Spore heat resistance plays an important role in disturbance-mediated assemblage shift of ectomycorrhizal fungi colonizing Pinus muricata seedlings

Journal of Ecology

Volumn 97, Issue 3, 2009, Pages 537-547

  Peay, Kabir G ^a   Garbelotto, Matteo ^a   Bruns, Thomas D ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Competition; Fugitive species; Functional traits; Intermediate disturbance hypothesis; Microbe; Mutualism; Mycorrhiza; Pinus muricata; Point Reyes; Succession

Indexed keywords

CONIFEROUS TREE; ECTOMYCORRHIZA; ENVIRONMENTAL DISTURBANCE; FUNGUS; HEATING; MUTUALISM; ROOT COLONIZATION; SEEDLING; SPECIES RICHNESS; SPORE; SUCCESSION; TEMPERATURE EFFECT;

BACTERIA (MICROORGANISMS); FUNGI; PINUS MURICATA;

EID: 64349093502     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/j.1365-2745.2009.01489.x     Document Type: Article

References (75)

1. Anderson, M.J. (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32 46.
2. Baar, J., Horton, T.R., Kretzer, A. Bruns, T.D. (1999) Mycorrhizal recolonization of Pinus muricata from resistant propagules after a stand-replacing wildfire. New Phytologist, 143, 409 418.
3. Bruns, T.D. (1995) Thoughts on the processes that maintain local species-diversity of ectomycorrhizal fungi. Plant and Soil, 170, 63 73.
4. Bruns, T.D., Peay, K.G., Boynton, P.J., Grubisha, L.C., Hynson, N.A., Nguyen, N.H. Rosenstock, N.P. (2009) Inoculum potential of Rhizopogon spores increases with time over the first four years of a 99-year spore burial experiment. New Phytologist, 181, 463 470.
5. Caswell, H. Cohen, J.E. (1991) Disturbance, Interspecific Interaction and Diversity in Metapopulations. Biological Journal of the Linnean Society, 42, 193 218.
6. Certini, G. (2005) Effects of fire on properties of forest soils: A review. Oecologia, 143, 1 10.
7. Connell, J.H. (1978) Diversity in tropical rain forests and coral reefs - high diversity of trees and corals is maintained only in a non-equilibrium state. Science, 199, 1302 1310.
8. Connell, J.H. Slatyer, R.O. (1977) Mechanisms of succession in natural communities and their role in community stability and organization. American Naturalist, 111, 1119 1144.
9. Conover, W.J., Johnson, M.E. Johnson, M.M. (1981) A comparative study of tests for homogeneity of variances, with applications to the outer continental shelf bidding data. Technometrics, 23, 351 361.
10. Erland, S. Söderström, B. (1991) Effects of lime and ash treatments on ectomycorrhizal infection of Pinus sylvestris L. seedlings planted in a pine forest. Scandinavian Journal of Forest Research, 14, 209 217.
11. Erland, S. Taylor, A.F.S. (2002) Diversity of ecto-mycorrhizal fungal communities in relation to the abiotic environment. Mycorrhizal Ecology (eds M.G.A. van der Heijden I.R. Sanders), pp. 163 200. Springer, Berlin.
12. Gardes, M. Bruns, T. (1993) ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology, 2, 113 118.
13. Garnica, S., Weiss, M., Oertel, B. Oberwinkler, F. (2005) A framework for phylogenetic classification in the genus Cortinarius (Basidiomycota, Agaricales) derived from morphological and molecular data. Canadian Journal of Botany, 83, 1457 1477.
14. Grogan, P., Baar, J. Bruns, T.D. (2000a) Below-ground ectomycorrhizal community structure in a recently burned bishop pine forest. Journal of Ecology, 88, 1051 1062.
15. Grogan, P., Bruns, T.D. Chapin, F.S. (2000b) Fire effects on ecosystem nitrogen cycling in a Californian bishop pine forest. Oecologia, 122, 537 544.
16. Grubb, P.J. (1977) Maintenance of species-richness in plant communities - importance of regeneration niche. Biological Reviews of the Cambridge Philosophical Society, 52, 107 145.
17. Hart, S.C., DeLuca, T.H., Newman, G.S., MacKenzie, M.D. Boyle, S.I. (2005) Post-fire vegetative dynamics as drivers of microbial community structure and function in forest soils. Forest Ecology and Management, 220, 166 184.
18. Hickey, P.C., Swift, S.R., Roca, M.G. Read, N.D. (2004) Live-cell imaging of filamentous fungi using vital fluorsescent dyes and confocal microscopy. Methods in Microbiology, 34, 63 87.
19. Hobbie, E.A. (2006) Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies. Ecology, 87, 563 569.
20. Hobbie, J.E. Hobbie, E.A. (2006) 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra. Ecology, 87, 823 828.
21. Horton, T.R., Cázares, E. Bruns, T.D. (1998) Ectomycorrhizal, vesicular-arbuscular and dark septat fungal colonization of bishop pine (Pinus muricata) seedlings in the first 5 months of growth after wildfire. Mycorrhiza, 8, 11 18.
22. Hutchinson, G.E. (1951) Copepodology for the Onithologist. Ecology, 32, 571 577.
23. Ishida, T.A., Nara, K. Hogetsu, T. (2007) Host effects on ectomycorrhizal fungal communities: Insight from eight host species in mixed conifer-broadleaf forests. New Phytologist, 174, 430 440.
24. Ishida, T.A., Nara, K., Tanaka, M., Akihiko, K. Hogetsu, T. (2008) Germination and infectivity of ectomycorrhizal fungal spores in relation to their ecological traits during primary succession. New Phytologist, 180, 491 500.
25. Izzo, A., Canright, M. Bruns, T.D. (2006) The effects of heat treatments on ectomycorrhizal resistant propagules and their ability to colonize bioassay seedlings. Mycological Research, 110, 196 202.
26. Kennedy, P.G. Peay, K.G. (2007) Different soil moisture conditions change the outcome of the ectomycorrhizal symbiosis between Rhizopogon species and Pinus muricata. Plant and Soil, 291, 155 165.
27. Kennedy, P.G. Sousa, W.P. (2006) Forest encroachment into a Californian grassland: examining the simultaneous effects of facilitation and competition on tree seedling recruitment. Oecologia, 148, 464 474.
28. Kennedy, P.G., Bergemann, S.E., Hortal, S. Bruns, T.D. (2007a) Determining the outcome of field-based competition between two Rhizopogon species using real-time PCR. Molecular Ecology, 16 (4 881 890.
29. Kennedy, P.G., Hortal, S., Bergemann, S.E. Bruns, T.D. (2007b) Competitive interactions among three ectomycorrhizal fungi and their relation to host plant performance. Journal of Ecology, 95, 1338 1345.
30. Koide, R.T., Xu, B., Sharda, J., Lekberg, Y. Ostiguy, N. (2005) Evidence of species interactions within an ectomycorrhizal fungal community. New Phytologist, 165, 305 316.
31. Larena, I., Salazar, O., Gonzalez, V., Julian, M.C. Rubio, V. (1999) Design of a primer for ribosomal DNA internal transcribed spacer with enhanced specificity for ascomycetes. Journal of Biotechnology, 2 3, 187 194.
32. Last, F.T., Dighton, J. Mason, P.A. (1987) Successsions of sheathing mycorrhizal fungi. Trends in Ecology and Evolution, 2, 157 161.
33. Lilleskov, E.A. Bruns, T.D. (2003) Root colonization dynamics of two ectomycorrhizal fungi of contrasting life history strategies are mediated by addition of organic nutrient patches. New Phytologist, 159, 141 151.
34. Lilleskov, E.A., Fahey, T.J., Horton, T.R. Lovett, G.M. (2002) Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology, 83, 104 115.
35. Mahmood, S. (2003) Colonisation of spruce roots by two interacting ectomycorrhizal fungi in wood ash amended substrates. FEMS Microbiology Letters, 221, 81 87.
36. Mahmood, S., Finlay, R.D., Erland, S. Wallander, H. (2001) Solubilisation and colonisation of wood ash by ectomycorrhizal fungi isolated from a wood ash fertilised spruce forest. FEMS Microbiology Ecology, 35, 151 161.
37. Mahmood, S., Finlay, R., Wallander, H. Erland, S. (2002) Ectomycorrhizal colonisation of roots and ash granules in a spruce forest treated with granulated wood ash. Forest Ecology and Management, 160, 65 74.
38. Mahmood, S., Finlay, R.D., Fransson, A.M. Wallander, H. (2003) Effects of hardened wood ash on microbial activity, plant growth and nutrient uptake by ectomycorrhizal spruce seedlings. FEMS Microbiology Ecology, 43, 121 131.
39. Mason, P.A., Last, F.T., Wilson, J., Deacon, J.W., Fleming, L.V. Fox, F.M. (1987) Fruiting and successions of ectomycorrhizal fungi. Fungal Infection in Plants (eds G.F. Pegg P.G. Ayres), pp. 253 268.
40. Miller, S.L., Torres, P. McClean, T.M. (1993) Basidiospore viability and germination in ectomycorrhizal and saprotrophic basidiomycetes. Mycological Research, 97, 141 149.
41. Neary, D.G., Klopatek, C.C., DeBano, L.F. Ffolliott, P.F. (1999) Fire effects on belowground sustainability: a review and synthesis. Forest Ecology and Management, 122, 51 71.
42. Oksanen, J. (2008) Multivariate analysis of ecological communities in R: Vegan tutor. Available at http://cc.oulu.fi/∼jarioksa/opetus/metodi/ vegantutor.pdf.
43. 2 and nitrogen fertilization. New Phytologist, 176, 164 174.
44. Peay, K.G., Bruns, T.D., Kennedy, P.G., Bergemann, S.E. Garbelotto, M. (2007) A strong species-area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecology Letters, 10, 470 480.
45. Pianka, E.R. (1970) R-Selection and K-Selection. American Naturalist, 104, 592 597.
46. Pickett, S.T.A. White, P.S. (1985) The Ecology of Natural Disturbance and Patch Dynamics. Academic Press, Orlando.
47. Pilz, D. Perry, D.A. (1984) Impact of clearcutting and slash burning on ectomycorrhizal associations of Douglas-fir seedlings. Canadian Journal of Forest Research, 14, 94 100.
48. Pyne, S.J., Andrews, P.L. Laven, R.D. (1996) Introduction to Wildland Fire. John Wiley & Sons, New York.
49. Quinn, G.P. Keough, M.J. (2006) Experimental Design and Data Analysis for Biologists. Cambridge University Press, New York.
50. R Core Development Team 2007) R: A Language and Environment For Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
51. Raup, D.M. Crick, R.E. (1979) Measurment of faunal similarity in paleontology. Journal of Paleontology, 53, 1213 1227.
52. Schoenberger, M.M. Perry, D.A. (1982) The effect of soil disturbance on growth and ectomycorrhizae of Douglas-fir and western hemlock seedlings: A greenhouse bioassay. Canadian Journal of Forest Research, 12, 343 353.
53. Skellam, J.G. (1951) Random dispersal in theoretical populations. Biometrika, 38, 196 218.
54. Smith, J.E., McKay, D., Niwa, C.G., Thies, W.G., Brenner, G. Spatafora, J.W. (2004) Short-term effects of seasonal prescribed burning on the ectomycorrhizal fungal community and fine root biomass in ponderosa pine stands in the Blue Mountains of Oregon. Canadian Journal of Forest Research, 34, 2477 2491.
55. Smith, S.E. Read, D.J. (1997) Mycorrhizal Symbiosis. Academic Press, New York.
56. Smith, M.L., Douhan, G.W. Rizzo, D.M. (2007) Intra-specific and intra-sporocarp ITS variation of ectomycorrhizal fungi as assessed by rDNA sequencing of sporocarps and pooled ectomycorrhizal roots from a Quercus woodland. Mycorrhiza, 18, 15 22.
57. Sousa, W.P. (1979) Experimental investigations of disturbance and ecological succession in a rocky inter-tidal algal community. Ecological Monographs, 49, 227 254.
58. Sousa, W.P. (1984) The role of disturbance in natural communities. Annual Review of Ecology and Systematics, 15, 353 391.
59. St. John, T.V. Rundel, P.W. (1976) The role of fire as a mineralizing agent in a Sierran coniferous forest. Oecologia, 25, 35 45.
60. Stendell, E.R., Horton, T.R. Bruns, T.D. (1999) Early effects of prescribed fire on the structure of the ectomycorrhizal fungus community in a Sierra Nevada ponderosa pine forest. Mycological Research, 103, 1353 1359.
61. Sugihara, N.G., van Wagtendonk, J.W., Shaffer, K.E., Fites-Kauffman, J. Thode, A.E. (2006) Fire in California's Ecosystems. University of California Press, Berkeley.
62. Terwilliger, J. Pastor, J. (1999) Small mammals, ectomycorrhizae, and conifer succession in beaver meadows. Oikos, 85, 83.
63. Tilman, D. (1994) Competition and biodiversity in spatially structured habitats. Ecology, 75, 2 16.
64. Tryon, E.H. (1948) Effect of charcoal on certain physical, chemical and biological properties of forest soils. Ecological Monographs, 18, 81 115.
65. Underwood, A.J. (1997) Experiments in Ecology. Cambridge University Press, New York.
66. Vellinga, E., de Kok, R.P.J. Bruns, T.D. (2003) Phylogeny and taxonomy of Macrolepiota (Agaricaceae). Mycologia, 95, 442 456.
67. Visser, S. (1995) Ectomycorrhizal fungal succession in jack pine stands following wildfire. New Phytologist, 129, 389 401.
68. Walker, L.R. Chapin, F.S. (1987) Interactions among Processes Controlling Successional Change. Oikos, 50, 131 135.
69. Wallander, H., Mahmood, S., Hagerberg, D., Johannesson, H. Pallon, J. (2003) Elemental composition of ectomycorrhizal mycelia identified by PCR-RFLP analysis and grown in contact with apatite or wood ash in forest soil. FEMS Microbiology Ecology, 44, 57 65.
70. Wardle, D.A., Zackrisson, O. Nilsson, M.-C. (1998) The charcoal effect in Boreal forests: Mechanisms and ecological consequences. Oecologia, 115, 419 426.
71. Weber, A., Karst, J., Gilbert, B. Kimmins, J.P. (2005) Thuja plicata exclusion in ectomycorrhiza-dominated forests: testing the role of inoculum potential of arbuscular mycorrhizal fungi. Oecologia, 143, 148 156.
72. White, T.J., Bruns, T.D., Lee, S. Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Method and Applications (eds M. Innis, D.H. Gefland, J.J. Sninsky T.J. White), pp. 315 322. Academic Press, San Diego.
73. Wiens, J.A. (1976) Population responses to patchy environments. Annual Review of Ecology and Systematics, 7, 81 120.
74. Wu, B., Nara, K. Hogetsu, T. (1999) Competition between ectomycorrhizal fungi colonizing Pinus densiflora. Mycorrhiza, 9, 151 159.
75. Zackrissson, O., Nilsson, M.-C., Wardle, D. (1996) Key ecological function of charcoal from wildfire in the Boreal forest. Oikos, 77, 10 19.