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Exotic cheatgrass and loss of soil biota decrease the performance of a native grass

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Abstract

Soil disturbances can alter microbial communities including arbuscular mycorrhizal (AM) fungi, which may in turn, affect plant community structure and the abundance of exotic species. We hypothesized that altered soil microbial populations owing to disturbance would contribute to invasion by cheatgrass (Bromus tectorum), an exotic annual grass, at the expense of the native perennial grass, squirreltail (Elymus elymoides). Using a greenhouse experiment, we compared the responses of conspecific and heterospecific pairs of cheatgrass and squirreltail inoculated with soil (including live AM spores and other organisms) collected from fuel treatments with high, intermediate and no disturbance (pile burns, mastication, and intact woodlands) and a sterile control. Cheatgrass growth was unaffected by type of soil inoculum, whereas squirreltail growth, reproduction and nutrient uptake were higher in plants inoculated with soil from mastication and undisturbed treatments compared to pile burns and sterile controls. Squirreltail shoot biomass was positively correlated with AM colonization when inoculated with mastication and undisturbed soils, but not when inoculated with pile burn soils. In contrast, cheatgrass shoot biomass was negatively correlated with AM colonization, but this effect was less pronounced with pile burn inoculum. Cheatgrass had higher foliar N and P when grown with squirreltail compared to a conspecific, while squirreltail had lower foliar P, AM colonization and flower production when grown with cheatgrass. These results indicate that changes in AM communities resulting from high disturbance may favor exotic plant species that do not depend on mycorrhizal fungi, over native species that depend on particular taxa of AM fungi for growth and reproduction.

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References

  • Barto EK, Antunes PM, Stinson K, Koch AM, Klironomos JN, Cipollini D (2011) Differences in arbuscular mycorrhizal fungal communities associated with sugar maple seedlings in and outside of invaded garlic mustard forest patches. Biol Invasions 13:2755–2762

    Article  Google Scholar 

  • Belnap J, Phillips SL (2001) Soil biota in an ungrazed grassland: response to annual grass (Bromus tectorum) invasion. Ecol Appl 11:1261–1275

    Article  Google Scholar 

  • Belnap J, Sherrod S (2009) Soil amendment effects on the exotic annual grass Bromus tectorum L. and facilitation of its growth by the native perennial grass Hilaria jamesii (Torr.) Benth. Plant Ecol 201:709–721

    Article  Google Scholar 

  • Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. TREE 25:468–478

    PubMed  Google Scholar 

  • Bradford JB, Lauenroth WK (2006) Controls over invasion of Bromus tectorum: the importance of climate, soil, disturbance and seed availability. J Veg Sci 17:693–704

    Google Scholar 

  • Brooks M, D’Antonio C, Richardson D, Grace J, Keeley J, DiTomaso J, Hobbs R, Pellant M, Pyke D (2004) Effects of invasive alien plants on fire regimes. Bioscience 54:677–688

    Article  Google Scholar 

  • Callaway RM, Cipollini D, Barto K, Thelen GC, Hallet SG, Prati D, Stinson K, Klironomos J (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043–1055

    Article  PubMed  Google Scholar 

  • Carey EV, Marler MJ, Callaway RM (2004) Mycorrhizae transfer carbon from a native grass to an invasive weed: evidence from stable isotopes and physiology. Plant Ecol 172:133–141

    Article  Google Scholar 

  • Carvalho LM, Antunes PM, Martins-Loução MA, Klironomos JN (2010) Disturbance influences the outcome of plant–soil biota interactions in the invasive Acacia longifolia and in native species. Oikos 119:1172–1180

    Article  Google Scholar 

  • Chambers JC, Roundy BA, Blank RR, Meyers SE, Whittaker A (2007) What makes Great Basin sagebrush ecosystems invasible by Bromus tectorum? Ecol Monogr 77:117–145

    Article  Google Scholar 

  • Coleman DC, Whitman WB (2005) Linking species richness, biodiversity and ecosystem function in soil systems. Pedobiologia 49:479–497

    Article  CAS  Google Scholar 

  • Condon L, Weisburg PJ, Chambers JC (2011) Abiotic and biotic influences on Bromus tectorum invasion and Artemisia tridentata recovery after fire. Int J Wildland Fire 20:597–604

    Article  Google Scholar 

  • D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle and global change. Annu Rev Ecol and Syst 23:63–87

    Google Scholar 

  • Davis MA, Grime JP, Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasability. J Ecol 88:528–534

    Article  Google Scholar 

  • Dodge RA, Fulé PZ, Sieg CH (2008) Dalmatian toadflax (Linaria dalmatica) response to wildfire in a southwestern USA forest. Ecoscience 15:213–222

    Article  Google Scholar 

  • Drigo B, Kowalchuk GA, van Veen JA (2008) Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44:667–679

    Article  Google Scholar 

  • Duncan CA, Jachetta JJ, Brown ML et al (2004) Assessing the economic, environmental, and societal losses from invasive plants on rangeland and wildlands. Weed Technol 18:1411–1416

    Article  Google Scholar 

  • Eschtruth A, Battles J (2009) Assessing the relative importance of disturbance, herbivory, diversity, and propagule pressure in exotic plant invasion. Ecol Monogr 79:265–280

    Article  Google Scholar 

  • Evans RD, Rimer R, Sperry L, Belnap J (2001) Exotic plant invasion alters nitrogen dynamics in an arid grassland. Ecol Appl 11:1301–1310

    Article  Google Scholar 

  • Harner MJ, Mummey DL, Stanford JA, Rillig MC (2010) Arbuscular mycorrhizal fungi enhance spotted knapweed growth across a riparian chronosequence. Biol Invasions 12:1481–1490

    Article  Google Scholar 

  • Haskins KE, Gehring CA (2004) Long-term effects of burning slash on plant communities and arbuscular mycorrhizae in a semi-arid woodland. J Appl Ecol 41:379–388

    Article  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 

  • Hernandez RR, Sandquist DR (2011) Disturbance of biological soil crust increases emergence of exotic vascular plants in California sage scrub. Plant Ecol 212:1709–1721

    Article  Google Scholar 

  • Hetrick BAD (1991) Mycorrhizas and root architecture. Experientia 47:355–362

    Article  Google Scholar 

  • Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC et al (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407

    Article  PubMed  Google Scholar 

  • Humphrey L, Schupp E (2004) Competition as a barrier to establishment of a native perennial grass (Elymus elymoides) in alien annual grass (Bromus tectorum) communities. J Arid Environ 58:405–422

    Article  Google Scholar 

  • Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? Ecol Appl 3:749–757

    Article  Google Scholar 

  • Johnson NC, Gehring CA (2007) Mycorrhizas: symbiotic mediators of rhizosphere and ecosystem processes. In: Cardon Z, Whitbeck J (eds) The rhizosphere: an ecological perspective. Academic Press, New York, pp 73–100

    Google Scholar 

  • Johnson NC, Graham JH, Smith AF (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phyt 135:575–585

    Article  Google Scholar 

  • Klemmedson JO, Smith JG (1964) Cheatgrass (Bromus tectorum L.C.). Bot Rev 30:226–262

    Article  Google Scholar 

  • Klironomos JN (2000) Host-specificity and functional diversity among arbuscular mycorrhizal fungi. In: Bell CR, Brylinsky M, and Johnson-Green P (eds) Microbial biosystems: new frontiers. Proceedings of the eighth international symposium on microbial ecology. Atlantic Canada Society for Microbial Ecology, Halifax, pp 845–851

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

    Article  PubMed  CAS  Google Scholar 

  • Korb JE, Johnson NC, Covington WW (2003) Arbuscular mycorrhizal densities respond rapidly to ponderosa pine restoration treatments. J Appl Ecol 40:101–110

    Article  Google Scholar 

  • Korb JE, Johnson NC, Covington WW (2004) Slash pile burning effects on soil biotic and chemical properties and plant establishment: recommendations for amelioration. Rest Ecol 12:52–62

    Article  Google Scholar 

  • Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant-soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992

    Article  PubMed  Google Scholar 

  • Lachat Instruments, Inc (1998) QuikChem method no. 13-115-01-1-B. Milwaukee, Wisconsin

  • Lankau R (2010) Soil microbial communities alter allelopathic competition between Alliaria petiolata and a native species. Biol Invasions 12:2059–2068

    Article  Google Scholar 

  • Leger EA (2008) the adaptive value of remnant native plants in invaded communities: an example from the Great Basin. Ecol Appl 18:1226–1235

    Article  PubMed  Google Scholar 

  • Lett CN, DeWald LE, Horton J (2011) Mycorrhizae and soil phosphorus affect growth of Celastrus orbiculatus. Biol Invasions 13:2339–2350

    Article  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–711

    Article  Google Scholar 

  • Mazzola MB, Chambers JC, Blank RR, Pyke DA, Schupp EW, Allcock KG, Doescher PS, Nowak RS (2011) Effects of resource availability and propagule supply on native species recruitment in sagebrush ecosystems invaded by Bromus tectorum. Biol Invasions 13:513–526

    Article  Google Scholar 

  • McGlone CM, Sieg CH, Kolb TE (2011) Invasion resistance and persistence: established plants win, even with disturbance and high propagule pressure. Biol Invasions 13:291–304

    Article  Google Scholar 

  • McGlone CM, Sieg CH, Kolb TE, Nietupsky T (2012) Established native perennial grasses out-compete an invasive annual grass regardless of soil water and nutrient availability. Plant Ecol 213:445–457

    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 Phytol 115:495–501

    Article  Google Scholar 

  • Meinhardt KA, Gehring CA (2012) Disrupting mycorrhizal mutualisms: a potential mechanism by which exotic tamarisk outcompetes native cottonwoods. Ecol Appl 22:532–549

    Article  PubMed  Google Scholar 

  • Miller M, Belnap J, Beatty S, Reynolds R (2006) Performance of Bromus tectorum L. in relation to soil properties, water additions, and chemical amendments in calcareous soils of southeastern Utah, USA. Plant Soil 288:1–18

    Article  CAS  Google Scholar 

  • Moles AT, Flores-Moreno H, Bonser SP et al (2012) Invasions: the trail behind, the path ahead, and a test of a disturbing idea. J Ecol 100:116–127

    Article  Google Scholar 

  • Monaco TA, Johnson DA, Norton JM, Jones TA, Connors KJ, Norton JB, Redinbaugh MB (2003) Contrasting responses of intermountain west grasses to soil nitrogen. J Range Manag 56:282–290

    Article  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 

  • Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793

    Article  PubMed  CAS  Google Scholar 

  • Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411

    Article  PubMed  CAS  Google Scholar 

  • Owen SM, Sieg CH, Gehring CA, Bowker MA (2009) Above- and belowground responses to tree thinning depend on the treatment of tree debris. For Ecol Manag 259:71–80

    Article  Google Scholar 

  • Perkins LB, Nowak RS (2013) Native and non-native grasses generate common types of plant–soil feedbacks by altering soil nutrients and microbial communities. Oikos 122:199–208

    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 

  • Ramsey DK (2003) Soil survey of cortez area, colorado, parts of Dolores and Montezuma Counties. USDA, National Resources Conservation Service, p 628

  • Ray-Mukherjee J, Jones TA, Adler PB, Monaco TA (2011) Immature seedling growth of two north American native perennial bunchgrasses and the invasive grass Bromus tectorum. Rangel Ecol Manag 64:358–365

    Article  Google Scholar 

  • Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457

    Article  PubMed  Google Scholar 

  • Rowe HI, Brown CS, Claassen VP (2007) Comparisons of mycorrhizal responsiveness with field soil and commercial inoculum for six montane species and Bromus tectorum. Rest Ecol 15:44–52

    Article  Google Scholar 

  • Rowe HI, Brown CS, Paschke MW (2009) The influence of soil inoculum and nitrogen availability on restoration of high-elevation steppe communities invaded by Bromus tectorum. Rest Ecol 17:686–694

    Article  Google Scholar 

  • SAS Institute, Inc (2010) JMP version 9.0.2, statistical analysis software. SAS Institute, Inc., Cary

  • Schnoor TK, Lekberg Y, Rosendahl S, Axel Olsson P (2011) Mechanical soil disturbance as a detriment of arbuscular mycorrhizal fungal communities in a semi-natural grassland. Mycorrhiza 21:211–220

    Article  PubMed  Google Scholar 

  • Sharma SK, Ramesh A, Sharma MP, Joshi OP, Govaerts B, Steenwerth KL, Karlen DL (2011) Microbial community structure and diversity as indicators for evaluating soil quality. Biodiv Biofuel Agrofor Conserv Agric 5:317–358

    Article  Google Scholar 

  • Sieg CH, Phillips BG, Moser LP (2003) Exotic invasive plants. In: Friederici P (ed) Ecological restoration of southwestern ponderosa pine forests. Island Press, Washington, DC, pp 251–267

  • Simberloff D, Parker IM, Windle PN (2005) Introduced species policy, management, and future research needs. Front Ecol Environ 3:12–20

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, San Diego

    Google Scholar 

  • Stampe ED, Daehler CC (2003) Mycorrhizal species identity affects plant community structure and invasion: a microcosm study. Oikos 100:362–372

    Article  Google Scholar 

  • 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 4:727–731

    Article  CAS  Google Scholar 

  • Thomsen M, D’Antonio C, Suttle K, Sousa W (2006) Ecological resistance, seed density and their interactions determine patterns of invasion in a California coastal grassland. Ecol Lett 9:160–170

    Article  PubMed  Google Scholar 

  • van de Voorde TFJ, van der Putten WH, Bezemer TM (2012) Soil inoculation method determines the strength of plant-soil interactions. Soil Biol Biochem 55:1–6

    Article  Google Scholar 

  • Veiga RSL, Jansa J, Frossard E, van der Heijden MGA (2011) Can arbuscular mycorrhizal fungi reduce the growth of agricultural weeds? PLoS ONE 6(12):e27825. doi:10.1371/journal.pone.0027825

    Article  PubMed  CAS  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbio 64:5004–5007

    CAS  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 

  • Wakelin SA, Macdonald LM, Rogers SL, Gregg AL, Bolger TP, Baldock JA (2008) Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural soils. Soil Biol Biochem 40:803–813

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wolfson BAS, Kolb TE, Sieg CH, Clancy KM (2005) Effects of post-fire conditions on germination and seedling success of diffuse knapweed in northern Arizona. For Ecol Manage 216:342–358

    Article  Google Scholar 

  • Yoshida LC, Allen EB (2001) Response to ammonium and nitrate by a mycorrhizal annual invasive grass and native shrub in southern California. Am J Bot 88:1430–1436

    Article  PubMed  CAS  Google Scholar 

  • Young JA, Evans RA (1978) Population dynamics after wildfires in sagebrush grasslands. J Range Manag 31:283–289

    Article  Google Scholar 

  • Zhang J, Zhang C (2012) Sampling and sampling strategies for environmental analysis. Intern J Environ Anal Chem 92:466–478

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Steve Overby, Breanne Fortin, Carolyn Myren, Colleen Cooley, John Hockersmith, Bradford Blake, Phil Patterson, Anita Antoninka, Andrew Owen and the Gehring and Johnson lab groups at NAU. This project was funded by the USDA Forest Service, Rocky Mountain Research Station under cost share agreement 05-CS-11221615-152. N. C. Johnson acknowledges financial support from the Fulbright Commission of the Czech Republic.

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Authors and Affiliations

  1. USDA Forest Service, Rocky Mountain Research Station, 2500 S. Pine Knoll Drive, Flagstaff, AZ, 86001, USA

    Suzanne M. Owen & Carolyn Hull Sieg

  2. School of Earth Sciences and Environmental Sustainability, Northern Arizona University, Flagstaff, AZ, 86011, USA

    Nancy Collins Johnson

  3. Department of Biological Sciences, Northern Arizona University, Box 5640, Flagstaff, AZ, 86011, USA

    Nancy Collins Johnson & Catherine A. Gehring

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  1. Suzanne M. Owen
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Correspondence to Suzanne M. Owen.

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Owen, S.M., Sieg, C.H., Johnson, N.C. et al. Exotic cheatgrass and loss of soil biota decrease the performance of a native grass. Biol Invasions 15, 2503–2517 (2013). https://doi.org/10.1007/s10530-013-0469-0

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