, Ii

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Area- Wide ControI of Insect PestsFrom Research to Field Implementation

Edited by

M.J.B. VreysenA.S. Robinson1. HendrichsJoint FAOIIAEA Programme o/Nuclear Techniquesin Food and Agriculture,Vienna, Austria

~ Springer

Eslablisnmenl of a, ..2007 SP-PP-00507

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A c.I.P. Catalogue record for this book is available from the Library of Congresso

ISBN 978-1-4020-6058-8 (l-! B)ISBN 978-1-4020-6059-5 (e-book)

Published by Springer,P.O. Box 17,3300 AA Dordrecht, The Netherlands.

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Photo credits:

Photos on the front cover were provided by Hendrik Hofmeyr, Frantisek Marec, llan Mizrahi,Marc Vreysen, Petr Pavlieek and SECNA (FAO).Photo's 011the back cover were provided by Patrick Robert (tsetse f1y), Ignacio Baez (cactus1110tll),Scott Bauer (USDA Agricultural Research Serviee, www.forestryimages.org -Mediterranean fruit fly, melon f1y), Jack Dykinga (USDA Agricultural Research Service,www.forestryimages.org - Mexican fruit f1y), Susan Ellis (www.forestryimages.org - Asiantiger mosquito), Alton N. Sparks (University ofGeorgia, www.forestryimages.org - boll wee-vil), Hcndrik Hofmeyr (false codling moth), and the Locust Group (FAO) (desert locust).

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A. MALAVASI1, A. S. NASCIMENT02, B. J. PARANHOS3,M. L. Z. COSTA4 and J. M. M. WALDER4

Establishment of a Mediterranean Fruít FlyCeratitis capitata, Fruit Fly Parasitoids, and

Codling Moth Cydia pomonella RearingFacility in North-Eastern Brazil

1Biofabrica Moscamed Brasil, Quadra D 13 Lote 15, Juazeiro, Bahia -48900-000, Brazil

2Embrapa Mandioca e Fruticultura Tropical, Rua Embrapa, s/n"; Cruzdas Almas, BA - 44380-000, Brazil

3Embrapa Semi-Àrido, BR 428, Km 152, Zona Rural - Caixa Postal 23,Petrolina, PE - 56302-970, Brazil

"Centro de Energia Nuclear na Agricultura - CENA/US?, Laboratóriode Irradiação de Alimentos e Radioentomologia, Av. Centenário 303,

São Dimas, Caixa Posta! 96, Piracicaba, SP - 13400-970, Brazil

ABSTRACT The Mediterranean fruit fly Ceratitis capitata (Wiedemann) is a major pest offruit cropsworldwide and its presence in rnany countries poses a lhreat for production and exporto The methodologythat has been integrated in many countries to contain, to eradicate, or to suppress Mediterranean fruit flypopulations is lhe sterile insect technique (SIT). Besides the Mediterranean fruit fly, Anastrepha fruit flyspecies of quarantine importance are also important pests affecting fruit crops in Brazil. Parasitoids that arenatural enemies of fruit flies will be mass-reared, together with Mediterranean fruit fly and Anastrephaspecies in the facility that is being established in Juazeiro, Bahia with the objective of suppressing fruitflies in the expanding comrnercial fruit production areas in the São Francisco river region. To take advan-tage of the availability of a large complex of buildings, the facility will eventually also produce sterilecodling moth Cydia pomonella (L.), a pest recently introduced into southem Brazil, where it threatens thecontinuously growing apple and pear industries. The production of sterile Mediterranean fruit flies andsterile codling rnoths, as well as sterile host larvae for natural enemy production, will use garnma radiationas the sterilization rnethod. The area-wide integrated pest management (AW-IPM) approach, including lherelease of these beneficia I insects in the field, is the rnost effective rneans to control (suppress or in somesituations even eradicate) such pests. The consumption of fresh fruits has increased worldwide and produc-tion in Brazil, either for domestic or export markets, has been intensified in the last decade. As food safetyis becoming a major concern for consurners, the use of environment-friendly technologies such as the SITwill be increasingly required. The final clients for the sterile flies and moths will be the fruit growers. The

, foreseen weekly production of 200 million sterile Mediterranean fruit flies and 10 millionDiachasmimorpha longicaudata (Ashrned) wasps will be released in the tropical fruit-growing areas ofnorthern Brazil: Bahia, Pernarnbuco (São Francisco Valley), Ceará, north of Minas Gerais and north ofEspirito Santo. The sterile codling moths would be sent by air to the apple and stone fruit production areasin the south of Brazil, Rio Grande do Sul and Santa Catarina, where this pest species is srill confincd tourban areas and hence amenable to eradication.

KEY WORDS Ceratitis capitata, Anastrepha spp., Cydia pomonella, Diachasmimorpha longicauda-ta, area-wide control, sterile insect technique, Brazil, São Francisco river valley

527MJB. v,-eysen, A.S. Robinson and J Hendrichs (eds.), Area-Wide Control of Insect Pests, 527-534.© 2007 JAEA.

528 A. MALAVASl ET AL.

1. Introduction

The sterile insect technique (SIT) is used inmany countries as part of an area-wide inte-grated pest management (AW-IPM) approachto control (suppress, contain, prevent or erad-icate) the Mediterranean fruit fly Ceratitiscapitata (Wiedemann) and other fruit flypests. This expanding use has proven success-fui in protecting critical production areas fromMediterranean fruit fly infestation and embar-gos on fresh fruit exports worth thousands ofmiJlions of USD. The SIT is incorporated intofruit fly control programmes to rninimize thecontinuous use of insecticides, protect theenvironment, and meet food safety standards.Fruit fly rearing facilities are in operation inArgentina, Australia, Chile, Guatemala,Israel, Mexico, Peru, the Philippines,Portugal, South Africa, Thailand, Tunisia, andthe USA (Hawaii and Texas). Others are beingplanned or under construction in Costa Ricaand Spain, and now in Brazil (Dyck et aI.2005). The Okinawa melon fly Bactroceracucurbitae (Coquillett) mass-rearing facilityin Japan is now producing low numbers ofinsects sufficient to maintain a continuouspreventive release progranune in the south-em-most islands of the Okinawa archipelagothat are susceptible to reinfestation since thispest was eradicated from that country(Koyama et aI. 2004). In these programmes,the SlT has proven to be successful in the sup-pression, containment, prevention or eradica-tion offruit flies (Wong et al. 1992, Hendrichs1996, Barry et aI. 2003, Hendrichs et aI.2005). Other sterile insect factories are inoperation to combat lepidopteran pests,screwworms, and tsetse flies (Dyck et al,2005).

2. Fruit Production in Brazil

Brazil is one of the largest fruit producers inthe world (38 million tons. in 2004), being firstin oranges (18.3 miJlion tons in 2004), secondin papayas (1.7 miJlions tons in 2003) andseventh in mangos (925 000 tons in 2003; alsosecond in exports) (Brazilian Fruits Yearbook

2005). In the last 20-30 years, the federal (.some state govemments have developed mairrigation programmes in the semi-arid noeastem part of Brazil focusing on the prodution of tropical, subtropical, and temper,{ I

fruit crops. As a result of such actions,' thénorth-eastern region is the largest producer.inthe country of mangos, table grapes, melonj,bananas, Antilles cherry, and guavas. The c~i~tivated area is continuously increasing and-atthe end of 2004 there were, for exarnple,68455 hectares of mangos in the whole ófBrazil, of which about 20000 hectares areIAthe São Francisco Valley (Brazilian Fruit~Yearbook 2005). Most ofthe citrus productio~(800000 hectares, as well ali 35 000 hectares

•. ".,,!

of apples) is concentrated in the southemstates of Brazil. j

Brazil exports annuaJly around USO 400.million in fresh fruits (850000 tons, which i~:only 2% of total production), and USD 1100million in concentrated juices to Canada!Japan, and the USA, and to countries in th~European Union (EU) and in the South Con~Free Trade Agreement (Mercosur) (BraziliarlFruits Yearbook 2005). J

To a large extent, the fresh products expot;t,. 'I"market requires some type of quarantine treat-'ment. Fortunately, however, large fruit pro-ducing areas in north-eastern Brazil aredeemed "low prevalence" in terms of pest§!

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and diseases, especiaJly fruit flies. The very,low humidity, high air ternperature, and lack'of host availability year-round keep fruit fly]populations low. However, in areas where tHe:harvest time for mangos was extended from I

the original 2-3 months to 6-8 months due toimprovements in technology, wild fly popula-.tions can now increase dramatically in afew!'months. lt is exactly in such areas ofthe Nil1ih,East that the integration of the SIT for sup-pression is both required and highly feasible, :

The new agricultura I frontier representedin the serni-arid North East is a consequenceof four main factors: (I) improved infrastruc-ture developed through governmental support, "(2) high technology such as computer-con-'trolled irrigation, hormone and physiologicalcontrol of blossoming, IPM techniques, and

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iESTABLISHMENT OF A REARTNG FACILITY TNBRAZIL

advanced postharvest processes, (3) positiveenvironmental factors such as good soil, cleanwater, low relative humidity, high ambienttemperature, and long periods of sunlight, and(4) a new generation ofyoung entrepreneurs.

3. History of the Project

At the end of 2000, a group of researchersproposed the implementation of aMediterranean fruit fly rearing facility innorth-eastern Brazil to the FederalGovemment ofBrazil in response to demandsfrom the private sector for better (i.e. econom-ically feasible and environment-friendly)technologies to control key fruit fly pests inthis region. During 200 I, the Plant ProtectionDepartment of the Ministry of Agriculture,Livestock and Food Supply called a series ofmeetings to bring together different stake-holders with an interest in the rearing facility.A Mediterranean fruit fly rearing facilityworking group was created by the Ministry ofAgriculture, Livestock and Food Supply tocarry out studies to assess the feasibility of afacility. In January 2002, the Ministry ofAgriculture, Livestock and Food Supplycalled for an intemational mission to visitpotential sites for the facility, make a firstevaluation of its feasibility, and recommenda-

I tions concerning the size and numbers of ster-ile fiies to be produced by the facility. Themission from the International Atomic EnergyAgency (IAEA), the United StatesDepartment of Agriculture (USDA) andInstituto de Sanidad y Calidad Agropecuariain Mendoza, Argentina (lSCAMEN) recom-mended that the facility should be sited in theSão Francisco Valley (Juazeiro-Petrolina) inthe centre of the largest fruit production are aof the country and also equidistant from mostother fruit producing areas in north-eastemBrazil. This site was also selected because ofthe availability of an empty cotton processingplant that ironically was shut down due to thecollapse of cotton production in the regionbecause of heavy infestation by the boI! wee-vil. The mission concluded that constructionof a mass-rearing facility to produce sterile

529

flies (SIT) for suppressing or eradicating med-fly is feasible in the north-eastern fruit pro-duction areas of Brazil (Enkerlin et al, 2002).In addition the report states that:

... this environment-friendly technology, comple-mented by minimum use of organic bail 10 lowerwildjly populations, is an important addition tothe technologies supporting Brazilian agricul-ture. The introduction of this IPM componentopens the door to other pest control tools suchas fruit jly parasitoids and expanded use of ster-ile insects to control other fruit jly species ofeconomic importance.

Following these recommendations, theMediterranean fruit fly rearing facility work-ing group carried out studies to define the bestlegal framework for creating the new entity.Special attention was given to its format inorder to avoid infiexibility and excessivebureaucracy, and to enable the establishmentof a!liances with the federal and state govern-ments, international organizations and the pri-vate sector. TnNovember 2002, the BiofábricaMoscamed Brasil (Mediterranean Fruit FlyFacility Brazil) was formally created as asocial organization attached to the Ministry ofAgriculture, Livestock and Food Supply, andorganized with an administration council withfederal, state and private representatives, andan executive board with three executive direc-tors.

ln January 2003, a technical group wascreated by the Biofábrica Moscamed Brasil toestablish the technical parameters for the rear-ing facility on premises obtained from theGovernment of the State of Bahia. This groupfrom the Food and Agriculture Organizationof the United Nations (FAO), IAEA andUSDA defined the baselines for the facilityincluding the basic drawings, rearing flow,and technical specifications in tenns ofpowerand water requirements, air conditioning, andother utilities. Its general conclusions(Cáceres et al, 2003) were:

The building site in the State of Bahia located inthe city of Juazeiro is ideal if the entire 5-hectares facility could be devoted 10 the rearingplant. Thi' dedicated use would simplify man-agement and provide adequate space for ali pro-

f"I

!ESTABLlSHMENT OF A REARfNG FACILITY lN BRAZIL

necessary to reduce populations prior to releas-es of sterile males, and public relation andextension activities.

Regarding the SIT per se, a key element tothe success of the programme is the design,construction, and operation of a sterile flymass-rearing facility capable ofproducing suf-ficient sterile insects of good quality and at rea-sonable cost, in combination with efficient SITprogramme implementation and support togrowers, the public and govemment. Since ahigh degree of responsiveness to clients' needspromotes sustainability, the initial focus of theprogramme is on effectivene~s and cost effi-ciency unless other mitigating issues takeprecedence. Factors such as the environment,public health, public and political opinion, and

" the future direction of plant health regulationscould influence lhe use 01'the SIT, even if theinitial cost efficiency is less than optima!.

5. Plans and Concept

The initial kick-off for the programme was thepositive political decision by the FederalGovemment of Brazil, especially the Ministryof Agriculture, Livestock and Food Supply,with strong support from the Govemmenl ofthe State 01'Bahia. Providing the plant site wasthe first step, followed by the building processthat required a large investment. The federaland state governments are responsible for alifunds earmarked for the building phase(around USD 4.5 million), with the fruit indus-try providing the essential political support tothe govemment agencies. After the operation isinitiated, industry - through the growers asso-ciations anel cooperative farms - will graduallycompensate the Biofábrica Moscamed Brasilfor the services being delivered to the farms,which will encompass monitoring and releasesof sterile males.

Presently, in most fruit production areas, thetrapping system in place is grower-operatedwith different arrangements in place accordingto the region and always supervised directly bythe Ministry of Agriculture, Livestock andFood Supply or by the state plant protectionagencies. Hence the growers are already pay-

531

ing for the trapping services. The proposal now- which is, supported by the industry - is tohave Biofábrica Moscamed Brasilmanage thetrapping op rations since these provi de essen-tial information for use of the SIT and for theother controlmeasures that are needed.

The integrated area-wide approach, funda-mental for a successful prograrnme, is the con-cepo to be àpplied and a public disseminationcampaign to explain the concept and its opera-tion will be essential to have large, middle andsmall growers join the programme. The broadacceprance ,?f, anel participation in, the fruit flyman~gemenl programme is largely expectedbecause a I w prevalence of fruit fly popula-tions is one of the requirements to export rnan-gos into the USA and Japan, and the EU alsonow requires new processes for fruir produc-tion.

After the government allocates the seedmoney to build the facility, the operation isexpected to be sustainable within a few years.An additional source of funding could be theexport of sterile Mediterranean fruit flies.Although a large number 01' sterile Mediter-ranean fruit flies are being produced in othermass-rearing facilities around the world,elemand is till larger than this productioncapacity. In addition, Biofábrica MoscamedBrasil production can be destined for local usein future area-wide fPM projects involving theSIT in other regions of Brazil, For example, theEI Pino mass-rearing facility in Guatemalaexports millions offlies per week to Califomiaand Florida in the USA and also to Israel in thepasto Argentina, Mexico, Portugal, and USAmass-rearing, facilities in Texas and Hawaiihave 'also upplied other users. Modestamounts of profit obtained frorn such transac-tions reduce plant production costs. The abilityto ship pupae long distances anel the technolo-gy under development for shippingMediterranean fruit fly eggs to intemationalclients, adds greatly to plant utility, financialviability, and overall cost effectiveness.

6. Strategic Alliances

A key aspect for a fruit fly management pro-

532 A. MALAVASI ET AL.

gramme that includes the SIT is to havealliances in the national and international are-nas. The federal and state govemments are thenatural national alliances. These are key part-ners ince, amongst others, the importation ofbiological material from foreign sourcesrequires permits and federal govemmentapproval, the transshipment f flies from onestate to another requires state ovemlPent col-laboration, and the developnient of technicalalliances with other intemational ehtities isdependent on federal and state govemmentparticipation. Within these, the Ministry ofAgriculture, Livestock and Food Supply, theMinistries of Science and Technology and ofNational Integration, and the state govem-ments through the agencies for plant protec-tion in Bahia, Pemambuco, and Ceará are par-ticularly critical for the success of the pro-gramme.

lmportant support for research and devel-opment is provided by two research centres,the Brazilian Agricultural Research Corpora-tion (Empresa Brasileira de PesquisaAgropecuária (EMBRAPA)), i.e. EmbrapaCassava and Fruits, and Embrapa TropicalSerni-Arid. Other important partners are theCentre for Nuclear Energy in Agriculture(CENA) and the 1nstitute of.Biosciences ofthe University of São Paulo (USP). Thesehave helped the Biofábrica Moscamed Brasilimplementation since the beginning, includ-ing in planning, training, carrying out appliedresearch, and permanent overseeing. \

In the. industry, the Biofábrica MoscamedBrasil has the support from three major grow-er associations, the Fruit and VegetablesExport Association of São Francisco Valley(Valexport), the Brazilian Fruit Institute(IBRAF) and the Brazilian Papaya ExportAssociation (BRAPEX). The private sectorhas also contributed financial and politicalsupport.

The IAEAlFAO, as intemational organiza-tions have also given support. This includedsupporting the first mission to define the siteof the plant in 200 I, and a current TechnicalCooperation Project that covers the endow-ment of a 60Co irradiator, and the costs of

Table 1. PUSP-CEN

short-term expert visits and training for thenewly-hired personnel. Two professionalsfrom EMBRAPA and CENA were trained for:three months in the rearing, irradiation and"quality control aspects of the Mediterraneanfruit fly temperature sensitive lethal (tsT)genetic sexing strains at the FAO/IAEAAgriculture and Biotechnology Laboratory,Seibersdorf in Austria. Additionally, throughthe El Pino Mediterranean Fruit Fly Facility inGuatemala, the United States Department ofAgriculture's Animal and Plant Protection :'Service (USDA-APHIS) has systematically ' ,I

provided technical assistance since the begin-ning of the project, with directors' visits to 'Brazil, and Brazilian professionals visitingGuatemala for training and obtaining informa-tion on the facility in order to design and pre-pare the operational aspects of the Biofábrica ,Moscamed Brasil. Finally, ISCAMEN,Argentina, has given technical advice and sentsterile Mediterranean fruit flies for prelimi-nary tests in Brazil.

Generatii(month/y

FIO (DeciO-F 11 (Jan/05F 12 (Feb/O~F 13 (MariOF 14 (Apr/O:}15 (May/O

lTheVlENteration F9 (C2No! ali coll

mango anwhere thely reportecSterile maland releasdetailed smeasures :high. ForestablisheAnimal(ADAB),lBahia (UnBahia (UEand logisti

At theVIENNAFAO/IAEJLaboratorjfully adapdeveloped(Walder 2(bagasse asbrewer yewheat floudrate sougrowth inlfunga I groregulator .'to that reStudies us

7. Research and DevelopmentComponent

The Biofábrica Moscamed Brasil is the firstfacility in Brazil to produce sterile insects ona large scale and, as a result, there is a smallcritical mass of trained personnel in the coun-try. There is however, no information regard-ing the effectiveness of the SIT under semi-arid conditions. A set of experiments andlarge-scale field tests were planned and arebeing carried out to answer basic questionsconceming the mating competitiveness of tslstrain VIENNA 8 (Franz 2005), sterile malescompeting with wild males for wild females,dispersion and longevity of sterile malesunder semi-arid conditions and related topics,1n collaboration with the AgriculturalResearch Service (ARS) of USDA, theUniversity ofTessaly in Greece, and the JointFAO/IAEA Programme, one staff member isleading a group in EMBRAPA to answer thesequestions with financial support from theBank of Nordeste.

Large pilot tests are also planned for two

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----------------~---------rI

ESTABLlSHMENT OF A REARING FACILlTY IN BRAZIL 533

Table 1.Production and basic biological data of the VIENNA 8 genetic sexing strain colony atUSP-CENA, Piracicaba, Sp, Brazil.

GenerationI Eggs-' Egg Number of Male Female Sex error in Sex error in(month/year) (ml) viability pupae viability viability brown pupae white pupae

(%) (x 1000) (%) (%) (%) (%)

FIO (Dec/04) 12.5 24.7 48 63.1 85.1 1.18 0.00F 11 (Janl05) 19.1 77.2 1257 84.9 80.3 0.30 0.00F 12 (Feb/05) 64.3 75.8 1680 76.9 86.6 0.85 0.18F \3 (Mar/05) 52.2 63.8 1430 83.5 90.7 0.50 0.00F 14 (Apr/05) 98.2 71.6 1390 83.1 89.6 0.26 0.08F 15 (May/05) 243.5 68.3 3240 n.a. 11.3 n.a n.a

lThe VTENNA8pupaereceived frorn theFAO/IAEAAgricultureand BiotechnologyLaboratorywere fromgen-erationF9 (CarlosCáceres,personalcornmunication) I !2Notali collectedeggs were used for pupal production

mango arcas - 3000 and 5000 hectares -where the Mediterranean fruit fly is historical-Iy reported as being of econornic importance.Sterile males will be brought from rSCAMENand released in the experimental areas after adetailed survey and following suppressionmeasures taken when the fera 1 population ishigh. For these pilot tests, partnerships wereestablished with EMBRAPA, the BahiaAnimal and Plant Protection Agency(ADAB), and the University of south-westernBahia (Universidade Estadual do Sudoeste daBahia (UESB)) to have good entomologicaland logistical support to carry them out.

At lhe USP-CENA laboratories, theVIENNA 8 strain received from lheFAO/TAEA Agriculture and BiotechnologyLaboratory in December 2004 was success-fully adapted to a larval diet, which wasdeveloped in 2002 with local ingredients(Walder 2002). This diet contains sugarcanebagasse as a bulking agent, wheat germ andbrewer yeast as protein sources, sugar andwheat flour as phagostimulants and carbohy-drate sources, an antibiotic . as bacterialgrowth inhibitor, sodium benzoate to avoidfunga I growth and hydrochloric acid as pHregulator. The rearing protocol is very similarto that recommended by Cáceres (2002).Studies using several quality tests including

,gamrha sterilization are being applied underlaborktory conditions (FAO/TAEA/USDA

I . . .2003). After SIX generations the strain showsgood quality and stability (Table 1), enablingcolony expansions to be planned for subse-quent generations.

USP-CENA will be responsible for main-taining the original strain imported from theFAO/IAEA Agriculture and BiotechnologyLaboratory and transferring it to theBiofábrica Moscamed Brasil when the mass-rearing process start . Also the tests forimproving the local diet and the quality con-trol of the rearing will be supervised by USP-CENA.

8. Conclusions

The location of the Biofábrica MoscamedBrasil in the São Francisco Valley is right inthe centre of ango and many other fruit pro-duction farms. This close proximity to produc-tion areas should promote more private sectorinterest and commitment. Privare sectorinvest ient *,ould be enhanced if theMediterraneart fruit fly rearing facility was anintegral part (of the community where thestakeholders Iíve and work, since local produc-ers and public sector officials are in a betterposition to support the plant and resolve any

534 A. MALAVASI ET AL.

probíems that might arise localiy or regionally.

9. References

Barry, J. D" T. E. SheUy, D. O. Mclnnis, andJ. G Morse. 2003. Potential for reducingoverflooding ratios of sterile Mediterraneanfruit flics (Diptera: Tephritidae) with the useof ginger root oil. Florida Entomologist 86:29-33. !

Brazilian Fruits Yearbook. 2005. Santa Cruzdo Sul, Rio Grande do Sul, Brazil,

Cáceres, C. 20Ó2. Mass rearing oftemperaturesensitive genetic sexing strains in theMediterranean fruit fly (Ceratitis capitata).Genetica 116: 107-116. '

Cáceres, c., J. Porro, P. Rendón, and GTween. 2003. Technical specification forthe medfly production plant in Brazil.Juazeiro, Bahia, Brazil. Repo 1: to the lAEA,BRA/5/G57, Vienna, Austria.

Dyck, V. A., J. Hendrichs, and ll. S. Robinson(eds.), :WOS. Sterile insect tcchnique. Prin-ci les c'J:,J practice in area-wide integratedpesr mr..-',g;õment. Springer, Dordrecht, TheNether.a :!d~.

Enkeriin -,\N, 1.'.Rendón, P. G Riera, und GTWCCil. :WlC. Medfly rearing facility feasi-bility ~;;l;iy I(1,' northeast of Erazil. Brasília,D. T: .• üri:,:il. Report to the HEA, BRN5/.957. L/\.l~;'"\~Vienna, Austria.

(FAO/{llf'!t!~JSDA) Food ando AgricuItnreOrganízsrion of the United Nations/Intc,-,1f'lt;m;al Atomic Energy Agency/Unitcr StstesDepartment 01 Agriculture.2003. FAOIIAEAlUSDA manual for prod-uct qualiry control and shipping proceduresfor sterile mass-reared tepluitid fruit flies.Version· 5.0. IAEA, Vienna, Austria.http://www.iaea.org/programI11es/nafald4/index.html

Franz, G 2005. Genetic sexing strains inMediterranean fruit fly, an example for other

species arnenable to large scale rearing forthe sterile insect technique, pp. 427-451. InDyck, Y. A., J. Hendrichs, and A. S.Robinson (eds.), Sterile insect technique,Principies and practice in area-wide integrat-ed pest management. Springer, Dordrecht,The Netherlands.

Hendrichs, J. 1996. Action programmesagainst fruit flies of economic importance:session overview, pp. 513-519. 1/1

McPheron, B" and G Steck (eds.), Fruit flypests: a world assessment of their biologyand management. SI. Lucie Press, Florida,USA.

Hendrichs, J., M. J. B. Vreysen, W. R.Enkerlin, and J. P. Cayol. 2005. Strategicoptions ÍJ1 using sterile insects for area-wideintegrated pest management, pp. 563-600.//1Dyck, Y. A., J. Hendrichs, and A. S.Robinson (eds.), Sterile insect technique.Principies and practice in area-wide integrat-ed pest management. Springer, Dordrecht,The Netherlands.

Koyama, J" H. Kakinohana, and T.Miyatake. 2004. Eradication of the melonfly, Bactrocera curcubitae, in Japan: impor-tance of behavior, ecology, genetics, andevolution. Annual Review of Entomology49: 331-349.

Walder, J. M. '\1. 2002. Produção de moscas-das-frutas e seus inimigos naturais: associ-ação de moscas estéreis e controle biológico,pp. 181-188. In Parra, R. P. (ed.), Controlebiológico no Brasil: parasitóides e preda-dores. Editora Manole, Barueri, Sao Paulo,Brazil.

Wong, T. T. Y., M. M. Ramadan, J. C. Herr,and D. O. McInnis. 1992. Suppression ofa Mediterranean fruit fly (Diptera:Tephritidae) population with concurrent par-asitoid and sterile fly releases in Kula, Maui,Hawaii. Joumal of Economic Entomology85: 1671-1681.

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