Abstract
The Oriental fruit fly, Bactrocera dorsalis (Hendel) is an economically devastating pest of fruit crops across the globe with stringent quarantine restrictions to limit its further spread. The current management programs increasingly depend on male annihilation but trapping female flies is equally important to reduce fruit damage. Considering the importance of kairomones in courtship and oviposition site selection behavior of B. dorsalis, the aim of this work was to isolate and identify potential cues from the volatiles of arils of jackfruit, Artocarpus heterophyllus. Using olfactometer assays and gas-chromatography linked to electroantennographic detection, attraction of both female and male B. dorsalis to specific jackfruit volatiles was demonstrated. Ethyl 3-methylbutanoate, ethyl hexanoate, pentyl butanote, 2-methylbutyl 3-methylbutanoate, 2-methylpropyl hexanoate, (Z)-3-hexenyl 3-methylbutanoate and dodecanal were found to attract female B. dorsalis specifically. Butyl acetate, 2 phenylethanol and pentyl 3-methylbutanoate elicited attraction in male B. dorsalis only. Synthetic blends of these compounds were found to attract female and male B. dorsalis in laboratory as well as field conditions. Using specific cues common to each set, a blend of methyl 3-methylbutanoate, butyl acetate, 3-methylbutyl acetate and hexyl acetate attracted both sexes of B dorsalis. This study demonstrates the use of kairomone-based lures for sex-specific as well as bisexual attraction for the first time.
Similar content being viewed by others
References
Alm SR, Hall FR, Ladd TL, Williams RN (1985) A chemical attractant for Glischrochilus quadrisignatus (Coleoptera: Nitidulidae). J Econ Entomol 78:839–843. https://doi.org/10.1093/jee/78.4.839
Alm SR, Hall FR, McGovern TP, Williams RN (1986) Attraction of Glischrochilus quadrisignatus (Coleoptera: Nitidulidae) to semiochemicals: butyl acetate and propyl propionate. J Econ Entomol 79:654–658. https://doi.org/10.1093/jee/79.3.654
Anfora G, Tasin M, De Cristofaro A et al (2009) Synthetic grape volatiles attract presumably mated Lobesia botrana females in laboratory and field bioassays. J Chem Ecol 35:1054–1062. https://doi.org/10.1007/s10886-009-9686-5
Armstrong KF, Cameron CM, Frampton ER (1997) Fruit fly (Diptera: Tephritidae) species identification: a rapid molecular diagnostic technique for quarantine application. Bull Entomol Res 87:111–118. https://doi.org/10.1017/s0007485300027243
Arthikirubha A, Kamala Jayanthi PD, Sridhar V, Verghese A (2017) Local host fruiting pattern and climate variations impact on fruit fly (Bactrocera dorsalis) population trends: a regional fruit fly population tracker for management options. Indian J Agric Sci 87:1460–1465
Beauchamp PS, Chea E, Dimaano JG, Dev V, Ly B, Miranda AE, Whaley WH (2009) Essential oil composition of six Lomatium species attractive to indra swallowtail butterfly Papilio indra: principal component analysis against essential oil composition of Lomatium dissectum var. multifidum. J Essent Oil Res 21:535–542. https://doi.org/10.1080/10412905.2009.9700238
Biasazin TD, Larsson Herrera S, Kimbokota F, Dekker T (2019) Translating olfactomes into attractants: shared volatiles provide attractive bridges for polyphagy in fruit flies. Ecol Lett 22:108–118. https://doi.org/10.1111/ele.13172
Cha DH, Adams T, Werle CT, Sampson BJ, Adamczyk JJ Jr, Rogg H, Landolt PJ (2014) A four-component synthetic attractant for Drosophila suzukii (Diptera: Drosophilidae) isolated from fermented bait headspace. Pest Manag Sci 70:324–331. https://doi.org/10.1002/ps.3568
Clarke AR, Armstrong KF, Carmichael AE, Milne 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. https://doi.org/10.1146/annurev.ento.50.071803.130428
Cornelius ML, Nergel L, Duan JJ, Messing RH (2000) Responses of female oriental fruit flies (Diptera: Tephritidae) to protein and host fruit odors in field cage and open field tests. Environ Entomol 29:14–19. https://doi.org/10.1603/0046-225x-29.1.14
Cruz-López L, Malo EA, Toledo J, Virgen A, del Mazo A, Rojas JC (2006) A new potential attractant for Anastrepha obliqua from Spondias mombin fruits. J Chem Ecol 32:351–365. https://doi.org/10.1007/s10886-005-9006-7
Egonyu JP, Torto B (2018) Responses of the ambrosia beetle Xylosandrus compactus (Coleoptera: Curculionidea: Scolytinae) to volatile constituents of its symbiotic fungus Fusarium solani (Hypocreales: Nectriaceae). Arthropod Plant Interact 12:9–20. https://doi.org/10.1007/s11829-017-9552-2
Eiceman GA, Tadjikov B, Krylov E, Nazarov EG, Miller RA, Westbrook J, Funk P (2001) Miniature radio-frequency mobility analyzer as a gas chromatographic detector for oxygen-containing volatile organic compounds, pheromones and other insect attractants. J Chromatogr A 917:205–217. https://doi.org/10.1016/S0021-9673(01)00656-2
El-Sayed AM, Byers JA, Manning LM et al (2008) Floral scent of Canada thistle and its potential as a generic insect attractant. J Econ Entomol 101:720–727. https://doi.org/10.1093/jee/101.3.720
Hendrichs J, Teresa Vera M, De Meye M, Clarke AR (2015) Resolving cryptic species complexes of major tephritid pests. Zookeys 540:5–39. https://doi.org/10.3897/zookeys.540.9656
Jacobson M, Lilly CE, Harding C (1968) Sex attractant of sugar beet wireworm: identification and biological activity. Science 159:208–210. https://doi.org/10.1126/science.159.3811.208
Jain SC, Dussourd DE, Conner WE, Eisner T, Guerrero A, Meinwald J (1983) Polyene pheromone components from an arctiid moth (Utetheisa ornatrix): characterization and synthesis. J Org Chem 48:2266–2270. https://doi.org/10.1021/jo00161a024
Jang EB, Carvalho LA, Stark JD (1997) Attraction of female oriental fruit fly, Bactrocera dorsalis, to volatile semiochemicals from leaves and extracts of a non-host plant, Panax (Polyscias guilfoylei) in laboratory and olfactometer assays. Can Field-Naturalist 111:1389–1401
Jantz Orlo K, Gerta RF, Wells MT (1967) Automobile Paint Effective as an Insect Attractant. Science 156:946–947
Jürgens A, Webber AC, Gottsberger G (2000) Floral scent compounds of Amazonian Annonaceae species pollinated by small beetles and thrips. Phytochemistry 55:551–558. https://doi.org/10.1016/S0031-9422(00)00241-7
Jürgens A, Witt T, Gottsberger G (2003) Flower scent composition in Dianthus and Saponaria species (Caryophyllaceae) and its relevance for pollination biology and taxonomy. Biochem Syst Ecol 31:345–357. https://doi.org/10.1016/S0305-1978(02)00173-4
Kamala Jayanthi PD, Verghese A (2011) Host-plant phenology and weather-based forecasting models for population prediction of the oriental fruit fly, Bactrocera dorsalis (Hendel). Crop Protect 30:1557–1562
Kamala Jayanthi PD, Woodcock CM, Caulfield J, Birkett MA, Bruce TJA (2012) Isolation and identification of host cues from mango, Mangifera indica, that attract sexually maturesexually mature female oriental fruit fly, Bactrocera dorsalis. J Chem Ecol 38:361–369. https://doi.org/10.1007/s10886-012-0093-y
Kamala Jayanthi PD, Kempraj V, Aurade RM, Venkataramanappa RK, Nandagopal B, Verghese A, Bruce TJA (2014) Specific volatile compounds from mango elicit oviposition in sexually maturesexually mature Bactrocera dorsalis females. J Chem Ecol 40:259–266. https://doi.org/10.1007/s10886-014-0403-7
Kamala Jayanthi PD, Aurade RM, Kempraj V et al (2015) Salicylic acid induces changes in mango fruit that affect oviposition behavior and development of the oriental fruit fly, Bactrocera dorsalis. PLoS One 10:1–18. https://doi.org/10.1371/journal.pone.0139124
Kloczko M, et al (2003) Device for luring and catching insects. United States patent US 6505434 B1
Knight AL, Light DM (2001) Attractants from Bartlett pear for codling moth, Cydia pomonella (L.), larvae. Naturwissenschaften 88:339–342. https://doi.org/10.1007/s001140100244
Kovats E (1965) Gas chromatographic characterization of organic substances in the retention index system. Adv Chromatogr 1:229–247
Leskey TC, Prokopy RJ, Wright SE, Phelan PL, Haynes LW (2001) Evaluation of individual components of plum odor as potential attractants for adult plum Curculios. J Chem Ecol 27:1–17. https://doi.org/10.1023/A:1005667430877
Lugemwa FN, Lwande W, Bentley MD, Mendel MJ, Alford AR (1989) Volatiles of wild blueberry, vaccinium angustifolium: possible attractants for the blueberry maggot fruit fly, Rhagoletis mendax. J Agric Food Chem 37:232–233. https://doi.org/10.1021/jf00085a053
Metcalf R, Kogan M (1987) Plant volatiles as insect attractants. CRC Crit Rev Plant Sci 5:251–301. https://doi.org/10.1080/07352688709382242
Patrick FDOWD, Bartelt RJ (1991) Pheromone synergists for Carpophilus hemipterus I 17: 285–308.
Peschke K (1983) Defensive and pheromonal secretion of the tergal gland of Aleochara curtula II. Release and inhibition of male copulatory behavior. J Chem Ecol 9:13–31. https://doi.org/10.1007/BF00987767
Pettersson J (1970) An aphid sex attractant. Entomol Scand 1:63–73
Pow EM, Bennison JA, Birkett MA, Luszniak MJ, Manjunatha M, Pickett JA, Segers IS, Wadhams LJ, Wardlow LR, Woodcock CM (1999) Behavioural responses of western flower thrips (Frankliniella occidentalis) to host plant volatiles. In: Vierbergen G, Tunc I (ed) Proceedings of the Sixth International Symposium on Thysanoptera, Antalya, Turkey, April 27- May 1. Akendiz University, Antalya, pp 121–128
Segura DF, Belliard SA, Vera MT, Bachmann GE, Ruiz MJ, Jofre-Barud F, Fernández PC, López ML, Shelly TE (2018) Plant chemicals and the sexual behavior of male tephritid fruit flies. Ann Entomol Soc Am 111:239–264. https://doi.org/10.1093/aesa/say024
Shelly TE, Edu J, Pahio E (2005) Influence of diet and methyl eugenol on the mating success of males of the oriental fruit fly, Bactrocera Dorsalis (Diptera: Tephritidae). Florida Entomol 88:307–313
Siderhurst MS, Jang EB (2006) Female-biased attraction of oriental fruit fly, Bactrocera dorsalis (Hendel), to a blend of host fruit volatiles from Terminalia catappa L. J Chem Ecol 32:2513–2524
Theron CD, Manrakhan A, Weldon CW (2017) Host use of the oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), in South Africa. J Appl Entomol 141:810–816. https://doi.org/10.1111/jen.12400
Verghese A, Kamala Jayanthi PD (2001) “Integrated pest management in fruits”. AAPMHE, (1st edn) capital publishing company, New Delhi 1:23
Verghese A, Shivananda TN, Jayanthi PK, Sreedevi K (2013) Frank Milburn Howlett (1877–1920): discoverer of the pied Piper's lure for the fruit flies (Tephritidae: Diptera). Curr Sci 105:260–262
Von Hoermann C, Ruther J, Reibe S et al (2011) The importance of carcass volatiles as attractants for the hide beetle Dermestes maculatus (De Geer). Forensic Sci Int 212:173–179. https://doi.org/10.1016/j.forsciint.2011.06.009
Wadhams LJ (1990) The use of coupled gas chromatography: electrophysiological techniques in the identification of insect pheromones, pheromones. In: McCaffery AR, Wilson ID (eds) Chromatography and isolation of insect hormones. Springer, New York, pp 289–298
Webster B, Bruce T, Pickett J, Hardie J (2008) Olfactory recognition of host plants in the absence of host-specific volatile compounds: host location in the black bean aphid, Aphis fabae. Commun Integr Biol 1:167–169
Acknowledgements
The authors thank the Director, IIHR, Bangalore for providing the research facilities. The authors duly acknowledge the constructive comments of the anonymous reviewers and editors which immeasurably improved the manuscript. This work was financially supported by the Indian Council for Agricultural Research (ICAR), New Delhi, India through the National Fellow Project. Efforts of Rajanna TS and Sagar J in maintaining insect cultures are sincerely appreciated.
Funding
Funding Award no. 27(3)/2010-HRD; award title: National Fellow Project - Studies on Phyto-semiochemicals involved in insect-plant interactions of major horticulture pests: Deciphering the chemical cues.
Author information
Authors and Affiliations
Contributions
Conceived and designed the experiments: PDKJ SKP. Performed the experiments: SKP. Analyzed the data: PDKJ SKP. Wrote the paper: PDKJ SKP MV.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that there is no conflict of interests.
Informed Consent
Informed consent was obtained from all authors included in the study.
Research Involving Human Participants and/or Animals
This article does not contain any studies with human participants or animals performed by any of the authors.
Rights and permissions
About this article
Cite this article
Kamala Jayanthi, P.D., Saravan Kumar, P. & Vyas, M. Odour Cues from Fruit Arils of Artocarpus heterophyllus Attract both Sexes of Oriental Fruit Flies. J Chem Ecol 47, 552–563 (2021). https://doi.org/10.1007/s10886-021-01269-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-021-01269-8