Interspecific Variation of Floral Scent Composition in Glochidion and its Association with Host-specific Pollinating Seed Parasite (Epicephala)

Abstract

Trees of the genus Glochidion (Phyllanthaceae) are pollinated by females of Epicephala moths (Gracillariidae) whose larvae consume the seeds of the flowers that they pollinate. Each Epicephala moth species is specific locally to a single host species, although two to four Glochidion hosts often cooccur. To investigate the role of olfactory signals in maintaining the plant−moth specificity, we analyzed floral scent composition of five Glochidion species by using gas chromatography–mass spectrometry (GC-MS) and conducted Y-tube olfactometer bioassays with Epicephala moths and their host flowers. The GC-MS analysis showed that the floral scents of the five Glochidion species are dominated by (R)-(−)- and (S)-(+)-linalool, and (E)- and (Z)-β-ocimene, and that each species produces 6–20 compounds. Transformation of scent profiles by using chord-normalized expected species shared distances and analysis of the data with nonmetric multidimensional scaling showed that floral volatiles of cooccurring Glochidion species can be distinguished by relative chemical composition, especially that of minor compounds. The bioassay with pollinators of Glochidion lanceolatum and Glochidion ruburm further indicated that Epicephala moths are capable of discriminating their hosts by using floral odor. The results suggest that the floral scent of Glochidion is one of the important key signals that mediate the encounters of the species-specific partners in the GlochidionEpicephala mutualism.

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References

  1. Andersson, S. and Dobson, H. E. M. 2003. Antennal responses to floral scents in the butterfly Heliconius melpomene. J. Chem. Ecol. 29:2319–2330.

    PubMed  CAS  Article  Google Scholar 

  2. Andersson, S., Nilsson, L. A., Groth, I., and Bergström, G. 2002. Floral scents in butterfly-pollinated plants: possible convergence in chemical composition. Bot. J. Linn. Soc. 140:129–153.

    Article  Google Scholar 

  3. Bäckmann, A. C., Bengtsson, M., Borg-Karlsson, A. K., Liblikas, I., and Witzgall, P. 2001. Volatiles from apple (Malus domestica) eliciting antennal responses in female codling moth Cydia pomonella (L.) (Lepidoptera: Tortricidae): effect of plant injury and sampling technique. Z. Naturforsch. C 56:262–268.

    Google Scholar 

  4. Borg-Karlson, A. K., Valterova, I., and Nilsson, L. A. 1994. Volatile compounds from flowers of six species in the family Apiaceae: bouquets for different pollinators? Phytochemistry 35:111–119.

    CAS  Article  Google Scholar 

  5. Bossart, J. L. 2003. Covariance of preference and performance on normal and novel hosts in a locally monophagous and locally polyphagous butterfly population. Oecologia 135:477–486.

    PubMed  CAS  Google Scholar 

  6. Clarke, K. R. 1993. Nonparametric multivariate analyses of changes in community structure. Aust. J. Ecol. 18:117–143.

    Article  Google Scholar 

  7. Cook, J. M. and Rasplus, J. Y. 2003. Mutualists with attitude: coevolving fig wasps and figs. Trends Ecol. Evol. 18:241–248.

    Article  Google Scholar 

  8. Corner, E. J. H. 1965. Check-list of Ficus in Asia and Australasia with keys to identification. Gard. Bull. (Singapore) 21:1–185.

    Google Scholar 

  9. Davies, N. W. 1990. Gas chromatographic retention indices of monoterpenes and sesquiterpenes on methyl silicone and Carbowax 20 M phases. J. Chromatogr. 503:1–24.

    CAS  Article  Google Scholar 

  10. Forister, M. L. 2004. Oviposition preference and larval performance within a diverging lineage of lycaenid butterflies. Ecol. Entomol. 29:264–272.

    Article  Google Scholar 

  11. Gallagher, E. D. 1999. COMPAH documentation. http://www.es.umb.edu/edgwebp.htm

  12. Gancel, A. L., Olle, D., Ollitrault, P., Luro, F., and Brillouet, J. M. 2002. Leaf and peel volatile compounds of an interspecific citrus somatic hybrid [Citrus aurantiflolia (Christm.) Swing. + Citrus paradisi MacFaydan]. Flavour Fragr. J. 17:416–424.

    CAS  Article  Google Scholar 

  13. Gerlach, G. and Schill, R. 1991. Composition of orchid scents attracting euglossine bees. Bot. Acta 104:379–391.

    CAS  Google Scholar 

  14. Govaerts, R., Frodin, D. G., and Radcliffe-Smith, A. 2000. World checklist and bibliography of Euphorbiaceae. Royal Botanic Gardens, Kew, UK.

    Google Scholar 

  15. Grison-Pigé, L., Bessière, J. M., and Hossaert-Mckey, M. 2002a. Specific attraction of fig-pollinating wasps: Role of volatile compounds released by tropical figs. J. Chem. Ecol. 28:283–295.

    PubMed  Article  Google Scholar 

  16. Grison-Pigé, L., Hossaert-Mckey, M., Greeff, J. M., and Bessière, J. M. 2002b. Fig volatile compounds—a first comparative study. Phytochemistry 61:61–71.

    PubMed  Article  Google Scholar 

  17. Hern, A. and Dorn, S. 1999. Sexual dimorphism in the olfactory orientation of adult Cydia pomonella in response to alpha-farnesene. Entomol. Exp. Appl. 92:63–72.

    CAS  Article  Google Scholar 

  18. Herre, E. A. 1989. Coevolution of reproductive characteristics in 12 species of New World figs and their pollinator wasps. Experientia 45:637–647.

    Article  Google Scholar 

  19. Herre, E. A. 1996. An overview of studies on a community of Panamanian figs. J. Biogeogr. 23:593–607.

    Article  Google Scholar 

  20. Herre, E. A. and West, S, A. 1997. Conflict of interest in a mutualism: documenting the elusive fig wasp–seed trade-off. Proc. R. Soc. Lond. B. 264:1501–1507.

    Article  Google Scholar 

  21. Hossaert-Mckey, M., Gibernau, M., and Frey, J. E. 1994. Chemosensory attraction of fig wasps to substances produced by receptive figs. Entomol. Exp. Appl. 70:185–191.

    Article  Google Scholar 

  22. Janzen, D. H. 1979. How to be a fig. Annu. Rev. Ecol. Syst. 10:13–51.

    Article  Google Scholar 

  23. Jürgens, A. and Dötterl, S. 2004. Chemical composition of anther volatiles in Ranunculaceae: genera-specific profiles in Anemone, Aquilegia, Caltha, Pulsatilla, Ranunculus, and Trollius species. Am. J. Bot. 91:1969–1980.

    Google Scholar 

  24. Kato, M., Takimura, A., and Kawakita, A. 2003. An obligate pollination mutualism and reciprocal diversification in the tree genus Glochidion (Euphorbiaceae). Proc. Natl. Acad. Sci. U S A 100:5264–5267.

    PubMed  CAS  Article  Google Scholar 

  25. Kawakita, A. and Kato, M. 2006. Assessment of the diversity and species specificity of the mutualistic association between Epicephala moths and Glochidion trees. Mol. Ecol. 15:3567–3581.

    PubMed  CAS  Article  Google Scholar 

  26. Kawakita, A., Takimura, A., Terachi, T., Sota, T., and Kato, M. 2004. Cospeciation analysis of an obligate pollination mutualism: Have Glochidion trees (Euphorbiaceae) and pollinating Epicephala moths (Gracillaridae) diversified in parallel? Evolution 58:2201–2214.

    PubMed  CAS  Google Scholar 

  27. Knudsen, J. T. and Tollsten, L. 1993. Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth-pollinated taxa. Bot. J. Linn. Soc. 113:263–284.

    Article  Google Scholar 

  28. Knudsen, J. T., Tollsten, L, and Bergströn, L. G. 1993. Floral scents—a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33:253–280.

    CAS  Article  Google Scholar 

  29. Lopez-Vaamonde, C., Dixon, D. J., Cook, J. M., and Rasplus, J. Y. 2002. Revision of the Australian species of Pleistodontes (Hymenoptera: Agaonidae) fig-pollinating wasps and their host–plant associations. Zool. J. Linn. Soc. 136:637–683.

    Article  Google Scholar 

  30. Machado, C. A., Jousselin, E., Kjellberg, F., Compton, S. G, and Herre, E. A. 2001. Phylogenetic relationships, historical biogeography, and character evolution of fig-pollinating wasps. Proc. R. Soc. Lond. B. 268:685–694.

    CAS  Article  Google Scholar 

  31. Makholela, T. and Manning, J. C. 2006. First report of moth pollination in Struthiola ciliata (Thymelaeaceae) in southern Africa. S. Afr. J. Bot. 72:597–603.

    CAS  Article  Google Scholar 

  32. Minh Tu, N. T., Onishi, Y., Son, U. S., Ogawa, E., Ukeda, H., and Sawamura, M. 2003. Characteristic odour components of Citrus inflata Hort. ex Tanaka (Mochiyu) cold-pressed peel oil. Flavour Fragr. J. 18:454–459.

    Article  CAS  Google Scholar 

  33. Miyake, T., Yamaoka, R., and Yahara T. 1998. Floral scents of hawkmoth-pollinated flowers in Japan. J. Plant. Res. 111:199–205.

    CAS  Article  Google Scholar 

  34. Molbo, D., Machado, C. A., Sevenster, J. G., Keller, L., and Herre, E. A. 2003. Cryptic species of fig-pollinating wasps: implications for the evolution of the fig–wasps mutualism, sex allocation, and precision of adaptation. Proc. Natl. Acad. Sci. U S A 100:5867–5872.

    PubMed  CAS  Article  Google Scholar 

  35. Nefdt, R. J C. and Compton, S. G. 1996. Regulation of seed and pollinator production in the fig–fig wasp mutualism. J. Anim. Ecol. 65:170–182.

    Article  Google Scholar 

  36. Pellmyr, O. 2003. Yuccas, yucca moths, and coevolution: a review. Ann. Mo. Bot. Gard. 90:33–55.

    Article  Google Scholar 

  37. Pellmyr, O., Tang, W., Groth, I., Bergstrom, G., and Thien, L. B. 1991. Cycad cone and angiosperm floral volatiles inferences for the evolution of insect pollination. Biochem. Syst. Ecol. 19:623–628.

    CAS  Article  Google Scholar 

  38. Pettersson, S., Ervik, F., and Knudsen, J. K. 2004. Floral scent of bat-pollinated species: West Africa vs. the New World. Biol. J. Linn. Soc. 82:161–168.

    Article  Google Scholar 

  39. Proctor, M., Yeo, P., and Lack, A. 1996. The natural history of pollination. Timber Press, Portland.

    Google Scholar 

  40. Raguso, R. A. and Pellmyr, O. 1998. Dynamic headspace analysis of floral volatiles: a comparison of methods. Oikos 81:238–254.

    CAS  Article  Google Scholar 

  41. Raguso, R. A., Light, D. M., and Pichersky, E. 1996. Electroantennogram responses of Hyles lineata (Sphingidae: Lepidoptera) to volatile compounds from Clarkia breweri (Onagraceae) and other moth-pollinated flowers. J. Chem. Ecol. 22:1735–1765.

    CAS  Article  Google Scholar 

  42. Raguso, R. A., Levin, R. A., Foose, S. E., Holmberg, M. W., and Mcdade, L. A. 2003. Fragrance chemistry, nocturnal rhythms and pollination “syndromes” in Nicotiana. Phytochemistry 63:265–284.

    PubMed  CAS  Article  Google Scholar 

  43. Sagrero-Nieves, L., Bartley, J. P., Espinosa, B. G., Domingues, X. A., and Verde S. J. 1997. Essential oil composition of Aristolochia brevipes Benth. Flavour Fragr. J. 12:401–403.

    CAS  Article  Google Scholar 

  44. Singer, M. C., Ng, D., and Thomas, C. D. 1988. Heritability of oviposition preference and its relationship to offspring performance within a single insect population. Evolution 42:977–985.

    Article  Google Scholar 

  45. Song, Q., Yang, D., Zhang, G., and Yang, C. 2001. Volatiles from Ficus hispida and their attractiveness to fig wasps. J. Chem. Ecol. 27:1929–1942.

    PubMed  CAS  Article  Google Scholar 

  46. Svensson, G. P., Hickman, M. O., Bartram, S., Boland, W., Pellmyr, O., and Raguso, R. A. 2005. Chemistry and geographic variation of floral scent in Yucca filamentosa (Agavaceae). Am. J. Bot. 92:1624–1631.

    CAS  Google Scholar 

  47. Traxler, M. A. and Joern, A. 1999. Performance tradeoffs for two hosts within and between populations of the oligophagous grasshopper Hesperotettix viridis (Acrididae). Oikos 87:239–250.

    Article  Google Scholar 

  48. Trueblood, D. D., Gallagher, E. D., and Gould, D. M. 1994. Three stages of seasonal succession on the Savin Hill Cove mudflat, Boston Harbor. Limnol. Oceanogr. 39:1440–1454.

    Article  Google Scholar 

  49. Via, S. 1986. Genetic covariance between oviposition preference and larval performance in an insect herbivore. Evolution 40:778–785.

    Article  Google Scholar 

  50. Ware, A. B. and Compton, S. G. 1994. Responses of fig wasps to host plant volatile cues. J. Chem. Ecol. 20:785–802.

    CAS  Article  Google Scholar 

  51. Weiblen, G. D. 2002. How to be a fig wasp. Annu. Rev. Ecol. Syst. 47:299–330.

    CAS  Google Scholar 

  52. Weiblen, G. D. 2004. Correlated evolution in fig pollination. Syst. Biol. 53:128–139.

    PubMed  Article  Google Scholar 

  53. Weiblen, G. D. and Bush, G. L. 2002. Speciation in fig pollinators and parasites. Mol. Ecol. 11:1573–1578.

    PubMed  Article  Google Scholar 

  54. Weiblen, G. D., Yu, D. W., and Stuart, S. A. 2001. Pollination and parasitism in functionally dioecious figs. Proc. R. Soc. Lond. B. 268:651–659.

    CAS  Article  Google Scholar 

  55. Yokoyama, J. 2003. Cospeciation of figs and fig-wasps: a case study of endemic species pairs in the Ogasawara Islands. Popul. Ecol. 45:249–256.

    Article  Google Scholar 

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Acknowledgements

We appreciate Y. Inui for providing the opportunity to conduct this study; T. Y. Chiang, T. W. Hsu, and S. C. Liu for assistance in the field in Taiwan; Y. Yamaoka and I. Shimizu for allowing us to use the GC and GC-MS; Y. Kumano and N. Fujiwara-Tsujii for technical advice in collecting and analyzing the floral scents; and the subject editor and anonymous reviewers for valuable comments on the manuscript. This work was supported by Grant-in-Aid for Scientific Research 15370012 from Japan Ministry of Education, Culture, Sports, Science and Technology (to M. K.) and by Grant for Basic Science Research Project from Sumitomo Foundation (to T. O.).

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Correspondence to Tomoko Okamoto.

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Okamoto, T., Kawakita, A. & Kato, M. Interspecific Variation of Floral Scent Composition in Glochidion and its Association with Host-specific Pollinating Seed Parasite (Epicephala). J Chem Ecol 33, 1065–1081 (2007). https://doi.org/10.1007/s10886-007-9287-0

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Keywords

  • Bioassay
  • Epicephala
  • Floral scent
  • Glochidion
  • Obligate pollination mutualism
  • Species specificity