Soil fertility, heterogeneity, and microbes: Towards an integrated understanding of grassland structure and dynamics

Applied Vegetation Science

Volumn 12, Issue 1, 2009, Pages 33-44

  Reynolds, Heather L ^a   Haubensak, Karen A ^b  

^a INDIANA UNIVERSITY   (United States)

^b NORTHERN ARIZONA UNIVERSITY   (United States)

Author keywords

Microbially mediated niche partitioning; Plant community diversity; Plant microbe feedback; Soil fertility; Soil heterogeneity

Indexed keywords

EID: 70249104638     PISSN: 14022001     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1654-109X.2009.01020.x     Document Type: Article

References (98)

1. Agrawal, A.A., Ackerly, D.D., Adler, F., Arnold, A.E., Cáceres, C., Doak, D.F., Post, E., Hudson, P.J., Maron, J., Mooney, K.A., Power, M., Schemske, D., Stachowicz, J., Strauss, S., Turner, M.G. & Werner, E. 2007. Filling key gaps in population and community ecology. Frontiers in Ecology and the Environment 5: 145-152. (Pubitemid 46598273)
2. Alpert, P. & Maron, J.L. 2000. Carbon addition as a countermeasure against biological invasion by plants. Biological Invasions 2: 33-40. (Pubitemid 30829649)
3. Amarasekare, P. 2003. Competitive coexistence in spatially structured environments: a synthesis. Ecology Letters 6: 1109-1122. (Pubitemid 37537833)
4. Baer, S.G., Blair, J.M., Collins, S.L. & Knapp, A.K. 2004. Plant community responses to resource availability and heterogeneity during restoration. Oecologia 139: 617-629. (Pubitemid 38752005)
5. Bardgett, R.D. & Wardle, D.A. 2003. Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84: 2258-2268.
6. Bever, J.D. 1994. Feedback between plants and their soil communities in an old field community. Ecology 75: 1965-1977.
7. Bever, J.D. 1999. Dynamics within mutualism and the maintenance of diversity: inference from a model of interguild frequency dependence. Ecology Letters 2: 52-61.
8. Bever, J.D. 2002. Negative feedback within a mutualism: host-specific growth of mycorrhizal fungi reduces plant benefit. Proceedings of the Royal Society of London B 269: 2595-2601.
9. Bever, J.D. 2003. Soil community feedback and the coexistence of competitors: conceptual frameworks and empirical tests. New Phytologist 157: 465-473.
10. Bever, J.D. & Schultz, P.A. 2003. Prairie mycorrhizal fungi inoculant may increase native plant diversity on restored sites (Illinois). Ecological Restoration 21: 311-312.
11. Bever, J.D., Westover, K.M. & Antonovics, A. 1997. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. Journal of Ecology 85: 561-573.
12. Blomqvist, M.M., Olff, H., Blaauw, B., Bongers, T. & van der Putten, W.H. 2000. Interactions between aboveand belowground biota: importance for small-scale vegetation mosaics in a grassland ecosystem. Oikos 90: 582-598. (Pubitemid 30778927)
13. Blumenthal, D.M., Jordan, N.R. & Russelle, M.P. 2003. Soil carbon addition controls weeds and facilitates prairie restoration. Ecological Applications 13: 605-615.
14. Bonanomi, G., Rietkerk, M., Dekker, S.C. & Mazzoleni, S. 2005. Negative plant-soil feedback and positive species interaction in a herbaceous plant community. Plant Ecology 181: 269-278. (Pubitemid 41712730)
15. Callaway, R.M., Thelen, G., Rodriquez, A. & Holben, W.E. 2004. Soil biota and exotic plant invasion. Nature 427: 731-733. (Pubitemid 38294590)
16. Casper, B.B. & Castelli, J.P. 2007. Evaluating plant-soil feedback together with competition in a serpentine grassland. Ecology Letters 10: 394-400.
17. Chapin, F.S. III 1980. The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 11: 233-260.
18. Collins, B. & Wein, G. 1998. Soil heterogeneity effects on canopy structure and composition during early succession. Plant Ecology 138: 217-230. (Pubitemid 28490433)
19. Cui, M. & Caldwell, M.M. 1996. Facilitation of plant phosphate acquisition by arbuscular mycorrhizas from enriched soil patches. I. Roots and hyphae exploiting the same soil volume. New Phytologist 133: 454-460. (Pubitemid 126568779)
20. Davies, K.F., Chesson, P., Harrison, S., Inouye, B.D., Melbourne, B.A. & Rice, K.J. 2005. Spatial heterogeneity explains the scale dependence of the nativeexotic diversity relationship. Ecology 86: 1602-1610. (Pubitemid 40793995)
21. Davis, M.A., Grime, J.P. & Thompson, K. 2000. Fluctuating resources in plant communities: a general theory of invisibility. Journal of Ecology 88: 528-534. (Pubitemid 30399963)
22. De Deyn, G.B., Raaijmakers, C.E. & Van der Putten, W.H. 2004. Plant community development is affected by nutrients and soil biota. Journal of Ecology 92: 824-834.
23. Farley, R.A. & Fitter, A.H. 1999. The responses of seven co-occurring woodland herbaceous perennials to localized nutrient-rich patches. Journal of Ecology 87: 849-859.
24. Gigon, A. & Leutert, A. 1996. The dynamic keyhole-key model of coexistence to explain diversity of plants in limestone and other grasslands. Journal of Vegetation Science 7: 29-40. (Pubitemid 27266786)
25. Gillespie, I.G. & Allen, E.B. 2006. Effects of soil and mycorrhizae from native and invaded vegetation on a rare California forb. Applied Soil Ecology 32: 6-12.
26. Goldberg, D.E. & Miller, T.E. 1990. Effects of different resource additions on species diversity in an annual plant community. Ecology 71:213-225.
27. Gough, L., Grace, J.B. & Taylor, K.L. 1994. The relationship between species richness and community biomass: the importance of environmental variables. Oikos 70: 271-279. (Pubitemid 2084853)
28. Gough, L., Osenberg, C.W., Gross, K.L. & Collins, S.L. 2000. Fertilization effects on species density and primary productivity in herbaceous plant communities. Oikos 89: 428-439. (Pubitemid 30343053)
29. Grace, J.B. 1999. The factors controlling species density in herbaceous plant communities: an assessment. In: Edwards, P.J. (ed.) Perspectives in plant ecology, evolution and systematics. pp. 1-28. Urban and Fischer Verlag, Jena, Germany.
30. Grace, J.B., Anderson, T.M., Smith, M.D., Seabloom, E., Andelman, S.J., Meche, G., Weiher, E., Allain, L.K., Jutila, H., Sankaran, M., Knops, J., Ritchie, M. & Willig, M.R. 2007. Does species diversity limit productivity in natural grassland communities? Ecology Letters 10: 680-689. (Pubitemid 46998296)
31. Grime, J.P. 1973. Control of species density in herbaceous vegetation. Journal of Environmental Management 1: 151-167.
32. Grime, J.P. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 111: 1169-1194.
33. Grime, J.P. 1979. Plant strategies and vegetation processes. John Wiley & Sons, London.
34. Gross, K.L., Willig, M.R., Gough, L., Inouye, R. & Cox, S.B. 2000. Patterns of species density and productivity at different spatial scales in herbaceous plant communities. Oikos 89:417-427. (Pubitemid 30343052)
35. Haubensak, K.A. & D'Antonio, C.M. 2006. Restoration of a coastal California grassland after invasion by the nitrogen-fixing shrubs, French broom (Genista monspessulana) and Scotch broom (Cytisus scoparius). Ecology Restoration 24: 94-100.
36. Hodge, A. 2001. Arbuscular mycorrhizal fungi influence decomposition of, but not plant nutrient capture from, glycine patches in soil. New Phytologist 151: 725-734. (Pubitemid 32812105)
37. Hodge, A. 2003. Plant nitrogen capture from organic matter as affected by spatial dispersion, interspecific competition and mycorrhizal colonization. New Phytologist 157: 303-314. (Pubitemid 36186155)
38. Hodge, A., Campbell, C.D. & Fitter, A.H. 2001. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413: 297-299. (Pubitemid 32905848)
39. Hodge, A., Robinson, D. & Fitter, A.H. 2000. An arbuscular mycorrhizal inoculum enhances root proliferation in, but not nitrogen capture from, nutrient-rich patches in soil. New Phytologist 145: 575-584. (Pubitemid 30165923)
40. Huenneke, L.F., Hamburg, S.P., Koide, R., Mooney, H.A. & Vitousek, P.M. 1990. Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71:478-491. (Pubitemid 20428097)
41. Huston, M. 1979. A general hypothesis of species diversity. American Naturalist 113: 81-101.
42. Hutchings, M.J., John, E.A. & Wijesinghe, D.K. 2003. Toward understanding the consequences of soil heterogeneity for plant populations and communities. Ecology 84: 2322-2334.
43. Hutchinson, G.E. 1959. Homage to Santa Rosalia, or why are there so many kinds of animals? American Naturalist 93: 145-159.
44. Jayachandran, K., Schwab, A.P. & Hetrick, B.A.D. 1992. Mineralization of organic phosphorus by vesiculararbuscular mycorrhizal fungi. Soil Biology and Biochemistry 24: 897-903. (Pubitemid 23403551)
45. Johnson, N.C., Graham, J.H. & Smith, F.A. 1997. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytologist 135: 575-585. (Pubitemid 27335974)
46. Kardol, P., Bezemer, T.M. & van der Putten, W.H. 2006. Temporal variation in plant-soil feedback controls succession. Ecology Letters 9: 1080-1088. (Pubitemid 44267791)
47. Kardol, P., Cornips, N.J., van Kempen, M.M.L., BakxSchotman, J.M.T. & van der Putten, W.H. 2007. Microbe-mediated plant-soil feedback causes historical contingency effects in plant community assembly. Ecological Monographs 77: 147-162. (Pubitemid 351342495)
48. Kielland, K. 1994. Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75: 2373-2383.
49. Klironomos, J.N. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417: 67-70.
50. Klironomos, J.N. 2003. Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84: 2292-2301. (Pubitemid 37435649)
51. Kulmatiski, A., Beard, K.H. & Stark, J.M. 2006. Soil history as a primary control on plant invasion in abandoned agricultural fields. Journal of Applied Ecology 43: 868-876. (Pubitemid 44268089)
52. Lundholm, J.T. & Larson, D.W. 2003. Relationships between spatial environmental heterogeneity and plant species diversity on limestone pavement. Ecography 26: 715-722.
53. McKane, R.B., Johnson, L.C., Shaver, G.R., Nadelhoffer, K.J., Rastetter, E.B., Fry, B., Giblin, A.E., Kielland, K., Kwiatkowski, B.L., Laundre, J.A. & Murray, G. 2002. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415: 68-71. (Pubitemid 34062449)
54. Miller, A.E. & Bowman, W.D. 2002. Variation in nitrogen-15 natural abundance and nitrogen uptake traits among co-occurring alpine species: do species partition by nitrogen form? Oecologia 130: 609-616.
55. Mills, K.E. & Bever, J.D. 1998. Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79: 1595-1601.
56. Mitchell, C.E., Agrawal, A.A., Bever, J.D., Gilbert, G.S., Hufbauer, R.A., Klironomos, J.N., Maron, J.L., Morris, W.F., Parker, I.M., Power, A.G., Seabloom, E.W., Torchin, M.E. & Vázquez, D.P. 2006. Biotic interactions and plant invasions. Ecology Letters 9: 726-740.
57. Mittelbach, G.G., Steiner, C.F., Scheiner, S.M., Gross, K.L., Reynolds, H.L., Waide, R.B., Willig, M.R., Dodson, S.I. & Gough, L. 2001. What is the observed relationship between species richness and productivity? Ecology 82: 2381-2396. (Pubitemid 32908136)
58. Näsholm, T., Huss-Danell, K. & Högberg, P. 2000. Uptake of organic nitrogen in the field by four agriculturally important plant species. Ecology 81: 1155-1161. (Pubitemid 30442016)
59. Newman, E.I. 1973. Competition and diversity in herbaceous vegetation. Nature 244: 310.
60. Oksanen, J. 1996. Is the humped relationship between species richness and biomass an artifact due to plot size? Journal of Ecology 84: 293-295. (Pubitemid 126539415)
61. Olff, H., Hoorens, B., de Goede, R.G.M., van der Putten, W.H. & Gleichman, J.M. 2000. Small-scale shifting mosaics of two dominant grassland species: the possible role of soil-borne pathogens. Oecologica 125:45-54. (Pubitemid 30787282)
62. Paschke, M.W., McLendon, T. & Redente, E.F. 2000. Nitrogen availability and old-field succession in a shortgrass steppe. Ecosystems 3: 144-158. (Pubitemid 30322911)
63. Prober, S.M., Thiele, K., Lunt, I.D. & Koen, T.B. 2005. Restoring ecological function in temperate grassy woodlands: manipulating soil nutrients, exotic annuals and native perennial grasses through carbon supplements and spring burns. Journal of Applied Ecology 42: 1073-1085. (Pubitemid 43140706)
64. Rajaniemi, T.K. 2003. Explaining productivity-diversity relationships in plants. Oikos 101: 449-457.
65. Rajaniemi, T.K. 2007. Root foraging traits and competitive ability in heterogeneous soils. Oecologia 153: 145-152.
66. Reever Morghan, K.J. & Seastedt, T.R. 1999. Effects of soil nitrogen reduction on nonnative plants in restored grasslands. Restoration Ecology 7: 51-55.
67. Reinhart, K.O. & Callaway, R.M. 2006. Soil biota and invasive plants. New Phytologist 170: 445-457.
68. Reynolds, H.L., Hartley, A.E., Vogelsang, K.M., Bever, J.D. & Schultz, P.A. 2005. Arbuscular mycorrhizal fungi do not enhance nitrogen acquisition and growth of old-field perennials under low nitrogen supply in glasshouse culture. New Phytologist 167: 869-880.
69. Reynolds, H.L., Hungate, B.A., D'Antonio, C.M. & Chapin, F.S. III 1997. Soil heterogeneity and plant competition in an annual grassland. Ecology 78: 2076-2090. (Pubitemid 28351351)
70. Reynolds, H.L., Mittelbach, G.G., Darcy-Hall, T.L., Houseman, G.R. & Gross, K.L. 2007. No effect of varying soil resource heterogeneity on plant species richness in a low fertility grassland. Journal of Ecology 95: 723-733.
71. Reynolds, H.L., Packer, A., Bever, J.D. & Clay, K. 2003. Grassroots ecology: plant-microbe-soil interactions as drivers of plant community structure and dynamics. Ecology 84: 2281-2291. (Pubitemid 37435648)
72. Reynolds, H.L., Vogelsang, K.M., Hartley, A.E., Bever, J.D. & Schultz, P.A. 2006. Variable responses of oldfield perennials to arbuscular mycorrhizal fungi and phosphorus source. Oecologia 147: 348-358.
73. Richter, B.S. & Stutz, J.C. 2002. Mycorrhizal inoculation of Big Sacaton: implication for grassland restoration of abandoned agricultural fields. Restoration Ecology 10: 607-616.
74. Schultz, C.B. 2001. Restoring resources for an endangered butterfly. Journal of Applied Ecology 38: 1007-1019.
75. Schwinning, S. & Weiner, J. 1998. Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia 113: 447-455. (Pubitemid 28126738)
76. Smilaurová, M. & Smilauer, P. 2002. Morphological responses of plant roots to heterogeneity of soil resources. New Phytologist 154: 703-715. (Pubitemid 34548638)
77. Smith, M.R., Charvat, I. & Jacobson, R.L. 1998. Arbuscular mycorrhizae promote establishment of prairie species in a tallgrass prairie restoration. Canadian Journal of Botany 76: 1947-1954. (Pubitemid 29266809)
78. Steinauer, E.M. & Collins, S.L. 1995. Effects of urine deposition on small-scale patch structure in prairie vegetation. Ecology 76: 1195-1205.
79. Stevens, M.H.H. & Carson, W.P. 1999. The significance of assemblage-level thinning for species richness. Journal of Ecology 87:490-502.
80. Suding, K.N., Collins, S.L., Gough, L., Clark, C., Cleland, E.E., Gross, K.L., Milchunas, D.G. & Pennings, S. 2005. Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proceedings of the National Academy of Sciences 102: 4387-4392. (Pubitemid 40397121)
81. Tarafdar, J.C. & Marschner, H. 1994. Phosphatase activity in the rhizosphere and hyphosphere of VA mycorrhizal wheat supplied with inorganic and organic phosphorus. Soil Biology and Biochemistry 26: 387-395. (Pubitemid 2057738)
82. Taylor, D.R., Aarssen, L.W. & Loehle, C. 1990. On the relationship between r/K selection and environmental carrying capacity: a new habitat template for plant life history strategies. Oikos 58: 239-250. (Pubitemid 20429816)
83. Tilman, D. 1982. Resource competition and community structure. Princeton University Press, Princeton, NJ.
84. Tilman, D. 1987. Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecological Monographs 57: 189-214. (Pubitemid 18289712)
85. Tilman, D. 1988. Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton, NJ.
86. Tilman, D. 1990. Constraints and tradeoffs: toward a predictive theory of competition and succession. Oikos 58: 3-15. (Pubitemid 20429054)
87. Tilman, D. 1993. Species richness of experimental productivity gradients: how important is colonization limitation? Ecology 74: 2179-2191. (Pubitemid 2013841)
88. Tilman, D. & Pacala, S. 1993. The maintenance of species richness in plant communities. In: Ricklefs, R. & Schluter, D. (eds.) Species diversity in ecological communities: historical and geographical perspectives. pp. 13-25. University of Chicago Press, Chicago, IL, USA.
89. Turnbull, M.H., Goodall, R. & Stewart, G.R. 1995. The impact of mycorrhizal colonization upon nitrogen source utilization and metabolism in seedlings of Eucalyptus grandis Hill ex Maiden and Eucalyptus maculata Hook. Plant Cell Environ. 18: 1386-1394. (Pubitemid 3009581)
90. Van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boiler, T., Wiemken, A. & Sanders, I.R. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69-72. (Pubitemid 28520449)
91. Van der Putten, W.H., Klironomos, J.N. & Wardle, D.A. 2007. Microbial ecology of biological invasions. ISME J.1:28-37.
92. Van der Putten, W.H., Maas, P.H.T., Van Gulik, W.J.M. & Brinkman, H. 1990. Characterization of soil organisms involved in the degeneration of Ammophila arenaria. Soil Biol. Biochem. 22: 845-852.
93. Van der Putten, W.H. & Peters, B.A.M. 1997. How soilborne pathogens may affect plant competition. Ecology 78: 1785-1795. (Pubitemid 27490898)
94. Van der Putten, W.H. & Troelstra, S.R. 1990. Harmful soil organisms in coastal foredunes involved in degeneration of Ammophila arenaria and Calammophila baltica. Canadian Journal of Botany 68: 1560-1568.
95. Van der Putten, W.H., Van Dijk, C. & Peters, B.A.M. 1993. Plant-specific soil-borne diseases contribute to succession in foredune vegetation. Nature 362: 53-56. (Pubitemid 23087287)
96. Vogelsang, K.M., Reynolds, H.L. & Bever, J.D. 2006. Mycorrhizal fungal identity and richness determine the species diversity and productivity of a tallgrass prairie system. New Phytologist 172: 554-562.
97. Wedin, D.A. & Tilman, D. 1996. Influence of nitrogen loading and species composition on the carbon balance of grasslands. Science 274: 1720-1723. (Pubitemid 26414906)
98. Whittaker, R.H. & Levin, S.A. 1977. The role of mosaic phenomena in natural communities. Theoretical Population Biology 12: 117-139.