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Mycorrhiza

, Volume 22, Issue 5, pp 327–336 | Cite as

Invasive warm-season grasses reduce mycorrhizal root colonization and biomass production of native prairie grasses

  • Gail W. T. WilsonEmail author
  • Karen R. Hickman
  • Melinda M. Williamson
Original Paper

Abstract

Soil organisms play important roles in regulating ecosystem-level processes and the association of arbuscular mycorrhizal (AM) fungi with a plant species can be a central force shaping plant species’ ecology. Understanding how mycorrhizal associations are affected by plant invasions may be a critical aspect of the conservation and restoration of native ecosystems. We examined the competitive ability of old world bluestem, a non-native grass (Caucasian bluestem [Bothriochloa bladhii]), and the influence of B. bladhii competition on AM root colonization of native warm-season prairie grasses (Andropogon gerardii or Schizachyrium scoparium), using a substitutive design greenhouse competition experiment. Competition by the non-native resulted in significantly reduced biomass production and AM colonization of the native grasses. To assess plant–soil feedbacks of B. bladhii and Bothriochloa ischaemum, we conducted a second greenhouse study which examined soil alterations indirectly by assessing biomass production and AM colonization of native warm-season grasses planted into soil collected beneath Bothriochloa spp. This study was conducted using soil from four replicate prairie sites throughout Kansas and Oklahoma, USA. Our results indicate that a major mechanism in plant growth suppression following invasion by Bothriochloa spp. is the alteration in soil microbial communities. Plant growth was tightly correlated with AM root colonization demonstrating that mycorrhizae play an important role in the invasion of these systems by Bothriochloa spp. and indicating that the restoration of native AM fungal communities may be a fundamental consideration for the successful establishment of native grasses into invaded sites.

Keywords

Arbuscular mycorrhizas Big bluestem Bothriochloa bladhii Bothriochloa ischaemum Little bluestem Old world bluestems Plant–soil feedback Tallgrass prairie Warm-season grasses 

Notes

Acknowledgments

This research was funded by the Oklahoma Agricultural Experiment Station, the National Science Foundation Long-Term Ecological Research Program (Konza Prairie Grant IBN-9632851), and the Oklahoma State University Department of Natural Resource Ecology and Management. We thank the Konza Prairie Biological Station, Fort Hays State University Department of Agriculture and Department of Biological Sciences, and the Oklahoma State University Field and Research Service Unit for permitting us to collect soil at their research sites.

References

  1. Abhilasha D, Quintana N, Vivanco J, Joshi J (2008) Do alleopathic compounds in invasive Solidago canadensis s.l. restrain the native European flora? J Ecol 96:993–1001CrossRefGoogle Scholar
  2. Allen MF, Allen EB (1990) Carbon source of VA mycorrhizal fungi associated with chenopodiaceae from a semiarid shrub-steppe. Ecology 71:2019–2021CrossRefGoogle Scholar
  3. Batten KM, Scow KM, Davies KF, Harrison SP (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions 8:217–230CrossRefGoogle Scholar
  4. Bennett AE, Bever JD (2009) Trade-offs between arbuscular mycorrhizal fungal competitive ability and host growth promotion in Plantago lanceolata. Oecologia 160:807–816PubMedCrossRefGoogle Scholar
  5. Bever JD (2002) Host-specificity of AM fungal population growth rates can generate feedback on plant growth. Plant Soil 244:281–290CrossRefGoogle Scholar
  6. Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. 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. J Ecol 85:561–573CrossRefGoogle Scholar
  8. Bever JD, Schultz PA, Miller RM, Gades L, Jastrow JD (2003) Prairie mycorrhizal fungi inoculant may increase native plant diversity on restored sites. Ecol Restoration 21:311–312CrossRefGoogle Scholar
  9. Bever JD, Richardson SC, Lawrence BM, Holmes J, Watson M (2009) Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol Let 12:13–21CrossRefGoogle Scholar
  10. Blair AC, Wolfe LM (2004) The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85:3035–3042CrossRefGoogle Scholar
  11. Calloway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443CrossRefGoogle Scholar
  12. Cano C, Bago A (2005) Competition and substrate colonization strategies of three polyxenically grown arbuscular mycorrhizal fungi. Mycologia 97:1201–1214PubMedCrossRefGoogle Scholar
  13. Ehrenfeld JG (2004) Implications of invasive species for belowground community and nutrient process. Weed Technol 18:1232–1235CrossRefGoogle Scholar
  14. Fargione J, Brown CS, Tilman D (2003) Community assembly and invasion: an experimental test of neutral versus niche processes. PNAS 100:8916–8920PubMedGoogle Scholar
  15. Grime JP, Macky JM, Hiller SH, Read DJ (1987) Mechanisms of floristic diversity: evidence from microcosm. Nature 328:420–422CrossRefGoogle Scholar
  16. Harmoney KR, Hickman KR (2004) Comparative morphology of Caucasian old world bluestem and native grasses. Agron J 96:1540–1544CrossRefGoogle Scholar
  17. Harmoney KR, Stahlman PW, Hickman KR (2004) Herbicide effects on established yellow old world bluestem (Bothriochloa ischaemum). Weed Technol 18:545–550CrossRefGoogle Scholar
  18. Harper JL (1977) Population biology of plants. Academic Press, San DiegoGoogle Scholar
  19. Hartnett DC, Wilson GWT (1999) Mycorrhizal mediation of plant species composition and diversity in tallgrass prairie. Ecology 80:122–130CrossRefGoogle Scholar
  20. Hartnett DC, Wilson GWT (2002) The role of mycorrhizas in plant community structure and dynamics: lessons from the grasslands. Plant Soil 244:319–331CrossRefGoogle Scholar
  21. Hawkes CV, Belnap J, D’Antonio C, Firestone MK (2006) Arbuscular mycorrhizal assemblages in native plant roots change in the presence of invasive exotic grasses. Plant Soil 281:369–380CrossRefGoogle Scholar
  22. Hepper CM, Sen R, Azconaguilar C, Grace C (1988) Variation in certain isozymes amongst different geographical isolates of the vesicular arbuscular mycorrhizal fungi Glomus clarum, Glomus monosporum and Glomus mosseae. Soil Biol Biochem 20:51–59CrossRefGoogle Scholar
  23. Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53PubMedCrossRefGoogle Scholar
  24. Hetrick BAD, Wilson GWT, Todd TC (1990) Differential responses of C3 and C4 grasses to mycorrhizal symbiosis, P fertilization, and soil microorganisms. Can J Bot 68:461–467CrossRefGoogle Scholar
  25. Inderjit, van der Putten WH (2010) Impacts of soil communities on exotic plant invasions. Trends Ecol Evol 25:512–519PubMedCrossRefGoogle Scholar
  26. Inderjit STR, Callaway RM, Pollock JL, Jasleen K (2008) Allelopathy and plant invasions: traditional, congeneric, and bio-geographical approaches. Biol Invasions 10:875–890CrossRefGoogle Scholar
  27. Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation as a driver of local adaptation in mycorrhizal symbioses. PNAS 107:2093–2098PubMedCrossRefGoogle Scholar
  28. Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plantrhizosphere mutualisms. Ann Rev Ecol Evol Syst 39:215–236Google Scholar
  29. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70PubMedCrossRefGoogle Scholar
  30. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA-mycorrhizas. Mycol Res 92:486–505CrossRefGoogle Scholar
  31. Leger EA, Rice KJ (2003) Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecol Lett 6:257–264CrossRefGoogle Scholar
  32. Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989CrossRefGoogle Scholar
  33. Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:1180–1186CrossRefGoogle Scholar
  34. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phyt 115:495–501CrossRefGoogle Scholar
  35. Middleton EL, Bever JD, Schultz PA (2009) The effect of restoration methods on the quality of the restoration and resistance to invasion by exotics. Restor Ecol 18:181–187CrossRefGoogle Scholar
  36. Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN et al (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740PubMedCrossRefGoogle Scholar
  37. Mummey DL, Rillig MC (2006) The invasive plant species Centaurea maculosa alters arbuscular mycorrhizal fungal communities in the field. Plant Soil 288:81–90CrossRefGoogle Scholar
  38. Mummey DL, Rillig MC, Holben WE (2005) Neighboring plant influences on arbuscular mycorrhizal fungal community composition as assessed by T-RFLP analysis. Plant Soil 271:83–90CrossRefGoogle Scholar
  39. Orr SP, Rudgersm JA, Clay K (2005) Invasive plants can inhibit native tree seedlings: testing potential allelopathic mechanisms. Plant Ecol 181:153–165CrossRefGoogle Scholar
  40. 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
  41. Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715CrossRefGoogle Scholar
  42. 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
  43. Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbesoil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291Google Scholar
  44. 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
  45. Seifert EK, Bever JD, Maron JL (2009) Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology 90:1055–1062PubMedCrossRefGoogle Scholar
  46. Shah MA, Reshi Z, Reshi I (2008) Mycorrhizosphere mediated mayweed chamomile invasion in the Kashmir Himalaya, India. Plant Soil 312:219–225CrossRefGoogle Scholar
  47. Shah MA, Reshi ZA, Khasa D (2009) Arbuscular mycorrhizal status of some Kashmir Himalayan alien invasive plants. Mycorrhiza 20:67–72PubMedCrossRefGoogle Scholar
  48. Smith MD, Knapp AK (1999) Exotic plant species in a C4-dominated grassland: invasibility, disturbance, and community structure. Oecologia 120:605–612CrossRefGoogle Scholar
  49. Smith MR, Charvat I, Jacobson RL (1998) Arbuscular mycorrhizae promote establishment of prairie species in a tallgrass prairie restoration. Can J Bot 76:1947–1954Google Scholar
  50. USDA NRCS (U.S. Department of Agriculture, Natural Resource Conservation Service) (2004) The PLANTS database: national plant data center, Baton Rouge, Louisiana, USAGoogle Scholar
  51. Vitousek PM, D’Antonio CM, Loope LL, Rejmanek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. New Zeal J Ecol 21:1–16Google Scholar
  52. Vitousek PM, Walker LR (1989) Biological invasions by Myrica-faya in Hawaii-plant demography, nitrogen-fixation, ecosystem effects. Ecol Monogr 59:247–265CrossRefGoogle Scholar
  53. Vogelsang KM, Bever JD (2009) Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology 90:399–407PubMedCrossRefGoogle Scholar
  54. Vogelsang KM, Bever JD, Griswold M, Schultz PA (2004) The use of mycorrhizal fungi in erosion control applications. Final report for Caltrans. California Department of Transportation Contract no. 65A0070. Sacramento, CaliforniaGoogle Scholar
  55. Watkins NK, Fitter AH, Graves JD, Robinson D (1996) Carbon transfer between C3 and C4 plants linked by a common mycorrhizal network, quantified using stable carbon isotopes. Soil Biol Biochem 28:471–477CrossRefGoogle Scholar
  56. Weidenhamer JD, Calloway RM (2010) Direct and indirect effects of invasive plants on soil chemistry and ecosystem function. J Chem Ecol 36:59–69PubMedCrossRefGoogle Scholar
  57. White JA, Tallaksen J, Charvat I (2008) The effects of arbuscular mycorrhizal fungal inoculation at a roadside prairie restoration site. Mycologia 100:6–11PubMedCrossRefGoogle Scholar
  58. Wilson GWT, Hartnett DC (1997) Effects of mycorrhizas on plant growth and dynamics in experimental tallgrass prairie microcosms. Am J Bot 84:478–482PubMedCrossRefGoogle Scholar
  59. 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
  60. 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
  61. Wilson GWT, Rice CW, Rillig MC, Springer A, and Hartnett DC (2009) Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol Lett 12:452–461Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Gail W. T. Wilson
    • 1
    Email author
  • Karen R. Hickman
    • 1
  • Melinda M. Williamson
    • 1
  1. 1.Natural Resource Ecology and ManagementOklahoma State UniversityStillwaterUSA

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