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Larval Feeding Stimulants for a Rutaceae-Feeding Swallowtail Butterfly, Papilio xuthus L. in Citrus unshiu Leaves

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Abstract

Larvae of a swallowtail butterfly, Papilio xuthus L., feed exclusively on plants of the family Rutaceae, including various Citrus crops. Larvae were strongly stimulated to feed on paper strips impregnated with ethanolic extracts of host-plant leaves. Stimulation of feeding on extracts of Citrus unshiu leaves required a mixture of chemicals including sugars (d-glucose, d-fructose, and d-sucrose), a betaine [(−)-stachydrine], a cyclic peptide (citrusin I), a polymethoxyflavone (isosinensetin), and the lipids 1-linolenoylglycerol, 1-linoleoylglycerol, 1-octadecenoylglycerol, 1-stearoylglycerol, and 1,2-dilinolenoyl-3-galactosyl-sn-glycerol. When these compounds were assayed individually, few larvae consumed test strips. However, larvae readily chewed the test strips treated with a mixture of all compounds, indicating that host recognition by P. xuthus larvae is mediated by a specific combination of both primary and secondary substances. Comparison of 11 stimulant components with 10 compounds from C. unshiu leaves previously reported as stimulant components for oviposition by P. xuthus adult females revealed only one compound, stachydrine, as an ingredient in common. While the larval feeding-stimulant mixture is dominated by nutrients and other compounds of general significance for primary metabolism, the component oviposition stimulants are mostly secondary substances, including flavonoid glycosides, protoalkaloids, a cyclitol, and a betaine, that have restricted distributions in plants. Reliance by adult females on unique profiles of secondary compounds presumably reflects the need to locate and recognize specific host-plant species within a diverse flora. Since the initial host choice for the larvae is made typically by the ovipositing female, however, unique secondary compounds may be less important for larval feeding than are compounds useful for indicating food and microhabitat quality once on the host plant.

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References

  • Berenbaum, M. R., and Feeny, P. P. 2008. Chemical mediation of host-plant specialization—the papilionid paradigm, pp. 3–19, in K. J. Tilmon (ed.). Specialization, Speciation and Radiation: The Evolutionary Biology of Herbivorous Insects, University of California Press, Berkeley.

    Google Scholar 

  • Bernays, E. A., and Simpson, S. J. 1982. Control of food intake. Adv. Insect Phys. 16:59–118.

    Article  Google Scholar 

  • Bowers, M. D. 1984. Iridoid glycosides and hostplant specificity in larvae of the buckeye butterfly, Junonia coenia (Nymphalidae). J. Chem. Ecol. 10:1567–1577.

    Article  CAS  Google Scholar 

  • David, W. A. L., and Gardiner, B. O. C. 1962. Oviposition and the hatching of the eggs of Pieris brassicae (L.) in a laboratory culture. Bull. Entmol. Res. 53:91–109.

    Article  CAS  Google Scholar 

  • Dayrit, F. M., Buenafe, O. E. M., Chainani, E. T., and Vera, I. M. S. 2008. Analysis of monoglycerides, diglycerides, sterols, and free fatty acids in coconut (Cocos nucifera L.) oil by 31P NMR spectroscopy. J. Agric. Food Chem. 56:5765–5769.

    Article  PubMed  CAS  Google Scholar 

  • Dethier, V. G. 1941. Chemical factors determining the choice of food plants by Papilio larvae. Am. Nat. 25:61–73.

    Article  Google Scholar 

  • Feeny, P., Rosenberry, L., and Carter, M. 1983. Chemical aspects of oviposition behavior in butterflies, pp. 27–76, in S. Ahmad (ed.). Herbivorous Insects, Academic, New York.

    Google Scholar 

  • Fraser, B. H., Perlmutter, P., and Wijesundera, C. 2007. Practical syntheses of triacylglycerol regioisomers containing long-chain polyunsaturated fatty acids. J. Amer. Oil Chem. Soc. 84:11–21.

    Article  CAS  Google Scholar 

  • Hanson, F. E., and Dethier, V. G. 1973. Role of gestation and olfaction in food plant discrimination in the tobacco hornworm, Manduca sexta. J. Insect Physiol. 19: 1019–1034.

    Article  PubMed  CAS  Google Scholar 

  • Hamamura, Y., and Naito, K. 1961 Food selection by silkworm larvae, Bombyx mori. Citral, linalyl acetate, linalol, and terpinyl acetate as attractants of larvae. Nature, 190:879–880.

    Article  CAS  Google Scholar 

  • Hamamura, Y., Hayashiya, K., Naito, K., Matsuura, K., and Nishida, J. 1962. Food selection by silkworm larvae. Nature, 194:754–755.

    Article  Google Scholar 

  • Hirata, T., Fujii, M., Akita, K., Yanaka, N., Ogawa, K., Kuroyanagi, M., and Hongo, D. 2009. Identification and physiological evaluation of the components from Citrus fruits as potential drugs for anti-corpulence and anticancer. Bioorg. Med. Chem., 17:25–28.

    Article  PubMed  CAS  Google Scholar 

  • Honda, K. 1990. Identification of host-plant chemicals stimulating oviposition by swallowtail butterfly, Papilio protenor. J. Chem. Ecol. 16:325–337.

    Article  CAS  Google Scholar 

  • Honda, K., and Hayashi, N. 1995. Chemical factors in Rutaceous plants regulating host selection by two swallowtail butterflies, Papilio protenor and P. xuthus (Lepidoptera: Papilionidae). Appl. Entomol. Zool. 30:327–334.

    CAS  Google Scholar 

  • Jassbi, A. R. 2003. Secondary metabolites as stimulants and antifeedants of Salix integra for the leaf beetle Plagiodera versicolora. Z. Naturforsch. 58c:573–579.

    Google Scholar 

  • Joyard, J., Marechal, E., Miege, C., Block, M. A., Dorne, A.-J., and Douce, R. 1998. Structure, distribution and biosynthesis of glycerolipids from higher chloroplasts, pp. 21–52, in P. A Siegenthaler and N. Murata (ed.). Lipids in Photosynthesis: Structure, Function, and Genetics, Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Kim, C., Ha, H., Kim, J. S., Kim, Y. T., Kwon, S.-C., and Park, S. W. 2003. Induction of growth hormone by the roots of Astragalus membranaceus in pituitary cell culture. Arch. Pharm. Res. 26:34–39.

    Article  PubMed  CAS  Google Scholar 

  • Machida, K., and Osawa, K. 1989. On the flavonoid constituents from the peels of Citrus hassaku Hort. Ex TANAKA. Chem. Pharm. Bull. 37:1092–1094.

    CAS  Google Scholar 

  • Matsubara, Y., Yusa, T., Sawabe, A., Iizuka, Y., Takekuma, S., and Yoshida, Y. 1991. Structure of new cyclic peptides in young unshiu (Citrus unshiu MARCOV.), orange (Citrus sinensis OSBECK.) and amanatsu (Citrus natsudaidai) Peelings. Agric. Biol. Chem. 55:2923–2929.

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto, T., Shishido, A., and Takeya, K. 2001. New cyclic peptides from higher plants. Tennen Yuki Kagobutsu Toronkai Koen Yoshishu. 43:407–412. (in Japanese)

    Google Scholar 

  • Matsumoto, T., Nishimura, K., and Takeya, K. 2002. New cyclic peptides from Citrus medica var. sarcodactylis SWINGLE. Chem. Pharm. Bull. 50:857–860.

    Article  PubMed  CAS  Google Scholar 

  • Mizuno, M., Iinuma, M., Ohara, M., Tanaka, T., and Iwamasa, M. 1991. Chemotaxonomy of the genus Citrus based on polymethoxyflavones. Chem. Pharm. Bull. 39:945–949.

    CAS  Google Scholar 

  • Morita, H., Enomoto, M., Hirasawa, Y., Iizuka, T., Ogawa, K., Kawahara, N., Goda, Y., Matsumoto, T., and Takeya, K. 2007. Cyclonatsudamine A, a new vasodilator cyclic peptide from Citrus natsudaidai. Bioorg. Med. Chem. Lett. 17:5410–5413.

    Article  PubMed  CAS  Google Scholar 

  • Murphy, S, and Feeny, P. 2006. Chemical facilitation of a naturally occurring host shift by Papilio machaon butterflies (Papilionidae). Ecol. Monogr. 76:399–414.

    Article  Google Scholar 

  • Nation, J. L. 2002. Insect Physiology and Biochemistry. CRC Press. Boca Raton.

    Google Scholar 

  • Nishida, R., Ohsugi, T., and Fukami, H. 1987. Oviposition stimulants of a Citrus-feeding swallowtail butterfly, Papilio xuthus L. Experientia 43:342–344.

    Article  CAS  Google Scholar 

  • Nishida, R., and Fukami, H. 1989a. Ecological adaptation of an Aristolochiaceae-feeding swallowtail butterfly, Atrophaneura alcinous, to aristolochic acids. J. Chem. Ecol. 15:2549–2563.

    Article  CAS  Google Scholar 

  • Nishida, R., and Fukami, H. 1989b. Oviposition stimulants of an Aristolochiaceae-feeding swallowtail butterfly, Atrophaneura alcinous. J. Chem. Ecol. 15:2565–2575.

    Article  CAS  Google Scholar 

  • Nishida, R. 1995. Oviposition stimulants of swallowtail butterflies. pp. 17–26. in J. M. Scriber, Y. Tsubaki and R. C. Lederhouse (eds.) Swallowtail Butterflies: Their Ecology and Evolutionary Biology. Scientific Publishers, Gainesville.

    Google Scholar 

  • Nishida, R. 2005. Chemosensory basis of host recognition in butterflies—multi-component system of oviposition stimulants and deterrents. Chem. Senses 30:i293-i294.

    Article  PubMed  Google Scholar 

  • Ohsugi, T., Nishida, R., and Fukami, H. 1991. Multi-component system of oviposition stimulants for a Rutaceae-feeding swallowtail butterfly, Papilio xuthus (Lepidoptera: Papilionidae). Appl. Entomol. Zool. 26:29–40.

    CAS  Google Scholar 

  • Ohta, H. A., Awai, K., and Takamiya, K. 2000. Glyceroglycolipids of photosynthetic organisms –their biosynthesis and evolutionary origin-. Trends Glycosci. Glycotechnol. 12:241–253.

    Article  CAS  Google Scholar 

  • Ono, H., Kuwahara, Y., and Nishida, R. 2004. Hydroxybenzoic acid derivatives in a nonhost rutaceous plant, Orixa japonica, deter both oviposition and larval feeding in a Rutaceae-feeding swallowtail butterfly, Papilio xuthus L. J. Chem. Ecol. 30:287–301.

    Article  PubMed  CAS  Google Scholar 

  • Pereyra, P. C., and Bowers, M.D. 1988. Iridoid glycosides as oviposition stimulants for the buckeye Junonia coenia (Nymphalidae). J. Chem. Ecol. 14:917–928.

    Article  CAS  Google Scholar 

  • Renwick, J. A. A., and Chew, F. S. 1994. Oviposition behavior in Lepidoptera. Annu. Rev. Entomol. 39:377–400.

    Article  Google Scholar 

  • Renwick, J. A. A., and Lopez, K. 1999. Experience-based food consumption by larvae of Pieris rapae: Addiction to glucosinolates?. Entomologia Exp. App. 91:51–58.

    Article  CAS  Google Scholar 

  • Renwick, J. A. A. 2002. The chemical world of crucivores: Lures, treats and traps. Entomologia Exp. App. 104:35–42.

    Article  CAS  Google Scholar 

  • Roughan, P. G., and Batt R. D. 1969. The glycerolipid composition of leaves. Phytochemistry 8:363–369.

    Article  CAS  Google Scholar 

  • Sachdev-Gupta, K., Feeny, P. P., and Carter, M. 1993. Oviposition stimulants for the pipevine swallowtail butterfly, Battus philenor (Papilionidae), from an Aristolochia host plant: Synergism between inositols, aristolochic acids and a monogalactosyl diglyceride. Chemoecology 4:19–28.

    Article  CAS  Google Scholar 

  • Saxena, K. N., and Prabha, S. 1975. Relationship between the olfactory sensilla of Papilio demoleus L. larvae and their orientation responses to different odours. J. Entomol. 50:119–126.

    Google Scholar 

  • Schoonhoven, L. M., Loon, J. J. A., and Dicke, M. 2005. Insect-Plant Biology. Oxford University Press Inc., New York.

    Google Scholar 

  • Selmair, P. L., and Koehler, P. 2008. Baking performance of synthetic glycolipids in comparison to commercial surfactants. J. Agric. Food Chem. 56:6691–6700.

    Article  PubMed  CAS  Google Scholar 

  • Städler, E. and Roessingh, P. 1990. Perception of surface chemicals by feeding and ovipositing insects. Symp. Biol. Hung. 39:71–86.

    Google Scholar 

  • Sugiyama, S., Umehara, K., Kuroyanagi, M., Ueno, A., and Taki, T. 1993. Studies on the differentiation inducers of myeloid leukemic cells from Citrus species. Chem. Pharm. Bull. 41:714–719.

    PubMed  CAS  Google Scholar 

  • Tanaka, K. Uda, Y. Ono, Y. Nakagawa, T. Suwa, M. Yamaoka, R. and Touhara, K. 2009. Highly selective tuning of a silkworm olfactory receptor to a key mulberry leaf volatile. Curr. Biol. 19:1–10.

    Article  Google Scholar 

  • Verschaffelt, E. 1910. The cause determining the selection of food in some herbivorous insects. Proc. K. Ned. Akad. Wet. 13:536–542.

    Google Scholar 

  • Wiklund, C. 1975. The evolutionary relationship between adult oviposition preferences and larval host plant range in Papilio machaon L. Oecologia 18:185–197.

    Article  Google Scholar 

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Acknowledgements

The authors thank Mr. S. Sato and Mr. T. Matsuki of Tohoku Pharmaceutical University for HR-EI-MS measurements, and Mr. Fumio Kodama for the supply of Citrus unshiu leaves. We also thank Prof. P. P. Feeny of Cornell University for useful comments and reviewing the manuscript. This work was partially supported by the Grant-in-Aid for Scientific Research from JSPS (No. 19310142) and a Grant-in-Aid for the 21st Century COE Program for Innovative Food and Environmental Studies Pioneered by Entomomimetic Sciences, from the Ministry of Education, Culture, Sports, Science and Technology of Japan.

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Correspondence to Ritsuo Nishida.

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Murata, T., Mori, N. & Nishida, R. Larval Feeding Stimulants for a Rutaceae-Feeding Swallowtail Butterfly, Papilio xuthus L. in Citrus unshiu Leaves. J Chem Ecol 37, 1099–1109 (2011). https://doi.org/10.1007/s10886-011-0022-5

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