COVER SHEET This is the author version of article published as: Clarke, Anthony R. and Armstrong, Karen F. and Carmichael, Amy E. and Milne, John R. and Roderick, George K. and Yeates, David K. (2005) Invasive Phytophagous Pests Arising Through a Recent Tropical Evolutionary Raditation : The bactrocera dorsalis complex of fruit flies . Annual Review of Entomology 50:pp. 293319. Copyright 2005 Annual Reviews Inc Accessed from http://eprints.qut.edu.au B. DORSALIS COMPLEX OF FRUIT FLIES Invasive Phytophagous Pests Arising Through a Recent Tropical Evolutionary Raditation: THE BACTROCERA DORSALIS COMPLEX OF FRUIT FLIES Anthony R. Clarke1, Karen F. Armstrong2, Amy E. Carmichael1, John R. Milne3, S. Raghu4, George K. Roderick5, and David K. Yeates6 1 School of Natural Resource Sciences, Queensland University of Technology, GPO Box 2434, Brisbane, Qld 4001, Australia; e-mail: a.clarke@qut.edu.au and a.carmichael@qut.edu.au 2 Soil, Plant and Ecological Sciences Division, PO Box 84 Lincoln University, Canterbury, New Zealand; e-mail: armstron@lincoln.ac.nz 3 Department of Biology, Faculty of Science, Mahidol University, Rama 6 Road, Bangkok 10400, Thailand; e-mail: frjrm@mucc.mahidol.ac.th 4 Alan Fletcher Research Station, Queensland Department of Natural Resources & Mines and CRC for Australian Weed Management, PO Box 36, Sherwood, Qld 4075, Australia; e-mail: raghu.s@nrm.qld.gov.au 5 Environmental Science, Policy and Management, Division of Insect Biology, 201 Wellman Hall MC 3112, University of California, Berkeley, CA 94720-3112, USA; e-mail: roderick@nature.berkeley.edu 6 Australian National Insect Collection, CSIRO Entomology, PO Box 1700, Canberra ACT 2601, Australia; e-mail: david.yeates@csiro.au Key Words diagnostics, larval host range, invasion biology, resource use, pest status Abstract The Bactrocera dorsalis complex of tropical fruit flies (Diptera: Tephritidae: Dacinae) contains 75 described species, largely endemic to South-east Asia. Within the complex are a small number of polyphagous pests of international significance, including B. dorsalis s.s., B. papayae, B. carambolae and B. philippinensis. The majority of species within the complex were first described in 1994 and since then substantial research has been undertaken in developing morphological and molecular diagnostic techniques for their recognition. Such techniques can now resolve most taxa adequately. Genetic evidence suggests that the complex has evolved in only the last few million years and development of a phylogeny of the group is considered a high priority to provide a framework for future evolutionary and ecological studies. As model systems, mating studies on B. dorsalis s.s. and B. cacuminata have substantially advanced our understanding of insect use of plant-derived chemicals for mating, but such studies have not been applied to help resolve the limits of biological species within the complex. Although commonly regarded as major pests, we note that there is very little published evidence documenting economic losses caused by flies of the B. dorsalis complex. Quantification of economic losses caused by B. dorsalis complex species is urgently needed to prioritise research for quarantine and management. Although documented invaders, relatively little work has been done on the invasion biology of the complex and this is a further area warranting work. B. DORSALIS COMPLEX OF FRUIT FLIES CONTENTS INTRODUCTION TAXONOMY, SYSTEMATICS AND DIAGNOSTICS Complex diagnosis and taxonomic history Diagnostic tools Non-genetic diagnostic tools Genetic diagnostic tools Evolutionary history ECOLOGY Adult resources and mating systems Larval host range PEST STATUS AND INVASION BIOLOGY Pest status in South-east Asia Invasion biology CONCLUSIONS Systematics and evolutionary history Pest status ACKNOWLEDGEMENTS REFERENCES ….. 3 ….. 6 ….. 6 ….. 8 ….. 8 ….. 9 …..12 …..13 …..14 …..16 …..18 …..18 …..22 …..24 …..24 …..26 …..27 …..28 INTRODUCTION Dacine fruit flies (Diptera: Tephritidae: Dacinae) are one of the key pest groups of Asia and the Pacific (126, 127), with the larval stages being frugivorous on a wide range of fruits and vegetables (3). Direct fruit damage, fruit drop and loss of export markets through quarantine restrictions are all mechanisms by which fruit fly infestation causes economic loss. With adult traits that include high mobility and dispersive powers, high fecundity and, in some species, extreme polyphagy, dacines are well documented invaders and rank high on quarantine target lists. Reviews of the general biology, ecology and pest status of the dacine fruit flies can be found in a variety of sources (13, 18, 35, 91, 132, 136). One decade ago, in a seminal taxonomic revision, Drew and Hancock (26) described 40 new species within the Bactrocera dorsalis complex of tropical fruit flies. Bactrocera dorsalis sensu lato had long been recognised as the most pestiferous, polyphagous and widespread species within a group of morphologically similar, but generally nonpestiferous dacine fruit flies (23, 44). However, the 1994 revision was critical in that B. dorsalis sensu stricto was redescribed and multiple sibling species existing under that name were recognised. Most notable among the newly described species was a small group of pest species, B. papayae Drew & Hancock, B. philippinensis Drew & Hancock and B. carambolae Drew & Hancock. Each of these species has a different geographic and host range to B. dorsalis s. s. While description of the new species was carried out using traditional morphological features (26), their recognition as separate biological units was based on a suite of evidence including allozyme, geographic, host range and pheromonal differences (26, 88, 90). These pest species, along with a number of non-pest species, form a sibling group within the B. dorsalis complex and their discrimination based on morphological criteria alone is extremely difficult. B. DORSALIS COMPLEX OF FRUIT FLIES Incursions of flies of the B. dorsalis complex into Australia, central America, mainland USA and Oceania, with resultant direct and indirect costs running into hundreds of millions of dollars, have kept the complex at the forefront of applied and quarantine research over the last decade. Because of their economic importance, much of the research on the complex has tended to be pragmatic, focusing on diagnostics (2, 50, 60, 78), quarantine (36, 56, 57, 83) and eradication (67, 101, 119, 129). Formal systematics on the complex has been limited, although new species have been described (116), or recognised based on cytogenetic grounds (10, 11). Pest management, behavioural and related work has tended, by its nature, to concentrate on individual species within the complex, with the extensive work on B. dorsalis in Hawaii (eg 105, 119, 120) and in Taiwan (eg 61, 62) being excellent examples. It is not our intent to review here all research undertaken on species belonging to the B. dorsalis complex. Compilations in recent publications (4, 5, 113, 115) offer a lead into much of the dacine literature, which in turn covers much of the B. dorsalis complex. Rather, this review will focus on studies which simultaneously treat multiple species within the complex (eg biogeography, systematics and diagnostics), biological studies which allow cross-species comparisons (eg mating and resource utilization studies) and areas where recognition of the complex in 1994 has significantly impacted on subsequent research aimed at managing the flies (eg invasion biology). We also include a section on the pest status of the complex within South-east Asia, its indigenous range, an issue which has received insufficient attention when trying to interpret the risk posed by the complex as potential invaders. TAXONOMY, SYSTEMATICS AND DIAGNOSTICS The B. dorsalis complex was originally defined to contain 16 species closely related to B. dorsalis (44). Since the early 1980’s a number of additional species have been described, beginning with B. opiliae in 1981 (27). The B. dorsalis species complex was redefined (23) and expanded (26), and now contains 75 described species (Table 1), with undescribed species remaining in collections (60). The complex shows its greatest diversity in the islands of the Indonesian Archipelago. To the east of Wallace’s line the diversity of B. dorsalis complex species rapidly declines such that Australia, with the World’s second most diverse Bactrocera fauna, contains only three endemic B. dorsalis complex species. Similarly the complex becomes rapidly less diverse moving into Asia, with only two species endemic to India. Complex diagnosis and taxonomic history Originally defined by Hardy (44), the B. dorsalis complex was redefined as one of 20 species complexes in the subgenus Bactrocera of the genus Bactrocera (23, 26). A contemporary morphological diagnosis of the complex is as follows: species with a clear wing membrane except for a narrow costal band not reaching R4+5 and a narrow anal streak, costal cells colourless or pale yellow-brown and without dense microtrichia, lateral postsutural vittae present but medial postsutural vittae absent, scutellum mostly yellow with a narrow brown basal band, scutum mostly black, abdominal terga 3-5 with a median longitudinal dark band and variable dark patterns on lateral margins (23, 26). Male flies of the complex are attracted to methyl eugenol or cue lure, plus a significant percentage have no known lure response (Table 1). B. DORSALIS COMPLEX OF FRUIT FLIES Table 1: Bactrocera species currently considered as belonging to the B. dorsalis complex of tropical fruit flies (23, 26, 28, 60, 116). Host Range Family Genera Species Economic Lure Speciesa Locationb B. abdolonginqua (Drew) B. aemula Drew B. affinidorsalis (Hardy) B. arecae (H&A) B. atrifemur D&H B. bimaculata D&H B. cacuminata (Hering) B. carambolae D&H B. caryeae (Kapoor) B. ceylanica T&W B. cibodasae Drew B. cognata (H&A) B. collita D&H B. consectorata Drew B. dapsiles Drew B. diallagma Drew B. dorsalis (Hendel) l l g, m a, i, n, q i g, r a c, f, g, i, n, q, r f, o o g, r m m l l l b, d, e, f, j, k, n,o, p, r m a, l 1 1 6 27 7 1 1 42 1 7 o g a, l m g, j, r j, r o j, m, r l l g g, i g q q, r o i i, r l i g, i, r m j f, i, n, q g l g g 3 1 13 1 1 - B. dorsaloides (H&A) B. endiandrae (Perkins & May) B. fernandoi T&W B. floresiae D&H B. fuliginus (D&H) B. fulvifemur D&H B. fuscitibia D&H B. gombokensis D&H B. hantanae T&W B. holtmanni (Hardy) B. inconstans Drew B. indecora (Drew) B. indonesiae D&H B. infulata D&H B. involuta (Hardy) B. irvingiae D&H B. kanchanaburi D&H B. kandiensis D&H B. kinabalu D&H B. lateritaenia D&H B. laticosta Drew B. latilineola D&H B. lombokensis D&H B. makilingensis D&H B. malaysiensis D&H B. melastomatos D&H B. merapiensis D&H B. mimulus Drew B. minuscula D&H B. muiri (H&A) 2 1 3 1 7 50 8 8 77 10 1 1 1 1 79 124 2 10 3 24 3 2 16 1 3 2 22 1 1 2 * * * ME CUE CUE ME CUE ME ME ME CUE CUE ME CUE ME ME ME ME * CUE ME CUE CUE CUE CUE CUE CUE CUE CUE ME ME ME CUE CUE CUE ME CUE CUE CUE CUE CUE ME ME - B. DORSALIS COMPLEX OF FRUIT FLIES B. neocognata D&H B. neopropinqua D&H B. nigrescens (Drew) B. occipitalis (Bezzi) B. opiliae (Drew & Hardy) B. osbeckiae D&H B. papayae D&H B. paraverbascifoliae Drew B. pedestris (Bezzi) B. penecognata D&H B. philippinensis D&H B. profunda T&W B. propinqua (H&A) B. pyrifoliae D&H B. quasipropinqua D&H B. raiensis D&H B. selenophora T&W B. sembaliensis D&H B. sulawesiae D&H B. sumbawaensis D&H B. syzygii T&W B. thailandica D&H B. trivialis (Drew) B. unimacula D&H B. usitata D&H B. verbascifoliae D&H B. vishnu D&H B. vulgaris (Drew) B. amarambalensis Drewc B. neoarecae Drewc g, i m l c, i, m a q, r a, g, i, l, n, q f g, m g m o d, g, i, n, q, r q, r m q, r o g g g o q, r a, l g, i i, m, n, r f, q, r f a, l f f 3 4 1 51 5 1 5 1 4 1 1 4 1 - 3 4 3 117 3 4 7 209 * * 5 6 * 1 6 2 4 9 7 2 5 1 1 4 1 1 4 1 5 * * CUE ME ME ME ME ME CUE CUE ME CUE CUE CUE CUE ME CUE CUE ME CUE ME CUE CUE ME ME a Authors: H&A =Hardy & Adachi; D&H = Drew & Hancock; T&W = Tsuruta & White b Location only includes countries within each species’ natural range. Country Codes: a, Australia; b, Bhutan; c, Brunei; d, Cambodia; e, China; f, India; g, Indonesia; h, Laos; i , Malaysia; j, Myanmar; k, Nepal; l, Papua New Guinea; m, Philippines; n, Singapore; o, Sri Lanka; p, Taiwan; q, Thailand; r, Vietnam c These species fit the description of the B. dorsalis complex and are morphologically similar to other B. dorsalis complex species, however, they have not officially been placed within the complex (28): in this paper they are not treated as part of the complex. As defined by Drew (23), in addition to B. dorsalis, the complex in 1989contained the following eight species from the Australasian and Oceanian regions: B. abdolonginqua (Drew), B. cacuminata (Hering), B. dapsiles (Drew), B. diallagma (Drew), B. endiandrae (Perkins and May), B. mimulus (Drew), B. nigrescens (Drew), B. opiliae (Drew and Hardy), all responding to methyl eugenol. When the B. dorsalis complex from Asia was revised a few years later (26), the definition of the group was expanded to include eight species from the B. aemula species complex of Drew (23), and numerous new species were described from Asia bringing the total to 68 species in Asia and Oceania. Concurrent with the addition of new species to the complex, a number of species originally included in B. DORSALIS COMPLEX OF FRUIT FLIES the complex by Hardy (44) were removed (B. bryoniae, B. breviaculeus, B. mayi, B. moluccensis, B. rutilus (23); B. limbifera, B. luzonae (26)) as the taxonomic scope of the complex was narrowed. Within the last four years, six new species belonging to the complex have been described from Sri Lanka (116) and one from India (28), bringing the total number of species to 75 (Table 1). Thirty-five species respond to cue lure, 26 species respond to methyl eugenol and 14 species have no known lure response. Identification of species in the complex is complicated because not all species are treated within a single key (26). This complication has been partly overcome with the development of an interactive, computer-based key to 68 species in the complex (60), while a similar key has been produced for the identification of Indo-Australasian dacine fruit flies as a whole (133). However, the six Sri Lankan members of the complex and B. paraverbascifoliae (from India) are still keyed separately (28, 116). Diagnostic tools Uncertainty in species limits based on the traditionally used adult morphological features, together with overlapping host and geographic ranges, impacts significantly on quarantine, pest management and general biological study. Accurate identification is essential for species found in fruit destined for export, for distinguishing exotic from native fauna and for providing crucial data on risk and invasion pathways. Frequently such identifications involve immature life stages, for which there are few morphologically distinguishable characters (132). Given these problems, significant effort has been spent in developing diagnostic tools for species within the complex since 1994. Non-genetic diagnostic tools Species belonging to the B. dorsalis complex are morphologically very similar, with species-specific diagnostic characters found in relatively minor variation in the colour patterns on the wings, thorax, legs and abdominal tergites (60). Large samples of flies, available from surveys using male lure traps or fruit rearing, reveal that many of these diagnostic characters are variable at species level and intermediates that span the morphological space between distinct species are found at non-trivial frequencies. Discriminant analyses using wing morphometrics can reliably distinguish (90% or greater correct) between small subsets of species from Sri Lanka and Thailand (2), although the performance of these diagnostics is likely to be reduced when discrimination is attempted between a larger number of species in the complex. Increasingly the shape and ornamentation of the ovipositor is used as a taxonomic character system for distinguishing species of the complex (23, 26, 27). More recently the length of the male aedeagus has also been used as a diagnostic feature at species level in this group (50, 54). Aedeagal length and length of the female ovipositor are significantly correlated in many Bactrocera species (53, 54, 131), due to the mechanics of mating, and these data provide a useful diagnostic for sympatric pest species of the B. dorsalis complex in Asia (50-52). Cuticular hydrocarbon analysis has also been found useful for distinguishing between two species of the complex from Malaysia (37). Computer-based, multi-access keys (60, 133) have gone a substantial way to resolving the problems of traditional dichotomous keys for flies of the B. dorsalis complex, as they have for many other taxa. Decision paths can be optimised dynamically, allowing the most discriminative character to be used at each step and thus minimising the number of decisions needed to reach an identification. Additionally, variation in character states can be accounted for in key development and can be more completely illustrated. However, B. DORSALIS COMPLEX OF FRUIT FLIES the available keys are still only suitable for identification of adult specimens in good condition. This has driven the exploration of other character systems for more reliable diagnostics, particularly of the larval stages. Genetic diagnostic tools Exploitation of genetic markers has been prompted largely through the frustration of not being able to confidently distinguish, morphologically, between the pest species B dorsalis, B. carambolae, B. papayae and B. philippinensis. Genetic approaches also provide stable characters for the identification of immature life stages and an alternative tool for routine identifications that avoids adding to the strain on expert taxonomists (130). Larval polytene chromosome differences (38) and metaphase karyotypes (10-12) have been used to distinguish Bactrocera species, including B. dorsalis. Electrophoretic data was used initially with limited success to distinguish between five species of the dorsalis complex, with B. dorsalis, B. carambolae and B. papayae lacking any species-specific alleles or loci (134). However, more success in finding species-specific differences has been subsequently reported between these species and B. occipitalis and B. philippinensis (65). Neither karyotyping nor allozyme electrophoresis are suitable for routine diagnostic testing, being compromised by the need for reasonable amounts of good quality tissue and allozyme analyses being vulnerable to differential expression of enzymes at different life stages and under different environmental conditions. DNA markers, however, are not restricted in this way and a number of diagnostic procedures have emerged. The first report of DNA markers used probes from genomic extracts to hybridise to anonymous repetitive DNA of B. dorsalis, B. cucurbitae and Ceratitis capitata (47). As a squash blot method it was proposed to be a simple, rapid and reliable method of distinguishing any life stage of these species and ideal for border quarantine application. However, it would be complicated to use for distinction of any more than a few species and has not been developed further. Polymerase chain reaction (PCR) based technologies offer more flexibility and a number of tests using PCR-RFLP (restriction fragment length polymorphism) analysis have been described for the most pestiferous species. Early methods targeting nuclear ribosomal DNA regions, 18S+ITS1 (8, 9) and ITS1 and ITS2 (68), are still used routinely within quarantine procedures to identify larvae and eggs of tephritids intercepted at the New Zealand and Australian borders, respectively. Both methods can reliably distinguish B. carambolae from B. dorsalis s.s. The latter method (ITS1 and ITS2) uses a more complicated series of primer sets with restriction analyses, but has the added benefit of being able to distinguish B. dorsalis s.s. from B. papayae and B. philippinensis as well as the Australian B. dorsalis complex species, B. opiliae, B. cacuminata and B. endiandrae. Neither of the two approaches can distinguish B. papayae and B. philippinensis. No population-level variation in the restriction patterns for 18S+ITS1 has been observed for morphologically confirmed species (8). Other DNA based methods targeting mitochondrial DNA D-loop+12S (80, 82) and 16S (77, 78, 81) gene regions appear to have greater resolution, such that the species B. dorsalis, B. papayae, B. philippinensis, B. carambolae, B. occipitalis and B. kandiensis, can all be distinguished. This was validated using 83 individuals across 18 Bactrocera species, but, in contrast to the nuclear DNA methods above, population-level variation was observed for four of those species (78). As restriction pattern variation occurs in only some of the 16S sections (I-IV) amplified, incorrect identification can be avoided through B. DORSALIS COMPLEX OF FRUIT FLIES choice of amplicon and restriction enzyme. Of note, however, was a difficulty discriminating between B. papayae and the majority of B. carambolae individuals, although PCR-RFLP of the nuclear ITS region found the haplotype to be specific for B. carambolae (78). Most recently, an original test based on EPIC (exon primed intron crossing)-RFLP of muscle actin to differentiate B. dorsalis s.s. populations (48) has been developed into a microarray-based test that can distinguish B. dorsalis, B. papayae and B. carambolae (79). Allele-specific 50-mer oligonucleotides, designed from the intron sequences of each species, are hybridised to the EPIC PCR product. The detection of heterozygote individuals and intra-specific variation suggest that this is a rapid and reliable means of documenting both the species and population genotype. However, the test is anticipated to be unable to discriminate species where alleles are shared and, as in all the other tests, highlights the need for several loci to be incorporated into any one diagnostic procedure. There is no molecular test to date that is designed to identify each of the nine Asian pest species, with B. caryeae and B. pyrifoliae not included in any studies. A more comprehensive test, comprising more than one gene region and more taxa within the complex, is clearly required. Further development of the oligonucleotide microarray format (79) could go some way towards this. Nonetheless, a reference nucleotide sequence database is essential to underpin this or any other advance in diagnostic capability for the complex. The collation of such data is currently underway to support an internet-based tool for New Zealand quarantine (6) and promises to provide a more flexible means of diagnosis. Evolutionary history Because of their pest and quarantine importance, species-level taxonomic work and diagnostics is relatively well advanced in the B. dorsalis complex, however, few authors have addressed the evolutionary relationships of the group, or addressed to what extent the contemporary classification reflects the phylogeny of the group. None have tackled the B. dorsalis complex per se and there is no phylogeny (either morphological or molecular) for the complex upon which to develop an evolutionary history. Species from the complex have been included in higher taxonomic analyses, sometimes though with B. dorsalis s.s. being the sole representative (17, 40, 41, 66). Studies enabling direct phylogenetic comparison of species within the complex are limited, but where done all have used nucleotide sequence data. An early study of the nuclear genes encoding the 18S rDNA, Cu/Zn superoxide dismutase enzyme and mitochondrial 12S rDNA gene, found those loci too conserved to differentiate B. dorsalis, B. carambolae and B. papayae (130). However, differences between the group and B. (B.) correcta (5% in Cu, Zn superoxide dismutase) and B. (Austrodacus) cucumis (1.5%, 7% and 18% at the respective loci) led to the proposal that the complex had diverged within Bactrocera less than a million years ago. This was consistent with another estimation of 87,000 years since divergence of the complexes B. (B.) dorsalis and B. (Zeugodacus) tau (55). Monophyly of the complex (n=3 to 6 species) within Bactrocera has been supported in analyses using 1,680 bp of the 16S+12S rDNA (77), 1,391 bases and combined trees for 16S, 12S and COII+tRNALys+tRNAAsp (111) and 841 bases from combined trees for 16S and COII+tRNALys+tRNAAsp (110). However, in a study of five Bactrocera subgenera, monophyly of the complex was questioned with B. (B.) musae, from outside the complex, B. DORSALIS COMPLEX OF FRUIT FLIES appearing within the clade (78). Clearly a more comprehensive phylogenetic analysis requires the inclusion of additional nucleotide characters and more taxa. Additional loci to consider may be those already examined in B. dorsalis s.s., such as the introns of muscle actin (48) and EF1-A (99) nuclear genes, plus the mitochondrial COI gene that successfully resolved relationships within the B. (Z.) tau complex and in which B. dorsalis and B. pyrifoliae formed the anticipated clade (55). ECOLOGY Few ecological studies have dealt concurrently with multiple species within the B. dorsalis complex and thus the known ecology of the complex is actually the ecology of a few select species, commonly pests, which have been studied in the context of pest management. Given this limitation, the following section is highly selective in the ecological areas covered and focuses on only two areas where research during the past decade has lead theoretical developments in a wider field (Adult resources and mating systems), or where compilation of species specific research offers insights into studying and management of flies of the B. dorsalis complex (Larval host range). Adult resources & mating systems Dacine fruit flies are anautogenous, i.e. they emerge from puparia as sexually immature adults that need to forage for resources to facilitate survival and reproduction (93). Key resources include moisture for metabolism, sugars to fuel flight, protein to attain sexual maturity and, in conjunction with lipids, for egg production (35). Sugar sources include honeydew and other plant exudates. Protein is derived from sources such as phylloplane bacteria (21, 25) and bird faeces (13, 35), while moisture is derived from dew and rain (70). Adult flies forage for these resources in the environment, although lipids are probably synthesized de novo (97). In addition, adults may also actively seek out certain plantderived phenyl propanoids (e.g. methyl eugenol and raspberry ketone) (72, 73) that are hypothesized to play a role in the mating behaviour of dacine species (33, 34, 84-86, 94, 95, 103, 104, 106, 108, 114). With respect to frequency of mating, female flies are considered monandrous, while male flies are polygynous (93). Within the B. dorsalis complex, mating behaviour of some of the major pest species (85, 103, 104, 106, 108, 114) and one non-pest species (93-96) has received considerable attention. Mating behaviour in dacine fruit flies has been explored from two main perspectives, though both rely on the functional significance of plant-derived chemicals to which dacine flies respond. The most common model of mating systems within those species of the complex studied suggests that mating occurs within a defined spatial arena (“lek” sensu lato) where resources for adult flies are absent (103, 107). Within these arenas sexual selection, driven by female mate choice for males that have fed on plant-derived phenyl propanoids, is hypothesized to operate. The ingested plant chemicals are integrated into the male fly’s sex pheromone (33, 34) and this subsequently makes them more attractive to female flies (8486, 103, 104, 106, 108). The mating behaviour of B. dorsalis s.s. most strongly supports this view of dacine mating behaviour. Male and female B. dorsalis aggregate on the larval host plant at dusk and females appear to choose among males that “call” to them, with males that have had prior exposure to methyl eugenol acquiring more mates than males that have not (106, 107). Contrary observations have been recorded for B. cacuminata, a non-pest species of the complex, where exposure to methyl eugenol appeared to confer no B. DORSALIS COMPLEX OF FRUIT FLIES advantage in mate acquisition (94). This suggests that the physiological usage of plant derived chemicals may vary between species. A second model of mating behavior observed for species within the complex hypothesizes that plant derived phenyl propanoids serve as a mate rendezvous stimulus that both male and female flies respond to for mate location (73). This hypothesis has been considered unlikely in the past, as these chemicals have not been found to be common among larval host plant species to which mating was thought to be restricted (33, 34, 106). However, unmated female flies are known to respond to lures (1, 34, 95), and with evidence indicating that mating need not be restricted to the larval host plant (95), direct experimentation has shown that natural phenyl propanoids, such as methyl eugenol, can serve as mate aggregation stimuli when resources are spatially separated (1, 34, 95). Research on mating systems for species within the B. dorsalis complex is still in its infancy, with the two most studied cases (B. dorsalis s.s. and B. cacuminata) giving quite different insights. Because species within the complex are thought to be quite recently evolved, with a high degree of genetic relatedness, the complex offers an ideal model system to study rapid speciation and the role of mate recognition, larval host plant use and the availability of other environmental resources in limiting gene pools. Such research will not only enable us to better understand the ecology and evolution of dacine fruit flies, but may also aid in the development of sustainable management strategies, relying on mating disruption, for the pest species within the complex. Larval host range Understanding larval host range in the complex is hampered by the fact that larval rearing records are known for only 28 species (38% of the complex): where records are known they are to be found in a variety of sources (3, 23, 26, 42, 117), but have been collated (60). Of those species with rearing records, six have only one known larval host (Table 1) and it is unclear if this is because they are truly monophagous, or simply under-sampled. Where two or more larval hosts have been recorded for a fly, only three species are restricted to a single plant genus (B. melastomatos on two species of Melastoma; B. propinqua on nine species of Garcinia; B verbascifoliae on five species of Solanum) and can be regarded as narrowly oligophagous. In contrast, the more general pattern of larval host use by flies of the complex appears to be multiple plant species across genera and families (Table 1). The key plant families containing B. dorsalis complex hosts include the Anacardiaceae, Annonaceae, Clusiaceae, Lauraceae, Moraceae, Myrtaceae, Rutaceae, Sapotaceae and Solanaceae, each with 15 or more known fruit fly host species. Excluding the three highly polyphagous species within the complex (see next paragraph), less than 5% of host plants (16/369) are shared by two or more fly species. Psidium guajava (common guava, exotic to South-east Asia) is the host most utilised by flies of the B. dorsalis complex, with eight species having been being reared (B. carambolae, B. caryeae, B. dorsalis, B. kandiensis, B. occipitalis, B. papayae, B. pyrifoliae, B. trivialis). It should be noted, however, that guava is an exceptionally common fruit fly host plant, being a known host for at least 20 Bactrocera species (3, 42). The host range for the majority of species for which larval hosts are not known can only be guessed. It is probably safe to assume that they are non-commercial, wild fruits, but whether the flies are monophagous or oligophagous is not known. Three species within the complex are known for their extreme polyphagy: B. papayae with 209 recorded larval hosts across 51 plant families; B. dorsalis, 124 host species across 42 B. DORSALIS COMPLEX OF FRUIT FLIES families; and B. carambolae, 77 host species across 27 families (Table 1). Detailed examination of host use by these species is in its infancy, but what is available strongly suggests that while large numbers of different host species may be utilised, not all are utilised equally. In laboratory trials, with limited numbers of hosts, host suitability (as assessed by oviposition preference, larval development times and survival rates) varied across hosts from different plant families (20, 59, 124) and within a family (98). From field collections, the yield of flies from fruits is rarely proportional to the presence of different fruit species within samples. For example, Terminalia catappa (Pacific almond) reared 2-5 times more B. dorsalis and B. papayae in samples from Thailand than would have been expected based on the number or weight of T. catappa fruit in overall samples (19). In stark contrast, no B. papayae were reared from rainforest fruit samples in far North Queensland during the incursion in the mid-1990’s, despite plant species recorded as hosts from South-east Asia being present (39), nor were any reared from fruit samples collected in tropical lowland rainforest of Papua New Guinea (87). Such results strongly imply that simple host lists (3) are not sufficient in themselves for identifying biological host range in these polyphagous species. PEST STATUS AND INVASION BIOLOGY A common perception among applied entomologists and quarantine biologists is that the B. dorsalis complex is a major pest group, arguably one of the most important pest species complexes in world agriculture. Two core assumptions underlie this accepted pest ranking: (i) the extreme polyphagy and hence assumed pest status of species within the complex; and (ii) the known invasiveness of at least some species within the complex. For quarantine and trade, particularly, the perception of risk posed by the complex is very large and the presence or absence of species within a country or region can have dramatic effects. It has been estimated that the mid-1990’s incursion of B. papayae into north Queensland caused losses of nearly Aus$100mill, most of this due to lost export markets (24). Because much of the real pest status of the B. dorsalis complex actually stems from these indirect trade losses, two areas crucial to understanding this issue are reviewed below. The first of these is the pest status of the complex in its native range, i.e. Southeast Asia, as an incomplete understanding of an organism’s pest status in its endemic range will confound any understanding of its potential pest status in a newly invaded region. The second area reviewed is the invasion biology of the complex: those factors which may influence invasiveness and current research methodology to understand this issue. Pest Status in South-east Asia The South-east Asian region comprises Brunei, Cambodia, Indonesia, Laos, Malaysia, Myanmar, the Philippines, Singapore, Thailand and Vietnam. This region lies at the center of distribution of the B. dorsalis complex, with 51 of the 75 species being found there (Table 1). South-east Asia is also a center for tropical fruit production, with approximately 400 edible tropical fruit and nut species being grown (122). Fruits are commonly grown for local consumption and domestic markets, however, several countries supply export markets with a diverse range of fresh tropical and temperate fruits. Given the coincidence of substantial fruit-growing areas with the geographic ranges of numerous frugivorous B. dorsalis complex species, it is not surprising that several of these fly species are fruit pests in the region. B. DORSALIS COMPLEX OF FRUIT FLIES Based on FAOSTAT production and export statistics (32), 28 fresh fruit commodities are of major economic importance to South-east Asia. Using South-east Asian literature to expand the FAOSTAT commodity categories, which combine many fruit species, lengthens the list to 42 economic fruit types (Table 2). Of the 51 B. dorsalis complex species present in South-east Asia, nine, viz B. carambolae, B. dorsalis, B. irvingiae, B. occipitalis, B. papayae, B. philippinensis, B. pyrifoliae, B. raiensis and B. trivialis, have been reared from fruits of 27 of these commercial fruits (Table 2). Table 2: Fruits of economic importance to South-east Asia and the members of the Bactrocera dorsalis complex that infest them. Fruit species (common name)a Countries in which crop is economically importantb Fly species recorded to infest fruit in SE Asiacd Abelmoschus esculentus (okra) Actinidia chinensis (kiwi fruit) Ananas comosus (pineapple) Annona spp. (custard apple) Artocarpus altilis (breadfruit) Artocarpus heterophyllus (jackfruit) Averrhoa carambola (carambola) Capsicum spp. (chillie) Carica papaya (papaya) Chrysophyllum spp. (star apple) Citrullus lanatus (watermelon) Citrus spp. (orange, lemon, lime, etc) Cucumis melo (cantaloupe) Cucumis sativus (cucumber) Cucurbita spp. (pumpkin, gourd) Dimocarpus longan (longan) Durio zibethinus (durian) Ficus carica (fig) Fragaria spp. (strawberry) Garcinia mangostana (mangosteen) Litchi chinensis (litchi) Lycopersicon esculentum (tomato) Malus domestica (apple) Mangifera indica (mango) Manilkara zapota (sapodilla) Musa spp. (banana and plantain) Nephelium lappaceum (rambutan) Passiflora edulis (passion fruit) Persea americana (avocado) Phoenix dactylifera (date) Pouteria sapota (sapote) Prunus armeniaca (apricot) Prunus avium (cherry) Prunus domestica (plum) Prunus persica (peaches, i i, n c, d, g, h, i, m, n, q, r m, q i i, m, q, r car, dor, pap car, dor, pap, phi, rai car, dor, irv, pap i g, m, n, q g, i, m, n, q, r m, r g, i, m, n, q, r c, d, g, h, i, m, n, q, r car, dor, pap car, dor, pap, tri dor, pap, phi car, dor, pap car, dor, occ, pap, tri g, h, i, m, n, q g, i, m, n, q g, i, m, q q, r g, i, m, q, r g g, i, n, q g, i, m, q, r dor dor, pap dor car, pap q, r g, i, m, n, q g, i, m, n, q g, h, i, m, n, q, r i, m, q c, d, g, h, i, j, m, n, q, r g, i, m, q, r i g, i, m, n, q g, i, n r g, n g, i, n i, n, q i, n dor car, pap dor car, dor, occ, pap, phi car, dor, pap dor, pap dor, pap pap car, dor, pap pap dor dor dor, pap, pyr, tri B. DORSALIS COMPLEX OF FRUIT FLIES nectarine) Prunus spp. – species not specified Psidium guajava (guava) Pyrus communis (pear) Rubus idaeus (raspberry) Solanum melongena (aubergine) Tamarindus indica (tamarind) Vitis vinifera (grape) h i, m, q, r g, i, n, q m g, i, m, q m, r g, i, m, n, q, r car, dor, occ, pap, pyr, tri pap - a Plant nomenclature follows (58). Country abbreviations as in Table 1. c Bactrocera dorsalis complex species infesting South-east Asian fruit derived from (60). car – B. carambolae; dor – B. dorsalis; irv – B. irvingiae; occ – B. occipitalis; pap – B. papayae; phi – B. philippinensis; pyr - B. pyrifoliae; rai - B. raiensis; tri – B. trivialis. d Note that columns two and three are independent. They are not meant to imply that for a particular fruit, every fly species listed as attacking that fruit does so in every listed country. For example, B. philippinensis attacks papaya in the Philippines, but not in other countries because it is absent from those countries (see Table 1 for country records). b The extent to which each B. dorsalis complex species affects fruit production and agricultural economics in the South-east Asian region is vital information for setting research priorities for these species. Several South-east Asian species within the B. dorsalis complex have been accorded status as pests ranging from “significant” (B. occipitalis), through “serious” (B. pyrifoliae) and “major” (B. carambolae, B. dorsalis), to the “most destructive of all dorsalis complex species” (B. papayae) (29). Similar terms have been used by others to describe the pest importance of B. dorsalis complex species (132). The justification for using these descriptors is seldom explicitly stated in the literature. Nevertheless, three ecological criteria, i.e., the range of host fruit species, especially that of economically important hosts, geographic distribution, and fruit infestation rates, seem important in the literature for defining a fly species importance as a pest. A fourth criterion for establishing pest status, their economic effects, is rarely addressed in the literature. Each of these criteria will be discussed here in relation to the nine pest species in the B. dorsalis complex that infest South-east Asian commercial fruit. The known distributions of the nine B. dorsalis complex pest species vary tremendously, both in terms of the commercial fruits they infest (Table 2) and of the countries in which they are found (Table 1). Bactrocera dorsalis and B. papayae have the greatest host ranges, with each having been found infesting, respectively, fruits of 21 and 22 of the 41 commercially-important crops in South-east Asia. Bactrocera carambolae also infests fruits from many plant species, having been recorded from 13 commercial fruits. The remaining six potentially pestiferous B. dorsalis complex species, B. irvingiae, B. occipitalis, B. philippinensis, B. pyrifoliae, B. raiensis and B. trivialis, have each been recorded from fruits of fewer than five economically-important crops. Bactrocera occipitalis, B. philippinensis, B. pyrifoliae and B. trivialis are all considered to need more extensive fruit surveys to establish their pest status (29). The addition of commercial fruits to the host fruit ranges of B. irvingiae (jackfruit and santol) and B. raiensis (breadfruit) (60), since these flies were described (26) highlights the need for further host fruit surveys. Bactrocera carambolae, B. dorsalis and B. papayae, the three members of the B. dorsalis complex with the greatest commercial host fruit ranges, also have the widest distributions, B. DORSALIS COMPLEX OF FRUIT FLIES with each having been recorded in four or more of the 10 South-east Asian countries. Each of the other six B. dorsalis complex pest species occurs in three or fewer countries. Bactrocera carambolae has been found in Vietnam and B. occipitalis in Brunei (60) since their first descriptions (26). The distributions of the nine B. dorsalis complex pest species will undoubtedly increase as more surveys are done throughout the region. Fruit infestation rates are of vital importance for determining the pest status of fruit flies. Generally, just one larva in a fruit is enough for rejection by a consumer (or by quarantine in an export destination country). The level of infestation determines the quantity of produce that can be sold and, therefore, the economic returns to farmers. Despite the importance of knowing infestation rates, virtually no literature is available concerning B. dorsalis complex species in South-east Asian fruit crops. Literature concerned with infestation from areas outside the region, where B. dorsalis complex species have been introduced (B. carambolae in Surinam and B. dorsalis s.s. in Hawaii), is therefore presented (Table 3). Infestation rates for both B. carambolae and B. dorsalis show a similar pattern, i.e., that infestation rates are markedly higher in some fruit species than in others. Thus, more than 40% of carambola fruit samples in Surinam were found infested with B. carambolae, whereas only 1.2% of sweet orange samples were infested by this fly, with a wide range of infestation rates in between (Table 3). Similar infestation patterns were found for B. dorsalis in Hawaii where a maximum 55% of papaya fruits were infested, compared with 0.026% for rambutan. Although infestation rates are of major importance for determining pest status, they may fluctuate considerably within the same fruit species with season and geographical location (7). Methods which take such fluctuations into account need to be developed so as to enable comparisons of infestation rates among fruit species. The final criterion for determining pest status of B. dorsalis complex species is their economic effects, e.g., losses or control costs associated with infestation. Some basic economic analyses have been conducted (123). However, these were concerned with tephritid fruit flies in general rather than individual fly species and do not ascertain the economic impact of one fly species relative to others. There is a clear need for speciesspecific economic analyses. Although some B. dorsalis complex species have been accorded status as “serious“ or “major” pests in South-east Asia, very little evidence has been published that supports these descriptors being placed on them. The efficient development of research effort towards the management of pest species of the B. dorsalis complex can only be done when such information becomes available. Invasion Biology Species within the B. dorsalis complex vary widely in the extent of their geographical range (26). Most species are very restricted (e.g., 50 of 75 species are recorded from only 1 country, Table 1), with relatively few species more widely distributed (e.g., only 5 of 75 are found in 5 or more countries). Only a few species, including B. dorsalis, B. carambolae, B. philippinensis and B. papayae, are actively expanding their range (15, 67, 109) and are by definition, invasive: these species are also characterized by a relatively broad host range and all are economically important. Explaining the ability of such species to invade new regions, and the consequences of these invasions, represent active areas of research and many of the scientific tools used to study biological invasions have B. DORSALIS COMPLEX OF FRUIT FLIES Table 3: Maximum infestation rates for B. carambolae and B. dorsalis in fruits of economic importance to the South-east Asian region. Data were not available from Southeast Asia and so infestation rates from other regions of the world, where the flies have been introduced, were used. – – – "# " ! Fruit % infested fruit samples * ,, 3 ' 1 2 , 1 , & 3 ' " % .%! % %" %. % #%. %! Fruit + , 0 + ,, % infested fruit (reference) #"% . % ! Fruit / 1 4 3 1 3 / ' 2 ' 2 ' ' $ %& ' ' ( )' & & "!% % %! #% ! % %. % 4 * ,, + , + & + ,, / originated through case studies of tephritid flies, including Bactrocera species. The impetus for this research stems largely from active programs to develop molecular genetic methods for diagnostics, particularly in Australia (125, 135), New Zealand (9), the US (71), and elsewhere (67, 75). Compared to our understanding of the invasion biology of Ceratitis capitata, the Mediterranean fruit fly (71) and B. tryoni, the Queensland fruit fly (112, 135), relatively little is known about species in the B. dorsalis complex. However, as with these other invasive tephritids, global and regional transport of fruit and vegetable products results in constant propagule pressure by species such as B. dorsalis (92). Fly interceptions at airports and other points of entry bear this out, but also demonstrate that actual colonization and establishment is less frequent than immigration (16). This conclusion is complicated, however, by the fact that recently established populations may persist below detection levels for some time. An important question for pest management, critical for assessing whether populations can be completely eradicated or merely controlled, is whether fruit fly populations represent transient outbreaks or have become established. To address this question, research on the historical demography of invasive fruit fly populations has prompted the development of novel approaches to determine population origins and structure, including statistical assignment tests (22) and resampling statistics based on heterozygosity and shared alleles (112). Using these approaches, studies of C. B. DORSALIS COMPLEX OF FRUIT FLIES capitata, B. tryoni and other Bactrocera species, show that population histories are typically not simple, with established populations comprising both ancestral and invading lineages (76). For estimation of other population parameters, such as invading population size and current gene flow, new Monte-Carlo approaches show much promise (14, 31). The impacts of invasions of Bactrocera species on other arthropods have been little studied with the noted exception of the interaction between B. dorsalis and previously established C. capitata in the Hawaiian Islands. Because of the disappearance of medfly in low elevation areas following introduction of B. dorsalis, it had been assumed that B. dorsalis would displace C. capitata elsewhere in the Hawaiian Islands and eradication strategies were developed based on this reasoning (121). However, more recent experimental work has shown that in higher elevation coffee plantations, C. capitata prevails as a result of a very different life history: C. capitata is more of an “r-selected” species, being smaller and capable of rapid colonization of newly planted coffee, while B. dorsalis is more of a “K-selected” species, being larger with a later onset of reproduction (120). However, the situation can be more complicated: for example, under certain conditions both species may lose in competition to another fly, B. latifrons (64). There is also evidence that parasitoids introduced for biological control may influence the competitive outcome between pest fly species and may also impact indigenous fly species (30, 49). The direct impacts of Bactrocera species on indigenous arthropod species have not been well studied (39, 87). A number of factors suggest that much will be learned about the invasion biology of the B. dorsalis group in the near future. In particular, a wealth of genetic tools is now available, active quarantine programs exist world-wide, and the infrastructure to share data concerning invasive species is rapidly growing. It is also likely that new molecular tools based on genetic modification will permit tracking of genetically marked individuals and provide alternative, albeit controversial, methods of control (43, 100). CONCLUSIONS Systematics and evolutionary history A common question which has circulated in the fruit fly community since 1994 has been: “did Dick Drew and Dave Hancock get it right when they split B. dorsalis into so many new species?” Accumulated evidence now suggests that in most cases they did. Combining cytological, allozyme and nucleotide data, there is generally support for separation of even the most closely related species within the group. However, some species, such as B. carambolae and B. papayae require molecular tools of extremely high precision for accurate diagnosis. How these slight differences relate to species concepts has not been addressed. For example, is the level of interspecific genetic difference detected between B. carambolae and B. papayae greater or lesser than intraspecific differences between populations of other species within the complex. Evidence to date suggests that the B. dorsalis complex represents an extremely rapidly evolving species complex and that much of the species diversity we currently see has been generated in very recent evolutionary time (last 1-2 million years). As such the complex represents a good example of a phytophagous insect evolutionary radiation. Contrary to a number of other phytophagous arthropod radiations, we do not in this example have B. DORSALIS COMPLEX OF FRUIT FLIES evidence of a tightly coevolving arthropod/host-plant system. Rather, the radiation has probably been driven by a complicated mixture of host shifting and host range expansion, all happening within the context of an extremely diverse rainforest plant community and a fast evolving South-east Asian geological mosaic of islands and accreted terranes (74). Because of their diversity and likely evolutionary histories, these flies offer a remarkably tractable system for testing the validity of different species concepts and speciation mechanisms. For the B. dorsalis complex to become useful as a model system for wider evolutionaryecology questions, development of a phylogeny for the group is critical. Phylogenetic work for the complex is in its infancy, currently relying on few morphological characters, short pieces of mitochondrial DNA and small taxon samples. That current taxonomic treatments are geographically limited (e.g. Australia/PNG, Asia, Sri Lanka) has also hindered an overall systematic understanding of the group. A complete phylogeny is urgently needed, developed from a combination of molecular and morphological data, in order to help resolve species limits and their relationship to each other. Hybridization, which has been reported or suspected between species within the complex (81, 128), needs to be studied further to determine if it is a rare event, with little impact on the integrity of species’ gene pools, or if it is common in which case species limits would need to be redefined. The unresolved issue of hybridization is a reflection that little or no effort has yet been made to establish the extent to which morphologically defined species within the complex reflect biological species. Studies of mating systems within the complex, which may help to resolve this issue, are still limited and, with respect to phytochemicals, give conflicting results. Studies of the mate recognition systems (89) of B. dorsalis complex flies are needed to help understand the functional cues by which individuals recognise potential mates and so set the limits to gene pools in the complex. Pest status The real pest status of flies within the B. dorsalis complex remains ambiguous. There is no doubt that in particular localities, and on selected crops, that complex species such as B. dorsalis, B. papayae and others cause major loss. There is also no ambiguity about the fact that the presence of even one of the pest species from the complex in a country or region can dramatically impact on freedom of market access. What is less well documented, in an economic sense, is exactly how pestiferous are even the best known and widespread of the B. dorsalis complex species. Exactly how economically damaging are species such as B. philippinensis and B. occipitalis, both in comparison to other flies within the complex, other dacine fruit flies, and other pests within the cropping system, has not been determined. If such information does exist, as we suspect it does for at least some localities, then it needs to be much more widely distributed in the standard literature, as such information is vital for directing research efforts for tackling the fruit fly problem. ACKNOWLEDGEMENTS In this review the following authors have taken lead responsibility for particular sections and are the best first contact for further discussion of those sections: ARC, overall coordination, ecology and larval host range; KA, molecular diagnostics and evolution; AC, morphological diagnostics; JM, pest status; SR, adult resources and mating behavior; GR, invasion biology; DKY, systematics. B. DORSALIS COMPLEX OF FRUIT FLIES REFERENCES 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. Abraham V, Verghese A. 1998. Methyl eugenol attracts female mango fruit fly, Bactrocera dorsalis Hendel. Insect Env. 4: 101 Adsavakulchai A, Baimai V, Prachyabrued W, Grote PJ, Lertlum S. 1999. Morphometric study for identification of the Bactrocera dorsalis complex (Diptera: Tephritidae) using wing image analysis. Biotropica 13: 3748 Allwood AJ, Chinajariyawong A, Drew RAI, Hamacek EL, Hancock DL, et al. 1999. Host plant records for fruit flies (Diptera: Tephritidae) in South East Asia. Raffles Bull. Zool. Supplement No. 7: 1-92 Allwood AJ, Drew RAI, eds. 1997. Management of Fruit Flies in the Pacific. Canberra: ACIAR Proc. No. 76. 267 pp. Aluja M, Norrbom AL, eds. 2000. Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton: CRC Press Appleton C. 2003. Bio-Identifier: DNA diagnostics for organisms intercepted at the border. Biosecurity 48: 13 Armstrong JW. 1983. Infestation biology of three fruit fly (Diptera: Tephritidae) species on 'Brazilian', 'Valery', and William's' cultivars of banana in Hawaii. J. Econ. Entomol. 76: 539 43 Armstrong KF, Cameron CM. 2000. Species identification of Tephritids across a broad taxonomic range. In Area-wide Control of Fruit Flies and other Insect Pests, ed. KH Tan, pp. 70310. Penang, Malaysia: CABI Publishing Armstrong KF, Cameron CM, Frampton ER. 1997. Fruit fly (Diptera: Tephritidae) species identification: a rapid molecular diagnostic technique for quarantine application. Bull. Entomol. Res. 87: 111-8 Baimai V, Phinchongsakuldit J, Tigvattananont S. 1999. Metaphase karyotypes of fruit flies of Thailand. IV. Evidence for six new species of the Bactrocera dorsalis complex. Cytologia 64: 371-7 Baimai V, Sumrandee C, Tigvattananont S, Trinachartvanit W. 2000. Metaphase karyotypes of fruit flies of Thailand. V. Cytotaxonomy of ten additional new species of the Bactrocera dorsalis complex. Cytologia 65: 409-17 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. Baimai V, Trinachartvanit W, Tigvattananont S, Grote PJ, Poramarcom R, Kijchalao U. 1995. Metaphase karyotypes of fruit flies of Thailand. I. Five sibling species of the Bactrocera dorsalis complex. Genome 38: 1015-22 Bateman MA. 1972. The ecology of fruit flies. Annu. Rev. Entomol. 17: 493-518 Bohonak AJ, Davies N, Villablanca FX, Roderick GK. 2001. Invasion genetics of New World medflies: testing alternative colonization scenarios. Biol. Invasions 3: 103-11 Cantrell B, Chadwick B, Cahill A. 2001. Fruit Fly Fighters: Eradication of the Papaya Fruit Fly. Collingwood, Vic: CSIRO Publishing Carey JR. 1991. Establishment of the Mediterranean fruit fly in California. Science 253: 1369-73 Chang HY, Tzeng CC, Tsai WH, Kao SS, Tseng YH. 2003. Phylogenetic study of the Dacinae (Diptera: Tephritidae) using partial sequences of mitochondrial 16S ribosomal DNA. Plant Protection Bull. Taipei 45: 1-15 Christenson LD, Foote RH. 1960. The biology of fruit flies. Annu. Rev. Entomol. 5: 171-92 Clarke AR, Allwood A, Chinajariyawong A, Drew RAI, Hengsawad C, et al. 2001. Seasonal abundance and host use patterns of seven Bactrocera Macquart species (Diptera: Tephritidae) in Thailand and Peninsular Malaysia. Raffles Bull. Zool. 49: 207-20 Cornelius ML, Duan JJ, Messing RH. 2000. Volatile host fruit odors as attractants for the oriental fruit fly (Diptera: Tephritidae). J. Econ. Entomol. 93: 93-100 Courtice AC, Drew RAI. 1984. Bacterial regulation of abundance in tropical fruit flies (Diptera: Tephritidae). Aust. Zool. 21: 251-68 Davies N, Villablanca FX, Roderick GK. 1999. Determining the sources of individuals in recently founded populations: multilocus genotyping in non-equilibrium genetics. Trends Ecol. Evol. 14: 17-21 Drew RAI. 1989. The tropical fruit flies (Diptera: Tephritidae: Dacinae) of the Australasian and Oceanian regions. Mem. Qld. Mus. 26: 1-521 Drew RAI. 1997. The economic and social impact of the Bactrocera papayae Drew and Hancock (Asian Papaya fruit B. DORSALIS COMPLEX OF FRUIT FLIES 25. 26. 27. 28. 29. 30. 31. 32. 33. 34. 35. 36. fly) outbreak in Australia. In Management of Fruit Flies in the Pacific. ACIAR Proceedings No. 76, ed. A Allwood, R Drew, pp. 205-7. Canberra: ACIAR Drew RAI, Courtice AC, Teakle DS. 1983. Bacteria as a natural source of food for adult fruit flies. Oecologia 60: 267-72 Drew RAI, Hancock DL. 1994. The Bactrocera dorsalis complex of fruit flies (Diptera: Tephritidae: Dacinae) in Asia. Bull. Entomol. Res. Suppl. No 2: iiii + 1-68 Drew RAI, Hardy DE. 1981. Dacus (Bactrocera) opiliae, a new sibling species of the dorsalis complex of fruit flies from northern Australia (Diptera: Tephritidae). J. Aust. Entomol. Soc. 20: 131-7 Drew RAI, Raghu S. 2002. The fruit fly fauna (Diptera: Tephritidae: Dacinae) of the rainforest habitat of the Western Ghats, India. Raffles Bull. Zool. 50: 32752 Drew RAI, Romig MC. 1997. Overview - Tephritidae in the Pacific and Southeast Asia. In Management of Fruit flies in the Pacific. ACIAR Proceedings No. 76, ed. A Allwood, RAI Drew, pp. 46-53. Canberra: ACIAR Duan JJ, Purcell MF, Messing H. 1996. Parasitoids of non-target tephritid flies in Hawaii: Implications for biological control of fruit fly pests. Entomophaga 41: 245-56 Estoup A, Beaumont M, Sennedot F, Moritz C, Cornuet JM. in press. Genetic analysis of complex demographic scenarios: the case of spatially expanding populations in cane toad, Bufo marinus. Evolution FAO. 1990-2002. FAOSTAT. http://apps.fao.org Fitt GP. 1981. The influence of age, nutrition and time of day on the responsiveness of male Dacus opiliae to the synthetic lure, methyl eugenol. Entomol. Exp. Applic. 30: 83-90 Fitt GP. 1981. Responses by female Dacinae to "male" lures and their relationship to patterns of mating behavior and pheromone response. Entomol. Exp. Applic. 29: 87-97 Fletcher BS. 1987. The biology of dacine fruit flies. Annu. Rev. Entomol. 32: 115-44 Follett PA, McQuate GT. 2001. Accelerated development of quarantine 37. 38. 39. 40. 41. 42. 43. 44. 45. 46. treatments for insects on poor hosts. J. Econ. Entomol. 94: 1005-11 Goh SH, Ooi KE, Chuah CH, Yong HS, Khoo SG, Ong SH. 1993. Cuticular hydrocarbons from two species of Malaysian Bactrocera fruit flies. Biochemical Systematics and Ecology 21: 215-26 Grewal JS, Kapoor VC. 1986. Morphotaxonomy and cytotaxonomy of larval stages of some Dacus spp. (Diptera: Tephritidae). Ann. Biol. (Ludhiana) 2: 58-66 Hadwen WL, Small A, Kitching RL, Drew RAI. 1998. Potential suitability of North Queensland rainforest sites as habitat for the Asian papaya fruit fly, Bactrocera papayae Drew and Hancock (Diptera: Tephritiade). Aust. J. Entomol. 37: 219-27 Han H-Y, McPheron BA. 1994. Phylogenetic study of selected tephritid flies (Insecta: Diptera: Tephritidae) using partial sequences of the nuclear 18S ribosomal DNA. Biochem. System. Ecol. 22: 447-57 Han H-Y, McPheron BA. 1997. Molecular phylogenetic study of Tephritidae (Insecta: Diptera) using partial sequences of the mitochondrial 16S ribosomal DNA. Mol. Phylogen. Evol. 7: 17-32 Hancock DL, Hamacek EL, Lloyd AC, Elson-Harris MM. 2000. The Distribution and Host Plants of Fruit Flies (Diptera: Tephritidae) in Australia. Brisbane: Department of Primary Industries, Queensland Handler AM, Beeman RW. 2003. United States Department of Agriculture Agricultural Research Service: advances in the molecular genetic analysis of insects and their application to pest management. Pest Manage. Sc. 59: 72835 Hardy DE. 1969. Taxonomy and distribution of the Oriental fruit fly and related species (Tephritidae-Diptera). Proc. Hawaiian Entomol. Soc. 20: 395428 Harris EJ, Lee CYL. 1987. Seasonal and annual distribution of the Mediterranean fruit fly (Diptera: Tephritidae) in Honolulu and suburban areas of Oahu, Hawaii. Environ. Entomol. 16: 1273-82 Harris EJ, Vargas RI, Gilmore JE. 1993. Seasonality in occurrence and distribution of Mediterranean fruit fly (Diptera: Tephritidae) in upland and B. DORSALIS COMPLEX OF FRUIT FLIES 47. 48. 49. 50. 51. 52. 53. 54. 55. lowland areas on Kauai, Hawaii. Environ. Entomol. 22: 404-10 Haymer DS, Tanaka T, Teramae C. 1994. DNA probes can be used to discriminate between tephritid species at all stages of the life cycle (Diptera: Tephritidae). J. Econ. Entomol. 87: 7416 He M, Haymer DS. 1997. Polymorphic intron sequences detected within and between populations of the oriental fruit fly (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 90: 825-31 Headrick DH, Goeden RD. 1996. Issues concerning the eradication or establishment and biological control of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), in California. Biol. Control 6: 412-21 Iwahashi O. 1999. Distinguishing between the two sympatric species Bactrocera carambolae and B. papayae (Diptera: Tephritidae) based on aedeagal length. Ann. Entomol. Soc. Am. 92: 63943 Iwahashi O. 1999. Distinguishing between two sympatric species Bactrocera occipitalis and B. philippinensis (Diptera: Tephritidae), based on aedeagal length. Ann. Entomol. Soc. Am. 92: 182-7 Iwahashi O. 2001. Aedeagal length of the Oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), and its sympatric species in Thailand and the evolution of a longer and shorter aedeagus in the parapatric species of B. dorsalis. Appl. Entomol. Zool. 36: 28997 Iwahashi O, Tan KH. 2000. Speciation of Bactrocera dorsalis complex based on aedeagus length. In Area-wide Control of Fruit Flies and other Insect Pests, ed. KH Tan, pp. 591-4. Penang, Malaysia: CABI Publishing Iwaizumi R, Kaneda M, Iwahashi O. 1997. Correlation of length of terminalia of males and females among nine species of Bactrocera (Diptera, Tephritidae) and differences among sympatric species of B. dorsalis complex. Ann. Entomol. Soc. Am. 90: 664-6 Jamnongluk W, Baimai V, Kittayapong P. 2003. Molecular phylogeny of tephritid fruit flies in the Bactrocera tau complex using the mitochondrial COI sequences. Genome 46: 112-8 56. 57. 58. 59. 60. 61. 62. 63. 64. 65. Jang EB. 1996. Systems approach to quarantine security: Postharvest application of sequential mortality in the Hawaiian grown 'Sharwil' avocado system. J. Econ. Entomol. 89: 950-6 Jang EB. 1996. Systems approach to quarantine security: Postharvest application of sequential mortality in the Hawaiian grown 'Sharwil' avocado system. Journal of Economic Entomology 89: 950-6 Jansen PCM, Lemmens RHMJ, Oyen LPA, Siemonsma JS, Stavast FM, van Valkenburg JLCH. 1993. Plant Resources of South-East Asia. Basic List of Species and Commodity Grouping. Final Version. Bogor, Indonesia: PROSEA Foundation Khan M, Shahjahan RM, Wadud MA. 2000. Evaluation of different hosts for laboratory rearing of oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Bangladesh J. Zool. 28: 41-7 Lawson AE, McGuire DJ, Yeates DK, Drew RAI, Clarke AR. 2003. Dorsalis: An interactive identification tool to fruit flies of the Bactrocera dorsalis complex. CD-ROM publication, Griffith University, Brisbane, Australia. Lee WY, Chang JC, Lin TL, Hwang YB. 1995. Ultrastructure of the antennal sensilla of the Oriental Fruit fly Bactrocera (= Dacus) dorsalis (Hendel) (Diptera: Tephritidae). Zool. Studies 34: 21-8 Lee WY, Chen ME, Lin TL. 1998. Morphology and ultrastructure of the alimentary canal of Oriental fruit fly Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) (I): The structure of the foregut and cardia. Zool. Studies 37: 95101 Liquido NJ, Cunningham RT, Couey HM. 1989. Infestation rates of papaya by fruit flies (Diptera: Tephritidae) in relation to the degree of fruit ripeness. J. Econ. Entomol. 82: 213-9 Liquido NJ, Harris EJ, Dekker LA. 1994. Ecology of Bactrocera latifrons (Diptera, Tephritidae) populations - Host plants, natural enemies, distribution, and abundance. Ann. Entomol. Soc. Am. 87: 71-84 Mahmood K. 1999. Verification of specific status of pest species allied to Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) using allozyme electrophoresis. Pakistan J. Zool. 31: 159-65 B. DORSALIS COMPLEX OF FRUIT FLIES 66. 67. 68. 69. 70. 71. 72. 73. 74. 75. 76. 77. Malacrida AR, Guglielmino CR, D' Adamo P, Torti C, Marinoni F, Gasperi G. 1996. Allozyme divergence and phylogenetic relationships among species of tephritid flies. Heredity 76: 592-602 Malavasi A, Sauers Muller Av, Midgarden D, Kellman V, Didelot D, et al. 2000. Regional programme for the eradication of the Carambola fruit fly in South America. In Area-wide Control of Fruit Flies and other Insect Pests, ed. KH Tan, pp. 395-9. Penang, Malaysia: CABI Publishing McKenzie L, Dransfield, L., Driver, F., Curran J. 1999. Molecular protocols for species identification of Tephritid fruit flies, CSIRO Entomology, Canberra McQuate GT, Follett PA, Yoshimoto JM. 2000. Field infestation of rambutan fruits by internal-feeding pests in Hawaii. J. Econ. Entomol. 93: 846-51 Meats A. 1981. The bioclimatic potential of the Queensland fruit fly, Dacus tryoni, in Australia. Proc. Ecol. Soc. Aust. 11: 151-61 Meixner MD, McPheron BA, Silva JG, Gasparich GE, Sheppard WS. 2002. The Mediterranean fruit fly in California: Evidence for multiple introductions and persistent populations based on microsatellite and mitochondrial DNA variability. Mol. Ecol. 11: 891-9 Metcalf RL. 1987. Plant volatiles as insect attractants. CRC Critical Rev. Plant Sc. 5: 251-301 Metcalf RL. 1990. Chemical ecology of dacine fruit flies (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 83: 1017-30 Michaux B. 1996. The origin of southwest Sulawesi and other Indonesian terranes: a biological view. Palaeogeography, Palaeoclimatology, Palaeoecology 122: 167-83 Mun J, Kim J, Song Y, Kim T, Roderick GK, et al. 2000. Molecular genetic diagnosis of four fruit fly species (Tephritidae). J. Asia Pacific Entomol. 3: 89-94 Mun J-H, Bohonak AJ, Roderick GK. 2003. Population structure of the pumpkin fruit fly Bactrocera depressa (Tephritidae) in Korea and Japan: Pliocene allopatry or recent invasion? Mol. Ecol. 12: 2941-51 Muraji M, Nakahara S. 2001. Phylogenetic relationships among fruit flies, Bactrocera (Diptera, Tephritidae), based on the mitochondrial rDNA sequences. Insect Mol. Biol. 10: 549-59 78. 79. 80. 81. 82. 83. 84. 85. 86. 87. Muraji M, Nakahara S. 2002. Discrimination among pest species of Bactrocera (Diptera: Tephritidae) based on PCR-RFLP of the mitochondrial DNA. Appl. Entomol. Zool. 37: 437-46 Naeole CKM, Haymer DS. 2003. Use of oligonucleotide arrays for molecular taxonomic studies of closely related species in the oriental fruit fly complex. Mol. Ecol. Notes 3: 662-5 Nakahara S, Kato H, Kaneda M, Sugimoto T, Muraji M. 2001. Identification of Bactrocera dorsalis complex species (Diptara: Tephritidae) by PCR-RFLP Analysis II. A study of genetic variation in B. dorsalis complex (Philippines population) and B. dorsalis (Taiwan population). Res. Bull. Plant Prot. Serv., Japan 37: 69-73 Nakahara S, Kato H, Kaneda M, Sugimoto T, Muraji M. 2002. Identification of the Bactrocera dorsalis complex (Diptera: Tephritidae) by PCRRFLP analysis: III. Discrimination between B. philippinensis and B. occipitalis. Res. Bull. Plant Prot. Serv., Japan 38: 73-80 Nakahara S, Masaki M, Kaneda M, Sugimoto T, Muraji M. 2000. Identification of Bactrocera dorsalis complex species (Diptera: Tephritidae: Dacinae) by PCR-RFLP analysis. I. A study of variation in Mitochondrial DNA D-loop region. Res. Bull. Plant Prot. Serv., Japan 36: 37-41 Nakahara S, Tsuchiya T, Sato M, Masaki M, Kaneda M. 2000. Research on infestation to many kinds of plants by the pests of quarantine importance. Bactrocera dorsalis complex. Res. Bull. Plant Prot. Serv., Japan: 53-6 Nishida R, Iwahashi O, Tan KH. 1993. Accumulation of Dendrobium superbum (Orchidaceae) fragrance in the rectal glands by males of the melon fly, Dacus cucurbitae. J. Chem. Ecol. 19: 713-22 Nishida R, Shelly TE, Kaneshiro K. 1997. Acquisition of female-attracting fragrance by males of the oriental fruit fly from a Hawaiian lei flower, Fagraea beteriana. J. Chem. Ecol. 23: 2275-85 Nishida R, Tan KH, Serit M, Lajis NH, Sukari AM, et al. 1988. Accumulation of phenylpropanoids in the rectal glands of males of the Oriental fruit fly, Dacus dorsalis. Experientia 44: 534-6 Novotny V, Clarke AR, Drew RAI, Balagawi S, Clifford B. in press. Host specialization and species richness of fruit flies (Diptera: Tephritidae) in a B. DORSALIS COMPLEX OF FRUIT FLIES 88. 89. 90. 91. 92. 93. 94. 95. 96. 97. 98. New Guinea rainforest. Journal of Tropical Ecology: in press Ooi CS. 1991. Genetic variation in populations of two sympatric taxa in the Dacus dorsalis complex and their relative infestation levels in various fruit hosts. Presented at Proceedings, 1st International Symposium on Fruit Flies in the Tropics, Kuala Lumpur Paterson HEH. 1985. The recognition concept of species. In Species and Speciation, ed. ES Vrba, pp. 21-9. Pretoria: Transvaal Museum Perkins MV, Fletcher MT, Kitching W, Drew RAI, Moore CJ. 1990. Chemical studies of rectal gland secretions of some species of Bactrocera dorsalis complex of fruit flies (Diptera: Tephritidae). J. Chem. Ecol. 16: 2475-87 Prokopy RJ. 1983. Tephritid relationships with plants. Presented at Fruit flies of economic importance, Proceedings of the CEC-IOBC International Symposium Athens, Greece, 16-19 November 1982 Putulan D, Sar S, Drew RAI, Raghu S, Clarke AR. 2004. Fruit and vegetable movement on domestic flights in Papua New Guinea and the risk of spreading pest fruit-flies (Diptera: Tephretidae). International Journal of Pest Management 50: 17-22 Raghu S. 2003. The autecology of Bactrocera cacuminata (Hering) (Diptera: Tephritidae: Dacinae): Functional significance of resources. Doctor of Philosophy thesis. Griffith University, Brisbane. 240 pp. Raghu S, Clarke AR. 2003. Sexual selection in a tropical fruit fly: role of a plant derived chemical in mate choice. Entomol. Exp. Applic. 107: 53-8 Raghu S, Clarke AR. 2003. Spatial and temporal partitioning of behaviour by adult fruit flies: direct evidence for methyl eugenol as a mate rendezvous cue for Bactrocera cacuminata. Physiol. Entomol. 28: 175-84 Raghu S, Clarke AR, Bradley J. 2002. Microbial mediation of fruit fly - host plant interactions: Is the host plant the "centre of activity"? Oikos 97: 319-28 Raghu S, Clarke AR, Yuval B. 2002. Investigation of physiological consequences of feeding on methyl eugenol by Bactrocera cacuminata (Diptera: Tephritidae). Environ. Entomol. 31: 941-6 Rajpoot SKS, Ali S, Rizvi SMA. 2002. Relative population and host preference 99. 100. 101. 102. 103. 104. 105. 106. 107. 108. 109. of fruit fly Bactrocera dorsalis on cucurbits. Ann. Plant Prot. Sc. 10: 62-4 Roderick GK, F.X. V. 1996. Genetic and statistical analysis of colonisation. In Fruit fly pests: A world assessment of their biology and management, ed. BA McPheron, GJ Steck, pp. 281-90. Delray Beach: St. Lucie Press Roderick GK, Navajas M. 2003. Genes in novel environments: Genetics and evolution in biological control. Nature Rev. Genetics 4: 889-99 Seewooruthun SI, Shradanand P, Bhubaneswar G, Soonnoo AR, Malini A, et al. 2000. Eradication of an exotic fruit fly from Mauritius. In Area-wide Control of Fruit Flies and other Insect Pests, ed. KH Tan. Penang, Malaysia: CABI Publishing Seo ST, Chambers Dl, Kobayashi RM, Lee CYL, Komura M. 1970. Infestation of Oriental fruit flies in 53-116 and smooth cayenne pineapple varieties grown near supporting guava or other host fruits. J. Econ. Entomol. 63: 1830-1 Shelly TE. 2000. Flower-feeding effects mating performance in male oriental fruit flies Bactrocera dorsalis. Ecol. Entomol. 25: 109-14 Shelly TE. 2001. Feeding on methyl eugenol and Fagraea berteriana flowers increases long-range female attraction by males of the oriental fruit fly (Diptera: Tephritidae). Florida Entomol. 84: 63440 Shelly TE. 2002. Feeding on papaya flowers enhances mating competitiveness of male oriental fruit flies, Bactrocera dorsalis (Diptera: Tephritidae). Proc. Hawaiian Entomol. Soc. 35: 41-7 Shelly TE, Dewire AM. 1994. Chemically mediated mating success in male oriental fruit flies. Ann. Entomol. Soc. Am. 87: 375-82 Shelly TE, Kaneshiro KY. 1991. Lek behaviour of the oriental fruit fly in Hawaii. J. Insect Behav. 4: 235-41 Shelly TE, Resilva S, Reyes M, Bignayan H. 1996. Methyl eugenol and mating competitiveness of irradiated male Bactrocera philippinensis. Florida Entomol. 79: 481-8 Smith ESC, Price NS, Seewooruthun I. 2000. Detection and eradication of the exotic fruit fly Bactrocera philippinensis from Australia. Presented at Proceedings of the Indian Ocean Commission, Regional Fruit Fly Symposium, Flic en Flac, Mauritius, 5th-9th June B. DORSALIS COMPLEX OF FRUIT FLIES 110. 111. 112. 113. 114. 115. 116. 117. 118. 119. 120. 121. Smith PT, Kambhampati S, Armstrong KA. 2003. Phylogenetic relationships among Bactrocera species (Diptera: Tephritidae) inferred from mitochondrial DNA sequences. Mol. Phylogenetics Evol. 26: 8-17 Smith PT, McPheron BA, Kambhampati S. 2002. Phylogenetic analysis of mitochondrial DNA supports the monophyly of Dacini fruit flies (Diptera: Tephritidae). Ann. Entomol. Soc. Am. 95: 658-64 Sved JA, Yu H, Dominiak B, Gilchrist AS. 2003. Inferring modes of colonization for pest species using heterozygosity comparisons and a shared-allele test. Genetics 163: 823-31 Tan KH, ed. 2000. Area-wide Control of Fruit Flies and other Insect Pests. Penang, Malaysia: CABI Publishing. 780 pp. Tan KH, Nishida R. 1998. Ecological significance of male attractant in the defence and mating strategies of the fruit fly, Bactrocera papayae. Entomol. Exp. Applic. 89: 155-8 Thompson FC, ed. 1998. Fruit Fly Expert Identification System and Systematic Information Database. Myia 9. Leiden: Backhuys Tsuruta K, White IM. 2001. Eleven new species of the Genus Bactrocera Macquart (Diptera: Tephritidae) from Sri Lanka. Entomol. Sc. 4: 69-87 Tsuruta K, White IM, Bandara HM, Rajapakse H, Sundaraperuma SA, et al. 1997. A preliminary note on the hostplants of fruit flies of the Tribe Dacini (Diptera, Tephritidae) in Sri Lanka. Esakia 37: 149-60 van Sauers-Muller A. 1991. An overview of the carambola fruit fly Bactrocera species (Diptera: Tephritidae) found recently in Suriname. Florida Entomol. 74: 432-41 Vargas RI, Stark JD, Kido MH, Ketter HM, Whitehand LC. 2000. Methyl eugenol and cue-lure traps for suppression of male oriental fruit flies and melon flies (Diptera: Tephritidae) in Hawaii: Effects of lure mixtures and weathering. J. Econ. Entomol. 93: 81-7 Vargas RI, Walsh WA, Kanehisa D, Stark JD, Nishida T. 2000. Comparative demography of three Hawaiian fruit flies (Diptera: Tephritidae) at alternating temperatures. Ann. Entomol. Soc. Am. 93: 75-81 Vargas RI, Walsh WA, Nishida T. 1995. Colonization of newly planted coffee 122. 123. 124. 125. 126. 127. 128. 129. 130. 131. fields - dominance of Mediterranean fruit-fly over Oriental fruit-fly (Diptera, Tephritidae). J. Econ. Entomol. 88: 6207 Verheij EWM, Coronel RE. 1992. Introduction. In Plant Resources of South-East Asia. No. 2. Edible Fruits and Nuts, ed. EWM Verheij, RE Coronel. Bogor, Indonesia: PROSEA Foundation Vijaysegaran S. 1991. The current situation on fruit flies in peninsular Malaysia. In Fruit Flies in the Tropics. Proceedings of the First International Symposium, 14-16 March 1988, Kuala Lumpur, Malaysia, ed. S Vijaysegaran, A Ibrahim, pp. 125-39. Kuala Lumpur: Malaysian Agricultural Research and Development Institute and Malaysian Plant Protection Society Vinod K, Agarwal ML. 1998. Effect of some tropical hosts on development and survival of Bactrocera dorsalis (Hendel). Shashpa 5: 185-8 Wang Y, Yu H, Raphael K, Gilchrist AS. 2003. Genetic delineation of sibling species of the pest fruit fly Bactocera (Diptera : Tephritidae) using microsatellites. Bull. Entomol. Res. 93: 351-60 Waterhouse DF. 1993. The Major Arthropod Pests and Weeds of Agriculture in Southeast Asia. Canberra: ACIAR Monograph No. 21. 141 pp. Waterhouse DF. 1997. The Major Invertebrate Pests and Weeds of Agriculture and Plantation Forestry in the Southern and Western Pacific. Canberra: ACIAR Monograph No. 44 Wee S, Tan K, Wee SL, Tan KH. 2000. Interspecific cross of the Bactrocera dorsalis complex (Diptera: Tephritidae): how did it happen? In Area-wide Control of Fruit Flies and Other Insect Pests, ed. KH Tan, pp. 667-74. Penang, Malaysia: CABI Publishing Wee SL, Hee AKW, Tan KH. 2002. Comparative sensitivity to and consumption of methyl eugenol in three Bactrocera dorsalis (Diptera: Tephritidae) complex sibling species. Chemoecology 12: 193-7 White IM. 1996. Fruit fly taxonomy: recent advances and new approaches. In Fruit fly pests a world assessment of their biology and management, ed. BA McPheron, GJ Steck, pp. 253-8. Delray Beach, FL: St. Lucie Press White IM. 2000. Morphological features of the tribe Dacini (Dacinae): their B. DORSALIS COMPLEX OF FRUIT FLIES 132. 133. 134. significance to behaviour and classification. In Fruit Flies (Tephritidae): phylogeny and evolution of behaviour, ed. M Aluja, AL Norrbom, pp. 505-33. Boca Raton: CRC Press White IM, Elson-Harris MM. 1992. Fruit flies of economic significance: Their identification and bionomics. Wallingford, Oxon.: C.A.B International in association with ACIAR White IM, Hancock DL. 1997. Computer Aided Biological Identification key (CABIKEY): IndoAustralasian Dacini Fruit Flies. London. (CD-ROM): CAB International and International Institute of Entomology. Yong HS. 1995. Genetic differentiation and relationships in five taxa of the 135. 136. Bactrocera dorsalis complex (Insecta: Diptera: Tephritidae). Bull. Entomol. Res. 85: 431-5 Yu H, Frommer M, Robson MK, Meats AW, Shearman DCA, Sved JA. 2001. Microsatellite analysis of the Queensland fruit fly Bactrocera tryoni (Diptera : Tephritidae) indicates spatial structuring: implications for population control. Bull. Entomol. Res. 91: 139-47 Zwolfer H. 1983. Life systems and strategies of resource exploitation in tephritids. Presented at Fruit flies of economic importance, Proceedings of the CEC-IOBC International Symposium Athens, Greece, 16-19 November 1982