205 is tested in the M. persicae sity of British Columbia, Vancouver er, Department of Environmental Sci- 2008 Society of Chemical Industry (Sulzer),isanimportantinsect and Murray c (: c Myzuspersicae T Astatkie . a,b t 2008 Published online in Wiley Interscience: 16 December 2008 llowing exposure to . No other measures for Department of Environmental Sciences, Nova Scotia Agricultural College, Truro B2N 5E3, NS, Canada Department of Engineering, Nova Scotia AgriculturalNS, Canada College, Truro B2N 5E3, Correspondence to: G Christopher Cutl ences, Nova Scotiamail: [email protected] Agricultural College, Truro B2N 5E3,Faculty of NS, Land and Canada. Food Systems, E- Univer V6T 1Z4, BC, Canada ecticide concentrations over time. Here, the hypothesis that ∗ c a b pplications is often attributed to natural enemy disturbance, n sublethal concentrations of insecticide, almost all measured This ispesticide certainly concentrations plausible maydegradation given occur that of followingcoverage exposure the environmental on to pesticide, individualpoor sublethal or plants spray via (e.g. distributionfields. under through heterogeneous Hormesis surfaces the resulting spatial only canopy) of in and leaves, result throughout pestlead in to resurgence additional increased could pesticide treatments,non-target not crop/commodity potentially exacerbating impacts, damageenvironmental insecticide but contamination. resistance Increased also gain, survival, development larval fecundity and weight and reproduction following sublethal dose ments suggest that exposure to sublethal concentrations of M. persicae 5–8 Myzus persicae ; Hemiptera; ; hormesis; imidacloprid; azadirachtin; sublethal effects Krilen Ramanaidu, ∗ 3,4 a,b The threshold model assumes Myzus persicae 1,2 : 205–209 www.soci.org 65 a 2009; green ;

05) stimulatory response was recorded for F2 production fo . 0

< 2008 Society of Chemical Industry The ramifications of hormesis in insect pest management P c may be significant.by While insecticides the isinsect pest the reduction resurgence following most of insecticideresponses treatment, commonly natural hormetic in cited the enemies pests explanation may for be an alternative mechanism. Pest Manag Sci pest of many crops worldwide that mayexposure be to exposed low to sublethal concentrations ins of imidacloprid and azadirachtin can induce hormetic responses in Toxicologists havedose–response generally relationships. used two models to describe 1INTRODUCTION and azadirachtin to sublethal concentrations of imidacloprid Abstract BACKGROUND: Resurgence of insect pests following insecticide a Aphididae), reproduction during exposure but hormesis could be an alternative or additional mechanism. Green peach aphid, G Christopher Cutler, (www.interscience.wiley.com) DOI 10.1002/ps.1669 Green peach aphid, Research Article Received: 17 July 2008 Revised: 12 August 2008 Accepted: 24 Augus there is a dose–responsesures threshold induce above a biological which effect, and chemical below expo- whichlinear none non-threshold occurs. model The has also been employedby – regulatory particularly agencies tochemicals extrapolate – risks and assumes to that verytionship at low between dose low doses and risk, doses of terminating there at zero.have is These been models a a cornerstone linear of rela- allinvaluable facets for of establishment toxicology of and harmful have exposure been limitstive doses and of effec- chemicals. However, there is also very strongof evidence a hormetic dose response,tion characterized and high-dose by inhibition. low-dose Hormesis has stimula- beensuch documented a for wide range of organisms, endpointsstressors and that physical/chemical it ismechanism, but not rather a thought general to overcompensation responsedisruption be to (e.g. a toxicity) the in product homeostasis. of any single BIsman laboratory. RESULTS: When were exposed to potatoendpoints leaf – discs dipped adult i longevity,( F1 production, F1hormesis were statistically survival significant, but and other trends F2 of hormetic response production were –CONCLUSIONS: consistently were observed. Given affected, that andof variable concentrations a distribution over statistically and timeimidacloprid degradation significant and and azadirachtin of space, could these stimulate insecticides reproduction laboratory in in experi the field would result in aKeywords: wide range . 16 et al Myzus : 205–209 65 20 2009; 1) or significant . 0 C,16:8hlight:dark < ◦ 2 (Table 2), but significant ± -value P < Pest Manag Sci 05 . M. persicae to be AR(1). 18 , 48 and 72 h old, were transferred to 5% RH). A high RH was maintained in the plastic ± M. persicae 05), the least-squares means were separated at . 0 Data that did not meet these assumptions were 05 level. To facilitate easy reading, backtransformed . 0 < 19 adult longevity was significantly affected by imidacloprid = α For all responses, the normal distribution and constant variance Adult fecundity was not significantly influenced by azadirachtin -value -values for tests of significance among factors incorporated in P the means are presented for theprocedure in transformed SAS responses. was used The to MIXED complete the analyses. ( assumptions on the errorresiduals. terms were verified by examining the concentration (Table 2), butaffected survival of by isolated F1 exposure(Table nymphs 1). to was While both significantly imidacloprid lower and fecundity azadirachtin was found with 3RESULTS P the statistical modelspersicae are presentedconcentration, in but Tables 1 notconcentrations and 2. by (Table 1). exposurestimulatory effect to Although on adult longevity different as there aconcentrations azadirachtin result of of imidacloprid, was exposure a to statistically significant low effect adetected was at trend the highest ofreduced imidacloprid longevity concentration was a observed only, (Table where influenced 3). Similarly, fecundity imidacloprid of adult effectswerefoundatthehighestimidaclopridconcentrationsonly, wheredecreasedproductivityoccurred(Table 3).ThenumberofF1 progeny produced was found to vary with day for(Table both insecticides 2), although no consistent trendsshown). were observed (data not Discs were replaced inAdult each survival dish was every recorded 2progeny days, every per for day, dish up while was to thethe recorded 8 number experiment, days. every of five second F1 each day. F1 dish and On nymphs moved Day to were separate 2 petritreated randomly dishes of containing with leaf selected insecticide discs as from describedthe above. F1 The nymphs was development tracked of for anothersurvival 8 and days, the after number which time of F1 F2 nymphs produced were recorded. 2.4 Experimental designFor and statistical both methods imidaclopridrandomizedcompleteblockdesign,withinsecticideconcentration and azadirachtin, thebeing experiment was the a mainbioassay replications factor (experimental replicates) of were each initiated interest.on a For separate eachEach day, insecticide, bioassay which consisted three of was atinsecticide considered least concentration. five the Where replicate data blocking petriwere on dishes factor. progeny per collected development overanalysis multiple was time conducted.the points, For error repeated the terms measures with repeated were constant measures assumed variance, to analysis, appropriate but have not covariance to a structuredependence be normal was that identified independent. distribution represents The most the type of square-root transformed. When concentration and/orwere day effects marginally significant (0 dishes containing eightapterous ventilation adult holes inthe discs the of bottom. eachwere Two dish placed using in atowel clear and fine held plastic in paintbrush, a containers growth and chamber lined (25 the with dishes moist paper photoperiod, 65 containers by periodically adding water to the paper towel. 1 − gL µ M. per- www.soci.org GC Cutler 5% RH) potting  ± (Sulzer), is 2008 Society of Chemical Industry azadirachtin the goal was 1 c − has widespread 3 gL L.) in the University were reared µ 16 (AZA 1.2% ME; Am- 1 − Myzus persicae Chinensis Myzuspersicae for azadirachtin. Concentrations 240F; Bayer CropScience Canada, ssp. 1  L. (cv. Warba), was grown in a − gL behavior or reproduction following the µ which determined the NOAEC for aphids (Admire 17 1 − rapa 05), C, 16 : 8 h light : dark photoperiod, 65 imidacloprid and 10–1000 used in this study were from a wild population 5,7,9–12 . ◦ 0 1 2 − M. persicae = ± gL α µ Solanum tuberosum . During preparation, two drops of emulsifier (Triton 13–15 1 and are used against this insect in a variety of cropping 1–30 − . In the present study, the hypothesis that exposure to low con- Myzus persicae leaf discs (20 mm diameter) were cut using a stainless economic importance, and its short lifespanreproduction and parthenogenetic make it aexposure useful to test sublethal insect insecticidethe to test concentrations. examine compounds Field have effects ratessicae demonstrated of of efficacy against systems, but they are veryaction. different in their insecticidal modes of 2.3 Exposure toAs treated leaf chemical discs hormesisservable becomes adverse more effect likely concentration below (NOAEC), the no ob- X-100; BDH Chemicals, Toronto, ON) per 100suspension. mL The control was solution added consisted to of the wateronly. and emulsifier using methodologies of Lowery and Boiteau. 2.2 Chemicals andImidacloprid solution 240 preparation g L on potato for approximately 3No weeks change before in use inswitch experiments. from pak choi to potato was observed. exposed to treated potato leaf discs to be approximately 10 to measure aphidtions response below at theexposed to NOAEC. several treatments To and insecticide controlsroot-transformed determine as concentra- described adult NOAECs, below. longevity Square- aphidsanalyzed and by were one-way reproduction ANOVA, dataration followed test by were ( a Tukey means sepa- tested under laboratory conditions. centrations of imidacloprid and azadirachtin canresponses induce hormetic in the green peach aphid, vac Chemicalpended Corporation, in deionized Newport waterAI to Beach, L give stock CA) solutions were of 1000 mg sus- www.interscience.wiley.com/journal/ps for imidacloprid and 300 22.1 MATERIALS AND METHODS Plant andPotato, insect culture greenhousein100 mmdiameterpotscontaining Pro-Mix exposure to insecticides have beenbeneficial insects. reported in several pest and soil. Soluble fertilizer (N20-P20-K20)plants were was watered given as needed. at Foliageexperiments planting, used was for from and insect plants rearing 4–6 or weeks old. of 0 were therefore used in theone concentration hormesis above the experiments, NOAEC incorporating and severaltions other concentra- up to 100-fold below the NOAEC for each compound. steel cork borer. Discs were individuallyazadirachtin dipped solution in for imidacloprid approximately or 5 s1 and h. air Two dried for overlapping about discs were each added to tight-sealing petri Calgary, AB) and azadirachtin 12 g L infesting pak choi ( of British Columbiawere reared horticulture in petri greenhouse. dishes on excised Collectedchamber potato leaf (25 discs aphids in a growth

206 207 1 a − 05 . c 05; 0 . gL 0 µ F2 = = 3 per F1 . progeny α 008 α . Myzus persicae a,c 24 F2 progeny per F1 F1 survival resurgence in the field a a,b in preliminary experiments. 029 0 . 0 F1 M. persicae progeny is often a late-season colonizer of per adult and their progeny were exposed to sublethal concentrations of imidacloprid. 05), trends of stimulatory responses in www.interscience.wiley.com/journal/ps a,b . 0 this species could be exposed to sublethal rvival and fecundity (number of F2 per F1) were were placed on treated potato leaf discs, and 6.4a 2.8b 2.4cd 3.2ab Adult = M. persicae (days) 23 longevity 0.11–0.13 0.21–0.42 0.37–0.47 0.39–0.76 0.607 α M. persicae As Adult longevity F1 survival 22 Myzus persicae Least-squares means of biological endpoints following M. persicae ) 1 a − e d r multiple means comparison are in bold gL Adult NOAEC; obtained by one-way ANOVA SEM ranges are due to differences in the number of values used to Data were square-root transformed before analysis. Backtransformed Longevity of five randomly selected F1 nymphs on treated foliage When adult µ calculate the means. fecundity was recorded every 2 days. Means sharing the same letter are not significantly different ( a b c d e Table 3. exposure of 00.10.31.03.010.0 5.4a 5.7a 6.7a 6.6a 3.3a 6.7a 3.7a 3.4a 3.6a 3.7ab 4.2a 3.4a 4.2a 2.8bc 3.1bc 3.8ab 3.4ab 4.2a 2.9bc 3.5ab was tracked for 8 days,recorded. and the relative production of F2 progeny was means are presented. SEM values are not backtransformed 30.0SEM 3.6b 1.9b 1.0c 1.7c LSD test) Concentration ( to potato leafimidacloprid discs or treated azadirachtin,response a with – as statistically sublethal significant per concentrations hormetic means of separation tests at the concentrations of imidacloprid onon potato the foliage, plant both and temporally spatially the as authors found the no season reports of progresses. Although following exposure to sublethal concentrations of imidaclopridazadirachtin, or organochlorine and organophosphorus insecticides with relatively long persistence haveresurgence been when shown residues to reach cause a sublethal aphid level. imidacloprid was significantlyuntreated greater control, than indicatinggeneration that a reproduction found from stimulatory in continuousAlthough effect the insecticide no exposure. on other second- were statistically found significant (at other hormetic responses measures atconsistently sublethal observed. Similar insecticide results concentrations have were been reported by of the plant. potato in Canada, level – was found forof only F2 one biological progeny endpoint: produced the number per F1 adult exposed to 0 032 . ration and experimental replicate (blocking factor), on adult 1 − F2 progeny per F1 gL µ 001 . 3 a . 0.123 a 2008 Society of Chemical Industry c 001 0 fecundity and F1 d foliage for 7 days, after which time their su . Imidacloprid Azadirachtin ory conditions. Effects requiring furthe F1 progeny per adult 001 087 0 Myzuspersicae . . 0 0 008 0.206 0.249 0.001 0.001 0.001 001 0 . e (blocking factor), day (repeated 0 : 205–209 65 that have high reproductive rates and short licate 0.001 0.001 over subsequent generations during exposure to 2009; -values for the effects of imidacloprid/azadirachtin con- -values for the effects of imidacloprid/azadirachtin concent and sublethal insecticide exposure www.soci.org P P imidacloprid is often applied as a drench or seed concentration 0.370 0.201 21 × M. persicae M. persicae The number of progeny per adult aphid was recorded every 2 days, Randomly selected F1 nymphs were held on treate Day a centration, experimental replicat measure) and their interaction on adult Source of variationExperimental rep Concentration Day Imidacloprid Azadirachtin Table 2. a longevity and F2 production, under laborat Source of VariationExperimental replicateConcentration Adult longevity F1 0. survival survival under laboratory conditions. Effects requiringmeans further comparison multiple are in bold Table 1. for 6 days. recorded. M. persicae Pest Manag Sci Hormesis in insectsinsecticide has been documented for exposed several taxa and compounds. Most to of these studies, sublethal however, have examined effectsgrowth concentrations on survival, and/or of fecunditypresent of laboratory study a an singleon attempt was cohort made of to assess insects. effects In the life cycles. Moreover,exposure to in sublethal concentrations the ofIn toxin case addition could of occur to often. world, imidacloprid, being prolonged the most widely used insecticide in the 4 DISCUSSION insecticideswithdifferentmodesofaction.Suchmultigenerational evaluations of sublethal effects arelike especially relevant for insects concentration was foundazadirachtin experiments, (Table significant 3). block effects were Infor observed some both factors, imidacloprid indicatingexperimental replicates differences and (Tables in 1 and response 2). among the exposure to highprolonged survival during exposure concentrations, to low concentrations acompound of each was non-significant observed (Tables trend 3both and insecticides 4). of The also concentrationof had of F2 a significant progenycase effect of produced on imidacloprid per the a F1 number stimulatory adult response (Table at 1), the and 0 in the treatment for systemic uptakebiological by activity the of plant,imidacloprid the which in potato extends compound. foliage following the in-furrow/seed For treatment applications example, decrease residues of aroundthereafter are 6 weeks unevenly distributedlower after throughout residues application, the occurring plant, and in with new foliage in the upper portion . Pest and et al 7 ,onrice. Toxicol Sci : 205–209 (Stal, 1860) :1169–1174 :1–8 (2005). 65 :7–12 (1968). 84 204 61 The occurrence Environ Entomol 4 2009; :941–947 (2003). Although it is highly (Coleopt.: Curculionidae). Nilaparvata lugens 22 24 :266–269 (1998). such as citrus thrips affecting insecticide-induced J Econ Entomol ,onrice. Supputius cincticeps 17 J Econ Entomol ology rethinks its central belief. of pesticide-induced hormesis of 26,34 duced hormoligosis of citrus thrips Pest Manag Sci chs EA, Effect of sub-lethal doses enings: the rebirth of hormesis as a Crop Prot 26 :378–411 (2005). Toxicol Appl Pharmacol (Say) (Coleoptera: Chrysomelidae). 138 could result in stimulated reproduction Sitophilus granarius :691–692 (2003). :147–152 (1958). Hum Exp Toxicol :773–777 (1980). 1 but nonetheless has been reported in aphids 9 421 8 Nilaparvata lugens :1060–1068 (2005). 61 M. persicae Environ Pollut :246–250 (2003). :778–780 (1980). central pillar of toxicology. Nature (London) more common than the threshold71 model in toxicology. hormesisasafundamentaldoseresponsemodelinthetoxicological sciences. insects and mites. (Thysanoptera: Thripidae) fecundity. (1991). resurgence of the brown planthopper, Environ Entomol multiplication rate of Entomol Exp Appl 9 induced hormesis on the predator (Heteroptera: Pentatomidae). sublethal toxicity of novaluron, a novel chitinLeptinotarsa synthesis decemlineata inhibitor, to Manag Sci of threeplanthopper, insecticides on the reproductive rate of the brown It is unknown whether sublethal exposures of imidacloprid or 1 Calabrese EJ, Toxicological awak 2 Calabrese EJ and Baldwin LA, Toxic 3 Calabrese EJ and Baldwin LA, The hormetic dose–response model is 4 Calabrese EJ, Paradigm lost, paradigm found: the re-emergence of 8 Chelliah S and Heinrichs EA, Factors 9 Kuenen DJ, Influence of sublethal doses of DDT upon the 5 Luckey TD, Insecticide6 hormoligosis. Morse JG, Agricultural implications 7 Morse JG and Zareh N, Pesticide-in 11 Zanuncio TV, Serrao JE, Zanuncio JC and Guedes RNC,12 Permethrin- Cutler GC, Scott-Dupree CD, Tolman JH and Harris CR, Acute and 10 Chelliah S, Fabellar LT and Heinri azadirachtin to andsubsequentpopulationresurgenceinthefield.Theoccurrence of pesticide-induced resurgence may becompared with less other common insect in pests, aphids of population heterogeneityfurther complicate study and of the phenomenon, temporal and maydifferences explain shifts the the authors detected in among the response bioassay replicates. during sublethal insecticide exposure. improbable that such precisepresent study dosage would be of uniformly distributed throughout insecticide a potato field, used it in is the very likelyactive that ingredients variable distribution in and or degradation onwould of result plants, in both insect spatially populations being andof exposed insecticide temporally, to concentrations a throughout wide a growing range season.that Given genetic variation in field populations isthat naturally of greater than laboratory strains,field may stimulated be more population pronounced. growth in the ACKNOWLEDGEMENTS The authors thankimidacloprid and Amvac Bayer Chemical Corporation CropScienceazadirachtin for used in providing Canada this the study. This for researchNSERC was Post-Doctoral supported providing Fellowship by to an GCCGrant and to an MBI. NSERC Discovery REFERENCES typically, only adifficult modest confidently hormetic towhen distinguish response from is a normal seen,experimental variation, stimulatory which designs even therefore trend is requireresource allocation is to extraordinary reduce experimental time error. repeatedly and evident. Adequate brown plant hopper, 28 c 05; . Such 0 F2 www.soci.org GC Cutler 30 = per F1 progeny α 2008 Society of Chemical Industry c c with exposure to F1 In the same study, survival thesestudiesexposed 25 Although others have 26 Most problematic is that, 27–30 a,b which manifested itself as in preliminary experiments. M. persicae 1,4 survival. 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SEM value is not backtransformed. d e a b c 010.030.0100.0300.0 5.3a 5.3a 6.0a 4.5a 3.2a 3.7a 4.1a 3.0a 2.9ab 3.0ab 3.8a 2.4bc 3.3ab 3.2ab 4.0a 3.2ab Table 4. exposure of Means sharing the same letter are not significantly different ( Concentration ( LSD test) was tracked for 8 days,recorded. and the relative production of F2 progeny was treatedcabbageleaveshadnoincreasedreproduction,stimulation of reproduction was seen in the subsequent F1 generation. trends in populationto growth sublethal insecticide were concentrations. observed during exposure aphids to fullhormesis field – a rates stimulatory effect of of stressorsinhibitory/toxic at active low symptoms levels at ingredient, along higher with doses likely – as precluding a mechanism. in two of the aforementioned studies, stimulationwas of reproduction delayed afteralthough initial adult insecticide application. 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For example, LC azadirachtin increased increased allocation ofwhen resources they became towards adults. reproductive output generally more sensitive thanpossible that adults in the present to study F1 toxicant nymphsimidacloprid exposed exposure, to sublethal concentrations it is for overcompensated their physiologically disrupted homeostasis, applications ofthe the LD synthetic pyrethroid fenvalerate around imidacloprid also resultedit in increased was reproduction,Myzus although not persicae clear if this effect was statistically significant. azinphosmethylandotherinsecticides,

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