Evaluation of the effect of different insecticides on the survival and capacity of 2 Eretmocerus mundus Mercet to control Bemisia tabaci (Gennadius) populations

1 Ti le 1 E alua ion o he e ec o di e en insec icides on he su i al and capaci y o 2 E e moce us mundus Me ce o con ol Bemisia abaci (Gennadius) popula ions 3 4 Au ho s 5 J. E. Gonzalez-Zamo a, D. Lei a, M.J. Bellido, C. A illa 6 7 A ilia ion 8 Depa amen o de Ciencias Ag o o es ales (Uni e sidad de Se illa) 9 Ca e e a de U e a km 1, E-41013 Se illa (Spain) 10 11 Co esponding au ho : 12 J.E. Gonzalez-Zamo a 13 e-mail: zamo [email protected] 14 Fax numbe : + 34 95 448 64 36 15 Phone numbe : + 34 95 448 64 59 16 17 18 19 20 Published in: C op P o ec ion 23 (2004) 611–618 21 doi:10.1016/j.c op o.2003.11.011 22 2 Abs ac 23 Two di e en expe imen s we e ca ied ou o e alua e h ee insec icides. In he 24 i s one, he e ec o wo insec icides, me homyl and indoxaca b, on pupae and 25 adul s o he whi e ly Bemisia abaci (Gennadius) pa asi oid E e moce us mundus 26 Me ce was e alua ed unde labo a o y and g eenhouse condi ions, using swee 27 peppe (Capsicum annuum L.) plan s. In he second expe imen , oxamyl was 28 es ed o s udy i s e ec on he abili y o E. mundus o pa asi ize and con ol B. 29 abaci in swee peppe plan s, using a g eenhouse cage e alua ion. Me homyl and 30 indoxaca b caused low mo ali y o E. mundus pupae (17.6 and 7.8% 31 espec i ely), al hough me homyl mo ali y was signi ican ly highe . Me homyl 32 p oduced 100% mo ali y on E. mundus adul s wi h esh and 24 hou -old 33 esidues on lea es, signi ican ly highe han he mo ali y p oduced by indoxaca b 34 ( alues anged om 43.9 o 34.4%). The ha m ul e ec o me homyl pe sis ed o 35 a long ime (up o 60 days). The esul s o he expe imen wi h oxamyl showed 36 ha E. mundus con olled whi e ly popula ion, wi hou signi ican in e ac ion 37 be ween he p esence o he pa asi oid and insec icide on whi e ly mo ali y. 38 Whi e ly mo ali y in he p esence o he pa asi oid was 87.8%, signi ican ly highe 39 han he mo ali y in he absence o E. mundus (59.3%). Oxamyl did no p oduce 40 a signi ican e ec on he eme gence o E. mundus adul s. Applica ion o he 41 p oduc s in IPM p og ams is discussed. 42 43 Keywo ds: E e moce us mundus, Bemisia abaci, indoxaca b, oxamyl, me homyl, swee 44 peppe , pa asi ism. 45 46 3 In oduc ion 47 48 E e moce us mundus Me ce (Hymenop e a: Aphelinidae), a pa asi oid o he 49 obacco, co on o swee po a o whi e ly Bemisia abaci (Gennadius) (Hemip e a: 50 Aley odidae), has a widesp ead dis ibu ion wo ldwide. This species is ecognized 51 as one o he mos impo an na u al enemies o B. abaci, and has gene a ed a 52 lo o in e es in coun ies whe e B. abaci is a p oblem. The use o hea y chemical 53 con ol agains his pes is also ecognized o be in ol ed in many o he ou b eaks 54 o B. abaci a ound he wo ld, o di e en easons: de elopmen o insec icide 55 esis ance, nega i e e ec s on na u al enemies, al e a ion o beha iou and 56 biology o he pes . 57 58 Ou b eaks o his whi e ly in di e en c ops and coun ies ha e s imula ed he 59 sea ch o di e en biological con ol agen s a ound he wo ld. The mos ac i e 60 coun y in his espec is he U.S.A., whe e many pa asi oid and p eda o species 61 ha e been es ed. One o he mos p omising species is E. mundus (Goolsby e al., 62 1998; Hoelme e al., 1999; Ki k e al., 2000), especially he s ain ob ained om 63 sou heas Spain. The i s ime his species was collec ed in Mu cia (Spain) on 64 co on, in 1991-92, i exhibi ed a good ole ance o he di e en pes icides applied 65 egula ly o he c op (Ki k e al., 2000). 66 67 Cu en pes con ol includes he use o pes icides, combined o no wi h na u al 68 enemies. The e a e many epo s and s udies ha p esen e idence o na u al 69 enemies o B. abaci ha can emain ac i e in di e en c ops a e he use o 70 some pes icides (Ge ling, 1996; Ge ling and Na anjo, 1998; Simmons and Jackson, 71 2000), especially pa asi oids, such as E. mundus. Possible explana ions o his 72 abili y o pa asi oids o emain in ea ed plo s include he p o ec ion ha 73 imma u e s ages can ob ain inside he hos , as well as he ype o compound 74 used, he incomple e co e age o he canopy o he iming o he applica ion. 75 76 The p esence o E. mundus in comme cial plo s ea ed ou inely wi h pes icides 77 has also been epo ed by o he au ho s (Rod iguez-Rod iguez e al. 1994; 78 4 Gonzalez-Zamo a e al., 1996) in sou heas Spain. They also s udied he 79 pa asi ism on B. abaci and T ialeu odes apo a io um (Wes .) by di e en species 80 and he abili y o E. mundus o con ol B. abaci popula ions in swee peppe , 81 melon, and oma o. In summa y, hese pape s show he abili y o di e en 82 whi e ly pa asi oids o es ablish and main ain a high le el o pa asi ism in plo s, 83 e en when hey a e ea ed wi h pes icides. Di e en pes icides a e conside ed o 84 be selec i e o his and o he pa asi oids and can be used oge he o ob ain 85 con ol o he pes popula ion below inju y le els (Koppe Biological Sys ems, 86 2003). 87 88 O he pape s ha e s udied he combina ion o pes icides and pa asi oids (wi h 89 special in e es in E e moce us spp.) o con ol whi e ly popula ions in di e en 90 condi ions. Fo example, Bi nie and Denholm (1992) used an ex ended labo a o y 91 ial o es he capaci y o E. mundus o con ol B. abaci popula ions on co on 92 wi h he applica ion o cype me h in, showing he abili y o he pa asi oid 93 popula ion o eco e a e only one applica ion o he compound. De ine e al. 94 (2000) e ealed he po en ial o pipe onyl bu oxide o imp o e he le el o E. 95 mundus pa asi ism on B. abaci, by slowing he de elopmen o he whi e ly, 96 inc easing he pa asi ism in he ea ed whi e ly popula ion by 7-8%. Van D iesche 97 e al. (2001) demons a ed he possibili y o using an insec g ow h egula o 98 (bup o ezin) in combina ion wi h E e moce us e emicus Rose and Zolne owich o 99 con ol T. apo a io um and B. abaci in poinse ias in comme cial g eenhouses. 100 101 The aim o his wo k was o s udy he e ec o h ee insec icides on di e en 102 de elopmen s ages (pupa and adul ) o E. mundus, and he capaci y o E. 103 mundus o con ol B. abaci popula ions oge he wi h one o he insec icides, 104 p esen ing e idence o he capaci y o his species o be used oge he wi h 105 insec icides. Two o hese insec icides (me homyl and oxamyl) a e cu en ly used 106 in sou heas Spain o con ol di e en pes s, and he hi d (indoxaca b) has been 107 in oduced ecen ly o con ol ca e pilla s in di e en c ops, including hose wi h B. 108 abaci in es a ion. Indoxaca b is a selec i e p oduc ha is compa ed wi h he 109 o he wo p oduc s, non-selec i e insec icides. These wo insec icides can be 110 5 applied in di e en ways in o de o con e selec i i y. Resul s a e discussed 111 conside ing he possibili ies o using hese p oduc s in a IPM p og am. 112 113 Ma e ial and Me hods 114 115 Two di e en expe imen s we e ca ied ou o es he insec icides: in he i s 116 one, me homyl (chemical name: S-me hyl-N-[(me hylca bamoyl)oxy] 117 hioace imida e) (comme cial p oduc Lanna e® 20 L, Du Pon Ibe ica S.L.), and 118 indoxaca b (chemical name: (S)-7-chlo o-3-[me hoxyca bonyl-(4- i luo ome hoxy- 119 phenyl)-ca bamoyl]-2,5-dihyd o-indenol 1,2 -e[1,3,4]oxadiazine-4a(3H)-ca boxylic 120 acid me hyl es e ) (comme cial p oduc S ewa d® 30 WG, Du Pon Ibe ica S.L.) 121 we e es ed on E. mundus pupae and adul s; in he second one, oxamyl (chemical 122 name: me hyl-N’,N’-dime hyl-N[(me hylca bamoyl)oxy]-1- hio-oxamimida e) 123 (comme cial p oduc Vyda e® 10L, Du Pon Ibe ica S.L.) was es ed o de e mine 124 i s e ec on he pa asi ism and capaci y o E. mundus o con ol a popula ion o 125 B. abaci, using a g eenhouse cage e alua ion. 126 127 A colony o B. abaci was c ea ed om adul s cap u ed in he Se ille p o ince 128 (sou hwes Spain), om co on and aube gine plan s, and kep in an insec 129 ea ing oom, eeding on swee peppe (Capsicum annuum L.) plan s (c . La go 130 I aliano, Semillas Ba lle S.A., C/Ma ade o 10, E-10100-Miajadas (Cace es, Spain)). 131 The bio ype o B. abaci was no de e mined. Adul s o E. mundus we e collec ed 132 in he egions o Alme ia (sou heas Spain) and Se ille, on swee peppe and 133 co on plan s, and ea ed on swee peppe plan s in es ed wi h B. abaci nymphs. 134 The ea ing oom was kep a 26±2 ºC wi h a pho ope iod o 16:8 (Ligh :Da k). 135 136 Expe imen 1: E ec o me homyl and indoxaca b on E e moce us 137 mundus pupae and adul s 138 139 Fou young swee peppe plan s we e selec ed o each ea men (i.e. p oduc ), 140 wi h 4-5 lea es each, o assess he e ec o insec icides on E. mundus pupae. 141 They we e in es ed wi h adul s o B. abaci, which we e allowed o lay eggs o 142 6 48-72 hou s and hen emo ed om he plan s. De elopmen o he o sp ing was 143 ollowed un il 2nd-3 d ins a nymphs we e p esen , hen emales o E. mundus 144 we e in oduced in o he cages o o iposi ion, oge he wi h se e al males. The 145 plan s we e kep in he ea ing oom un il he pa asi oid pupa was obse ed inside 146 he whi e ly pupal case: he o m o he pupa was e iden and he eyes ook on a 147 che y colou (Ga ido e al. , 1982; Ga ido, 1992). A ha momen , a minimum o 148 wen y- i e pupae pe plan we e ma ked wi h an indelible pen, and he plan s 149 we e pu in a plas ic g eenhouse. The o al numbe o pupae used in each 150 ea men was 115, 107, and 114 o indoxaca b, me homyl and he con ol, 151 espec i ely. The p oduc s we e applied in ha momen , using a igge -ope a ed 152 hand sp aye , a he ecommended ield a es: me homyl, 0.4 g a.i./l; indoxaca b, 153 0.0375 g a.i./l un il un-o . A g oup o ou plan s was ea ed wi h wa e , as 154 con ol. 155 156 Coun s we e done e e y 3-4 days wi h he help o a 5x magni ying hand lens, 157 coun ing dead and li e pupae and pupal cases om whe e an insec had eme ged. 158 The expe imen inished when all he adul s had eme ged. 159 160 The e ec o he insec icides on E. mundus adul s was e alua ed by applying he 161 p oduc s and wa e a he same a es wi h he igge -ope a ed hand sp aye on 162 se e al swee peppe plan s wi h de eloped lea es. The p oduc s we e allowed o 163 d y and hen wo ypes o cages we e moun ed: wi h esh esidues and wi h 164 wen y- ou hou old esidues. The me hodology used was desc ibed in Jones e 165 al. (1995). 166 167 The expe imen al uni s (cages) consis ed o 5-6 newly eme ged adul s o E. 168 mundus, con ined o a Pe i dish o 55 mm diame e and 14 mm heigh . The Pe i 169 dishes we e modi ied by eplacing mos o he bo om wi h o gandy clo h 170 (subsequen ly in e ed o become he op). The new bo om hal o he Pe i dish 171 was used as a empla e o cu ou a ci cula sec ion o sp ayed lea . The lea discs 172 we e i ed in he inne su ace o a dish lid (now he bo om), wi h he bo om 173 lea su ace acing upwa ds. A co on clo h mois ened wi h wa e and honey was 174 7 pu inside he cage. The pa asi oids we e collec ed om he ea ing uni s and 175 b ie ly chilled be o e being in oduced in he expe imen al uni s. The en ila ed 176 dish bo om was eplaced, becoming he op. Dish hal es we e secu ed using a 177 pai o clips, and he cages we e pu in a labo a o y oom. Six eplica es pe 178 ea men (wi h a o al o 32-36 indi iduals pe ea men ) we e used wi h he 179 esh esidues lea es, and eigh eplica es pe ea men (wi h a o al o 53-61 180 indi iduals pe ea men ) wi h he lea es wi h wen y- ou hou old esidues. The 181 adul s we e kep in he cages o wen y- ou hou s, hen opened and he adul s 182 coun ed, sepa a ing dead and li e insec s. 183 184 A simila es was pe o med o s udy me homyl pe sis ence in swee peppe plan 185 lea es. Di e en g oups o plan s we e selec ed, and in each g oup one o he 186 plan s was ea ed wi h wa e and he o he s wi h me homyl a he p e ious a e. 187 The plan s we e allowed o d y and a e di e en ime pe iods, anging om 188 se en o six y- wo days a e ea men , cages we e moun ed wi h lea discs om 189 plan s ea ed wi h me homyl and wa e . The numbe o adul s in oduced in each 190 cage a ied be ween eigh and hi een. The adul s we e in oduced in he cages 191 as explained abo e, and a e wen y- ou hou s he cages we e opened and he 192 numbe o dead and li e adul s coun ed. T ea ed plan s and cages we e kep in 193 labo a o y condi ions. 194 195 Expe imen 2: E ec o oxamyl on he capaci y o E e moce us mundus 196 o con ol Bemisia abaci 197 198 The expe imen al design s udied wo le els (p esence and absence) o wo ac o s 199 (pa asi oid and insec icide). The e we e, he e o e, ou ea men s: 1) applica ion 200 o oxamyl, 2) applica ion o oxamyl and in oduc ion o E. mundus, 3) in oduc ion 201 o E. mundus, and 4) no applica ion o oxamyl and no in oduc ion o E. mundus 202 (con ol). Each ea men was eplica ed ou imes, using one swee peppe plan 203 pe ea men and eplica e, making a o al o 16 plan s. 204 205 8 The plan s we e in es ed wi h B. abaci adul s in he ea ing oom, allowed o lay 206 eggs o h ee days only on one lea and hen emo ed. The plan s we e kep in 207 he ea ing oom and, a e nine days, i s and second ins a whi e ly nymphs 208 we e p esen on he lea es. The numbe o nymphs pe lea anged om 132 o 209 198. Plan s we e hen main ained in a g eenhouse inside a me allic s uc u e 210 co e ed wi h o gandy o he es o he expe imen . 211 212 Oxamyl was applied a a a e o 0.028 g a.i./plan (equi alen o 500 g a.i./ha, 213 wi h 18,000 plan s/ha) in ea men s 1) and 2). I was applied on a weekly basis, 214 a maximum o eigh imes, beginning he same day he plan s had been pu in he 215 g eenhouse. The oxamyl was dilu ed in 100 ml o wa e pe plan . The pH o he 216 b o h was adjus ed o 4.5-5.5 wi h phospho ic acid. A d ip i iga ion sys em was 217 used o wa e he plan s, simula ing he no mal i iga ion managemen o his 218 c op, and he b o h was injec ed wi h a p e ious-p essu e sp aye in he i iga ion 219 sys em. 220 221 E. mundus was in oduced in ea men s 2) and 3) a a o al a e o 12 o 18 222 emales pe eplica e, ollowing he ecommended a io p oposed by Jones e al. 223 (1999). Adul pa asi oids we e placed in he cages in wo o ou sepa a e 224 in oduc ions, beginning on he i s day ha he plan s we e pu in he 225 g eenhouse. 226 227 Plan s we e e alua ed e e y 3-4 days du ing he i s wo weeks, and hen weekly 228 un il all he adul s o B. abaci and E. mundus eme ged. The numbe o li ing 229 whi e ly nymphs and pupae, he numbe o pa asi ized whi e ly nymphs and 230 pa asi oid pupae, and he numbe o pupal cases om whe e an adul (whi e ly o 231 pa asi oid) had eme ged we e coun ed. This expe imen included only one 232 gene a ion o he whi e ly B. abaci and he pa asi oid E. mundus. 233 234 Analysis o a iance was pe o med on mo ali y and pa asi ism (S a is ical 235 G aphics Co po a ion, 1999) in bo h expe imen s, wi h he ans o ma ion o 236 z=a csin p , whe e p is mo ali y o pa asi ism. A 2x2 ac o ial analysis was applied 237 9 in expe imen 2. I ea men s we e signi ican a P < 0.05, hen di e ences 238 be ween means we e de e mined using he LSD es a 95% con idence le el. 239 Abbo ’s o mula (Abbo , 1925) was used o co ec he mo ali y in expe imen 1. 240 241 Vouche specimens o he pa asi oid a e main ained by he i s au ho in he 242 Depa men collec ion (Depa amen o de Ciencias Ag o o es ales, Uni e sidad de 243 Se illa). 244 245 Resul s 246 247 Expe imen 1: E ec o me homyl and indoxaca b on E e moce us 248 mundus pupae and adul s 249 250 Me homyl signi ican ly inc eased he mo ali y o E. mundus pupae pa asi izing B. 251 abaci (Figu e 1) se en days a e applica ion (F=4.7, d. .=2, 9, P=0.04), while 252 indoxaca b was no signi ican ly di e en om he con ol. Mo ali y inc eased 253 h ee days la e o 17.6 % in me homyl, g ea e han indoxaca b and he con ol, 254 wi h 7.8 and 5.1% mo ali y espec i ely (F=8.20, d. .=2, 9, P=0.009). 255 256 Bo h insec icides signi ican ly inc eased he mo ali y o E. mundus adul s (Figu e 257 2), hough me homyl was mo e ha m ul (100 % mo ali y in bo h cases, wi h esh 258 and 24 hou -old esidues in lea es) han indoxaca b (43.9% and 34.4%, 259 espec i ely), wi h F=59.8, d. .=2, 6, P<0.0001, and F=84.60, d. .=2, 9, 260 P<0.0001, o esh and 24 hou -old esidues espec i ely. 261 262 The ha m ul e ec o me homyl on E. mundus adul s las ed up o six y days a e 263 applica ion (Figu e 3A), when he mo ali y was s ill signi ican ly highe han he 264 con ol ea ed wi h wa e . The mo ali y was co ec ed wi h he Abbo ’s o mula 265 and adjus ed o a cu e (Figu e 3B; R2 = 0.88; P<0.01). A leas 55 days we e 266 equi ed o adul mo ali y a e ea men wi h me homyl o d op o 50%. 267 268 16 Re e ences 437 438 Abbo , W.S. 1925. 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Pe cen age mo ali y o E e moce us mundus pupae pa asi izing 559 Bemisia abaci ea ed wi h me homyl ( ), indoxaca b ( ), and con ol ( ). 560 T ea men s wi h di e en le e s in he same day a e signi ican ly di e en wi h 561 95% o con idence, using he LSD es . Ve ical ba s indica e he s anda d e o 562 o he mean. 563 564 Figu e 2. Pe cen age mo ali y o E e moce us mundus adul s ea ed wi h 565 me homyl, indoxaca b, and he con ol, wi h esh and 24-hou old esidues. 566 T ea men s wi h di e en le e s a e signi ican ly di e en wi h 95% o 567 con idence, using he LSD es . Ve ical ba s indica e he s anda d e o o he 568 mean. 569 570 Figu e 3. Pe cen age mo ali y o E e moce us mundus adul s ea ed wi h 571 me homyl o e a pe iod o 60 days, (A) compa ed wi h he con ol ea ed wi h 572 wa e ; me homyl ( ), wa e ( ); and (B) mo ali y co ec ed using Abbo ’s 573 o mula and wi h an adjus ed cu e (R2=0.88, P<0.01). Ve ical ba s indica e 574 he s anda d e o o he mean. 575 576 Figu e 4. Cumula i e pe cen age mo ali y o Bemisia abaci la ae in he 577 expe imen wi h oxamyl, (A) conside ing he ou ea men s, oxamyl ( ), 578 oxamyl plus E e moce us mundus ( ), E. mundus ( ), and con ol ( ); and (B) 579 conside ing he ea men s wi h E. mundus ( ), and wi hou pa asi oids ( ). 580 Ve ical ba s indica e he s anda d e o o he mean. 581 582 Figu e 5. E ec o oxamyl on E e moce us mundus pa asi izing Bemisia abaci 583 la ae. (A) Pe cen age e olu ion o pa asi ized whi e ly la ae ea ed wi h 584 oxamyl ( ) and wa e ( ); and (B) Cumula i e pe cen age eme gence o 585 E e moce us mundus adul s om Bemisia abaci la ae ea ed wi h oxamyl ( ) 586 and wa e ( ). Ve ical ba s indica e he s anda d e o o he mean. 587 588 21 589 590 591 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 Figu e 1 615 616 0 5 10 15 20 25 day 3 day 7 day 10 days a e ea men % mo ali y b ab a a b a 22 617 618 619 620 621 622 623 624 625 626 627 628 629 630 631 632 633 634 635 636 637 638 639 640 Figu e 2 641 642 0 20 40 60 80 100 wa e indoxaca b me homyl % mo ali y esh 24 hou s a b c c b a 23 643 644 645 646 647 648 649 650 651 652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668 669 670 671 672 673 674 675 676 Figu e 3 677 678 0 20 40 60 80 100 010 20 30 40 50 60 % mo ali y 0 20 40 60 80 100 010 20 30 40 50 60 days a e ea men % mo ali y A B 24 679 Figu e 4 680 681 682 683 684 685 686 687 688 0 20 40 60 80 100 3 7 10 14 21 28 35 42 49 52 days a e pa asi oid in oduc ion % mo ali y o whi e ly la ae 0 20 40 60 80 100 3 7 10 14 21 28 35 42 49 52 days a e pa asi oid in oduc ion % mo ali y o whi e ly la ae A B 25 689 690 691 692 Figu e 5 693 694 695 696 0 10 20 30 40 3 7 10 14 21 28 35 42 49 52 days a e pa asi oid in oduc ion % pa asi ized whi e ly la ae 0 10 20 30 40 3 7 10 14 21 28 35 42 49 52 days a e pa asi oid in oduc ion % pa asi oid eme gence A B 21 14 10 7 3 100 80 60 40 20 0 28 35 42 49 52 days a e pa asi oi d in oduc i on % mo ali y o whi e ly la ae whi e ly la ae % mo ali y o days a e pa asi oi d in oduc i on 52 49 42 35 28 21 14 10 7 3 100 80 60 40 20 0 whi e ly la ae % mo ali y o days a e pa asi oi d in oduc i on 52 49 42 35 28 21 14 10 7 3 100 80 60 40 20 0 whi e ly la ae % mo ali y o days a e pa asi oid in oduc i on 52 49 42 35 28 21 14 10 7 3 100 80 60 40 20 0