Ecological niche and potential geographic distribution of the invasive fruit fly Bactrocera invadens (Diptera, Tephritidae) M. De Meyer1* , M.P. Robertson2, M.W. Mansell2,3, S. Ekesi4, K. Tsuruta5, W. Mwaiko6, J-F Vayssieres7` and A.T. Peterson8 1Royal Museum for Central Africa, Entomology Section, Tervuren, B-3080 Tervuren, Belgium: 2Department of Zoology and Entomology, University of Pretoria, Pretoria, 0001, South Africa: 3United States Department of Agriculture, APHIS, Pretoria, 0001, South Africa: 4International Centre of Insect Physiology and Ecology, PO Box 30772-00100, GPO, Nairobi, Kenya: 5Moji Plant Protection Station, MAFF, Nishikaigan, Moji-ku, Kitakyushu, 801-0841, Japan: 6Ministry of Agriculture and Food Security, Plant Health Services, P.O.Box 9071, Dar es Salaam, Tanzania: 7CIRAD, UPR Production Fruitiere, ` Montpellier, F-34398 France IITA, Cotonou, Benin: �� 8Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, Kansas 66045 USA Abstract Two correlative approaches to the challenge of ecological niche modeling (genetic algorithm, maximum entropy) were used to estimate the potential global distribution of the invasive fruit fly, Bactrocera invadens, based on associations between known occurrence records and a set of environmental predictor variables. The two models yielded similar estimates, largely corresponding to Equatorial climate classes with high levels of precipitation. The maximum entropy approach was somewhat more conservative in its evaluation of suitability, depending on thresholds for presence/absence that are selected, largely excluding areas with distinct dry seasons the genetic algorithm models, in contrast, indicate that climate class as partly suitable. Predictive tests based on independent distributional data indicate that model predictions are quite robust. Field observations in Benin and Tanzania confirm relationships between seasonal occurrences of this species and humidity and temperature. Keywords: Fruit flies, Bactrocera invadens, ecological niche models, potential distribution, GARP, Maxent (Accepted 23 December 2008) Introduction Fruit flies (Diptera: Tephritidae) are globally distributed, picture-winged flies of variable size. With 4000 species described, the family ranks among the most diverse groups of true flies (White & Elson-Harris, 1992 Thompson, 1999). *Author for correspondence Fax: +32 (0)2 7695695 E-mail: demeyer@africamuseum.be Bulletin of Entomological Research (2010) 100, 35���48 doi:10.1017/S0007485309006713 �� Cambridge University Press 2009 First published online 27 March 2009

Most are phytophagous, with larvae developing in the seed- bearing organs of plants. Although commonly named ���fruit flies,��� larval development can take place in other parts of host plants besides fruits, including flowers and stems. About 35% of fruit fly species attack soft fruits, including many commercially important ones (White & Elson-Harris, 1992). Several tephritids are critically important as fruit crop pests (Thompson, 1999). Economic impacts can be enormous, and control or eradication requires substantial budgets. For example, Dowell & Wange (1986) stated that establishment of major fruit fly threats to the Californian fruit industry would cause crop losses of US $910M yearly, and an era- dication program would cost US $290M. Annual losses in the eastern Mediterranean (Israel, Palestinian Territories, Jordan) linked to fruit fly infestations are estimated at US $192M (Enkerlin & Mumford, 1997). Indirect losses resulting from quarantine restrictions imposed by importing countries to prevent entry and establishment of unwanted fruit fly species can also be enormous. Most economically important fruit fly pests belong to four genera: Anastrepha Schiner (New World Tropics), Bactrocera Macquart, Ceratitis MacLeay and Dacus Fabricius (Old World Tropics). In recent decades, several Bactrocera species have been introduced accidentally in other parts of the world with estab- lished fruit industries in spite of quarantine procedures, often with major economic consequences. For example, the papaya fruit fly (B. papayae Drew & Hancock), introduced in Australia in 1995, led to a major blockade of papaya exports from northern Queensland and major losses to local growers in 1995���1998. Only through an eradication program, costing US $32.5M, could the pest be eradicated and commercial trade restored (Cantrell et al., 2002). The carambola fruit fly (B. carambolae Drew & Hancock), introduced into Suriname, has lead to drastic export reductions in the region, threaten- ing the US $1M annual export from Guyana to neighboring Caribbean countries (USDA/APHIS, 2000). Bactrocera invadens, a species native to Asia, was recorded for the first time on the African mainland in 2003 (Lux et al., 2003) and has already become a pest species of major con- cern to fruit growers. Here, we develop correlative ecological niche models (ENMs) for this species, which can be projected geographically to estimate the global distributional potential of the species (Peterson, 2003). ENMs are based on digital geospatial data layers and how they correlate with known occurrences of the species in its region of origin. We develop ENM predictions of invasive potential and test them quanti- tatively in Africa to measure the predictive power of the methodology for anticipating the species��� global potential distribution. Invasion history and economic impact of Batrocera invadens In 2003, an unknown Bactrocera species was found in Kenya (Lux et al., 2003). Taxonomic expertise showed that it was a member of the B. dorsalis complex, an Asian complex including several pest species (Drew & Hancock, 1994). Identical specimens from earlier surveys in Sri Lanka were initially classified as aberrant forms of B. dorsalis (Hendel) but eventually were re-identified as B. invadens (Drew et al., 2005). Immediately subsequent to its discovery in Kenya, the species was recorded in several countries on the African mainland (Mwatawala et al., 2004, Drew et al., 2005). It is now known to occur in tropical Africa from Senegal to Mozambique, as well as in the Comoro Islands in the Indian Ocean (De Meyer et al., 2007). The native range, known so far, ranges from Sri Lanka to southern India (Drew et al., 2005 Sithanantham et al., 2006) with some isolated records from Bhutan (Drew et al., 2007). It is not clear whether Bhutan should be considered as part of the native range. The B. dorsalis species complex comprises several morphologically very similar taxa (Drew et al., 2008). Other representatives of this complex occur in the same region (e.g. B. dorsalis and B. kandiensis: Drew & Hancock 1994). The native range of B. invadens is likely larger than currently assumed, since specimens may be misidentified as other representatives of the complex (see, for example, records for B. dorsalis distribution by Stephens et al., 2007). Therefore, the Bhutan records are considered here as part of the native range. This invasive species has major economic impacts, ranking among the most devastating pests of local horticul- tural products, particularly mango (Pouilles-Duplaix, 2007). Research in West (Vayssieres ` et al., 2005) and East Africa (Ekesi et al., 2006 Mwatawala et al., 2006a,b Rwomushana et al., 2008) has demonstrated that it can become dominant in mango monocultures. In Benin, 60% losses due to fruit flies were recorded on main mango cultivars of economic interest in the second half of the mango season (Vayssieres, ` 2007a), and phytosanitary pressure lead to uprooting mango plan- tations in one area (Borgou) in this country (Vayssieres,` 2007b). Native pest species, such as the mango fruit fly (Ceratitis cosyra (Walker)), appear to be outcompeted by this invasive species, although pre-invasion data are largely lacking. In addition, B. invadens is polyphagous in nature and has been reported from 44 different hosts belonging to 23 plant families (De Meyer et al., 2007). The timing and exact pathway of invasion by B. invadens into Africa are not known. An intensive 1999���2004 sam- pling program (Copeland et al., 2006) examined 4000 fruit samples ( 980,000 pieces of fruit) from 882 plant taxa and 116 plant families from coastal and western Kenya, and from the Central Highlands. However, not until March 2003 was B. invadens collected in the coastal region (Lux et al., 2003). Fruit flies were sampled intensively in commercial mango orchards across coastal Guinea in West Africa in 1992���1996 (Vayssieres ` & Kalabane, 2000) and Mali in 2000 (Vayssieres ` et al., 2004) but did not detect B. invadens the first B. invadens specimens in that part of the African mainland were not detected until June 2004 (Drew et al., 2005). This species��� presence in these countries before 2000 is, therefore, unlikely. Unfortunately, no similar studies were conducted at that time elsewhere in Africa where the fly currently occurs. That the first specimens were from the East African coast may indicate that the species��� port of entry was the East African coast, although clear proof is lacking. A brief outbreak of a methyl eugenol-responding species in Mauritius in 1996, attributed to B. dorsalis (White et al., 2001), may actually have been B. invadens. The available non- teneral sample was recently re-examined, but results were inconclusive (White, 2006). In Asia, the earliest specimens date to 1993 in Sri Lanka (Drew et al., 2005), 2000 for Bhutan (Drew et al., 2007) and 2005 for India (Sithanantham et al., 2006). However, given likely confusion with B. dorsalis, careful revision of all Bactrocera material from that region is needed. 36 M. De Meyer et al.