Germano Leão Demolin Leite 1, Marcelo Picanço 2, Gulab Newandran Jham 3, Flávio Marquini 4

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1 INTENSITY OF Tut solut (Meyrick, 1917) (Lepidopter: Gelechiide) AND Liriomyz spp. (Dipter: Agromyzide) ATTACKS ON Lycopersicum esculentum Mill. LEAVES Intensidde de tque de Tut solut (Meyrick, 1917) (Lepidopter: Gelechiide) e de Liriomyz spp. (Dipter: Agromyzide) em folhs de Lycopersicum esculentum Mill. Germno Leão Demolin Leite 1, Mrcelo Picnço 2, Gul Newndrn Jhm 3, Flávio Mrquini ABSTRACT The ojective of this study ws to determine the effect of height of leves in the cnopy of plnts, lef orgnic compounds, concentrtions of lef nitrogen nd potssium, lef trichomes nd cristlliferous idiolsts densities on the ttck intensity of three tomto (Lycopersicon esculentum Mill. cv. Snt Clr) crops y Tut solut (Meyrick) (Lepidopter: Gelechiide) nd Liriomyz spp. (Dipter: Agromyzide), under field conditions. The experimentl design ws rrnged in rndomized locks, with three replictions, ech eing one tomto crop. Anlysis of vrince nd the Tukey s multiple rnge test (% significnce) were used to test the effect of cnopy height, trichome nd cristlliferous idiolsts densities on the numer of mines produced y T. solut nd Liriomyz spp. nd on the numer of T. solut eggs. Person s correltion (% significnce) ws used to evlute the reltionships etween lef orgnic compounds, lef N nd K concentrtions, lef trichome nd cristlliferous idiolsts densities nd the numer of mines produced y T. solut nd Liriomyz spp. nd the numer of T. solut eggs. Highest insect ttck occurred in the finl stge of the culture. A higher numer of Liriomyz spp. mines/lef ws recorded in the lower (1.) thn in the upper (.2) level of the tomto plnts, the opposite ws oserved for the numer of T. solut eggs/lef (.13 nd.7, respectively). The numer of T. solut mines/lef concentrted more on the medin (1.23) nd picl regions (.63) thn on the sl (.93). No significnt effect of the trichomes nd cristlliferous idiolsts densities of leves ws noted on T. solut nd Liriomyz ssp. popultions. Apprently, the terpenes ffected oviposition of T. solut while lef potssium ffected Liriomyz spp. ttck. Index terms: Tomto, popultion dynmics, tomto lefminer, terpenes. RESUMO Ojetivou-se com este estudo determinr s influêncis d posição ds folhs no dossel ds plnts, dos compostos orgânicos folires, ds concentrções de nitrogênio e potássio folir, ds densiddes de tricoms e dos idiolstos cristlíferos folires n intensidde de tque de Tut solut (Meyrick) (Lepidopter: Gelechiide) e de Liriomyz spp. (Dipter: A- gromyzide) em três cultivos de tomte (Lycopersicum esculentum Mill. cv. Snt Clr) em condições de cmpo. O desenho experimentl foi em locos csulizdos com três repetições, sendo cd um dos cultivos de tomte. Form relizdos nálise de vriânci e teste de médi de Tukey (% de significânci) pr testr o efeito de dossel ns densiddes de tricoms e de idiolstos cristlíferos, no número de mins de T. solut e de Liriomyz spp. e o número de ovos de T. solut. Foi usd correlção de Person (% de significânci) pr vlir s relções entre compostos orgânicos folires, concentrções de N e de K folires, densidde de tricoms e de idiolstos cristlíferos e o número de mins de T. solut e de Liriomyz spp. e o número de ovos de T. solut. O mior tque desses insetos ocorreu no estágio finl d cultur. Mior número de mins de Liriomyz spp. foi oservdo ns folhs sis (1,), se comprndo com s picis (,2), sendo o contrário oservdo pr o número de ovos de T. solut (,13 e,7, respectivmente). Mins de T. solut/folh concentrrm-se mis nos terços medio (1,23) e picl (,63) do que no sl (,93). Não foi detectd influênci ds densiddes de tricoms e de idiolstos cristlíferos folires ns populções de T. solut e de Liriomyz ssp. Possivelmente, os terpenos fetrm oviposição de T. solut, enqunto o potássio folir fetou o tque de Liriomyz spp. Termos pr indexção: Tomte, dinâmic populcionl, trç-do-tomteiro, terpenos. (Receido pr pulicção em de dezemro de 22 e provdo em 1 de mrço de 23) 1. Agronomist; D.Sc.; Professor; NCA/UFMG; Montes Clros, MG, 39-6, CP: 13; gldleite@ufmg.r. Corresponding uthor. 2. Agronomist; D.Sc.; Professor; Universidde Federl de Viços (UFV); Viços, MG, 3671-; picnco@mil.ufv.r. 3. Chemist; PhD; Professor; UFV. E-mil: gul@mil.ufv.r.. Agronomist; M.Sc.; Grdute student; UFV.

2 Intensity of Tut solut (Meyrick, 1917) (Lepidopter... 3 INTRODUCTION The tomto lefminers, Tut solut (Meyrick) (Lepidopter: Gelechiide) nd Liriomyz spp. (Dipter: Agromyzide) re importnt tomto pests in South Americ, with severl morphologicl nd chemicl fctors of plnts influencing their popultions (LETOURNEAU et l., 1996; PICANÇO et l., 199; LEITE et l., 1999). The NK fertiliztion cn ffect the degree of ttck from insects (MARSCHNER, 199): n excess of N nd deficiency in K hve een reported to led to higher ccumultion of mino cids in plnts, leding to higher degree of insect ttck (MARSCHNER, 199). Also, the lef position on the plnt cnopy hs een reported to influence T. solut nd Liriomyz spp. ttcks, with preferentil oviposition on the picl leves proly due to the fct tht these leves re more tender nd of higher nutritionl vlue (SILVA et l., 199; LEITE et l., 1999, ; OLIVEIRA, 1999). The possile effect of trichomes on insects cn result from chemicl nd/or mechnicl fctors. The chemicl fctor could prtly e due to exudtes produced y glndulr trichomes which cn contin compounds tht re toxic to insects (FERY e KENNEDY, 197; LEITE et l., 21). Other possile resistnce fctors include mechnicl rriers, density, length nd form of trichomes (LEITE et l., 1999, ). The presence of crystls in the leves is nother fctor tht cn difficult feeding y insects (FRANCESCHI e HORNER JÚNIOR, 19; LEITE et l., 1999c), with high occurrence of clcium oxlte crystls in Lycopersicon (LEITE et l., 1997; LEITE et l., 1999c). The ojective of this study ws to determine the effects of height of leves in the cnopy of plnts, lef orgnic compounds, concentrtions of lef nitrogen nd potssium, lef trichomes nd cristlliferous idiolsts densities on the intensity of ttck of three Snt Clr tomto crops, y T. solut nd Liriomyz spp., under field conditions. MATERIAL AND METHODS The experiment ws conducted using three Snt Clr tomto crops (crops n o. 1, 2 nd 3) from April to Novemer of 1999 in Guidovl, Mins Geris Stte, Brzil. Culturl prctices utilized hve een descried y Filgueir (2). The experimentl design ws rrnged in rndom locks, with three replictions, ech eing one tomto crop. Ech tomto crop hd 1 plnts spced. m prt within rows nd 1. m etween rows, trellised nd pruned ove the 7 th rnch. The four outside rows nd the first ten plnts on ech side of the row formed the outer order nd the remining crop ws considered to e the experimentl plot. The numer of lef mines produced y T. solut nd Liriomyz spp. nd the eggs of T. solut t the lower, middle nd upper portions of 3 plnts/crop (one lef/plnt) ws determined weekly (LEITE et l., 1999, ; OLIVEIRA, 1999, LEITE et l., 21). In order to estimte trichome nd cristlliferous idiolst densities, one picl leflet from ech portion of the cnopy of nine plnts/crop (one leflet/plnt) ws collected monthly. These leflets were plced in white trnsprent plstic gs, immeditely seled, nd stored in 7% ethnol for further evlution. Leflets were clered in NOH (1%) for 2h nd in sodium hypochlorite (2%) for 1h. After wshing nd during dehydrtion, the mterils were stined for three min. y immersing in fst green (JOHANSEN, 19) nd mounted etween slides using Cndin lsm. The trichomes (dxil nd xil) nd cristlliferous idiolst densities were clculted using light microscope nd y counting the numer of trichomes or cristlliferous idiolsts in the leflet. For ech smple, twenty-four sections of.6 mm 2 ech etween the min vein nd the mrgin were nlyzed. The trichomes were clssified s glndulr nd non-glndulr (LEITE et l., 1999c). Three countings for ech prt of the cnopy (one leflet/counting) were mde for ech smpling of the three crops. For determintion of concentrtions of lef N nd K, fully expnded lef from the upper prt of the cnopy of ech of plnts/crop ws collected monthly. The leves were plced in Krft pper gs, dried in forced ir circultion oven t 67 o C for 3 dys nd ground in Wiley mill (2 mesh). Concentrtion of lef K ws determined with Flme Photometer nd concentrtion of lef N ws nlyzed y the Nessler method (JACKSON, 19). Three replictions (four leves/repliction) were mde for ech smpling of the three crops. For gs chromtogrphy/mss spectrometry (GC/MS) nlysis, fully expnded leves from the upper prt of the cnopy of fifty tomto plnts/crop were otined monthly. The leves were collected nd plced Ciênc. grotec., Lvrs, v. 2, n. 1, p. 2-, jn./fev., 2

3 LEITE, G. L. D. et l. in plstic gs nd seled. Fresh leves (1g) were cut with scissors nd immersed in 1ml of distilled hexne for 2 h. The hexne extrct ws dehydrted with nhydrous N 2 SO, evported t 3 o C in rottory evportor, seled in nitrogen nd stored in freezer. One reding ws mde for ech smpling of the three crops. The hexne extrcts were nlyzed y GC/MS equipped with n uto smpler nd computer sed system to ccumulte dt, nd mss spectr dtse with, compounds using the following conditions: initil oven temperture of 33 C ws progrmmed to C t 2 C min. -1 nd finlly rised to 2 C t C min. -1. The injector nd trnsfer line tempertures were 1 nd 2 C, respectively. The split rtio ws five, with He s the crrier gs. All nlyses were crried on the DB 1 fused cpillry column (3mx.2mm nd film thickness of.2 µm). The mss spectrometer ws scnned etween mu nd the minimum re used for pek integrtion ws 2. ions sec The retention times for the peks with totl ion current (TIC) higher thn 2 x 1 6 ions sec. -1 were recorded nd the compounds identified using the mss spectr dtse. Only compounds with similrity index (SI) greter thn % were considered. Anlysis of vrince nd the Tukey s multiple rnge test (% significnce) were used to test the effect of cnopy height on trichome nd cristlliferous idiolsts densities, nd the numer of mines produced y T. solut nd Liriomyz spp. nd the numer of T. solut eggs. Person s correltion (% significnce) were used to evlute the reltionships etween lef orgnic compounds, lef N nd K concentrtions, lef trichome nd cristlliferous idiolsts densities nd the numer of mines produced y T. solut nd Liriomyz spp. nd the numer of T. solut eggs. RESULTS AND DISCUSSION The 1 nd 2 tomto crops were less ttcked y T. solut s compred to the 3, while the opposite ws oserved for Liriomyz spp. (Figure 1A, B nd C). In crops tht suffered higher ttck y these insects, the ttck ws more intense t the end of the growing seson (Figure 1A, B nd C), proly due to the fct tht these crops were fr from other tomto crops. Thus, they were pprently not colonized y T. solut nor Liriomyz spp. No effect of lef N nd K ws oserved on the T. solut ttck nd positive effect of K (r =.6) ws oserved on the Liriomyz spp. ttck. Letourneu et l. (1996) oserved tht dmge to tomto folige from lefminers did not increse with incresed N concentrtion of the 17 commercil frms. Kneshiro e Johnson (1996) noted tht, lthough pupl weights of Liriomyz trifolii (Burgess) lrve incresed significntly with the lef nitrogen increse, L. trifolii fecundity ws not significntly ffected y nitrogen in the leves upon which the femles developed. However, Leite (1997) reported tht n increse in the lef N content of L. esculentum, grown in greenhouse, reduced the lrvl mortlity, higher pupl weight nd T. solut egg eclosion. Also, this uthor oserved tht n incresed K fertiliztion reduced the numer of lrge mines/lef in L. esculentum nd the rte of egg eclosion of T. solut in wild tomte Lycopersicum hirsutum f. glrtum C.M. Mull (PI 1317). No significnt effect of the trichomes nd cristlliferous idiolsts densities of leves ws noted on T. solut nd Liriomyz ssp. popultions under field conditions, such s oserved y Leite et. l. (199, 1999,, c) with T. solut on L. esculentum in greenhouse. A higher lef trichome density/mm 2 ws recorded on the xil (21.29 ± 1.2) thn on the dxil surfce (.19 ±.7) with the trichomes eing mostly non-glndulr (99.6%), such s oserved y Leite et l. (1999c). The glndulr trichomes nd cristlliferous idiolst densities were reported to show negtive effects on popultions of M. persice in L. hirsutum f. glrtum (PI 1317) (LEITE et l., 1999c). However, L. esculentum possesses minly non-glndulr trichomes (types III, V, nd V) (CHANNARAYAPPA et l., 1992), which re known to e less efficient thn the glndulr trichomes of L. hirsutum in the defense ginst insect ttck (LEITE et l., 1999,, c; LEITE et l., 21). Ciênc. grotec., Lvrs, v. 2, n. 1, p. 2-, jn./fev., 2

4 Intensity of Tut solut (Meyrick, 1917) (Lepidopter... Mines of T. solut/lef Crop 1 Crop 2 Crop 3 A Eggs of T. solut/lef B. Mines of Liriomyz spp./lef C Cristlliferous idiolsts/mm D Broken trichomes (%) E Trichomes/mm F Potssium (% on dry mtter) Apr. My Jun. Jul. Sep. Oct. Nov. G Nitrogen (% on dry mtter) Apr. My Jun. Jul. Sep. Oct. Nov. FIGURE 1 Popultion dynmics of mines (A) nd eggs (B) of Tut solut/lef, nd mines of Liriomyz spp./lef (C), densities of crystlliferous/mm 2 (D) nd percentgem of roken trichomes (E), trichomes (dxil + xil/2)/mm 2 (F), nd potssium (G) nd nitrogen (H) concentrtions (% on dry mtter) in the tomto Lycopersicon esculentum. Symols represent verges of 3 leves for figures A, B nd C, nine evlutions for D, E nd F nd three evlutions for G nd H nd verticl rs stndrd erros of the men. A higher numer of Liriomyz spp. mines ws higher on the upper level thn on the middle nd recorded in the lower thn in the upper level of the lower levels (Figure 2D nd E) nd the percentge tomto plnts (Figure 2A). The opposite ws oserved of roken trichomes ws higher in the middle nd for the numer of T. solut eggs (Figure 2B). lower levels thn t the upper levels (Figure 2F). T. solut mines tended to concentrte on leves on This results re similr to the ones oserved y Leite the middle nd upper levels (Figure 2C). Lef trichome et l. (1999c) in greenhouse for L. esculentum nd nd cristlliferous idiolst densities were L. hirsutum. Ciênc. grotec., Lvrs, v. 2, n. 1, p. 2-, jn./fev., Month H

5 6 LEITE, G. L. D. et l. The results on the preferentil deposition of T. solut nd Liriomyz spp. eggs on the picl leves were in greement with those reported y Coelho et l. (19), Silv et l. (199) nd Oliveir (1999). As leves get older, T. solut mines tended to concentrte in the middle prts of the cnopy while those of Liriomyz spp. on the lower prt of the plnt cnopy (LEITE et l., 1999; OLIVEIRA, 1999). The preferentil oviposition in the upper leves ws proly due to the fct tht these leves re more tender, s they hve lower clcium content (prt of the cellulr wll) nd percentge of lef fire insolule in cid detergent s compred to the middle nd lower leves (MARSCHNER, 199; SILVA et l., 199; LEITE et l., 1999; WEI et l., 2) nd higher nitrogen content (LEITE et l., 199). Four peks of orgnic compounds with retention time (r t ) of 2., 2.23, 2.2 nd.36 min were recorded in the totl ion chromtogrm (TIC) of the hexne extrcts of the L. esculentum leves on GC/MS nlysis (Figure 3). The peks with r t of 2., 2.2 nd.36 min were identified s plmitic cid, hexcosne nd tricontne with similrity index (SI) of 7, 9 nd 9%, respectively. The pek with (r t ) of 2.23 min ws identified s one of the following terpenes: mircene/frnesol/α-humulene/trns cryophyllene with SI of 3%. These compounds hve not een reported in the literture for L. esculentum. Although these compounds were identified with very high SI index, their identity should e confirmed y other methods. These compounds cn e isolted in lrge quntities nd their Mines of Liriomyz spp./lef A Eggs of T. solut/lef B Mines of T. solut/lef C Cristlliferous idiolsts/mm 2 2 D Trichomes/mm 2 2 E Broken trichomes (%) F Upper Middle Lower FIGURE 2 Numer of mines of Liriozyz spp./lef (A), numers of eggs(b) nd mines/lef (C) of Tut solut, densities of crystlliferous idiolsts/mm 2 (D) nd trichome density (dxil + xil/2)/mm 2 (E), nd percentge of roken trichomes (F) in the tomto Lycopersicon esculentum in different levels of the cnopy plnts. Mens followed y the sme letter do not differ y Tukey s multiple rnge test (P <.). Ciênc. grotec., Lvrs, v. 2, n. 1, p. 2-, jn./fev., 2 Cnopy level Upper Middle Lower

6 Intensity of Tut solut (Meyrick, 1917) (Lepidopter... 7 Pek 2. (*1 6 *ions*seg) Crop 1 Crop 2 Crop 3 A Pek 2.23 (*1 6 *ions*seg) B Pek 2.2 (*1 6 *ions*seg) Apr. My Jun. Jul. Sep. Oct. Nov. C Pek.36 (*1 6 *ions*seg) Month Apr. My Jun. Jul. Sep. Oct. Nov. D FIGURE 3 Peks of orgnic compounds leves with retention time of 2. (A), 2.23 (B), 2.2 (C) nd.36 (D) min. in the tomte Lycopersicon esculentum. Symols represent one evlution. identifiction with more precise spectroscopic methods nd the conduction of iossys with the compound with r t of 2. min. re of gret interest, since it positively correlted with T. solut oviposition (r =.7). CONCLUSIONS The tomto lefminers, T. solut nd Liriomyz spp., initite their ttck in the upper leves of the cnopy (site of preferentil oviposition) with their mines concentrting in the middle nd lower prt of the plnt cnopy. When the initil insect popultion is low, higher ttck occurred t the end of the growing seson, showing the importnce of eliminting crop residue nd rotting crops using plnts tht re not hosts of T. solut nd Liriomyz spp. The non glndulr trichomes re not importnt to regulte insect density in these species. Apprently, terpenes re positively ssocited with the oviposition of T. solut while lef K ppers to positively fvor Liriomyz spp. ttck. REFERENCES CHANNARAYAPPA, C.; SHIVASHANKAR, G.; MUNIYAPPA, V.; FRIST, R. H. Resistnce of Lycopersicon species to Bemisi tci, tomto lef curl virus vector. Cndin Journl of Botny, Ottw, v. 7, n. 3, p , COELHO, M. C. F.; FRANÇA, F. H.; CORDEIRO, C. M. T.; YOSHIHIKI, H. Biologi e distriuição espcil de ovos e mins d trç-do-tomteiro. Horticultur Brsileir, Brsíli, v. 1, n. 1, p., 19. FERY, R. L.; KENNEDY, G. G. Genetic Anlysis of 2-tridecnone concentrtion, lef trichome chrcteristics, nd tocco hornworm resistnce in tomto. Journl of the Americn Society for Horticulturl Science, Alexndri, v. 1, n., p. 6-91, 197. FILGUEIRA, F. A. R. Novo mnul de olericultur. Viços: UFV, 2. 2 p. Ciênc. grotec., Lvrs, v. 2, n. 1, p. 2-, jn./fev., 2

7 LEITE, G. L. D. et l. FRANCESCHI, V. R.; HORNER JUNIOR, H. T. Clcium oxlte crystls in plnts. Botnicl Review, New York, v. 6, n. 1, p , 19. JACKSON, M. L. Soil chemicl nlysis. New Jersey: Prentice Hll, p. JOHANSEN, D. A. Plnt microtechnique. New York: McGrw Hill Book, p. KANESHIRO, L. N.; JOHNSON, M. W. Tritrophic effects of lef nitrogen on Liriomyz trifolii (Burgess) nd n ssocited prsitoid Chrysochris oscinidis (Ashmed) on en. Biologicl Control, Sn Diego, v. 6, n. 2, p. -192, LEITE, G. L. D. Efeito d idde, prte do dossel e níveis de dução NK n resistênci de Lycopersicon hirsutum f. glrtum à Tut solut f. Dissertção (Mestrdo em Entomologi) - Universidde Federl de Viços, Viços, LEITE, G. L. D.; PICANÇO, M.; AZEVEDO, A. A.; MOURA, M. F. Efeito de idde de plnts n resistênci por ntixenose de Lycopersicon hirsutum à Tut solut. Agro-Cienci, Chilln, v. 1, n. 1, p. 9-3, 199. LEITE, G. L. D.; PICANÇO, M.; AZEVEDO, A. A.; SILVA, D. J. H.; GUSMÃO, M. R. Intensidde de tque de Frnkliniell schulzei e Myzus persice em três introduções de Lycopersicon peruvinum. Revist d Universidde Rurl, Série Ciênci d Vid, Seropédic, v. 19, n. 1, p. 27-3, LEITE, G. L. D.; PICANÇO, M.; AZEVEDO, A. A.; GONRING, A. H. R. Efeito de tricoms, leloquímicos e nutrientes n resistênci de Lycopersicon hirsutum à trç-do-tomteiro. Pesquis Agropecuári Brsileir, Brsíli, v. 3, n. 11, p , LEITE, G. L. D.; PICANÇO, M.; DELLA L.; MOREIRA, M. D. Role of cnopy height in the resistnce of Lycopersicon hirsutum f. glrtum to Tut solut (Lep.; Gelechiide). Journl Applied of Entomology, Berlin, v. 3, n., p. 9-63, LEITE, G. L. D.; PICANÇO, M.; GUEDES, R. N. C.; SKOWRONSKI, L. Effect of fertiliztion levels, ge nd cnopy height of Lycopersicon hirsutum on the resistnce to Myzus persice. Entomologi Experimentlis et Applict, Dordrecht, v. 91, n. 2, p , 1999c. LEITE, G. L. D.; PICANÇO, M.; GUEDES, R. N. C.; ZANUNCIO, J. C. Role of plnt ge in the resistnce of Lycopersicon hirsutum f. glrtum to the tomto lefminer Tut solut (Lepidopter: Gelechiide). Scienti Horticulture, Amsterdm, v. 9, n. 2, p , 21. LETOURNEAU, D. K.; DRINKWATER, L. E.; SHENNAN, C. Effects of soil mngement on crop nitrogen nd insect dmge in orgnic vs conventionl tomto fields. Agriculture, Ecosystems & Environment, College Prk, v. 7, n. 2-3, p , MARSCHNER, H. Minerl nutrition of higher plnts. London: Acdemic, p. OLIVEIRA, I. R. Ftores que fetm intensidde do tque de Liriomyz trifolii (Burgess) o repolho f. Dissertção (Mestrdo em Entomologi) - Universidde Federl de Viços, Viços, PICANÇO, M.; LEITE, G. L. D.; GUEDES, R. N. C.; SILVA, E. E. A. Yield loss in trellised tomto ffected y insecticidl sprys nd plnt spcing. Crop Protection, London, v. 17, n., p. 7-2, 199. SILVA, C. C.; JHAM, G. N.; PICANÇO, M.; LEITE, G. L. D. Comprison of lef chemicl composition nd ttck ptterns of Tut solut (Meyrick) (Lepidopter: Gelechiide) in three tomto species. Agronomi Lusitn, Liso, v. 6, n. 2-, p , 199. WEI, J. N.; ZOU, L.; KUANG, R. P.; HE, L. P. Influence of lef tissue structure on host feeding selection y pe lef miner Liriomyz huidorensis (Dipter: Agromyzide). Zoologicl Studies, Tokio, v. 39, n., p. 29-3, 2. Ciênc. grotec., Lvrs, v. 2, n. 1, p. 2-, jn./fev., 2