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Biological Invasions

, Volume 17, Issue 4, pp 987–1003 | Cite as

Searching for Heracleum mantegazzianum allelopathy in vitro and in a garden experiment

  • Kateřina Jandová
  • Petr Dostál
  • Tomáš Cajthaml
Original Paper

Abstract

One theory concerning the invasiveness of exotic plants suggests that they exude phytotoxic compounds that are novel in areas being invaded. For most invasive plants, however, little is known about the effects of their bioactive chemicals and how novel they are in invaded areas. From a methodological point of view, it also remains largely untested whether phytotoxicity found in vitro translates into allelopathic effects in more complex ecological settings. In this study, we tested for allelopathic effects of root exudates of the invasive plant Heracleum mantegazzianum (giant hogweed), its native congener Heracleum sphondylium (common hogweed) and two less-related native species. We also performed chemical analyses of the invader’s root exudates to identify bioactive compounds. We found that root exudates of H. mantegazzianum contain allelopathic compounds which are not likely to be furanocoumarins, but other as yet unidentified molecules. Allelopathy of the invader detected in vitro conditions and in our garden experiment did not, however, differ from the allelopathy of the native species tested. A meta-analysis of two independent garden experiments indicated significantly negative, though similar, phytotoxic effects of H. mantegazzianum, its native congener and Dactylis glomerata in the absence of activated carbon. Our study thus indicates that allelopathy by producing unique compounds, as predicted by the novel weapons hypothesis, is not a principal driver of the invasion success of H. mantegazzianum.

Keywords

Activated carbon Germination bioassay Giant hogweed Invasive plant Novel weapons Root exudates Secondary metabolites Soil microbiota UHPLC–TOF-MS 

Notes

Acknowledgments

This study was funded by grant P504/10/0132 from the Czech Science Foundation and grant GAUK512712 from the Charles University Grant Agency. Zdeněk Kameník from the Laboratory for Biology of Secondary Metabolism, Institute of Microbiology, Academy of Sciences of the Czech Republic carried out the LC–MS analyses. Frederick Rooks kindly improved our English. We thank Tereza Klinerová, Zdena Křesinová, Dana Parysová and Daniel Samek for their technical assistance, Lenka Moravcová for her advice during the germination experiments and three anonymous reviewers for their helpful comments on the manuscript.

References

  1. Abhilasha Quintana DN, Vivanco J, Joshi J (2008) Do allelopathic compounds in invasive Solidago canadensis s.l. restrain the native European flora? J Ecol 96:993–1001CrossRefGoogle Scholar
  2. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plants: from genes to invasion. Science 301:1377–1380CrossRefPubMedGoogle Scholar
  3. Baskin JM, Ludlow CJ, Harris TM, Wolf FT (1967) Psoralen, an inhibitor in the seeds of Psoralea subacaulis (Leguminoseae). Phytochemistry 6:1209–1213CrossRefGoogle Scholar
  4. Berenbaum M (1981) Patterns of furanocoumarin distribution and insect herbivory in the umbelliferae—plant chemistry and community structure. Ecology 62:1254–1266. doi: 10.2307/1937290 CrossRefGoogle Scholar
  5. Bertin C, Weston LA, Huang T, Jander G, Owens T, Meinwald J, Schroeder FC (2007) Grass roots chemistry: meta-Tyrosine, an herbicidal nonprotein amino acid. PNAS 104:16964–16969. doi: 10.1073/pnas.0707198104 CrossRefPubMedCentralPubMedGoogle Scholar
  6. Blair AC, Nissen SJ, Brunk GR, Hufbauer RA (2006) A lack of evidence for an ecological role of the putative allelochemical (±)-catechin in spotted knapweed invasion success. J Chem Ecol 32:2327–2331CrossRefPubMedGoogle Scholar
  7. Blair AC, Weston LA, Nissen SJ, Brunk GR, Hufbauer RA (2009) The importance of analytical techniques in allelopathy studies with the reported allelochemical catechin as an example. Biol Invasions 11:325–332CrossRefGoogle Scholar
  8. Blossey B, Notzgold R (1995) Evolution of increased competitive ability in invasive non-indigenous plants: a hypothesis. J Ecol 83:887–889CrossRefGoogle Scholar
  9. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to meta-analysis. Wiley, ChichesterCrossRefGoogle Scholar
  10. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523CrossRefPubMedGoogle Scholar
  11. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443CrossRefGoogle Scholar
  12. Cappuccino N, Arnason JT (2006) Novel chemistry of invasive exotic plants. Biol Lett 2:189–193CrossRefPubMedCentralPubMedGoogle Scholar
  13. Casinovi CG, Cerrini S, Motl O, Fardella G, Walter F et al (1983) On terpenes 274. The structure of a new sesquiterpene siol acetate from Sium latifolium L. Collect Czech Chem C 48:2411–2422CrossRefGoogle Scholar
  14. Catford JA, Jansson R, Nilsson C (2009) Reducing redundancy in invasion ecology by integrating hypotheses into a single theoretical framework. Divers Distrib 15:22–40CrossRefGoogle Scholar
  15. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  16. Crawley MJ (2007) The R Book. Wiley, ChichesterCrossRefGoogle Scholar
  17. Del Fabbro C, Güsewell S, Prati D (2014) Allelopathic effects of three plant invaders on germination of native species: a field study. Biol Invasions 16:1035–1042CrossRefGoogle Scholar
  18. Dostál P (2011) Plant competitive interactions and invasiveness: searching for the effects of phylogenetic relatedness and origin on competition intensity. Am Nat 177:655–667CrossRefPubMedGoogle Scholar
  19. Dostál P, Müllerová J, Pyšek P, Pergl J, Klinerová T (2013) The impact of an invasive plant changes over time. Ecol Lett 16:1277–1284CrossRefPubMedGoogle Scholar
  20. Duke SO (2010) Allelopathy: current status of research and future of the discipline: a commentary. Allelopathy J 25:17–29Google Scholar
  21. Eppinga MB, Rietkerk M, Dekker SC, Ruiter PCD, van der Putten WH (2006) Accumulation of local pathogens: a new hypothesis to explain exotic plant invasions. Oikos 114:168–176CrossRefGoogle Scholar
  22. Fischer FC, Van Doorne H, Dannenberg G (1978) Glycosides and glycosidase in Heracleum mantegazzianum—their possible role in resistance against fungi. In: Cauwet-Marc AM, Carbonnier J (eds) Actes du 2e Symposium International sur les Ombelliferes. CNRS, Perpignan, pp 783–792Google Scholar
  23. Garcia C, Moyna P, Fernandez G, Heinzen H (2002) Allelopathic activity of Ammi majus L. fruit waxes. Chemoecology 12:107–111CrossRefGoogle Scholar
  24. Harborne JB (1971) Flavonoid and phenylpropanoid patterns in the Umbelliferae. Bot J Linnean Soc 64(Suppl. 1):293–314Google Scholar
  25. Hattendorf J, Hansen SO, Nentwig W (2007) Defense system of Heracleum mantegazzianum. In: Pyšek P, Cock MJW, Nentwig W, Ravn HP (eds) Ecology and management of giant hogweed (Heracleum mantegazzianum). CAB International, Wallingford, pp 209–225CrossRefGoogle Scholar
  26. Hejda M, Pyšek P, Jarošík V (2009) Impact of invasive plants on the species richness, diversity and composition of invaded communities. J Ecol 97:393–403CrossRefGoogle Scholar
  27. Herde A (2005) Untersuchung der Cumarinmuster in Fruchten ausgewahlter Apiaceae. Dissertation, University of HamburgGoogle Scholar
  28. Hierro JL, Callaway RM (2003) Allelopathy and exotic plant invasion. Plant Soil 256:29–39CrossRefGoogle Scholar
  29. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stn 347:1–32Google Scholar
  30. Inderjit, Nilsen ET (2003) Bioassays and field studies for allelopathy in terrestrial plants: progress and problems. Crit Rev Plant Sci 22:221–238CrossRefGoogle Scholar
  31. Inderjit, Seastedt TR, Callaway RM, Pollock JL, Kaur J (2008) Allelopathy and plant invasions: traditional, congeneric, and bio-geographical approaches. Biol Invasions 10:875–890CrossRefGoogle Scholar
  32. Ivie GW (1978) Toxicological significance of plant furocoumarins. In: Keeler RF, van Kamper KR, James LF (eds) Effects of poisonous plants on livestock. Academic Press, New York, pp 475–485CrossRefGoogle Scholar
  33. Jahodová S, Trybush S, Pyšek P, Wade M, Karp A (2007) Invasive species of Heracleum in Europe: an insight into genetic relationships and invasion history. Divers Distrib 13:99–114CrossRefGoogle Scholar
  34. Jain SR (1969) Investigations on essential oil of Heracleum mantegazzianum L. Planta Med 17:230–235CrossRefPubMedGoogle Scholar
  35. Jandová K, Klinerová T, Müllerová J, Pyšek P, Pergl J, Cajthaml T, Dostál P (2014) Long-term impact of Heracleum mantegazzianum invasion on soil chemical and biological characteristics. Soil Biol Biochem 68:270–278CrossRefGoogle Scholar
  36. Joshi J, Vrieling K (2005) The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol Lett 8:704–714CrossRefGoogle Scholar
  37. Junttila O (1975) Allelopathy in Heracleum laciniatum: inhibition of lettuce seed germination and root growth. Physiol Plant 33:22–27CrossRefGoogle Scholar
  38. Junttila O (1976) Allelopathic inhibitors in seeds of Heracleum laciniatum. Physiol Plant 36:374–378CrossRefGoogle Scholar
  39. Kartesz JT, Meacham CA (1999) Synthesis of the North American Flora, Version 1.0. North Carolina Botanical Garden, Chapel Hill, NCGoogle Scholar
  40. Kaur H, Kaur R, Kaur S, Baldwin IT, Inderjit (2009) Taking ecological function seriously: soil microbial communities can obviate allelopathic effects of released metabolites. PloS One 4:e4700CrossRefPubMedCentralPubMedGoogle Scholar
  41. Kavli G, Krokan H, Midelfart K, Volden G, Raa J (1983) Extraction, separation, quantification and evaluation of the phototoxic potency of furocoumarins in different parts of Heracleum laciniatum. Photobioch Photobiop 5:159–168Google Scholar
  42. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  43. KNApSAcK (2014) A Comprehensive Species-Metabolite Relationship Database. Version 1.000.01 (2008/06/23). Accessed 28 Apr 2014Google Scholar
  44. Lankau R (2010) Soil microbial communities alter allelopathic competition between Alliaria petiolata and a native species. Biol Invasions 12:2059–2068CrossRefGoogle Scholar
  45. Lankau RA, Nuzzo V, Spyreas G, Davis AS (2009) Evolutionary limits ameliorate the negative impact of an invasive plant. PNAS 106:15362–15367CrossRefPubMedCentralPubMedGoogle Scholar
  46. Lind EM, Parker JD (2010) Novel weapons testing: Are invasive plants more chemically defended than native plants? Plos One 5:e10429CrossRefPubMedCentralPubMedGoogle Scholar
  47. Macias FA, Galindo JCG, Massanet GM, Rodriguez-Luis F, Zubia E (1993) Allelochemicals from Pilocarpus goudotianus leaves. J Chem Ecol 19:1371–1379CrossRefPubMedGoogle Scholar
  48. Miski M, Mabry T (1985) Daucane esters from Ferula communis subsp. communis. Phytochemistry 24:1735–1742CrossRefGoogle Scholar
  49. Molho D, Jossang P, Jarreau MC, Carbonnier J (1971) Derives furannocoumariniques du genre Heracleum. Bot J Linnean Soc 64(Suppl. 1):337–360Google Scholar
  50. Müllerová J, Pyšek P, Jarošík V, Pergl J (2005) Aerial photographs as a tool for assessing the regional dynamics of the invasive plant species Heracleum mantegazzianum. J Appl Ecol 42:1042–1053CrossRefGoogle Scholar
  51. Myras H, Junttila O (1981) Interaction between Heracleum laciniatum and some other plants. Holarctic Ecol 4:43–48Google Scholar
  52. Nielsen BE (1971) Coumarin patterns in the Umbelliferae. Bot J Linnean Soc 64(Suppl. 1):325–336Google Scholar
  53. Page NA, Wall RE, Darbyshire SJ, Mulligan GA (2006) The biology of invasive alien plants in Canada. 4. Heracleum mantegazzianum Sommier & Levier. Can J Plant Sci 86:569–589CrossRefGoogle Scholar
  54. Pandita K, Agarwal SG, Thappa RK, Dhar KL (1984) 1-alpha-acetoxy-6-alpha-hydroxy-9-oxo-carot-2-ene, a new derivative from Sium latijugum seeds. Indian J Chem B 23:956–957Google Scholar
  55. Pergl J, Mullerová J, Perglová I, Herben T, Pyšek P (2011) The role of long-distance seed dispersal in the local population dynamics of an invasive plant species. Divers Distrib 17:725–738CrossRefGoogle Scholar
  56. Perglová I, Pergl J, Pyšek P (2006) Flowering phenology and reproductive effort of the invasive alien plant Heracleum mantegazzianum. Preslia 78:265–285Google Scholar
  57. Prati D, Bossdorf O (2004) Allelopathic inhibition of germination by Alliaria petiolata (Brassicaceae). Am J Bot 91:285–288CrossRefPubMedGoogle Scholar
  58. Pyšek P, Pyšek A (1995) Invasion by Heracleum mantegazzianum in different habitats in the Czech Republic. J Veg Sci 6:711–718CrossRefGoogle Scholar
  59. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  60. Reaxys database (2014) version 2.15212.2, Elsevier. Accessed 28 Apr 2014Google Scholar
  61. Sheppard AW (1991) Biological flora of the British Isles: Heracleum sphondylium L. J Ecol 79:235–258CrossRefGoogle Scholar
  62. Thiele J, Otte A (2007) Impact of Heracleum mantegazzianum on invaded vegetation and human activities. In: Pyšek P, Cock MJW, Nentwig W, Ravn HP (eds) Ecology and management of giant hogweed (Heracleum mantegazzianum). CAB International, WallingfordGoogle Scholar
  63. Thiele J, Kollmann J, Markussen B, Otte A (2010) Impact assessment revisited: improving the theoretical basis for management of invasive alien species. Biol Invasions 12:2025–2035CrossRefGoogle Scholar
  64. Tiley GED, Dodd FS, Wade PM (1996) Heracleum mantegazzianum Sommier et Levier. J Ecol 84:297–319CrossRefGoogle Scholar
  65. Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36:1–48Google Scholar
  66. Wille W, Thiele J, Walker EA, Kollmann J (2013) Limited evidence for allelopathic effects of giant hogweed on germination of native herbs. Seed Sci Res. doi: 10.1017/S096025851300007X Google Scholar
  67. Yi T, Zhang L, Fu HW, Yang SL, Tian JK (2009) Two new guaiane sesquiterpenes from the fruits of Daucus carota. Helv Chim Acta 92:2769–2773CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Kateřina Jandová
    • 1
    • 2
  • Petr Dostál
    • 2
  • Tomáš Cajthaml
    • 1
    • 3
  1. 1.Faculty of Science, Institute for Environmental StudiesCharles University in PraguePrague 2Czech Republic
  2. 2.Institute of BotanyAcademy of Sciences of the Czech RepublicPrůhoniceCzech Republic
  3. 3.Institute of MicrobiologyAcademy of Sciences of the Czech RepublicPrague 4Czech Republic

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