Abstract
Males of many tephritid fruit fly species of the genus Bactrocera show a very strong affinity to methyl eugenol (ME). An attracted male compulsively ingests ME, which is then biotransformed before its metabolites are accumulated into the rectal gland. The glandular organ is known to serve as a reservoir for sex pheromone in some species. Upon ME-feeding, males of the oriental fruit fly, Bactrocera dorsalis, selectively accumulated two metabolites, 2-allyl-4,5-dimethoxyphenol (DMP) and (E)-coniferyl alcohol (E-CF), in the rectal pheromone gland. We compared the profiles of phenylpropanoid metabolites accumulated by three other species of very high economic and quarantine importance—Bactrocera invadens, Bactrocera zonata and Bactrocera correcta, with that of B. dorsalis. Males of each species were fed artificially on ME and the metabolites stored in the rectal glands were examined by means of chromatography and spectroscopy. Similar to B. dorsalis, males of laboratory-raised B. invadens accumulated DMP and E-CF, in almost equal quantities, in the rectal sac. The sum of DMP and E-CF increased gradually with time after ME consumption and reached as high as 150 μg/male 2 days post ME-feeding. Wild males of B. invadens captured in Kenya also possessed both the compounds in varying quantities. In contrast, males of B. zonata accumulated DMP and (Z)-coniferyl alcohol (Z-CF) in an approximate ratio of 1:1; whereas B. correcta is known to convert ME to (Z)-3,4-dimethoxycinnamyl alcohol (Z-DMC) and Z-CF also in an approximately 1:1 ratio. Thus, there are three types of binary combinations of rectal phenylpropanoid volatiles (i.e. DMP + E-CF; DMP + Z-CF; Z-CF + Z-DMC) utilized among the four Bactrocera species. Such differences in phenylpropanoid ingredients may play a critical role in differentiating these species if encountered in the natural habitat. In this context, the two putative sibling species—B. invadens and B. dorsalis, possess the identical subset of rectal volatiles (DMP and E-CF) in a similar proportion. Furthermore, the phylogenetic analyses of the four Bactrocera species by comparing nucleotide sequences in the mitochondrial genes showed that B. invadens clearly belonged to the same clade as B. dorsalis species. Therefore, we consider the two as the same biological species, and certainly not distinct.
Similar content being viewed by others
References
Akhila A (2009) Chemistry and biogenesis of essential oil from the genus Cymbopogon, chap. 2. In: Akhila A (ed) Essential oil bearing grasses: the genus Cymbopogon. CRC Press, Boca Raton, pp 20–106
Barnes BN (2004) In: Proceedings of the 6th international symposium on fruit flies of economic importance. Isteg Scientific Publications, South Africa, 510 pp
Bezzi M (1915) On the fruit-flies of the genus Dacus (s. 1.) occurring in India, Burma, and Ceylon. Bull Entomol Res 7:99–121
Carroll LE, White IM, Freidberg A, Norrbom AL, Dallwitz MJ, Thompson FC (2006) Pest fruit flies of the world. Version: 8th December 2006. http://delta-intkey.com
Christenson LD, Foote RH (1960) Biology of fruit flies. Annu Rev Entomol 5:171–192
Clarke AR, Armstrong KF, Carmichael AE, Mine JR, Raghu S, Roderick GK, Yeates DK (2005) Invasive phytophagous pests arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis Complex of fruit flies. Annu Rev Entomol 50:293–319
Ekesi S, Nderitu PW, Chang CL (2007) Adaptation to and small-scale rearing of invasive fruit fly Bactrocera invadens (Diptera: Tephritidae) on artificial diet. Ann Entomol Soc Am 100:562–567
Fletcher BS (1987) The biology of Dacine fruit flies. Annu Rev Entomol 32:115–144
Gilbert A, Cannon C (2007) 2006 Peach fruit fly eradication in Fresno. Abstract, 9th exotic fruit fly symposium, Fresno, California, 25–26 April, 2007, p 19
Hamilton BA, Zinn K (1994) From clone to mutant gene. Methods Cell Biol 44:81–94
Hee AKW, Tan KH (1998) Attraction of female and male Bactrocera papayae to conspecific males fed with methyl eugenol and attraction of females to male sex pheromone components. J Chem Ecol 24:753–764
Hee AKW, Tan KH (2006) Transport of methyl eugenol-derived sex pheromonal components in the male fruit fly, Bactrocera dorsalis. Comp Biochem Physiol Part C 143:422–428
Hoffman KM (2007) Update on exotic fruit fly detections in California 2005–2007. Abstract, 9th exotic fruit fly symposium, Fresno, California 25–26 April, 2007, p 18
Howlett FM (1912) VII. The effect of oil of Citronella on two species of Dacus. Trans Entomol Soc Lond 1912:412–418
Howlett FM (1915) Chemical reactions of fruit-flies. Bull Entomol Res 6:297–305
IAEA (2000) Action Plan–peach fruit fly, Bactrocera zonata (Saunders) Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture. International Atomic Energy Agency, Vienna, p 50
IAEA (2003) Trapping guidelines for area-wide fruit fly programmes Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture. International Atomic Energy Agency, Vienna, p 47
Iwahashi O, Routhier W (2001) Aedeagal length and its variation of the peach fruit fly. Bactrocera zonata (Saunders) (Diptera: Tephritidae), which recently invaded Egypt. Appl Entomol Zool 36:13–17
Khoo CCH, Tan KH (2005) Rectal gland of Bactrocera papayae: ultrastructure, anatomy and sequestration of auto fluorescent compounds upon methyl eugenol consumption by the male fly. Microsc Res Tech 67:219–226
Khoo CCH, Yuen KH, Tan KH (2000) Attraction of female Bactrocera papayae to sex pheromone components with two different release devices. J Chem Ecol 26:2487–2496
McInnis DO, Rendon P, Jang EB, Van Saruers-Muller A, Sugayama R, Malavasi A (1999) Interspecific mating of introduced, sterile Bactrocera dorsalis with wild B. carambolae (Diptera: Tephritidae) in Suriname: a potential case for cross-species sterile insect technique. Ann Entomol Soc Am 92:758–765
McPheron BA, Steck GJ (eds) (1996) Fruit fly pests: a world assessment of their biology and management. St. Lucie Press, Florida, p 586
Medina FIS, Carillo PAV, Gregorio JS, Aguillar CP (1998) The mating compatibility between Bactrocera philippinensis and Bactrocera dorsalis, In: Abstracts of 5th international symposium on fruit flies of economic importance, June 1–5, 1998, Penang, Malaysia, p 155
Metcalf RL (1990) Chemical ecology of Dacinae fruit flies (Diptera: Tephritidae). Ann Entomol Soc Am 83:1017–1030
Metcalf RL, Kogan M (1987) Plant volatiles as insect attractants. CRC Critic Rev Plant Sci 5:251–301
Muraji M, Nakahara S (2001) Phylogenetic relationships among fruit flies, Bactrocera (Diptera, Tephritidae), based on the mitochondrial rDNA sequences. Insect Mol Biol 10:549–559
Naeole CKM, Haymer DS (2003) Use of oligonucleotide arrays for molecular taxonomic studies of closely related species in the Oriental fruit fly (Bactrocera dorsalis) complex. Mol Ecol Notes 3:662–665
Nishida R, Tan KH, Serit M, Lajis NH, Sukari AM, Takahashi S, Fukami H (1988a) Accumulation of phenylpropanoids in the rectal glands of males of the Oriental fruit fly, Dacus dorsalis. Experientia 44:534–536
Nishida R, Tan KH, Fukami H (1988b) cis-3, 4-Dimethoxycinnamyl alcohol from the rectal glands of male Oriental fruit fly, Dacus dorsalis. Chem Express 3:207–210
Nishida R, Shelly TE, Kaneshiro KY, Tan KH (2000) Roles of semiochemicals in mating systems: a comparison between oriental fruit fly and medfly. In: Tan KH (ed) Area-wide control of fruit flies and other insect pests. Penerbit USM, Penang, pp 631–637
Orankanok W, Chinvinijkul S, Thanaphum S, Sitilob P, Enkerlin WR (2007) Area-wide integrated control of oriental fruit fly Bactrocera dorsalis and guava fruit fly Bactrocera correcta in Thailand. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests. Springer, The Netherlands, pp 517–526
Orankanok W, Chinvinijkul S, Sawatwangkhoungm A, Pinkaew S, Orankanok S (2009) Application of chemical supplements to enhance Bactrocera dorsalis and B. correcta sterile males performance in Thailand. In: Fourth FAO/IAEA research co-ordination meetings on “improving sterile male performance in fruit fly SIT Programmes” 21–25 September 2009, Péreybère, Mauritius
Page RDM (1996) TREEVIEW: An application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358
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 16:2475–2487
Poramarcom R, Baimai V (1996) Sexual behavior and signals used for mating of Bactrocera correcta. In: McPheron BA, Steck GJ (eds) Fruit fly pests: a world assessment of their biology and management. St. Lucid Press, Florida, pp 51–58
Quilici S, Duyck PF, Franck A (2004) Preliminary experiments on the influence of exposure to methyleugenol on mating success of males in the peach fruit fly, Bactrocera zonata. In: 1st RCM on improving sterile male performance in fruit fly SIT, Antigua, Guatemala, 25–29 October, 2004
Shelly TE, Dewire A-LM (1994) Chemically mediated mating success in male Oriental fruit flies (Diptera: Tephritidae). Ann Entomol Soc Am 87:375–382
Shelly TE, Dewire A-LM (2000) Flower-feeding affects mating performance in male Oriental fruit flies (Diptera: Tephritidae). Ecol Entomol 25:109–114
Shelly TE, Nishida R (2004) Larval and adult feeding on methyl eugenol and the mating success of male oriental fruit flies, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Entomol Exp Appl 112:155–158
Sookar P, Alleck M, Ahseek N, Khayrattee FB, Permalloo S (2009) Improving male reproductive performance of Bactrocera zonata and Bactrocera cucurbitae. In: Fourth FAO/IAEA research co-ordination meetings on “improving sterile male performance in fruit fly SIT Programmes” 21–25 September 2009, Péreybère, Mauritius
Steck GJ (2002) Pest alert: a guava fruit fly Bactrocera correcta (Bezzi) (Tephritidae). http://www.doacs.state.fl.us/pi/enpp/ento/bcorrecta.html
Sugayama R, Zucchi RA, Ovruski SM, Sivinski J (eds) (2008) Fruit flies of economic importance: from basic to applied knowledge. Biofabrics Moscamed Brasil, Salvador, p 351
Tan KH (ed) (2000a) Area-wide control of fruit flies and other insect pests. Penerbit USM, Penang, p 782
Tan KH (2000b) Behaviour and chemical ecology of fruit flies. In: Tan KH (ed) Area-wide control of fruit flies and other insect pests. Penerbit USM, Penang, pp 647–656
Tan KH (2003) Interbreeding and DNA analysis of sibling species within the Bactrocera dorsalis complex. In: Recent trends on sterile insect technique and area-wide integrated pest management—economic feasibility, control projects, farmer organization and Bactrocera dorsalis complex control study. Research Institute for subtropics, Okinawa, pp 113–122
Tan KH (2009) Fruit fly pests as pollinators of wild orchids. Orchid Digest 73:180–187
Tan KH, Nishida R (1996) Sex pheromone and mating competition after methyl eugenol consumption in the Bactrocera dorsalis complex. In: McPheron BA, Steck GJ (eds) Fruit fly pests—a world assessment of their biology and management. St. Lucid Press, Florida, pp 147–153
Tan KH, Nishida R (1998) Ecological significance of male attractant in the defence and mating strategies of the fruit fly, Bactrocera papayae. Entomol Exp Appl 89:155–158
Tan KH, Nishida R, Toong YC (2002) Floral synomone of a wild orchid, Bulbophyllum cheiri, lures Bactrocera fruit flies for pollination. J Chem Ecol 28:1161–1172
Tan KH, Tan LT, Nishida R (2006) Floral phenylpropanoid cocktail and architecture of Bulbophyllum vinaceum orchid in attracting fruit flies for pollination. J Chem Ecol 32:2429–2441
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Tokushima I, Orankanok W, Tan KH, Nishida R (2010) Accumulation of phenylpropanoid and sesquiterpenoid volatiles in male rectal pheromonal glands of the fruit fly, Bactrocera correcta. J Chem Ecol 36:1–8. doi: 10.1007/s10886-010-9874-3. http://www.springerlink.com/content/k3877018132rrr07
Wee SL, Tan KH (2000) Sexual maturity and intraspecific mating success of two sibling species of the Bactrocera dorsalis complex. Entomol Exp Appl 94:133–139
Wee SL, Tan KH (2001) Allomonal and hepatotoxic effects following methyl eugenol consumption in Bactrocera papayae male against Gekko monarchus. J Chem Ecol 27:953–964
Wee SL, Tan KH (2005) Evidence of natural hybridization between two sympatric sibling species of Bactrocera dorsalis complex based on pheromone analysis. J Chem Ecol 31:845–858
Wee SL, Tan KH (2007) Temporal accumulation of phenylpropanoids in male fruit flies, Bactrocera dorsalis and B. carambolae (Diptera: Tephritidae) following methyl eugenol consumption. Chemoecology 17:81–85
Wee SL, Tan KH, Nishida R (2007) Pharmacophagy of methyl eugenol by males enhances sexual selection of Bactrocera carambolae. J Chem Ecol 33:1272–1282
Zimowska GJ, Handler AM (2005) PiggyBac transposons in Bactrocera dorsalis and their use for species identification. In: Abstract in eight exotic fruit fly symposium, California, March 2005
Acknowledgments
The authors would like to thank Andrew Jessup (FAO/IAEA Agriculture and Biotechnology Laboratory, Seibersdorf, Austria), W. Orankanok and S. Chinvinijkul (Department of Agricultural Extension, Bangkok), and S. Permalloo (Entomology Division, Ministry of AgroIndustry & Fisheries, Mauritius), for the supply of sexually mature live male flies of B. invadens, B. correcta, and B. zonata, respectively. Their kind assistance in enabling K. H. Tan to perform rectal gland extractions and preservations in their respective countries is also appreciated. K. H. Tan also acknowledges J. Hendrichs of IAEA and L. T. Tan of University College London for the indirect financial support in his travels to Austria and Mauritius, respectively. We also thank S. Ekesi and S. M. Faris of the International Centre of Insect Physiology and Ecology, Nairobi, for the individually preserved wild males of B. invadens. This work was partly supported by the Grant-in-Aid for Scientific Research from JSPS (No. 19310142) from the Ministry of Education, Culture, Sports, Science and Technology of Japan, and JST in Research for Promoting Technological Seeds (under R. Nishida).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tan, K.H., Tokushima, I., Ono, H. et al. Comparison of phenylpropanoid volatiles in male rectal pheromone gland after methyl eugenol consumption, and molecular phylogenetic relationship of four global pest fruit fly species: Bactrocera invadens, B. dorsalis, B. correcta and B. zonata . Chemoecology 21, 25–33 (2011). https://doi.org/10.1007/s00049-010-0063-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00049-010-0063-1