Advertisement

Plant and Soil

, Volume 385, Issue 1–2, pp 165–179 | Cite as

Experimental evidence that invasive grasses use allelopathic biochemicals as a potential mechanism for invasion: chemical warfare in nature

  • Mitchell J. GreerEmail author
  • Gail W. T. Wilson
  • Karen R. Hickman
  • Stuart M. Wilson
Regular Article

Abstract

Background and aims

Bothriochloa spp. are non-native warm-season grasses invading native grasslands of the southern and central Great Plains, altering ecological services these grasslands supply. Our study investigated potential allelopathic effects of the invasive grass species B. ischaemum on native grass germination, growth, and survival.

Methods

Leachate or litter from Andropogon gerardii (native) or B. ischaemum were applied to two native grass species (A. gerardii; Schizachyrium scoparium). Leachate and litter were also added to B. ischaemum and a water control was included. Germination, above- and belowground biomass, and survival were determined.

Results

Application of B. ischaemum leachate or litter significantly reduced the germination, growth, and survival of both A. gerardii and S. scoparium but had no conspecific effects, while A. gerardii treatments had no effect on any species.

Conclusions

Bothriochloa spp. may gain a competitive advantage through allelopathic biochemicals. It is unclear if these allelopathic effects directly hinder competitors or indirectly hinder them through alterations in soil microbial communities, however, reductions in germination of native seeds strongly support direct allelopathic effects. Greater phenolic content in native grass leachates suggest allelopathic biochemical production may not be unique to non-native species and may be a mechanism for maintenance of plant species biodiversity in native systems.

Keywords

Allelopathy Bothriochloa spp Invasive species Leachate Leaf litter Yellow bluestem 

References

  1. Abhilasha D, Quintana N, Vivanco J, Joshi J (2008) Do allelopathic compounds in invasive Solidago canadensis s.I. Restrain the native european flora? J Ecol 96:993–1001CrossRefGoogle Scholar
  2. Agrawal AA, Kotanen PM, Mitchell CE, Power AG, Godsoe W, Klironomos J (2005) Enemy release? an experiment with congeneric plant pairs and diverse above- and belowground enemies. Ecology 86:2979–2989CrossRefGoogle Scholar
  3. Bais HP, Vepachedu R, Gilroy S, Callaway RM, Vivanco JM (2003) Allelopathy and exotic plants: from genes to invasion. Science 301:1377–1380PubMedCrossRefGoogle Scholar
  4. Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de0etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221PubMedCrossRefGoogle Scholar
  5. Bever JD (2002) Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. P R Soc London 269:2595–2601CrossRefGoogle Scholar
  6. Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical test. New Phytol 157:465–473CrossRefGoogle Scholar
  7. Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. Ecology 85:561–573CrossRefGoogle Scholar
  8. Blossey B, Nötzgold R (1995) Evolution of increased competitive ability in invasive non-indigenous plants: a hypothesis. J Ecol 83:887–889CrossRefGoogle Scholar
  9. Blum U, Gerig TM, Worsham AD, King LD (1993) Modification of allelopathic effects of p-coumaric acid on morning-glory seedling biomass by glucose, methionine, and nitrate. J Chem Ecol 19:2791–2811PubMedCrossRefGoogle Scholar
  10. Bossdorf O, Auge H, Lafuma L, Rogers WE, Siemann E, Prati D (2005) Phenotypic and genetic variation between native and introduced plant population. Oecologia 144:1–11PubMedCrossRefGoogle Scholar
  11. Butcko VM, Jensen RJ (2002) Evidence of tissue-specific allelopathic activity in Euthamia graminifolia and Solidago canadensis (Asteraceae). Am Midl Nat 148:253–262CrossRefGoogle Scholar
  12. Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523PubMedCrossRefGoogle Scholar
  13. Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, Prati D, Stinson K, Klironomos J (2008) Novel weapons: invasive plant suppresses fungal mutualisms in America but not in its native Europe. Ecology 89:1043–1055PubMedCrossRefGoogle Scholar
  14. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–433CrossRefGoogle Scholar
  15. Casper BB, Bentivenga SP, Ji B, Doherty JH, Edenborn HM, Gustafson DJ (2008) Plant-soil feedback: testing the generality with the same grasses in serpentine and prairie soils. Ecology 89:2154–2164PubMedCrossRefGoogle Scholar
  16. Chapin FS III, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU (2000) Consequences of changing biodiversity. Nature 405:234–242PubMedCrossRefGoogle Scholar
  17. Chon SU, Kim JD (2002) Biological activity and quantification of suspected allelochemicals from alfalfa parts. J Agron Crop Sci 188:281–285CrossRefGoogle Scholar
  18. Cipollini D, Rigsby DM, Barto EK (2012) Microbes as targets and mediators of allelopathy in plants. J Chem Ecol 38:714–727PubMedCrossRefGoogle Scholar
  19. Coulter CB, Stone FM, Kabat EA (1936) The structure of ultraviolet absorption spectra of certain proteins and amino acids. J Gen Physiol 19:739–752PubMedCentralPubMedCrossRefGoogle Scholar
  20. Cusack DF, Chou WW, Yang WH, Hanmon ME, Silver WL (2009) Controls on long-term root and leaf litter decomposition in neotropical forest. Glob Chang Biol 15:1339–1355CrossRefGoogle Scholar
  21. D’Antonio CM, Vitousek PM (1992) Biological invasion by exotic grasses, the grass-fire cycle, and global change. Annu Rev Ecol Syst 23:63–87Google Scholar
  22. Dabo SM, Taliaferro CM, Coleman SW, Horn FP, Claypool PL (1988) Chemical composition of old world bluestem grasses as affected by cultivar and maturity. J Range Manage 41:40–48CrossRefGoogle Scholar
  23. Devi SR, Pellissier F, Prasad MNV (1997) Allelochemicals. In: Prasad MNV (ed) Plant ecophysiology. Wiley, New York, pp 253–303Google Scholar
  24. Dirvi GA, Hussain F (1979) Allelopathic effects of Dichanthium annulatum (Forsk) Stapf on some cultivated plants. Pakistan J Sci Ind R 22:194–197Google Scholar
  25. Dorning M, Cipollini D (2006) Leaf and root extracts of the invasive shrub, Lonicera maackii, inhibit seed and germination of three herbs with no autotoxic effects. Plant Ecol 184:287–296CrossRefGoogle Scholar
  26. Einhellig FA, Rassmussen JA (1979) Effects of three phenolic acids on chlorophyll content and growth of soybean and grain sorghum seedlings. J Chem Ecol 5:815–824CrossRefGoogle Scholar
  27. Ervin GN, Wetzel RG (2000) Allelochemical autotoxicity in the emergent wetland macrophyte Juncus effuses (Juncaceae). Am J Bot 87:853–860PubMedCrossRefGoogle Scholar
  28. Evans RA (1961) Effects of different densities of downy brome (Bromus tectorum) on growth and survival of crested wheatgrass (Agropyron desertorum) in the greenhouse. Weeds 9:216–223CrossRefGoogle Scholar
  29. Flores HE, Vivanco JM, Loyola-Vargas M (1999) ‘Radicle’ biochemistry: the biology of root-specific metabolism. Trends Plant Sci 4:220–226PubMedCrossRefGoogle Scholar
  30. Freund RJ, Wilson WJ (2003) Statistical methods, 2nd edn. Academic, San DiegoGoogle Scholar
  31. Gibson DJ (2002) Methods in comparative plant population ecology. Oxford University Press, New YorkGoogle Scholar
  32. Greer MJ (2013) Grassland invasions by non-native grass species: ecological issues for multiple species at multiple trophic levels. Oklahoma State University, DissertationGoogle Scholar
  33. Grove S, Haubensak KA, Parker IM (2012) Direct and indirect effects of allelopathy in the soil legacy of an exotic plant invasion. Plant Ecol 213:1869–1882CrossRefGoogle Scholar
  34. Hagen DL, Jose S, Lin C-H (2013) Allelopathic exudates of cogongrass (imperata cylindrical): implications for performance of native pine savanna plant species in the southeastern U.S. J Chem Ecol 39:312–322CrossRefGoogle Scholar
  35. Hardie M, Doyle R (2012) Measuring soil salinity. Methods Mol Biol 913:415–425PubMedGoogle Scholar
  36. Harmoney KR, Hickman KR (2004) Comparing morphology of caucasian old world bluestem and native grass. Agon J 96:1540–1544Google Scholar
  37. Harmoney KR, Stahlman PW, Hickman KR (2007) Suppression of caucasian old world bluestem with split application of herbicides. Weed Technol 21:573–577CrossRefGoogle Scholar
  38. Harmoney KR, Stahlman PW, Hickman KR (2004) Herbicide effects on established yellow old world bluestem (Bothriochloa ischaemum). Weed Technol 18:545–550CrossRefGoogle Scholar
  39. Harnden J, MacDougall AS, Sikes BA (2011) Field-based effects of allelopathy in invaded tallgrass prairie. Botany 89:227–234CrossRefGoogle Scholar
  40. Hättenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–242PubMedCrossRefGoogle Scholar
  41. Heywood VH (1989) Patterns, extents and modes of invasions by terrestrial plants. In: Drake JA, Mooney HA, di Castri F, Grovers RH, Kruger FJ, Rejmanek M, Williamson M (eds) Biological invasions: a global perspective. Wiley, Chichester, pp 31–60Google Scholar
  42. Hierro JL, Callaway RM (2003) Allelopathy and exotic plant invasion. Plant Soil 256:29–39CrossRefGoogle Scholar
  43. Hu G, Zhang ZH (2013a) Aqueous tissue extracts of Conyza canadensis inhibit the germination and shoot growth of three native herbs with no autotoxic effects. Planta Daninha 31:805–811CrossRefGoogle Scholar
  44. Hu G, Zhang ZH (2013b) Allelopathic effects of Chromolaena odorata on native and non-native herbs. J Food Agric Environ 11:878–882Google Scholar
  45. Hulbert LC (1969) Fire and litter effects in undisturbed bluestem prairie in Kansas. Ecology 5:874–877CrossRefGoogle Scholar
  46. Inderjit, Duke S (2003) Ecophysiological aspects of allelopathy. Planta 217:529–539PubMedCrossRefGoogle Scholar
  47. Inderjit U, van der Putten WH (2010) Impacts of soil microbial communities on exotic plant invasion. Trends Ecol Evol 25:512–519PubMedCrossRefGoogle Scholar
  48. Jackman S (2012) pscl: Classes and Methods for R Developed in the Political Science Computational Laboratory, Stanford University. Department of Political Science, Stanford University. Stanford, California. R package version 1.04.4Google Scholar
  49. Jameson DA (1966) Pinyon-juniper litter reduces growth of blue grama. J Range Manage 4:214–217CrossRefGoogle Scholar
  50. Johnstone IM (1986) Plant invasion windows: A time-based classification of invasion potential. Biol Rev 61:369–394CrossRefGoogle Scholar
  51. Jones M, Fleming SA (2010) Organic chemistry, 4th edn. Norton, New YorkGoogle Scholar
  52. Kardol P, Cornips NJ, van Kempen MLL, Tanja Bakx-Schotman JM, Van der Putten WH (2007) Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecol Monogr 77:147–162CrossRefGoogle Scholar
  53. Keeley JE, Fotheringham CJ (1998) Smoke-induced seed germination in California chaparral. Ecology 79:2320–2336CrossRefGoogle Scholar
  54. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Lett Nat 417:67–70CrossRefGoogle Scholar
  55. Koch AM, Antunes PM, Barto EK, Cipollini D, Mummey DL, Klironomos JN (2011) The effects od arbuscular mycorrhizal (AM) fungal and garlic mustard introductions on native AM fungal diversity. Biol Invasions 13:1627–1639CrossRefGoogle Scholar
  56. Meiners SJ (2014) Functional correlates of allelopathic potential in a successional plant community. Plant Ecol 215:661–672CrossRefGoogle Scholar
  57. Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG, Seabloom EW, Torchin ME, Vázquez (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740PubMedCrossRefGoogle Scholar
  58. Muscolo A, Sidari M, Texeira da Silva JA (2013) Biological effects of water-soluble soil phenol and soil humic extracts on plant systems. Acta Physiol Plant 35:309–320CrossRefGoogle Scholar
  59. Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281PubMedCrossRefGoogle Scholar
  60. Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65CrossRefGoogle Scholar
  61. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288CrossRefGoogle Scholar
  62. Pisula NL, Meiners SJ (2010a) Allelopathic effects of goldenrod species on turnover in successional communities. Am Midl Nat 163:161–172CrossRefGoogle Scholar
  63. Pisula NL, Meiners SJ (2010b) Relative allelopathic potential of invasive plant species in a young disturbed woodland. J Torrey Bot Soc 137:81–87CrossRefGoogle Scholar
  64. Prati D, Bossdorf O (2004) Allelopathic inhibition of germination by Alliaria petiolata (Brassicaceae). Am J Bot 91:285–288PubMedCrossRefGoogle Scholar
  65. Qin R-M, Zheng Y-L, Valiente-Banuet A, Callaway RM, Barclay GF, Pereyra CS, Feng Y-U (2013) The evolution of increased competitive ability, innate competitive advantages, and novel biochemical weapons act in concert for a tropical invader. New Phytol 197:979–988PubMedCrossRefGoogle Scholar
  66. Core Team R (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  67. Reed HE, Seastedt TR, Blair JM (2005) Ecological consequences of C4 grass invasion of a C4 grassland: A dilemma for management. Ecol Appl 15:1560–1569CrossRefGoogle Scholar
  68. Reynolds HL, Packer A, Bever JD, Clay K (2003) Grass roots ecology: Plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291CrossRefGoogle Scholar
  69. Rice EL (1974) Allelopathy. Academic, New YorkGoogle Scholar
  70. Rice EL (1984) Allelopathy 2nd edn. Academic, OrlandoGoogle Scholar
  71. Roberts KJ, Anderson RC (2001) Effects of garlic mustard (Alliaria petiolata [Bieb. Cavara & Grande]) extracts on plants and arbuscular mycorrhizal (AM) fungi. Am Midl Nat 146:146–152CrossRefGoogle Scholar
  72. Ruiz ON, Hussein HS, Terry N, Daniell H (2003) Phytoremediation of organomercurial compounds vis chloroplast genetic engineering. Plant Physiol 132:1344–1352PubMedCentralPubMedCrossRefGoogle Scholar
  73. Samson FB, Knopf FL, Ostlie WR (2004) Great Plains ecosystem: past, present and future. Wildlife Soc B 32:6–15CrossRefGoogle Scholar
  74. Schmidt CD, Hickman KR, Channell R, Harmoney K, Stark W (2008) Competitive abilities of native grasses and non-native (Bothriochloa spp.) grasses. Plant Ecol 197:69–80CrossRefGoogle Scholar
  75. Singleton VL, Rossi JA Jr (1965) Colorimetry of total phenolics with phosphomolybdic–phosphotungstic acid reagents. Am J Enol Viticult 16:144–158Google Scholar
  76. Soil Survey Staff, Natural Resources Conservation Service, United States Department of Agriculture (2007) Web Soil Survey. http://websoilsurvey.nrcs.usda.gov/. Accessed 13 September 2013
  77. Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. Plos Biol 4:727–731CrossRefGoogle Scholar
  78. Uren NC (2007) Types, amounts, and possible functions of compounds released into rhizosphere by soil-grown plants. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere: biochemistry and organic substances at the soil-plant interface, 2nd edn. CRC Press, Boca Raton, pp 1–21CrossRefGoogle Scholar
  79. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New YorkCrossRefGoogle Scholar
  80. Vitousek PM, Mooney HA, Lubchenco J, Melillo M (1997) Human domination of earth’s ecosystems. Science 277:494–499CrossRefGoogle Scholar
  81. White LM, Dewald CL (1996) Yield and Quality of WW-Iron Master and caucasian bluestem regrowth. J Range Manage 49:42–45CrossRefGoogle Scholar
  82. Whittaker RJ, Feeny PP (1971) Allelochemics: chemical interactions between species. Science 171:757–770PubMedCrossRefGoogle Scholar
  83. Wilson GWT, Hartnett DC (1998) Interspecific variation in plant responses to mycorrhizal colonization in prairie grasses and forbs. Am J Bot 85:1732–1738PubMedCrossRefGoogle Scholar
  84. Wilson GWT, Hartnett DC, Rice CW (2006) Mycorrhizal-mediated phosphorus transfer between the tallgrass prairie plants Sorghastrum nutans and Artemisia ludoviciana. Funct Ecol 20:427–435CrossRefGoogle Scholar
  85. Wilson GWT, Hickman KR, Williamson MM (2012) Invasive warm-season grasses reduce mycorrhizal root colonization and biomass production of native prairie grasses. Mycorrhiza 22:327–336PubMedCrossRefGoogle Scholar
  86. Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Evol S 25:443–466CrossRefGoogle Scholar
  87. Zhou B, Kong C-H, Li Y-H, Wang P, Xu X-H (2013) Crabgrass (Digitaria sanguinalis) allelochemiclas that interfere with crop growth and soil microbial community. J Agr Food Chem 61:5310–5317CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Mitchell J. Greer
    • 1
    • 2
    Email author
  • Gail W. T. Wilson
    • 1
  • Karen R. Hickman
    • 1
  • Stuart M. Wilson
    • 3
  1. 1.Natural Resource Ecology and ManagementOklahoma State UniversityStillwaterUSA
  2. 2.Department of Biological SciencesFort Hays State UniversityHaysUSA
  3. 3.Plant and Soil SciencesOklahoma State UniversityStillwaterUSA

Personalised recommendations