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

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.

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References

  • 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 96:993–1001

    Article  Google Scholar 

  • Allen MF, Allen EB (1990) Carbon source of VA mycorrhizal fungi associated with chenopodiaceae from a semiarid shrub-steppe. Ecology 71:2019–2021

    Article  Google Scholar 

  • Batten KM, Scow KM, Davies KF, Harrison SP (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biol Invasions 8:217–230

    Article  Google Scholar 

  • Bennett AE, Bever JD (2009) Trade-offs between arbuscular mycorrhizal fungal competitive ability and host growth promotion in Plantago lanceolata. Oecologia 160:807–816

    Article  PubMed  Google Scholar 

  • Bever JD (2002) Host-specificity of AM fungal population growth rates can generate feedback on plant growth. Plant Soil 244:281–290

    Article  CAS  Google Scholar 

  • Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473

    Article  Google Scholar 

  • Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573

    Article  Google Scholar 

  • 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 21:311–312

    Article  Google Scholar 

  • Bever JD, Richardson SC, Lawrence BM, Holmes J, Watson M (2009) Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol Let 12:13–21

    Article  Google Scholar 

  • Blair AC, Wolfe LM (2004) The evolution of an invasive plant: an experimental study with Silene latifolia. Ecology 85:3035–3042

    Article  Google Scholar 

  • Calloway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443

    Article  Google Scholar 

  • Cano C, Bago A (2005) Competition and substrate colonization strategies of three polyxenically grown arbuscular mycorrhizal fungi. Mycologia 97:1201–1214

    Article  PubMed  Google Scholar 

  • Ehrenfeld JG (2004) Implications of invasive species for belowground community and nutrient process. Weed Technol 18:1232–1235

    Article  Google Scholar 

  • Fargione J, Brown CS, Tilman D (2003) Community assembly and invasion: an experimental test of neutral versus niche processes. PNAS 100:8916–8920

    PubMed  CAS  Google Scholar 

  • Grime JP, Macky JM, Hiller SH, Read DJ (1987) Mechanisms of floristic diversity: evidence from microcosm. Nature 328:420–422

    Article  Google Scholar 

  • Harmoney KR, Hickman KR (2004) Comparative morphology of Caucasian old world bluestem and native grasses. Agron J 96:1540–1544

    Article  Google Scholar 

  • Harmoney KR, Stahlman PW, Hickman KR (2004) Herbicide effects on established yellow old world bluestem (Bothriochloa ischaemum). Weed Technol 18:545–550

    Article  CAS  Google Scholar 

  • Harper JL (1977) Population biology of plants. Academic Press, San Diego

    Google Scholar 

  • Hartnett DC, Wilson GWT (1999) Mycorrhizal mediation of plant species composition and diversity in tallgrass prairie. Ecology 80:122–130

    Article  Google Scholar 

  • Hartnett DC, Wilson GWT (2002) The role of mycorrhizas in plant community structure and dynamics: lessons from the grasslands. Plant Soil 244:319–331

    Article  CAS  Google Scholar 

  • 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 281:369–380

    Article  CAS  Google Scholar 

  • 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 20:51–59

    Article  CAS  Google Scholar 

  • Herre EA, Knowlton N, Mueller UG, Rehner SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14:49–53

    Article  PubMed  Google Scholar 

  • 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 68:461–467

    Article  Google Scholar 

  • Inderjit, van der Putten WH (2010) Impacts of soil communities on exotic plant invasions. Trends Ecol Evol 25:512–519

    Article  PubMed  CAS  Google Scholar 

  • Inderjit STR, Callaway RM, Pollock JL, Jasleen K (2008) Allelopathy and plant invasions: traditional, congeneric, and bio-geographical approaches. Biol Invasions 10:875–890

    Article  Google Scholar 

  • Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation as a driver of local adaptation in mycorrhizal symbioses. PNAS 107:2093–2098

    Article  PubMed  CAS  Google Scholar 

  • Kiers ET, Denison RF (2008) Sanctions, cooperation, and the stability of plantrhizosphere mutualisms. Ann Rev Ecol Evol Syst 39:215–236

    Google Scholar 

  • Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70

    Article  PubMed  CAS  Google Scholar 

  • Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA-mycorrhizas. Mycol Res 92:486–505

    Article  Google Scholar 

  • Leger EA, Rice KJ (2003) Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecol Lett 6:257–264

    Article  Google Scholar 

  • Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of biotic resistance to exotic plant invasions. Ecol Lett 7:975–989

    Article  Google Scholar 

  • Marler MJ, Zabinski CA, Callaway RM (1999) Mycorrhizae indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:1180–1186

    Article  Google Scholar 

  • 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 115:495–501

    Article  Google Scholar 

  • 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 18:181–187

    Article  Google Scholar 

  • Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN et al (2006) Biotic interactions and plant invasions. Ecol Lett 9:726–740

    Article  PubMed  Google Scholar 

  • Mummey DL, Rillig MC (2006) The invasive plant species Centaurea maculosa alters arbuscular mycorrhizal fungal communities in the field. Plant Soil 288:81–90

    Article  CAS  Google Scholar 

  • Mummey DL, Rillig MC, Holben WE (2005) Neighboring plant influences on arbuscular mycorrhizal fungal community composition as assessed by T-RFLP analysis. Plant Soil 271:83–90

    Article  CAS  Google Scholar 

  • Orr SP, Rudgersm JA, Clay K (2005) Invasive plants can inhibit native tree seedlings: testing potential allelopathic mechanisms. Plant Ecol 181:153–165

    Article  Google Scholar 

  • Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. Bioscience 50:53–65

    Article  Google Scholar 

  • Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol Syst 40:699–715

    Article  Google Scholar 

  • Reed HE, Seastedt TR, Blair JM (2005) Ecological consequences of C4 grass invasion of a C4 grassland: a dilemma for management. Ecol Appl 15:1560–1569

    Article  Google Scholar 

  • Reynolds HL, Packer A, Bever JD, Clay K (2003) Grassroots ecology: plant-microbesoil interactions as drivers of plant community structure and dynamics. Ecology 84:2281–2291

    Google Scholar 

  • Schmidt CD, Hickman KR, Channell R, Harmoney K, Stark W (2008) Competitive abilities of native grasses and non-native (Bothriochloa spp.) grasses. Plant Ecol 197:69–80

    Article  Google Scholar 

  • Seifert EK, Bever JD, Maron JL (2009) Evidence for the evolution of reduced mycorrhizal dependence during plant invasion. Ecology 90:1055–1062

    Article  PubMed  Google Scholar 

  • Shah MA, Reshi Z, Reshi I (2008) Mycorrhizosphere mediated mayweed chamomile invasion in the Kashmir Himalaya, India. Plant Soil 312:219–225

    Article  CAS  Google Scholar 

  • Shah MA, Reshi ZA, Khasa D (2009) Arbuscular mycorrhizal status of some Kashmir Himalayan alien invasive plants. Mycorrhiza 20:67–72

    Article  PubMed  Google Scholar 

  • Smith MD, Knapp AK (1999) Exotic plant species in a C4-dominated grassland: invasibility, disturbance, and community structure. Oecologia 120:605–612

    Article  Google Scholar 

  • Smith MR, Charvat I, Jacobson RL (1998) Arbuscular mycorrhizae promote establishment of prairie species in a tallgrass prairie restoration. Can J Bot 76:1947–1954

    Google Scholar 

  • USDA NRCS (U.S. Department of Agriculture, Natural Resource Conservation Service) (2004) The PLANTS database: national plant data center, Baton Rouge, Louisiana, USA

  • 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 21:1–16

    Google Scholar 

  • Vitousek PM, Walker LR (1989) Biological invasions by Myrica-faya in Hawaii-plant demography, nitrogen-fixation, ecosystem effects. Ecol Monogr 59:247–265

    Article  Google Scholar 

  • Vogelsang KM, Bever JD (2009) Mycorrhizal densities decline in association with nonnative plants and contribute to plant invasion. Ecology 90:399–407

    Article  PubMed  Google Scholar 

  • 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, California

    Google Scholar 

  • 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 28:471–477

    Article  CAS  Google Scholar 

  • Weidenhamer JD, Calloway RM (2010) Direct and indirect effects of invasive plants on soil chemistry and ecosystem function. J Chem Ecol 36:59–69

    Article  PubMed  CAS  Google Scholar 

  • White JA, Tallaksen J, Charvat I (2008) The effects of arbuscular mycorrhizal fungal inoculation at a roadside prairie restoration site. Mycologia 100:6–11

    Article  PubMed  Google Scholar 

  • Wilson GWT, Hartnett DC (1997) Effects of mycorrhizas on plant growth and dynamics in experimental tallgrass prairie microcosms. Am J Bot 84:478–482

    Article  PubMed  CAS  Google Scholar 

  • Wilson GWT, Hartnett DC (1998) Interspecific variation in plant responses to mycorrhizal colonization in prairie grasses and forbs. Am J Bot 85:1732–1738

    Article  PubMed  CAS  Google Scholar 

  • Wilson GWT, Hartnett DC, Rice CW (2006) Mycorrhizal-mediated phosphorus transfer between the tallgrass prairie plants Sorghastrum nutans and Artemisia ludoviciana. Funct Ecol 20:427–435

    Article  Google Scholar 

  • 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 12:452–461

    Google Scholar 

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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.

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Correspondence to Gail W. T. Wilson.

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Wilson, G.W.T., Hickman, K.R. & Williamson, M.M. Invasive warm-season grasses reduce mycorrhizal root colonization and biomass production of native prairie grasses. Mycorrhiza 22, 327–336 (2012). https://doi.org/10.1007/s00572-011-0407-x

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  • DOI: https://doi.org/10.1007/s00572-011-0407-x

Keywords

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