, 19:73 | Cite as

Sequestration of prenylated benzoic acid and chromenes by Naupactus bipes (Coleoptera: Curculionidae) feeding on Piper gaudichaudianum (Piperaceae)

  • Clécio S. Ramos
  • Sergio A. Vanin
  • Massuo J. KatoEmail author
Research Paper


The curculionid beetle Naupactus bipes (Germar, 1824) (Coleoptera: Curculionidae: Brachycerinae) has shown feeding preference for leaves of Piper gaudichaudianum, demonstrating an unexpected specificity for an insect considered to be a generalist. The leaves of P. gaudichaudianum contain the prenylated chromenes gaudichaudianic acid (4, major compound) and its methyl ester (5) in addition to a chromene (3) lacking one prenyl residue. In addition to 4, roots contain the chromone methyl ester (1) and methyl taboganate (2, major compound). Feeding on roots, larvae of N. bipes sequester exclusively the root-specific compounds 1 and 2. Adult beetles sequester the leaf-specific chromenes 3 and 4, but were found to also contain compounds 1 and 2 that are absent in leaves. Therefore, it is suggested that 1 and 2 are sequestered by larvae and can be found in the body of adult insects after long-term storage. In addition, 3 and 4, the major compounds in leaves were found to be associated with the eggs.


Piperaceae Naupactus bipes Piper gaudichaudianum Sequestration Chromenes Prenylated benzoic acid derivatives 



Investigations were funded by grants from FAPESP and CNPq. The authors acknowledge Dr. Elsie F. Guimarães (Jardim Botânico do Rio de Janeiro, Rio de Janeiro, Brazil) for the identification of plant species. Special acknowledgments are due to the two anonymous referees who made important contributions to the manuscript.


  1. Aliabadi A, Renwick JAA, Whitman DW (2002) Sequestration of glucosinolates by harlequin bug Murgantia histrionica. J Chem Ecol 28:1749–1762PubMedCrossRefGoogle Scholar
  2. Baldoqui DC, Furlan M, Kato MJ, Cavalheiro AJ, Young MCM, Bolzani VS (1999) A chromene and prenylated benzoic acid from Piper aduncum. Phytochemistry 51:899–902PubMedCrossRefGoogle Scholar
  3. Batista JMJ, Lopes AA, Ambrósio DL, Regasini LO, Kato MJ, Bolzani VS, Cicarelli RMB, Furlan M (2008) Natural chromenes and chromene derivatives as potential anti-trypanosomal agents. Biol Pharm Bull 31:538–540PubMedCrossRefGoogle Scholar
  4. Benevides PJC, Sartorelli P, Kato MJ (1999) Phenypropanoids and neolignans from Piper regnellii. Phytochemistry 52:339–343CrossRefGoogle Scholar
  5. Bloem S, Mizell RF, O’Brien CW (2002) Old traps for new weevils: new records for Curculionids (Coleoptera: Curculionidae), Brentids (Coleoptera: Brentidae) and Anthribids (Coleoptera: Anthribidae) from Jefferson Co., Florida. Fla Entomol 85:632–637CrossRefGoogle Scholar
  6. Boppré M (1990) Lepidoptera and pyrrolizidine alkaloids: exemplification of complexity in chemical ecology. J Chem Ecol 309:707–709Google Scholar
  7. Brower LP (1984) Chemical defence in butterflies. In: Vane Wright RI, Ackers PR (eds) The biology of butterflies. Academic Press, London, pp 109–134Google Scholar
  8. Carroll M, Berenbaum MR (2006) Lutein sequestration and furanocoumarin metabolism in parsnip webworms under different ultraviolet light regimes in the montane west. J Chem Ecol 32:277–305PubMedCrossRefGoogle Scholar
  9. Chauret DC, Bernard CB, Arnason JT, Durst T (1996) Insecticidal neolignans from Piper decurrens. J Nat Prod 59:152–158PubMedCrossRefGoogle Scholar
  10. Costantin MB, Sartorelli P, Limberger R, Henriques AT, Steppe M, Ferreira MJP, Ohara MT, Emerenciano VP, Kato MJ (2001) Essential oils from Piper cernuum and Piper regnellii—antimicrobial activities and analysis by GC/MS and 13C NMR. Planta Med 67:771–773PubMedCrossRefGoogle Scholar
  11. Danelutte AP, Lago JHG, Young MCM, Kato MJ (2003) Antifungal flavanones and prenylated hydroquinones from Piper crassinervium Kunth. Phytochemistry 64:555–559PubMedCrossRefGoogle Scholar
  12. Danelutte AP, Costantin MB, Delgado GR, Braz-Filho R, Kato MJ (2005) Divergence of secondary metabolism in cell suspension cultures and differentiated plants of Piper cernuum and P. crassinervium. J Braz Chem Soc 16:1425–1430CrossRefGoogle Scholar
  13. Davies TJ, Barraclough TG, Chase MW, Soltis PS, Soltis DE, Savolainen V (2004) Darwin’s abominable mystery: Insights from a supertree of the angiosperms. Proc Natl Acad Sci USA 101:1904–1909PubMedCrossRefGoogle Scholar
  14. Dyer LA, Dodson CD, Stireman JO, Tobler MA, Smilanich AM, Fincher RM, Letourneau DK (2003) Synergistic effects of three Piper amides on generalist and specialist herbivores. J Chem Ecol 29:2499–2514PubMedCrossRefGoogle Scholar
  15. Figueiredo RA, Sazima M (2000) Pollination biology of Piperaceae species in south-eastern Brazil. Ann Bot 85:455–460CrossRefGoogle Scholar
  16. Fucarino A, Millar JG, Mcelfresh JS, Colazza S (2004) Chemical and physical signals mediating conspecific and heterospecific aggregation behaviour of first instar stink bugs. J Chem Ecol 30:1257–1269PubMedCrossRefGoogle Scholar
  17. Gbewonyo WR, Garnett H (1993) Structure-activity relationships of insecticidal amides from Piper guineense root. Pestic Sci 37:57–66CrossRefGoogle Scholar
  18. Herrera MC, Pellmyr O (2002) Plant-animal interactions: an evolutionary approach. Blackwell, AustraliaGoogle Scholar
  19. Hundsdoerfer AK, Tshibangu JN, Wetterauer B, Wink M (2005) Sequestration of phorbol esters by aposematic larvae of Hyles euphorbiae (Lepidoptera: Sphingidae). Chemoecology 15:261–267CrossRefGoogle Scholar
  20. Klitzke FA, Brown KS Jr (2000) The occurrence of aristolochic acids in neotropical troidine swallowtails (Lepidoptera: Papilionidae). Chemoecology 10:99–102CrossRefGoogle Scholar
  21. Lago JHG, Kato MJ (2007) 3a,4a-Epoxy-2-piperidone, a new minor derivative from leaves of Piper crassinervium Kunth (Piperaceae). Nat Prod Res 21:910–914PubMedCrossRefGoogle Scholar
  22. Lago JHG, Ramos CS, Casanova DCC, Morandim AA, Bergamo DCB, Cavalheiro AJ, Bolzani VS, Furlan M, Guimarães EF, Young MCM, Kato MJ (2004) Benzoic acid derivatives from Piper species and their fungitoxic activity against Cladosporium cladosporioides and C. sphaerospermum. J Nat Prod 67:1783–1788PubMedCrossRefGoogle Scholar
  23. Lago JHG, Tanizaki T, Young MCM, Guimarães EF, Kato MJ (2005) Antifungal piperolides from Piper malacophyllum (Prels) C. DC. J Braz Chem Soc 16:153–156Google Scholar
  24. Lanteri AA, Guedes JC, Parra JRP (2002) Systematic, morphology and physiology weevils injurious for roots of citrus in São Paulo state, Brazil. Neotropical Entomol 31:561–569Google Scholar
  25. Le-Van N, Phan TVC (1981) An unusual m-hydroxyacetophenone and three new chromanone derivatives from Chrysothamnus viscidiflorus. Phytochemistry 20:485–487CrossRefGoogle Scholar
  26. Lopes AA, Baldoqui DCB, López SN, Kato MJ, Bolzani VS, Furlan M (2007) Biosynthetic origin of the isoprene units of gaudichaudianic acid in Piper gaudichaudianum (Piperaceae). Phytochemistry 68:2053–2058PubMedCrossRefGoogle Scholar
  27. Martins RCC, Sartorelli P, Latorre LR, Kato MJ (2000) Phenylpropanoids and tetrahydrofuran lignans from Piper solmsianum. Phytochemistry 7:843–846CrossRefGoogle Scholar
  28. Martins RCC, Lago JHG, Kato MJ (2003) Trypanocidal tetrahydrofuran lignans from Piper solmsianum. Phytochemistry 64:667–670PubMedCrossRefGoogle Scholar
  29. Mikich SB, Bianconi GV, Maia BHLN, Teixeira SD (2003) Attraction of the fruit-eating bat Carollia perspicillata to Piper gaudichaudianum essential oil. J Chem Ecol 29:2379–2383PubMedCrossRefGoogle Scholar
  30. Miranda JE, Navickiene HMD, Nogueira-Couto RH, Bortoli SA, Kato MJ, Bolzani VS, Furlan M (2003) Susceptibility of Apis mellifera (Hymenoptera: Apidae) to pellitorine, an amide isolated from Piper tuberculatum Jacq. (Piperaceae). Apidology 34:409–415CrossRefGoogle Scholar
  31. Müller C, Agerbirk N, Olsen CF (2003) Lack of sequestration of host plant glucosinolates in Pieris rapae and P. brassicae. Chemoecology 13:47–54CrossRefGoogle Scholar
  32. Narberhaus I, Theuring C, Hartmann T, Dobler S (2004) Time course of pyrrolizidine alkaloid sequestration in longitarsus flea beetles (Coleoptera: Chrysomelidae). Chemoecology 14:17–23CrossRefGoogle Scholar
  33. Navickiene HMD, Alecio AC, Kato MJ, Bolzani VS, Young MC, Furlan M (2000) Antifungal amides from Piper hispidum and Piper tuberculatum. Phytochemistry 6:621–626CrossRefGoogle Scholar
  34. Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47:57–92PubMedCrossRefGoogle Scholar
  35. O’Brien CW, Wibmer GJ (1982) Annotated checklist of the weevils (Curculionidae sensu lato) of North America, Central America, and the West Indies (Coleoptera: Curculionoidea). Mem Am Entomol Inst 34:1–382Google Scholar
  36. Orjala J, Erdelmeier CAJ, Wright P, Rali T, Sticher O (1993) Two chromenes and prenylated benzoic acid derivative from Piper aduncum. Phytochemistry 34:813–818CrossRefGoogle Scholar
  37. Paula VF, Barbosa LCD, Demuner AJ, Piló-Veloso D, Picanço MC (2000) Synthesis and activity of new amide derivative of piperine. Pest Manag Sci 56:168–174CrossRefGoogle Scholar
  38. Péres VF, Saffi J, Melecchi MIS, Abad FC, Martinez MM, Oliveira EC, Assis R, Jacques EBC (2006) Optimization of pressurized liquid extraction of Piper gaudichaudianum Kunth leaves. J Chromatogr A 1105:148–153PubMedCrossRefGoogle Scholar
  39. Quijano-Abril MA, Callejas-Posada R, Miranda-Esquivel DR (2006) Areas of endemism and distribution patterns for Neotropical Piper species (Piperaceae). J Biogeogr 33:1266–1278CrossRefGoogle Scholar
  40. Ramos CS, Vanin SA, Kato MJ (2008) Metabolism of (−)-grandisin from Piper solmsianum in Coleoptera and Lepidoptera species. Phytochemistry 69:2157–2161PubMedCrossRefGoogle Scholar
  41. Roussis V, Ampofo SA, Wiemer DF (1990) A prenylated benzoic acid derivative from the leaves of Piper taboganum. Phytochemistry 29:1787–1788CrossRefGoogle Scholar
  42. Sartorelli P, Benevides PJC, Ellensohn RE, Rocha MVAF, Moreno PRH, Kato MJ (2001) Enantioselective conversion of p-hydroxypropenylbenzene to (+)-conocarpan in Piper regnellii. Plant Sci 6:1083–1088CrossRefGoogle Scholar
  43. Silva RV, Navickiene HMD, Kato MJ, Bolzani VS, Meda CI, Young MC, Furlan M (2002) Antifungal amides from Piper arboreum and Piper tuberculatum. Phytochemistry 59:521–527CrossRefGoogle Scholar
  44. Terreaux C, Gupta MP, Hostettmann K (1998) Antifungal benzoic acid derivatives from Piper dilatatum. Phytochemistry 49:461–464CrossRefGoogle Scholar
  45. Trigo JR (2000) The chemical of antipredator defence by secondary compounds in neotropical Lepidoptera: facts, perspectives and caveats. J Braz Chem Soc 6:551–561Google Scholar
  46. Vanin SA, Ramos CS, Guimarães EF, Kato MJ (2008) Insect feeding preferences on Piperaceae species observed in São Paulo city, Brazil. Rev Bras Entomol 52:72–77CrossRefGoogle Scholar
  47. Wanke S, Jaramillo MA, Borsch T, Samain MS, Quandt D, Neinhuis C (2007) Evolution of piperales-matk gene and trnk intron sequence data reveal lineage specific resolution contrast. Mol Phylogenet Evol 42:477–497PubMedCrossRefGoogle Scholar
  48. Wheeler GS, Massey LM, Southwell IA (2003) Dietary influence on terpenoids sequestered by the biological control agent Oxyops vitiosa effect of plant volatiles from different Melaleuca quinquenervia chemotypes and laboratory host species. J Chem Ecol 29:189–208PubMedCrossRefGoogle Scholar
  49. Wibmer GJ, O’Brien CW (1986) Annotated checklist of the weevils (Curculionidae sensu lato) of South America (Coleoptera: Curculionidae). Mem Am Entomol Inst 39:1–563Google Scholar
  50. Willinger G, Dobler S (2001) Selective sequestration of iridoid glycosides from their host plants in Longitarsus flea beetles. Biochem Syst Ecol 29:335–346PubMedCrossRefGoogle Scholar
  51. Yamaguchi LF, Lago JHG, Tanizaki TM, Di Mascio P, Kato MJ (2006) Antioxidant activities of prenylated hydroquinones and benzoic acid from Piper crassinervium. Phytochemistry 67:1838–1843PubMedCrossRefGoogle Scholar
  52. Yasui H (2001) Sequestration of host plant-derived compounds by geometrid moth, milionia basalis, toxic to a predatory stink bug, Eocanthecona furcellata. J Chem Ecol 27:1345–1353PubMedCrossRefGoogle Scholar
  53. Youngsteadt E, Nojima S, Haberlein C, Schulz S, Schal C (2008) Seed odor mediates an obligate ant–plant mutualism in Amazonian rainforests. Proc Nat Acad Sci 105:4571–4575PubMedCrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag, Basel/Switzerland 2009

Authors and Affiliations

  • Clécio S. Ramos
    • 1
  • Sergio A. Vanin
    • 2
  • Massuo J. Kato
    • 1
  1. 1.Instituto de QuímicaUniversidade de São PauloSão PauloBrazil
  2. 2.Museu de Zoologia e Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil

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