regultors ppered to be trying to bend over bckwrds to mke the compound pss their qutic triggers. Even fter the ppliction of drconin mitigtion steps in the wter modeling work (e.g. reducing drift by 95%) they were unble to mke common uses of the insecticide (e.g. tomtoes) not trigger their criteri for concern. As discussed bove, the sitution would be worse still if they dopted more relistic toxicity reference levels. The sitution is lrgely repeted with clothinidin, nd to lesser extent thimethoxm (see section 1). Regultors fully expected these compounds to hve n impct on the qutic environment Empiricl dt to dte A review of dt on groundwter contmintion is beyond our scope; however, s of 1997, Byer ws lredy reporting concentrtions of imidcloprid s high s 1 ug/l in Cliforni groundwter (Bcey 2003). USEPA (2008) reported detections rnging from 0.2 to 7 ug/l in New York Stte. In Quebec, smples from wells in potto-growing res were reporting levels s high s 6.4 ug/l nd detections in 35% of 28 wells smpled (Giroux 2003). Detection of three imidcloprid metbolites ws lso reported. Dt re sprser nd just emerging with the other neonicotinoids. useth nd Groves (2013) reported contmintion with thimethoxm in Wisconsin wells in 2008 nd The levels rnged s high s 9 ug/l with severl wells hving vlues bove 1 ug/l. These re levels t which we would expect cute effects on qutic invertebrtes -- this my be totlly unprecedented in the history of pesticide registrtion to hve groundwter smples show such high biologicl ctivity to qutic systems. There isn t much empiricl dt for surfce wter monitoring for the neonicotinoids. The most comprehensive effort is the recently published dt by Strner nd Goh (2012) who reported on imidcloprid lone in three irrigted griculturl regions of Cliforni (Imperil Vlley, Slins nd Snt Mri). They smpled 23 rivers, smll creeks or drins. The dt re reproduced below (Tble 7.11) by smpling site (the originl publiction listed residues by dte). Bsed on crops grown in the res, the uthors believe tht most of the contmintion is from the production of lettuce nd, to lesser extent, cole crops nd wine grpes. Tble Imidcloprid wter monitoring results from griculturl wtersheds in Cliforni (Strner nd Goh 2012). Dte Site Time Imidcloprid conc. (ug/l) My :45: June :45: April :45: June :00: Mx. for site (ug/l) July :15: My :30:

59 Neonicotinoid Insecticides nd Birds June :30: April :15: My :10: June :45: July :00: August :00: April :30:00 ND ND October :00: October :00: My :50: June :45: April :45: My :30: June :00: August :15: April :15: June :30: July :20: August :15: October :30: October :45: October :30: October :00: October :45: October :15: October :20: October :15: October :45: October :25: October :40: October :00:00 ND ND April :00:00 ND ND My :50:00 ND April :30:00 ND My :30: June :45:00 ND July :20:00 ND August :45:00 ND 0.05 June :40: My :45: June :30: April :30: My :00:

60 Neonicotinoid Insecticides nd Birds June :00: June :15: July :20: August :15: My :00: June :00: April :00: My :45: June :20: July :55: August :30: June :15: August :45: June :00: August :00: June :40: June :15: June :15: My :45: My :45: My :45: My :45: My :15: August :10: August :30: August :20: Most of the smples re bove ny resonbly set reference level for cute effects nd t lest n order of mgnitude higher thn chronic effect level (see tbles 7.5 nd 7.6). Yet, most remrkble is the fct tht on sites where multiple smples were tken, concentrtions remin consistently high nd often bove cute impct levels throughout the entire seson. ving rerrnged the dt by site mkes this esy to see (Tble 7.11). This is exctly wht we would expect from compound either used repetedly throughout the growing period or compound with very high persistence being grdully relesed to the qutic environment fter ny rin or irrigtion period. It is notble tht grb smples such s these never revel true mxim (by chnce lone, how could grb smple find the mximum?) so the sitution (lredy looking very blek) is worse thn depicted. As the uthors point out, true picture would require tht other neonicotinoids s well s the mny imidcloprid degrdtes be mesured s well. ldik nd Clhoun (2012), in methods-oriented report for the USGS, provide dt on two Georgi strems: Scope creek nd the Chtthoochee River smpled between October 2011 nd April A full interprettion of the results will be given in lter publiction for this ongoing smpling effort, but Scope creek ws described s being primrily urbn. On this site, imidcloprid ws detected in 86% of the smples t concentrtions rnging from 4.5 (essentilly the detection limit) to 59

61 Neonicotinoid Insecticides nd Birds 35.3 ng/l. The Chtthoochee River drins much lrger re of mixed forest, urbn nd griculturl res. Imidcloprid ws detected in 60% of the smples t concentrtions rnging from 3.4 to 10.1 ng/l. The other neonicotinoid insecticides cetmiprid, clothinidin, thicloprid nd thimethoxm were not detected t detection limits rnging from 3.6 to 6 ng/l. An erlier effort ( ) to smple imidcloprid in drinking wter supplies (Smith 2011) hd reveled tht imidcloprid ws one of the more frequently detected pesticides from the obbs nd Stony Brook bsins in Msschusetts. Most smples were composites tken during storm flow. One of the 5 smpling sttions on the reservoir tributries recorded imidcloprid in ll of the bse flow smples nd in 83% of the storm flow smples (detection limit of 0.06 ug/l) with mximum detected level estimted to be 1.21 ug/l. These lst two smpling efforts highlight the fct tht, becuse of the use of imidcloprid on turf nd ornmentls, we cnnot discount urbn res s sources of qutic contmintion. In its review of imidcloprid in Cnd, the CCME (2007) reported the results of erly monitoring efforts by Environment Cnd to ssess runoff from potto fields in Estern Cnd (Tble 7.12). These results were inconsistent, with erly detections reching s high s 11.9 ug/l but lter smples showing either lower or no residues. Detection limits were often high, however, mening tht the frequency of detection ws consistently underestimted. Tble Summry of erly smpling for imidcloprid by Environment Cnd in runoff nd surfce wters in proximity to potto fields. Bsed on unpublished reports reviewed by CCME Loction Yer Type of smple No. smples Detection limit (ug/l) No. positive ighest level detected (ug/l) Source cited in CCME (2007) Prince Edwrd Islnd Runoff Denning 2004 Prince Edwrd Islnd New Brunswick 2004 Nov scoti Prince Edwrd 2005 Islnd Nov scoti New Brunswick 2005 New Brunswick 2005 Runoff Murphy nd Mutch 2005 Runoff Murphy nd Mutch 2005 Runoff Murphy nd Mutch 2005 Surfce wters Murphy et l. (strem) 2006 Surfce wters (strem) Surfce wters (strem) Runoff nd surfce wter single site Murphy et l Murphy et l ewitt 2006 The first effort to look for wider suite of neonicotinoids in Cnd ws in the Fll (October 4-15) of For seed tretment uses, this would be 5-6 months fter ppliction. Single smples were 60

62 Neonicotinoid Insecticides nd Birds tken from strems in southern Ontrio drining either urbn or rurl res, the ltter being either orchrd-dominted or field-crop dominted. The dt re summrised in Tble oneybees by Jessic Lwrence, Eurofins Agroscience Services, Bugwood.org 23 We re indebted to the following individuls for use of their unpublished dt: John Struger nd John Krft, Environment Cnd Wter Qulity Monitoring nd Surveillnce (WQM&S) Ontrio; nd Josey Grbuski, Steve Cgmpn nd Ed Sverko, Environment Cnd Ntionl Lbortory for Environmentl Testing (NLET) Burlington. 61

63 Neonicotinoid Insecticides nd Birds Tble Environment Cnd surveillnce dt for neonicotinoid insecticides; Fll Minimum Detection Limit (ng/l) URBAN OR TURF SITES tylor 4-11 indin 5-11 highlnd 5-11 credit 5-11 mimico 5-11 spencer 4-11 kossuth 5-11 Anlytes ng/l ng/l ng/l ng/l ng/l ng/l ng/l ng/l clothinidin 1.76 nd nd nd nd nd <MDL <MDL nd thicloprid 0.49 nd nd nd nd nd nd nd nd thimethoxm 1.39 nd nd nd nd nd <MDL <MDL nd imidcloprid <MDL 1.66 nd nd dinotefurn 3.28 nd nd nd nd nd nd nd nd TOTAL indin Minimum Detection Limit (ng/l) ROW CROPS POTATOES PRIMARILY nottbxter nott- SR VINES AND ORCARDS wellnd biley westbrk 4-11 LThmes 5-11 LGrnd 5-11 innisfil Anlytes ng/l ng/l ng/l ng/l ng/l ng/l ng/l ng/l ng/l clothinidin nd nd <MDL nd 34.8 thicloprid 0.49 nd nd <MDL nd nd nd nd nd 3.49 thimethoxm nd <MDL imidcloprid 1.28 nd 26.9 nd dinotefurn 3.28 nd nd nd nd nd nd nd nd nd TOTAL vinelnd

64 Neonicotinoid Insecticides nd Birds Although the highest reported vlue (0.23 ug/l totl neonicotinoids) from row crop site is much lower thn imidcloprid concentrtions reported by Strner nd Goh (2012) for Cliforni, we need to remember tht these vlues represent wter concentrtions 5-6 months fter use, t lest in the cse of the thimethoxm seed tretment likely responsible for the highest level recorded downstrem from the Ontrio corn/soy field. This clerly puts us into the concentrtion rnge where chronic effects re likely. Wter collections were extended to the full summer in 2012 (J. Struger, pers. comm.) but these dt re not yet vilble. It is interesting to see tht detected residues follow predicted use ptterns: urbn nd turf sites showing primrily imidcloprid; griculturl sites showing mixture of the three min products. useth nd Groves (2013) nlysed lechte smples (collected t depth of 75 cm) following the use of thimethoxm. The insecticides hd been pplied to potto seed pieces before plnting or pplied s folir spry fterwrds. For one of the two yers of the study, lechte concentrtions verged between ug/l regrdless of ppliction method; in the following yer they verged pproximtely 5 ug/l. The most worrisome nlysis is tht of Vn Dijk (2010) for the Netherlnds. Bsed on ntionl monitoring dt for wter nlyses from 1998 to 2007, she reports tht imidcloprid ws detected s high s 325 ug/l 24 with the bulk of detections flling between nd 1.6 ug/l 25. She ws ble to mtch these monitoring dt to qutic invertebrte species bundnce dt (nother ntionl monitoring scheme in the Netherlnds). She ws ble to see cler inverse reltionship between imidcloprid residues nd the bundnce of dipter. Nonsignificnt differences were lso seen in coleoptern, mphipod nd odont. To be fir, few positive reltionships were lso seen (especilly hydrcrin), suggesting tht some species might be more ffected thn others nd tht imidcloprid my be ffecting the reltive competing bility of different tx. This is well known from mesocosm work where insensitive tx cn exhibit lrge increses s result of relese from competition or predtion. Unfortuntely, Vn Dijk (2010) could not ssess whether neonicotinoids hd resulted in temporl chnges in invertebrte bundnce over the decdes of use becuse, even in the Netherlnds, the historicl dt proved indequte to the tsk. The specil cse of pririe potholes 24 This is bsed on the uthor reporting tht the highest concentrtion detected ws 25,000 times the older Dutch reference vlue of 13 ng/l. 25 In the Netherlnds, mjor uses of imidcloprid include flower bulbs lrge industry in tht country s well s pottoes nd chicory. 63

65 Neonicotinoid Insecticides nd Birds The cse hs long been mde tht pesticide ppliction to, or runoff into, smll pririe wetlnds (sloughs) could hve disstrous consequences on wterfowl s well s other qutic bird species tht depend on the rich supply of invertebrtes for egg production s well s chick growth nd development (Mineu et l. 1987; Sheehn et l. 1987, 1995). The griculturl res of the priries re criticl to North Americn wterfowl popultions. Euliss nd Mushet (1999) smpled wetlnds in croplnd nd grsslnd in North Dkot nd confirmed tht wetlnds in croplnd res were much more likely to be devoid of cldocer nd hve reduced numbers of key invertebrte species recognised s wterfowl food. Morrissey nd Min (2010) concluded tht the highest intensity of neonicotinoid use in the Cndin priries overlps directly with res of high wetlnd density. Sediment nd mcroinvertebrte collections s well s tree swllow nest box study re underwy. In June of 2012, they lso smpled number of wetlnds. In ll, 63% of their smples were positive, with the following mxim being reported: imidcloprid 0.19 ug/l, thimethoxm 1.1 ug/l, clothinidin 2.3 ug/l, cetmiprid ug/l 26. Seed tretments in cnol were the principl sources. 8. Putting it together: Next steps 8.1. Priority reserch directions A rigorous nlysis of vin trends in North Americ, nd ttempts to link these to neonicotinoid uses, is beyond wht we cn ccomplish in this review. As discussed in section 3, vin declines re likely to be multi-fceted nd respond to mny fctors, both here nd on their wintering grounds. The nlysis will not be simple. As discussed more fully in the section below, we believe tht it is essentil to design biochemicl ssys tht will llow dignosis of poisonings in wildlife. It is lso criticl to ssess the potentil of neonicotinoids to ffect vin reproduction given the lbortory evidence to dte. The hypothesis tht neonicotinoid exposure might result in incresed vulnerbility of wildlife to pthogens deserves further investigtion, s well. It is cler tht we re witnessing contmintion of the qutic environment t levels tht will ffect qutic food chins. This hs cler potentil to ffect consumers of those qutic resources, be they birds, fish or mphibins. Bsed on this review, few priority venues of reserch re indicted: For popultion trend nlyses, we recommend expnding the ssessment from frmlnd/grsslnd species (the usul plce where reserchers strt looking for pesticide impcts) to those species known to be more relint 26 We re indebted to Dr. Christy Morrissey nd her reserch tem t the University of Ssktchewn for these erly (preliminry) results. 64

66 Neonicotinoid Insecticides nd Birds on the qutic or emergent insect food supply even if further from croplnd. The cse of pririe potholes ws mentioned bove. Becuse these re sttic wter bodies often surrounded by field crops, they re the idel testing ground for looking t qutic impcts resulting from the use of neonicotinoids in cerel nd oilseed crops. Aeril insectivores, s group, re currently experiencing widespred popultion declines. Their dependence on emergent insects is well known; seeing whether popultion declines cn be linked to the incresed contmintion of qutic systems with neonicotinoids my be worthwhile direction, especilly in light of the existing work linking poor reproductive success in some species with prey reduction following mosquito control opertions. Any nlysis will need to refer to pesticide use sttistics. This will be difficult to crry out in Cnd becuse these dt re not collected. owever, some simplifying ssumptions cn be mde s to the incresing populrity of the neonicotinoid seed tretments since their introduction in the erly 2000s. For USbsed nlyses, informtion on pesticide use does llow for enquiries into the role of pesticides in bird declines (Mineu end Whiteside, 2013). owever, we do not believe current USDA pesticide surveys cover seed tretment chemicls if pplied to the seed by commercil seed tretment opertions. This is serious knowledge gp Needed chnges to the regultory system This review hs shown how current regultory procedures re inconsistent, scientificlly outmoded, nd prone to the vgries of chnce. There is significnt disconnect between the red flgs rised by scientists who evlute the neonicotinoid ingredients nd the risk mngers who pprove the neonicotinoid product registrtions. This problem hs been rised previously in the context of the lethl impct of insecticides to birds (Mineu, 2004). Simply put, EPA hs not been heeding the wrnings of its own toxicologists. Internl Agency reviews voice mjor concerns bout neonicotinoid risks, prticulrly with respect to developmentl nd reproductive toxicity. Their officil cutions would be even more dire if EPA scientists went beyond their ntiquted protocols nd correctly ssessed the full extent of the impcts. For exmple, risk 65

67 Neonicotinoid Insecticides nd Birds ssessment methods for birds fil to fully ccount for the interspecies vrition in toxicity, underestimting cute risk by up to 10 fold for the universe of species beyond mllrds nd bobwhites. As for qutic invertebrtes, EPA hs underestimted the toxicity of imidcloprid by over n order of mgnitude, becuse of the Agency s filure to consider dt from the peer-reviewed literture. The Agency hs grossly underestimted the toxicity of the other neonicotinoids s well, in prt due to the Agency s relince on test species, Dphni mgn, tht is uniquely insensitive to neonicotinoids. Recent studies in the U.S. nd Europe hve shown tht smll mounts of neonicotinoids from treted seeds cn cuse disorienttion, suppressed immunity, nd erly deth in honeybees. This report mkes cler tht birds criticl gents in the control of griculturl pests -- re dversely ffected s well. A single seed treted with imidcloprid is enough to kill blue-jy-sized bird, nd less thn one corn seed per dy treted with ny of the neonicotinoid insecticides is sufficient to cuse reproductive bnormlities. This is extremely worrisome given the extensive use of neonicotinoids s seed tretments for corn, soy, cnol, nd incresingly for cerels. As this report shows, unlimited quntities of these treted seeds re redily vilble to birds while regultors mistkenly ssume tht exposure cn be minimized by lbel sttements or dherence to good griculturl prctices. Neonicotinoid-treted seeds present lethl risk for the birds tht et them. Yet when stte or county officer receives report of ded birds or other wildlife, the inspector hs no wy of determining whether neonicotinoids contributed to the deth. There is no redily vilble biomrker for neonicotinoids s there is for cholinesterse inhibitors such s the orgnophosphorous pesticides. It is stonishing tht EPA would llow pesticide to be used in hundreds of products without ever requiring the registrnt to develop the tools needed to dignose poisoned wildlife. It would be reltively simple to crete binding ssy for the neurl receptor which is ffected by this clss of insecticides. It is perplexing, s well, tht EPA does not require registrnts to report ny bird kills involving fewer thn 200 of flocking species, 50 individuls of songbird species, or 5 rptors. The gency s

68 Neonicotinoid Insecticides nd Birds revisions to its incident reporting requirements under FIFRA section 6()2 essentilly plce the Agency in stte of enforced ignornce in this regrd. These feeble reporting requirements nd the filure to require the development of bsic biomrkers help keep the government in the drk on rnge of pesticide effects on wildlife. The neonicotinoids re systemic, persistent in soils (nd thus prone to ccumultion from yer to yer), nd susceptible to runoff nd groundwter infiltrtion. These physicl properties nd their nerubiquity in pest control products hve led to strikingly high groundwter contmintion levels, lredy beyond the threshold found to kill mny qutic invertebrtes. The resulting effects on birds nd other orgnisms re cuse for concern. It is cler tht these chemicls hve the potentil to ffect entire food chins. Neonicotinoids hve been suspended for some uses in severl Europen countries. The Europen Commission nd the British government re currently tking steps to ssess the risks. Menwhile the U.S. continues to snction new uses. There is evidence tht U.S. regultors historiclly hve wited fr too long to impose needed restrictions on toxic insecticides responsible for millions of bird deths per yer (Mineu 2004) nd tht these chemicls likely contributed to the significnt decline of grsslnd birds in North Americ (Mineu nd Whiteside, 2013). Given the red flgs rised by this new clss of pesticides, serious independent review of the neonicotinoids is wrrnted, one tht goes well beyond the effects on honeybees. The results of this study nd others hve led Americn Bird Conservncy nd prtners in the Ntionl Pesticide Reform Colition to urge the EPA to tke the following ctions: - Suspend ll pplictions of neonicotinoids pending independent review of these products effects on birds, terrestril nd qutic invertebrtes, nd other wildlife. - Expnd its re-registrtion review of neonicotinoids beyond bees to include birds, qutic invertebrtes, nd other wildlife. - Bn the use of neonicotinoids s seed tretments. - Require tht registrnts of cutely toxic pesticides develop the tools necessry to dignose poisoned birds nd other wildlife. 67

69 Neonicotinoid Insecticides nd Birds Northern Bobwhite by Bill ubick 68

70 References Cited Open literture Neonicotinoid Insecticides nd Birds Adms, J. S., R. L. Knight, L. C. Mcewen, nd T. L. George Survivl nd growth of nestling Vesper Sprrows exposed to experimentl food reductions. Condor 96: Aldenberg, T. nd R. Luttik Extrpoltion fctors for tiny toxicity dt sets from species sensitivity distributions with known stndrd devition. IN Species Sensitivity Distributions in Ecotoxicology, L. Posthum, G.W. Suter II nd T.P. Trs [eds.], Lewis Publishers, Boc Rton, Florid, pp Alexnder, A.C., J.M. Culp, K. Liber, nd A.J. Cessn Effects of insecticide exposure on feeding inhibition in myflies nd oligochetes. Env. Toxicol. Chem. 26(8): Alexnder, A.C., K. erd, nd J.M. Culp Emergent body size of myfly survivors. Freshwter Biology 53, Avery, M.L., G.G. Decker, D.L. Fisher nd T.R. Stfford Responses of cptive blckbirds to new insecticidl seed tretment. J. Wildl. Mnge. 57: Avery, M.L., D.G. Decker, nd D.L. Fischer Cge nd flight pen evlution of vin repellency nd hzrd ssocited with imidcloprid-treted rice seed. Crop protection 13(7): Avery, M.L., D.L. Fischer, nd T.M. Primus Assessing the hzrd to grnivorous birds feeding on chemiclly treted seeds. Pestic Sci 49: Bcey, J Environmentl fte of imidcloprid. Cliforni Deprtment of Pesticide Regultion. 8 pp. Brbee, G.C. nd M. J. Stout Comprtive cute toxicity of neonicotinoid nd pyrethroid insecticides to non-trget cryfish (Procmbrus clrkii) ssocited with rice cryfish crop rottions. Pest Mnge Sci. 65: Beecher, N. A., R. J. Johnson, J. R. Brndle, R. M. Cse, nd L. J. Young Agroecology of birds in orgnic nd nonorgnic frmlnd. Conservtion Biology 16: Beketov, M.A. nd M. Liess Potentil of 11 pesticides to initite downstrem drift of strem mcroinvertebrte. Archives of Environ Contm Tox. 55: Beketov, M.A. nd M. Liess. 2008b. Acute nd delyed effects of the neonicotinoid insecticide thicloprid on seven freshwter rthropods. Environ Tox. 28: Bennett, R.S., I.C Dewhurst, A. Firbrother, A.D.M. rt, M.J. ooper, A. Leopold, P. Mineu, S.R. Mortensen, R.F. Shore nd T.A. Springer A new interprettion of vin nd mmmlin reproduction toxicity test dt in ecologicl risk ssessment. Ecotoxicology 14(8): Berny, P.J., F. Buronfosse, B. Videmnn,T. Buronfosse Evlution of the toxicity of imidcloprid in wild birds. A new high performnce thin lyer chromtogrphy (PTLC) method for the nlysis of liver nd crop smples in suspected poisoning cses. J. Liq. Chrom. & Rel. Technol., 22(10),

71 Neonicotinoid Insecticides nd Birds Best, L. B., R. C. Whitmore, nd G. M. Booth Use of cornfields by birds during the breeding seson: The importnce of edge hbitt. Americn Midlnd Nturlist 123: Botmn, N. D., N. W. Brickle, J. D. rt, T. P. Milsom, A. J. Morris, A. W. A. Murry, K. A. Murry, nd P. A. Robertson Evidence for the indirect effects of pesticides on frmlnd birds. Ibis 146: Böttger, R., J. Schller nd, S.Mohr Closer to relity the influence of toxicity test modifictions on the sensitivity of Gmmrus roeseli to the insecticide imidcloprid. Ecotox Environm Sfety 81: Boutin, C., K. E. Freemrk, nd D. A. Kirk Frmlnd birds in southern Ontrio: field use, ctivity ptterns nd vulnerbility to pesticide use. Agriculture Ecosystems & Environment 72: Brdbury, R. B., A. Kyrkos, A. J. Morris, S. C. Clrk, A. J. Perkins, nd J. D. Wilson bitt ssocitions nd breeding success of yellowhmmers on lowlnd frmlnd. Journl of Applied Ecology 37: Brdbury, R. B., J. D. Wilson, D. Moorcroft, A. J. Morris, nd A. J. Perkins bitt nd wether re wek correltes of nestling condition nd growth rtes of four UK frmlnd psserines. Ibis 145: Brickle, N. W., D. G. C. rper, N. J. Aebischer, nd S.. Cockyne Effects of griculturl intensifiction on the breeding success of corn buntings Miliri clndr. Journl of Applied Ecology 37: Brickle, N. W. nd W. J. Pech The breeding ecology of Reed Buntings Emberiz schoeniclus in frmlnd nd wetlnd hbitts in lowlnd Englnd. Ibis 146: Britschgi, A., R. Spr, nd R. Arlettz Impct of grsslnd frming intensifiction on the breeding ecology of n indictor insectivorous psserine, the Whincht Sxicol rubetr: Lessons for overll Alpine medowlnd mngement. Biologicl Conservtion 130: Butler, S. J., E.. A. Mttison, N. J. Glithero, L. J. Robinson, P. W. Atkinson, S. Gillings, J. A. Vickery, nd K. Norris Resource vilbility nd the persistence of seed-eting bird popultions in griculturl lndscpes : mechnistic modelling pproch. Journl of Applied Ecology 47: CADPR Deprtment of Pesticide Regultion (Cliforni) Pesticide Registrtion nd Evlution Committee. Meeting minutes July pp. 70

72 Neonicotinoid Insecticides nd Birds Cllhn, J. nd P. Mineu Evlution of clinicl sign dt from vin cute orl toxicity studies. Appendix 11; Scientific Opinion of the Pnel on Plnt Protection Products nd their Residues on Risk Assessment for Birds nd Mmmls, EFSA Journl (2008) 734, 10pp. CCME Cndin wter qulity guidelines: Imidcloprid. Scientific supporting document. Cndin Council of Ministers of the Environment. PN pp. Chen X.D., E. Culbert, V. ebert nd, J.D. Strk Mixture effects of the nonylphenyl polyethoxylte, R-11 nd the insecticide, imidcloprid on popultion growth rte nd other prmeters of the crustcen, Ceriodphni dubi. Ecotoxicology nd Environmentl Sfety 73: CSL (Centrl Science Lbortory) Risks to birds nd mmmls from solid formultions. Finl Project report. 39 pp. Dvis, B.N.K Levels of dieldrin in dressed whet seed fter drilling nd exposure on the soil surfce. Environmentl Pollution. 7: Dunn, J. C., K. C. mer, nd T. G. Benton Fer for the fmily hs negtive consequences: indirect effects of nest predtors on chick growth in frmlnd bird. Journl of Applied Ecology 47: EFSA (Europen Food sfety Authority) Conclusion on the peer review of imidcloprid. 120 pp. Ellis, C.R A survey of grnulr ppliction equipment nd insecticide rtes used for control of corn rootworms (coleopter:chrysomelide) in southern Ontrio. Proceedings of the Entomologicl Society of Ontrio. 113: Englert, D., M. Bundschuh, R. Schulz Thicloprid ffects trophic interction between gmmrids nd myflies. Environm. Pollution 167: Euliss, N.. Jr. nd D.M. Mushet Influence of griculture on qutic invertebrte communities of temporry wetlnds in the pririe pothole region of North dkot, USA. Wetlnds 19(3): Europen Commission Acetmiprid. SANCO/1392/2001 Finl. 34 pp. Europen Commission Clothinidin. SANCO/10533/05 Finl. 26 pp. Fernández Pere, M.T., E.A. Prdos, A.N. Villjos, J. L.A. Prdos, nd J.M. Grcí Budín Influence of vin reproduction ecotoxicologicl endpoints in the ssessment of plnt protection products. Journl of Environmentl Science nd elth, Prt B 44: Frnk, R., P. Mineu,.E. Brun, I.K. Brker, S.W. Kennedy nd S. Trudeu Deths of Cnd Geese following sprying of turf with dizinon. Bull. Env. Contm. Toxicol. 46: Freemrk, K. E. nd D. A. Kirk Birds on orgnic nd conventionl frms in Ontrio: prtitioning effects of hbitt nd prctices on species composition nd bundnce. Biologicl Conservtion 101: Ghilin, A. nd M. Bélisle Breeding success of Tree Swllows long grdient of griculturl intensifiction. Ecologicl Applictions 18:

73 Neonicotinoid Insecticides nd Birds Geis, A.D Reltive ttrctiveness of different foods t wild bird feeders. U.S. Dept. of the Interior, Fish nd Wildlife Service, Specil Scientific Report-Wildlife No. 233, Wshington D.C., pp11. Girrd, J. M., A. Bril, P. Mineu, nd L. Fhrig Forging hbitt nd diet of Song Sprrows (Melospiz melodi) nesting in frmlnd: A stble isotope pproch. Cndin Journl of Zoology Girrd, J. M The effects of conventionl nd orgnic cropping systems on food nd reproductive success of Song Sprrows in estern Ontrio frmlnd. PhD thesis, Crleton university, Ottw. Giroux, I Contmintion de l eu souterrine pr les pesticides et les nitrtes dns les régions en culture de pommes de terre. Cmpgne d échntillonnge de Direction de suivi de l étt de l environnement, Ministère de l Environnement, Gouvernement du Québec, Québec. Golwski, A. nd W. Meissner The influence of territory chrcteristics nd food supply on the breeding performnce of the Red-bcked Shrike (Lnius collurio) in n extensively frmed region of estern Polnd. Ecologicl Reserch 23: Green, R Fctors ffecting the diet of frmlnd skylrks, Alud rvensis. Journl of Animl Ecology. 47: Greer, R. D. nd S.. Anderson Reltionships between popultion demogrphy of McCown's Longspurs nd hbitt resources. Condor 91: rt, J. D., T. P. Milsom, G. Fisher, V. Wilkins, S. J. Moreby, A. W. A. Murry, nd P. A. Robertson The reltionship between yellowhmmer breeding performnce, rthropod bundnce nd insecticide pplictions on rble frmlnd. Journl of Applied Ecology 43: ysk, D., T. Koreng, F. Snchez-Byo, K. Gok Differences in ecologicl impcts of systemic insecticides with different physicochemicl properties on biocenosis of experimentl pddy fields. Ecotoxicology 21: ysk, D., T. Koreng, K. Suzuki, F. Sánchez-Byo, K. Gok. 2012b. Differences in susceptibility of five cldocern species to two systemic insecticides, imidcloprid nd fipronil. Ecotoxicology 21: ldik ML nd Clhoun DL Anlysis of the herbicide diuron, three diuron degrdtes, nd six neonicotinoid insecticides in wter Method detils nd ppliction to two Georgi strems. USGS Scientific Investigtions Report pp. ole, D. G., M. J. Whittinghm, R. B. Brdbury, G. Q. A. Anderson, P. L. M. Lee, J. D. Wilson, nd J. R. Krebs Widespred locl house-sprrow extinctions. Nture 418:931- owe, F. P., R. L. Knight, L. C. Mcewen, nd T. L. George Diet switching nd food delivery by shrubsteppe psserines in response to n experimentl reduction in food. Western North Americn Nturlist 60: useth, A.S. nd R.L. Groves Environmentl fte of neonicotinoids: potto cse study. (ccessed Februry 2013). Jemec, A., T. Tisler, D. Drobne, K. Sepcic, D. Fournier, nd P. Trebse Comprtive toxicity of imidcloprid, of its commercil liquid formultion nd of dizinon to non-trget rthropod, the microcrustcen Dphni mgn. Chemosphere 68(8):

74 Neonicotinoid Insecticides nd Birds Jeschke, P., R. Nuen, M. Schindler, nd A.Elbert Overview of the Sttus nd Globl Strtegy for Neonicotinoids. J. Agric. Food Chem. 59: Key, P., K. Chung, T. Siewicki, nd M. Fulton Toxicity of three pesticides individully nd in mixture to lrvl grss shrimp. Ecotoxicol Environ Sf 68(2): Kreuzberg, E Effects of lndscpe structure nd griculturl prctices on frmlnd birds in Ontrio. Kreutzweiser, D.P., K.P. Good, D. Chrtrnd, T.A. Scrr, nd D.G. Thompson Toxicity of the systemic insecticide, imidcloprid, to forest strem insects nd microbil communities. Bull Environ Contm Toxicol. 80(3): Lnyon, W.E Western Medowlrk (Sturnell neglect). In The Birds of North Americ, No Americn Ornothologists Union. The Acdemy of Sciences of Phildelphi. Leblnc,.M., K. LeBlnc, J.M. Culp, D.J. Bird, A.C. Alexnder, nd A.J. Cessn Single versus combined lethl effects of three griculturl insecticides on lrve of the freshwter insect Chironomus dilutes. Arch Environ Contm Toxicol 63: Leeuw, J.de, M. Gorree, G.R. de Snoo, W.L.M. Tmis, R.J.vn der Poll, nd R. Luttik Risks of grnules nd treted seeds to birds on rble fields. Ntionl Institute of Public elth nd the Environment. CML report Section Ecosystems & Environmentl Qulity, Leiden. Lopez-Anti, A., M.E. Ortiz-Sntliestr, F. Mougeot, nd R. Mteo Experimentl exposure of red-legged prtridges (Alectoris ruf) to seeds coted with imidcloprid, thirm nd difenoconzole. Ecotoxicology (online) DOI /s x. Lorenzen, B. nd J. Mdsen Feeding by geese on the Filso Frmlnd, Denmrk, nd the effect of grzing on yield structure of spring brley. olrctic Ecology. 9: Luknčič, S., U. Žibrt, T. Mezek, A. Jerebic, T. Simčič, A. Brncelj Effects of exposing two non-trget crustcen species, Asellus quticus L., nd Gmmrus fossrum Koch., to trzine nd imidcloprid. Bull Environ Contm Toxicol: 84: Luttik, R. nd Aldenberg, T Extrpoltion fctors for smll smples of pesticide toxicity dt: specil focus on LD50 vlues for birds nd mmmls. Environ. Toxicol. Chem. 16, Luttik, R., P. Mineu, nd W. Roelofs A review of interspecies toxicity extrpoltion in birds nd mmmls nd proposl for long-term toxicity dt. Ecotoxicology 14(8): Luttik, R.L., A. rt, W. Roelofs, P. Crig nd P. Mineu Vrition in the level of protection fforded to birds nd crustcens exposed to different pesticides under stndrd risk ssessment procedures. Integrted Environmentl Assessment nd Mngement 7(3): Mlev, O., R. Suerborn Klobučr, E. Fbbretti, P. Trebše Comprtive toxicity of imidcloprid nd its trnsformtion product 6-chloronicotinic cid to non-trget qutic orgnisms: Microlge Desmodesmus subspictus nd mphipod Gmmrus fossrum. Pesticide Biochemistry nd Physiology In Press. Mltby, L., Blke, N., Brock, T.C.M., Vn den Brink, P.J Insecticide species sensitivity distributions: importnce of test species selection nd relevnce to qutic ecosystems. Environmentl Toxicology nd Chemistry 24:

75 Neonicotinoid Insecticides nd Birds Mrtin, P. A., D. L. Johnson, D. J. Forsyth, nd B. D. ill Indirect effects of the pyrethroid insecticide deltmethrin on reproductive success of chestnut-collred longspurs. Ecotoxicology 7: Mrtin, P. A., D. L. Johnson, D. J. Forsyth, nd B. D. ill Effects of two grsshopper control insecticides on food resources nd reproductive success of two species of grsslnd songbirds. Environmentl Toxicology nd Chemistry 19: Mrtin, T. E Food s limit on breeding birds: A life-history perspective. Annul Review of Ecology Evolution nd Systemtics 18: Mson, R.,. Tennekes, F. Sánchez-Byo, P.U. Jepsen Immune suppression by neonicotinoid insecticides t the root of globl wildlife declines. Journl of Environmentl Immunology nd Toxicology; In Press September/October Mus, C. nd R. Nuen Response to the publiction: Tennekes,.A. (2010):The significnce of the Druckrey Küpfmüller eqution for risk ssessment The toxicity of neonicotinoid insecticides to rthropods is reinforced by exposure time. Toxicology 280(3): Myer, F.L. nd M.R. Ellersieck Mnul of cute toxicity: Interprettion nd dtbse for 410 chemicls nd 66 species of freshwter nimls. USDI Fish nd Wildlife Service Resource Publiction 160, Wshington D.C. 63 pp. Mze, R.C., R.P. Atkins, P. Mineu nd B.T. Collins Mesurement of pesticide residue in seeding opertions. Trns. Amer. Soc. Agric. Eng. 34(3): McKy,.V., Prosser, P.J., rt, A.D.M., Lngton, S.D., Jones, A., McCoy, C., Chndler-Morris, S.A. nd Pscul, J.A Do wood pigeons void pesticide treted cerel seed? Journl of Applied Ecology 36, Miller, C. K., R. L. Knight, L. C. Mcewen, nd T. L. George Responses of nesting Svnnh Sprrows to fluctutions in grsshopper densities in interior Alsk. Auk 111: Mineu, P., P.J. Sheehn nd A. Bril Pesticides nd wterfowl on the Cndin priries: A pressing need for reserch nd monitoring. (In) The vlue of birds. A.W. Dimond nd F. Filion (eds.) I.C.B.P. Technicl Publiction No. 6, Cmbridge, U.K. pp Mineu, P., B. Jobin, A. Bril A critique of the vin 5-dy dietry test (LC50) s the bsis of vin risk ssessment. Technicl Report Series. No Environment Cnd, Cndin Wildlife Service, Ottw. 23 pp. Mineu, P., D.C. Boersm, nd B. Collins An nlysis of vin reproduction studies submitted for pesticide registrtion. Ecotoxicology nd Environmentl Sfety 29: Mineu, P., B.T. Collins nd A. Bril On the use of scling fctors to improve interspecies extrpoltion of cute toxicity in birds. Regultory Toxicology nd Phrmcology 24: Mineu, P., R. Blcomb, R. Bennett, S. Dobson, M. Fry, M. Jber, A. Leopold, R. Munk, B. Ringer, A. Rispin, L. Sileo, R.Solecki nd. Thompson. 1996b. Testing for effects on reproduction. [In] Report of the SETAC/OECD Workshop on Avin Toxicity Testing. Inter- Orgniztionl Progrmme for the Sound Mngement of Chemicls, OECD Environmentl elth nd Sfety Publictions, Series on Testing nd Assessment No. 5, pp Mineu, P., A. Bril, B.T. Collins, J. Duffe, G. Joermn, R. Luttik Reference vlues for compring the cute toxicity of pesticides to birds. Reviews of Environmentl Contmintion nd 74

76 Neonicotinoid Insecticides nd Birds Toxicology 170: Mineu, P., M. ooper, N. Elmegrd, R. Gru, R. Luttik, R. Ringer. 2001b. Cse Study 5: Folir Insecticide II, Chpter 8. In: rt, A., D. Blluff, R. Brfknecht, P. Chpmn, A. wkes, G. Joermnn, A. Leopold, nd R. Luttik (eds.) Avin effects ssesment: A frmework for contminnt studies. SETAC Press, Penscol, Florid. pp Mineu, P Birds nd pesticides: Are pesticide regultory decisions consistent with the protection fforded migrtory bird species under the Migrtory Bird Trety Act? The Willim nd Mry Environmentl Lw nd Policy Review 28(2): Mineu, P A review nd nlysis of study endpoints relevnt to the ssessment of long term pesticide toxicity in vin nd mmmlin wildlife. Ecotoxicology. 14(8): Mineu, P. C. Morrison, M. Whiteside, nd K. rding Developing risk-bsed rnkings for pesticides in support of stndrd development t Environment Cnd: Preliminry terrestril rnkings. Ntionl Agri-Environmentl Stndrds Inititive Technicl Series Report No. 2-43, Environment Cnd, 92 pp. Mineu, P. nd M. Whiteside. In press. Pesticide cute toxicity is better correlte of U.S. grsslnd bird declines thn griculturl intensifiction. PLOS ONE. Mirnd G.R.B., C.G. Retno, E. Silv, M.A. Dm, nd M.J. Cerejeir Environmentl fte of neonicotinoids nd clssifiction of their potentil risks to hypogen, epygen, nd surfce wter ecosystems in Brzil. umn nd Ecologicl Risk Assessment: An Interntionl Journl17:4: Mirrchi, R.E. nd T.S. Bskett Mourning Dove (Zenid mcrour). In The Birds of North Americ, No Americn Onrothologists Union. The Acdemy of Sciences of Phildelphi. Mohr, S., R. Berghhn, R. Schmiediche, V. übner, S. Loth, M. Feibicke, W. Milhn, J. Wogrm Mcroinvertebrte community response to repeted short-term pulses of the insecticide imidcloprid. Aqutic Toxicology : Moller, A. P The effect of diry frming on brn swllow irundo rustic bundnce, distribution nd reproduction. Journl of Applied Ecology 38: Morris, A. J., J. D. Wilson, M. J. Whittinghm, nd R. B. Brdbury Indirect effects of pesticides on breeding yellowhmmer (Emberiz citrinell). Agriculture Ecosystems & Environment 106:1-16. Morrissey, C. nd A. Min Anlysis nd identifiction of neonicotinoid pplictions in pririe wtersheds. University of Ssktchewn. Unpublished report to Environment Cnd. 19pp. Murton, R.K. nd M. Vizoso Dressed cerel seed s hzrd to wood-pigeons. Annls of Applied Biology. 52: Ngi, T. nd A. Yokohom Comprison of ecologicl risks of insecticides for nursery-box ppliction using species sensitivity distribution. J. Pestic. Sci. 37(3): Ngy, K.A Field metbolic rte nd food requirement scling in mmmls nd birds. Ecologicl Monogrphs 57(2): Ngy, L. R. nd R. T. olmes Fctors influencing fecundity in migrtory songbirds: is nest predtion the most importnt? Journl of Avin Biology 35:

77 Neonicotinoid Insecticides nd Birds Ngy, L. R. nd R. T. olmes Food limits nnul fecundity of migrtory songbird: An experimentl study. Ecology 86: Overmyer, J.P., B.N. Mson, K.L.Armbrust. 2005, Acute toxicity of imidcloprid nd fipronil to nontrget qutic insect, Simulium vitttum Zetterstedt cytospecies IS-7. Bull Environ Contm Tox. 74: Plmer, T.K The house finch nd strling in reltion to Cliforni s griculture. In Productivity, Popultion Dynmics nd Systemtics of Grnivorous Birds. Proceedings of Generl Meeting of the Working Group on Grnivorous Birds, IBP, PT Section, ollnd. Pscul, J.A., rt, A.D.M., Sunders, P.J., McKy,.V., Kilptrik, J. & Prosser, P Agriculturl methods to reduce the risk to birds from cerel seed tretments on fenlnds in estern Englnd. I. Sowing depth mnipultion. Agricultrure, Ecosystems nd the Environment 72, Pscul, J.A., Sunders, P.J., rt, A.D.M. & Mottrm, J. 1999b. Agriculturl methods to reduce the risk to birds from cerel seed tretments on fenlnds in estern Englnd II. Rolling nd hrrowing s post-sowing cultivtions. Agricultrure, Ecosystems nd the Environment 72, Pwlin, I.M. nd Proulx, G Study of house sprrow (Psser domesticus) feeding preference to nturl color nd gurd cot blue coted seeds. Crop Protection. 15(2): Pech, W. J., G. M. Siriwrden, nd R. D. Gregory Long-Term chnges in over-winter survivl rtes explin the decline of Reed Buntings Emberiz schoeniclus in Britin. Journl of Applied Ecology 36: Pestn, J.L.T., S. Loureiro, D.J. Bird, A.M.V.M. Sores Fer nd lothing in the benthos: Responses of qutic insect lrve to the pesticide imidcloprid in the presence of chemicl signls of predtion risk. Aqutic Toxicology 93: Pestn, J.L.T., A.C. Alexnder, J.M. Culp, D.J. Bird, A.J. Cessn, A.M.V.M. Sores. 2009b. Structurl nd functionl responses of benthic invertebrtes to imidcloprid in outdoor strem mesocosms. Environ Pollution. 157(8-9): PMRA Admire. Regultory Note R pp. PMRA Imidcloprid. Regultory Note pp. Potts, G. R The Prtridge: pesticides, predtion nd conservtion. Poulin, B., G. Lefebvre, nd L. Pz Red flg for green spry: dverse trophic effects of Bti on breeding birds. Journl of Applied Ecology 47: Poulin, B Indirect effects of bioinsecticides on the nontrget fun: The Cmrgue experiment clls for future reserch. Act Oecologic 44: Poulin, B., F. Alblt, C. Cleys, L. Després, C. Jkob nd C. Tétrel Rpport intermédiire sur le suivi scientifique nnuel mené en 2012 en prllèle ux opértions de démoustiction u Bti sur le périmètre du Prc Nturel Régionl de Cmrgue. Rpport présenté u Prc Nturel Régionl de Cmrgue le 30 novembre pp. Powell, G. V. N Reproduction by n ltricil songbird, the Red-winged Blckbird, in fields treted with the orgnophosphte insecticide fenthion. Journl of Applied Ecology 21:

78 Neonicotinoid Insecticides nd Birds Puckett,. L., J. R. Brndle, R. J. Johnson, nd E. E. Blnkenship Avin forging ptterns in crop field edges djcent to woody hbitt. Agriculture, Ecosystems nd Environment 131:9-15. Ruter, C. M., P. A. Brodmnn, nd. Reyer Provisioning behviour in reltion to food vilbility nd nestling food demnd in the Wter Pipit Anthus spinolett. Arde 88: RIVM Environmentl risk limits for imidcloprid. C.J.A.M. Posthum-Doodemn. RIVM Letter report / pp. Rodenhouse, N. L. nd L. B. Best Forging ptterns of Vesper Sprrows (Pooecetes grmineus) breeding in croplnd. Americn Midlnd Nturlist 131: Snchez-Byo, F. nd K. Gok Influence of light in cute toxicity biossys of imidcloprid nd zinc pyrithione to zooplnkton crustcens. Aqutic Toxicology 78: Snchez-Byo, F. nd K. Gok Simplified models to nlyse time- nd dose-dependent responses of popultions to toxicnts Ecotoxicology 16: Snchez-Byo, F From simple toxicologicl models to prediction of toxic effects in time. Ecotoxicology 18: S n chez-byo, F.,.A. Tennekes nd K. Gok Impct of Systemic Insecticides on Orgnisms nd Ecosystems, Insecticides - Development of Sfer nd More Effective Technologies, Stnislv Trdn (Ed.), DOI: / Avilble from: Selås, V., R. Steen, S. Kobro, T. Lislevnd, nd I. Stenberg Direct nd indirect wether impcts on spring popultions of lesser spotted woodpecker (Dendrocopos minor) in Norwy. Scndinvin Journl of Forest Reserch 23: Setchfield, R. P., C. Mucklow, A. Dvey, U. Brdter, nd G. Q. A. Anderson An grienvironment option boosts productivity of Corn Bunting Emeriz clndr in the UK. Ibis 154: Sheehn, P.K., A. Bril, P. Mineu, D.K. Smith, A. rfenist nd W.K. Mrshll The impct of pesticides on the ecology of pririe-nesting ducks. Cndin Wildlife Service Technicl Report Series No. 19. Environment Cnd, Ottw. 653 pp. Sheehn, P., A. Bril, P. Mineu nd D. Pustenbch Predicting the effects of insecticides on qutic systems nd the wterfowl tht use them. In: G.M. Rnd. (Ed.) Fundmentls of Aqutic Toxicology (Second Edition), Tylor nd Frncis, North Plm Bech, Florid, pp Shore, R.F., D.R. Crocker,.R. Akcky, R.S. Bennett, P.F. Chpmn, M. Clook, M. Crne, I.C. Dewhurst, P.J. Edwrds, A. Firbrother, S. Ferson, D. Fischer, A.D.M. rt, M. olmes, M.J. ooper, M. Lvine, A. Leopold, R. Luttik, P. Mineu, D.R.J. Moore, S.R. Mortenson, D.G. Noble, R.J. O'connor, W. Roelofs, R.M. Sibly, G.C. Smith, M. Spendiff, T. A. Springer,.M. Thompson, C. Topping Cse Study Prt 1: ow to Clculte Approprite Deterministic Long-term Toxicity to Exposure Rtios (TERs) for Birds nd Mmmls. Ecotoxicology. 14(8): Simons, L. S. nd T. E. Mrtin Food limittion of vin reproduction: An experiment with the Cctus Wren. Ecology 71:

79 Neonicotinoid Insecticides nd Birds Siriwrden, G. M., S. R. Bllie,. Q. P. Crick, nd J. D. Wilson The importnce of vrition in the breeding performnce of seed-eting birds in determining their popultion trends on frmlnd. Journl of Applied Ecology 37: Snchez-Byo, F. nd K. Goy Influence of light in cute toxicity biossys of imidcloprid nd zinc pyrithione to zooplnkton crustcens. Aqut Toxicol 78(3): Smith, G.K Risks to Birds from Pesticide-treted Seed nd the Possible Role of Ultrviolet Reflection in Seed Colour Preferences nd Repellent Strtegies. Unpublished MSc. Thesis. Crleton University. 176 pp. Smith, K.P., 2011, Surfce-wter, wter-qulity, nd meteorologicl dt for the Cmbridge, Msschusetts, drinking-wter source re, wter yers : U.S. Geologicl Survey Open- File Report , 109 p., t Song, M.Y., J.D. Strk, J.J. Brown Comprtive toxicity of four insecticides, including imidcloprid nd tebufenozide, to four qutic rthropods. Environ Tox Chem. 16: Strner, K. nd KS Goh Detections of the neonicotinoid insecticide imidcloprid in surfce wters of three griculturl regions of Cliforni, USA, Bull Environ Contm Toxicol 88(3): Stephn C.E., Mount, D.I., nsen, D.J., Gentile, J., Chpmn, G.A., Brungs, W.A Guidelines for deriving numericl ntionl wter qulity criteri for the protection of qutic orgnisms nd their uses. U.S. Environmentl Protection Agency. PB , Springfield, VA. 98pp. Stoughton, S., J. Leber, J. Culp, nd A. Cessn Acute nd chronic toxicity of imidcloprid to the qutic invertebrtes Chironomus tentns nd ylell ztec under constnt- nd pulseexposure conditions. Arch. Environ. Contm. Toxicol. 54(4): Strong, A. M., C. C. Rimmer, nd K. P. McFrlnd Effect of prey biomss on reproductive success nd mting strtegy of Bicknell's Thrush (Cthrus bicknelli), polygynndrous songbird. Auk 121: Sullivn, K. A Predtion nd strvtion: Age-specific mortlity in juvenile juncos (Junco phenotus). Journl of Animl Ecology 58: Tmis, W.L.M., Gorree, M., J. Leeuw, G.R. De Snoo, nd R. Luttik The number of exposed dressed seeds in the field; n outline for field reserch. In Seed tretment: Progress nd prospects. BCPC Monogrph 57: Tennekes,.A The systemic insecticides: disster in the mking. Weevers Wlburg Communictie, Zutphen, Netherlnds, 72 pp. Tennekes,.A. 2010b. The significnce of the Druckrey Küpfmüller eqution for risk Assessment The toxicity of neonicotinoid insecticides to rthropods is reinforced by exposure time. Toxicology 276:1-4. Tennekes,.A The significnce of the Druckrey Küpfmüller eqution for risk ssessment The toxicity of neonicotinoid insecticides to rthropods is reinforced by exposure time: Responding to Letter to the Editor by Drs. C. Mus nd R. Nuen of Byer Crop Science AG. Toxicology 280(3):

80 Neonicotinoid Insecticides nd Birds Tennekes,.A., F. Snchez-Byo Time-dependent toxicity of neonicotinoids nd other toxicnts: implictions for new pproch to risk ssessment. J Environ Anl Toxicol. S4:001. Tokumoto, J., M. Dnjo, Y. Kobyshi, K. Kinoshit, T. Omotehr, A. Ttsumi, M. shiguchi, T. Sekijim,. Kmisoym, T. Yokoym,. Kitgw, nd N. oshi Effects of Exposure to Clothinidin on the Reproductive System of Mle Quils. The Journl of Veterinry Medicl Science J-STAGE Advnce Published Dte: 29 Jn Tišler, T., A. Jemec, B. Mozeticˇ, P. Trebše zrd identifiction of imidcloprid to qutic environment. Chemosphere.. 76: U.S. Environmentl Protection Agency Imidcloprid. Review rebuttl to erlier EEB risk ssessment on cotton, pottoes nd pple. DP Brcode: D pp. U.S. Environmentl Protection Agency. 1994b. Registrtion for imidcloprid (NTN33893). Decision Memorndum.9 pp. U.S. Environmentl Protection Agency Response to Assessment of hndler exposure resulting from the commercil ppliction of cetmiprid to cnol nd mustrd MRID PC Code No , DP Brcode U.S. Environmentl Protection Agency EFED Risk Assessment for the Seed Tretment of Clothinidin 600FS on Corn nd Cnol (PC Code ; DP Brcode: D278110). 99pp. U.S. Environmentl Protection Agency. 2003b. Addendum referring to EFED s risk ssessment on clothinidin use s seed tretment on corn nd cnol (PC code ). 4 pp. U.S. Environmentl Protection Agency EFED Registrtion Chpter for Clothinidin for use on Tobcco, Turf, Apples, Pers nd Ornmentls. DP Brcodes: D nd D pp. U.S. Environmentl Protection Agency EFED Registrtion Chpter for Clothinidin for use on Pottoes nd Grpes s Spry tretment nd s Seed Tretment for Sorghum nd Cotton. DP Brcodes: D313414, D nd D pp. U.S. Environmentl Protection Agency Section 18 Request for Use of Clothinidin on Sugr Beet Seed to Control the Bet Lefhopper (Vector of Beet Curly Top Virus). U.S. Environmentl Protection Agency EFED Section 3 nd IR-4 risk ssessment for imidcloprid for use on soybens, penuts, kv, millet, ots, rtichoke, wild rspberry, nd cneberry subgroup 13A. PC code pp. U.S. Environmentl Protection Agency. 2007b. EFED Sction 3 Registrtion for Clothinidin nd Bet-Cyfluthrin combintion prodct for use on sugr beets s seed tretment. DP brcode: D pp. U.S. Environmentl Protection Agency Imidcloprid summry document registrtion review: Initil docket December Docket Number: EPA-Q-OPP U.S. Environmentl Protection Agency. 2008b. Ecologicl Risk Assessment for the Section 3 New Use Registrtion of Thimethoxm on Citrus Fruits nd Tree Nuts. U.S. Environmentl Protection Agency Clothinidin Registrtion of New products Sepresto 75WS nd PROCEED TM OPTIMUM, for Seed Tretment; New Uses for the Chemicl on 79

81 Neonicotinoid Insecticides nd Birds Tuberous nd Corm Vegetbles (CSG 1C), Bulb Vegetbles (Seed Tretment only) (CG 3), Lefy Greens (CG4), Brssic (Cole) Vegetbles (CG 5), Fruiting Vegetbles (CG8), Cucurbit Vegetbles (CG9), Crnberry nd Low Growing Berries (Except Strwberry) (GSG13-07), Tree Nuts (CG 14), Cerel Grins (Except Rice, Seed Tretment Only) (CG 15), Figs, Pomegrntes, Cotton, Soybens, Pech nd Potto Seed Pieces Tretment. DP Brcodes: , , , , , , U.S. Environmentl Protection Agency Clothinidin (Aren 50 WDG Insecticide): increse in ppliction rte to vegetbles nd ddition of bsl brk ppliction to trees. DP Brcode: D U.S. Environmentl Protection Agency Revised Assessment for Clothinidin Registrtion of Prosper T400 Seed Tretment on Mustrd Seed (Oilseed nd Condiment) nd PonchoN otivo Seed Tretment on Cotton. 101pp. U.S. Environmentl Protection Agency. 2011b. Thimethoxm summry document registrtion review: Initil docket December Docket Number: EPA-Q-OPP pp. Vn Dijk, T Effects of neonicotinoid pesticide pollution of Dutch surfce wter on nontrget species bundnce. Unpublished MSc Thesis in Sustinble Development Trck Lnd use, Environment nd Biodiversity,Utrecht University. 75pp. Vn Vlrdingen, P.L.A., T.P. Trs, A.M. Wintersen, nd T. Aldenberg ETX2.0. A progrm to clculte hzrdous concentrtions nd frction ffected, bsed on normllydistributed toxicity dt. RIVM report (nd softwre) /2004. Ntionl Institute for Public elth nd the Environment, The Netherlnds. Verbeek, N.A.M The use of grit in pipits, especilly the Americn pipit. Journl of Field Ornithology. 65(4): Whiteside, M., P. Mineu, C. Morrison, nd L.D. Knopper Comprison of score-bsed pproch with risk bsed rnking of in-use griculturl pesticides in Cnd to qutic receptors. Integrted Environmentl Assessment nd Mngement 4(2): Wilson, L., J. Elliot, S. Szeto, nd B.Vernon Degrdtion of four grnulr insecticides in Frser Delt soils nd impliction for wildlife poisonings. Preliminry report, CWS & Agriculture nd Agri-Food Cnd Reserch Sttion, British Columbi. Yckel Adms, A. A., S. K. Skgen, nd J. A. Svidge Modeling post-fledgling survivl of Lrk Buntings in response to ecologicl nd biologicl fctors. Ecology 87: Yokoym, A., K. Ohtsu, T. Iwfune, T. Ngi, S. Ishihr, Y. Kobr, T. orio nd S. Endo Sensitivity difference to insecticides of riverine cddisfly, Cheumtopsyche brevilinet (Trichopter: ydropsychide), depending on the lrvl stges nd strins. J. Pestic. Sci., 34(1), Zlik, N. J. nd A. M. Strong Effects of hy cropping on invertebrte biomss nd the breeding of Svnnh Sprrows (Psserculus sndwichensis). Auk 125: Znette, L., M. Clinchy, nd J. N. M. Smith Combined food nd predtor effects on songbird nest survivl nd nnul reproductive success: results from bi-fctoril experiment. Oecologi 147:

82 Neonicotinoid Insecticides nd Birds Industry studies obtined through the US Freedom of Informtion process nd reviewed for the current report Avery, M.L., D.G. Decker nd D.L. Fischer. 1993b. Cge nd flight pen evlution of vin repellency nd hzrd ssocited with imidcloprid-treted rice seed. Miles Incorported. 57 pp. Brfknecht, R Acceptnce of TI 435 FS coted rpe seeds (1.67 L product/100 kg seed) by Jpnese Quil (Coturnix coturnix jponic). Byer AG. 30 pp. Brfknecht, R. 1998b. Acceptnce of TI 435 FS Coting of Mize Seeds (50 g.i./50000 seeds) by Domestic Pigeon (Columb Iivi-f domestic) ccording to BBA -Test Guideline Byer AG. 24 pp. Brfknecht, R Acceptnce of TI 435 FS 600 (25 g.i./unit) Treted Seeds by Domestic Pigeons (Columb livi f. domestic). Byer AG. 18 pp. Brewer, L.W., M.C. Tliferro nd V.C. Miller The reproductive toxicity test of CGA technicl with the mllrd duck (Ans pltyrhynchos). Novrtis Crop Protection Inc. 322 pp. Gllgher, S.P. nd J.B. Bevers TI-435 Technicl: An cute orl toxicity study with the Jpnese quil. Byer Corp. 41 pp. Gllgher, S.P., C.S. Csey, J.B. Bevers, M.J. Jber nd T.Z. Kendll TI-435 Technicl. A reproduction study with the northern bobwhite (Colinus virgininus). Byer Corp. 183 pp. Gllgher, S.P., C.S. Csey, J.B. Bevers, M.J. Jber nd T.Z. Kendll. 2000b. TI-435 Technicl. A reproduction study with the mllrd (Ans pltyrhinchos). Byer Corp. 182 pp. Gru, R Bird toxicity orl / Cnry Bird (Serinus cnries). NTN techn. Byer AG. 2 pp. Gru, R Bird toxicity orl / pigeon (Columb livi). NTN techn. Byer AG. 2 pp. Gru, R Acute orl LD50 of NTN to Jpnese quil. Byer AG. 42pp. Gru, R YRC 2894 techn. Acute orl Toxicity to Bobwhite Quil. Byer AG. 39 pp. ncock, G.A NTN Technicl: An cute orl LD50 with mllrds. Byer Corp. 32 pp. ncock, G.A Effect of technicl YRC 2894 on mllrd reproduction. Byer Corp. 106 pp. ncock, G.A Effect of technicl YRC 2894 on mllrd reproduction. Byer Corp. 106 pp. ubbrd, P Acetmiprid: An Acute Orl Toxicity Study with the Zebr Finch (Poephil guttt). Nippon Sod Co. 76 pp. Johnson, A.J NI-25. Acute toxicity (LD50) to the mllrd duck. Nippon Sod Co. 50 pp. Johnson, A.J TI-435 Technicl cute orl toxicity (LD50) to Bobwhite quil. Ayer Corp. 47 pp. Schmuck, R Effects of subchronic dietry exposure of YRC 2894 on bobwhite quil including effects on reproduction nd helth. Byer AG. 163 pp. 81

83 Neonicotinoid Insecticides nd Birds Stfford, J.M Acetmiprid (NI-25) Reproductive toxicity test with mllrd duck (Ans pltyrhinchos). Nippon sod Co. 153 pp. Tliferro, M.C., L.W. Brewer nd V. Miller Reproduction study with cetmiprid in the Northern Bobwhite. Amended Finl report. Rhone Poulenc Ag Compny. 319 pp. Tliferro, M.C., nd V. Miller Tliferro, M.C. nd V. Miller Reproduction study with cetmiprid in the mllrd duck. Rhone Poulenc Ag Compny. 346 pp. Temple, D.L., K.. Mrtin, J.B. Bevers, nd M. Jber. Acetmiprid: A reproduction study with the Northern Bobwhite. Nippon Sod Co. Ltd. 186 pp. Toll, P.A Technicl NTN 33893: An Acute Orl LD50 with Bobwhite Quil. Moby Corportion. 25 pp. Toll, P.A Technicl NTN 33893: A one genertion reproduction study with mllrd ducks. Moby Corportion. 114 pp. Toll, P.A. 1991b. Technicl NTN 33893: A one genertion reproduction study with Bobwhite Quil. Moby Corportion. 105 pp. Dickcissel by Owen Deutsch 82

84 Neonicotinoid Insecticides nd Birds Cliforni Quil chick by Precocil, wikimedi.org Cddisfly by Bruce Mrlin, Wikimedi.org 83

85 Neonicotinoid Insecticides nd Birds ANNEX 1 Toxicity of imidcloprid to qutic invertebrtes Under Form of pesticide: FORM = formultion, = Technicl.i., DEG = degrdte. Under study type: A = Acute, C = Chronic. Under exposure type: S = Sttic, F = Flow through, SR = Sttic renewl. Chemicl i Form Txon1 Txon2 Acetmiprid Anlytic l grde Acetmiprid 99 EXP 60707A Acetmiprid (20%) Acetmiprid Acetmiprid 99.9 Acetmiprid Acetmiprid Anlytic l grde FOR M Acetmiprid (IC-0 Metbolite) 99.7 DEG Acetmiprid (IM-1-2 Metbolite) 99.6 DEG Acetmiprid (IM DEG Common Nme Crustce Amphipod Scud Crustce Crustce Crustce Crustce Brnchiopo d Brnchiopo d Brnchiopo d Mlcostrc Wter fle Wter fle Wter fle Opossum shrimp Insect Midge Insect Blck fly Crustce Crustce Crustce Brnchiopo d Brnchiopo d Brnchiopo Wter fle Wter fle Wter fle Txonomic Ag e AGE Clss Study Time (Vlu e) Stud y time (Unit ) Stud y type Exposur e type Mesure Qulifi er for Toxicit y Toxicity (ug/l) Gmmrus pulex 96 h A S LC50 50 Dphni mgn Dphni mgn CL (in originl units) <2 4 hr LARVAE 48 h A S EC <2 4 hr LARVAE 48 h A S EC50 > NOEC (reproductio n) 5000 Dphni mgn 24 d C <2 Americmysis 4 bhi hr LARVAE 96 h A F LC50 66 Chironomus riprius 28 d C NOEC (emergence & development ) 5 Simulium ltigonium LARVAE 96 h A S LC Dphni mgn Dphni mgn Dphni mgn Prob it slop <2 4 hr LARVAE 48 h A SR EC50 > N.A. N.A. <2 4 hr LARVAE 48 h A SR EC50 > N.A. N.A. <2 4 LARVAE 48 h A SR EC e Source Reference Beketov Originl nd Liess publiction 2008b Stud y Dte One liner 2007, EU 2004 review 1998 EU 2004 review EU 2004 review 1998 One liner EU 2004 review Beketov Originl nd Liess publiction 2008b One liner 2007, EU 2004 review 1997 One liner 2007, EU 2004 review 1997 One liner Notes 84

86 Neonicotinoid Insecticides nd Birds Metbolite) d hr Acetmiprid (IM-1-4 Metbolite) 98.7 DEG Acetmiprid (IM-1-4 Crustce Crustce Brnchiopo d Mlcostrc Wter fle Opossum shrimp Metbolite) 99.6 DEG Acetmiprid (IM-1-4 Metbolite) DEG Insect Midge Clothinidin 97.6 Clothinidin 97.6 Clothinidin Clothinidin Crustce Crustce Crustce Crustce Brnchiopo d Brnchiopo d Brnchiopo d Brnchiopo d Wter fle Wter fle Wter fle Wter fle Dphni mgn Americmysis bhi <2 4 hr 48 h A EC <2 4 hr LARVAE 96 h A F LC Chironomus riprius 48 h A LC Dphni mgn Dphni mgn <2 4 hr LARVAE 48 h A S EC50 > N.A. <2 4 hr LARVAE 48 h A EC N.A. Dphni mgn 21 d C Dphni mgn 21 d C NOEC (number of young) 120 N.A. N.A. NOEC (number of young) 42 N.A. N.A. One liner 2007, EU 2004 review 1997 One liner EU 2004 review One Liner 2007, EPA 2003 ssessmen t for corn nd cnol Plmer EPA 2003 Fct Sheet 2000 EU 2005 Summry; PMRA 2011 EPA 2003 ssessmen t for corn Nock et nd cnol l Clothinidin Clothinidin 97.6 Clothinidin Clothinidin Clothinidin Crustce Crustce Crustce Crustce Brnchiopo d Mlcostrc Mlcostrc Mlcostrc Wter fle Opossum shrimp Opossum shrimp Opossum shrimp Insect Midge Dphni mgn 21 d C LC N.A. N.A. Americmysis bhi <2 4 hr LARVAE 96 h A F LC50 51 Americmysis bhi 39 d C Americmysis bhi 39 d C Chironomus riprius 28 d C NOEC (number of young) 5.1 N.R. EC50 (reproductio n) 7.6 N.R. EC15 (lrvl emergence) 0.72 PMRA 2011 One Liner 2007, EPA 2003 Fct sheet; PMRA EPA 2003 ssessmen t for corn nd cnol; PMRA 2011 PMRA 2011 EU 2005 Summry; Footprint Drottr et l Drottr et l Note fctor of 10 from cute dt. Very different from Dphni rtio of >2800 Footprint DB gives this s the NOEC 85

87 Neonicotinoid Insecticides nd Birds Clothinidin Clothinidin Clothinidin Clothinidin Clothinidin MNG metbolite 99 DEG Clothinidin TNG metbolite 95.1 DEG Clothinidin TZNG metbolite 99 DEG Insect Midge Insect Midge Insect Midge Chironomus riprius 28 d C EC50 (emergence) 1 Chironomus riprius 48 h A EC50 22 Chironomus riprius 48 h A EC50 29 microcos m micocosm C EAC 3.1 Crustce Crustce Crustce Brnchiopo d Brnchiopo d Brnchiopo d Wter fle Wter fle Wter fle Clothinidin MU metbolite DEG Insect Midge Clothinidin TMG metbolite 98.2 DEG Insect Midge Clothinidin TZMU metbolite DEG Insect Midge Clothinidin TZNG metbolite DEG Insect Midge Dphni mgn Dphni mgn Dphni mgn Chironomus riprius Chironomus riprius Chironomus riprius Chironomus riprius <2 4 hr LARVAE 48 h A S EC50 > N.A. N.A. <2 4 hr LARVAE 48 h A S EC50 > N.A. N.A. <2 4 hr LARVAE 48 h A S EC N.A. N.A. 2-3 D LARVAE 48 h A LC50 > NA NA 2-3 D LARVAE 672 h C S LC50 < 18 NA NA 2-3 D LARVAE 48 h A LC50 > NA NA 2-3 D LARVAE 48 h A LC NA NA DB; PMRA 2011 PMRA 2011 EPA 2003 Fct Sheet, corn nd cnol ssessmen t EU 2005 Summry EU 2005 Summry EPA 2003 corn nd cnol ssessmen t. EPA 2003 corn nd cnol ssessmen t. EPA 2003 corn nd cnol ssessmen t EPA 2003 corn nd cnol ssessmen t. Mttlock 2001 endel endel endel One liner 2005 BAY 1998 EPA 2003 corn nd cnol ssessmen t. EPA 2003 corn nd cnol ssessmen Footprint DB gives this s the NOEC Note tht One Liner 2007 refers to this vlue s TZNG Note possible inconsistenc y between test species in nming of metbolites Note possible inconsistenc y between test species in nming of metbolites Note possible inconsistenc y between 86

88 Neonicotinoid Insecticides nd Birds Dinotefurn 99.2 Dinotefurn Dinotefurn dinotefurn Dinotefurn dinotefurn NR Imidcloprid 96.2 Imidcloprid 22.7 Imidcloprid Imidcloprid 96.2 Imidcloprid 240 g/l Imidcloprid 96.2 Imidcloprid >95% Imidcloprid Imidcloprid 40.00% Imidcloprid 99.50% Imidcloprid FOR M FOR M FOR M FOR M FOR M Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Mlcostrc Brnchiopo d Brnchiopo d Brnchiopo d Mlcostrc Mlcostrc Mlcostrc Mlcostrc Mlcostrc Mlcostrc Mlcostrc Mlcostrc Cldocer Opossum shrimp Wter fle Wter fle Wter fle Cryfish Cryfish Opossum shrimp Opossum shrimp Sltwter shrimp Sltwter shrimp Sltwter shrimp Sltwter shrimp Americmysis bhi Dphni mgn Dphni mgn Dphni mgn Orconectes nis Orconectes nis Americmysis bhi Americmysis bhi <2 4 r 96 h A F LC < NA r 48 h A EC50 > NA NA <2 4 r LARVAE 48 h A S EC50 > NA NA NR NR t. test species in nming of metbolites One Liner One Liner One Liner UNKNOW FOOTPRI N 48 h A EC NT DB Pesticide UNKNOW Mnul N 48 h A LC (14th ed) UNKNOW N 48 h A LC50 12 PM 2000 JUVENIL One liner E 96 h A F LC N.R. 2004, 2007 TES 1990 Juv <2 4 hr LARVAE 96 h A S LC Americmysis bhi 96 h A LC50 37 Americmysis bhi 96 h A LC Americmysis bhi 96 h A LC50 36 Americmysis bhi 96 h A LC Brine shrimp Artemi sp. 48 h A LC Asellus Isopod quticus 48 h A S LC Cldocer Ceriodphni n dubi 48 h A S LC Crustce Amphipod Scud ylell ztec Chydorus sphericus 24 h A S EC50 (immobility) d 28 d C SR LC N.R One liner 2004, 2007 TES 1992 Cox 2001 nd Felsot Stoughton & Ruppert et l CCME 2007 CCME 2007 CCME 2007 Originl publiction Originl publiction Originl publiction Originl publiction Originl publiction Wrd 1990b (Byer) Lintott 1992 (Byer) Wrd 1990b (Byer) Song et l Lukncic et l Chen et l Snchez- Byo nd Gok 2006 Stoughton et l Test t 27 degrees C Observtion time extended to 28 d 87

89 Neonicotinoid Insecticides nd Birds Imidcloprid 99.50% Imidcloprid 99.50% Imidcloprid Imidcloprid 99.50% Imidcloprid 99.50% Imidcloprid 99.50% Imidcloprid 99.50% Imidcloprid 99.50% Imidcloprid 99.50% Imidcloprid 99.50% Imidcloprid Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Crustce Ostrcod Ostrcod Ostrcod Ostrcod Brnchiopo Sltwter shrimp Wter fle Chydorus sphericus 48 h A S EC50 (immobility) 832 Cyprett seurti 24 h A S LC Americmysis bhi 28 d C Cyprett seurti 24 h A S EC50 (body length) EC50 (immobility) Cyprett seurti 48 h A S LC Cyprett seurti 48 h A S EC50 (immobility) Cypridopsis vidu 24 h A S LC50 > 4000 Cypridopsis vidu 24 h A S EC50 (immobility) Cypridopsis vidu 48 h A S LC Cypridopsis vidu 48 h A S EC50 (immobility) Dphni mgn 24 h A LC Originl publiction Originl publiction Stoughton et l Originl publiction Originl publiction Originl publiction Originl publiction Originl publiction Originl publiction Originl publiction Originl publiction Snchez- Byo nd Gok 2006 Snchez- Byo nd Gok 2006 Cox 2001 nd Felsot & Ruppert 2002 Snchez- Byo nd Gok 2006 Snchez- Byo nd Gok 2006 Snchez- Byo nd Gok 2006 Snchez- Byo nd Gok 2006 Snchez- Byo nd Gok 2006 Snchez- Byo nd Gok 2006 Snchez- Byo nd Gok 2006 Tisler et l Note wide spred between immobility EC50 nd LC50 Note wide spred between immobility EC50 nd LC50 Note wide spred between immobility EC50 nd LC50 Note wide spred between immobility EC50 nd LC50 Note lrge difference between EC50 nd LC50 Note lrge difference between EC50 nd LC50 Note lrge difference between EC50 nd LC50 Note lrge difference between EC50 nd LC50 88

90 Neonicotinoid Insecticides nd Birds d Imidcloprid Imidcloprid 95.4 FOR M Crustce Crustce Brnchiopo d Brnchiopo d Wter fle Wter fle Dphni mgn 24 h A LC Dphni mgn <2 4 hr LARVAE 48 h A S EC50 (immobility) Originl publiction One liner 2004, 2007; Pesticide Mnul, EPA 2007 ssessmen t Tisler et l Young 1990 (Byer) 1990 Imidcloprid >95% Crustce Brnchiopo d Wter fle Dphni mgn 48 h A LC Originl publiction Song et l Test t 20 degrees C Imidcloprid Crustce Brnchiopo d Wter fle Dphni mgn 48 h A LC Originl publiction Tisler et l Imidcloprid imidcloprid NR FOR M Crustce Crustce Brnchiopo d Brnchiopo d Wter fle Wter fle Dphni mgn 48 h A LC Originl publiction Dphni UNKNOW mgn NR N 48 h A EC50 > Agritox Tisler et l Byer Frnce Imidcloprid Crustce Brnchiopo d Wter fle Dphni mgn 48 h A LC Originl publiction Snchez- Byo 2009 Imidcloprid >95% Imidcloprid Imidcloprid Imidcloprid Imidcloprid Imidcloprid Imidcloprid Imidcloprid Anlytic l grde FOR M FOR M FOR M Crustce Crustce Brnchiopo d Wter fle Scud Crustce Amphipod Scud Crustce Amphipod Scud Dphni mgn 48 h A LC Gmmrus fossrum 48 h A S LC Gmmrus pulex 96 h A S LC Gmmrus roselli ADULTS 96 h A EC50 29 Crustce Amphipod Scud ylell ztec 48 h A EC Crustce 2-9 Amphipod Scud ylell ztec d 96 h A S LC Crustce 2-9 Amphipod Scud ylell ztec d 96 h A S LC Crustce Amphipod Scud ylell ztec 2-9 d 96 h A S LC Originl publiction Originl publiction Originl publiction Mohr et l EPA 2007 ssessmen t Originl publiction Originl publiction Originl publiction Song et l Lukncic et l Beketov nd Liess 2008b R. Boettger, pers. Comm. Englnd & Bucksth 1991 (Byer) 1991 Stoughton et l Stoughton et l Stoughton et l Test t 27 degrees C Drift seen t pprox. 1/10 of LC50 Stoughton et l. using the sme industry source give EC50 of 55 Observtion time extended to 28 d 89

91 Neonicotinoid Insecticides nd Birds Imidcloprid Imidcloprid Imidcloprid 95.9 Imidcloprid Imidcloprid Imidcloprid 99.50% FOR M Crustce Amphipod Scud ylell ztec 96 h A LC Crustce Amphipod Scud Crustce Crustce Crustce Crustce Brnchiopo d Brnchiopo d Brnchiopo d Wter fle Wter fle Wter fle Gmmrus pulex 28 d C S Dphni mgn 21 d C SR Dphni mgn 21 d C SR Dphni mgn 21 d C SR NOEC (swimming behviour) 64 NOEC (Reproductio n) 1800 NOEC (Reproductio n) 5000 NOEC (Reproductio n) 2500 Ilyocypris dentifer 24 h A S LC Stoughton et l Drft ssessmen t report from Germny (rpporteur Stte) 2005 EPA 2007 ssessmen t, EFSA 2008 Scientific Report Originl publiction Originl publiction Originl publiction Englnd & Bucksth 1991 (Byer) 1991 Young 1990 (Byer) 1990 Jemec et l Jemec et l Snchez- Byo nd Gok 2006 Reporting error? Much higher thn 48h vlue. NOEC for protein content of 2500 NOEC for protein content of 1250 Note lrge difference between EC50 nd LC50 Imidcloprid Imidcloprid 99.50% Imidcloprid 96.2 Imidcloprid 99.50% Imidcloprid 99.50% Crustce Crustce Crustce Crustce Crustce Brnchiopo d Mlcostrc Wter fle Opossum shrimp Dphni mgn 10 d C LC Ilyocypris dentifer 24 h A S Americmysis bhi C EC50 (immobility) NOEC (growth nd survivl) 0.6 Ilyocypris dentifer 48 h A S LC Ilyocypris dentifer 48 h A S EC50 (immobility) Originl publiction Originl publiction EPA 2007 ssessmen t Originl publiction Originl publiction Snchez- Byo 2009 Snchez- Byo nd Gok 2006 Wrd 1990 (Byer) 1990 Snchez- Byo nd Gok 2006 Snchez- Byo nd Gok 2006 Note lrge difference between EC50 nd LC50 Note lrge difference between EC50 nd LC50 Note lrge difference between EC50 nd LC50 90

92 Neonicotinoid Insecticides nd Birds Imidcloprid 99.50% Imidcloprid 99.50% Imidcloprid Imidcloprid Imidcloprid Imidcloprid Imidcloprid Imidcloprid Imidcloprid Imidcloprid Imidcloprid Confido r SL 200 Crustce Crustce Grss shrimp Grss shrimp Insect Midge Insect Midge Insect Midge FOR M Insect Midge FOR M Insect Myfly FOR M Insect Myfly FOR M Insect Midge Insect Midge FOR M Insect Midge Plemonetes pugio LARVAE 96 h A SR LC Plemonetes pugio ADULTS 96 h A SR LC Chironomus tentns LARVAE 48 h A EC50 69 Chironomus riprius 24 h A LC Chironomus riprius 28 d C S EC50 (emergence) 3.11 Chironomus riprius 28 d C S EC50 (emergence) 3.6 Epeorus longimnus LARVAE 24 h A S LC Epeorus longimnus LARVAE 96 h A S LC Chironomus riprius LARVAE 96 h A S EC Chironomus tentns LARVAE 96 h A S LC Chironomus tentns LARVAE 96 h A S LC Originl publiction Originl publiction EPA 2007 ssessmen t EFSA 2008 Scientific report EFSA 2008 Scientific report EFSA 2008 Scientific report Originl publiction Originl publiction Originl publiction Originl publiction Originl publiction Key et l Key et l Gglino 1991 (Byer) 1991 Imidcloprid Insect Midge Chironomus tentns LARVAE 28 d C EC50 (emergence) Originl publiction Stoughton et l Gglino Chironomus Stoughton 1991 Imidcloprid Insect Midge tentns LARVAE 96 h A LC et l (Byer) 1991 Leblnc et l FOR eptgeniid Leblnc et (unpublish Imidcloprid M Insect Myfly myfly' LARVAE 96 h A LC l ed thesis) FOR Chironomus Originl Leblnc et Imidcloprid M Insect Midge dilutus LARVAE 96 h A LC publiction l Gglino FOR Chironomus Stoughton 1991 Imidcloprid M Insect Midge tentns LARVAE 10 d C LC et l (Byer) 1991 Freshwt er Originl Song et l. Test t 27 Imidcloprid >95% Insect mosquito Aedes egypti 48 h A LC publiction 1997 degrees C Imidcloprid >95% Insect Freshwt Aedes egypti 48 h A LC Originl Song et l. Test t 20 Alexnder et l Alexnder et l Pestn et l Stoughton et l Stoughton et l Antipredtor behvious compromise d Observtion period extended to 28 d 91

93 Neonicotinoid Insecticides nd Birds Imidcloprid >95% Imidcloprid >98% Imidcloprid Imidcloprid Imidcloprid Imidcloprid 200 g/l Anlytic l grde Anlytic l grde Imidcloprid 20.00% Imidcloprid 20.00% Imidcloprid 20.00% Imidcloprid 20.00% Imidcloprid 20.00% Imidcloprid Imidcloprid Anlytic l grde Insect er mosquito Sltwter mosquito Insect Blck fly FOR M Insect Insect Blck fly Aedes teniorhynchus 48 h A LC50 13 Simulium vitttum 48 h A S LC Pteronrcys dorst LARVAE 14 d C LC Simulium ltigonium LARVAE 96 h A S LC Insect Myfly Betis rhodni LARVAE 48 h A S LC FOR M FOR M FOR M FOR M FOR M S (2X t microcos m microcosm C 21 d intervl) NOEC 0.6 Crustce Cldocer Ceriodphni EC50 Cldocer n dubi 48 h A SR (immobility) 572 Crustce Cldocer Ceriodphni EC50 Cldocer n reticult 48 h A SR (immobility) 5553 Crustce Cldocer Dphni EC50 Cldocer n mgn 48 h A SR (immobility) Crustce EC50 Dphni pulex 48 h A SR (immobility) Crustce Moin EC50 Cldocer mcrocop 48 h A SR (immobility) Insect Cddisfly FOR M Insect Midge Imidcloprid- 5-hydroxy DEG Insect Midge Imidcloprid- AMCP DEG Insect Midge Cheumtopsyc he brevilinet LARVAE 48 h A S LC Chironomus riprius LARVAE 48 h A S EC Chironomus riprius 24 h A LC Chironomus riprius 28 d C S EC50 (emergence) > publiction 1997 degrees C Originl publiction Originl publiction vn Dijk 2010 Originl publiction Originl publiction EFSA 2008 Scientific report Originl publiction Originl publiction Originl publiction Originl publiction Originl publiction Originl publiction Leblnc et l EFSA 2008 Scientific report EFSA 2008 Scientific report Song et l Overmyer et l Kreutzweiz er et l Beketov nd Liess 2008b Beketov nd Liess 2008b ysk et l ysk et l ysk et l ysk et l ysk et l Yokoym et l Azevedo- Pereir et l Test t 27 degrees C Geomen from 3 seprte tests bsed on mesured concentrtio ns Not found with ref provided Drift seen t pprox. 1/10 of LC50 Bsed on toxicity to chironomids nd Btide First instr results (most sensitive). Geomen of two popultions 92

94 Neonicotinoid Insecticides nd Birds Imidclopriddesnitro DEG Insect Midge Imidclopriddesnitroolefine DEG Insect Midge Imidclopridnitroso DEG Insect Midge Imidclopridure DEG Insect Midge Thicloprid 97.5 Insect Midge Thicloprid 44SC Thicloprid 99.3 Thicloprid 97.2 Thicloprid 97.2 Thicloprid Thicloprid Thicloprid Thicloprid Thicloprid FOR M FOR M FOR M FOR M Crustce Mlcostrc Opossum shrimp Chironomus riprius 28 d C S Chironomus riprius 28 d C S EC50 (emergence) EC50 (emergence) Chironomus riprius 24 h A LC Chironomus riprius 28 d C S EC50 (emergence) Chironomus 1st riprius in LARVAE 672 h C S EC <2 Americmysis 4 bhi hr LARVAE 96 h A F LC Crustce Mlcostrc Opossum shrimp Americmysis bhi <2 4 hr 96 h A F LC50 31 Crustce 14- Amphipod Scud ylell ztec h A S LC50 37 Crustce Brnchiopo Wter Dphni 1st d fle mgn in LARVAE 48 h A S EC Crustce Brnchiopo Wter Dphni d fle mgn 48 h A EC Crustce Crustce Crustce Brnchiopo d Brnchiopo d Wter fle Wter fle Isopod Crustce Amphipod Scud Dphni mgn 21 d C NOEC 580 Dphni mgn 24 h A S LC Asellus quticus 24 h A S LC Gmmrus pulex 24 h A S LC NR NR EFSA 2008 Scientific report EFSA 2008 Scientific report EFSA 2008 Scientific report EFSA 2008 Scientific report One liner 2005 BCA 1996 One liner 2007 WLI 1997 One Liner One Liner One Liner Footprint DB Footprint DB Originl publiction Originl publiction Originl publiction Beketov nd Liess 2008 Beketov nd Liess 2008 Beketov nd Liess 2008 Extended post tretment observtion period - evidence of delyed effects Extended post tretment observtion period - evidence of delyed effects Extended post tretment observtion 93

95 Neonicotinoid Insecticides nd Birds Thicloprid Thicloprid Thicloprid Thicloprid Thicloprid Thicloprid Anlytic l grde FOR M Insect Drgon fly FOR M Insect Cddisfly FOR M Insect Blck fly Sympetrum strioltum LARVAE 24 h A S LC Notidobi ciliris LARVAE 24 h A S LC Simulium ltigonium LARVAE 24 h A S LC FOR M Insect Mosquito Culex pipiens LARVAE 24 h A S LC FOR M Insect Midge Crustce Amphipod Scud Chironomus tepperi LARVAE 24 h A LC Gmmrus pulex 96 h A S LC Thicloprid Anlytic l grde Insect Myfly Betis rhodni LARVAE 96 h A S LC Thicloprid Crustce 14- UNKNOW (Metbolite) 97.4 DEG Amphipod Scud ylell ztec 21 N 96 h A S LC Thicloprid (Sulfonic Acid Crustce Brnchiopo Wter Dphni 1st metbolite) 89.9 DEG d fle mgn in LARVAE 48 h A S LC50 > NA NA Thimethox m 98.6 Crustce Brnchiopo d Wter fle Dphni mgn <2 4 LARVAE 48 h A S EC50 > N.A. N.A Originl publiction Originl publiction Originl publiction Originl publiction Beketov nd Liess 2014 Originl publiction Beketov nd Liess 2008 Beketov nd Liess 2008 Beketov nd Liess 2008 Beketov nd Liess 2008 Stevens et l Beketov nd Liess 2008b Beketov nd Liess 2008b Originl publiction One liner 2005 BCA 1997 One Liner One liner 2007 NCP 1996 period - evidence of delyed effects Extended post tretment observtion period - evidence of delyed effects Extended post tretment observtion period - evidence of delyed effects Extended post tretment observtion period - evidence of delyed effects Extended post tretment observtion period - evidence of delyed effects 94

96 Neonicotinoid Insecticides nd Birds Thimethox m 99.2 Thimethox m Thimethox m Thimethox m WG25 Thimethox m 98.6 Thimethox m Thimethox m Thimethox m hr <2 Crustce Mlcostrc Opossum Americmysis 4 shrimp bhi hr LARVAE 96 h A F LC Crustce seed Ostrcod shrimp Choborus sp. 48 h A EC Insect Cloeon sp. 48 h A EC50 14 FOR Crustce Brnchiopo Wter Dphni M d fle mgn 48 h A EC50 > N.A. N.A. FOR Crustce Brnchiopo Wter Dphni M d fle mgn 48 h A EC N.A. N.A. Crustce Brnchiopo Wter Dphni d fle mgn 21 d C NOEC Insect Midge Insect Midge Thimethox m Crustce Thimethox m Crustce Brnchiopo Wter CGA DEG d fle Thimethox m CGA DEG Insect Midge Thimethox m Crustce Brnchiopo Wter CGA DEG d fle Thimethox m NOA DEG Crustce Brnchiopo d Wter fle Thimethox m NOA DEG Insect Midge Chironomus riprius 30 d C NOEC (emergence) 10 Chironomus riprius h A EC50 35 Americmysis bhi 96 h A EC Dphni mgn 48 h A EC50 > Chironomus riprius 28 d C NOEC (emergence) 0.67 Dphni mgn 48 h A EC50 > Dphni mgn 48 h A EC NOEC (emergence & Chironomus development riprius 28 d C ) > 1000 One liner 2007 WLI 1997 EU 2006 review EU 2006 review EU 2006 review EU 2006 review EU 2006 review EU 2006 review PMRA 2007 PMRA 2007 EU 2006 review EU 2006 review EU 2006 review EU 2006 review PMRA 2007 gives the chronic EC50 s 11 Given s cute endpoint for exposure period not stted Given s cute endpoint for exposure period not stted. Assumed to be 96 h bsed on US info from sme test 95

97 Neonicotinoid Insecticides nd Birds Thimethox m NOA DEG Crustce Brnchiopo d Wter fle Thimethox m NOA DEG Insect Midge Dphni mgn 48 h A EC50 > NOEC Chironomus (developmen riprius 28 d C t) EU 2006 review Altricil chicks, wikimedi.org 96

Treatment Spring Late Summer Fall 0.10 5.56 3.85 0.61 6.97 3.01 1.91 3.01 2.13 2.99 5.33 2.50 1.06 3.53 6.10 Mean = 1.33 Mean = 4.88 Mean = 3.

Treatment Spring Late Summer Fall 0.10 5.56 3.85 0.61 6.97 3.01 1.91 3.01 2.13 2.99 5.33 2.50 1.06 3.53 6.10 Mean = 1.33 Mean = 4.88 Mean = 3. The nlysis of vrince (ANOVA) Although the t-test is one of the most commonly used sttisticl hypothesis tests, it hs limittions. The mjor limittion is tht the t-test cn be used to compre the mens of only

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