Oviposition of Anstreph frterculus nd Certitis cpitt (Dipter: Tephritide) in Citrus Fruits, nd Development in Reltion to Mturity of Ornge Fruits Authors: Nymã P. Dis, Srin Ongrtto, Muro S. Grci, nd Dori E. Nv Source: Florid Entomologist, 100(2) : 468-473 Pulished By: Florid Entomologicl Society URL: https://doi.org/10.1653/024.100.0209 BioOne Complete (complete.bioone.org) is full-text dtse of 200 suscried nd open-ccess titles in the iologicl, ecologicl, nd environmentl sciences pulished y nonprofit societies, ssocitions, museums, institutions, nd presses. Your use of this PDF, the BioOne Complete wesite, nd ll posted nd ssocited content indictes your cceptnce of BioOne s Terms of Use, ville t www.ioone.org/terms-of-use. Usge of BioOne Complete content is strictly limited to personl, eductionl, nd non-commercil use. Commercil inquiries or rights nd permissions requests should e directed to the individul pulisher s copyright holder. BioOne sees sustinle scholrly pulishing s n inherently collortive enterprise connecting uthors, nonprofit pulishers, cdemic institutions, reserch lirries, nd reserch funders in the common gol of mximizing ccess to criticl reserch.
Oviposition of Anstreph frterculus nd Certitis cpitt (Dipter: Tephritide) in citrus fruits, nd development in reltion to mturity of ornge fruits Nymã P. Dis 1, Srin Ongrtto 1, Muro S. Grci 1, nd Dori E. Nv 2, * Astrct Fruit flies (Dipter: Tephritide) re considered to e one of the principl groups of pests in fruit culture worldwide. The ojective of this study ws to investigte oviposition y Anstreph frterculus (Wiedemnn) nd Certitis cpitt (Wiedemnn) in citrus fruits nd to ssess the development of these species in reltion to the mturity of ornge fruits. The experiments were crried out under controlled temperture conditions (25 ± 2 C), RH (70 ± 10%), nd photoperiod (12:12 h L:D). Oviposition ws evluted y exposure (with nd without choice) to fruits of Nvelin ornge [Citrus sinensis (L.) Oseck], Clemenules tngerine (C. reticult Blnco), nd Sicilino lemon [C. limon (L.)] (Rutcee). Insect development ws studied on Nvelin ornge t 4 stges of mturity (I: 5 cm in dimeter, II: 6 to 7 cm in dimeter, III: skin with color chnge, nd IV: yellow-ornge skin). We evluted oviposition y counting the numer of eggs, nd we ssessed iologicl prmeters of the immture nd dult stges. The numer of eggs deposited in ornge nd tngerine y oth fruit fly species did not differ significntly, nd oviposition did not occur in lemon. Anstreph frterculus preferred to oviposit in tngerine fruits, wheres C. cpitt showed preference for ornge fruits. Development from egg to dult y A. frterculus nd C. cpitt occurred only in stge IV ornges, nd required 30.9 nd 31.0 d, respectively. Femles of A. frterculus nd C. cpitt developing in mture ornge fruits produced men of 378.7 nd 183.5 eggs, respectively. Key Words: South Americn fruit fly; Mediterrnen fruit fly; fruit fly iology; Citrus Resumo As moscs-ds-fruts (Dipter: Tephritide) são considerds um dos principis grupos de prgs n fruticultur mundil. O ojetivo deste trlho foi verificr oviposição de Anstreph frterculus (Wiedemnn) e de Certitis cpitt (Wiedemnn) em frutos cítricos e vlir o desenvolvimento dests espécies em relção o estádio de mturção de frutos de lrnjeir. Os experimentos form relizdos em condições controlds de tempertur (25 ± 2 C), UR (70 ± 10%) e fotoperíodo (12:12 hors L:E). A oviposição foi vlid trvés d exposição (com e sem chnce de escolh) de frutos de lrnjeir [Citrus sinensis (L.) Oseck] cultivr Nvelin, tngerineir (C. reticult Blnco) cultivr Clemenules e limoeiro [C. limon (L.)] cultivr Sicilino (Rutcee). O desenvolvimento foi estuddo trvés d exposição de frutos de lrnjeir Nvelin em qutro estádios (I: 5 cm de diâmetro, II: 6 7 cm de diâmetro, III: csc com mudnç de colorção e IV: csc mrelo-lrnjd). Pr o experimento de oviposição foi vlido o número de ovos e pr o de desenvolvimento determinou-se os prâmetros iológicos ds fses imturs e dult. O número de ovos colocdos em lrnj e tngerin pr ms s espécies de mosc-ds-fruts, não diferiu significtivmente, sendo que em limão não ocorreu oviposição. Anstreph frterculus preferiu ovipositr em frutos de tngerineir, enqunto C. cpitt presentou preferênci por frutos de lrnjeir. O desenvolvimento de ovo-dulto de A. frterculus e C. cpitt em lrnjs Nvelin ocorreu somente no estádio IV e teve durção de 30,90 e 31,04 dis, respectivmente. Fêmes de A. frterculus e de C. cpitt oriunds de frutos deste estádio colocrm em médi 378,7 e 183,5 ovos. Plvrs Chve: mosc-ds-fruts sul-mericn; mosc-do-mediterrâneo; iologi de moscs-ds-fruts; Citrus Fruit flies (Dipter: Tephritide) re considered thret to fruit orchrds worldwide due to the dmge cused y loss of fruit qulity nd to qurntine rriers imposed y importing countries (Ruiz et l. 2014). In southern Brzil, Anstreph frterculus (Wiedemnn) nd Certitis cpitt (Wiedemnn) re the 2 principl fruit fly species of griculturl importnce (Nv & Botton 2010). Economic loss in citrus cn rech 20% in orchrds infested with A. frterculus (Silv et l. 2014) nd up to 7.5% in those infested with C. cpitt (Piv & Prr 2013). The South Americn fruit fly, A. frterculus, is ntive to South Americ nd occurs in tropicl nd sutropicl regions. It infests 109 plnt species in Brzil (Zucchi 2008). The Mediterrnen fruit fly, C. cpitt, is indigenous to Afric nd occurs worldwide. In Brzil, it infests 88 species of fruit (Zucchi 2008; Peñrrui-Mrí et l. 2014). One importnt event in the life cycle of holometolous phytophgous insects is choosing n oviposition site s this choice is essentil for the survivl nd success of offspring (Segur et l. 2007). The lrve hve little moility nd depend on nutritionl resources selected y femles t the time of oviposition (Ionnou et l. 2012). In generl, insects use physicl stimuli such s texture, color, shpe, nd size, plus chemicl spects such s nutrients, wter content, ttrctive nd repellent sustnces, to choose host (López-Guillén et l. 2010). 1 Universidde Federl de Pelots, Deprtmento de Fitossnidde, 96900-010, Pelots, Brzil; E-mil: nym.dis@gmil.com (N. P. D.), srin.ongrtto@hotmil.com (S. O.), grcismuro@yhoo.com.r (M. S. G.) 2 Emrp Clim Temperdo, Lortório de Entomologi, 96010-971, Pelots, Brzil; E-mil: dori.edson-nv@emrp.r (D. E. N.) *Corresponding uthor; E-mil: dori.edson-nv@emrp.r (D. E. N.) 468 2017 Florid Entomologist Volume 100, No. 2
Dis et l.: Oviposition nd development of fruit flies in citrus 469 Tephritids hve rnge of hosts to choose from, nd these hosts provide vrying levels of physicl nd chemicl stimuli. Monophgous species respond positively to restricted set of voltile nd visul stimuli, compred with polyphgous species (Díz-Fleischer et l. 2000). Although this differentition my confer n dvntge to polyphgous insects, host selection does not occur without ny costs ecuse highly polyphgous femles commonly oviposit in species tht llow only low lrvl performnce (Aluj & Mngn 2008). Certitis cpitt provides good exmple; it is considered to e one of the most polyphgous pests, s it infests pproximtely 300 species of fruit, including Citrus species (Rutcee) (Peñrrui-Mrí et l. 2014). Fruit fly infesttion levels vry ccording to cultivr, orchrd loction, nd climte (Ruiz et l. 2014; Silv et l. 2014). Fruit trees feture mechnisms tht ffect the development nd reproduction of Tephritide (Bck & Pemerton 1918; Bodenheimer 1951), including chnges in the physiochemicl properties of fruits (Ppchristos et l. 2008). However, despite the importnt influence of citrus hosts on the occurrence of Tephritide, their reltionship is still little studied. Becuse physicl nd chemicl properties of host fruits chnge with mturity, this study investigted oviposition y A. frterculus nd C. cpitt in ornge, tngerine, nd lemon fruits. We lso evluted the development of these species in ornge fruits of differing mturity. Mterils nd Methods CULTURE OF A. FRATERCULUS AND C. CAPITATA Culture nd experiments were conducted in the Lortory of Entomology of Emrp Clim Temperdo (Pelots, Rio Grnde do Sul Stte, Brzil), in ir conditioned rooms, with temperture set t 25 ± 2 C, RH of 70 ± 10%, nd photoperiod of 12:12 h L:D. Anstreph frterculus ws rered in mngo fruits (Mngifer indic L.; Ancrdicee) nd C. cpitt in ppy fruits (Cric ppy L.; Criccee). Both cultures were estlished with wild insects otined from fruits of tngoreiro [Citrus sinensis (L.) Oseck C. reticult Blnco] cultivr Ortnique, collected in commercil orchrd in the municiplity of Rosário do Sul (Rio Grnde do Sul, Brzil) (30.1512861 S, 55.2049694 W). Fruits were offered to the fruit flies for oviposition in wooden cges (50 50 40 cm) for period of 24 h. Then, the fruits were pcked in plstic continers (11 12 19 cm) (Snremo, Esteio, Rio Grnde do Sul, Brzil) contining lyer of finely textured vermiculite (Crolin Soil do Brsil, Snt Cruz do Sul, Rio Grnde do Sul, Brzil) nd topped with nonwoven fric. At puption, the insects were trnsferred to Petri dishes (10 cm in dimeter 1.5 cm high) (Ksvi, Curiti, Prná, Brzil) contining moistened vermiculite, where they remined until emergence. The dults were kept in wooden cges (50 50 40 cm) covered with voile fric. Adults were provided solid diet of sugr (União, São Pulo, Brzil), whet germ (Wlmon, São Pulo, Brzil), nd yest (Biorigin, Lençóis Pulist, São Pulo, Brzil) t the rtio of 3:1:1 in plstic continer (50 ml). In similr continer, distilled wter ws offered vi sponge cloth (Spontex, Ilhéus, Bhi, Brzil). Wter nd diet were provided continuously. FRUITS We used fruits of Nvelin ornge, Clemenules tngerine, nd Sicilino lemon otined from commercil orchrds in the municiplity of Rosário do Sul (30.1011111 S, 54.7172250 W nd 30.1512861 S, 55.2049694 W). For the oviposition experiments, mture fruits were collected ner the hrvest period sed on the outside color of the peel (Agustí et l. 1995). The fruits were protected from insect ttck for 45 d efore the collections y using wire cges (1.20 m long 0.45 m high) wrpped with voile fric (1.80 m long 0.50 m high) nd ttched to the rnches. Also, Nvelin ornges were collected nd used to chrcterize insect development in reltion to fruit mturity. OVIPOSITION IN CITRUS FRUITS: CHOICE TESTS Femles were offered 3 fruits simultneously or comined in pirs, for period of 24 h. Ornge, tngerine, nd lemon fruits were offered simultneously using 10 cges (24 12 17 cm), ech contining thirty 15-d-old femles. The pired fruit comintions studied were ornge nd tngerine, ornge nd lemon, nd tngerine nd lemon. For pired fruit tests, we used 10 cges (24 12 17 cm) for ech comintion, nd 20 insects (15-d-old femles) were plced in ech cge. After 24 h, the fruits were removed, sliced with sclpel nd inspected with stereoscopic microscope (Zeiss, model Stemi SV 11, t 10 mgnifiction) to count the eggs. The pired fruit experiments were conducted in completely rndomized design. OVIPOSITION IN CITRUS FRUITS: NO-CHOICE TESTS We provided 10 fruits of ech prospective plnt host in wooden cges (50 50 40 cm) to ech fruit fly species for 24 h. Ech cge contined one hundred 15-d-old femles. The sme procedure performed in the choice experiment ws used to count eggs. The experiment ws conducted in completely rndomized design with 10 repetitions (cges). FRUIT MATURITY After the ornge trees flowered in 2013/14, fruit development ws monitored to chrcterize 4 stges using methods dpted from Agustí et l. (1995). We collected 10 fruits per plnt from ech of 6 plnts every 15 d throughout the fruiting period. The plnts were identified with white rions fixed to the rnches nd the fruits were gged in wire cges. The 4 stges were defined s: I, fruit of pproximtely 5.0 cm dimeter (three-qurters of finl size); II, fruit of 6 to 7 cm dimeter (green fruit ner the finl size); III, fruit color chnging from green to yellow; nd IV, end of ripening, when the fruit is yellow-ornge in color [in this stge, the rtio of totl solule solids to totl titrtle cidity (TSS/TTA) is 20]. For the physicochemicl nlyses, 10 fruit smples of ech stge were used. In the physicl nlysis, we determined fruit weight (g), dimeter (cm), nd skin thickness (mm). The fruits were weighed on semi-nlyticl scle (Shimdzu do Brsil, model BL 3200H). Fruit dimeter nd skin thickness were mesured using digitl cliper (Stinless, Hrdened model). Chemicl nlyses determined the ph, totl solule solids, nd totl titrtle cidity, nd ll the nlyses were mde in triplicte. The ph ws determined using ph meter (Phtek, model PHS 3B with Ruosull E-900 electrode). This nlysis mesured the ph in juice smples otined in microprocessor (Philips Wlit, model RI7620). Totl solule solids were determined from the smple of fruit juice y using digitl Refrctometer (Biorix, model 106-D) with utomtic temperture compenstion, nd the results were expressed in Brix. Totl titrtle cidity of the juice ws determined y titrtions with solution of 0.1 N NOH nd phenolphthlein indictor. Totl titrtle cidity results were expressed s percentge of citric cid, using the formul Vg N f Eq.Ac. 10 V (Brsil 1986), where Vg: volume of NOH required (ml); N: normlity of NOH solution used (0.1 N); f: correction fctor otined for stndrdiztion of NOH = 1.00; Eq. Ac.: equivlent grm of citric cid (64.04); nd V: volume of smple (1 ml). The mturtion index ws clculted y the reltionship Totl solule solids/totl titrle cidity.
470 2017 Florid Entomologist Volume 100, No. 2 DEVELOPMENT OF A. FRATERCULUS AND C. CAPITATA Fruits were offered to femles in wooden cges (50 50 40 cm). Six replicte cges were used for ech species, ech contining one hundred 15-d-old femles. In ech cge, 10 ornges were exposed to the flies for 24 h. Afterwrds, the fruits were plced individully in plstic continers (10 8.5 cm) on lyer of vermiculite. The continers were closed with fine mesh. After 10 d, the fruits were checked dily, nd the pupe were removed nd fter 24 h weighed on precision nlyticl scle (Shimdzu do Brsil, model AUY 220). The pupe were then individully plced in crylic tues (2.5 4.8 2.5 cm) contining moist vermiculite until emergence. This procedure enled determintion of the pupl weight, durtion, nd viility. After dult emergence, the sex rtio ws determined nd 25 individul pirs were held in cges mde of 500 ml trnsprent plstic cups with 6 mm dimeter holes on top. The pirs were fed with solid diet s descried for insect culture. We lso provided wter in 10 ml crylic continers. Fecundity ws determined using n rtificil sustrte for oviposition s descried y Slles (1992). This sustrte ws offered to femles of A. frterculus nd C. cpitt nd ws replced dily. We conducted dily oservtions to determine the numer of eggs, the periods of pre-oviposition nd oviposition, fecundity, nd longevity of oth mles nd femles. To ssess fertility, 30 eggs from the second oviposition of ech femle were removed from the rtificil sustrtes. The eggs were removed with surgicl lde nd rush, nd plced on moist sustrte inside Petri dishes, wrpped with PVC film, nd mintined in room t 25 C until htching, when the numer of lrve ws counted. This experiment ws conducted in rndomized lock design with 4 tretments (stges of mturity) nd 60 repetitions (fruits). For the iology of the 2 species of fruit fly, 25 repetitions were used, ech consisting of n insect pir. STATISTICAL ANALYSES The men numers of eggs in the fruit were checked for normlity using the Shpiro Wilk test (Shpiro & Wilk 1965) nd outliers detected using stndrd devitions. The men numers of eggs deposited in 3-wy choice tests were sujected to ANOVA nd compred using Tukey s test. In 2-choice tests, the men numers of eggs were squre root trnsformed ( x + 0.5 ) nd nlyzed with Student s t test. We lso compred the influence of the presence of lemon in ech comintion of fruits with Student s t test. The physicl nd chemicl chrcteristics of the ornges t 4 stges of mturity were nlyzed y ANOVA nd the mens seprted using Tukey s test. Anlyses were conducted using the sttisticl progrm BioEstt 5.3 (Ayres et l. 2007). In ddition, mle nd femle longevity dt were nlyzed in the sttisticl progrm JMP 5.0.1 (SAS Version 5.0.1, SAS Institute, Cry, North Crolin) using the survivl nlysis function. Survivl curves were determined for ech species of fruit fly y using the Kpln Meier estimtor, nd were compred using the log-rnk test (Frncis et l. 1993). Results OVIPOSITION IN CITRUS FRUITS In the 3-wy choice test, A. frterculus preferred to oviposit in tngerine nd C. cpitt in ornge. There ws no oviposition in lemon fruits y either species (Tle 1). This ehvior ws lso recorded when the fruits were offered in pirs (Tle 2). With respect to the potentil influence of lemon on oviposition in ornge or tngerine, there were Tle 1. Men numers (± SD) of eggs of Anstreph frterculus nd Certitis cpitt recovered from citrus fruit offered simultneously in 3-wy comprison. Fruit Anstreph frterculus Certitis cpitt Ornge 1.5 ± 1.5 3.0 ± 1.7 Tngerine 3.5 ± 0.9 1.7 ± 1.4 Lemon 0.0 ± 0.0 c 0.0 ± 0.0 c Overll men 1.7 1.5 CV (%) 1.3 1.4 Mens within column followed y the sme lowercse letters did not differ y the Tukey test (P > 0.05). Coefficient of vrition. no significnt differences (P = 0.4970 nd P = 0.6633, respectively) in the numer of eggs deposited y A. frterculus (Tle 3). For C. cpitt, we oserved greter oviposition in ornge when it ws offered in comintion with lemon (P = 0.0336) nd less significnt trend (0.0975) for the sme pttern with tngerine (Tle 3). In no-choice tests, there ws no significnt difference in frequency of oviposition in ornge or tngerine y either A. frterculus or C. cpitt (Tle 4). In lemon, there ws no oviposition y either species of fruit fly. DEVELOPMENT OF A. FRATERCULUS AND C. CAPITATA Fruit fly lrve could develop successfully only in stge IV fruits (lte mturtion, rtio TSS/TTA 20), when there ws significnt reduction in the peel thickness, in totl cidity, nd consequently n increse of the rtio TSS/TTA (Tle 5). Infesttion indices t this stge were 0.72 nd 2.05 pupe per fruit for A. frterculus nd C. cpitt, respectively (Tle 5). The durtion of the egg-to-dult period of A. frterculus nd C. cpitt ws on verge 30.9 nd 31.0 d, respectively (Tle 6). The pre-oviposition period of A. frterculus nd C. cpitt ws on verge 15.2 nd 14.1 d, respectively, nd the oviposition period lsted on verge 14.2 nd 18.2 d, respectively (Tle 6). Most oviposition (80%) occurred in the first 17 to 20 d of the oviposition period for A. frterculus nd C. cpitt, respectively, nd the oviposition pek occurred on dy 11 (299 eggs) for A. frterculus nd on dy 16 for C. cpitt (269 eggs) (Fig. 1). Femles of oth A. frterculus nd C. cpitt survived on verge for 40.5 d. Mle longevity ws on verge 46.5 nd 65.2 Tle 2. Men numers (± SD) of eggs of Anstreph frterculus nd Certitis cpitt in citrus fruits offered in pired comprison tests. Comintion Men no. of eggs t vlue P vlue CV (%) c Anstreph frterculus Ornge 1.2 ± 1.6 3.2913 0.0040 1.30 Tngerine 3.3 ± 1.6 0.49 Ornge 1.8 ± 1.8 1.00 Tngerine 3.5 ± 1.2 0.33 Certitis cpitt Ornge 2.2 ± 1.5 2.9430 0.0087 0.70 Tngerine 0.5 ± 0.8 1.69 Ornge 3.8 ± 1.1 0.29 Tngerine 1.7 ± 1.7 1.00 Men numers of eggs were compred y the Student t test (P = 0.05). The t tests were not conducted where no oviposition occurred. c Coefficient of vrition.
Dis et l.: Oviposition nd development of fruit flies in citrus 471 Tle 3. Effects of the presence of lemon on oviposition y Anstreph frterculus nd Certitis cpitt when offered in comintion with ornge or tngerine. Comintion Men no. of eggs t vlue P vlue Anstreph frterculus Ornge (with lemon) 1.8 (1.8) 0.6932 0.4970 Ornge (with tngerine) 1.2 (1.6) Tngerine (with lemon) 3.5 (1.2) 0.4426 0.6633 Tngerine (with ornge) 3.3 (1.6) Certitis cpitt Ornge (with lemon) 3.8 (1.1) 2.4260 0.0336 Ornge (with tngerine) 2.2 (1.5) Tngerine (with lemon) 1.7 (1.7) 1.7473 0.0975 Tngerine (with ornge) 0.5 (0.8) Men numers of eggs for ech fruit, within ech comintion (± stndrd devition), compred using the Student t test (P = 0.05). Tle 4. Men numers (± SD) of eggs of Anstreph frterculus nd Certitis cpitt exposed to only 1 type of citrus fruit (no-choice tests). Fruit Anstreph frterculus Certitis cpitt Ornge 2.8 ± 1.9 5.1 ± 1.7 Tngerine 3.1 ± 2.0 5.7 ± 2.1 Lemon 0.0 ± 0.0 0.0 ± 0.0 Overll men 1.9 2.8 CV (%) 1.4 0.7 Mens within column followed y the sme letters did not differ y the Tukey test (P > 0.05). Coefficient of vrition. d, respectively, ut no significnt differences were oserved etween A. frterculus nd C. cpitt for longevity of femles (P = 0.7382) or mles (P = 0.6185). Discussion Oviposition in choice tests for tngerine nd ornge indicted no influence of the presence of lemon fruit in the choice of the host y A. frterculus. However, C. cpitt femles displyed preference for oviposition in ornge when lemon ws present. Fruiting of Nvelin ornge nd Sicilino lemon occurs in the sme period (Fe to Jul). Therefore, there my e preference for oviposition in ornge when these citrus cultivrs re found in the sme site. López-Guillén et l. (2010) stted tht choice for the host is influenced y visul nd chemicl stimuli. Thus, femles of C. cpitt my hve identified compounds unsuitle for the development of their offspring in lemon. Also, Slvtore et l. (2007) found tht the citrus compounds coumrin nd linlool, which re found in fruits of Sicilino lemon, were toxic to lrve of C. cpitt. Aluj et l. (2003) reported the preference of A. frterculus for tngerine fruits. However, they reported tht infesttion of A. frterculus in ornge fruits did not generte vile individuls. For C. cpitt, Stu et l. (2008) found tht Vlenci ornge ws more susceptile thn Imperil tngerine nd Sicilino lemon, corroorting the results otined in this study. The preference of tephritid femles for ornge nd tngerine fruits my e relted to the suitility of the hosts for their offspring. Thus, femles would prefer to oviposit in hosts tht optimize lrvl performnce (Nufio & Ppj 2004), descried y Emlen (1966) s optiml forging. In lemon fruits, there ws no oviposition for oth species of fruit fly, supporting the dt otined y Sá et l. (2008), Alvreng et l. (2009), nd Dis & Silv (2014). Although Quyle (1916) ttriutes the non-cceptnce of lemon for oviposition y Tephritide to fruit pulp cidity, other uthors elieve tht lemon pulp cn e suitle for lrvl development nd the non-cceptnce would e linked to voltile compounds in the fruit skin (Ruiz et l. 2014). However, Slvtore et l. (2007) rtificilly infested Sicilino lemon with eggs of C. cpitt nd otined up to 98% mortlity of lrve. The uthors ttriuted the high mortlity to the comined ction of egg encpsultion in essentil oil glnds of the flvedo nd the toxicity of the ledo. However, the reltionship of fruit cidity with the development of fruit flies hs not yet een demonstrted. Our dt on infesttion of mture Nvelin ornge fruits confirm the results otined y Greny et l. (1985), showing tht unripe fruits do not provide idel conditions for development of tephritid lrve. Silv et l. (2014) nd Dis et l. (2013) reported similr results with A. frterculus in ornge (0.86 pupe per fruit). It ws evident tht there ws greter susceptiility of mture ornge, especilly to C. cpitt, which supports the work of Joquim-Brvo et l. (2001), Lopes et l. (2009), nd Arredondo et l. (2015). Overll, oth ornge nd tngerine fruits were ccepted for oviposition y A. frterculus nd C. cpitt, ut lemon fruits were not. Anstreph frterculus showed preference for oviposition in Clemenules Tle 5. Men vlues (± SD) of physicl nd chemicl chrcteristics of ornge, nd the infesttion index (IF) of Anstreph frterculus (A.f.) nd of Certitis cpitt (C.c.) in 4 mturtion stges. Agriculturl crop 2013/14. Stge Weight Dimeter Thickness ph of juice TSS TTA c Rtio TSS/TTA I 55.03 ± 5.11 c 4.74 ± 0.19 c 7.68 ± 0.71 2.85 ± 0.09 c 9.90 ± 0.88 c 0.84 ± 0.01 11.75 ± 1.07 d (49.43 67.00) (4.46 5.01) (6.63 8.71) (2.71 3.04) (8.60 11.30) (0.83 0.86) (9.95 13.27) II 120.04 ± 8.02 6.19 ± 0.24 4.43 ± 0.28 3.12 ± 0.09 10.20 ± 0.30 c 0.78 ± 0.01 13.04 ± 0.34 c (106.78 132.39) (5.86 6.67) (4.03 4.99) (2.99 3.23) (9.90 10.90) (0.76 0.79) (12.47 13.73) III 245.87 ± 22.45 7.80 ± 0.27 3.48 ± 0.34 c 3.56 ± 0.14 10.7 ± 0.50 0.59 ± 0.00 c 17.95 ± 0.99 (210.80 284.07) (7.35 8.30) (3.03 3.99) (3.32 3.73) (10.00 11.40) (0.59 0.61) (16.44 19.18) IV 257.30 ± 23.89 7.98 ± 0.32 2.49 ± 0.37 d 3.56 ± 0.05 11.10 ± 0.25 0.52 ± 0.00 d 21.27 ± 0.70 0.72 2.05 (217.37 281.89) (7.36 8.43) (1.82 2.97) (3.48 3.66) (10.80 11.60) (0.51 0.54) (20.08 22.17) CV (%) d 10.07 3.97 10.20 3.10 5.19 1.50 5.18 Vlues in column followed y the sme letter did not differ significntly using Tukey s test (P > 0.05). Vlues in prentheses indicte the rnge. Stges: I, fruit of pproximtely 5.0 cm dimeter; II, fruit of 6.0 to 7.0 cm dimeter; III, green fruit chnging to yellow; nd IV, mture ornge fruit (TSS/TTA 20). Totl solule solids. c Totl titrtle cidity, expressed s percentge of citric cid. d Coefficient of vrition. A.f. IF C.c.
472 2017 Florid Entomologist Volume 100, No. 2 Tle 6. Men vlues (± SD) nd rnge of iologicl prmeters of immtures nd dults of Anstreph frterculus nd Certitis cpitt when developing in stge IV ornges. Biologicl prmeter Anstreph frterculus Certitis cpitt CV (%) Period egg to dult (d) 30.9 ± 1.30 31.0 ± 2.01 5.34 (29.0 32.0) (28.0 37.0) Weight of pupe (mg) 12.6 ± 0.31 11.5 ± 0.53 3.55 (11.8 12.9) (10.2 13.0) Numer of pupe 0.7 ± 1.35 2.1 ± 3.18 17.21 (1.0 5.0) (1.0 13.0) Viility of pupe (%) 61.1 ± 30.46 70.3 ± 19.60 38.88 (25.0 100.0) (50.0 100.0) Sex rtio (femle/mle) 0.48 0.50 Pre-oviposition period (d) 15.2 ± 1.54 14.1 ± 2.64 14.45 (13.0 18.0) (8.0 21.0) Oviposition period (d) 14.2 ± 2.94 18.2 ± 4.60 22.86 (10.0 19.0) (10.0 25.0) Fecundity (numer of eggs) 378.7 ± 61.54 183.5 ± 56.08 23.40 (306.0 473.0) (106.0 294.0) Fertility (%) 60.4 ± 7.48 62.0 ± 5.20 10.38 (43.8 69.2) (50.0 67.7) Vlues in prentheses indicte the rnge. Coefficient of vrition. tngerine fruits, wheres C. cpitt preferred Nvelin ornge fruits. Bsed on the infesttion of fruit flies determined in ornge, oth species preferred to oviposit in ripe fruits. Fig. 1. Frequency of oviposition y femles of Anstreph frterculus (A) nd Certitis cpitt (B) when provided with ornges s n oviposition sustrte. Acknowledgments The uthors wish to thnk the Ntionl Council of Technologicl nd Scientific Development (CNPq), Coordintion for the Improvement of Higher Eduction Personnel (CAPES), nd the Brzilin Agriculturl Reserch Corportion (EMBRAPA) for the finncil support nd scholrship. References Cited Agustí M, Zrgoz S, Bleiholder H, Buhr L, Hck H, Klose R, Stu R. 1995. Escl BBCH pr l descripción de los estdios fenológicos del desrrollo de los grios (Gén. Citrus). Levnte Agrícol 332: 189 199. Aluj M, Mngn RL. 2008. Fruit fly (Dipter: Tephritide) host sttus determintion criticl conceptul, methodologicl nd regultory considertions. Annul Review of Entomology 53: 473 502. Aluj M, Pérez-Stples D, Mcís-Ordóñez R, Piñero J, McPheron B, Hernández- Irtiz V. 2003. Nonhost sttus of Citrus sinensis cultivr Vlenci nd C. prdisi cultivr Ruy Red to Mexicn Anstreph frterculus (Dipter: Tephritide). Journl of Economic Entomology 96: 1693 1703. Alvreng CD, Mtrngolo CAR, Lopes GN, Silv MA, Alves DA, Nscimento AS, Zucchi RA. 2009. Moscs-ds-fruts (Dipter: Tephritide) e seus prsitoides em plnts hospedeirs de três municípios do norte do estdo de Mins Geris. Arquivos do Instituto Biológico 76: 195 204. Arredondo J, Ruiz L, López G, Díz-Fleischer F. 2015. Determintion of the host sttus of the Persin lime (Citrus ltifoli Tnk) for Anstreph ludens (Loew) (Dipter: Tephritide). Journl of Economic Entomology 108: 77 87. Ayres M, Ayres Jr M, Ayres DL, dos Sntos AAS. 2007. BioEstt plicções esttístics ns áres ds Ciêncis Bio-médics. Mmiruá ONG [ed.], Belém, Prá, Brzil. Bck EA, Pemerton CE. 1918. The Mediterrnen Fruit Fly. Bulletin of the United Sttes Deprtment of Agriculture 640: 1 43. Bodenheimer FS. 1951. Citrus Entomology in the Middle Est. Dr. W. Junk, The Hgue, The Netherlnds. Brsil. 1986. Ministério d Agricultur. Portri nº 76 de 26 de novemro de 1986. Dispõe sore os métodos nlíticos de eids e vingre. Seção 1, pt. 2. Diário Oficil d Repúlic Federtiv do Brsil, Brsíli, Brzil. Dis NP, Silv FFD. 2014. Moscs-ds-fruts (Dipter: Tephritide e Loncheide) n região d Fronteir Oeste do Rio Grnde do Sul. Revist de Ciêncis Agráris 57: 29 34. Dis NP, Silv FFD, Areu JAD, Pzini JB, Bott RA. 2013. Nível de infestção de moscs-ds-fruts em fix de fronteir, no Rio Grnde do Sul. Revist Ceres 60: 589 593. Díz-Fleischer F, Ppj DR, Prokopy RJ, Aluj M, Norrom AL. 2000. Evolution of fruit fly oviposition ehvior, pp. 811 841 In Aluj M, Norrom AL [eds.], Fruit Flies (Tephritide): Phylogeny nd Evolution of Behvior. CRC Press, Boc Rton, Florid. Emlen JM. 1966. The role of time nd energy in food preference. The Americn Nturlist 100: 611 617. Frncis B, Green M, Pyne C. 1993. Sttisticl system for generlized liner interctive modelling, 4th Edition. Clrendon Press, Oxford, United Kingdom. Greny PD, Shw PE, Dvis PL, Htton TT. 1985. Senescence-relted susceptiility of Mrsh grpefruit to lortory infesttion y Anstreph suspens. Florid Entomologist 68: 144 150. Ionnou CS, Ppdopoulos NT, Kouloussis NA, Tnnki CI, Ktsoynno BI. 2012. Essentil oils of citrus fruit stimulte oviposition in the Mediterrnen fruit fly Certitis cpitt (Dipter: Tephritide). Physiologicl Entomology 37: 330 339. Joquim-Brvo IS, Fernndes OA, Bortoli SA, Zucoloto FS. 2001. Oviposition preference hierrchy in Certitis cpitt (Dipter: Tephritide) Influence of femle ge nd experience. Iheringi Série Zoológic 91: 93 100. Lopes EB, Brito CHD, Btist JDL, Aluquerque ICD. 2009. Preferênci de oviposição de Certitis cpitt em tngerin (Citrus reticult) so condições de lortório. Tecnologi & Ciênci Agropecuári 3: 41 45. López-Guillén G, Toledo J, Rojs JC. 2010. Response of Anstreph oliqu (Dipter: Tephritide) to fruit odors nd protein-sed lures in field trils. Florid Entomologist 93: 317 318. Nv DE, Botton M. 2010. Bioecologi e controle de Anstreph frterculus e Certitis cpitt em pessegueiro. Emrp Clim Temperdo, http://www. infotec.cnpti.emrp.r/hndle/doc/889693 (lst ccessed 15 Apr 2015). Nufio CR, Ppj DR. 2004. Superprsitism of lrvl hosts y the wlnut fly, Rhgoletis juglndis, nd its implictions for femle nd offspring performnce. Oecologi 141: 460 467.
Dis et l.: Oviposition nd development of fruit flies in citrus 473 Piv PEB, Prr JRP. 2013. Hydrogen ionic potentil (ph) of the ttrctnt, trp density nd control threshold for Certitis cpitt (Dipter: Tephritide) on Hmlin ornges in São Pulo centrl region, Brzil. Revist Brsileir de Fruticultur 35: 464 470. Ppchristos DM, Ppdopoulos NT, Nnos GD. 2008. Survivl nd development of immture stges of the Mediterrnen fruit fly (Dipter: Tephritide) in citrus fruit. Journl of Economic Entomology 101: 866 872. Peñrrui-Mrí E, Quilici S, Schmitt C, Escudero-Colomr LA. 2014. Evlution of cndidte systems for mss trpping ginst Certitis spp. on L Réunion Islnd. Pest Mngement Science 70: 448 453. Quyle HJ. 1916. Citrus fruit insects in Mediterrnen countries. Bulletin of the United Sttes Deprtment of Agriculture 134: 1 36. Ruiz MJ, Júrez ML, Alzogry RA, Arrighi F, Arroyo L, Gstminz G, Willink E, Brdo ADV, Ver T. 2014. Toxic effect of Citrus peel constituents on Anstreph frterculus Wiedemnn nd Certitis cpitt Wiedemnn immture stges. Journl of Agriculturl nd Food Chemistry 62: 84 91. Sá RF, Cstellni MA, Nscimento AS, Brndão MHST, Silv AND, Pérez-Mluf R. 2008. Índice de infestção e diversidde de moscs-ds-fruts em hospedeiros exóticos e ntivos no pólo de fruticultur de Angé, BA. Brgnti 67: 401 411. Slles LAB. 1992. Metodologi de crição de Anstreph frterculus (Wiedemnn, 1830) (Dipter: Tephritide) em diet rtificil em lortório. Anis d Sociedde Entomológic do Brsil 21: 479 486. Slvtore A, Borkosky S, Willink E, Brdón A. 2007. Mecnismos de resistenci químic ofrecidos por el limón l tque de Certitis cpitt, pp.1 5 In Ploper LD [ed.], Moscs de los frutos y su relevnci curentenri en l citricultur del noroeste de Argentin, once ños de investigciones 1996 2007. EEAOC, Sn Miguel del Tucumán, Argentin. Segur DF, Viscrret MM, Pldino LZC, Ovruski SM, Clder JL. 2007. Role of visul informtion nd lerning in hitt selection y generlist prsitoid forging for conceled hosts. Animl Behvior 74: 131 142. Shpiro SS, Wilk MB. 1965. An nlysis of vrince test for normlity (complete smples). Biometrik 52: 591 611. Silv FFD, Redelli LR, Meirelles RN, Dl Soglio FK. 2014. Dnos de moscs-dsfruts (Dipter, Tephritide) em citros, mnejdos no sistem orgânico de produção. Revist Ceres 61: 637 642. Stu C, Lim DF, Mjer JD. 2008. Determintion of host sttus of citrus fruits ginst the Mediterrnen fruit fly, Certitis cpitt (Wiedemnn) (Dipter: Tephritide). Austrlin Journl of Entomology 47: 184 187. Zucchi RA. 2008. Fruit flies in Brzil. Universidde de São Pulo, Deprtmento de Entomologi e Acrologi, http://www.le.eslq.usp.r/fruitflies (lst ccessed 15 Apr 2015).