Hostname: page-component-7479d7b7d-767nl Total loading time: 0 Render date: 2024-07-11T22:18:20.692Z Has data issue: false hasContentIssue false
  • English
  • Français

Functional significance of phytochemical lures to dacine fruit flies (Diptera: Tephritidae): an ecological and evolutionary synthesis

Published online by Cambridge University Press:  09 March 2007

S. Raghu
S. Raghu*
Affiliation:
Tropical Fruit Fly Research Group, Faculty of Environmental Sciences, Griffith University, Nathan, Queensland 4111, Australia
*
*Alan Fletcher Research Station, CRC for Australian Weed Management and Queensland Department of Natural Resources and Mines, Sherwood, QLD 4075, Australia Fax: +61 7 3379 6815 E-mail: raghu.s@nrm.qld.gov.au
Get access Rights & Permissions [Opens in a new window]

Abstract

While lures of plant origin are vital tools in dacine (Diptera: Tephritidae) pest management, the ecological and evolutionary significance of this lure response remains enigmatic. Two hypotheses (the ancestral host hypothesis and sexual selection by female choice) have been invoked to explain the functional significance of these chemicals to dacine fruit flies. These hypotheses are often treated as alternatives to one another and evidence favouring one is used to reject the other. This review highlights that these two hypotheses are not logical alternatives to each other as the ancestral host hypothesis attempts to explain the ultimate function of the response of Dacinae to these plant-derived parapheromones while the sexual selection hypothesis provides a proximate explanation for lure response. Research on lure response, dacine mating behaviour, functional significance of lures, plant phylogeny and biochemistry and dacine pheromone chemistry are used to evaluate the evidence in relation to both these hypotheses. Some of the key findings are that there is evidence both in support of and against these two hypotheses. Response of fruit flies to related phenyl propanoids to those commonly used as lures in pest management and distribution of phenyl propanoids attractive to dacines among plant orders strongly support the ancestral host hypothesis. Evidence from pheromone chemistry, dacine mating behaviour and the functional significance of lures both support and contradict the sexual selection hypothesis. Lures appear to have different proximate functions in different dacine species. Considerably greater research is needed to clarify the functional role of phytochemical lures to dacine fruit flies. The two prevalent hypotheses should be investigated independently. Specific research on dacine phylogeny and distribution of lures in plants in relation to ecological roles played by adult dacines is required to elucidate the ultimate roles of the chemicals. Exploration of female response to lures and the behavioural consequences of dacine response to these chemicals to both the insect and plant may shed light on the proximate functions of these chemicals.

Type
Review Article
Information
Bulletin of Entomological Research , Volume 94 , Issue 5 , October 2004 , pp. 385 - 399
Copyright
Copyright © Cambridge University Press 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abraham, V. & Verghese, A. (1998) Methyl eugenol attracts female mango fruit fly, Bactrocera dorsalis Hendel. Insect Environment 4 101Google Scholar
Alyokhin, A.V., Messing, R.H. & Duan, J.J. (2001) Abundance and mating behaviour of Oriental fruit flies (Diptera: Tephritidae) near methyl eugenol-baited traps. Pan-Pacific Entomologist 77, 161–167.Google Scholar
Andersson, M. (1994) Sexual selection. Princeton, New Jersey, Princeton University Press.Google Scholar
Armbuster, W.S., Howard, J.J., Clausen, T.P., Debevec, E.M., Loquvam, J.C., Matsuki, M., Cerendelo, B. & Andel, F. (1997) Do biochemical exaptations link evolution of plant defense and pollination systems? Historical hypotheses and experimental tests with Dalechampia vines. American Naturalist 149, 461–484.CrossRefGoogle Scholar
Baker, R. & Bacon, A.J. (1985) The identification of spiroacetals in the volatile secretions of two species of fruit flies (Dacus dorsalis, Dacus cucurbitae). Experientia 44, 1484–1485.CrossRefGoogle Scholar
Baker, R. & Herbert, R.H. (1987) Isolation and synthesis of 1,7-dioxaspiro[5.5]undecane and 1,7-dioxaspiro[5.5]undecan-3- and 4-ols from the olive fly (Dacus oleae). Journal of the Chemical Society, Perkins Transactions 1, 1123–1127.CrossRefGoogle Scholar
Baker, R., Herbert, R.H., House, P.E., Jones, O.T., Francke, W. & Ruth, W. (1980) Identification and synthesis of the major sex pheromone of the olive fly (Dacus oleae). Journal of the Chemical Society, Chemical Communications 1, 52–54.CrossRefGoogle Scholar
Bellas, T.E. & Fletcher, B.S. (1979) Identification of the major components in the secretion from the rectal pheromone glands of the Queensland fruit flies, Dacus tryoni and Dacus neohumeralis. Journal of Chemical Ecology 5, 795–803.CrossRefGoogle Scholar
Berenbaum, M.R. (1988) Allelochemicals in insect–microbe–plant interactions; agent provocateurs in the coevolutionary arms race. pp. 97–163New York, John Wiley & Sons.Google Scholar
Berenbaum, M.R. (1995) Turnabout is fair play: secondary roles for primary compounds. Journal of Chemical Ecology 21, 925–940.CrossRefGoogle ScholarPubMed
Brieze-Stegeman, R., Rice, M.A. & Hooper, G.H.S. (1978) Daily periodicity in attraction of male tephritid fruit flies to synthetic chemical lures. Journal of the Australian Entomological Society 17, 341–346.CrossRefGoogle Scholar
Clarke, A.R., Balagawi, S., Clifford, B., Drew, R.A.I., Leblanc, L., Mararuai, A., McGuire, D., Putulan, D., Sar, S.A. & Tenakanai, D. (2002) Evidence for orchid visitation by Bactrocera species (Diptera: Tephritidae) in Papau New Guinea. Journal of Tropical Ecology 18, 441–448.CrossRefGoogle Scholar
Crepet, W.L. & Friis, E.M. (1987) The evolution of insect pollination in angiosperms. The origin of angiosperms and the their biological consequences pp 181–201 in Friis, E.M., Chaloner, W.G. & Crane, P.R. (Eds)Cambridge, Cambridge University Press.Google Scholar
Cunningham, R.T. (1989a) Population detection. pp. 169–173 in Robinson, A.S. & Hooper, G. (Eds). Fruit flies: their biology, natural enemies and control. Amsterdam, Elsevier.Google Scholar
Cunningham, R.T. (1989b) Parapheromones. pp. 221–230 in Robinson, A.S., Hooper, G. (Eds). Fruit flies: their biology, natural enemies and control. Amsterdam, Elsevier.Google Scholar
Dodson, C.H. & Hills, H.G. (1966) Gas chromatography of orchid fragrances. American Orchid Society Bulletin 35, 720–725.Google Scholar
Dodson, C.H., Dressler, R.L., Hills, H.G., Adams, R.M. & Williams, N.H. (1969) Biologically active compounds in orchid fragrances. Science 164, 1243–1249.CrossRefGoogle ScholarPubMed
Drew, R.A.I. (1989) The tropical fruit flies (Diptera: Tephritidae: Dacinae) of the Australasian and Oceanian regions. Memoirs of the Queensland Museum 26, 1–521.Google Scholar
Drew, R.A.I. & Hancock, D.L. (1994) The Bactrocera dorsalis complex of fruit flies (Diptera: Tephritidae: Dacinae) in Asia. Bulletin of Entomological Research Supplement 2, 1–68.Google Scholar
Dudareva, N., Piechulla, B. & Pichersky, E. (1999) Biogenesis of floral scents. Horticultural Reviews 24, 31–54.Google Scholar
Edwards, R. & Gatehouse, J.A. (1999) Secondary metabolism. pp. 193–218 in Lean, P.J. & Leegood, R.C. (Eds). Plant biochemistry and molecular biology Chichester, England John Wiley & Sons.Google Scholar
Fabre, J.H. (1912) Social life in the insect world London, T. Fisher UnwinCrossRefGoogle Scholar
Fitt, G.P. (1981a) Responses by female Dacinae to ‘male’ lures and their relationship to patterns of mating behavior and pheromone response. Entomologia Experimentalis et Applicata 29, 87–97.CrossRefGoogle Scholar
Fitt, G.P. (1981b) The influence of age, nutrition and time of day on the responsiveness of male Dacus opiliae to the synthetic lure, methyl eugenol. Entomologia Experimentalis et Applicata 30, 83–90.CrossRefGoogle Scholar
Fletcher, B.S. (1968) Storage and release of a sex pehromone by the the Queensland fruit fly, Dacus tryoni (Diptera: Tephritidae). Nature 219, 631–632.CrossRefGoogle Scholar
Fletcher, M.T. & Kitching, W. (1995) Chemistry of fruit flies. Chemical Reviews 95, 789–828.CrossRefGoogle Scholar
Fletcher, B.S., Bateman, M.A., Hart, N.K. & Lamberton, J.A. (1975) Identification of fruit fly attractant in an Australian plant, Zieria smithii, as o-methyl eugenol. Journal of Economic Entomology 68, 815–816.CrossRefGoogle Scholar
Fletcher, M.T., Wells, J.A., Jacobs, M.F., Krohn, S., Kitching, W., Drew, R.A.I., Moore, C.J. & Francke, W. (1992) Chemistry of fruit flies. Spiroacetal-rich secretions in several Bactrocera species from the south-west Pacific region. Journal of the Chemical Society, Perkins Transactions 1, 2827–2831.CrossRefGoogle Scholar
Fletcher, M.T., Wood, B.J.I.M. B., Stok, J.E., De Voss, J.J. & Kitching, W. (2002) [18O]-Oxygen incorporation reveals novel pathways in spiroacetal biosynthesis by Bactrocera cacuminata and B. cucumis. Journal of the American Chemical Society 124, 7666–7667.CrossRefGoogle Scholar
Francke, W., Hindorf, G. & Reith, W. (1979) Alkyl-1,6-dioxaspiro[4.4]nonane: a new class of pheromones. Naturwissenschaften 66, 618–619.CrossRefGoogle Scholar
Friedrich, H. (1976) Phenylpropanoid constituents of essential oils. Lloydia 39, 1–7.Google ScholarPubMed
Friis, E.M. & Crepet, W.L. (1987) Time of appearance of floral features. pp. 145–179 in Friis, E.M., Chaloner, W.G. & Crane, P.R. (Eds). The origin of angiosperms and the their biological consequences Cambridge, Cambridge University Press.Google Scholar
Friis, E.M., Chaloner, W.G. & Crane, P.R. (Eds). (1987) The origin of angiosperms and the their biological consequences Cambridge, Cambridge University Press.Google Scholar
Gallois, A. (1982) Dosage rapide de la parahydroxyphenyl-1-butanone dans la framboise par chromatographie sur couche mince. Sciences des Aliments 2, 99–106.Google Scholar
Gardner, M.C. & Gillman, M.P. (2002) The taste of nectar–a neglected area of pollination ecology. Oikos 98, 551–556.Google Scholar
Geissman, T.A. & Crout, D.H.G. (1969) Organic chemistry of secondary plant metabolism San Francisco, Freeman, Cooper & Co.Google Scholar
Graham, G.C., Yeates, D.K. & Drew, R.A.I. (1998) Dacine tephritids: evolutionary studies for identification, ethology and ecology. Sixth Australasian Applied Entomological Research ConferenceUniversity of Queensland, Brisbane. pp. 456–462.Google Scholar
Hancock, D.L. (1985) A specific male attractant for the melon fly, Dacus vertebratus. Zimbabwe Science News 19, 118–119.Google Scholar
Haniotakis, G., Mazomenos, B.E. & Tumlinson, J.H. (1977) A sex attractant of the olive fruit fly, Dacus oleae, and its biological activity under laboratory and field conditions. Entomologia Experimentalis et Applicata 21, 81–87.CrossRefGoogle Scholar
Haniotakis, G., Francke, W., Mori, K., Redlich, H. & Schurig, V. (1986) Sex-specific activity of (R)-(-)-and (S)-(+)-1,7, dioxaspiro[5.5]undecane, the major pheromone of Dacus oleae. Journal of Chemical Ecology 12, 1559–1568.CrossRefGoogle Scholar
Harbourne, J.B. & Turner, B.L. (1984) Plant chemosystematics. London, Academic Press.Google Scholar
Harrewijn, P., Minks, A.K. & Mollema, C. (1995) Evolution of plant volatile production in insect–plant relationships. Chemoecology 5/6, 55–73.Google Scholar
Haslam, E. (1995) Secondary metabolism – evolution and function: products or processes? Chemoeoclogy 5/6 89–95.Google Scholar
Haukioja, E., Ossipov, V., Koricheva, J., Honkanen, T., Larsson, S. & Lempa, K. (1998) Biosynthetic origin of carbon-based secondary compounds: cause of variable responses of woody plants to fertilization? Chemoecology 8, 133–139.CrossRefGoogle Scholar
Herrmann, K.M. (1995a) The Shikimate pathway: early steps in the biosynthesis of aromatic compounds. Plant Cell 7, 907–919.CrossRefGoogle ScholarPubMed
Herrmann, K.M. (1995b) The Shimikate pathway as an entry to aromatic secondary metabolism. Plant Physiology 107, 7–12.CrossRefGoogle ScholarPubMed
Herrmann, K.M. & Weaver, L.M. (1999) The shikimate pathway. Annual Review of Plant Physiology and Plant Molecular Biology 50, 473–503.CrossRefGoogle ScholarPubMed
Hirvi, T. & Hokkanen, E. (1984) The aroma of fruit of the sea buckthorn Hippophae rhamnoides L. Zeitschrift für Lebensmittel-Untersuchung und-Forschung 179, 387–388.CrossRefGoogle Scholar
Hirvi, T., Hokkanen, E., Pyysalo, T.. (1981) The aroma of cranberries. Zeitschrift für Lebensmittel-Untersuchung und-Forschung 172, 365–367.CrossRefGoogle Scholar
Hokkanen, E., Pyysalo, T. & Hirvi, T. (1980) The aroma of Finnish wild raspberries. Rubus idaeus L. Zeitschrift für Lebensmittel-Untersuchung und-Forschung 171, 180–182.CrossRefGoogle Scholar
Howlett, F.M. (1912) The effect of citronella oil in two species of Dacus. Transactions of the Entomological Society, London 60, 412–418.CrossRefGoogle Scholar
Howlett, F.M. (1915) Chemical reactions of fruit flies. Bulletin of Entomological Research 6, 297–305.CrossRefGoogle Scholar
Janssen, A., Bruin, J., Jacobs, G., Schraag, R. & Sabelis, M.W. (1997) Predators use volatiles to avoid prey patches with conspecifics. Journal of Animal Ecology 66, 223–232.CrossRefGoogle Scholar
Judd, W.S., Campbell, C.S., Kellogg, E.A. & Stevens, P.F. (1999) Plant systematics–a phylogenetic approach Sunderland, Massachusetts, Sinauer Associates Inc.Google Scholar
Karlson, P. & Butenandt, A. (1959) Pheromones (ectohormones) in insects. Annual Review of Entomology 4, 39–58.CrossRefGoogle Scholar
Kitching, W., Lewis, J.A., Perkins, M.V., Drew, R.A.I., Moore, C.J., Schurig, V., Konig, W.A. & Francke, W. (1989) Chemistry of fruit flies. Composition of the rectal gland secretion of (male) Dacus cucumis (cucumber fly) and Dacus halfordiae. Characterization of (Z, Z)-2,8-dimethyl-1,7-dioxaspiro[5.5]undecane. Journal of Organic Chemistry 54, 3893–3902.CrossRefGoogle Scholar
Knudsen, J.T., Tollsten, L. & Gunnar Bergström, L. (1993) Floral scents–a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33, 253–280.CrossRefGoogle Scholar
Korneyev, V.A. (2000) Morphological features of the Tribe Dacini (Dacinae): their significance to behaviour and classification. pp. 3–22 in Aluja, M., Norrbom, A. (Eds). Fruit flies: phylogeny and evolution of behaviour. Boca Raton, Florida, CRC Press.Google Scholar
Koyama, J. (1989) Mating pheromones: tropical dacines. pp. 165–168 in Robinson, A.S., Hooper, G. (Eds). Fruit flies: their biology, natural enemies and control Amsterdam, Elsevier.Google Scholar
Krohn, S., Fletcher, M.T., Kitching, W., Drew, R.A.I., Moore, C.J. & Francke, W. (1991) Chemistry of fruit flies: nature of glandular secretion and volatile emission of Bactrocera cacuminatus (Hering). Journal of Chemical Ecology 17, 485–495.CrossRefGoogle ScholarPubMed
Labandeira, C.C. (1997) Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Annual Review of Ecology and Systematics 28, 153–193.CrossRefGoogle Scholar
Landolt, P.J. & Phillips, T.W. (1997) Host plant influences on sex pheromone behaviour of phytophagous insects. Annual Review of Entomology 42, 371–391.CrossRefGoogle ScholarPubMed
Lewis, J.A., Moore, C.J., Fletcher, M.T., Drew, R.A.I. & Kitching, W. (1988) Volatile compounds from the flowers of Spathiphyllum cannaefolium. Phytochemistry 27, 2755–2757.CrossRefGoogle Scholar
Marco, J.A., Barbera, O., Rodriguez, S., Domingo, C. & Adell, J. (1988) Flavonoids and other phenolics from Artemisia hispanica. Phytochemistry 27, 3155–3159.CrossRefGoogle Scholar
Matsuki, M. (1996) Regulation of plant phenolic synthesis: from biochemistry to ecology and evolution. Australian Journal of Botany 44, 613–634.CrossRefGoogle Scholar
Mazomenos, B.E. (1989) Dacus oleae. pp. 169–178 in Robinson, A.S., Hooper, G. (Eds). Fruit flies: their biology, natural enemies and control. Amsterdam, Elsevier.Google Scholar
McKey, D. (1979) The distribution of secondary compounds within plants. pp. 56–133 in Rosenthal, G., Janzen, D. (Eds). Herbivores: their interactions with plant secondary metabolites. New York, Academic Press.Google Scholar
Meats, A. & Hartland, C.L. (1999) Upwind anemotaxis in response to cue-lure by the Queensland fruit fly, Bactrocera tryoni. Physiological Entomology 24, 90–97.CrossRefGoogle Scholar
Meats, A. & Osborne, A. (2000) Dose-related upwind anemotaxis and movement up odour gradients in still air in the presence of methyl eugenol by the wild tobacco fruit fly, Bactrocera cacuminata. Physiological Entomology 25, 41–47.CrossRefGoogle Scholar
Metcalf, R.L. (1979) Plants, chemicals and insects. Some aspects of coevolution. Bulletin of the Entomological Society of America 25, 30–35.CrossRefGoogle Scholar
Metcalf, R.L. (1987) Plant volatiles as insect attractants. CRC Critical Reviews in Plant Sciences 5, 251–301.CrossRefGoogle Scholar
Metcalf, R.L. (1990) Chemical ecology of dacine fruit flies (Diptera: Tephritidae). Annals of the Entomological Society of America 83, 1017–1030.CrossRefGoogle Scholar
Metcalf, R.L. & Metcalf, E.R. (1992) Plant kairomones in insect ecology and control. New York, Chapman and Hall.Google Scholar
Metcalf, R.L., Metcalf, E.R., Mitchell, W.E. & Lee, L.W.Y. (1979) Evolution of the olfactory receptor in the oriental fruit fly, Dacus dorsalis. Proceedings of the National Academy of SciencesUSA76, 1561–1565.CrossRefGoogle Scholar
Metcalf, R.L., Metcalf, E.R. & Mitchell, W.C. (1981) Molecular parameters and olfaction in the oriental fruit fly Dacus dorsalis. Proceedings of the National Academy of SciencesUSA 78, 4007–4010.CrossRefGoogle Scholar
Metcalf, R.L., Mitchell, W.C. & Metcalf, E.R. (1983) Olfactory receptors in the melon fly Dacus cucurbitae and the oriental fruit fly Dacus dorsalis. Proceedings of the National Academy of Sciences, USA 80, 3143–3147.CrossRefGoogle ScholarPubMed
Mori, K. (1997) Pheromones: synthesis and bioactivity. Journal of the Chemical Society, Chemical Communications 1997, 1153–1158.CrossRefGoogle Scholar
Muraji, M. & Nakahara, S. (2001) Phylogenetic relationships among fruit flies, Bactrocera (Diptera, Tephritidae), based on the mitochondrial rDNA sequences. Insect Molecular Biology 10, 549–559.CrossRefGoogle ScholarPubMed
Nakagawa, S., Farias, G.J. & Steiner, L.F. (1970) Response of female Mediterranean fruit flies to male lures in the relative absence of males. Journal of Economic Entomology 63, 227–229.CrossRefGoogle Scholar
Nation, J.L. (1981) Sex-specific glands in tephritid fruit flies of the genera Anastrepha, Ceratitis, Dacus and Rhagoletis (Diptera: Tephritidae). Journal of Insect Morphology and Embryology 10, 121–129.CrossRefGoogle Scholar
Niklas, K.J. (1982) Chemical diversification and evolution of plants as inferred from paleobiochemical studies. pp. 29–91 in Nitecki, M.H. (Eds). Biochemical aspects of evolutionary biology. Chicago, University of Chicago Press.Google Scholar
Nishida, R. & Fukami, H. (1990) Sequestration of distasteful compounds by some pharmacophagous insects. Journal of Chemical Ecology 16, 151–164.CrossRefGoogle ScholarPubMed
Nishida, R., Tan, K.H., Serit, M., Lajis, N.H., Sukari, A.M., Takahashi, S. & Fukami, H. (1988) Accumulation of phenylpropanoids in the rectal glands of males of the Oriental fruit fly, Dacus dorsalis. Experientia 44, 534–536.CrossRefGoogle Scholar
Nishida, R., Iwahashi, O. & Tan, K.H. (1993) Accumulation of Dendrobium superbum (Orchidaceae) fragrance in the rectal glands by males of the melon fly, Dacus cucurbitae. Journal of Chemical Ecology 19, 713–722.CrossRefGoogle Scholar
Nishida, R., Shelly, T.E. & Kaneshiro, K. (1997) Acquisition of female-attracting fragrance by males of the oriental fruit fly from a Hawaiian lei flower, Fagraea beteriana. Journal of Chemical Ecology 23, 2275–2285.CrossRefGoogle Scholar
Nursten, H.E. (1970) Volatile compounds: the aroma of fruits. pp. 239–268 in Hulme, A.C. (Eds). The biochemistry of fruits and their products. London, Academic Press.Google Scholar
Paterson, H.E.H. (1993) Evolution and the recognition concept of species. Baltimore, Johns Hopkins University Press.Google Scholar
Pellmyr, O. & Thien, L.B. (1986) Insect reproduction and floral fragrances: keys to the evolution of the angiosperms. Taxon 35, 76–85.CrossRefGoogle Scholar
Perkins, M.V., Fletcher, M.T., Kitching, W., Drew, R.A.I. & Moore, C.J. (1990) Chemical studies of the rectal gland secretions of some species of Bactrocera dorsalis complex of fruit flies (Diptera: Tephritidae). Journal of Chemical Ecology 16, 2475–2487.CrossRefGoogle Scholar
Pichersky, E. & Gershenzon, J. (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Current Opinion in Plant Biology 5, 237–243.CrossRefGoogle ScholarPubMed
Poramarcom, R. & Boake, C.R. (1991) Behavioural influences on male mating success in the Oriental fruit fly, Dacus dorsalis Hendel. Animal Behaviour 42, 435–460.CrossRefGoogle Scholar
Raghu, S. (2003) The autecology of Bactrocera cacuminata (Hering) (Diptera: Tephritidae: Dacinae): functional significance of resources PhD thesis. Griffith University Brisbane.Google Scholar
Raghu, S. & Clarke, A.R. (2003a) Sexual selection in a tropical fruit fly: role of a plant derived chemical in mate choice. Entomologia Experimentalis et Applicata 107, 53–58.CrossRefGoogle Scholar
Raghu, S. & Clarke, A.R. (2003b) Spatial and temporal partitioning of behaviour by adult fruit flies: direct evidence for methyl eugenol as a mate rendezvous cue for Bactrocera cacuminata. Physiological Entomology 28, 175–184.CrossRefGoogle Scholar
Raghu, S. & Lawson, A.E. (2003) Feeding behaviour of Bactrocera cacuminata (Hering) (Diptera: Tephritidae) on methyl eugenol: a laboratory assay. Australian Journal of Entomology 42, 149–152.CrossRefGoogle Scholar
Raghu, S., Clarke, A.R. & Bradley, J. (2002a) Microbial mediation of fruit fly–host plant interactions: is the host plant the ‘centre of activity'? Oikos 97, 319–328.CrossRefGoogle Scholar
Raghu, S., Clarke, A.R. & Yuval, B. (2002b) Investigation of physiological consequences of feeding on methyl eugenol by Bactrocera cacuminata (Diptera: Tephritidae). Environmental Entomology 31, 941–946.CrossRefGoogle Scholar
Rohdendorf, B.B. (1974) The historical development of Diptera. Edmonton, University of Alberta.Google Scholar
Schmid, J. & Amrhein, N. (1999) The shikimate pathway. pp. 147–160 in Singh, B.K. (Ed). Plant amino acids: biochemistry and biotechnology. New York, Marcel Dekker.Google Scholar
Severin, H.P. & Severin, H.S. (1913) A historical account on the use of kerosene to trap the Mediterranean fruit fly. Journal of Economic Entomology 6, 347–351.CrossRefGoogle Scholar
Shelly, T.E. (2000) Flower-feeding effects mating performance in male oriental fruit flies Bactrocera dorsalis. Ecological Entomology 25, 109–114.CrossRefGoogle Scholar
Shelly, T.E. & Dewire, A.M. (1994) Chemically mediated mating success in male oriental fruit flies. Annals of the Entomological Society of America 87, 375–382.CrossRefGoogle Scholar
Shelly, T.E. & Villalobos, E.M. (1995) Cue lure and the mating behaviour of male melon flies (Diptera: Tephritidae). Florida Entomologist 78, 473–482.CrossRefGoogle Scholar
Shelly, T.E., Whittier, T.E. & Villalobos, E.M. (1996b) Trimedlure affects mating success and mate attraction in male Mediterranean fruit flies. Entomologia Experimentalis et Applicata 78, 181–185.CrossRefGoogle Scholar
Shelly, T.E., Resilva, S., Reyes, M. & Bignayan, H. (1996a) Methyl eugenol and mating competitiveness of irradiated male Bactrocera philippinensis. Florida Entomologist 79, 481–488.CrossRefGoogle Scholar
Smith, P.T., McPheron, B.A. & Kambhapati, S. (2002) Phylogenetic analysis of mitochondrial DNA supports the monophyly of Dacini fruit flies (Diptera: Tephritidae). Annals of the Entomological Society of America 95, 658–664.CrossRefGoogle Scholar
Smith, P.T., Kambhapati, S. & Armstrong, K.A. (2003) Phylogenetic relationship among Bactrocera species (Diptera: Tephritidae) inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 26, 8–17.CrossRefGoogle ScholarPubMed
Steiner, L.F., Mitchell, W.C., Harris, E.J., Kozuma, T.T. & Fujimoto, M.S. (1965) Oriental fruit fly eradication by male annihilation. Journal of Economic Entomology 58, 961–964.CrossRefGoogle Scholar
Stewart, W.N. (1983) Paleobotany and the evolution of plants. Cambridge, Cambridge University Press.Google Scholar
Stok, J.E., Lang, C., Schwartz, B.D., Fletcher, M.T., Kitching, W. & De Voss, J.J. (2001) Carbon hydroxylation of alkyltetrahydropyranols: a paradigm for spiroacetal biosynthesis in Bactrocera sp. Organic Letters 3, 397–400.CrossRefGoogle ScholarPubMed
Swain, T. (1977) Secondary compounds as protective agents. Annual Review of Plant Physiology 28, 479–501.CrossRefGoogle Scholar
Tallamy, D.W., Mullin, C.A. & Frazier, J.L. (1999) An alternate route to insect pharmacophagy: the loose receptor hypothesis. Journal of Chemical Ecology 25, 1987–1997.CrossRefGoogle Scholar
Tan, K.H. (2000) Sex pheromone components in defense of melon fly, Bactrocera cucurbitae against Asian house gecko, Hemidactylus frenatus. Journal of Chemical Ecology 26, 697–704.CrossRefGoogle Scholar
Tan, K.H. & Nishida, R. (1998) Ecological significance of male attractant in the defence and mating strategies of the fruit fly, Bactrocera papayae. Entomologia Experimentalis et Applicata 89, 155–158.Google Scholar
Tan, K.H. & Nishida, R. (2000) Mutual reproductive benefits between a wild orchid, Bulbophyllum patens, and Bactrocera fruit flies via a floral synomone. Journal of Chemical Ecology 26, 533–546.CrossRefGoogle Scholar
Tan, K.H., Nishida, R. & Toong, Y.C. (2002) Floral synomone of a wild orchid, Bulbophyllum cheiri, lures Bactrocera fruit flies for pollination. Journal of Chemical Ecology 28, 1161–1172.CrossRefGoogle ScholarPubMed
Thien, L.B., Heimermann, W.H. & Holman, R.T. (1975) Floral odours and quantitative taxonomy of Magnolia and Liriodendron. Taxon 24, 557–568.CrossRefGoogle Scholar
van Buren, J. (1970) Fruit phenolics. pp. 269–304 in Hulme, A.C. (Eds). The biochemistry of fruits and their products. London, Academic Press.Google Scholar
Van der Pijl, L. (1960) Ecological aspects of flower evolution. I. Phyletic evolution. Evolution 14, 403–416.CrossRefGoogle Scholar
Van der Pijl, L. (1961) Ecological aspects of flower evolution. II. Zoophilous flower classes. Evolution 15, 44–59.CrossRefGoogle Scholar
Walker, J.R.L. (1975) The biology of plant phenolics. London, Edward Arnold.Google Scholar
White, I.M. (2000) Morphological features of the Tribe Dacini (Dacinae): their significance to behaviour and classification. Fruit flies: phylogeny and evolution of behaviour pp. 505–533 in Aluja, M., Norrbom, A. (Eds). Boca Raton, Florida CRC Press.Google Scholar