Soil fungi alter interactions between the invader Centaurea maculosa and North American natives

Ecology

Volumn 85, Issue 4, 2004, Pages 1062-1071

  Callaway, Ragan M ^a   Thelen, Giles C ^a   Barth, Sara ^a   Ramsey, Philip W ^a   Gannon, James E ^a  

^a UNIVERSITY OF MONTANA   (United States)

Author keywords

Centaurea; Communities; Competition; Fungi; Invasive exotics; Mutualism; Mycorrhizae; Phospholipid fatty acids (PLFA); Rhizosphere; Soil microbes; Spotted knapweed; Weeds

Indexed keywords

BIOLOGICAL INVASION; FUNGUS; INTERSPECIFIC INTERACTION; INVASIVE SPECIES; MICROBIAL COMMUNITY; SOIL MICROORGANISM; WEED CONTROL;

NORTH AMERICA; UNITED STATES; WESTERN HEMISPHERE; WORLD;

ACHILLEA; ACHILLEA MILLEFOLIUM; CELLULAR ORGANISMS; CENTAUREA; CENTAUREA MACULOSA; FESTUCA; FESTUCA IDAHOENSIS; FUNGI; GALLARDIA ARISTATA; KOELERIA; KOELERIA CRISTATA; KOELERIA MACRANTHA; LINUM; LINUM LEWISII; PSEUDOROEGNERIA; PSEUDOROEGNERIA SPICATA;

EID: 5344264323     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/02-0775     Document Type: Article

References (74)

1. Allen, E. B., and M. F. Allen. 1990. The mediation of competition by soil fungi in successional and patchy environments. Pages 367-389 in J. B. Grace and D. Tilman, editors. Perspectives on plant competition. Academic Press, New York, New York, USA.
2. Bais, H. P., T. S. Walker, F. R. Stermitz, R. A. Hufbauer, and J. M. Vivanco. 2002. Enantiomeric-dependent phytotoxic and antimicrobial activity of (±)-catechin. A rhizosecreted racemic mixture from spotted knapweed. Plant Physiology 128:1173-1179.
3. Bever, J. D. 1994. Feedback between plants and their soil communities in an old field community. Ecology 75:1965-1977.
4. Bever, J. D., J. Morton, J. Antonovics, and P. Schultz. 1996. Host-specificity of glomalean fungi: an experimental approach in an old field community. Journal of Ecology 84:71-82.
5. Bever, J, D., K. Westover, and J. Antonovics. 1997. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. Journal of Ecology 85:561-573.
6. Bligh, E. G., and W J. Dyer. 1956. A rapid method of total lipid extraction and purification. Canadian Journal Biochemistry Physiology 37:911-917.
7. Callaway, R. M., and E. T. Aschehoug. 2000. Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521-523.
8. Callaway, R. M., B. E. Mahall, C. Wicks, J. Pankey, and C. Zabinski. 2003. Soil fungi and the effects of an invasive forb on native versus naturalized grasses: neighbor identity matters. Ecology 84:565-573.
9. Callaway, R. M., B. Newingham, C. A. Zabinski, and B. E. Mahall. 2001. Compensatory growth and competitive ability of and invasive weed are enhanced by soil fungi and native neighbors. Ecology Letters 4:1-5.
10. Callaway, R. M., and S. C. Pennings. 2000. Facilitation may buffer competitive effects: indirect and diffuse interactions among salt marsh plants. American Naturalist 156:416-424.
11. Callaway, R. M., G. C. Thelen, A. Rodriguez, and W. E. Holben. In press. Release from inhibitory soil biota in Europe may promote plant invasion in North America. Nature.
12. Chiarello, N., J. C. Hickman, and H. A. Mooney. 1982. Endomycorrhizal role in interspecific transfer of phosphorus in a community of annual plants. Science 217:941-943.
13. Clay, K., and W. H. Van der Putten. 1999. Pathogens and plant life histories. Pages 275-319 in T. O. Vourisalo and P. K. Mutikainen, editors. Life history in plants. Kluwer Academic Publishers, New York, New York, USA.
14. Egerton-Warburton, L. M., and E. B. Allen. 2000. Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecological Applications 10:484-496.
15. Eom, A., D. C. Hartnett, and G. W. T. Wilson. 2000. Host plant species effects on arbuscular mycorrhizal fungal communities in tallgrass prairie. Oecologia 122:435-444.
16. Federle, T. W. 1986. Microbial distribution in soil-new techniques. Pages 493-498 in F. Megusar and M. Gantar, editors. Perspectives in microbial ecology. Slovene Society for Microbiology, Ljuljana, Slovenia.
17. Fitter, A. H., and R. Nichols. 1988. The use of benomyl to control infection by vesicular- arbuscular mycorrhizal fungi. New Phytologist 110:210-206.
18. Francis, R., and D. J. Read. 1984. Direct transfer of carbon between plants connected by vesicular-arbuscular mycorrhizal mycelium. Nature 307:53-56.
19. Frostegård, Å., and E. Bååth. 1996. The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biology and Fertility of Soils 22:59-65.
20. Frostegård, Å., A. Tunlid, and E. Bååth. 1993. Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Applied Environmental Microbiology 59:3605-3617.
21. Griffith, D., and J. R. Lucey. 1991. Economic evaluation of spotted knapweed (Centaurea maculosa) control using picloran. Journal of Range Management 44:43-47.
22. Grime, J. P., J. M. L. Mackey, S. H. Hillier, and D. J. Read. 1987. Floristic diversity in a model system using experimental microcosms. Nature 328:420-422.
23. Hartnett, D. C., B. A. D. Hetrick, G. W. T. Wilson, and D. J. Gibson. 1993. Mycorrhizal influence of intra- and inter-specific neighbor interactions among co-occurring prairie grasses. Journal of Ecology 81:787-795.
24. Hetrick, B. A. D., D. C. Hartnett, G. W. T. Wilson, and D. J. Gibson. 1994. Effects of mycorrhizae, phosphorus availability, and plant density on yield relationships among competing tallgrass prairie grasses. Canadian Journal of Botany 72:168-176.
25. Hetrick, B. A. D., G. T. Wilson, and D. C. Hartnett. 1989. Relationship between mycorrhizal dependence and competitive ability of two tallgrass prairie grasses. Canadian Journal of Botany 67:2608-2615.
26. 4 plants to mycorrhizal symbiosis, phosphorus fertilization, and soil microorganisms. Canadian Journal of Botany 68:461-467.
27. Hill, M. O. 1979. DECORANA - a FORTRAN program for detrended correspondence analysis. Cornell University, Ithaca, New York, USA.
28. Hooper, D. U., D. E. Bignell, V. K. Brown, L. Brussaard, J. M. Dangerfield, D. H. Wall, D. A. Wardle, D. C. Coleman, K. E. Giller, and P. Lavelle. 2000. Interactions between above and belowground biodiversity in terrestrial ecosystems: patterns, mechanisms, and feedbacks. BioScience 50:1049-1061.
29. Johnson, N. C., J. H. Graham, and F. A. Smith. 1997. Func-tioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytologist 135:575-585.
30. Klironomos, J. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67-70.
31. Koske, R. E., J. N. Gemma, and T. Flynn. 1992. Mycotrophy in Hawaiian angiosperms: a survey with implications for the origin of the native flora. American Journal of Botany 79:853-862.
32. Kroppenstedt, R. M. 1985. Fatty acids and menaquinone analysis of actinomycetes and related organisms. Pages 173-199 in M. Goodfellow and D. E. Minnikin, editors. Chemical methods in bacterial systematics. Academic Press, London, UK.
33. LeJeune, K. D., and T. R. Seastedt. 2001. Centaurea species: the forb that won the west. Conservation Biology 15:1568-1574.
34. Levine, J. M. 1999. Indirect facilitation: evidence and predictions from a riparian community. Ecology 80:1762-1769.
35. Lesica, P, and J. S. Shelley. 1996. Competitive effects of Centaurea maculosa on the population dynamics of Arabis fecundis. Bulletin of the Torrey Botanical Club 123:111-121.
36. Marler, M. J., C. A. Zabinski, and R. M. Callaway. 1999. Soil fungi indirectly enhance competitive effects of an invasive forb on a native bunchgrass. Ecology 80:1180-1186.
37. McCune, B. 1997. PC-ORD. Multivariate analysis of ecological data. Version 3.0. MjM Software Design, Gleneden Beach, Oregon, USA.
38. McGonigle, T. P., M. H. Miller, D. G. Evans, G. L. Fairchild, and J. A. Swan. 1990. A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytologist 115:495-501.
39. Miller, T. E. 1994. Direct and indirect species interactions in an early old-field plant community. American Naturalist 143:1007-1025.
40. Moora, M., and M. Zobel. 1996. Effect of arbuscular mycorrhiza on inter- and intraspecific competition of two grassland species. Oecologia 108:79-84.
41. Muir, A. D., and W. Majak. 1983. Allelopathic potential of diffuse knapweed (Centaurea diffusa) extracts. Canadian Journal of Plant Science 63:989-996.
42. Newsham, K. K., A. H. Fitter, and A. R. Watkinson. 1994. Root pathogenic and arbuscular mycorrhizal fungi determine fecundity of asmptomatic plants in the field. Journal of Ecology 82:805-814.
43. Olsson, P. A. 1999. Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiology Ecology 29:303-310.
44. Olsson, P. A., E. Bååth, and B. Jakobsen. 1995. The use of phospholipids and neutral fatty acids to estimate the biomass of arbuscular mycorrhizal fungi in soil. Mycological Research 99:623-629.
45. Packer, A., and K. Clay. 2000. Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278-281.
46. Paul, N. D., P. G. Ayres, and L. E. Wyness. 1989. On the use of fungicides for experimentation in natural vegetation. Functional Ecology 3:759-769.
47. Pedersen, C. T., and D. M. Sylvia. 1997. Limitations to using benomyl in evaluating mycorrhizal functioning. Biology and Fertility of Soils 25:163-168.
48. Phillips, J. M., and D. S. Hayman. 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55:158-161.
49. Reynolds, H. L. 1999. Plants interactions: competition. Pages 649-676 in F. I. Pugnaire and F. Valladares, editors. Handbook of functional ecology. Marcel and Dekker, New York, New York, USA.
50. Richardson, D. M., N. Allsopp, C. M. D'Antonio, S. J. Milton, M. Rejmánek. 2000. Plant invasions - the role of mutualisms. Biological Reviews 75:65-93.
51. Richardson, D. M., P. A. Williams, and R. J. Hobbs. 1994. Pine invasions in the Southern Hemisphere: determinants of spread and invadability. Journal of Biogeography 21:511-527.
52. Ridenour, W. M., and R. M. Callaway. 2001. The relative importance of allelopathy in interference: the effects of an invasive weed on a native bunchgrass. Oecologia 126:444-450.
53. Robinson, D., and A. Fitter. 1999. The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. Journal of Experimental Botany 50:9-13.
54. Saetre, P., and E. Bååth. 2000. Spatial variation and patterns of soil microbial community structure in a mixed sprucebirch stand. Soil Biology and Biochemistry 32:909-91.
55. Schmidt, S. K., and K. M. Scow. 1986. Mycorrhizal fungi on the Galapagos Islands. Biotropica 18:236-240.
56. Sheley, R. L., and J. S. Jacobs. 1997. "Acceptable" levels of spotted knapweed (Centaurea maculosa) control. Weed Technology 11:363-368.
57. Simard, S. W., D. S. Perry, M. D. Jones, D. D. Myrold, D. M. Durall, and R. Molina. 1997. Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579-582.
58. Smith, M. D., D. C. Hartnett, and C. W. Rice. 2000. Effects of long-term fungicide applications on microbial properties in tallgrass prairie soil. Soil Biology and Biochemistry 32:935-946.
59. SPSS. 1999. SPSS version 10.0.5. SPSS, Chicago, Illinois, USA.
60. van der Heijden, J. N. Klironomos, M. Ursic, P. Moutoglis, R. Streitwolf-Engel, T. Boller, A. Wiemken, and I. R. Sanders. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69-72.
61. Van der Putten, W. H. 1997. Plant-soil feedback as a selective force. Trends in Ecology and Evolution 12:169-170.
62. Van der Putten, W. 2002. How to be invasive. Nature 417:32-33.
63. Van der Putten, W. H., P. W. T. Maas, W. J. M. Van Gulik, and H. Brinkman. 1990. Characterization of soil organisms involved in the degeneration of Ammophila arenaria. Soil Biology and Biogeochemistry 22:845-852.
64. Van der Putten, W. H., and B. A. M. Peters. 1997. How soil-borne pathogens may affect plant competition. Ecology 78:1785-1795.
65. Van der Putten, W. H., C. van Dijk, and B. A. M. Peters. 1993. Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362:53-56.
66. Walter, L. E. Fisher, D. C. Hartnett, B. A. D. Hetrick, and A. P. Schwab. 1996. Interspecific nutrient transfer in a tall-grass prairie plant community. American Journal of Botany 83:180-184.
67. Wardle, D. A. 2002. Communities and ecosystems: linking the aboveground and belowground components. Princeton University Press, Princeton, New Jersey, USA.
68. Wardle, D. A., and K. S. Nicholson. 1996. Synergistic effects of grassland plants species on soil microbial biomass and activity: implications for ecosystem-level effects of enriched plant diversity. Functional Ecology 10:410-416.
69. 4 plants linked by a common mycorrhizal network, quantified using stable carbon isotopes. Soil Biology and Biogeochemistry 28:471-477.
70. West, H. M. 1996. Influence of arbuscular mycorrhizal infection on competition between Holcus lanatus and Dactylis glomerata. Journal of Ecology 84:429-438.
71. West, H. M., A. H. Fitter, and A. R. Watkinson. 1993. The influence of three biocides on the fungal associates of the roots of Vulpia ciliata ssp. ambigua under natural conditions. Journal of Ecology 81:345-350.
72. Westover, K. M., A. C. Kennedy, and S. E. Kelley. 1997. Patterns of rhizosphere microbial community structure associated with co-occurring plant species. Journal of Ecology 85:863-873.
73. White, D. C., and D. B. Ringelberg. 1998. Signature lipid biomarker analysis. Pages 255-272 in R. S. Burlage, editor. Techniques in microbial ecology. Oxford University Press, New York, New York, USA.
74. Zabinski, C. A., L. Quinn, and R. M. Callaway. 2002. Phosphorus uptake, not carbon transfer, explains arbuscular mycorrhizal enhancement of Centaurea maculosa in the presence of native grasses. Functional Ecology 16:758-765.