Journal of Chemical Ecology

, Volume 27, Issue 12, pp 2505–2516 | Cite as

Sequestration of Host Plant Glucosinolates in the Defensive Hemolymph of the Sawfly Athalia rosae

  • Caroline Müller
  • Niels Agerbirk
  • Carl Erik Olsen
  • Jean-Luc Boevé
  • Urs Schaffner
  • Paul M. Brakefield
Article

Abstract

Interactions between insects and glucosinolate-containing plant species have been investigated for a long time. Although the glucosinolate–myrosinase system is believed to act as a defense mechanism against generalist herbivores and fungi, several specialist insects use these secondary metabolites for host plant finding and acceptance and can handle them physiologically. However, sequestration of glucosinolates in specialist herbivores has been less well studied. Larvae of the turnip sawfly Athalia rosae feed on several glucosinolate-containing plant species. When larvae are disturbed by antagonists, they release one or more small droplets of hemolymph from their integument. This “reflex bleeding” is used as a defense mechanism. Specific glucosinolate analysis, by conversion to desulfoglucosinolates and analysis of these by high-performance liquid chromatography coupled to diode array UV spectroscopy and mass spectrometry, revealed that larvae incorporate and concentrate the plant's characteristic glucosinolates from their hosts. Extracts of larvae that were reared on Sinapis alba contained sinalbin, even when the larvae were first starved for 22 hr and, thus, had empty guts. Hemolymph was analyzed from larvae that were reared on either S. alba, Brassica nigra, or Barbarea stricta. Leaves were analyzed from the same plants the larvae had fed on. Sinalbin (from S. alba), sinigrin (B. nigra), or glucobarbarin and glucobrassicin (B. stricta) were present in leaves in concentrations less than 1 μmol/g fresh weight, while the same glucosinolates could be detected in the larvae's hemolymph in concentrations between 10 and 31 μmol/g fresh weight, except that glucobrassicin was present only as a trace. In larval feces, only trace amounts of glucosinolates (sinalbin and sinigrin) could be detected. The glucosinolates were likewise found in freshly emerged adults, showing that the sequestered phytochemicals were transferred through the pupal stage.

Athalia rosae sawfly Hymenoptera Sinapis alba Barbarea stricta Brassica nigra Brassicaceae glucosinolates hemolymph sequestration 

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REFERENCES

  1. ABE, F., YAMAUCHI, T., HONDA, K., OMURA, H., and HAYASHI, N. 2001. Sequestration of phenanthroindolizidine alkaloids by an Asclepiadaceae-feeding danaid butterfly, Ideopsis similis. Phytochemistry 56:697–701.PubMedGoogle Scholar
  2. AGERBIRK, N., OLSEN, C. E., and NIELSEN, J. K. 2001a. Seasonal variation in leaf glucosinolates and insect resistance in two types of Barbarea vulgaris ssp. arcuata. Phytochemistry 58:91–100.PubMedGoogle Scholar
  3. AGERBIRK, N., PETERSEN, B. L., OLSEN, C. E., HALKIER, B. A., and NIELSEN, J. K. 2001b. 1,4-Dimethoxyglucobrassicin in Barbarea and 4-hydroxyglucobrassicin in Arabidopsis and Brassica. J. Agric. Food Chem. 49:1502–1507.PubMedGoogle Scholar
  4. AMANO, T., NISHIDA, R., KUWAHARA, Y., and FUKAMI, H. 1999. Pharmacophagous acquisition of clerodendrins by the turnip sawfly (Athalia rosae ruficornis) and their role in the mating behavior. Chemoecology 9:145–150.Google Scholar
  5. APLIN, R. T., D'ARCY WARD, R., and ROTHSCHILD, M. 1975. Examination of the large white butterfly and small white butterflies (Pieris spp.) for the presence of mustard oils and mustard oil glycosides. J. Entomol. A 50:73–78.Google Scholar
  6. BLUM, M. S. 1981. Chemical Defenses of Arthropods. Academic Press, New York.Google Scholar
  7. 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
  8. BOWERS, M. D., BOOCKVAR, K., and COLLINGE, S. K. 1993. Iridoid glycosides of Chelone glabra (Scrophulariaceae) and their sequestration by larvae of the sawfly, Tenthredo grandis (Tenthredinidae). J. Chem. Ecol. 19:815–823.Google Scholar
  9. BRATTSTEN, L. B. 1992. Metabolic defenses against plant allelochemicals, pp. 175–242, in G. A. Rosenthal and M. R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites, Vol. II: Evolutionary and Ecological Processes. Academic Press, New York.Google Scholar
  10. BROWER, L. P. and FINK, L. S. 1985. A natural toxic defense system: Cardenolides in butterflies versus birds. Ann. NY Acad. Sci. 443:171–186.PubMedGoogle Scholar
  11. BUCHNER, R. 1987. Approach to determination of HPLC response factors for glucosinolates, pp. 50–58, in J.-P. Wathelet (ed.). Glucosinolates in Rapeseeds: Analytical Aspects. Martinus Nijhoff Publishers, Dordrecht, The Netherlands.Google Scholar
  12. CARROLL, M., HANLON, A., HANLON, T., ZANGERL, A. R., and BERENBAUM, M. R. 1997. Behavioral effects of carotenoid sequestration by the parsnip webworm, Depressaria pastinacella. J. Chem. Ecol. 23:2707–2719.Google Scholar
  13. CHEW, F. S. 1988a. Searching for defensive chemistry in the Cruciferae, or, do glucosinolates always control interactions of Cruciferae with their potential herbivores and symbionts? No!, pp. 81–112, in K. C. Spencer (ed.). Chemical Mediation of Coevolution. Academic Press, Toronto, Canada.Google Scholar
  14. CHEW, F. S. 1988b. Biological effects of glucosinolates, pp. 155–181, in H. G. Cutler (ed.). Biologically Active Natural Producs-Potential Use in Agriculture. American Chemical Society Symposium, Washington, D.C.Google Scholar
  15. CODELLA, S. G., and RAFFA, K. F. 1993. Defense strategies of folivorous sawflies, pp. 261–294, in M. R. Wagner and K. F. Raffa (eds.). Sawfly Life History. Adaptations toWoody Plants. Academic Press, San Diego, California.Google Scholar
  16. DOBLER, S., DALOZE, D., and PASTEELS, J.M. 1998. Sequestration of plant compounds in a leaf beetle's defensive secretion: Cardenolides in Chrysochus. Chemoecology 8:111–118.Google Scholar
  17. DOBLER, S., HABERER,W., WITTE, L., and HARTMANN, T. 2000. Selective sequestration of pyrrolizidine alkaloids from diverse host plants by Longitarsus flea beetles. J. Chem. Ecol. 26:1281–1298.Google Scholar
  18. DUFFEY, S. S. 1980. Sequestration of plant natural products by insects. Annu. Rev. Entomol. 25:447–477.Google Scholar
  19. EISNER, T., JOHANESSEE, J. S., CARREL, J., HENDRY, L. B., and MEINWALD, J. 1974. Defensive use by an insect of a plant resin. Science 184:996–999.PubMedGoogle Scholar
  20. FAHEY, J. W., ZALCMANN, A. T., and TALALAY, P. 2001. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51.PubMedGoogle Scholar
  21. HALKIER, B. A. 1999. Glucosinolates, pp. 193–223, in R. Ikan (ed.). Naturally Occuring Glycosides. John Wiley & Sons Ltd., London.Google Scholar
  22. HEADS, P. A. 1986. Bracken, ants and extrafloral nectaries. IV. Dowood ants (Formica lugubris) protect the plant against insect herbivores? J. Anim. Ecol. 55:795–809.Google Scholar
  23. HEADS, P. A. and LAWTON, J. H. 1985. Bracken, ants and extrafloral nectaries. III. Howinsect herbivores avoid ant predation. Ecol. Entomol. 10:29–42.Google Scholar
  24. HODGSON, E. and ROSE, R. 1991. Insect Cytochrome P 450, pp. 75–91, in E. Arinc, J. B. Schenkman, and E. Hodgson (eds.). Molecular Aspects of Monooxygenases and Bioactivation of Toxic Compounds. Plenum Press, New York.Google Scholar
  25. ISMAN, M. B. 1992. A physiological perspective, pp. 156–176, in B. D. Roitberg and M. B. Isman (eds.). Insect Chemical Ecology. An Evolutionary Approach. Chapman and Hall, New York.Google Scholar
  26. KUNZE, A., AREGULLIN, M., RODRIGUEZ, E., and PROKSCH, P. 1996. Fate of the chromene encecalin in the interactions of Encelia farinosa and its specialized herbivore Trirhabda geminata. J. Chem. Ecol. 22:491–498.Google Scholar
  27. LI, Q., EIGENBRODE, S. D., STRINGHAM, G. R., and THIAGARAJAH, M. R. 2000. Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. J. Chem. Ecol. 26:2401–2419.Google Scholar
  28. LISTON, A. 1995. Compendium of European sawflies. Chalastos Forestry, Gottfrieding, Germany.Google Scholar
  29. LOUDA, S. and MOLE, S. 1991. Glucosinolates: Chemistry and ecology, pp. 123–164, in G. A. Rosenthal and M. R. Berenbaum (eds.): Herbivores and Their Interactions with Secondary Plant Metabolites 2E (1): Chemical Participants. Academic Press, New York.Google Scholar
  30. MANICI, L. M., LAZZERI, L., and PALMIERI, S. 1997. In vitro fungitoxic activity of some glucosinolates and their enzyme-derived products towards plant pathogenic fungi. J. Agric. Food Chem. 45:2768–2773.Google Scholar
  31. MCGREGOR, D. I. 1985. Determination of glucosinolates in Brassica seed. Eucarpia Cruciferae Newsl. 10:132–136.Google Scholar
  32. MITHEN, R. F., DEKKER, M., VERVERK, R., RABOT, S., and JOHNSON, I. T. 2000. The nutritional significance, biosynthesis and bioavailability of glucosinolates in human foods. J. Sci. Food Agric. 80:967–984.Google Scholar
  33. MORROW, P. A., BELLAS, T. E., and EISNER, T. 1976. Eucalyptus oil in the defensive oral discharge of Australian sawfly larvae (Hymenoptera: Pergidae). Oecologia 24:193–206.Google Scholar
  34. MURRAY, C. L., QUAGLIA, M., ARNASON, J. T., and MORRIS, C. E. 1994. A putative nicotine pump at the metabolic blood-brain barrier of the tobacco hornworm. J. Neurobiol. 25:23–34.PubMedGoogle Scholar
  35. NIELSEN, J. K. 1988. Crucifer-feeding Chrysomelidae: Mechanisms of host plant finding and acceptance, pp. 25–40, in P. Jolivet, E. Petitpierre, and T. H. Hsiao (eds.): Biology of Chrysomelidae. Kluwer Academic Publishers, Dordrecht, The Netherlands.Google Scholar
  36. NIELSEN, J. K., HANSEN, M. L., AGERBIRK, N., PETERSEN, B. L., and HALKIER, B. A. 2001. Responses of the flea beetles Phyllotreta nemorum and P. cruciferae to metabolically engineered Arabidopsis thaliana with an altered glucosinolate profile. Chemoecology 11:75–83.Google Scholar
  37. NISHIDA, R. and FUKAMI, H. 1990. Sequestration of distasteful compounds by some pharmacophagous insects. J. Chem. Ecol. 16:151–164.Google Scholar
  38. OHARA, Y., NAGASAKI, K., and OHSAKI, N. 1993. Warning coloration in sawfly Athalia rosae larva and concealing coloration in butterfly Pieris rapae larva on similar plants evolved through individual selection. Res. Popul. Ecol. 19:223–230.Google Scholar
  39. POTTER, M. J., VANSTONE, V. A., DAVIES, K. A., and RATHJEN, A. J. 2000. Breeding to increase the concentration of 2-phenylethyl glucosinolate in the roots of Brassica napus. J. Chem. Ecol. 26:1811–1820.Google Scholar
  40. PROP, N. 1960. Protection against birds and parasites in some species of tenthredinid larvae. Arch. Neerl. Zool. 13:380–447.Google Scholar
  41. RASK, L., ANDRéASSON, E., EKBOM, B., ERIKSSON, S., PONTOPPIDAN, B., and MEIJER, J. 2000. Myrosinase: Gene family evolution and herbivore defense in Brassicaceae. Plant Mol. Biol. 42:93–113.PubMedGoogle Scholar
  42. RENWICK, J. A. A., RADKE, C. D., SACHDEV-GUPTA, K., and STäDLER, E. 1992. Leaf surface chemicals stimulating oviposition by Pieris rapae (Lepidoptera: Pieridae) on cabbage. Chemoecology 3:33–38.Google Scholar
  43. RODMAN, J. E., SOLTIS, P. S., SOLTIS, D. E., SYTSMA, K. J., and KAROL, K. G. 1998. Parallel evolution of glucosinolate biosynthesis inferred from congruent nuclear and plastid gene phylogenies. Am. J. Bot. 85:997–1006.Google Scholar
  44. ROTHSCHILD, M. and EDGAR, J. A. 1978. Pyrrolizidine alkaloids from Senecio vulgaris sequestered and stored by Danaus plexippus. J. Zool. 186:347–349.Google Scholar
  45. SANG, J. P., MINCHINTON, I. R., JOHNSTONE, P. K., and TRUSCOTT, R. J. W. 1984. Glucosinolate profiles in the seed, root and leaf tissue of cabbage, mustard, rapeseed, radish and swede. Can. J. Plant Sci. 64:77–93.Google Scholar
  46. SCHAFFNER, U. and BOEVé, J.-L. 1996. Sequestration of plant alkaloids by the sawfly Rhadinoceraea nodicornis: Ecological relevance for different life stages and occurence among related species. Entomol. Exp. Appl. 80:283–285.Google Scholar
  47. 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.Google Scholar
  48. SCHITTKO, U., BURGHARDT, F., FIEDLER, K., WRAY, V., and PROKSCH, P. 1999. Sequestration and distribution of flavonoids in the common blue butterfly Polyommatus icarus reared on Trifolium repens. Phytochemistry 51:609–614.Google Scholar
  49. SCUDDER, G. G. E., MOORE, L. V., and ISMAN, M. B. 1986. Sequestration of cardenolides in Oncopeltus fasciatus: Morphological and physiological adaptations. J. Chem. Ecol. 12:1171–1187.Google Scholar
  50. SEVASTOPULO, D. G. 1958. Defensive action of a sawfly larva (Hym., Symphyta). Entomol. Month. Mag. 94:275.Google Scholar
  51. TRIGO, J. R. 2000. The chemistry of antipredator defense by secondary compounds in neotropical Lepidoptera: Facts, perspectives and caveats. J. Braz. Chem. Soc. 11:551–561.Google Scholar
  52. WITTHOHN, K. and NAUMANN, C. M. 1987. Cyanogenesis—a general phenomenon in the Lepidoptera? J. Chem. Ecol. 13:1789–1809.Google Scholar

Copyright information

© Plenum Publishing Corporation 2001

Authors and Affiliations

  • Caroline Müller
    • 1
  • Niels Agerbirk
    • 2
  • Carl Erik Olsen
    • 2
  • Jean-Luc Boevé
    • 3
  • Urs Schaffner
    • 4
  • Paul M. Brakefield
    • 1
  1. 1.Institute of Evolutionary and Ecological SciencesLeiden UniversityLeidenThe Netherlands
  2. 2.Chemistry DepartmentRoyal Veterinary and Agricultural UniversityFrederiksberg CDenmark
  3. 3.Department of EntomologyRoyal Belgian Institute of Natural SciencesBruxellesBelgium
  4. 4.CABI-Bioscience Switzerland CentreDelémontSwitzerland

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