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Development of Anastrepha fraterculus (Diptera Tephritidae)Related to the Phenology of Blueberry Blackberry StrawberryGuava and Surinam Cherry FruitsAuthor(s) M Bisognin D E Nava G I Diez-Rodriacuteguez R A Valgas M SGarcia A C R Krolow and L E C AntunesSource Journal of Economic Entomology 108(1)192-200Published By Entomological Society of AmericaURL httpwwwbiooneorgdoifull101093jeetou002

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HORTICULTURAL ENTOMOLOGY

Development of Anastrepha fraterculus (Diptera Tephritidae)Related to the Phenology of Blueberry Blackberry Strawberry

Guava and Surinam Cherry Fruits

M BISOGNIN1 D E NAVA23 G I DIEZ-RODRIGUEZ2 R A VALGAS2 M S GARCIA1

A C R KROLOW2 AND L E C ANTUNES2

J Econ Entomol 108(1) 192ndash200 (2015) DOI 101093jeetou002

ABSTRACT Anastrepha fraterculus (Wiedemann 1830) is the main pest of temperate climate orchard-ing The study investigated the development of A fraterculus related to phenological stage of blueberryblackberry strawberry guava and Surinam cherry trees The phenological stages I (green fruits) II(intermediate ripening stage of fruits) and III (fruits close to harvesting) were determined and they arefrom 8th 10th and 11th week 6th 8th and 9th week 8th 13th and 16th week and 5th 6th and 7thweek after the first flowering of blueberry blackberry strawberry guava and Surinam cherry treesrespectively We collected fruits from orchards to determine the infestation index using the formulanumber of pupafruit weight To investigate the development of A fraterculus we determined thefollowing biological parameters egg-to-adult period weight of pupae oviposition period fecunditynumber of pupae and number of infested fruits The infestation index for the fruits collected in the fieldwas greater in strawberry guava and Surinam cherry fruits In the laboratory the development ofA fraterculus occurred in stage III of blueberry In blackberry besides stage III we also observedthe development in stage II however at lower infestation In strawberry guava the development ofA fraterulus occurred in stages II and III and the development in both stages was similar For Surinamcherry the development occurred in the three phenological stages with similar values for biologicalparameters Overall of the four hosts studied the strawberry guava and Surinam cherry fruits allowed abetter biological development of A fraterculus corroborating its preference for fruits native to Brazil

KEY WORDS fruit fly berry native fruit biology infestation season

Introduction

The South American fruit fly [Anastrepha fraterculus(Wiedemann 1830) (Diptera Tephritidae)] is one ofthe main pests of fruit orchards in South AmericaA fraterculus is distributed from southern Texas inthe United States to northern Argentina (Calkins andMalavasi 1995) It is the main fruit pest in the south-eastern states in Brazil requiring control measures toprevent economic loss (Harter et al 2010)

In Brazil 81 hosts of A fraterculus have been identi-fied and the families Myrtaceae species and Rosaceaeare among the favorite fruit trees (Salles 1995 Zucchi2008) The native fruit trees like the strawberry guava[Psidium cattleianum Sabine 1821 (Myrtaceae)] andthe Surinam cherry [Eugenia uniflora L 1753 (Myrta-ceae)] are considered multiplying hosts of A fratercu-lus and thus are sources of infestation in peachorchards [Prunus persica (L) Batsch 1801 (Rosaceae)]

and apple trees [Malus domestica Borkhausen 1803(Rosaceae)] that have commercial importance to thesouthern states of Brazil

The cultivation of small fruits like blueberry [Vacci-nium ashei (Reade 1931) (Ericaceae)] or blackberry[Rubus sp (Rosaceae)] and native fruits like the straw-berry guava and Surinam cherry has increased recentlyIn Brazil the cultivation of blueberry blackberry andSurinam cherry covers an area of approximately 150250 and 300 ha respectively (Strik et al 2007 Fachi-nello 2008 Franzao and Melo 2012) Most commercialfruits of Surinam cherry and strawberry guava comefrom native areas

The losses caused by A fraterculus to small fruitsand particularly native fruits are limiting productionfactors To date information is scarce and is related tothe occurrence of A fraterculus in blackberry straw-berry guava and Surinam cherry fruits (Salles 1995)while for blueberry there are no records of attacks tofruits Information on the effects of different phenolog-ical stages of the fruit on the larval development ofA fraterculus is important for pest managementTherefore this study identified the phenological stageof blueberry blackberry strawberry guava and Suri-nam cherry fruits susceptible to the development ofA fraterculus

1 Departamento de Fitossanidade Universidade Federal de PelotasFaculdade de Agronomia Eliseu Maciel 96010-900 Pelotas RioGrande do Sul Brazil

2 Laboratorio de Entomologia Embrapa Clima Temperado 96010-971 Pelotas Rio Grande do Sul Brazil

3 Corresponding author e-mail doriedson-navaembrapabr

VC The Authors 2015 Published by Oxford University Press on behalf of Entomological Society of AmericaAll rights reserved For Permissions please email journalspermissionsoupcom

Materials and Methods

Definition of Maturation Stages We studied thedevelopment of blueberry blackberry strawberryguava and Surinam cherry fruits after flowering inorder to characterize three phenological stages basedon physical and chemical characteristics (Table 1) andthrough field observation using the methodologydescribed by Antunes et al (2000) The study was car-ried out in orchards of Embrapa Temperate Climate(CPACT) with clonal selections Stage I (green fruits)II (intermediate ripening stage of fruits) and III (fruitsclose to harvesting) were defined as the 8th 10th and11th week of blueberry 6th 8th and 9th week ofblackberry 8th 13th and 16th week of strawberryguava and 5th 6th and 7th week of Surinam cherryafter the first flowering (Fig 1)

The physical and chemical analyses of the fruits wereperformed in the Laboratory of Food Science and Tech-nology of Embrapa Temperate Climate The analyseswere performed according to the methodologies pro-posed by Instituto Adolfo Lutz (1985) For the physicalanalysis the average weight of fruits was obtained froma sample of approximately 150 fruits (for each fruit treeand stage of interest) on a semi-analytical scale (Shi-madzu of Brazil BL model 3200 with 001 g precision)For the chemical analysis it was determined the totalsoluble solids (TSS) titratable acidity (ATT) withsodium hydroxide and the concentration of hydrogenions (Hthorn) (pH) and all the analyses were made in tripli-cate The TSS was determined from a sample of theextraction of approximately 150 fruits using a micro-processor (Walita model 320 [Varginha Minas Gerais])

For the reading of TSS a digital refractometer wasused with automatic temperature compensationexpressing the results in Brix For the AAT 10 ml ofhomogenized juice was diluted in 90 ml of distilledwater and subsequently it was titrated with a solutionof 01 N NaOH The reading was performed with adigital pH meter (Mettler Toledo [model 320] witha Mettler Toledo electrode [Inlab 413]) until the pHreached 810 (turning point) and the results wereexpressed as percentage of citric acid The pH wasdetermined by means of the digital peagameter (Met-tler Toledo [model 320] with a Mettler Toledo

electrode [Inlab 413]) and automatic compensation oftemperature At this temperature the concentration ofhydrogen ions (Hthorn) was measured which correspondsto the pH of a solution

Infestation of A fraterculus Blueberry black-berry strawberry guava and Surinam cherry fruitswere collected weekly from the first flowering to har-vesting and from a single orchard corresponding to theperiods of 9 December 2011 to 9 January 2012 from 7October 2011 to 6 January 2012 from 14 November2011 to 26 March 2012 and from 19 September 2011to 13 December 2011 respectively We collected 50fruits per week for each developmental stage of eachplant host The fruits were transported to the labo-ratory groups of 10 fruits were formed and stored inplastic containers (11 by 11 by 35 cm3 length by widthby height) containing a 5-cm layer of medium-texturedvermiculite Afterwards the containers were packed ina room with conditions controlled (25 6 2C 70 6 10relative humidity (RH) and a photoperiod of 1212[LD] h) where they remained for 30 d for countingthe number of pupae

The infestation index was determined by the numberof pupae in the three developmental stages of thefruits using the formula number of pupaeaveragefruit weight The infestation data were used to preparegraphs of population fluctuation regarding the threedevelopmental stages of the fruit in the years2010ndash2011 In addition to collecting fruit to check nat-ural infestation adults of A fraterculus were monitoredduring the fructification period using three McPhailtraps in each orchard with protein-hydrolyzed baits at3 The traps were inspected weekly to change thehydrolyzed protein and count the number of adults ofA fraterculus captured

Biology of A fraterculus in ThreeDevelopmental Stages of Blueberry BlackberryStrawberry Guava and Surinam Cherry In the4th week after flowering fruits of the four hosts wereprotected from the attack of flies with wire cages (120by 045 m2 length by height) and lined with voile fabric(180 by 050 m2 length by height) The cages werefixed on the branches with strings When the fruitsreached the developmental stages I II and III theywere collected for the biological analyses in the lab

Table 1 Average values 6 SE of chemical and physical characteristics of blueberry blackberry strawberryguava and Surinam cherry fruits in three developmental stages

Hosts Stages Fruit weight (g) Brix pH Acidity ()

Blueberry I 074 6 0017 720 6 0115 283 6 0004 189 6 0002II 118 6 0041 873 6 0066 296 6 0018 155 6 0050III 149 6 0055 1180 6 0346 315 6 0029 044 6 0015

Blackberry I 209 6 0167 587 6 0176 277 6 0011 280 6 0034II 410 6 0112 553 6 0133 272 6 0012 244 6 0117III 582 6 0109 887 6 0437 331 6 0032 082 6 0072

Strawberry guava I 404 6 0201 693 6 0290 357 6 0012 136 6 0036II 827 6 0417 853 6 0176 361 6 0009 133 6 0033III 1520 6 0431 1067 6 0066 412 6 0014 105 6 0054

Surinam cherry I 115 6 0123 920 6 0305 278 6 0005 239 6 0022II 218 6 0138 1027 6 0176 279 6 0011 233 6 0003III 414 6 0210 1453 6 0352 301 6 0007 153 6 0037

Agricultural crop 2011ndash2012 Municipality of Pelotas Rio Grande do Sul State Brazil

February 2015 BISOGNIN ET AL A fraterculus DEVELOPMENT RELATED TO PHENOLOGY 193

One hundred fruits were offered during 24 h to 100females of A fraterculus of 15 d of age obtained fromthe rearing performed in papaya fruit [Carica papayaL 1753 (Caricaceae)] inside wooden cages (500 by500 by 400 cm3 length by width by height) accordingto the methodology of Machotta et al (2010) After thisperiod the fruits were identified individually in plasticcontainers (50 by 60 by 40 cm3 length by width byheight) which were closed with TNT type fabric (non-woven fabric) tied with a rubber band The fruits wereplaced on a vermiculite layer of medium texture toabsorb excess moisture and avoid contamination

After the 10th day daily observations were carriedout to determine the pupation date The pupae werecounted weighed and transferred to acrylic tubes (25by 48 by 25 cm3 length by width by height) contain-ing medium-texture vermiculite where they remaineduntil the emergence of adults For the immature stagesof development the eggndashadult period weight andnumber of pupae per fruit as well as the number ofinfested fruits were determined

The biological parameters for the adult stage wereobtaned from 25 couples of upto 24 h for each treat-ment The pairs were placed in cages of transparentplastic containers (500 ml) on an acrylic plate contain-ing holes (8 mm) at the top for air circulation The pairswere fed with a solid diet based on brown sugar wheatmeal and soy protein at the ratio 113 respectivelysupplied in plastic containers (40 g) Water was offeredby capillarity in acrylic containers (10 ml) through den-tal roll of cotton wool

We registered daily the number of eggs and adultmortality to determine the period of ovipositionfecundity and longevity of males and females Fecund-ity was determined using an artificial fruit cage elabo-rated with 750 ml of blackberry juice 35 g of agar04 g methyl-parahydroxybenzoate (Nipagin) and350 ml of distilled water as described by Salles (1992)After mixing these ingredients at a boiling point theliquid was placed in oval trays and after solidificationit was wrapped in a plastic sheet (Parafilm) in order toavoid the direct contact of the fly with the ingredients

Fig 1 Schematic representation of the maturation stages of blueberry (0-flowering I-8 weeks after flowering II-10weeks after flowering and III-11 weeks after flowering) blackberry (0-flowering I-6 weeks after flowering II-8 weeks afterflowering and III-9 weeks after flowering) strawberry guava (0-flowering I-8 weeks after flowering II-13 weeksafter flowering and III-16 weeks after flowering) and Surinam cherry (0-flowering I-5 weeks after flowering II-6 weeks afterflowering and III-7 weeks after flowering)

194 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 108 no 1

of the artificial fruit The ingredients were offeredto pairs of A fraterculus and replaced on a dailybasis to determine the period of oviposition andfecundity

Statistical Analysis The data on the eggndashadultperiod oviposition and longevity of males and femaleswere analyzed through the statistical program R (RDevelopment Core Team 2011) using the technique ofsurvival analysis For each period the survival curves ofeach treatment were determined considering theKaplanndashMeier estimator which were compared by theLog-rank test The data on pupae weight were sub-jected to the analysis of variance (ANOVA) performedby the GLM procedure of SAS (SAS Institute 922002) and the means of the treatments were comparedby the Tukey test (Plt 005) The data on the variablenumber of pupae and fecundity were submitted toanalysis of generalized linear models using the GEN-MOD procedure of SAS (SAS Institute 92 2002) andthe least squares were compared in the Chi-square test(Plt 005)

Results

In the four orchards adults of A fraterculus werecollected indicating the presence of the pest in thearea (Fig 2) Fruits collected in the field showed theoccurrence of A fraterculus in blueberry in the 13thweek after the first flowering possibly from subsequentblooming as ripe fruits collected prior to and after thisdate were not infested (Fig 3A) The infestation indexwas 201 pupae per fruit (Table 2) In blackberryA fraterculus was registered in the 10th week after thefirst flowering for 20 d (Fig 3B) totaling an infestationindex of 049 and 396 pupae per fruit for the pheno-logical stages II and III respectively (Table 2) Forblackberry the presence of A fraterculus was observed

for a longer period (Fig 3C and D) In strawberryguava the first insects were observed in the 13th weekafter the first flowering in fruits of stage II and in thefollowing weeks of stage III with an infestation indexof 2454 and 2296 pupae per fruit respectively(Table 2) For Surinam cherry the first insects wereobserved in the 6th week after the first flowering infruits of phenological stage II (1468 pupae per fruit)and in the following weeks insects were also recordedin stages III (1086 pupae per fruit) and I (2000 pupaeper fruit Fig 3D Table 2)

The larval development of A fraterculus in the phe-nological stages of fruits observed in the field was pro-ven in laboratory experiments observing however thatsome of the stages did not offer favorable conditionsfor insects (Table 3) For blueberry laboratory develop-ment occurred only in stage III of maturation and thelength of preimaginal was similar to the other hosts(Table 3) For blackberry the development of A frater-culus occurred in stages II and III of the fruit and sig-nificant differences were observed in the duration ofthe eggndashadult period (v2frac14 71 dffrac14 1 Pfrac14 00078Table 3) longevity of females (v2frac14 47 dffrac14 1Pfrac14 00296 Fig 4A) and longevity of males (v2frac14 109dffrac14 1 Pfrac14 00009 Fig 4B) For the weight of pupae(Ffrac14 208 dffrac14 1 Pfrac14 015) number of pupae(v2frac14 015 dffrac14 1 Pfrac14 069) oviposition period(v2frac14 14 dffrac14 1 Pfrac14 024) and fecundity (Ffrac14 251dffrac14 1 Pfrac14 01241) no significant differences wereobserved (Table 3) For strawberry guava the develop-ment of A fraterculus in lab also occurred in stages IIand III and significant differences were observed inthe eggndashadult period (v2frac14 1140 dffrac14 1 Pfrac14 00007)weight of pupae (Ffrac14 5355 dffrac14 1 Pfrac14 0) number ofpupae (v2frac14 161 dffrac14 1 Pfrac14 00001) and fecundity(Ffrac14 409 dffrac14 1 Pfrac14 0043 Table 3) For the oviposi-tion period (v2frac14 06 dffrac14 1 Pfrac14 042) longevity of

Fig 2 Population fluctuation of adults of A fraterculus in blueberry blackberry strawberry guava and Surinam cherryin the field Agricultural crop 2011ndash2012

February 2015 BISOGNIN ET AL A fraterculus DEVELOPMENT RELATED TO PHENOLOGY 195

females (v2frac14 04 dffrac14 1 Pfrac14 052) and males (v2frac14 04dffrac14 1 Pfrac14 055) no significant differences wereobserved (Fig 4A and B) In Surinam cherry thedevelopment of A fraterculus was observed in thethree maturation stages (Table 3) For the duration ofthe eggndashadult period significant differences wereobserved which were higher for fruits in stage III(v2frac14 191 dffrac14 2 Pfrac14 0) The weight of pupae wasgreater for insects reared on fruits in stage III(Ffrac14 1486 dffrac14 2 Pfrac14 00001) while the number ofpupae obtained was greater in stage II compared withthe others differing significantly among each other(v2frac14 4134 dffrac14 2 Pfrac14 00001) The oviposition perioddiffered significantly between treatments and wasgreater in stages II and III (v2frac14 228 dffrac14 2 Pfrac14 0)A similar behavior was registered for fecundity asfemales reared in stage III had greater fecundity thanfemales of other stages (Ffrac14 955 dffrac14 2 Pfrac14 00004)Insects reared in stage III also had greater longevitythan those reared in stage II which in turn hadgreater longevity than those in stage I differing signifi-cantly among each other for both females (v2frac14 358dffrac14 2 Pfrac14 0) and males (v2frac14 702 dffrac14 2 Pfrac14 0Fig 4A and B)

Discussion

The strawberry guava and Surinam cherry fruitsshowed the highest infestation indexes and allowed abetter biological development of A fraterculus underlaboratory conditions showing that native fruits aremore susceptible to South American fruit flies Thedefinition of the three phenological stages of the fourhost fruits allowed to relate the infestation of A frater-culus under field conditions with the biological study inthe laboratory although fruit development in the fieldis affected by several climatic factors such as tempera-ture rainfall luminosity etc

Regarding the preference of A fraterculus for nativeor exotic host fruits Selivon (2000) found that popula-tions of A fraterculus sp 2 collected in southern andsoutheastern Brazil were generally from nonnativehosts occurring the contrary in the northeasternregion The relationship between the host plant andthe insect is complex and can be affected by the spe-cific ecological factors of each site In this study weobserved that for the conditions in the Rio Grande doSul State A fraterculus infested native fruits withgreater intensity and precocity and in the specific caseof Surinam cherry infestation occurred in the 5th week

after flowering in fruits of stage I For small fruits how-ever infestation occurred at low intensity observed inphenological stages near ripeness

In blueberry during all stages of phenological devel-opment we collected only three fruit flies in a singlecollection (13th week stage III) which indicates a lowinfestation level (Table 2 Fig 2) This is probablyrelated to the fact that blueberry is an exotic speciesintroduced in Brazil in the 1980s (Madail and Santos2004) and started to be grown commercially from the1990s and therefore A fraterculus native to thisregion is in the adaptation process to cultivation Thepresence of A fraterculus in blueberry is the first refer-ence to a species of fruit fly infestation in Brazilalthough fruit flies were already collected in trapsinstalled in orchards (Bogus et al 2008) Species offruit flies were found in other countries such as A fra-terculus and Ceratitis capitata (Wiedemann 1824)(Diptera Tephritidae) in blueberry orchards in Argen-tina (Vaccaro and Bouvet 2006) C capitata Bactroceradorsalis (Hendel 1912) (Diptera Tephritidae) andBactrocera cucurbitae (Coquillet 1849) (DipteraTephritidae) were used in experiments to assess sus-ceptibility of blueberry to these pests in the UnitedStates (Follett et al 2011)

In the lab the larval development was also observedin stage III where an average of 14 pupae per fruitwas obtained from 84 infested fruits (Table 3) Theeggndashadult developmental period was close to the phe-nological stage III of the other hosts however theperiod of oviposition fecundity and longevity werelower compared with the values observed in the nativefruits in stage III (strawberry guava and Surinamcherry Table 3 Fig 4) Thus in a situation wherefemales of A fraterculus have no chance of choice theblueberry had the larval development near the fruitmaturation stage (stage III) Therefore it is necessaryto monitor if A fraterculus can eventually adapt in thisfruit

For blackberry infestation of A fraterculus infruits occurred in the phenological stage III in the10th week after the first flowering fruits in stage IIalso allowed the development of fruit fly in the 11thweek although only two pupae were recorded(Table 2 Fig 2) Blackberry also an exotic specieshowever unlike the blueberry has native species toBrazil such as Rubus urticaefolius Rubus erythrocla-dos Rubus brasiliensis Rubus sellowii and Rubusimperialis (Reitz 1996) that can host A fraterculusand therefore there is a better adaptation in

Table 2 Average values of the number of pupae and infestation index of A fraterculus obtained in blueberryblackberry strawberry guava and Surinam cherry fruits in three maturation stages

Hosts No of pupaefruit weight Infestation index for Anastrephaa

I II III I II III

Blueberry 0074 0118 3149 000 000 201Blackberry 0209 2410 16582 000 049 396Strawberry guava 0404 373827 3491520 000 2454 2296Surinam cherry 23115 32218 45414 200 1468 1086

Agricultural crop 2011ndash2012 Embrapa Clima Temperado Municipality of Pelotas Rio Grande do Sul State BrazilaInfestation index determined by the number of pupae per fruit weight

196 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 108 no 1

blackberry cultivated as demonstrated in this studywhere infestation indices were higher (Fig 3A andB Table 2) On the other hand insect developmentalso occurred in stage II although the number ofinfested fruits and longevity period were lower thanthe values found in stage III in the lab (Table 3Fig 4) The remaining parameters evaluated seem tobe close for the two stages

In strawberry guava the beginning of the infestationof A fraterculus occurred in the 13th week after firstflowering (stage II) and after that until the end of theharvesting in both stages II and III (Fig 3C Table 2)Although strawberry guava is nutritionally suitable forthe development of the South American fruit fly (Salles1995) probably the larger number of insects observedis because of the ripeness period of the fruits whichextends until the end of March when the populationinsect possibly migrates from the peach orchards Pru-nus persica L and plum tree Prunus domestica L1753 (Rosaceae) and other native fruit trees like Suri-nam cherry blackberry cherry from Rio Grande do Sulstate Brazil [Eugenia involucrata De Candolle 1828(Myrtaceae)] to the orchards of Surinam cherry (Salles1995 Nava and Botton 2010)The infestation indicesfor both developmental stages were high when com-pared with the other hosts especially in Surinamcherry (Table 2 Fig 2) but they were lower whencompared with other studies Nunes et al (2012) andGarcia and Norrbom (2011) found 180 and 357 pupaeper fruit respectively In the lab the larval develop-ment also occurred in the phenological stages II andIII however stage II was more infested than stage IIIand probably this explains the lower weight of pupaeobserved in stage II (Table 3) The eggndashadult periodand fecundity despite significant differences biologi-cally can be considered negligible as in both stagesfecundity is higher than that registered for papaya(294 eggs) and apple (330 eggs) and eggndashadult periodis similar to that recorded for papaya (28 d Nunes2010 Table 3) For longevity we observed that bothmale and female insects reared in stage II hadshorter longevity than those in stage III indicating thatfor this parameter ripe fruits apparently provide a bet-ter development of A fraterculus although in generalthe values of the biological parameters are close(Fig 4A and B)

For Surinam cherry the occurrence of A fraterculuswas observed in the 6th week after the first floweringcorresponding to the phenological stage II of develop-ment and afterwards until the end of the harvestingThe fruits in stage I were also infested however thisinfestation occurred in the 8th week after the first flow-ering (Fig 3D) The infestation index for stages II andIII was considered low when compared with 072pupae per fruit determined for Surinam cherry byNunes et al (2012) but similar to results found by Gar-cia and Norrbom (2011) who observed 024 pupae perfruit (Table 2) In the lab the larval development of Afraterculus occurred in three maturation stages similarto the occurrence observed in the field (Table 3Fig 3D) However based on the biological parameterssuch as weight of pupae period of oviposition

Table

3A

vera

ge

valu

es6

EP

ofbio

logic

alpara

mete

rsofA

fr

ate

rculu

sre

are

din

blu

eberr

ybla

ckberr

yst

raw

berr

yguava

and

Suri

nam

cherr

yfr

uit

sin

thre

em

atu

rati

on

stages

Bio

logi

calp

aram

eter

sB

lueb

erry

Bla

ckb

erry

Str

awb

erry

guav

aS

uri

nam

cher

ry

III

III

[25]

III

[7]

III

[25]

III

[25]

III

[25]

I[8

]II

[25]

III

[9]

Egg

ndashad

ult

per

iod

(d)1

ndashndash

267

60

15(2

40ndash

300

)ndash

288

60

23a

(26

0ndash32

0)

275

60

21b

(25

0ndash31

0)

ndash27

36

008

b(2

30ndash

310

)27

86

009

a(2

50ndash

320

)26

66

013

b(2

40ndash

290

)26

96

011

b(2

30ndash

310

)27

73

60

19a

(25

0ndash32

0)

Pu

pae

wei

ght

(mg)

2ndash

ndash8

76

061

(43

ndash14

3)ndash

112

60

60a

(43

ndash18

6)10

32

60

30a

(40

ndash16

6)ndash

84

60

33b

(26

ndash16

0)12

36

043

a(3

1ndash2

50)

68

60

37b

(14

ndash13

0)8

56

046

b(3

8ndash1

80)

114

86

051

a(3

0ndash1

80)

Ovi

pos

itio

np

erio

d(d

)1ndash

ndash12

96

11

(50

ndash21

0)ndash

123

61

69a

(60

ndash17

0)14

04

61

12a

(60

ndash26

0)ndash

311

62

96a

(70

ndash68

0)35

66

381

a(6

0ndash7

10)

862

61

92b

(30

ndash18

0)25

86

315

a(4

0ndash5

90)

330

66

02a

(14

0ndash66

0)

Fec

un

dit

y3ndash

ndash19

73

619

9(4

8ndash38

9)ndash

206

46

285

a(9

50ndash

301

0)21

33

620

6a

(63

0ndash54

10)

ndash38

28

635

2b

(74

0ndash80

50)

394

16

372

a(4

20ndash

770

0)81

06

169

c(3

20ndash

156

0)25

88

633

7b

(23

0ndash77

20)

460

26

877

8a(1

910

ndash979

0)

No

ofp

up

ae3

ndashndash

14

60

06(1

0ndash3

0)

ndash1

46

014

a(1

0ndash4

0)

15

60

06a

(10

ndash30

)ndash

38

60

24a

(10

ndash13

0)2

76

014

b(1

0ndash6

0)

18

60

11b

(10

ndash40

)2

96

016

a(1

0ndash5

0)

140

60

08b

(10

ndash30

)

No

ofin

fect

edfr

uit

sndash

ndash84

ndash31

78ndash

8580

5678

58

Tem

per

atu

re2

56

2C

RH

70

610

p

hot

oper

iod

of12

12

(LD

)h

V

alu

esin

bra

cket

sin

dic

ate

the

nu

mb

erof

rep

etit

ion

s(p

airs

)u

sed

for

the

bio

logi

cals

tud

yof

adu

lts

ofA

fra

terc

ulus

V

alu

esfo

llow

edb

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esa

me

lett

erin

line

per

hos

td

on

otd

iffe

rb

yL

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February 2015 BISOGNIN ET AL A fraterculus DEVELOPMENT RELATED TO PHENOLOGY 197

fecundity and longevity the best developmentoccurred in stage III followed by stage II and finallystage I (Table 3 Fig 4) The greater weight of pupaein stage III occurred due to smaller number of pupae

in fruits when compared with the other stages (Table3) Probably smaller hosts such as small fruits andnative fruits provide a lower food supply for the larvaldevelopment and consequently with the competition

Fig 3 Field infestation of A fraterculus in blueberry (A) blackberry (B) strawberry guava (C) and Surinam cherry (D)during the three maturation stages Agricultural crop 2011ndash2012 WAF weeks after flowering fruits from the first flowering

198 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 108 no 1

the insects are smaller thus affecting fecundity andlongevity as observed in this work

The analysis in laboratory and in the field showedthat A fraterculus is more harmful to native fruits thansmall fruits although its presence should be monitoredin all fruits as phenological stages near fruit ripenessare susceptible to larval development

Acknowledgments

We thank the Conselho Nacional de DesenvolvimentoCientıfico e Tecnologico (CNPq Brazilian National Councilfor Scientific and Technological Development) for financialsupport for part of the study and research scholarships for thesecond author

References Cited

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Bogus G M L Abreu L M Sartoreto G N Zilli SLampert M Savaris F R M Garcia and C Gubert2008 Ocorrencia de moscas-das-frutas (Diptera Tephriti-dae) em pomar de mirtilo Vaccinium ashei (AngiospermaeEricaceae) no municıpio de Ita-Santa Catarina p 1 In XXIIResumos do Congresso Brasileiro de Entomologia Uberlan-dia-MG Uberlandia SEB

Calkins C O and A Malavasi 1995 Biology and control offruit flies (Anastrepha) in tropical and temperate fruit RevBras Fruticultura 17 36ndash45

Fachinello J C F 2008 Mirtilo Rev Bras Fruticultura 30285ndash288

Follett P A F T Zee R T Hamasaki K Hummer TStuart and S Nakamoto 2011 Susceptibility of low-chillblueberry cultivars to mediterranean fruit fly oriental fruit flyand melon fly (Diptera Tephritidae) J Econ Entomol 104566ndash570

Franzao A A and B Melo 2012 Cultura da pitangueira(httpwwwfruticulturaiciagufubrpitangueirahtml) (ac-cessed 8 July 2012)

Garcia F R M and A L Norrbom 2011 Tephritoid flies(Diptera Tephritoidea) and their plant hosts from the Stateof Santa Catarina in Southern Brazil Fla Entomol 94151ndash157

Fig 4 Laboratory survival curves of females (A) and males (B) of A fraterculus from fruits of blueberry blackberrystrawberry guava and Surinam cherry in three phenological stages Temperature 25 6 2C RH 70 6 10 photoperiod of1212 (LD) h Arrows indicate the survival period Curves followed by different letters differ statistically from each other bythe t-test (P 005)

February 2015 BISOGNIN ET AL A fraterculus DEVELOPMENT RELATED TO PHENOLOGY 199

Instituto Adolfo Lutz 1985 Normas analıticas metodos quı-micos e fısicos para analises de alimentos Instituto AdolfoLutz Sao Paulo Brazil 533p

Machotta R L C Bortoli A Tolotti and M Botton 2010Tecnica de criacao de Anastrepha fraterculus (Weid 1830)(Diptera Tephritidae) em laboratorio utilizando o hospedeironatural Embrapa Uva e Vinho Bento Goncalves RS

Madail J C M and A M Santos 2004 Aspectos economi-cos pp 63ndash67 In MCB Raseira and LEC Antunes (eds)A cultura do mirtilo Embrapa Clima Temperado Pelotas RS

Nava D E and M Botton 2010 Bioecologia e controle deAnastrepha fraterculus e Ceratitis capitata em pessegueiroEmbrapa Clima Temperado Pelotas RS

Nunes A M 2010 Moscas frugıvoras (Tephritoidea) seus para-sitoides e estudos bioecologicos de Anastrepha fraterculus(Wiedemann 1830) (Diptera Tephritidae) e Doryctobraconareolatus (Szepligeti 1911) (Hymenoptera Braconidae)Tese (Doutorado) - Faculdade de Agronomia Eliseu MacielUniversidade Federal de Pelotas Pelotas RS 93p

Nunes A M F A Muller R S Goncalves M S Garcia VA Costa and D E Nava 2012 Moscas frugıvoras e seusparasitoides nos municıpios de Pelotas e Capao do Leao RioGrande do Sul Brasil Ciencia Rural 42 6ndash12

R Development Core Team 2011 R a language and environ-ment for statistical computing R Foundation for StatisticalComputing Vienna Austria

Reitz R 1996 Flora ilustrada catarinense rosaceas HerbarioBarbosa Rodrigues Itajai 135p

Salles L A B 1995 Bioecologia e controle da moscas-das-frutas sul-americana Embrapa Clima TemperadoPelotas RS

Salles L A B 1992 Metodologia de criacao de Anastrepha fra-terculus (Wied 1830) (Diptera Tephritidae) em dieta artifi-cial em laboratorio Anais da Sociedade Entomologica doBrasil 21 479-486

SAS Institute 2002 SAS System - SASSTAT Computer pro-gram version 92 SAS Institute Cary NC

Selivon D 2000 Relacoes com as plantas hospedeiras pp41ndash54 In A Malavasi and R A Zucchi (eds) Moscas-das-frutas de importancia economica no Brasil conhecimentobasico e aplicado Holos Ribeirao Preto

Strik C B J R Clark C E Finn and M P Banados2007 Worldwide blackberry production In ComprehensiveCrop Reports Hortechnology 2 1ndash10

Vaccaro N C and J P Bouvet 2006 Presence ofCeratitis capitata (Wied) and A fraterculus in blueberries(Vaccinium spp) of the Department of Concordia EntreRıos and in the Department of Curuzu Cuatia CorrientesArgentina Anais 7th International Symposium on Fruit Fliesof Economic Importance 10-15 September 2006 SalvadorBrazil

Zucchi R A 2008 Fruit flies in Brazil - Anastrepha species andtheir hosts (httpwwwleaesalquspbranastrepha) (ac-cessed 17 June 2012)

Received 18 March 2014 accepted 26 September 2014

200 JOURNAL OF ECONOMIC ENTOMOLOGY Vol 108 no 1