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.
Bernays, E. A., and Simpson, S. J. 1982. Control of food intake. Adv. Insect Phys. 16:59–118.
Bowers, M. D. 1984. Iridoid glycosides and hostplant specificity in larvae of the buckeye butterfly, Junonia coenia (Nymphalidae). J. Chem. Ecol. 10:1567–1577.
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.
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.
Dethier, V. G. 1941. Chemical factors determining the choice of food plants by Papilio larvae. Am. Nat. 25:61–73.
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.
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.
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.
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.
Hamamura, Y., Hayashiya, K., Naito, K., Matsuura, K., and Nishida, J. 1962. Food selection by silkworm larvae. Nature, 194:754–755.
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.
Honda, K. 1990. Identification of host-plant chemicals stimulating oviposition by swallowtail butterfly, Papilio protenor. J. Chem. Ecol. 16:325–337.
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.
Jassbi, A. R. 2003. Secondary metabolites as stimulants and antifeedants of Salix integra for the leaf beetle Plagiodera versicolora. Z. Naturforsch. 58c:573–579.
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.
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.
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.
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.
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)
Matsumoto, T., Nishimura, K., and Takeya, K. 2002. New cyclic peptides from Citrus medica var. sarcodactylis SWINGLE. Chem. Pharm. Bull. 50:857–860.
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.
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.
Murphy, S, and Feeny, P. 2006. Chemical facilitation of a naturally occurring host shift by Papilio machaon butterflies (Papilionidae). Ecol. Monogr. 76:399–414.
Nation, J. L. 2002. Insect Physiology and Biochemistry. CRC Press. Boca Raton.
Nishida, R., Ohsugi, T., and Fukami, H. 1987. Oviposition stimulants of a Citrus-feeding swallowtail butterfly, Papilio xuthus L. Experientia 43:342–344.
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.
Nishida, R., and Fukami, H. 1989b. Oviposition stimulants of an Aristolochiaceae-feeding swallowtail butterfly, Atrophaneura alcinous. J. Chem. Ecol. 15:2565–2575.
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.
Nishida, R. 2005. Chemosensory basis of host recognition in butterflies—multi-component system of oviposition stimulants and deterrents. Chem. Senses 30:i293-i294.
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.
Ohta, H. A., Awai, K., and Takamiya, K. 2000. Glyceroglycolipids of photosynthetic organisms –their biosynthesis and evolutionary origin-. Trends Glycosci. Glycotechnol. 12:241–253.
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.
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.
Renwick, J. A. A., and Chew, F. S. 1994. Oviposition behavior in Lepidoptera. Annu. Rev. Entomol. 39:377–400.
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.
Renwick, J. A. A. 2002. The chemical world of crucivores: Lures, treats and traps. Entomologia Exp. App. 104:35–42.
Roughan, P. G., and Batt R. D. 1969. The glycerolipid composition of leaves. Phytochemistry 8:363–369.
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.
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.
Schoonhoven, L. M., Loon, J. J. A., and Dicke, M. 2005. Insect-Plant Biology. Oxford University Press Inc., New York.
Selmair, P. L., and Koehler, P. 2008. Baking performance of synthetic glycolipids in comparison to commercial surfactants. J. Agric. Food Chem. 56:6691–6700.
Städler, E. and Roessingh, P. 1990. Perception of surface chemicals by feeding and ovipositing insects. Symp. Biol. Hung. 39:71–86.
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.
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.
Verschaffelt, E. 1910. The cause determining the selection of food in some herbivorous insects. Proc. K. Ned. Akad. Wet. 13:536–542.
Wiklund, C. 1975. The evolutionary relationship between adult oviposition preferences and larval host plant range in Papilio machaon L. Oecologia 18:185–197.
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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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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DOI: https://doi.org/10.1007/s10886-011-0022-5