Proceedings of 6th International Fruit Symposium 6–10 May 2002, Stellenbosch, South Africa pp. 173–177

South American cucurbit fruit fly-free area in

R. Braga Sobrinho1*, R.N. Lima1, M.A. Peixoto2 & A.L.M. Mesquita1 1EMBRAPA – National Tropical Agroindustry Research Center, Rua Dra. Sara Mesquita 2270, 60.511-110 Fortaleza – Ceara Brazil 2EMBRAPA Assistantship

Among tephritid fruit , the South American cucurbit fruit fly, grandis (Macquart) (Diptera: ), is considered a pest of quarantine importance in the melon-producing zones of the State of , Brazil. The northeastern part of the State, comprising , Icapui, Itaiçaba, Aracati, and Quixeré counties, has become a melon-producing zone with an estimated area under production of approximately 4000 ha. This area borders the A. grandis-free area of the neighbouring State of Rio Grande do Norte, Brazil. However, the melon-producing area of Ceará State is not recognized as an A. grandis-free area by national and international phytosanitary agencies. The future A. grandis-free area in the State of Ceará is intended to be 4063 km2 in extent (3.8% of the total geographic area of the state of Ceará). Fruit fly ,especially A.grandis, as well as host plants,were surveyed. The most common host fami- lies found, besides , were Anacardiaceae, Myrtaceae, Annonaceae, Sapotaceae and Malpighiaceae.The highest populations counted were 0.2 and 1.6 flies per trap per day in 2000 and 2001, respectively. During the survey period McPhail traps captured 16 488 adult flies of which 10.3% were Anastrepha and 89.7% were Ceratitis capitata. In a search for immature stages of fruit flies,fruit samples kept in the laboratory and melon fruits cut in the field did not yield any A. grandis. No adult or immature stages of A. grandis were detected during the study period.

INTRODUCTION Zucchi (1988), in which 77 Brazilian species were Among tephritid fruit flies, the South American listed. In the last 20 years only 17 additional cucurbit fruit fly, Anastrepha grandis (Macquart), is Anastrepha species were found in Brazil. Of 92 considered a pest of quarantine importance in the Anastrepha species found in Brazil, hosts have production zone of melon (Cucumis melo L.) in the been recognized for only 41 species. Anastrepha State of Ceará, Brazil. This zone is situated in the is the most polyphagous genus in Brazil, with 58 area called ‘Median River Valley’ and species of host plants recorded. Only a single is located between 5° and 7° S and 46° and 47° W. host has been recorded for 21 Anastrepha species, The area under melon has recently been esti- while A. obliqua is associated with 23 host species. mated as 4000 ha. This area borders the A.grandis- However, A. grandis has been found only on hosts free area of the neighboring state of Rio Grande do of the family Cucurbitaceae (Zucchi 2000). Norte. However, the melon-producing zone of The Mediterranean fruit fly, Ceratitis capitata Ceará is not yet recognized as an A. grandis-free (Wied.) is one of the most serious fruit pests in the area by national and international phytosanitary world, infesting more than 300 plant species agencies (Braga Sobrinho et al. 1999b, 2001). (Liquido & Cunningham 1991). Several studies on The tephritid genus Anastrepha is an economi- the population dynamics of C. capitata have been cally important fruit fly, infesting over 100 plant conducted in the tropics (Vargas & Carey 1989; species from northern to southern Brazil (Malavasi Nishida et al. 1985; Zucchi 1988; Harris et al. 1993; et al. 1980; Norrbom & Kim 1988; Zucchi 2000). Souza & Nascimento 1999). Important species such as A. fraterculus (Wiede- Fruits of the family Cucurbitaceae,such as water- mann), A. obliqua (Macquart), A. sorocula (Zucchi) melon (Citrullus lanatus L.), melon and several and A. grandis are highly destructive pests of tropi- species of pumpkin ( spp.), have been cal and temperate fruits (Braga Sobrinho et al. mentioned as hosts of A. grandis. The geographic 1999a).Adults of A.grandis are easily distinguished distribution of A. grandis includes Brazil, northern from the other species by their larger size.The other Argentina, Paraguay and the Andean Mountain species require detailed examination of the Chain from Bolivia to Venezuela (Norrbom & Kim ovipositor for accurate identification (Malavasi 1988; Silva & Malavasi 1996). In Brazil its distribu- 1984; Steck 1991; Zucchi 1978). The most recent tion encompasses the southern, southeastern and catalogue of Anastrepha spp. was published by central states and part of the northern state of Bahia (Silva & Malavasi 1996; Lima 1934; Silva et al. *To whom correspondence should be addressed. E-mail [email protected] 1968; Zucchi 1988; Zahler 1990). 174 Proceedings of the 6th International Fruit Fly Symposium

The objective of this study was to monitor, Table 1. Trap placement in fruit trees and in melon determine and study the population dynamics fields in 2000 and 2001. of tephritids, based on international protocols with respect to proof of the area-free status of No. of traps A. grandis. Year Fruit trees Melon fields McPhail Jackson McPhail Jackson MATERIALS AND METHODS Surveying and monitoring studies in commercial 2000 17 11 228 0 melon and fruit-producing areas were under- 2001 671 61 418 0 taken from August 2000 to December 2001. Six counties in the State of Ceará, Brazil, located in the area called ‘Median Jaguaribe River Valley’ fruit areas such as small orchards and backyards, between latitude 5° and 7° south and longitude 46° and in strategic locations such as crossroads and and 47° west were included in this study. The packing houses in the above counties. In melon counties involved were Aracati (1276 km2), Icapuí fields McPhail traps were placed under small (429 km2),Itaiçaba (240 km2),Jaguaruana (771 km2), wooden shelters 50 cm above soil level. In other Quixeré (746 km2) and Limoeiro do Norte (600 km2), areas traps were hung in the upper two-thirds of with a total area of 4062 km2. In order to facilitate fruit fly host trees. operations,the area of the six counties was divided A total of 1406 traps (1334 McPhail and 72 in two sectors, based on methodology established Jackson) were installed in fruit trees and in melon by IPLANCE (State of Ceará Planning Institute). fields in 2000 and 2001 (Table 1). Of these, 54% Sector A included the first three counties, and were placed in fruit trees and the remaining 46% Sector B the other three.These counties border the were placed in melon fields. Sectors A and B had A.grandis-free area in the neighboring State of Rio 1637 ha and 1261 ha of melon, respectively. The Grande do Norte. However, the melon-produc- average trap density was one McPhail trap per 5 ha ing area of the State of Ceará has not been recog- of melon. In fruit trees one McPhail trap per 2 km2 nized as an A. grandis-free area by national and was used,while in urban areas one McPhail and one international phytosanitary agencies. Jackson trap were installed per 1 km2. In this study a highly accurate system for moni- The fruit fly population index used was flies per toring and detecting fruit fly pests was used, trap per day (FTD). Climatic data were recorded at consisting of McPhail and Jackson traps baited strategic points in the survey areas. Fruits were with food attractants and pheromone lures. The systematically collected and kept in the laboratory pheromone for Jackson traps was a polymeric to determine adult emergence. Adults collected dispenser containing trimedlure. The food attrac- from traps were taken to the laboratory for sex tant for McPhail traps was 5.0% hydrolysed protein separation and species identification. (600 ml in each trap) with 3.0% borax. In each Jackson trap a sticky carton panel was inserted to RESULTS AND DISCUSSION ensure retention. This panel was replaced During the study period the McPhail and Jackson each week at trap inspection. Every four weeks traps captured 1698 Anastrepha spp. and 14 790 the pheromone dispensers were replaced. The C. capitata. Approximately eight times more hydrolysed protein was replaced weekly and the Medfly were captured in 2001 than in 2000 were collected, counted and taken to labo- (Table 2), highlighting the progressive population ratory for species identification. McPhail Traps increase of C. capitata in these fruit-producing were installed in melon-producing areas, other counties. The highest catches of Medfly in Aracati

Table 2. Number of fruit flies captured, and the flies/trap/day (FTD) index in fruit trees and in melon fields in 2000 and 2001.

No. of fruit flies captured Year Anastrepha spp. Ceratitis capitata FTD Fruit trees Melon fields Fruit trees Melon fields

2000 2 700 120 492 0.2 2001 591 405 13 939 239 1.6 Braga Sobrinho et al.: South American cucurbit fruit fly-free area in Brazil 175

Table 3. Numbers of Ceratitis capitata and Anastrepha spp. trapped in counties of Sectors Aand B during 2001.

Sector A County C. capitata

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Aracati 0 442 6103 000013028414824438 Icapuí 0 0 0 0004 95732816097 Itaiçaba 0 0 51 0040 1487849 Total 0 442 6154 0044140345484482184

Sector B County C. capitata

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Quixeré 0 35 210 0 0 1400 0 396 488 126 46 35 Jaguaruana 0 0 499 00804080832 Limoeiro do Norte 36 7 168 0 0 2007 0 6 7 27 7 13 Total 36 42 877 0 0 3415 0 810 495 161 56 50

Sector A County Anastrepha spp.

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Aracti 0 0 138 13 25 0 6 02000 Icapuí 0 0 0 1115 42231911 Itaiçaba 0 0 0 2 24 29 110 01000 Total 0 0 138 16 50 30 121 4 25 3 19 11

Sector B County Anastrepha spp.

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Quixeré 0 7 160 18 31 40 0 31000 Jaguaruana 0 0 69 6 42 0 0 51000 Limoeiro do Norte 0 1 191 1300 00000 Total 0 8 420 25 76 40 0 82000 were probably due to the existence of several spectively, and average maximum and minimum small orchards of Barbados cherry (acerola) and relative humidity of 95.4% and 47.7%, respec- guava in this county. Of the total number of tively. Most rain falls between January and May, Anastrepha and C. capitata captures, 88.8% with an average annual precipitation less than came from traps placed in other fruit trees such as 600 mm. During the rainy season most growers mango (Mangifera indica), acerola (Malpighia do not produce melon due to rain damage and emarginata), papaya (Carica papaya), Indian al- diseases. mond (Terminalia catappa), guava (Psidium guava), In 2000 zero captures of fruit flies were recorded star fruit (Averrhoa carambola), grape (Vitis spp.), in Icapuí and Itaiçaba counties. In that year the citrus (Citrus spp.), while 11.2% were from traps number of traps placed in fruit trees was very low. in melon fields. It was observed that more fruit flies were caught Climatic conditions in the whole study area did in traps placed in fruit trees outside the melon not vary much, with average maximum and field. For this reason, in 2001 the proportion of minimum temperatures of 32.8°C and 22.5°C, re- traps placed in melon fields was reduced. 176 Proceedings of the 6th International Fruit Fly Symposium

Table 4. Numbers of fruit flies emerged from edible and non-edible host fruits collected in the Jaguaribe River Valley during 2001.

Common name Scientific name Weight (kg) No. of fruits No. of adults Anastrepha spp. C. capitata

Mango Mangifera indica 76 316 0 61 Acerola Malpighia emarginata 28 2770 17 149 Papaya Carica papaya 27 88 0 0 Indian almond Terminalia catappa 18.6 480 32 187 Guava Psidium guava 63 562 245 112 Canapum Phyllis angulata 0.95 137 0 0 Cajá Spondias mombin 8.5 485 32 95 Star fruit Averrhoa carambola 2.5 45 05 08 Grape Vitis spp. 3.6 396 0 0 Orange Citrus spp. 13 99 0 0 Total 5378 331 612

Hydrolysed protein and the Brazilian McPhail been found in Cucurbitaceae fruits or captured in trap have played an important role in monitoring traps in the study area. fruit flies. However, problems include the number of other insects captured and the fact that they are ACKNOWLEDGEMENTS cumbersome to deploy and service. This work was supported by Brazilian Northeast The monthly captures of Anastrepha spp. and Bank (BNB). We thank to Dr Francisco das Chagas C. capitata in Sectors A and B during 2001 is shown Oliveira Freire for reading the manuscript and in Table 3. The number of Medflies captured in making valuable suggestions. We thank to Ana Aracati, Quixeré and Limoeiro do Norte (Sector A) Carina Fernandes Ometto, Carlos Augusto Teixeira was very high, especially during the rainy season Braga, Maria do Socorro C. S. Mota and Antônia from January to June. Localized areas of guava, Régia A.Cabral for their help in field and laboratory Barbados cherry and spondias are spread out in tasks. these three counties. Traps placed in these hosts caught high numbers of C. capitata, higher than REFERENCES those of Anastrepha spp. In 2001 most Medfly BRAGA SOBRINHO, R., OMETTO, A.C.F. & MALAVASI, A. were caught in traps placed in fruit crops rather 2001. Free area for South American cucurbit fruit fly in than in melons. the State of Ceará-Brazil. In: De Longo, O. & Mellado, R. (Eds) Proceedings of the 4th Meeting of the Working Host fruit collections in Sectors A and B showed Group on Fruit Flies of the Western Hemisphere. that C.capitata was present in most collected fruits 203–204.Working Group on Fruit Flies of the Western (Table 4). Fruit hosts such as Barbados cherry, Hemisphere, Mendoza, Argentina. Cajá, guava and Indian almond are very impor- BRAGA SOBRINHO, R., MESQUITA,A.L.M.& OMETTO, A.C.F. tant Medfly hosts in the monitored areas. 1999a. Estratégias fitossanitária de pré-colheita para exportação de frutas (Áreas Livres, Baixa Prevalência The population of Medfly in this region has e Erradicação). In: Memoria de Exigências quarente- increased over the last 10 years due to increasing nárias para exportação de frutas tropicais e areas of Barbados cherry and guava. Even though subtropicais.57–86.EMBRAPA/CNPAT,Fortaleza Ceará, Indian almond is a highly preferred host for Brazil. Medfly, the distribution of this host in the counties BRAGA SOBRINHO, R., OMETTO, A.C.F, MESQUITA, A.L.M. was very narrow and it is very scarce as a shade & MALAVASI, A. 1999b. Survey and population monitoring of fruit flies in the state of Ceará-Brazil. plant in streets and villages. The increasing areas In: Proceedingsofthe3rdMeetingoftheWorkingGroup and host diversity of edible fruits highly preferred on Fruit Flies of the Western Hemisphere. 17. 3rd by fruit flies, especially Medfly, without any Working Group on Fruit Flies of the Western Hemi- programme for population reduction,constitutes a sphere, Guatemala City, Guatemala. threat to the development of fruit production for HARRIS, E.J., VARGAS, R.I. & GILMORE, J.E. 1993. Seasonal export in these counties. occurrence and distribution of Mediterranean fruit fly (Diptera: Tephritidae) in upland and lowland The most important result from this study is that areas on Kauai, Hawaii. Environmental Entomology to date, no adult or immature A. grandis have 22: 404–410. Braga Sobrinho et al.: South American cucurbit fruit fly-free area in Brazil 177

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