LESA #676494, VOL 47, ISS 12 Concentration-mortality responses of Myzus persicae and natural enemies to selected insecticides LEANDRO BACCI, JANDER F. ROSADO, MARCELO C. PICANC ¸O, ELISEU J. G. PEREIRA, GERSON A. SILVA, AND J ´ ULIO C. MARTINS QUERY SHEET This page lists questions we have about your paper. The numbers displayed at left can be found in the text of the paper for reference. In addition, please review your paper as a whole for correctness. Q1. Au: Ref 7 skipped in text citations. Please cite 7 between and 8, re-numbering refs if necessary so that they can be cited in order. Q2. Au: Ref 17 skipped. Please cite 17 between 16 and 18, re-numbering refs if necessary, so refs are cited in order. Q3. Au: Is running head OK? Must be fewer than 50 characters. Q4. Au: Please clarify “... and this finding agrees with a previous study, in which the insecticide was incompatible with conversation biological control in potato because of its lower toxicity to Phthorimaea operculella (Zeller) ...” Should conversation be conservation? Q5. Au: Please add publisher’s location city for ref 37. TABLE OF CONTENTS LISTING The table of contents for the journal will list your paper exactly as it appears below: Concentration-mortality responses of Myzus persicae and natural enemies to selected insecticides Leandro Bacci, Jander F. Rosado, Marcelo C. Picanc ¸o, Eliseu J. G. Pereira, Gerson A. Silva, and J´ ulio C. Martins
Transcript
LESA #676494, VOL 47, ISS 12
Concentration-mortality responses of Myzus persicae andnatural enemies to selected insecticidesLEANDRO BACCI, JANDER F. ROSADO, MARCELO C. PICANCO, ELISEU J. G. PEREIRA, GERSON A.SILVA, AND JULIO C. MARTINS
QUERY SHEET
This page lists questions we have about your paper. The numbers displayed at left can be found in the text of the paperfor reference. In addition, please review your paper as a whole for correctness.
Q1. Au: Ref 7 skipped in text citations. Please cite 7 between and 8, re-numbering refs if necessary so that they can becited in order.
Q2. Au: Ref 17 skipped. Please cite 17 between 16 and 18, re-numbering refs if necessary, so refs are cited in order.Q3. Au: Is running head OK? Must be fewer than 50 characters.Q4. Au: Please clarify “. . . and this finding agrees with a previous study, in which the insecticide was incompatible
with conversation biological control in potato because of its lower toxicity to Phthorimaea operculella (Zeller) . . .”Should conversation be conservation?
Q5. Au: Please add publisher’s location city for ref 37.
TABLE OF CONTENTS LISTING
The table of contents for the journal will list your paper exactly as it appears below:
Concentration-mortality responses of Myzus persicae and natural enemies to selected insecticidesLeandro Bacci, Jander F. Rosado, Marcelo C. Picanco, Eliseu J. G. Pereira, Gerson A. Silva, and Julio C. Martins
Concentration-mortality responses of Myzus persicae andnatural enemies to selected insecticides
LEANDRO BACCI1, JANDER F. ROSADO2, MARCELO C. PICANCO2, ELISEU J. G. PEREIRA2, GERSONA. SILVA3 and JULIO C. MARTINS2
1Departamento de Engenharia Agronomica, Universidade Federal de Sergipe, Aracaju, SE, Brazil52Departamento de Entomologia, Universidade Federal de Vicosa, Vicosa, Brazil3Departamento de Fitotecnia, Universidade Federal de Vicosa, Vicosa, Brazil
The toxicity of six insecticides was determined for the peach-potato aphid, Myzus persicae (Hemiptera: Aphididae), and some of itsnatural enemies – the predatory beetles Cycloneda sanguinea (Coccinellidae) and Acanthinus sp. (Anthicidae), and the wasp parasitoidDiaeretiella rapae (Aphidiidae). Natural enemies from these groups are important natural biological control agents in a number ofagroecosystems, and insecticides potentially safe to these non-target organisms should be identified using standardized tests. Thus,concentration-mortality bioassays were carried out with both the aphid and its natural enemies to assess the toxicity and selectivityof acephate, deltamethrin, dimethoate, methamidophos, methyl parathion, and pirimicarb. The latter insecticide was highly selectiveto all natural enemies tested, and its LC90 for M. persicae was 14-fold lower than the field rate recommended for control of the aphidin brassica crops. Methyl parathion also showed selectivity to C. sanguinea and Acanthinus sp., but not to D. rapae. Acephate wasthe least potent insecticide against M. persicae and was equally or more toxic to the natural enemies relative to the aphid. Pirimicarband methyl parathion were efficient against M. persicae and selective in favor of two of the natural enemies tested. Acanthinus sp.and C. sanguinea were more tolerant to the insecticides than was the parasitoid D. rapae. This study shows that there are selectiveinsecticides that may be compatible with conservation of natural enemies in brassica crops, which is important practical informationto improve integrated pest management systems in these crops.
The peach-potato aphid, Myzus persicae (Sulzer)(Hemiptera: Aphididae), is a polyphagous pest that at-tacks numerous crops worldwide.[1] This insect causes se-25vere damage in brassica crops by sucking the plant sap,injecting toxins, and transmitting viruses.[2,3,4] Unlike intemperate regions, in Brazil, M. persicae colonies consistcompletely of females, and reproduction does not involvemating or egg laying (thelytokous parthenogenesis). Fe-30males give birth to live female nymphs that rapidly reachthe reproductive phase. Dispersive alate morphs are pro-duced when population density becomes high such thatnew hosts are rapidly colonized. Generations are overlap-ping and continuous throughout the year, and life cycle35duration is usually short, ranging from 16 to 50 days.[5] Be-cause of this high capacity for reproduction and dispersion,
Address correspondence to Julio C. Martins, Campus Vicosa,Federal University of Vicosa, Vicosa, MG 36570-000, Brazil;E-mail: [email protected]; E-mailReceived October 21, 2011.
high population densities are easily attained and efforts tosuppress them are often necessary.
Since the early 1950s, the use of insecticides has been the 40main method used to suppress M. persicae populations,which has selected aphid populations for resistance anddisrupted the natural biological control.[6,8] Disruption of Q1biological control by broad-spectrum insecticides causesresurgence of aphid populations and an increase in the in- 45festation levels by secondary pests.[6,9,10] As a consequence,growers tend to increase rates of insecticide use, resultingin high cost-benefit ratio and environmental contamina-tion. Selection of less harmful insecticides to the environ-ment is one of the strategies commonly used in programs of 50Integrated Pest Management (IPM). Reinforcing this phi-losophy, the concern about safety use of this practice inagriculture has increased.[11,12] New compounds have beendeveloped in response to such demands.[13,14] However, pes-ticides continue to be regarded as pollutants of deliberate 55use, and so remains the concern associated with their use.
Natural enemies can impose high levels of mortalityin aphid populations.[15] Coccinellid and anthicid preda-tors and braconid parasitoids are too recognized asimportant mortality factors of aphids.[16,18] Cycloneda Q260
2 Bacci et al.
sanguinea (L.) (Coleoptera: Coccinellidae) and Acanthinussp. (Coleoptera: Anthicidae) are often observed occurringin high density in fields cultivated with brassicas. Simi-larly, Diaeretiella rapae (McIntosh) (Hymenoptera: Bra-conidae) has been reported as an important agent of natu-65ral biological control of M. persicae populations in brassicacrops.[2,8]
Conservation of natural enemies in Integrated Pest Man-agement programs is enhanced through habitat manipula-tion and/or use of selective insecticides.[19,20] The selectivity70of insecticides can be classified as ecological and physiolog-ical.[21] Ecological selectivity is related to the different waysto apply insecticides as a means to minimize exposure ofnatural enemies to the insecticide.[21] Physiological selectiv-ity is based on the use of insecticides that are more toxic to75the target pest than the natural enemies.[22]
Because insecticides are likely to remain a major com-ponent of pest suppression for M. persicae, minimizing theeffects of insecticides on natural enemies will require moreselective approaches for use of broad-spectrum insecticides80and/or more selective products. Concentration-mortalitycurves can be used to compare the insecticide toxicity todetermine which insecticide is more toxic for a particu-lar species or population, and therefore, select insecticidesand/or concentrations that are harmless to natural enemies85and efficient to manage the insect-pest population. Stud-ies determining insecticide selectivity to natural enemies ofM. persicae in brassicas are limited.[23,24] Therefore, in thepresent study, we conducted a series of bioassays and usedconcentration-mortality curves to determine insecticide (i)90toxicity to M. persicae, (ii) selectivity to the predators C.sanguinea and Acanthinus sp. and parasitoid D. rapae, (iii)potency to M. persicae and natural enemies, and (iv) toler-ance of natural enemies to the insecticides used for controlof M. persicae. The results of this research have impor-95tant practical implications regarding insecticides that canbe used to manage M. persicae while conserving naturalenemies in brassica crops.
Materials and methods100
Insects
Individuals of M. persicae were maintained in a greenhousein the campus of the Federal University of Vicosa (UFV),Vicosa (20o48′45′′S, 42o56′15′′W; altitude 600m), MinasGerais State, Brazil. To initiate the colony, leaves of cabbage105(Brassica oleracea var. capitata) infested with M. persicaewere collected in fields free of insecticide applications inthe UFV experimental station. The leaves collected wereinspected for removal of other aphid species and parasitoid-infected nymphs, and then placed on leaves of potted110cabbage plants inside cages (50 × 50 × 50 cm) built withwood frames and covered with organza. Cabbage plantswere produced by transplanting seedlings in 3 L plastic
pots using three parts of soil and one part of livestockcattle manure as the substrate and were maintained in the 115greenhouse until use free of pests and diseases. Old cabbageplants were regularly replaced by new plants free of aphids.
Parasitized aphids were periodically removed and trans-ferred to new cages to isolate D. rapae, and the newlyemerged parasitoids were used in the bioassays. Adults of 120D. rapae, C. sanguinea and Acanthinus sp. were collecteddaily from cabbage fields. The field collections were per-formed using aspirators and plastic containers. The natu-ral enemies were collected from random plants in the samecabbage fields utilized to collect M. persicae. Specimens of 125each natural enemy were stored in 4-mL vials with 70 % ofalcohol and sent to taxonomists for identification.
Insecticides
Six insecticides were utilized in the bioassays: acephate (Or-thene 750 BR, Arysta LifeScience do Brasil, Sao Paulo, SP), 130deltamethrin (Decis 25 CE, Bayer CropScience, Sao Paulo,SP), dimethoate (Perfekthion, Basf S.A., Sao Bernardo doCampo, SP), methamidophos (Tamaron BR, Bayer Crop-Science, Sao Paulo, SP), methyl parathion (Folidol 600 CE,Bayer CropScience, Sao Paulo, SP) and pirimicarb (Pi- 135Rimor 500 PM, Syngenta Protecao de Cultivos, Paulınea,SP). These insecticides are frequently used for control ofM. persicae in Brazil. The anionic surfactant polyoxyethy-lene alkyl phenol ether (Haiten 200, Arysta LifeScience doBrasil) was included in all treatments at 15 mL AI by 100 140L−1. Water and surfactant were used as control to estimatenatural mortality. [25]
Bioassays
Bioassays were conducted in four replications in a com-pletely randomized design using late-instar nymphs of M. 145persicae and adults of C. sanguinea, Acanthinus sp., and D.rapae. We used the leaf-dipping method, which provides auniform treated area on the leaf surface. Collard (Brassicaoleracea var. acephala) leaf disks (90 mm diameter) wereimmersed in insecticide solution for five seconds. Treated 150leaves dried at room temperature for 2 h and were placedon the bottom of plastic Petri dishes (90 mm × 20 mm).Ten to thirteen insects were transferred to the Petri dishescontaining the treated leaves.
Initially, we tested three concentrations of each insec-ticide to identify the range of concentrations that wouldcause mortality greater than zero and less than 100 %. 165
Concentration-mortality and Myzus persicae 3
Once the range of concentration was defined, we tested five
Q3
to ten concentrations for each insecticide in four replica-tions. The Petri dishes with the treated leaves and insects(i.e. experimental units) were maintained at 25 ± 0.5◦C andrelative humidity of 75 ± 5 %. Mortality was recorded 24170h after treatment, with mortality defined as immobility ofthe insects upon stimulation with a fine camel-hair brush.To evaluate mortality, Petri dishes were open inside plasticbags to avoid individuals flying away.
Statistical analysis175
Concentration-mortality data were analyzed by probitregression to obtain the regression equation and theinsecticide concentration needed to kill 90 % of the testpopulation (LC90) with their 95 % confidence intervals.[26]
Probit regression were analyzed using SAEG software 9.1180version.[27] Mortality was corrected for control mortalityusing the method of Abbott.[28] We accepted curves whichhad probability greater than 0.05 by the χ2 test.[29]
To determine the magnitude of selectivity of the insec-ticides to the natural enemies, we calculated the selectivity185ratio using the formula SLR90 of the insecticide for thenatural enemy/LC90 of the insecticide for M. persicae. Todetermine which insecticide was more toxic to a particularspecies, we calculated the toxicity ratio for each insecticideby the formula TXR90.190
The value TXR90 = LC90 of the least toxicinsecticide/LC90 of the insecticide. The toxicity ratio in-dicates how many times an insecticide is more potent (i.e.toxic) than the least toxic insecticide for a given insect popu-lation under test. Because most of the insecticides exhibited195the lowest LC90 values for D. rapae, we used it as referenceand calculated the tolerance ratio of C. sanguinea and Acan-thinus sp. relative D. rapae for each one of the insecticides.
The formula used was TLR90 = LC90 of the insecticidefor C. sanguinea or Acanthinus sp./LC90 of the insecticide200for D. rapae. Finally, we used the concentration-mortalityregression lines of each insecticide to estimate the mortalityof M. persicae, C. sanguinea, Acanthinus sp., and D. rapae,at field rates recommended for control of M. persicae inBrazil.205
Results and discussion
Concentration-mortality regression lines of the six insec-ticides for M. persicae, C. sanguinea, Acanthinus sp., andD. rapae are presented in Figure 1. The natural enemiestended to respond more homogeneously to the insecti-210cides than did M. persicae as indicated by steeper slopesin concentration-mortality regression lines for the natu-ral enemies relative to M. persicae, especially for acephateand methamidophos. For Acanthinus sp., concentration-mortality curves of all insecticides exhibited steeper slopes215than those observed for M. persicae. Similarly, curves for
all insecticides but dimethoate exhibited higher slopes forD. rapae relative to the aphid, and only methyl parathiondid not exhibit steeper concentration-mortality for C. san-guinea relative to M. persicae. 220
Insecticide concentrations needed to kill 90 % of the testpopulation (i.e. LC90) were determined for the aphid andnatural enemies (Table 1) and utilized to calculate selectiv-ity ratios of the insecticides for the three natural enemies(Table 2). Pirimicarb was highly selective to the natural en- 225emies as LC90 values for Acanthinus sp., C. sanguinea, andD. rapae (Table 1) were respectively 10, 195 and 59-foldhigher than the LC90 for M. persicae (Table 2, selectivityratios). The selectivity of pirimicarb to the natural enemieswas also evident from its concentration-mortality curve for 230the aphid, which was located on the left of those for thenatural enemies (Fig. 1). These results are in agreementwith those obtained by Gusmao et al.[30], who observedhigh selectivity of pirimicarb to C. sanguinea and Eriopisconnexa (German) (Coleoptera: Coccinellidae). The selec- 235tivity of pirimicarb was also demonstrated by Angeli etal.[31] in Orius majusculus (Reuter) (Heteroptera: Antho-coridae), and by Bacci et al.[25] the parasitoid Diaeretiellarapae (Nees) (Hymenoptera: Braconidae). The toleranceof natural enemies to pirimicarb relative to M. persicae 240could be related to lower rates of insecticide penetrationthrough the integument, higher rate of insecticide breakdown, and/or relative insensitivity of the target site in nat-ural enemies.[25,32,33]
Penetration rates of insecticides in the insect integu- 245ment are associated with physicochemical properties ofthe insecticide and the insect cuticle, including cuticlethickness and biochemical composition.[34–36] Soft-bodiedinsects such as M. persicae have a thinner cuticle com-pared with Acanthinus sp., C. sanguinea and D. rapae, 250which supports this hypothesis. The selectivity of pirimi-carb may also be associated with higher rates of metaboliza-tion in natural enemies than in M. persicae by detoxificationenzymes such as P450-dependent monooxigenases, whichtransform lipophilic xenobiotics into polar metabolites that 255are then excreted.[37] This hypothesis is based on the highlipophilic character of pirimicarb (2.7 g L−1 water at 25◦C),and the fact that P450-dependent monooxigenases are themain enzyme complex involved in metabolism of carba-mates in insects.[34,38] Differences in both substrate speci- 260ficity and velocity of acetylcholinesterase enzymes (i.e. thetarget site of pirimicarb) present in the natural enemies mayalso account for the relative tolerance of these insects topirimicarb.[39]
Methyl parathion showed selectivity to the predators 265Acanthinus sp., and C. sanguinea with selectivity ratios of71.5 and 6.7 respectively (Table 2). In contrast, this in-secticide was about 2.9 times more toxic to the parasitoidD. rapae than the aphid (Table 1), thus not showing se-lectivity to D. rapae (Table 2). Fragoso et al.[40] tested the 270LC99 of methyl parathion for Leucoptera coffeella (Guerin-Meneville) (Lepidoptera: Lyonetiidae) on Iphiseiodes
4 Bacci et al.
Fig. 1. Concentration-mortality regression lines of six insecticides tested against late-instar nymphs of Myzus persicae and adults ofCycloneda sanguinea, Acanthinus sp., and Diaeretiella rapae.
zuluagai Denmark & Muma (Acari: Phytoseiidae) obtain-ing less than 20 % mortality of the predatory mite. Incontrast, this insecticide was highly toxic to Cotesia sp. (Hy-275menoptera: Braconidae) thus corroborating our results.[41]
Dimethoate also showed some selectivity to Acanthinussp. and C. sanguinea as LC90 values for M. persicae (Table1) were about 2-fold lower than those for Acanthinus sp.or C. sanguinea (Table 2). On the other hand, the LC90 of280dimethoate for M. persicae was 2.6-fold higher than theLC90 of dimethoate for D. rapae (Table 2), indicating that it
was harmful to the parasitoid. Acephate and deltamethrinwas selective to Acanthinus sp. but not to C. sanguinea andD. rapae (Table 2) as LC90 values of these insecticides for 285M. persicae were lower than their LC90 values for Acan-thinus sp. but higher than those for C. sanguinea and D.rapae (Table 2). Similar results were obtained by Angeliet al.[31], who observed high toxicity of these insecticidesto the minute predatory bug O. majusculus. Additionally, 290methamidophos was more toxic to Acanthinus sp., C. san-guinea and D. rapae than to the aphid and therefore was
Concentration-mortality and Myzus persicae 5
Table 1. Results of Probit analysis on mortality of Myzus persicae, Acanthinus sp., Cycloneda sanguinea, and Diaeretiella rapae exposedto six insecticides.
† Sample size or number of insects utilized to generate the concentration-mortality curves.‡ Y′ is the expected mortality in Probit and X is the logarithm of the insecticide concentration [mg of active ingredient (a.i.) mL−1].§ Concentration needed to kill 90 % of the test population with its respective 95 % confidence interval.
not selective to the natural enemies (Table 2). These resultsshowed that methamidophos is harmful to all natural ene-mies tested, and this finding agrees with a previous study, in295which the insecticide was incompatible with conversationbiological control in potato because of its lower toxicityto Phthorimaea operculella (Zeller) (Lepidoptera: Gelechi-idae) relative to the parasitoid Orgilus lepidus Muesebeck(Hymenoptera: Braconidae).[42]300
In our bioassays, D. rapae was the most susceptible in-Q4sect to the majority of the insecticides as indicated by lowerLC90 values for the parasitoid relative to the other insects(Table 1). As a result, we used it as a reference to calcu-late the tolerance ratio, a measure of the relative tolerance305of the natural enemies to the insecticides (Table 2, bot-tom part). Tolerance ratios for Acanthinus sp. relative toD. rapae varied between 2 and 8 times for most insecti-cides, but the tolerance of this anthicid beetle to methylparathion relative to the parasitoid was 200 times higher.310Likewise for C. sanguinea, tolerance ratios varied between2 and 4, and again for methyl parathion, the coccinellid
was 19 times more tolerant than was the aphidiid par-asitoid D. rapae. The LC90 of pirimicarb for Acanthicussp. was the lowest among the natural enemies (Table 1); 315consequently, the tolerance ratio as defined generated avalue less than one (Table 2), which if inverted (1/TLR90),yields a value of 5.98 meaning that Acanthinus sp. wasabout 6 times more tolerant to pirimicarb than was D.rapae. Similarly for C. sanguinea with deltamethrin, D. ra- 320pae was approximately 9 times more tolerant than was thecoccinellid.
Overall, the predators Acanthinus sp. and C. sanguineawere more tolerant to the insecticides than was the par-asitoid D. rapae. Perhaps these results are related to the 325large body size of the predators relative to the parasitoid.This hypothesis is supported by observations by Rathmanet al.[43] and Picanco et al.[24], who observed that, as thebody size increases, the specific area decreases, and con-sequently there is less exposure to the insecticide. These 330results may also be related to the higher metabolic activityin predators than parasitoids and/or the thicker cuticle of
6 Bacci et al.
Table 2. Insecticide selectivity to adults of Acanthinus sp., Cycloneda sanguinea and Diaeretiella rapae relative to late-instar nymphsof Myzus persicae, and insecticide tolerance of Acanthinus sp., Cycloneda sanguinea relative to Diaeretiella rapae.
Acanthinus sp./ D. rapae C. sanguinea/ D. rapaeAcephate 8.13 2.18Deltamethrin 6.70 0.11 (9.22)Dimethoate 4.45 4.20Methamidophos 2.70 3.86Methyl parathion 204.84 19.21Pirimicarb 0.17 (5.98) 3.32
† SLR90 = LC90 of the insecticide for the natural enemy/LC90 of the insecticide for M. persicae. Selectivity ratio followed by a value betweenparentheses indicates how many times an insecticide was more toxic to the natural enemy relative to the aphid.‡ TLR90 = LC90 of the insecticide for Acanthinus sp. or C. sanguinea/LC90 of insecticide for D. rapae. Tolerance ratio followed by a value betweenparentheses indicates how many times more tolerant to an insecticide was D. rapae relative to Acanthinus sp. or C. sanguinea.
the predators compared with the parasitoid cuticle, whichcan hinder insecticide penetration.[34,35]
To determine which insecticide was more toxic for a335particular species, we calculated the toxicity ratio (TXR90)(Table 3, upper part) utilizing as reference the insecticidewith the lowest potency (i.e. highest LC90) for the species.Acephate showed the highest LC90 value for M. persicaeamong the insecticides tested, so did methyl parathion for340Acanthinus sp. and pirimicarb for C. sanguinea and D. ra-pae (Table 1), and therefore the TXR90 as defined generatedthe value of one for these insecticides (Table 3). Methylparathion and pirimicarb were the most potent insecticidesagainst M. persicae with potencies 12- and 8-fold higher345than acephate (Table 3). Deltamethrin, dimethoate, andmethamidophos showed similar potency against M. persi-cae with toxicity ratios 2–3 times higher than acephate.
Methamidophos, deltamethrin, were the most potent in-secticides against Acanthinus sp., and so were deltamethrin350and acephate against C. sanguinea, and methyl parathionand deltamethrin against D. rapae (Table 3). Deltamethrinwas 2700-fold more potent to kill Acanthinus sp. than pir-imicarb, and methyl parathion was 260-fold more potentto D. rapae than was pirimicarb (Table 3).355
Utilizing the concentration-mortality regression equa-tions, mortality by each insecticide at the concentrationcorresponding to the field rate for control of M. persicaewas estimated (Table 3, bottom part). Mortality of M. per-sicae by all insecticides tested was higher than 90 %, except360for deltamethrin, which caused only 40 % aphid mortal-ity. In addition, estimated mortality of Acanthinus sp. bydeltamethrin and methyl parathion, and mortalities of C.
Table 3. Toxicity ratio of and estimated mortality by six insec-ticides tested against late-instar nymphs of Myzus persicae andadults of Acanthinus sp., Cycloneda sanguinea, and Diaeretiellarapae.
† For a particular species, TXR90 = LC90 of the least toxic insecticidedivided by the LC90 of the insecticide of interest.‡ Mortality by each insecticide was estimated by plugging in the rec-ommended field rate for control of M. persicae in the concentration-mortality regression equation. The concentration of each insecticidecorresponding to the field rate was (mg a.i. mL−1): acephate = 0.75;deltamethrin = 0.0075; dimethoate = 0.4; methamidophos = 0.6;methyl parathion = 0.6 and pirimicarb = 0.5.
Concentration-mortality and Myzus persicae 7
sanguinea and D. rapae estimated for pirimicarb were lowerthan 40 %.365
Among the insecticides tested, acephate exhibited thelowest toxicity (i.e. the highest LC90) to M. persicae (seeTable 1). Despite these results, this insecticide may stillbe used against M. persicae if sprayed correctly becausethe estimated mortality at the recommended field rate for370control of the aphid was 98.7 % (see Table 3). The in-secticides dimethoate, methamidophos, methyl parathionand pirimicarb should be also efficient for control of M.persicae because of the high estimated mortality at therecommended field rates (see Table 3).375
The present study showed, under laboratory conditions,that pirimicarb is highly selective to Acanthinus sp., C. san-guinea and D. rapae. Pirimicarb is likely to exhibit high effi-ciency against M. persicae in field sprays because its recom-mended field rate (0.5 mg a.i. mL−1) is 13-fold higher than380the LC90 value (0.0369 mg a.i. mL−1) obtained here. There-fore, pirimicarb could be used in IPM systems of brassicasto manage M. persicae populations because of its efficiencyagainst M. persicae and selectivity to the main natural ene-mies. However, the recommended field rates may still cause385some mortality to Acanthinus sp. (see Table 3). To ensureselectivity, pirimicarb sprays should be timed to avoid expo-sure of Acanthinus sp. to the insecticide. Thus, pirimicarbcould be sprayed when this predator is less active in thefield.[40] The present study also showed the importance of390correct calibration of pirimicarb sprays to prevent negativeimpacts of this insecticide on natural enemies such as D.rapae.
With few restrictions, methyl parathion could still be auseful tool in IPM systems for suppression of M. persicae395populations in brassica crops. This insecticide exhibited thehighest potency against M. persicae and its LC90 (0.0235mg a.i. mL−1) was 26-fold lower than the field rate (0.6mg a.i. mL−1) for control of M. persicae. However, methylparathion was harmful to D. rapae and the estimated mor-400tality of C. sanguinea at the field rate was high. Therefore,for the selective use of this insecticide it is important toensure preservation of these species.[25]
Although pirimicarb and methyl parathion were efficientagainst M. persicae and selective in favor of natural ene-405mies, the slopes of concentration-mortality curves for somenatural enemies were higher than slopes of concentration-mortality curves for M. persicae. These results indicate thatsmall variations in the concentration of pirimicarb andmethyl parathion may cause higher variation in mortal-410ity of natural enemies. Therefore, the preservation of thesespecies will also depend on the correct calibration of fieldrates for use of pirimicarb and methyl parathion becausetheir selectivity to natural enemies can be reduced or lostat high concentrations.415
Several methods to evaluate toxicity of insecticides areavailable, including injections, topical applications andbioassays with prey or substrate treated with insecti-cide.[32,44] These bioassay techniques will differ on how
mortality correlates to mortality observed in field condi- 420tions. In our study, we used a brassica leaves treated withinsecticides, and therefore this technique provides a surfacewith a substrate similar to the plant canopy, which is im-portant because insecticide activity can be affected by thesubstrate.[45] 425
Laboratory studies are useful to predict the response ofnatural enemies to insecticide applications, but field studiesmay be necessary to provide the ultimate evidence of theirselectivity to non-target organisms.[46] Laboratory studiesuse uniform deposit structure and disregard insect behav- 430ior which can change the dose transfer process and affecttoxicity.[47] Despite this simplification, our studies are ap-propriate to understand the relative toxicity of insecticideson insect-pests and natural enemies because their responseto insecticides using the same conditions. Future studies 435should test additional insecticides that are currently usedto manage M. persicae for their efficiency and selectivity.
Conclusions
The present study identified selective insecticides that couldbe compatible with conservation of natural enemies in bras- 440sica crops. Anthicid and coccinellid predators as well asaphidiid parasitoids are recognized by their relative im-portance in different agroecosytems are often observed inhigh abundance in brassica crops. In addition, the presentstudy provided important practical information to improve 445IPM systems in brassicas using insecticides. Conservationof natural enemies is an important strategy of integratedpest management and can be achieved with the use of selec-tive insecticides, which allows integration of chemical andbiological methods to suppress pest populations in agri- 450cultural systems. The availability of insecticides efficientagainst M. persicae and selective to natural enemies is im-portant for development of sound IPM systems in brassicacrops.
Acknowledgments 455
We thank Dr. Ayr de Moura Bello for the identifica-tion of Cycloneda sanguinea and Acanthinus sp., and Dr.Angelica Maria Penteado-Dias for the identification ofDiaeretiella rapae. This research was funded by the Con-selho Nacional de Desenvolvimento Cientıfico and Tec- 460nologico (CNPq), the Fundacao de Amparo a Pesquisa doEstado de Minas Gerais (Fapemig), and the Coordenacaode Aperfeicoamento de Pessoal de Nıvel Superior (Capes).
References
[1] Blackman, R.L.; Eastop, V.F. Aphids on the World’s Crops: An iden- 465tification and information guide; John Wiley & Sons: New York,2000; 476 pp.
8 Bacci et al.
[2] Desneux, N.; Rabasse, J.M.; Ballanger, Y.; Kaiser, E.L. Parasitismof canola aphids in France in autumn. J. Pest Sci. 2006, 79 (2),95–102.470
[3] Devi, P.B.; Singh, T.K.; Jiten Singh, H. Studies on the natural enemycomplex of the green peach aphid, Myzus persicae (Sulzer) on Knol-Khol, Brassica oleracea gongylodes. Ann. Plant. Protec. Sci. 1999, 7(1), 37–40.
[4] Bacci, L.; Picanco, M.C.; Gusmao, M.R.; Barreto, R.W.; Galvan,475T.L. Inseticidas seletivos a tesourinha Doru luteipes (Scudder) uti-lizados no controle do pulgao verde em brassicas. Hort. Bras. 2002,20 (2), 174–179.
[5] Barbosa, L.R.; Carvalho, C.F.; Auad, A.M.; Souza, B.; Batista,E.S.P. Fertility and life expectancy tables of Myzus persicae on pep-480per in laboratory and greenhouse. Bragantia 2011, 70 (2), 375–382.
[6] Hardin, M.R.; Benrey, B.; Coll, M.; Lamp, W.O.; Roderick, G.K.;Barbosa, P. Arthropod pest resurgence: an overview of potentialmechanisms. Crop Prot. 1995, 14 (1), 3–18.
[7] Devonshire, A.L.; Field, L.M.; Foster, S.P.; Moores, G.D.;485Williamson, M.S.; Blackman, R.L. The evolution of insecticide re-sistance in the peach-potato aphid, Myzus persicae. Philos. Trans.R. Soc. Lond. B Biol. Sci. 1998, 353 (1376), 1677–1684.
[8] Desneux, N.; Wajnberg, E.; Fauvergue, X.; Privet, S.; Kaiser, L.Oviposition behaviour and patch-time allocation in two aphid para-490sitoids exposed to deltamethrin residues. Entomol. Exp. Appl. 2004,112 (3), 227–235.
[9] Stern, V.M.; Smith, R.F.; Van den Bosch, R.; Hagen, K.S. Theintegrated control concept. Hilgardia. 1959, 29 (2), 81–101.
[10] Longley, M.; Jepson, P.C.; Izquierdo, J.; Sotherton, N. Temporal495and spatial changes in aphid and parasitoid populations followingapplications of deltamethrin in winter wheat. Entomol. Exp. Appl.1997, 83 (1), 41–52.
[11] Matsumura, F. Contemporary issues on pesticide safety. J. Pestic.Sci. 2004, 29 (4), 299–303.500
[12] Matthews, G.A. Attitudes and behaviours regarding use of cropprotection products - A survey of more than 8500 smallholders in26 countries. Crop Prot. 2008, 27 (3–5), 834–846.
[13] Nauen, R.; Bretschneider, T. New modes of action of insecticides.Pestic. Outlook. 2002, 13 (6), 241–245.505
[14] Nicholson, G.M. Fighting the global pest problem. Toxicon. 2007,49 (4), 413–422.
[15] Alyokhin, A.; Drummond, F.A.; Sewell, G.; Storch, R.H. Differen-tial Effects of Weather and Natural Enemies on Coexisting AphidPopulations. Environ. Entomol. 2011, 40(3), 570–580.510
[16] Chambers, R.J.; Sunderland, K.D.; Stacey, D.L.; Wyatt, I.J. Controlof cereal aphids in winter wheat by natural enemies: aphid-specificpredators, parasitoids and pathogenic fungi. Ann. Appl. Biol. 1986,108 (2), 219–231.
[17] Elmali, M. Anthicus unicolor (Coleoptera: Anthicidae), a new preda-515tor of Diuraphis noxia (Homoptera: Aphididae) from Turkey. En-tomol. News. 1997, 108, 208.
[18] Miranda, M.M.M.; Picanco, M.C.; Matioli, A.L.; Pallini-Filho,A. Distribution in the plant and biological control of aphids, (Ho-moptera, Aphididae) in tomato. Rer. Bras. Entomol. 1998, 42 (1–2),52013–16.
[19] Desneux, N.; Decourtye, A.; Delpuech, J.M. The sublethal effectsof pesticides on beneficial arthropods. Annu. Rev. Entomol. 2007,52, 81–106.
[20] Galvan, T.L.; Koch, R.L.; Hutchison, W.D. Toxicity of commonly525used insecticides in sweet corn and soybean to multicolored Asianlady beetle (Coleoptera: Coccinellidae). J. Econ. Entomol. 2005, 98(3), 780–789.
[22] Bacci, L.; Picanco, M.C.; Barros, E.C.; Rosado, J.F.; Silva, G.A.;Silva, V.F.; Silva, N.R. Physiological Selectivity of Insecticides toWasps (Hymenoptera: Vespidae) Preying on the DiamondbackMoth. Sociobiology 2009, 53 (1), 151–167.
[23] Picanco, M.C.; Ribeiro, L.J.; Leite, G.L.D.; Gusmao, M.R. Sele- 535tividade de inseticidas a Polybia ignobilis (Haliday) (Hymenoptera:Vespidae) predator de Ascia monuste orseis (Godart) (Lepidoptera:Pieridae). An. Soc. Entomol. Bras. 1998, 27 (1), 85–90.
[24] Picanco, M.C.; Ribeiro, L.J.; Leite, G.L.D.; Zanuncio, J.C. Seletivi-dade de inseticidas a Podisus nigrispinus predator de Ascia monuste 540orseis. Pesq. Agropec. Bras. 1997, 32 (4), 369–372.
[25] Bacci, L.; Picanco, M.C.; Rosado, J.F.; Silva, G.A.; Crespo, A.L.B.;Pereira, E.J.G.; Martins, J.C. Conservation of natural enemies inbrassica crops: comparative selectivity of insecticides in the manage-ment of Brevicoryne brassicae (Hemiptera: Sternorrhyncha: Aphi- 545didae). Appl. Entomol. Zool. 2009, 44 (1), 103–113.
[26] Finney, D.J. Probit analysis; Cambridge University Press, London,UK, 1971; 333 pp.
[27] SAEG. Sistema para Analises Estatısticas, Versao 9.1; FundacaoArthur Bernardes, Universidade Federal de Vicosa: Vicosa, Brazil, 5502007.
[28] Abbott, W.S. A method of computing the effectiveness of an insec-ticide. J. Econ. Entomol. 1925, 18 (2), 265–267.
[29] Young, L.J.; Young, J.H. Statistical ecology: A population perspec-tive. Kluwer Academic: Boston, 1998; 565 pp. 555
[30] Gusmao, M.R.; Picanco, M.C.; Leite, G.L.D.; Moura, M.F. Sele-tividade de inseticidas a predadores de pulgoes. Hort. Bras. 2000,18 (2), 130–133.
[31] Angeli, G.; Forti, D.; Cappelletti, C. Selettivita verso Orius di diecifitofarmaci. Colt. Prot. 1998, 27 (1), 73–77. 560
[32] Yu, S.J. Selectivity of insecticides to the spined bug (Heteroptera:Pentatomidae) and its lepidopterous prey. J. Econ. Entomol. 1988,81 (1), 119–122.
[33] Guedes, R.N.C. Resistencia de insetos a inseticidas. In Manejo in-tegrado de doencas e pragas; Zambolin, L. (Ed.); Editora UFV: 565Vicosa, Brazil, 1999, 101–107.
[34] Hackman, R.H. Chemistry of the cuticle. In The physiology ofInsecta; Rockstein, M. (Ed.); Academic Press: New York, 1974,216–270.
[35] Hollingworth, R.M. The biochemical and physiological basis of 570selective toxicity. In Insecticide biochemistry and physiology; Wilkin-son, C.F., (Ed.); Plenum Press: New York, 1976; 431–506.
[36] Leite, G.L.D.; Picanco, M.; Guedes, R.N.C.; Gusmao, M.R. Selec-tivity of insecticides with and without mineral oil to Brachygastralecheguana (Hymenoptera: Vespidae): a predator of Tuta absoluta 575(Lepidoptera: Gelechiidae). Ceiba. 1998, 39 (1), 191–194.
[37] Onstad, D.W. Insecticide Resistance Management: Biology, Eco-nomics and Prediction. Academic Press: U.K., 2008; 305 pp. Q5
[38] Berg, G.L.; Sine, C.; Meister, R.T.; Poplyk, J. Farm Chemicals Hand-book; Meister Publishing Co: Willoughby, Ohio, USA, 2003; 1000 580pp.
[39] Silver, A.R.J.; Vanemden, H.F.; Battersby, M. A biochemical mech-anism of resistance to pirimicarb in two glasshouse clones of Aphisgossypii. Pest. Manag. Sci. 1995, 43 (1), 21–29.
[40] Fragoso, D.B.; Filho, P.J.; Filho, A.P.; Badji, C.A. Acao de inseti- 585cidas organofosforados utilizados no controle de Leucoptera cof-feella (Guerin-Meneville) (Lepidoptera: Lyonetiidae) sobre o acaropredator Iphiseiodes zuluagai Denmark & Muma (Acari: Phytosei-idae). Neotrop. Entomol. 2002, 31 (3), 463–467.
[41] Picanco, M.C.; Moura, M.F.; Miranda, M.M.M.; Gontijo, L.M.; 590Fernandes, F.L. Seletividade de inseticidas a Doru luteipes (Scudder,1876) (Dermaptera: Forficulidae) and Cotesia sp. (Hymenoptera:Braconidae) inimigos naturais de Ascia monuste orseis (Godart,1818) (Lepdoptera: Pieridae). Cienc. Rural. 2003, 33 (2), 183–188.
[42] Symington, C.A. Lethal and sublethal effects of pesticides on the 595potato tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera:Gelechiidae) and its parasitoid Orgilus lepidus Muesebeck (Hy-menoptera: Braconidae). Crop Prot. 2003, 22 (3), 513–519.
[43] Rathman, R.J.; Johnson, M.W.; Rosenheim, J.A.; Tabashnik, B.E.;Purcell, M. Sexual differences in insecticide susceptibility and syner- 600gism with piperonyl butoxide in the leafminer parasitoid Diglyphus
Concentration-mortality and Myzus persicae 9
begini (Hymenoptera, Eulophidae). J. Econ. Entomol. 1992, 85 (6),15–20.
[44] Trisyono, A.; Puttler, B.; Chippendale, G.M. Effect of the ecdysoneagonists, methoxyfenozide and tebufenozide, on the lady bee-605tle, Coleomegilla maculata. Entomol. Exp. Appl. 2000, 94 (1),103–105.
[45] Jain, S.; Yadav, T.D. Persistence of deltamethrin, etrimfos andmalathion on different storage surfaces. Pestic. 1989, 23 (1), 21–24.
[46] Naranjo, S.E. Conservation and evaluation of natural enemies in 610IPM systems for Bemisia tabaci. Crop Prot. 2001, 20 (9), 835–852.
[47] Ebert, T.A.; Hall, F.R. Deposit structure effects on insecticide bioas-says. J. Econ. Entomol. 1999, 92 (5), 1007–1013.
