Plant and Soil

, Volume 288, Issue 1–2, pp 81–90 | Cite as

The invasive plant species Centaurea maculosa alters arbuscular mycorrhizal fungal communities in the field

Original Paper

Abstract

While several recent studies have described changes in microbial communities associated with exotic plant invasion, how arbuscular mycorrhizal fungi (AMF) communities respond to exotic plant invasion is not well known, despite the salient role of this group in plant interactions. Here, we use molecular methods (terminal restriction fragment length polymorphism analyses based on the large subunit of the rRNA gene) to examine AMF community structure in sites dominated by the invasive mycorrhizal forb, Centaurea maculosa Lam. (spotted knapweed), and in adjacent native grassland sites. Our results indicate that significant AMF community alteration occurs following C. maculosa invasion. Moreover, a significant reduction in the number of restriction fragment sizes was found for samples collected in C. maculosa-dominated areas, suggesting reduced AMF diversity. Extraradical hyphal lengths exhibited a significant, on average 24%, reduction in C. maculosa-versus native grass-dominated sites. As both AMF community composition and abundance were altered by C.maculosa invasion, these data are strongly suggestive of potential impacts on AMF-mediated ecosystem processes. Given that the composition of AMF communities has the potential to differentially influence different plant species, our results may have important implications for site restoration after weed invasion.

Keywords

Centaurea maculosa Arbuscular mycorrhiza Terminal restriction fragment length polymorphism Invasive species Extraradical hyphae 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgments

This work was supported by grants from NSF Ecology (0515904) and USDA-CSREES (2005-35320-16267). We thank Eli Loomis and Kaerlek Janislampi for assistance with sampling and hyphal analyses.

References

  1. Allen MF (1991) The ecology of mycorrhizae. Cambridge University Press, UK, pp 84–95Google Scholar
  2. Bais HP, Walker TS, Stermitz FR, Hufbauer RA, Vivanco JM (2002) Enantiomeric-dependent phytotoxic and antimicrobial activity of ( ± )-catechin. A rhizosecreted racemic mixture from spotted knapweed. Plant Physiol 128:1173–1179PubMedCrossRefGoogle 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. Belnap J, Phillips SL (2001) Soil biota in an ungrazed grassland: response to annual grass (Bromus tectorum) invasion. Ecol Appl 11:1261–1275Google Scholar
  5. 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
  6. Bever JD (2003) Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytol 157:465–473CrossRefGoogle Scholar
  7. Bonnet E, Van de Peer Y (2002) zt: a software tool for simple and partial Mantel tests. J State Softw 7:1–12Google Scholar
  8. Booth MS, Caldwell MM, Stark JM (2003) Overlapping resource use in three Great Basin species: implications for community invasibility and vegetation dynamics. J Ecol 91:36–48CrossRefGoogle Scholar
  9. Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology 82:3057–3068CrossRefGoogle Scholar
  10. Callaway RM, Newingham B, Zabinski CA, Mahall BE (2001) Compensatory growth and competitive ability of an invasive weed are enhanced by soil fungi and native neighbors. Ecol Lett 4:429–433CrossRefGoogle Scholar
  11. Callaway RM, Mahall BE, Wicks C, Pankey J, Zabinski C (2003) Soil fungi and the effects of an invasive forb on grasses: neighbor identity matters. Ecology 84:129–135Google Scholar
  12. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasions. Nature 427:731–733PubMedCrossRefGoogle Scholar
  13. 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 172:133–141CrossRefGoogle Scholar
  14. Clark RB (1997) Arbuscular mycorrhizal adaptation, spore germination, root colonization, and host plant growth and mineral acquisition at low pH. Plant Soil 192:15–22CrossRefGoogle Scholar
  15. Eliason SA, Allen EB (1997) Exotic grass competition in suppressing native shrubland re-establishment. Restor Ecol 5:245–255CrossRefGoogle Scholar
  16. Enloe SF, DiTomaso JM, Orloff SB, Drake DJ (2004) Soil water dynamics differ among rangeland plant communities dominated by yellow starthistle (Centaurea solstitialis), annual grasses, or perennial grasses. Weed Sci 52:929–935CrossRefGoogle Scholar
  17. Gollotte A, van Tuinen D, Atkinson D (2004) Diversity of arbuscular mycorrhizal fungi colonizing roots of the grass species Agrostis capillaries and Lolium perenne in a field experiment. Mycorrhiza 14:111–117PubMedCrossRefGoogle Scholar
  18. Hart MM, Reader RJ, Klironomos JN (2003) Plant coexistence mediated by arbuscular mycorrhizal fungi. Trends Ecol Evol 18:418–423CrossRefGoogle Scholar
  19. Hartnett DC, Wilson GWT (1999) Mycorrhizae influence plant community structure and diversity in tallgrass prairie. Ecology 80:1187–1195CrossRefGoogle Scholar
  20. Hartnett DC, Wilson GWT (2002) The role of mycorrhizas in plant community structure and dynamics: lessons from grasslands. Plant Soil 244:319–331CrossRefGoogle Scholar
  21. Hawkes CV, Wren IF, Herman DJ, Firestone MK (2005) Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecol Lett 8:976–985CrossRefGoogle Scholar
  22. 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
  23. Helgason T, Merryweather JW, Denison J, Wilson P, Young JPW, Fitter AH (2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. J Ecol 90:371–384CrossRefGoogle Scholar
  24. Hobbie SE (1992) Effects of plant species on nutrient cycling. Trends Ecol Evol 7:336–339CrossRefGoogle Scholar
  25. Jakobsen I, Abbott LK, Robson AD (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. spread of hyphae and phosphorus inflow into roots. New Phytol 120:371–380CrossRefGoogle Scholar
  26. Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP, Young PW, Read DJ (2003) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515CrossRefGoogle Scholar
  27. Klein DA, Paschke MW (2000) A soil microbial community structural-functional index: the microscopy-based Total/Active/Active Fungal Bacterial (TA/AFB) Biovolumes Ratio. Appl Soil Ecol 14:257–268CrossRefGoogle Scholar
  28. Klein DA, Paschke MW, Heskett TL (2006) Comparative fungal responses in managed plant communities infested by spotted (Centaurea maculosa Lam.) and diffuse (C.diffusa Lam.) knapweed. Appl Soil Ecol 32:89–97CrossRefGoogle Scholar
  29. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70PubMedCrossRefGoogle Scholar
  30. Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301Google Scholar
  31. Kourtev PS, Ehrenfeld JG, Häggblom M (2002) Exotic plant species alter the microbial community structure and function in soil. Ecology 83:3152–3166Google Scholar
  32. Kourtev PS, Ehrenfeld JG, Häggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35:895–905CrossRefGoogle Scholar
  33. Kropf S, Heurer H, Gruning M, Smalla K (2004) Significance test for comparing complex microbial community fingerprints using pairwise similarity measures. J␣Microbiol Meth 57:187–195CrossRefGoogle Scholar
  34. Lacey JR, Marlow CB, Lane JR (1989) Influence of spotted knapweed (Centaurea maculosa) on surface runoff and sediment yield. Weed Technol 3:627–631Google Scholar
  35. Levine JM, Vila M, D’Antonio CMD, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond 270:775–781CrossRefGoogle Scholar
  36. Lutgen ER, Rillig MC (2004) Influence of spotted knapweed (Centaurea maculosa) management treatments on arbuscular mycorrhizae and soil aggregation. Weed Sci 52:172–177CrossRefGoogle Scholar
  37. Lutgen ER, Clairmont DL, Graham J, Rillig MC (2003) Seasonality of arbuscular mycorrhizal hyphae and glomalin in a western Montana grassland. Plant Soil 257:71–83CrossRefGoogle Scholar
  38. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  39. 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
  40. 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
  41. Mummey DL, Holben WE, Six J, Stahl PD (2006a) Spatial stratification of soil bacterial populations in aggregates of diverse soils. Microb Ecol 51(3):404–411Google Scholar
  42. Mummey DL, Six J, Rillig MC (2006b) Influence of endogeic earthworm activities on bacterial communities associated with different soil aggregate size fractions. Soil Biol Biochem (10.1016/j.soilbio.2005.11.014)Google Scholar
  43. Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol 10:407–411CrossRefGoogle Scholar
  44. Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extracting with sodium bicarbonate. USDA Circ. 939. US Gov. Print. Office, Washington, DCGoogle Scholar
  45. 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
  46. Rees GN, Baldwin DS, Watson GO, Perryman S, Nielsen DL (2004) Ordination and significance testing of microbial community composition derived from terminal restriction fragment length polymorphisms: application of multivariate statistics. Antonie van Leeuwenhoek 86:339–347PubMedCrossRefGoogle Scholar
  47. Rillig MC, Field CB, Allen MF (1999) Soil biota responses to log-term atmospheric CO2 enrichment in two California annual grasslands. Oecologia 119:572–577CrossRefGoogle Scholar
  48. Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754CrossRefGoogle Scholar
  49. Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53PubMedCrossRefGoogle Scholar
  50. Simard SW, Durall DM (2004) Mycorrhizal networks: a review of their extent, function, and importance. Can J Bot 82:1166–1176CrossRefGoogle Scholar
  51. Tennant D (1975) A test of a modified line intersect method of estimating root length. J Ecol 63:995–1001CrossRefGoogle Scholar
  52. Trouvelot S, van Tuinen D, Hijri M, Gianinazzi-Pearson V (1999) Visualisation of ribosomal DNA loci in spore interphasic nuclei of glomalean fungi by fluorescence in situ hybridization. Mycorrhiza 8:203–206CrossRefGoogle Scholar
  53. Van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal biodiversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72CrossRefGoogle Scholar
  54. Van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plants. New Phytol 157:569–578CrossRefGoogle Scholar
  55. Van der Heijden MGA (2004) Arbuscular mycorrhizal fungi as support systems for seedling establishment in grassland. Ecol Lett 7:293–303CrossRefGoogle Scholar
  56. Vandenkoornhuyse P, Husband R, Daniell TJ, Watson IJ, Duck M, Fitter A H, Young JPW (2002) Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol Ecol 11:1555–1564PubMedCrossRefGoogle Scholar
  57. Vandenkoornhuyse P, Ridgeway KP, Watson IJ, Duck M, Fitter AH, Young JPW (2003) Co-existing grass species have distinctive arbuscular mycorrhizal communities. Mol Ecol 12:3085–3095PubMedCrossRefGoogle Scholar
  58. Van Tuinen D, Jacquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V (1998) Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25S rDNA-targeted nested PCR. Mol Ecol 7:879–887PubMedCrossRefGoogle Scholar
  59. Vivanco JM, Bais HP, Stermitz FR, Thelen GC, Callaway RM (2004) Biogeographical variation in community response to root allelochemistry: novel weapons and exotic invasion. Ecol Lett 7:285–292CrossRefGoogle Scholar
  60. Walling SZ, Zabinski CA (2004) Host plant differences in arbuscular mycorrhizae: extra radical hyphae differences between an invasive forb and a native bunchgrass. Plant Soil 265:335–344CrossRefGoogle Scholar
  61. Wolfe BE, Klironomos JN (2005) Breaking new ground: soil communities and exotic plant invasion. Bioscience 55:477–487CrossRefGoogle Scholar
  62. Wood YA, Meixner T, Shouse PJ, Allen EB (2006) Altered ecohydrologic response drives native shrub loss under conditions of elevated nitrogen deposition. J Environ Qual 35:76–92PubMedCrossRefGoogle Scholar
  63. Zabinski CA, Quinn L, Callaway RM (2002) Phosphorus uptake, not carbon transfer, explains arbuscular mycorrhizal enhancement of Centaurea maculosa in the presence of native grassland species. Funct Ecol 16:758–765CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  1. 1.Microbial Ecology Program, Division of Biological SciencesThe University of MontanaMissoulaUSA

Personalised recommendations