Effects of pyrrolizidine alkaloids and sesquiterpenes on snail feeding

Oecologia - Tập 92 - Trang 257-265 - 1992
B. Speiser1, J. Harmatha2, M. Rowell-Rahier1
1Zoologisches Institut der Universität Basel, Switzerland
2Institute of Organic Chemistry and Biochemistry, Czechoslovak Academy of Sciences, Prague, Czechoslovakia

Tóm tắt

We determined in the laboratory the feeding response of two populations of the generalist herbivorous snail Arianta arbustorum (Helicidae) towards the composite Adenostyles alliariae and towards various allelochemicals. These were: a pyrrolizidine alkaloid (PA) extract of Adenostyles leaves; senecionine (a PA present in Adenostyles); retrorsine (a PA not present in Adenostyles) and two sesquiterpene (ST) fractions from Adenostyles: a mixture of the STs adenostylone and neoadenostylone, and deacyladenostylone. Tertiary PAs and PA N-oxides were tested separately. For each allelochemical, we tested whether it was deterrent or whether it induced changes of feeding behaviour (i.e. whether it had pre- or postingestive effects), and whether the effects were more pronounced with younger (smaller) snails. The tertiary PA extract from Adenostyles was deterrent, especially for young snails, but did not induce changes of feeding behaviour. Tertiary PA senecionine was deterrent for young snails only and induced changes of feeding behaviour. Also, consumption of untreated Petasites was higher after this treatment. Tertiary PA retrorsine was not deterrent, but induced changes of feeding behaviour. The PA N-oxides showed no activity against the snails. The mixture of adenostylone and neoadenostylone was deterrent and induced feeding aversions. Deacyladenostylone was highly deterrent, but did not induce changes of feeding behaviour. At the Jura site, PA content of Adenostyles was lower than at the Black Forest site. The snails from Jura consumed much less Adenostyles than the snails from Black Forest, and also ate a little less of the treated leaf discs. The PAs which are encountered by the snails in their natural food plants (PA extract and senecionine) were more deterrent than retrorsine (a novel compound). This suggests that the snails have mechanisms for the rejection of allelochemicals which they encounter in their natural food plants, but not for novel allelochemicals. The results suggest two hypotheses regarding the function of the allelochemicals in Adenostyles: (1) The allelochemicals act mainly on very young snails. (2) PAs render Adenostyles toxic, while STs act as feeding deterrents.

Tài liệu tham khảo

Alarcon MCBV, Lopes JLC, Herz W (1990) Glaucolide b, a molluscicidal sesquiterpene lactone, and other constituents of Vernonia eremophila. Planta Med 56: 271–273 Arter HE (1990) Spatial relationship and gene flow paths between populations of the alpine snail Arianta arbustorum (Pulmonata: Helicidae). Evol 44: 966–980 Baig MA, Banthorpe DV, Gutowski JA (1989) Accumulation in cultivars of Santolina chamaecyparissus of a rare sesquiterpene with gastropod-repellent activity. Fitoterapia 60: 373–375 Balaban PM, Vehovszky A, Maximova OA, Zakharov IS (1987) Effect of 5, 7-dihydroxytryptamine on the food-aversive conditioning in the snail Helix lucorum L. Brain Res 404: 201–210 Barros DAD, Lopes JLC, Vichnewski W, Lopes JNC, Kulanthaivel P, Herz W (1985) Sesquiterpene lactones in the molluscicidal extract of Eremanthus glomerulatus. Planta Med 0: 38–39 Bentley MD, Leonard DE, Stoddard WF, Zalkow LH (1984) Pyrrolizidine alkaloids as larval feeding deterrents for spruce budworm, Choristoneura fumiferana (Lepidoptera: Tortricidae). Ann Entomol Soc Am 77: 393–397 Berenbaum M (1986) Postingestive effects of phytochemicals on insects: on Paracelsus and plants. In: Miller JR, Miller TA (eds) Insect-Plant Interactions, Springer, Berlin Heidelberg New York, pp 121–153 Bernays EA, Bright KL (1991) Dietary mixing in grasshoppers: switching induced by nutritional imbalances in foods. Entomol Exp Appl 61: 247–253 Bernays EA, Chapman RF (1977) Deterrent chemicals as a basis of oligophagy in Locusta migratoria (L.). Ecol Entomol 2: 1–18 Bernays E, Edgar JA, Rothschild M (1977) Pyrrolizidine alkaloids sequestered and stored by the aposematic grasshopper Zonocercus variegatus. J Zool 182: 85–87 Brattsten LB (1988) Enzymic adaptations in leaf-feeding insects to host-plant allelochemicals. J Chem Ecol 14: 1919–1939 Champagne DE, Bernays EA (1991) Phytosterol unsuitability as a factor mediating food aversion learning in the grasshopper Schistocerca americana. Physiol Entomol 16: 391–400 Charrier M (1990) Evolution, during digestion, of the bacterial flora in the alimentary system of Helix aspersa (Gastropoda: Pulmonata): A scanning electron microscope study. J Moll Stud 56: 425–433 Cruz Reyes A, Chavarin C, Arias MPC, Taboada J, Jimenez EM (1989) The molluscicide activity of piquerol a isolated from Piqueria trinervia (Compositae) against eight species of pulmonate snails. Mem Inst Oswaldo Cruz Rio J 84: 35–40 Delaney K, Gelperin A (1986) Post-ingestive food-aversion learning to amino acid deficient diets by the terrestrial slug Limax maximus. J Comp Physiol A 159: 281–295 Dreyer DL, Jones KC, Molyneux RJ (1985) Feeding deterrency of some pyrrolizidine, indolizidine, and quinolizidine alkaloids towards pea aphid (Acyrtosiphon pisum) and evidence for phloem transport of indolizidine alkaloid swainsonine. J Chem Ecol 11: 1045–1051 Edwards PJ, Gillman MP (1987) Herbivores and plant succession. In: Gray AJ, Crawley MJ, Edwards PJ (eds) Colonization, succession and stability. Blackwell Sci Publ, Oxford, pp 295–314 Gelperin A (1975) Rapid food-aversion learning by a terrestrial mollusk. Science 189: 567–570 Glendinning JI, Brower LP, Montgomery CA (1990) Responses of three mouse species to deterrent chemicals in the monarch butterfly. I. Taste and toxicity tests using artificial diets laced with digitoxin or monocrotaline. Chemoecology 1: 114–123 Guerrero C, Campos G, Taboada J (1988) Chemical studies on Eupatorium brevipes and some biological activities of brevipenin. Rev Latinoam Quim 19: 147–149 Harmatha J, Nawrot J (1984) Comparison of the feeding deterrent activity of some sesquiterpene lactones and a lignan lactone towards selected insect storage pests. Biochem Syst Ecol 12: 95–98 Harmatha J, Samek Z, Novotny H, Herout V, Sorm F (1969) The structure of adenostylone, isoadenostylone and neoadenostylone — components of the rhizome of Adenostyles alliariae (Gouan) Kern. Coll Czech Chem Comm 34: 1739–1749 Hartmann T, Zimmer M (1986) Organ-specific distribution and accumulation of pyrrolizidine alkaloids during the life history of two annual Senecio species. J Plant Physiol 122: 67–80 Hartmann T, Ehmke A, Eilert U, Von Borstel K, Theuring C (1989) Sites of synthesis, translocation and accumulation of pyrrolizidine alkaloid N-Oxides in Senecio vulgaris L. Planta 177:98–107 Jansen BJM, De Groot A (1991) The occurrence and biological activity of drimane sesquiterpenoids. Nat Prod Rep 8: 309–318 Lee JH, Chang JJ (1986) Learning of post-ingestive food-aversion by the land slug Incilaria frühstorferi daiseniana to amino acid deficient diets. Soc Neurosci Abstr 12: 39 Lüthy J, Zweifel U, Schmid P, Schlatter C (1983) Pyrrolizidin-Alkaloide in Petasites hybridus L. und P. albus L. Pharm Acta Helv 58: 98–100 Marchant YY, Balza F, Abeysekera BF, Towers GHN (1984) Molluscicidal activity of sesquiterpene lactones. Biochem Syst Ecol 12: 285–286 Masters AR (1991) Dual role of pyrrolizidine alkaloids in nectar. J Chem Ecol 17: 195–205 Mattocks AR (1967) Detection of pyrrolizidine alkaloids on thinlayer chromatograms. J Chromatogr 27: 505–508 Mattocks AR (1986) Chemistry and Toxicology of Pyrrolizidine Alkaloids. Academic Press, London Nawrot J, Harmatha J, Novotny L (1984) Insect feeding deterrent activity of Bisabolangelone and of some sesquiterpenes of eremophilane type. Biochem Syst Ecol 12: 99–101 Nawrot J, Bloszyk E, Harmatha J, Novotny L, Drozdz B (1986) Action of antifeedants of plant origin on beetles infesting stored products. Acta Entomol Bohemoslov 83: 327–335 Nawrot J, Drozdz B, Holub M (1987) Feeding-deterrent activity of some natural sesquiterpene lactones for selected storage pests. Herba Pol 31: 209–214 Nawrot J, Koul O, Isman MB, Harmatha J (1991) Naturally occurring antifeedants effects on two polyphagous lepidopterans. J Appl Entomol 112: 194–201 Neuenschwander M, Neuenschwander A, Steinegger E (1979a) Struktur der Sesquiterpene von Petasites hybridus (L.) G.M. et SCH.: Petasol und Isopetasol-Abkömmlinge. Helv Chim Acta 62: 609–626 Neuenschwander M, Neuenschwander A, Steinegger E (1979b) Struktur der Sesquiterpene von Petasites hybridus (L.) G.M. et SCH.: Neopetasol-Abkömmlinge. Helv Chim Acta 62: 627–634 Novotny L, Samek Z, Harmatha J, Sorm F (1969) 9-Hydroxyfuroeremophilane, a further dominating component from light petrolcum extract of Petasites hybridus (L.) Gaertn., Mey et Scherr rhizomes. Coll Czech Chem Comm 31: 336–339 Raffaelli D, Mordue AJ (1990) The relative importance of molluscs and insects as selective grazers of acyanogenic white clover (Trifolium repens). J Moll Stud 56: 37–46 Rees SB, Harborne JB (1985) The role of sesquiterpene lactones and phenolics in the chemical ecology of the chicory plant. Phytochemistry 24: 2225–2231 Robert PC, Blaisinger P, Bouchery Y, Simonis MT, Kienlen JC, Muckensturm B, Riss B, Pflieger D (1987) Influence de la bisabolangélone, un antiappétant sesquiterpénöide, sur le développement des chenilles de Mythimna (Pseudaletia) unipuncta Haw. (Lepidoptera, Noctuidae). Agronomie Paris 7: 167–174 Rowell-Rahier M, Witte L, Ehmke A, Hartmann T, Pasteels J (1991) Sequestration of plant pyrrolizidine alkaloids by chrysomelid beetles and selective transfer into the defensive secretions. Chemoecol 2: 41–48 Sahley C, Gelperin A, Rudy JW (1981a) One-trial associative learning modifies food odor preferences of a terrestrial mollusc. Proc Natl Acad Sci USA 78: 640–642 Sahley C, Rudy JW, Gelperin A (1981b) An analysis of associative learning in a terrestrial mollusc. J Comp Physiol A 144: 1–8 Samek Z, Harmatha J, Novotny L, Sorm F (1969) Absolute configuration of Adenostylone, Neoadenostylone and Isoadenostylone from Adenostyles alliariae and of Decompostin from Cacalia decomposita. Coll Czech Chem Comm 34: 2792–2808 Sharrow SH, Ueckert DN, Johnson AE (1988) Ecology and toxicology of Senecio species with special reference to Senecio jacobaea and Senecio longilobus. In: James LF, Ralphs MH, Nielsen DB (eds) The Ecology and Economic Impact of Poisonous Plants on Livestock Production. Westview Press, Boulder London, pp 181–196 Simpson SJ, Simpson CL (1990) The mechanisms of nutritional compensation by phytophagous insects. In: Bernays EA (ed) Insect-Plant Interactions, vol II. CRC Press, Boca Raton Ann Arbor Boston, pp 111–160 Speiser B, Rowell-Rahier M (1991) Effects of food availability, nutritional value, and alkaloids on food choice in the generalist herbivore Arianta arbustorum (Gastropoda: Helicidae). Oikos 62: 306–318 Sterner O, Bergman R, Kihlberg J, Wickberg B (1985) The sesquiterpenes of Lactarius vellereus and their role in a proposed chemical defense system. J Nat Prod 48: 279–288 Toman J, Harmatha J, Novotny L (1968) Verwandtschaftsbeziehungen der Gattung Adenostyles und die Berechtigung ihrer Einreihung in die Tribus Senecioneae. Preslia (Praha) 40: 122–132 Whelan RJ (1982) Response of slugs to unacceptable food items. J Appl Ecol 19: 79–87 Wurzel G, Becker H, Eicher T, Tiefensee K (1990) Molluscicidal properties of constituents from the liverwort Ricciocarpos natans and of synthetic lunularic acid derivatives. Planta Med 56: 444–445