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CARIBBEAN FOOD CROPS SOCIETY 44 Forty Fourth Annual Meeting 2008

Miami, Florida, USA

Vol. XLIV - Number 1 T-STAR Invasive Species Symposium

MEETING HOST:

TIP UNIVERSITY of UF FLORIDA IFAS 2008 Proceedings of the Caribbean Food Crops Society. 44(1):135-174. 2008

CARAMBOLA FRUIT FLY SITUATION IN LATIN AMERICA AND THE CARIBBEAN

Alies van Sauers-Muller, Carambola Fruit Fly Program Coordinator, Agricultural Experiment Station, Ministry of Agriculture, Animal Husbandry and Fisheries Letitia Vriesde laan 8, Paramaribo, Suriname. Email [email protected]

ABSTRACT: The carambola fruit fly, Bactrocera carambolae Drew and Hancock (CFF) is a member of the oriental fruit fly species complex. CFF was recognized to be present in Suriname in 1986, but it appears to have been present since at least 1975. CFF originated in Asia, where it occurs in Indonesia, Malaysia and southern Thailand. Fifteen percent of Suriname's human population originated in Indonesia. Probably the CFF was introduced into the Western Hemisphere by persons traveling from Indonesia to Suriname. The spread of the CFF infestation and infested host plants were delimited soon after 1986. By 1990, the fly had spread throughout the northern (inhabited) part of Suriname and eastward into French Guiana. Subsequently the CFF spread westward to infest two border villages in Guyana, and, east of French Guiana, into the Brazilian State of Amapa. CFF's major hosts are carambola (Oxalidaceae: Averrhoa carambola L.) and curaçao apple (Myrtaceae: Syzygium samarangense (Blume) Merr. and Perry), which originated in Asia. Most tropical fruits are good hosts of CFF. In 1990 the first control actions were undertaken to prevent the fly from spreading westwards, and in 1997 a regional eradication program was initiated. The male annihilation technique (MAT) served as the main method for eliminating CFF populations. This technique involved the area-wide placement of 5 cm χ 5 cm χ 1 cm wood fiber blocks impregnated with methyl-eugenol mixed with malathion to lure and annihilate CFF males. Additional methods used were bait sprays, soil treatments, host fruit destruction, and pruning of host fruits. In urban areas the MAT technique was applied by spraying min-u-gel containing methyl eugenol and malathion onto tree trunks, electric-line poles etc. After good progress in freeing areas of CFF, the project closed in 2003 due to lack of funding, and by 2007 the CFF had reclaimed all cleared areas that had been infested at the initiation of the control project. In addition, the CFF has spread to new areas in Guyana. In the Brazilian State of Amapa, containment activities will continue relentlessly, due to the threat the pest represents to the Brazilian fruit industry. For Suriname, control of fruit flies in the future will have to include suppression of the CFF as one of the major economically important tropical fruit fly species. Alternative methods will be evaluated including biological control and localized application of bait sprays in fruit production areas. The establishment and expanding distribution of the CFF in the Guyana's represents a continuous threat to the fruit production in the Caribbean and the Latin American region.

KEY WORDS: Bactrocera carambolae, carambola fruit fly, hosts, geographical distribution, male annihilation technique, bait sprays, biological control

RESUMEN: La mosca de la carambola, Bactrocera carambolae Drew and Hancock (CFF) es una especie en el complejo de la mosca de la fruta Oriental. Su presencia en Suriname fue reconocida en 1986, pero parece haber estado presente al menos desde 1975. La CFF es originaria de Asia, donde se encuentra en Indonesia, Malasia y el sur de Tailandia. El 15 % de la

170 poblaciôn de Suriname es originaria de Indonesia. Probablemente la mosca fue introducida en el Hemisferio Occidental por personas que viajaron de Indonesia a Suriname. La delimitaciôn de la infestaciôn de la CFF y sus hospedantes fueron determinados poco tiempo después de 1986. Para 1990 la mosca se habia expandido a través del Norte (la parte habitada) de Suriname y en el Este hacia adentro de la Guayana Francesa. Subsecuentemente la CFF se dispersé hacia dos aldeas en la frontera con Guayana y, en el este de Guayana Francesa, hacia adentro del estado de Amapâ en Brasil. Los principales hospedantes de la CFF son carambola (Oxalidaceae: Averrhoa carambola L.) y perita de agua (Myrtaceae: Syzygium samarangense (Blume) Merr. and Perry), ambos de origen asiâtico. Muchas frutas tropicales son buenos hospedantes de la CFF. En 1990 se iniciaron las primeras acciones de control para prévenir la diseminaciôn de la mosca hacia el Oeste y en 1997 se iniciô un programa regional de erradicaciôn. La técnica de aniquilaciôn de machos (ΤΑΜ) fue usada como principal método para eliminar poblaciones de la CFF. Esta técnica consiste en la colocaciôn en forma extensiva de bloques fibrosos de 5 cm χ 5 cm χ 1 cm que fueron impregnados con metilo-eugenol y malatiôn para atraer y aniquilar los machos de la CFF. Métodos adicionales usados fueron la aspersion de cebos tôxicos y aplicaciones al suelo, destrucciôn de frutas de hospedantes, y la poda de hospedantes. En zonas urbanas la ΤΑΜ fue aplicada en forma de aspersiones de min-u-gel con metilo-eugenol y malatiôn sobre troncos de ârboles, postes de electricidad, etc. Después de buen progreso en liberar areas de la CFF, el proyecto cerrô en 2003 a falta de recursos y para 2007 la CFF se habia dispersado nuevamente a todas las areas que estaban infestadas al inicio del proyecto de control. Asimismo, la mosca se dispersé hacia nuevas areas en Guayana. En el Estado de Amapâ en Brasil, las actividades de control en la barrera de contenciôn continuaran inexorable, en vista de la amenaza que esta plaga representa para la fruticultura brasilena. Para Suriname, el control de moscas de la fruta tendrâ que incluir la supresiôn de la CFF como una de las especies tropicales de mosca de la fruta de mayor importancia econômica. Métodos alternatives serân evaluados, incluyendo el control biolôgico y la aplicaciôn localizada de cebos tôxicos en âreas de produccion de frutas. El establecimiento de la CFF en las Guayanas representa una continua amenaza para la produccion fruticola en el Caribe y la region de América Latina.

PALABRAS CLAVES: Bactrocera carambolae, mosca de la carambola, hospederos, distribuciôn geogrâfica, técnica de aniquilaciôn de machos, aspersion de cebos tôxicos, control biolôgico.

INTRODUCTION

The carambola fruit fly, Bactrocera carambolae Drew and Hancock, also known as CFF, is a member of the oriental fruit fly species complex. This fly appears to have been present in Suriname since at least 1975, because preserved specimens of that date are present in the insect collection of the Suriname Agricultural Experiment Station (van Sauers-Muller, 1991). It was collected again in 1981 from curaçao apple, and finally in 1986 identified as Dacus dorsalis, the oriental fruit fly. However, it became clear soon that what was thought to be the oriental fruit fly was a complex of over forty (Drew and Hancock, 1994) to seventy-five species (Clarke et al., 2005). Hereafter this complex is know as the Bactrocera dorsalis complex. The carambola fruit fly is one of these species.

136 CFF originated in Asia, where it occurs in Indonesia, Malaysia and southern Thailand (White et al., 1992) and several surrounding countries (Clarke et al., 2005). The introduction of CFF into the Western Hemisphere is thought to have been mediated by persons traveling from Indonesia to Suriname, since Suriname has a diverse human population, 15 % of which originated in Indonesia.

MATERIALS AND METHODS

After the discovery of CFF in Suriname, surveys were conducted by collecting fruits to delimit the spread of the infestation and to identify the infested host plants. By 1990, the fly had spread mainly into the northern (inhabited) part of Suriname and eastward into French Guyana. Subsequently, CFF spread westward to infest two border villages in Guyana, and southeastward into the Brazilian State of Amapä (Fig. 1). By that time, surveys were conducted using McPhail traps baited with Torula yeast tablets and with Jackson traps baited with methyl-eugenol, and after several years (1990 in Suriname) also with malathion as the killing agent in these Jackson traps.

From 1986 to the present, fruits have been collected to determine the host plants of the carambola fruit fly. This collection also provided information on native Anastrepha fruit flies and the parasitoids present in the country. In all four countries detection systems were harmonized using standardized methods with Jackson traps (baited with methyl-eugenol and the killing agent malathion); in areas where the MAT technique was applied trapping with plastic McPhail traps with Torula yeast served as the detection system.

The male annihilation technique (MAT) served as one of the main methods for eliminating CFF populations. This involved the area-wide placement 5 cm χ 5 cm χ 1 cm pressed wood fiber blocks (P.T. O'Malley Lumber in Baltimore, Maryland) impregnated with methyl-eugenol mixed with malathion to lure and kill CFF males. In urban areas this method was replaced by the use of min-u-gel, a powder mixed with methyl-eugenol and malathion sprayed on tree trunks, electricity poles, etc. Only in certain parts in the city, with larger backyards with fruit trees and streets wider apart, blocks were applied additionally. In manuals for the oriental fruit fly control a distribution rate of 4 fiber blocks per hectare is advised. In 2001, calculations based on field experience showed that over 18 blocks per hectare were needed to eradicate the carambola fruit fly from an area.

Additional methods were applied in areas with more persistent fly populations. These were bait sprays (Nulure with malathion (57%) 4:1), applied using manual backpack or motorized backpack sprayers and in several areas aided with aerial applications with an agricultural plane. Also host fruit destruction, pruning of host fruits, and occasionally soil treatments to control pupae (using the insecticide diazinon) were used (van Sauers-Muller and Fleurkens, in preparation).

RESULTS AND DISCUSSION

CFF infests a number of hosts. Its major hosts are carambola (Oxidalidaceae: Averrhoa carambola L.) and Curaçao apple, also referred to in the literature as Java apple (Myrtaceae:

137 Syzygium samarangense (Blume) Merr. and Perry). These two fruit species originated, as did several others, in Asia. Other good hosts are mango (Anacardiaceae: Mangifera indica L.), sapodilla (Sapotaceae: Manilkara achras (Mill.) Fosberg), West-Indian cherry (Malpighiaceae: Malpighia punicifolia L.) - also known as Barbados cherry and acerola, guava (Myrtaceae: Psidium guajava L.), star apple (Sapotaceae: Chrysophyllum cainito L.), jujube (Rhamnaceae: Ziziphus jujuba Mill.). Minor hosts are golden apple (Anacardiaceae: Spondias cytherea), Surinam cherry (Myrtaceae: Eugenia uniflora L.),

Fig. 1. Known distribution of the carambola fruit fly in Guyana, Suriname, French Guiana and Brazil just before activities of the regional eradication program were initiated. sweet orange (Rutaceae: Citrus sinensis Osbeck), grapefruit (Rutacea: Citrus χ paradisi Macfad.), mandarin (Rutaceae: Citrus reticulata Blanco), tropical almond (Combretaceae: Terminalia catappa L.), cashew (Anacardiaceae: Anacardium occidentale L.), hog plum (Anacardiaceae: Spondias mombin L.) and Malay apple (Myrtaceae: Syzygium malaccense (L.) Merr. and Perry). Infestations were also found in some forest fruits; although mainly in areas with high CFF populations. Apart from hog plum, infestations were found in Eugenia cf patrisii Vahl, a forest cherry (Myrtaceae) (van Sauers-Muller, 2005) and in Inga sp., a Mimosaceae; all these samples came from locations in villages. None of these forest fruits were found infested when they were collected from locations further away from CFF populations.

This fruit collection also provided information on the local fruit fly species and their parasitoids (van Sauers-Muller, 2004). Although more than six local parasitoids were found, none of these

138 seemed of any importance as parasitoid for the Carambola fruit fly. One important fruit fly species, which is present in many parts of South America, the Mediterranean fruit fly (medfly), Ceratitis capitata Wied., has not been found in Suriname during all trapping and fruit collection activities.

In 1990 the first control actions were undertaken in Suriname to prevent the fly from spreading further westwards. Actions were undertaken in Wageningen (district Nickerie) and Coronie (Fig. 2 and 3) (van Sauers-Muller, 1993). In the village of Wageningen (approx. 3 km2), min-u-gel was applied as the MAT method; in Coronie (50 km2) first several major host trees were pruned

Fig. 2. Carambola fruit fly control action area, 1990-1997. to decrease the population of the fly, followed by min-u-gel applications and later with the use of the impregnated pressed wood fiber blocks. The relatively isolated conditions of these infested areas (bordered in the north by the Atlantic Ocean, to the south by extensive swamps) made the successful application of MAT possible.

These control actions were extended to larger areas at the start of the regional program in 1997. The countries involved in this program were Guyana, Suriname, French Guiana and Brazil (especially with the state of Amapa, which borders French Guiana) (Fig. 3). In 1997, large scale control of CFF was initiated in a number of areas where CFF was found, working in Suriname from west to east and in French Guiana from east (St. Georges) to west. The main control method was the ground application of pressed wood fiber blocks impregnated with a 4:1 mixture of methyl-eugenol and malathion 96 % u.l.v. This resulted in a reduction of the infested areas in the following years (Fig. 4).

139 intries and regions involved in CFF project ^ Georgetown Saramacca "Jick^fiJoronie j I Paramaribo ^Wageningeij Δηι irc^roniage'nar i sparute-jsi^ ?Ri ( WWWwpayenne ' ^rojfdiondq 1 rrench Guyai; Sipaliwini ^ st &9e>rses-"^ Suriname Camepi^ i'Äis Sautesj

Fig. 3. Countries (Guyana, Suriname, French Guiana and Brazil) involved in the Regional Carambola Fruit Fly Control Program.

In Guyana, trapping for carambola fruit fly started in 1987; CFF was first found in 1993 in two villages (Orealla and Siparuta) on the border with Suriname. The infestation was eradicated by 1998 when the last fly was found in April, 1998. Two years later the whole country was declared free of CFF (Malavasi, A. and D. Midgarden, 2000), and eradication gradually progressed eastward, freeing most of Suriname from CFF (Fig. 4).

To the east, in French Guiana, the first carambola fruit fly was found in 1989 and in Brazil in 1996 in the Oiapoque area, adjacent to the heavily infested St. Georges village (Fig. 3) in French Guiana (Malavasi et al. 2000). CFF was eradicated from these areas bordering Brazil and in the eastern half of French Guiana (Fig. 4).

140 Γ \ . Geographical distribution carambola fruit fly 2002

distribution of caramboIMralt fly -- tree of carambola fruit fly control operations ongoing • Infested wllh carambola f ru»lty

600 Kilometers

Fig. 4. Reduction in distribution of the CFF in the four countries before the regional program had to be closed.

Since the closing down of the regional program in 2003, due to lack of funding, CFF has gradually spread and re-infested areas that had previously been freed from infestation. By 2007, all areas that had been infested at the initiation of the control project had again become infested (van Sauers-Muller, Α., 2006). In addition, the CFF has spread to new areas in Guyana (Fig. 5). In the Coronie district of Suriname this happened gradually, suggesting a natural spread of the fly. However the village of Apura on the border with Guyana is over 90 km from infested areas, so it is likely that re-infestation was caused by movement of infested fruits. The same is valid for the new areas in Guyana, as the distance between these and the infested areas either in Suriname or on the Corantijn River is over 180 km. Apart from the official border controls and ports of entry (Macapa and Belem) controls in all involved countries and the road controls in the State of Amapa, Brazil, no quarantine measures are in place to control the human spread of CFF. A public relation campaign is in place in the State of Amapa in order to decrease the transit of host material in the State.

141 Fig. 5. Re-infestation of areas in the four countries.

In Brazil, an extensive detection system is in place and CFF is usually eradicated every time an outbreak occurs (Godoy, M.J.S. 2006). Surveillance and eradication efforts are continuing on a permanent basis, due to the importance of the pest for the fruit industry. Due to the cessation of all eradication activities in French Guiana, a continuous containment and control program will be necessary along the Oiapoque River, since CFF is not under control in the village of Saint Georges (French Guiana). For Suriname, control of fruit flies in the future will have to take into account the control ofthe CFF as one ofthe major tropical fruit fly species. Alternative methods will be evaluated including biological control and localized application of bait sprays for suppression oftropical fruit flies in orchards.

In some islands in the Caribbean, trapping surveys include trapping for Bactrocera species; but up to the present no CFF has been caught.

CONCLUSIONS

In conclusion, the closure of the successful Regional Carambo1a Fruit fly Program resulted not only in the discontinuation of eradication activities, but also in the loss of all progress made and the reinvasion ofthe freed areas. The permanent establishment and expanding distribution ofthe CFF in Guyana, Suriname, French Guiana and Brazil represents a continuous threat to the fruit production in the Caribbean and the Latin American region. Areas in the region most exposed to the potential spread ofCFF are shown in Figure 6.

142 Fig. 6. Potential spread of the carambola fruit fly in northern South America and in the Greater Caribbean Region.

ACKNOWLEDGEMENTS

I am very grateful to several anonymous reviewers in helping improve the clarity and accuracy of this report.

REFERENCES

Clarke, A.R., K.F. Armstrong, A.E. Carmichael, J.R. Milne, S.Raghu, G.K. Roderick and D.K. Yeates. 2005. Invasive phytophagous pests arising through a recent tropical evolutionary radiation: The Bactrocera dorsalis complex of fruit flies. Annu. Rev. Entomol. 50: 293-319. Drew, R.A.I, and D.L. Hancock. 1994. The Bactrocera dorsalis complex of fruit flies (Diptera: Tephritidae: Dacinae) in Asia. Bulletin of Entomological Research, Suppl. 2, p. 1-68. Godoy, M.J.S. 2006. The Carambola fruit fly program in state of Amapa, Brazil. Abstracts 7th International Symposium on fruit flies of economic importance. Bahia, Brazil. Area wide action programs, ID 372-1. Malavasi, A. and D. Midgarden. 2000. Annual report, Carambola fruit fly programme. 15 p. Malavasi, Α., A. van Sauers-Muller, D. Midgarden, V. Kellman, D. Didelot, Ph. Caplong and O. Ribeiro. 2000. Regional programme for the Eradication of the Carambola Fruit Fly in South America. In: Proceedings of 5^ Int. Symp. of Fruit Flies of Economic Importance, Penang, Malaysia, June 1-5, 1998, p. 395-399. Van Sauers-Muller, A. 1991. An overview of the Carambola fruit fly Bactrocera species (Diptera: Tephritidae) found recently in Suriname. Florida Entomologist, 74 (3): 432- 440. Van Sauers-Muller, A. 1993. Pilot eradication project for the Carambola fruit fly in Coronie, Suriname. In: M. Aluja and P. Liedo, Fruit Flies: Biology and Management, pp 439-442.

143 Van Sauers-Muller, A. 2004. Records of native parasitoids of fruit flies in Suriname, South America. 5th Meeting of the Working Group on Fruit flies of the Western Hemisphere. Ft. Lauderdale, Florida, p.68. Van Sauers-Muller, A. 2005. Host plants of the Carambola Fruit Fly, Bactrocera carambolae Drew & Hancock (Diptera: Tephritidae), in Suriname, South America. Neotropical Entomology 34 (2), 203-214. Van Sauers-Muller, A. 2006. Carambola fruit fly programme Suriname. Abstracts 7th International Symposium on fruit flies of economic importance. Bahia, Brazil. Area wide action programs, ID 310-1. Van Sauers-Muller, A. and M. Fleurkens. 2009. Control methods applied for suppression and eradication of the Carambola fruit fly in Suriname, South America. In preparation.

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