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Pyrrolizidine Alkaloids of Probable Host-Plant Origin in the Pronotal and Elytral Sécrétion of the Leaf Beetle Oreina Cacaliae

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Pyrrolizidine Alkaloids of Probable Host-Plant Origin in the Pronotal and Elytral Sécrétion of the Leaf Beetle Oreina Cacaliae Entomol. exp. appl. 49: 55-58 (1988) © Kluwer Académie Publishers, Dordrecht - Printed in the Netherlands 55 Pyrrolizidine alkaloids of probable host-plant origin in the pronotal and elytral sécrétion of the leaf beetle Oreina cacaliae J. M. Pasteels', M. Rowell-Rahier^, T. Randoux^, J. C. Braekman^ & D. Daloze^ ^Laboratoire de Biologie Animale et Cellulaire, University of Brussels, B-1050 Brussels, Belgium; ^Zoologisches Institut, CH-405I Basel, Switzerland; ^Laboratoire de Chimie Bio-organique, University of Brussels, Belgium Key words: pyrrolizidine alkaloids, seneciphylline N-oxide, Oreina, Chrysomelidae, leaf beetles, défensive sécrétion, séquestration, host­plant influence, Adenostyles leucophylla Abstract Oreina cacaliae (Coleoptera, Chrysomelidae) produces in its elytral and pronotal défensive sécrétion seneciphylline N­oxide together with small amounts of another pyrrolizidine alkaloid tentatively identified as senecionine N­oxide. This is a strong departure from the chemical composition of the défensive sécrétions in related species, characterized by complex mixtures of cardenolides, synthesized by the beetles from cholestérol. It is suggested that O. cacaliae sequesters the alkaloids from its host­plant, Adenostyles leucophylla. Other spécimens of O. cacaliae from far distant populations feeding on Senecio nemorensis, Petasites paradoxus or P. album also produced pyrrolizidine alkaloids, but not O. speciosissima feeding on the same food plants and producing cardenolides. In addition to pyrrolizidine alkaloids, O. cacaliae secrètes ethanolamine, which is also found in ail the cardenolide­producing species. Introduction Sukawara, 1980) most probably dérives from a glucoside présent in the Jugions leaves on which they Numerous leaf beetles (Chrysomelidae) are well feed. Another well documented example is the sé­ known for their chemical defences. Most of the questration and accumulation of the cucumber cu­ chemically defended species studied so far bio­ curbitacins by ail life stages of several Diabrotica synthesize toxins de novo (review in Pasteels et al., species and Acalymna vittatum (Ferguson & Met­ 1988). However there have been several reports re­ calf, 1985). Bowers (in press) found iridoid gluco­ cently on the utilization of food plant precursors or, sides in the alticine Dibolia borealis feeding on of direct séquestration of, plant toxins by oligopha­ Scrophulariaceae, although further quantitative gous leaf beetles to produce toxins (Pasteels et al, in work is necessary to détermine if thèse compounds press). For example, the larvae of the genus are accumulated in quantities large enough for Chrysomela and of Phratora vitellinae dérive the défensive purpose. There has been a report of sé­ salicylaldehyde, secreted by their sériai défensive questration of hypericin by the specialized glands, from salicin, a phenolglucoside présent in Hypericum-îeeder Chrysolina brunsvicensis (Rees, their food plant (Salix and Populus (Rowell­Rahier 1969), but Duffey & Pasteels (in préparation) have & Pasteels, 1982; Pasteels a/., 1983; Rowell­Rahier not been able to confirm it. & Pasteels, 1986)). Similarly, the juglone produced We présent here results suggesting a new example by larvae of Gastrolina depressa (Matsuda & of chemical influence of the food plant on a leaf bee­ 56 tle défensive sécrétion. paratus. Rotation measurements were made on a Oreina spp. are large and very brightly coloured Perkin-Elmer 141 polarimeter. leaf beetles. They are particularly abundant and rich in species in the alpine région of central Europe, and their distribution ranges from 600 to 2500 m in élé• Réduction of seneciphylline N-oxide vation. In this genus, the adults but not the larvae have défensive glands. Like many other leaf beetles Seneciphylline N-oxide (8 mg) was treated (Christie of the closely related genus Chrysolina, they secrète et ai, 1949) for 2 h at room température with an ex- cardenolides (Pasteels et ai, 1984; Van Oycke et al., cess of zinc and CUSO4 in 2N H2SO4 (4 ml). The 1988), which they biosynthesise from cholestérol reaction mixture was basified with NH4OH, ex- (Van Oycke et al, 1987). We have now found one spe• tracted three times with CH2CI2 and the combined cies, Oreina cacaliae which stands out as an excep• organic phases were evaporated to dryness. The resi- tion: the major component of the sécrétion is the due was purified by silica gel column chromatogra• pyrrolizidine alkaloid seneciphylline N-oxide. This phy (eluent:dichloromethane-methanol 95:5), yield- species is a specialist on Asteraceae known to con- ing 6 mg of seneciphylUne, identified on the basis of tain pyrrolizidine alkaloids. Until now, there was no its physical properties (see Results). known example of séquestration of plant natural products into the elytral and pronotal glands of aduh leaf beetles, although plant derived défensive Results toxins were found either in the larval exocrine sécré• tions or in the adult body fluids. 1200 Milkings of O. cacaliae afforded 66 mg of crude sécrétion after the evaporation of the solvent. No cardenolides were detected on the tic plates Material and methods (Kedde reagent). However, a single major compo• nent was visualised by UV light, ceric sulfate and The beetles were collected near Vallouise (Briançon, Dragendorff reagent. An additional more polar con• France) at élévations between 1800 and 2300 m. In stituent was revealed by spraying the plates with nin• that locality and altitude, ail the O. cacaliae belong hydrin. Flash chromatography afforded 28 mg of to a blue colour morph and feed exclusively on the major constituent identified as seneciphylline N- Adenostyles leucophylla (Asteraceae). The beetles oxide on the following grounds: amorphous solid; were manipulated with fine forceps in order to cause [a]l% = -68° (CH3OH, c = 0.65); FAB/MS, posi• émission of sécrétion which was collected on filter tive mode: (M -1- H)+ at m/z 350; négative mode: papers and immediately placed in methanol for stor- M- at m/z 349; DCI/MS: (M -l- H) + : m/z 350; age until further use. The beetles were kept in labora- (M + H - 0)+: m/z 334; IR: 3500-2900, 1730 tory cultures on their food plants and 'milked' at and 1715 cm"'; UV: \^^^ 210 nm (£9.900); 'H and weekly intervais. '^C NMR spectra nearly identical with those of Thin layer chromatographic analyses were donc seneciphylline N-oxide (Molyneuxe/a/., 1982; Segall on silica gel F254 plates (Macherey-Nagel); eluent: & Dallas, 1983). dichloromethane-methanol 8:2; visualisation by UV This identification was confirmed by zinc dust light at 254 nm, or sprayed with ceric sulfate, réduction of the natural constituent (see Methods) Dragendorff reagent, Kedde reagent or ninhydrin. into seneciphylline, identified on the basis of its Seneciphylline N-oxide was isolated by flash silica physical properties: m.p. 206-208°; {a]l%: -132° gel column chromatography (eluent:dichloro- (CHCI3, c = 0.23) ((literature: m.p. 208-209°; methane-methanol 8:2). [a]?? = -129°(CHCl3,c = 1.86), Orekhov & Tide- The NMR spectra were recorded on a Bruker WM bel, 1935)); 'H NMR nearly identical with that 250 spectrometer in CD3OD with TMS as internai reported for seneciphylline (Segall & Dallas, 1983). standard. Mass spectra were run on a VG 70 S ap- The 'H NMR spectrum of the sample shows, be- 57 sides the signais of seneciphylline N-oxide, those of Thèse sécrétions are somewhat différent quantita- a minor component (about 15%) which is tentatively tively and qualitatively to that of the Vallouise popu• identified as senecionine N-oxide. lation. We do not know at this point if the observed The ninhydrin positive constituent was identified différences are the resuit of différences in the as ethanolamine, by comparison with an authentic alkaloid patterns in the différent host plants and/or sample on tel (eluent:n-BuOH-AcOH-:H20, 8:2:2). to différences between the beetle populations in the way they sequester and metabolize the alkaloids. A closely related species, O. speciosissima (in fact so Discussion difficult to separate from O. cacaliae that it was con- fused with it in previous publications, Pasteels & Da- Comparative studies of chrysomelid beetles have loze, 1977; Pasteels a/., 1984,1988) feeds on exactly demonstrated a good corrélation between current the same range of asteraceous food plants, but does classification and the chemical nature of the sécré• not sequester pyrrolizidine alkaloids. Like the adults tions (Pasteels et ai, 1984, 1988). In most species of of other Oreina species feeding on Apiaceae or on Oreina and Chrysomela (Chrysolinina, Chrysomeli- Centaurea, those of O. speciosissima secrète ni, Chrysomelinae), the défensive sécrétion are cardenolides. A similar évolution from de nova syn- characterized by complex mixtures of cardenolides thesis of toxins to the use of plant-derived com- accompanied by ethanolamine (Pasteels et ai, 1988; pounds is known in some chrysomelid larvae (i.e. Van Oycke et ai, 1988). Contrary to well known ex• Chrysomela spp., Phratora vitellinae and Gastrolina amples of the use of cardenolides for defence in oth- depressa, see Introduction), but not in the adults. er insects {e.g. von Euw et ai, 1967; Brower & The situation of O. cacaliae and O. speciosissima Glazier, 1975; Scudder et ai, 1986), thèse parallels that observed in the larvae of Phratora cardenolides are not sequestered directly from the vitellinae and Ph. laticollis or Ph. tibialis. Ail three plants, but the beetles synthesize them from Phratora species feed on Salix or Populus, their cholestérol
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