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Attraction and consumption of methyl eugenol by male Bactrocera umbrosa Fabricius (Diptera: Tephritidae) promotes conspecific sexual communication and mating performance

Published online by Cambridge University Press:  19 June 2017

S.L. Wee ,
M.Z. Abdul Munir  and
A.K.W. Hee
S.L. Wee*
Affiliation:
School of Environmental and Natural Resource Sciences, Universiti Kebangsaan Malaysia, Bangi 43600, Selangor Darul Ehsan, Malaysia Centre of Insect Systematics, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, Bangi 43600, Selangor Darul Ehsan, Malaysia
M.Z. Abdul Munir
Affiliation:
School of Environmental and Natural Resource Sciences, Universiti Kebangsaan Malaysia, Bangi 43600, Selangor Darul Ehsan, Malaysia
A.K.W. Hee
Affiliation:
Department of Biology, Faculty of Science, Universiti Putra Malaysia, Serdang 43400, Selangor Darul Ehsan, Malaysia
*
*Author for correspondence: Tel: +(603) 8921-5925 Fax: +(603) 8925-3357 E-mail: slwee@ukm.edu.my
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Abstract

The Artocarpus fruit fly, Bactrocera umbrosa (Fabricius) (Diptera: Tephritidae), is an oligophagous fruit pest infesting Moraceae fruits, including jackfruit (Artocarpus heterophyllus Lamarck), a fruit commodity of high value in Malaysia. The scarcity of fundamental biological, physiological and ecological information on this pest, particularly in relation to behavioural response to phytochemical lures, which are instrumental to the success of many area-wide fruit fly control and management programmes, underpins the need for studies on this much-underrated pest. The positive response of B. umbrosa males to methyl eugenol (ME), a highly potent phytochemical lure, which attracts mainly males of many Bactrocera species, was shown to increase with increasing age. As early as 7 days after emergence (DAE), ca. 22% of males had responded to ME and over 50% by 10 DAE, despite no occurrence of matings (i.e. the males were still sexually immature). Male attraction to ME peaked from 10 to 27 DAE, which corresponded with the flies’ attainment of sexual maturity. In wind-tunnel assays during the dusk courtship period, ME-fed males exhibited earlier calling activity and attracted a significantly higher percentage of virgin females compared with ME-deprived males. ME-fed males enjoyed a higher mating success than ME-deprived males at 1-day post ME feeding in semi-field assays. ME consumption also promotes aggregation behaviour in B. umbrosa males, as demonstrated in wind-tunnel and semi-field assays. We suggest that ME plays a prominent role in promoting sexual communication and enhancing mating performance of the Artocarpus fruit fly, a finding that is congruent with previous reports on the consequences of ME acquisition by other economically important Bactrocera species.

Keywords

Artocarpus fruit flymethyl eugenolattractionsexual maturationmating competitiveness
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 1 , February 2018 , pp. 116 - 124
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Copyright
Copyright © Cambridge University Press 2017 

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References

Allwood, A.J. (1997) Biology and ecology: pre-requisite for understanding and managing fruit flies (Diptera: Tephritidae). pp. 95–101 in Allwood, A.J. & Drew, R.A.I. (Eds) Management of Fruit Flies in the Pacific: A Regional Symposium. ACIAR Proceedings No. 76. Canberra, Australian Centre for International Agricultural Research.Google Scholar
Allwood, A.J., Chinajariyawong, A., Drew, R.A.I., Hameck, E.L., Hancock, D.L., Hengsawad, J.C., Jipanin, M., Kon Krong, C., Kritsaneepaiboon, S., Leong, C.T.S. & Vijaysegaran, S. (1999) Host plant records for fruit flies (Diptera: Tephritidae) in South East Asia. Raffles Bulletin of Zoology 47(Suppl. 7), 1–92.Google Scholar
Anscombe, F.J. (1948) The transformation of Poisson, binomial andnegative binomial data. Biometrika 35, 246–254.Google Scholar
Boppré, M. (1984) Redefining “pharmacophagy”. Journal of Chemical Ecology 10, 1151–1154.CrossRefGoogle ScholarPubMed
Clarke, A.R., Allwood, A.J., Chinajariyawong, A., Drew, R.A.I., Hengsawad, C., Jirasurat, M., Kong Krong, C., Kritsaneepaiboon, S. & Vijaysegaran, S. (2001) Seasonal abundance and host use patterns of seven Bactrocera MacQuart species (Diptera: Tephritidae) in Thailand and Peninsular Malaysia. Raffles Bulletin of Zoology 49, 207–220.Google Scholar
Clarke, A.R., Powell, K.S., Weldon, C.W. & Taylor, P.W. (2011) The ecology of Bactrocera tryoni (Diptera: Tephritidae): what do we know to assist pest management? Annals of Applied Biology 158, 26–54.Google Scholar
Drew, R.A.I., Hooper, G.H.S. & Bateman, M.A. (1982) Economic Fruit Flies of the South Pacific Region. 2nd edn. Brisbane, Queensland Department of Primary Industries.Google Scholar
Emlen, S.T. & Oring, L.W. (1977) Ecology, sexual selection and the evolution of mating systems. Science 197, 215–223.CrossRefGoogle ScholarPubMed
Fiske, P., Rintamaki, P.T., & Karvonen, E. (1998) Mating success in lekking males: a meta-analysis. Behavioral Ecology 9, 328–338.CrossRefGoogle Scholar
Fletcher, B.S. (1987) The biology of dacine fruit flies. Annual Review of Entomology 32, 115–144.CrossRefGoogle Scholar
Haq, N. (2006) Jackfruit, Artocarpus heterophyllus. Southampton, UK, Southampton Centre for Underutilised Crops, University of Southampton. 192 p.Google Scholar
Hardy, D.E. (1973) The fruit flies (Tephritidae – Diptera) of Thailand and bordering countries. Pacific Insects Monograph 31, 1–353.Google Scholar
Hee, A.K.W. & Tan, K.H. (1998) Attraction of female and male Bactrocera papayae to conspecific males fed with methyl eugenol and attraction of females to male sex pheromone components. Journal of Chemical Ecology 24, 753–764.Google Scholar
Hendrichs, J., Vreysen, M.J.B., Robinson, A.S. & Kenmore, P. (2007) Area-wide integrated pest management (AW-IPM): principles, practice and prospects. pp. 3–33 in Vreysen, M.J.B., Robinson, A.S. & Hendrichs, J. (Eds) Area-Wide Control of Insect Pests – from Research to Field Implementation. Netherlands, Springer.Google Scholar
Kaspi, R. & Yuval, B. (1999) Mediterranean fruit fly leks: factors affecting male location. Functional Ecology 13, 539–545.CrossRefGoogle Scholar
Kennedy, J.S. & Marsh, D. (1974) Pheromone-regulated anemotaxis in flying moths. Science 184, 999–1001.Google Scholar
Khoo, C.C.H. & Tan, K.H. (2000) Attraction of both sexes of melon fly, Bactrocera cucurbitae to conspecific males – a comparison after pharmacophagy of cue-lure and a new attractant – zingerone. Entomologia Experentalis et Applicata 97, 317–320.CrossRefGoogle Scholar
Koyama, J., Kakinohana, H. & Miyatake, T. (2004) Eradication of the melon fly, Bactrocera cucurbitae, in Japan: importance of behavior, ecology, genetics and evolution. Annual Review of Entomology 49, 331–349.Google Scholar
Kumaran, N.K., Balagawi, S., Schutze, M. & Clarke, A.R. (2013) Evolution of lure response in tephritid fruit flies: phytochemicals as drivers of sexual selection. Animal Behavior 85, 781–789.CrossRefGoogle Scholar
Kumaran, N.K., Prentis, P., Mangalam, K.P., Schutze, M.K. & Clarke, A.R. (2014 a) Sexual selection in true fruit flies (Diptera: Tephritidae): transcriptome and experimental evidences for phytochemicals increasing male competitive ability. Molecular Ecology 23, 4645–4657.CrossRefGoogle ScholarPubMed
Kumaran, N.K., Hayes, R.A. & Clarke, A.R. (2014 b) Cuelure but not zingerone make the sex pheromone of male Bactrocera tryoni (Tephritidae: Diptera) more attractive to females. Journal of Insect Physiology 68, 36–43.Google Scholar
McInnis, D.O., Rendon, P., Jang, E.B., van Sauers-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. Annals of Entomological Society of America 92, 758–765.Google Scholar
Mengersen, K., Quinlan, M.M., Whittle, P.J.L., Knight, J.D., Mumford, J.D., Wan Ismail, W.N., Tahir, H., Holt, J., Leach, A.W., Johnson, S., Sivapragrasam, A., Lum, K.Y., Sue, M.J., Othman, Y., Jumaiyah, L., Tu, D.M., Anh, N.T., Pradyabumrung, T., Salyapongse, C., Marasigan, L.Q., Palacpac, M.B., Dulce, L., Panganiban, G.G.F., Soriano, T.L., Carandang, E. & Hermawan., (2012) Beyond compliance: project on an integrated systems approach for pest risk management in South East Asia. EPPO Bulletin 42, 109–116.CrossRefGoogle Scholar
Michaux, B. & White, I.M. (1999) Systematics and biogeography of southwest Pacific Bactrocera (Diptera: Tephritidae: Dacini). Palaeogeography, Palaeoclimatology, Palaeoecology 153, 337–351.Google Scholar
Ooi, Y.T. & Wee, S.L. (2016) Sexual maturation, mating propensity and remating incidence of Zeugodacus tau (Walker) (Diptera: Tephritidae). Journal of Asia-Pacific Entomology 19, 451–457.CrossRefGoogle Scholar
Orankanok, W., Chinvinijkul, S., Sawatwangkhoungm, A., Pinkaew, S. & Orankanok, S. (2009) Application of chemical supplements to enhance Bactrocera dorsalis and B. correcta sterile male 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.Google Scholar
Qureshi, Z.A., Bughio, A.R. & Siddiqui, Q.H. (1981) Population suppression of fruit fly, Dacus zonata (Saund.) (Diptera, Tephritidae) by male annihilation technique and its impact on fruit infestation. Journal of Applied Entomology 91, 521–524.Google Scholar
Raghu, S. & Clarke, A.R. (2003) Spatial and temporal partitioning of behaviour by adult dacines: direct evidence for methyl eugenol as a mate rendezvous cue for Bactrocera cacuminata . Physiological Entomology 28, 175–184.CrossRefGoogle Scholar
Roitberg, B.D. (2007) Why pest management needs behavioral ecology and vice versa. Entomological Research 37, 14–18.CrossRefGoogle Scholar
Shelly, T.E. (2000). Male signaling and lek attractiveness in the Mediterranean fruit fly. Animal Behaviour 60, 245–251.Google Scholar
Shelly, T.E. (2001). Lek size and female visitation in two species of tephritid fruit flies. Animal Behaviour 62, 33–40.CrossRefGoogle Scholar
Shelly, T.E. (2010) Effects of methyl eugenol and raspberry ketone/cue lure on the sexual behavior of Bactrocera species (Diptera: Tephritidae). Applied Entomology and Zoology 45, 349–361.Google Scholar
Shelly, T.E. & Dewire, A.M. (1994) Chemically mediated mating success in male oriental fruit flies (Diptera: Tephritidae). Annals of Entomological Society of America 87, 375–382.Google Scholar
Shelly, T.E. & Kaneshiro, K.Y. (1991). Lek behaviour of the oriental fruit fly in Hawaii. Journal of Insect Behavior 4, 235–241.CrossRefGoogle Scholar
Shelly, T.E. & Whittier, T.S. (1997). Lek behavior of insects. The evolution of mating systems in insects and arachnids. pp. 273–292 in Choe, J.C. & Crespi, B.J. (Eds) The Evolution of Mating Systems in Insects and Arachnids. Cambridge, Cambridge.CrossRefGoogle Scholar
Shelly, T.E., Edu, J. & McInnis, D.O. (2010) Pre-release consumption of methyl eugenol increases the mating competitiveness of sterile males of the oriental fruit fly, Bactrocera dorsalis, in large field enclosures. Journal of Insect Science 10, 8.Google Scholar
Sookar, P., Alleck, M., Ahseek, N., Khayrattee, F.B. & 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.Google Scholar
Tan, K.H. (1985) Estimation of natiye populations of male Dacus spp. by Jolly's stochastic method using a new designed attractant trap in a village ecosystem. Journal of Plant Protection in the Tropics 2, 87–95.Google Scholar
Tan, K.H. & Jaal, Z. (1986) Comparison of male adult population densities of the Oriental and Artocarpus fruit flies, Dacus spp. (Diptera: Tephritidae), in two nearby villages in Penang, Malaysia. Research on Population Ecology 28, 85–89.Google Scholar
Tan, K.H. & Nishida, R. (1996) Sex pheromone and mating competiton after methyl eugenol consumption in the Bactrocera dorsalis complex. pp. 147–153 in McPheron, B.A. & Steck, G.A. (Eds) Fruit Fly Pests: A World Assessment of their Biology and Management. Delray Beach, Florida, St. Lucie Press.Google Scholar
Tan, K.H. & Nishida, R. (1998) Ecological significance of male attractant in the defence and mating strategies of the fruit fly pest, Bactrocera papayae . Entomologia Experimentalis et Applicata 89, 155–158.Google Scholar
Tan, K.H. & Nishida, R. (2012) Methyl eugenol: Its occurrence, distribution, and role in nature, especially in relation to insect behavior and pollination. Journal of Insect Science 12, 56.CrossRefGoogle ScholarPubMed
Tan, K.H., Tokushima, I., Ono, H. & Nishida, R. (2011) 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.Google Scholar
Vagalo, M., Hollingsworth, R. & Tsatsia, F. (1997) Fruit fly fauna in Solomon Islands. pp. 81–86 in Allwood, A.J. & Drew, R.A I. (Eds) Management of Fruit Flies in the Pacific. Canberra, Australian Centre for International Agricultural Research.Google Scholar
Vargas, R.I., Stark, J.D., Kido, M.H., Ketter, H.M. & Whitehand, L.C. (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. Journal of Economic Entomology 93, 81–87.Google Scholar
Vargas, R.I., Piňero, J.C., Mau, R.F.L., Jang, E.B., Klungness, L.M., McInnis, D.O., Harris, E.B., McQuate, G.T., Bautista, R.C. & Wong, L. (2010) Area-wide suppression of the Mediterranean fruit fly, Ceratitis capitata, and the Oriental fruit fly, Bactrocera dorsalis, in Kamuela, Hawaii. Journal of Insect Science 10, 135.Google Scholar
Vijaysegaran, S. (1988) The current situation on fruit flies in Peninsular Malaysia. pp. 125–139 in Proceedings of the First International Symposium on Fruit Flies in the Tropics, Kuala Lumpur, 14–16 March 1988 Malaysia.Google Scholar
Walker, G.P., Vueti, E.T., Hamacek, E.L. & Allwood, A.J. (1997) Laboratory-rearing techniques for tephritid fruit flies in the South Pacific. pp. 145–152 in Allwood, A.J. & Drew, R.A.I. (Eds) Management of Fruit Flies in the Pacific. Canberra, Australian Centre for International Agricultural Research.Google Scholar
Wee, S.L. & Tan, K.H. (2000) Sexual maturity and intraspecific mating success of two sibling species of the Bactrocera dorsalis complex. Entomologia Experimentalis et Applicata 94, 133–139.Google Scholar
Wee, S.L. & Tan, K.H. (2005) Female sexual response to male rectal volatile constituents in the fruit fly Bactrocera carambolae (Diptera: Tephritidae). Applied Entomology and Zoology 40, 365–372.CrossRefGoogle Scholar
Wee, S.L., Tan, K.H. & Nishida, R. (2007) Pharmacophagy of methyl eugenol by males enhances sexual selection of Bactrocera carambolae . Journal of Chemical Ecology 33, 1272–1282.CrossRefGoogle ScholarPubMed
Wong, T.T.Y., Couey, H.M. & Nishimoto, J.I. (1982) Oriental fruit fly: sexual development and mating response of laboratory-reared and wild flies. Annals of Entomological Society of America 75, 191–194.Google Scholar
Wong, T.T.Y., McInnis, D.O. & Nishimoto, J.I. (1989) Relationship of sexual maturation rate to response of oriental fruit fly strains (Diptera: Tephritidae) to methyl eugenol. Journal of Chemical Ecology 15, 1939–1405.Google Scholar