Skip to main content
Log in

Do Fruit Ripening Volatiles Enable Resource Specialism in Polyphagous Fruit Flies?

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Frugivorous tephritid fruit flies have lineages with high levels of host generalism. These insects use olfaction to locate fruits, but how they are able to recognize the odors of so many different host species is poorly understood. We used a series of behavioral experiments to investigate the role of fruit ripening volatiles as host cues in the Queensland fruit fly, Bactrocera tryoni (Froggatt), a polyphagous pest in Australia. Odors of mature guava (Psidium guajava) attracted female and male flies more strongly than three other ripening stages and guava pulp. We analyzed volatiles from guava odor and selected eleven compounds, all of which elicited an electrophysiological response in the antenna of female flies. Three of these, ethyl acetate, ethyl butyrate, and ethyl propionate, were released at the highest rates from the most attractive ripening stage. In behavioral trials, these three esters were not attractive individually, whereas a combination was necessary and sufficient in attracting female flies. The three-component blend was as attractive as the entire 11-component blend, which without these key volatiles was not attractive. Moreover, injecting low ranking hosts (squash and cucumber) with the three volatiles increased attraction in ovipositing female flies. These fruit flies are classed as generalists, but like many polyphagous insects they could be regarded as resource specialists, preferring specific plant reproductive stages with predictable odor cues. Exploring olfaction from this perspective could improve our understanding of host choice in polyphagous insects, and the selection of volatiles to be used as attractants in insect pest management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alagarmalai J, Nestel D, Dragushich D, Nemny-Lavy E, Anshelevich L, Zada A, Soroker V (2009) Identification of host attractants for the Ethiopian fruit fly, Dacus ciliatus Loew. J Chem Ecol 35:542–551

    Article  CAS  PubMed  Google Scholar 

  • Balagawi S, Drew RAI, Clarke AR (2013) Simultaneous tests of the preference-performance and phylogenetic conservatism hypotheses: is either theory useful? Arthropod Plant Interact 7:299–313

    Article  Google Scholar 

  • Becher PG, Bengtsson M, Hansson BS, Witzgall P (2010) Flying the fly: long-range flight behavior of Drosophila melanogaster to attractive odors. J Chem Ecol 36:599–607

    Article  CAS  PubMed  Google Scholar 

  • Becher PG et al. (2012) Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development. Funct Ecol 26:822–828

    Article  Google Scholar 

  • Bernays EA, Funk DJ (1999) Specialists make faster decisions than generalists: Experiments with aphids. Proc R Soc Lond Ser B Biolog Sci 266:151–156

    Article  Google Scholar 

  • Biasazin TD, Karlsson MF, Hillbur Y, Seyoum E, Dekker T (2014) Identification of host blends that attract the African invasive fruit fly, Bactrocera invadens. J Chem Ecol 40:966–976

    Article  CAS  PubMed  Google Scholar 

  • Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects - finding the right mix. Phytochemistry 72:1605–1611

    Article  CAS  PubMed  Google Scholar 

  • Carlsson MA, Knusel P, Verschure P, Hansson BS (2005) Spatio-temporal Ca2+ dynamics of moth olfactory projection neurones. Eur J Neurosci 22:647–657

    Article  PubMed  Google Scholar 

  • Cini A, Ioriatti C, Anfora G (2012) A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management. Bull Insectol 65:149–160

    Google Scholar 

  • Clarke AR et al. (2001) Seasonal abundance and host use patterns of seven Bactrocera macquart species (Diptera: Tephritidae) in Thailand and peninsular Malaysia. Raffles Bull Zool 49:207–220

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Clarke AR, Powell KS, Weldon CW, Taylor PW (2011) The ecology of Bactrocera tryoni (Diptera: Tephritidae): what do we know to assist pest management? Ann Appl Biol 158:26–54

    Article  Google Scholar 

  • Clifford MR, Riffell JA (2013) Mixture and odorant processing in the olfactory systems of insects: A comparative perspective. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 199:911–928

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cruz-Lopez 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

    Article  CAS  PubMed  Google Scholar 

  • Cugala D, Ekesi S, Ambasse D, Adamu RS, Mohamed SA (2014) Assessment of ripening stages of Cavendish dwarf bananas as host or non-host to Bactrocera invadens. J Appl Entomol 138:449–457

    Article  Google Scholar 

  • Cunningham JP (2012) Can mechanism help explain insect host choice? J Evol Biol 25:244–251

    Article  CAS  PubMed  Google Scholar 

  • Cunningham JP, Zalucki MP (2014) Understanding heliothine (Lepidoptera: Heliothinae) pests: what is a host plant? J Econ Entomol 107:881–896

    Article  PubMed  Google Scholar 

  • Dominiak BC, Ekman JH (2013) The rise and demise of control options for fruit fly in Australia. Crop Prot 51:57–67

    Article  CAS  Google Scholar 

  • Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dweck HKM et al. (2013) Olfactory preference for egg laying on citrus substrates in Drosophila. Curr Biol 23:2472–2480

    Article  CAS  PubMed  Google Scholar 

  • Egan SP, Funk DJ (2006) Individual advantages to ecological specialization: Insights on cognitive constraints from three conspecific taxa. Proc Roy Soc B Biolog Sci 273:843–848

    Article  Google Scholar 

  • El-Sayed AM, Suckling DM, Byers JA, Jang EB, Wearing CH (2009) Potential of "lure and kill" in long-term pest management and eradication of invasive species. J Econ Entomol 102:815–835

    Article  CAS  PubMed  Google Scholar 

  • Ero MM, Hamacek E, Clarke AR (2011) Foraging behaviours of Diachasmimorpha kraussii (Fullaway) (hymenoptera: Braconidae) and its host Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) in a nectarine (Prunus persica (L.) Batsch Var. Nectarina (Aiton) maxim) orchard. Aust J Entomol 50:234–240

    Google Scholar 

  • Fein BL, Reissig WH, Roelofs WL (1982) Identification of apple volatiles attractive to apple maggot, Rhagoletis pomonella (Diptera, Tephritidae. J Chem Ecol 8:1473–1487

    Article  CAS  PubMed  Google Scholar 

  • Forister ML et al. (2015) The global distribution of diet breadth in insect herbivores. Proc Natl Acad Sci U S A 112:442–447

    Article  CAS  PubMed  Google Scholar 

  • Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233

    Article  Google Scholar 

  • Gonzalez R, Toledo J, Cruz-Lopez L, Virgen A, Santiesteban A, Malo EA (2006) A new blend of white sapote fruit volatiles as potential attractant to Anastrepha ludens (Diptera: Tephritidae. J Econ Entomol 99:1994–2001

    Article  CAS  PubMed  Google Scholar 

  • Hardy NB, Otto SP (2014) Specialization and generalization in the diversification of phytophagous insects: Tests of the musical chairs and oscillation hypotheses. Proc Roy Soc B Biolog Sci. doi:10.1098/rspb.2013.2960

    Google Scholar 

  • Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273

    Article  Google Scholar 

  • Janz N (2003) The cost of polyphagy: oviposition decision time vs error rate in a butterfly. Oikos 100:493–496

    Article  Google Scholar 

  • Jayanthi PDK, Woodcock CM, Caulfield J, Birkett MA, Bruce TJA (2012) Isolation and identification of host cues from mango, Mangifera indica, that attract gravid female oriental fruit fly, Bactrocera dorsalis. J Chem Ecol 38:361–369

    Article  CAS  PubMed  Google Scholar 

  • Keesey IW, Knaden M, Hansson BS (2015) Olfactory specialization in Drosophila suzukii supports an ecological shift in host preference from rotten to fresh fruit. J Chem Ecol 41:121–128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei H, Vickers N (2008) Central processing of natural odor mixtures in insects. J Chem Ecol 34:915–927

    Article  CAS  PubMed  Google Scholar 

  • Levins R, Macarthur R (1969) An hypothesis to explain the incidence of monophagy. Ecology 50:910–911

    Article  Google Scholar 

  • Light DM, Jang EB, Flath RA (1992) Electroantennogram responses of the mediterranean fruit-fly, Ceratitis capitata, to the volatile constituents of nectarines. Entomol Exp Appl 63:13–26

    Article  CAS  Google Scholar 

  • Liscia A, Angioni P, Sacchetti P, Poddighe S, Granchietti A, Setzu MD, Belcari A (2013) Characterization of olfactory sensilla of the olive fly: behavioral and electrophysiological responses to volatile organic compounds from the host plant and bacterial filtrate. J Insect Physiol 59:705–716

    Article  CAS  PubMed  Google Scholar 

  • Lloyd AC, Hamacek EL, Smith D, Kopittke RA, Gu H (2013) Host susceptibility of citrus cultivars to Queensland fruit fly (Diptera: Tephritidae. J Econ Entomol 106:883–890

    Article  CAS  PubMed  Google Scholar 

  • Loxdale HD, Lushai G, Harvey JA (2011) The evolutionary improbability of 'generalism' in nature, with special reference to insects. Biol J Linn Soc 103:1–18

    Article  Google Scholar 

  • Malacrida AR, Gomulski LM, Bonizzoni M, Bertin S, Gasperi G, Gugliclmino CR (2007) Globalization and fruitfly invasion and expansion: the medfly paradigm. Genetica 131:1–9

    Article  CAS  PubMed  Google Scholar 

  • Malo EA, Cruz-Lopez L, Toledo J, Del Mazo A, Virgen A, Rojas JC (2005) Behavioral and electrophysiological responses of the Mexican fruit fly (Diptera: Tephritidae) to guava volatiles. Fla Entomol 88:364–371

    Article  Google Scholar 

  • Malo EA, Gallegos-Torres I, Toledo J, Valle-Mora J, Rojas JC (2012) Attraction of the west Indian fruit fly to mango fruit volatiles. Entomol Exp Appl 142:45–52

    Article  CAS  Google Scholar 

  • Massa MJ, Robacker DC, Patt J (2008) Identification of grape juice aroma volatiles and attractiveness to the Mexican fruit fly (Diptera: Tephritidae. Fla Entomol 91:266–276

    Article  CAS  Google Scholar 

  • Münch D, Galizia CG (2016) DoOR 2.0 - Comprehensive mapping of Drosophila melanogaster odorant responses. Scientific Rep 6:21841, http://www.nature.com/articles/srep21841 - supplementary-information

  • Nojima S, Linn C, Morris B, Zhang AJ, Roelofs W (2003) Identification of host fruit volatiles from hawthorn (Crataegus spp.) attractive to hawthorn-origin Rhagoletis pomonella flies. J Chem Ecol 29:321–336

    Article  CAS  PubMed  Google Scholar 

  • Pawliszyn J (2009) Handbook of solid phase microextraction. Chemical Industry Press, Chicago

    Google Scholar 

  • Prokopy RJ, Jacome I, Bigurra E (2005) An index for assigning distances between odor-baited spheres on perimeter trees of orchards for control of apple maggot flies. Entomol Exp Appl 115:371–377

    Article  Google Scholar 

  • Rasgado MA, Malo EA, Cruz-Lopez L, Rojas JC, Toledo J (2009) Olfactory response of the Mexican fruit fly (Diptera: Tephritidae) to Citrus aurantium volatiles. J Econ Entomol 102:585–594

    Article  CAS  PubMed  Google Scholar 

  • Rattanapun W, Amornsak W, Clarke AR (2009) Bactrocera dorsalis Preference for and performance on two mango varieties at three stages of ripeness. Entomol Exp Appl 131:243–253

    Article  Google Scholar 

  • Robacker DC, Warfield WC, Flath RA (1992) A 4-component attractant for the Mexican fruit-fly, Anastrepha ludens (Diptera, Tephritidae), from host fruit. J Chem Ecol 18:1239–1254

    Article  CAS  PubMed  Google Scholar 

  • Royer JE, De Faveri SG, Lowe GE, Wright CL (2014) Cucumber volatile blend, a promising female-biased lure for Bactrocera cucumis (French 1907) (Diptera: Tephritidae: Dacinae), a pest fruit fly that does not respond to male attractants. Aust Entomol 53:347–352

    Article  Google Scholar 

  • Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106–1117

    PubMed  Google Scholar 

  • Sarles L, Verhaeghe A, Francis F, Verheggen FJ (2015) Semiochemicals of Rhagoletis fruit flies: potential for integrated pest management. Crop Prot 78:114–118

    Article  CAS  Google Scholar 

  • Schutze MK et al. (2015) Synonymization of key pest species within the Bactrocera dorsalis species complex (Diptera: Tephritidae): taxonomic changes based on a review of 20 years of integrative morphological, molecular, cytogenetic, behavioural and chemoecological data. Syst Entomol 40:456–471

    Article  Google Scholar 

  • 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. J Chem Ecol 32:2513–2524

    Article  CAS  PubMed  Google Scholar 

  • Siderhurst MS, Jang EB (2010) Cucumber volatile blend attractive to female melon fly, Bactrocera cucurbitae (Coquillett. J Chem Ecol 36:699–708

    Article  CAS  PubMed  Google Scholar 

  • Singer MC (1982) Quantification of host preference by manipulation of oviposition behaviour in the butterfly Euphydryas editha. Oecologia 52:224–229

    Article  Google Scholar 

  • Stensmyr MC et al. (2012) A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151:1345–1357

    Article  CAS  PubMed  Google Scholar 

  • Weldon CW, Perez-Staples D, Taylor PW (2008) Feeding on yeast hydrolysate enhances attraction to cue-lure in Queensland fruit flies, Bactrocera tryoni. Entomol Exp Appl 129:200–209

    Article  Google Scholar 

Download references

Acknowledgments

The research was supported jointly through Horticulture Innovation Australia Ltd. (SF12013) and the Plant Biosecurity CRC (CRC3066). M.A.C. was supported by a research grant from Olle Engkvist Byggmästare (2014/792). We thank Zacchary Crookes and Owen Webb for assistance in cage trials.

Disclosure Statement

The authors declare there that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John Paul Cunningham.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cunningham, J.P., Carlsson, M.A., Villa, T.F. et al. Do Fruit Ripening Volatiles Enable Resource Specialism in Polyphagous Fruit Flies?. J Chem Ecol 42, 931–940 (2016). https://doi.org/10.1007/s10886-016-0752-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-016-0752-5

Keywords

Navigation