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Sequestration of Furostanol Saponins by Monophadnus Sawfly Larvae

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Abstract

Sawfly larvae of the tribe Phymatocerini (Hymenoptera: Tenthredinidae), which are specialized on toxic plants in the orders Liliales and Ranunculales, exude a droplet of deterrent hemolymph upon attack by a predator. We investigated whether secondary plant metabolites from Ranunculaceae leaves are sequestered by phymatocerine Monophadnus species, i.e., Monophadnus alpicola feeding upon Pulsatilla alpina and Monophadnus monticola feeding upon Ranunculus lanuginosus. Moreover, two undescribed Monophadnus species were studied: species A collected from Helleborus foetidus and species B collected from Helleborus viridis. Comparative high-performance liquid chromatographic–photodiode array detection–electrospray ionization–mass spectrometric analyses of plant leaf and insect hemolymph extracts revealed the presence of furostanol saponins in all samples. Larvae of species A and B actively sequestered (25R)-26-[(α-l-rhamnopyranosyl)oxy]-22α-methoxyfurost-5-en-3β-yl O-β-d-glucopyranosyl-(1→3)-O-[6-acetyl-β-d-glucopyranosyl-(1→3)]-O-β-d-glucopyranoside (compound 1). This compound occurred at a 65- to 200-fold higher concentration in the hemolymph of the two species (1.6 and 17.5 μmol/g FW, respectively) than in their host plant (0.008 and 0.268 μmol/g FW, respectively). In M. monticola, compound 1 was found at a concentration (1.2 μmol/g FW) similar to that in the host plant (1.36 μmol/g FW). The compound could not be detected consistently in M. alpicola larvae where, however, a related saponin may be present. Additional furostanol saponins were found in H. foetidus and H. viridis, but not in the two Monophadnus species feeding on them, indicating that sequestration of compound 1 is a highly specific process. In laboratory bioassays, crude hemolymph of three Monophadnus species showed a significant feeding deterrent activity against a potential predator, Myrmica rubra ant workers. Isolated furostanol saponins were also active against the ants, at a concentration range similar to that found in the hemolymph. Thus, these compounds seem to play a major role for chemical defense of Monophadnus larvae, although other plant secondary metabolites (glycosylated ecdysteroids) were also detected in their hemolymph. Physiological and ecological implications of the sequestered furostanol saponins are discussed.

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References

  • Applebaum, S. W. and Birk, Y. 1979. Saponins, pp. 539–566, in G. A. Rosenthal and D. H. Janzen (eds.). Herbivores: Their Interactions with Secondary Metabolites. Academic Press, New York.

    Google Scholar 

  • Barker, A., Schaffner, U., and Boevé, J.-L. 2002. Host-specificity and host recognition in a chemically defended herbivore, the tenthredinid sawfly Rhadinoceraea nodicornis. Entomol. Exp. Appl. 104:61–68.

    Article  CAS  Google Scholar 

  • Boevé, J.-L. and Müller, C. 2005. Defence effectiveness of easy bleeding sawfly larvae towards invertebrate and avian predators. Chemoecology 15:51–58.

    Article  CAS  Google Scholar 

  • Boevé, J.-L. and Schaffner, U. 2003. Why does the larval integument of some sawfly species disrupt so easily? The harmful hemolymph hypothesis. Oecologia 134:104–111.

    Article  PubMed  Google Scholar 

  • Bowers, M. D. 1992. The evolution of unpalatability and the cost of chemical defense in insects, pp. 216–244, in B. D. Roitberg and M. B. Isman (eds.). Insect Chemical Ecology. An Evolutionary Approach. Chapman and Hall, New York.

    Google Scholar 

  • Bowers, M. D., Boockvar, K., and Collinge, S. K. 1993. Iridoid glycosides of Chelone glabra(Scrophulariaceae) and their sequestration by larvae of a sawfly, Tenthredo grandis (Tenthredinidae). J. Chem. Ecol. 19:815–823.

    Article  CAS  Google Scholar 

  • Braca, A., Prieto, J. M., De Tommasi, N., Tomè, F., and Morelli, I. 2004. Furostanol saponins and quercetin glycosides from the leaves of Helleborus viridis L. Phytochemistry 65:2921–2928.

    Article  PubMed  CAS  Google Scholar 

  • de Combarieu, E., Falzoni, M., Fuzzati, N., Gattesco, F., Giori, A., Lovati, M., and Pace, R. 2002. Identification of Ruscus steroidal saponins by HPLC–MS analysis. Fitoterapia 73:583–596.

    Article  PubMed  Google Scholar 

  • Duffey, S. S. 1980. Sequestration of plant natural products by insects. Annu. Rev. Entomol. 25:447–477.

    Article  CAS  Google Scholar 

  • Evans, W. C. 1989. Trease and Evans’ Pharmacognosy, 13th edn. Bailliere Tindall, London, pp 514–516.

    Google Scholar 

  • Gillespie, J. J., Kjer, K. M., Duckett, C. N., and Tallamy, D. W. 2003. Convergent evolution of cucurbitacin feeding in spatially isolated rootworm taxa (Coleoptera: Chrysomelidae; Galerucinae, Luperini). Mol. Phylogenet. Evol. 29:161–175.

    Article  PubMed  CAS  Google Scholar 

  • Hardman, R. and Benjamin, T. V. 1976. The co-occurrence of ecdysones with bufadienolides and steroidal saponins in the genus Helleborus. Phytochemistry 15:1515–1516.

    Article  CAS  Google Scholar 

  • Harmatha, J. 2000. Chemo-ecological role of spirostanol saponins in the interaction between plants and insects, pp. 129–141, in W. Olezsek and A. Marston (eds.). Saponins in Food, Feedstuffs and Medicinal Plants. Kluwer, Dordrecht.

    Google Scholar 

  • Laurent, P., Braekman, J.-C., and Daloze, D. 2005. Insect chemical defence. Topics Curr. Chem. 240:167–229.

    CAS  Google Scholar 

  • Liang, F., Li, L.-J., Abliz, Z., Yang, Y.-C., and Shi, J.-G. 2002. Structural characterization of steroidal saponins by electrospray ionization and fast-atom bombardment tandem mass spectrometry. Rap. Commun. Mass Spectrom. 16:1168–1173.

    Article  CAS  Google Scholar 

  • Liston, A. 1995. Compendium of European Sawflies. Chalastos Forestry, Gottfrieding, Germany.

    Google Scholar 

  • Morton, T. C. and Vencl, F. V. 1998. Larval beetles form a defense from recycled host-plant chemicals discharged as fecal wastes. J. Chem. Ecol. 24:765–785.

    Article  CAS  Google Scholar 

  • Müller, C., Agerbirk, N., Olsen, C. E., Boevé, J.-L., Schaffner, U., and Brakefield, P. M. 2001. Sequestration of host plant glucosinolates in the defensive hemolymph of the sawfly Athalia rosae. J. Chem. Ecol. 27:2505–2516.

    Article  PubMed  Google Scholar 

  • Müller, C. and Brakefield, P. M. 2003. Analysis of a chemical defense in sawfly larvae: easy bleeding targets predatory wasps in late summer. J. Chem. Ecol. 29:2683–2694.

    Article  PubMed  Google Scholar 

  • Petricic, J. 1974. Genus Helleborus. Chemistry of subterranean parts. Acta Pharm. Jugosl. 24:179–185.

    CAS  Google Scholar 

  • Schaffner, U., Boevé, J.-L., Gfeller, H., and Schlunegger, U. P. 1994. Sequestration of Veratrum alkaloids by specialist Rhadinoceraea nodicornis Konow (Hymenoptera, Tenthredinidae) and its ecoethological implications. J. Chem. Ecol. 20:3233–3250.

    Article  CAS  Google Scholar 

  • Termonia, A., Pasteels, J. M., Windsor, D. M., and Milinkovitch, M. C. 2002. Dual chemical sequestration: a key mechanism in transitions among ecological specialization. Proc. R. Soc. Lond. B 269:1–6.

    Article  CAS  Google Scholar 

  • Teuscher, E. and Lindequist, U. 1987. Biogene Gifte. Biologie, Chemie, Pharmakologie. Gustav Fischer Verlag, Stuttgart.

    Google Scholar 

  • Tschesche, R., Wagner, R., and Jha, H. C. 1984. A furostanol glycoside from Helleborus macranthus. Phytochemistry 23:695–696.

    Article  CAS  Google Scholar 

  • Vencl, F. V., Morton, T. C., Mumma, R. O., and Schultz, J. C. 1999. Shield defense of a larval tortoise beetle. J. Chem. Ecol. 25:549–566.

    Article  CAS  Google Scholar 

  • Wissner, W. and Kating, H. 1974. Botanical and phytochemical investigations of species of the genus Helleborus growing in Europe and Asian Minor. II. Comparative phytochemical investigations of the cardio active glycosides and saponins. Planta Med. 26:228–249.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgement

We thank Prof. N. de Tommasi (Dipartimento di Scienze Farmaceutiche, Università di Salerno, Italy) for advice and registering the NMR spectra available for our studies; Dr A. Taeger for advice on sawfly identification; and Prof. M. Hilker and two anonymous referees for their constructive reviews. The authors acknowledge the financial support provided by the European Community’s Improving Human Potential Programme under contract HPRN-CT-1999-00054 (INCHECO) and the Swiss Bundesamt für Bildung und Wissenschaft.

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Correspondence to Jean-Luc Boevé.

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Dedicated to the memory of Professor Ivano Morelli (1940–2005)

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Prieto, J.M., Schaffner, U., Barker, A. et al. Sequestration of Furostanol Saponins by Monophadnus Sawfly Larvae. J Chem Ecol 33, 513–524 (2007). https://doi.org/10.1007/s10886-006-9232-7

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