Journal of Chemical Ecology

, Volume 40, Issue 3, pp 276–284 | Cite as

Roots of the Invasive Species Carduus nutans L. and C. acanthoides L. Produce Large Amounts of Aplotaxene, a Possible Allelochemical

  • Ferdinando M. L. Silva
  • Mateus A. Donega
  • Antonio L. Cerdeira
  • Natália Corniani
  • Edivaldo D. Velini
  • Charles L. Cantrell
  • Franck E. Dayan
  • Mariana N. Coelho
  • Katriona Shea
  • Stephen O. Duke


The invasive thistle Carduus nutans has been reported to be allelopathic, yet no allelochemicals have been identified from the species. In a search for allelochemicals from C. nutans and the closely related invasive species C. acanthoides, bioassay-guided fractionation of roots and leaves of each species were conducted. Only dichloromethane extracts of the roots of both species contained a phytotoxin (aplotaxene, (Z,Z,Z)-heptadeca-1,8,11,14-tetraene) with sufficient total activity to potentially act as an allelochemical. Aplotaxene made up 0.44 % of the weight of greenhouse-grown C. acanthoides roots (ca. 20 mM in the plant) and was not found in leaves of either species. It inhibited growth of lettuce 50 % (I 50) in soil at a concentration of ca. 0.5 mg g−1 of dry soil (ca. 6.5 mM in soil moisture). These values gave a total activity in soil value (molar concentration in the plant divided by the molarity required for 50 % growth inhibition in soil = 3.08) similar to those of some established allelochemicals. The aplotaxene I 50 for duckweed (Lemna paucicostata) in nutrient solution was less than 0.333 mM, and the compound caused cellular leakage of cucumber cotyledon discs in darkness and light at similar concentrations. Soil in which C. acanthoides had grown contained aplotaxene at a lower concentration than necessary for biological activity in our short-term soil bioassays, but these levels might have activity over longer periods of time and might be an underestimate of concentrations in undisturbed and/or rhizosphere soil.


Allelochemical Allelopathy Aplotaxene Carduus nutans Carduus acanthoides Phytotoxin 



We thank Robert Johnson, Solomon Green III, Joe Keller, and Britta Teller for technical assistance and Dr. Martin Locke for providing soils.

Supplementary material

10886_2014_390_MOESM1_ESM.docx (315 kb)
Fig. S-1 (DOCX 314 kb)


  1. Abdallah OM, Ramadan MA, El-Shanawany MA (1989) Phytochemical study of Carduus nutans L. (Asteraceae). Bull Fac Sci Assiut Univ 18:69–76Google Scholar
  2. Bain JF, Desrochers AM (1988) Flavonoids of Carduus nutans and C. acanthoides. Biochem Syst Ecol 16:265–268CrossRefGoogle Scholar
  3. Binder RG, Benson M, Haddon WF, French RC (1992) Aplotaxene derivatives from Cirsium arvense. Phytochemistry 31:1033–1034CrossRefGoogle Scholar
  4. Bohlmann F, Abraham WR (1981) Aplotaxene epoxide from Cirsium hypoleucum. Phytochemistry 20:855–856CrossRefGoogle Scholar
  5. Bokadia MM, MacLoed AJ, Mehta SC, Mehta BK, Patel H (1986) The essential oil of Inula racemosa. Phytochemistry 25:2887–2888CrossRefGoogle Scholar
  6. Bonner KI, Rahman AR, James TK, Nicholson KS, Wardle DA (1998) Relative intra-species competitive ability of nodding thistle biotypes with varying resistance to 2,4-D. New Zealand J Agric Res 41:291–297CrossRefGoogle Scholar
  7. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443CrossRefGoogle Scholar
  8. Choi JY, Na M-K, Hwang IH, Lee SH, Bae EY, Kim BY, Ahn JS (2009) Isolation of betulinic acid, its methyl ester and guaiane sesquiterpenoids with protein tyrosine phosphatase 1B inhibitory activity from the roots of Saussurea lappa. C.B. Clarke. Molecules 14:266–272CrossRefPubMedGoogle Scholar
  9. Chon S-U, Kim Y-M, Lee J-C (2003) Herbicidal and potential quantification of causative allelochemicals from several Compositae weeds. Weed Res 43:444–450CrossRefGoogle Scholar
  10. Christensen LP (1992) Aplotaxene derivatives from Cirsium helenioides. Phytochemistry 31:2039–2041CrossRefGoogle Scholar
  11. Cossy J, Aclinou P (1990) Isolation and total synthesis of the major constituents of the roots of Centaurea incana: aplotaxene. Tetrahedron Lett 31:7615–7618CrossRefGoogle Scholar
  12. Dayan FE, Duke SO (2009) Biological activity of allelochemicals. In: Osbourn A, Lanzotti V (eds) Plant-derived natural products – synthesis, function and application. Springer, Dordrecht, pp 361–384CrossRefGoogle Scholar
  13. Dayan FE, Watson SB (2011) Plant cell membrane as a marker for light-dependent and light-independent herbicide mechanisms of action. Pestic Biochem Physiol 101:182–190CrossRefGoogle Scholar
  14. Dayan FE, Romagni JG, Duke SO (2000) Investigating the mode of action of natural phytotoxins. J Chem Ecol 26:2079–2094CrossRefGoogle Scholar
  15. Desrochers AM, Bain JF, Warwick SI (1988) The biology of Canadian weeds 89. Carduus nutans L. and Carduus acanthoides L. Can J Plant Sci 68:1053–1068CrossRefGoogle Scholar
  16. Duke SO (2010) Allelopathy: current status of research and future of the discipline: a commentary. Allelopathy J 25:17–30Google Scholar
  17. Farag RS, Badei AZMA, Hewedi FM, El-Baroty GSA (1989) Antioxidant activity of some spice essential oils on linoleic acid oxidation in aqueous media. J Am Oil Chem Soc 66:792–799CrossRefGoogle Scholar
  18. Formisano C, Rigano D, Senatore F, De Feo V, Bruno M, Rosselli S (2007) Composition and allelopathic effect of essential oils of two thistles: Cirsium creticum (Lam.) D’.Urv. ssp. triumfetti (Lacaita) Werner and Carduus nutans L. J. Plant Interact 2:115–120CrossRefGoogle Scholar
  19. French RC, Turner SK, Sonnett PE, Pfeffer P, Piotrowski E (1988) Properties of an extract of Canada thistle roots that stimulates germination of dormant teliospores of Canada thistle rust (Puccinia punctiformis). J Agric Food Chem 36:1043–1047CrossRefGoogle Scholar
  20. Havlik J, Budesinsky M, Kloucek P, Kokoska L, Valterova I, Vasickova S, Zeleny V (2009) Norsesquiterpene hydrocarbon, chemical composition and antimicrobial activity of Rhaponticum carthamoides root essential oil. Phytochemistry 70:414–418CrossRefPubMedGoogle Scholar
  21. Hierro JL, Callaway RM (2003) Allelopathy and exotic plant invasion. Plant Soil 256:29–39CrossRefGoogle Scholar
  22. Hiradate S (2006) Isolation strategies for finding bioactive compounds: specific activity vs. total activity. Am Chem Soc Symp Ser 927:113–126Google Scholar
  23. Hiradate S, Ohse K, Furubayashi A, Fujii Y (2010) Quantitative evaluation of allelopathic potentials in soils: total activity approach. Weed Sci 58:258–264CrossRefGoogle Scholar
  24. Jongehans E, Shea K, Skarpaas O, Kelly D, Sheppard AW, Woodburn TL (2008) Dispersal and demography contributions to population spread of Carduus nutans in its native and invaded ranges. J Ecol 96:687–697CrossRefGoogle Scholar
  25. Jongejans E, Sheppard AW, Shea K (2006) What controls the population dynamics of the invasive thistle Carduus nutans in its native range? J Appl Ecol 43:877–886CrossRefGoogle Scholar
  26. Jorodon-Thaden IE, Louda SM (2003) Chemistry of Cirsium and Carduus: a role I ecological risk assessment for biological control of weeds? Biochem Syst Ecol 31:1353–1396CrossRefGoogle Scholar
  27. Kaloshina NA, Mazulin AV (1988) Flavonoids of Carduus nutans. Khim Prir Soedin 3:453Google Scholar
  28. Khan AL, Hussain J, Hamayun M, Shinwari ZK, Khan H, Kang Y-H, Kang S-M, Lee I-J (2009) Inorganic profile and allelopathic effect of endemic Inula koelzii from Himalaya Pakistan. Pak J Bot 41:2517–2527Google Scholar
  29. Michel A, Johnson RD, Duke SO, Scheffler BE (2004) Dose–response relationships between herbicides with different modes of action and growth of Lemna paucicostata – an improved ecotoxicological method. Environ Toxicol Chem 23:1074–1079CrossRefPubMedGoogle Scholar
  30. Miyazawa M, Yamafuji C, Tabata J, Ishikwawa Y (2003) Oviposition-stimulatory activity against Ostrinia zealis by essential oil root part from Cirsium japonicum DC. Nat Prod Res 17:341–345CrossRefPubMedGoogle Scholar
  31. Mulligan GA, Moore RJ (1961) Natural selection among hybrids between Carduus acanthoides and C. nutans in Ontario. Can J Bot 39:421–430Google Scholar
  32. Naves YR (1949) Costus oil. Manuf Chem 20:318–320Google Scholar
  33. Nazaruk J, Karna E, Kelemba D (2012) The chemical composition of the essential oils of Cirsium palustre and C. rivulare and their antiproliferative effect. Nat Prod Comm 7:269–272Google Scholar
  34. Quintana N, El Kassis EG, Stermitz FR, Vivanco JM (2009) Phytotoxic compounds from roots of Centaurea diffusa Lam. Plant Signal Behav 4:9–14CrossRefPubMedPubMedCentralGoogle Scholar
  35. Rauschert ESJ, Shea K (2012) Influence of microsite disturbance on the establishment of two congeneric invasive thistles. PLoS ONE 7(9):e45490. doi: 10.1371/journal.pone.0045490 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Rauschert ESJ, Shea K, Bjørnstad ON (2012) Coexistence patterns of two invasive thistle species, Carduus nutans and C. acanthoides, at three spatial scales. Biol. Invasions 14:151–164CrossRefGoogle Scholar
  37. Shea K, Kelly D, Sheppard AW, Woodburn TL (2005) Context-dependent biological control of an invasive thistle. Ecology 86:3174–3181CrossRefGoogle Scholar
  38. Skarpaas O, Shea K (2007) Dispersal patterns, dispersal mechanisms, and invasion wave speeds for invasive thistles. Am Natl 170:517–526CrossRefGoogle Scholar
  39. Soil Survey Staff (2010) Keys to soil taxonomy, 11th edn. USDA-Natural Resources Conservation Service, Washington, DCGoogle Scholar
  40. Takano S, Kawaminami S (1988) Cyperenyl acetate and cyperenal from Cirsium dipscolepis. Phytochemistry 29:197–1199Google Scholar
  41. Tesevic V, Djokovic D, Vajs V, Marin P, Milosavljevic S (1994) Constituents of the roots of plant species Centauria scabiosa. J Serb Chem Soc 59:979–981Google Scholar
  42. Tesevic V, Milosavljevic S, Vajs V, Janackovic P, Popsavin M (2003) Dithiophenes and other constituents of roots of Centauria nicolai. Biochem Syst Ecol 31:89–90CrossRefGoogle Scholar
  43. Wardle DA, Ahmed M, Nicholson KS (1991) Allelopathic influence of nodding thistle (Carduus nutans L.) seeds on germination and radical growth of pasture plants. New Zealand J Agric Res 34:185–191CrossRefGoogle Scholar
  44. Wardle DA, Nicholson KS, Rahman A (1993) Influence of plant age on the allelopathic potential of nodding thistle (Carduus nutans L.) against pasture grasses and legumes. Weed Res 33:69–78CrossRefGoogle Scholar
  45. Wardle DA, Nicholson KS, Ahmed M, Rahman A (1994) Interference effects of the invasive plant Carduus nutans L. against the nitrogen fixation ability of Trifolium repens L. Plant Soil 163:287–297CrossRefGoogle Scholar
  46. Wardle KA, Nicholson KS, Rahman A (1996) Use of a comparative approach to identify allelopathic potential and relationship between allelopathy bioassays and “competition” experiments for ten grassland and plant species. J Chem Ecol 22:933–948CrossRefPubMedGoogle Scholar
  47. Wardle DA, Nilsson M-C, Gallet C, Zackrisson O (1998) An ecosystem-level perspective of allelopathy. Biol Rev 73:305–319CrossRefGoogle Scholar
  48. Warwick SI, Bain JF, Wheatcroft R, Thompson BK (1989) Hybridization and introgression in Carduus nutans and Carduus acanthoides reexamined. Syst Bot 14:476–494CrossRefGoogle Scholar
  49. Yano K, Shirashi N, Furukawa T (1983) Ontogenetic variations in C17 hydrocarbon composition in the root oil of Cirsium japonicum. Phytochemistry 22:1030–1031CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York (outside the USA) 2014

Authors and Affiliations

  • Ferdinando M. L. Silva
    • 2
  • Mateus A. Donega
    • 3
  • Antonio L. Cerdeira
    • 4
  • Natália Corniani
    • 2
  • Edivaldo D. Velini
    • 2
  • Charles L. Cantrell
    • 1
  • Franck E. Dayan
    • 1
  • Mariana N. Coelho
    • 5
  • Katriona Shea
    • 6
  • Stephen O. Duke
    • 1
  1. 1.NPURU, USDA, ARSUniversityUSA
  2. 2.Faculty of Agronomic Sciences, Experimental Station Lageado, Laboratory of Weed ScienceSão Paulo State UniversityBotucatuBrazil
  3. 3.Escola Superior de Agricultura Luiz de Queiroz, Departamento de Produção VegetalUniversidade de São PauloPiracicabaBrazil
  4. 4.Brazilian Department of Agriculture, Agricultural Research Service, EMBRAPA/EnvironmentJaguariúnaBrazil
  5. 5.Faculdade de FarmáciaUniversidade Federal FluminenseNiteróiBrazil
  6. 6.Department of Biology, 208 Mueller LaboratoryThe Pennsylvania State UniversityUniversity ParkUSA

Personalised recommendations