Spore dispersal of basidiomycete fungi at the landscape scale is driven by stochastic and deterministic processes and generates variability in plant-fungal interactions

New Phytologist

Volumn 204, Issue 1, 2014, Pages 180-191

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

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Landscape ecology; Macroecology; Metacommunity; Microbial biogeography; Mycorrhizal fungi; Pinus muricata; Spatial ecology; Storage effect

Indexed keywords

COMMUNITY COMPOSITION; CONIFEROUS TREE; DISPERSAL; ECTOMYCORRHIZA; FUNGUS; LANDSCAPE ECOLOGY; MACROECOLOGY; SPATIOTEMPORAL ANALYSIS; SPORE; STOCHASTICITY;

BACTERIA (MICROORGANISMS); BASIDIOMYCOTA; FUNGI; PINUS MURICATA;

BASIDIOMYCETES; BIODIVERSITY; CALIFORNIA; ECOSYSTEM; FUNGUS; FUNGUS SPORE; GENETICS; MARKOV CHAIN; MICROBIOLOGY; MOLECULAR GENETICS; MYCORRHIZA; PHYSIOLOGY; PINE; SEASON; SEEDLING;

BASIDIOMYCOTA; BIODIVERSITY; CALIFORNIA; ECOSYSTEM; FUNGI; MOLECULAR SEQUENCE DATA; MYCORRHIZAE; PINUS; SEASONS; SEEDLINGS; SPORES, FUNGAL; STOCHASTIC PROCESSES;

EID: 84906942808     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12906     Document Type: Article

References (89)

1. Aerts R. 1997. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79: 439-449.
2. Agrawal AA, Ackerly DD, Adler F, Arnold AE, Caceres C, Doak DF, Post E, Hudson PJ, Maron J, Mooney KA et al. 2007. Filling key gaps in population and community ecology. Frontiers in Ecology and the Environment 5: 145-152.
3. Amend A, Samson R, Seifert K, Bruns T. 2010a. Indoor fungal composition is geographically patterned and more diverse in temperate zones than in the tropics. Proceedings of the National Academy of Sciences, USA 107: 13748-13753.
4. Amend A, Seifert K, Bruns T. 2010b. Quantifying microbial communitieswith 454 pyrosequencing: does read abundance count? Molecular Ecology 19: 5555-5565.
5. Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32-46.
6. Baldrian P, Kolarik M, Stursova M, Kopecky J, Valaskova V, Vetrovsky T, Zifcakova L, Snajdr J, Ridl J, Vlcek C et al. 2012. Active and total microbial communities in forest soil are largely different and highly stratified during decomposition. ISME Journal 6: 248-258.
7. Bates D, Maechler M, Bolker B, Walker S. 2014. lme4: Linear mixed-effects models using Eigen and S4. R package version 1.0-6: [WWW document] URL http://CRAN.R-project.org/package=lme4 [accessed February 2014].
8. Baxter JW, Dighton J. 2001. Ectomycorrhizal diversity alters growth and nutrient acquisition of grey birch (Betula populifolia) seedlings in host-symbiont culture conditions. New Phytologist 152: 139-149.
9. Bell T. 2010. Experimental tests of the bacterial distance-decay relationship. ISME Journal 4: 1357-1365.
10. Bogar LM, Kennedy PG. 2012. New wrinkles in an old paradigm: neighborhood effects can modify the structure and specificity of Alnus-associated ectomycorrhizal fungal communities. FEMS Microbiology Ecology 83: 767-777.
11. Bowers RM, Lauber CL, Wiedinmyer C, Hamady M, Hallar AG, Fall R, Knight R, Fierer N. 2009. Characterization of airborne microbial communities at a high-elevation site and their potential to act as atmospheric ice nuclei. Applied and Environmental Microbiology 75: 5121-5130.
12. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335-336.
13. Chase JM. 2010. Stochastic community assembly causes higher biodiversity in more productive environments. Science 328: 1388-1391.
14. Chesson P. 2000. Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31: 343-366.
15. Connell JH. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: Den Boer PJ, Gradwell GR, eds. Dynamics of populations. Wageningen, the Netherlands: PUDOC, 298-312.
16. Corner EJH. 1935. The seasonal fruiting of agarics in Malaya. Gardens' Bulletin, Straits Settlements 9: 79-88.
17. Courty PE, Buee M, Diedhiou AG, Frey-Klett P, Le Tacon F, Rineau F, Turpault MP, Uroz S, Garbaye J. 2010. The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biology & Biochemistry 42: 679-698.
18. DeSantis TZ, Stone CE, Murray SR, Moberg JP, Andersen GL. 2005. Rapid quantification and taxonomic classification of environmental DNA from both prokaryotic and eukaryotic origins using a microarray. FEMS Microbiology Letters 245: 271-278.
19. Dickie IA, Fukami T, Wilkie JP, Allen RB, Buchanan PK. 2012. Do assembly history effects attenuate from species to ecosystem properties? A field test with wood inhabiting fungi. Ecology Letters 15: 133-141.
20. Dickie IA, Xu B, Koide RT. 2002. Vertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis. New Phytologist 156: 527-535.
21. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
22. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
23. Egli S, Peter M, Buser C, Stahel W, Ayer F. 2006. Mushroom picking does not impair future harvests - results of a long-term study in Switzerland. Biological Conservation 129: 271-276.
24. Fierer N, McCain CM, Meir P, Zimmerman M, Rapp JM, Silman MR, Knight R. 2011. Microbes do not follow the elevational diversity patterns of plants and animals. Ecology 92: 797-804.
25. Fine PVA, Mesones I, Coley PD. 2004. Herbivores promote habitat specialization by trees in amazonian forests. Science 305: 663-665.
26. Forrestel AB, Moritz MA, Stephens SL. 2011. Landscape-scale vegetation change following fire in Point Reyes, California, USA. Fire Ecology 7: 114-128.
27. Fukami T. 2010. Community assembly dynamics in space. In: Verhoef HA, Morin PJ, eds. Community ecology: processes, models and applications. Oxford, UK: Oxford University Press, 45-54.
28. Fukami T, Beaumont HJE, Zhang XX, Rainey PB. 2007. Immigration history controls diversification in experimental adaptive radiation. Nature 446: 436-439.
29. Fukami T, Dickie IA, Wilkie JP, Paulus BC, Duckchul P, Roberts A, Buchanan PK, Allen RB. 2010. Assembly history dictates ecosystem functioning: evidence from wood decomposer communities. Ecology Letters 13: 675-684.
30. Galante TE, Horton TR, Swaney DP. 2011. 95% of basidiospores fall within one meter of the cap- a field and modeling based study. Mycologia 103: 1175-1183.
31. Gange AC, Gange EG, Sparks TH, Boddy L. 2007. Rapid and recent changes in fungal fruiting patterns. Science 316: 71.
32. Gao C, Shi N-N, Liu Y-X, Peay KG, Zheng Y, Ding Q, Mi X-C, Ma K-P, Wubet T, Buscot F et al. 2013. Host plant genus-level diversity is the best predictor of ectomycorrhizal fungal diversity in a Chinese subtropical forest. Molecular Ecology 22: 3403-3414.
33. 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.
34. Gaston KJ. 2000. Global patterns in biodiversity. Nature 405: 220-227.
35. Gilbert GS. 2002. Evolutionary ecology of plant diseases in natural ecosystems. Annual Review of Phytopathology 40: 13-43.
36. Gilbert GS, Hubbell SP, Foster RB. 1994. Density and distance-to-adult effects of a canker disease of trees in a moist tropical forest. Oecologia 98: 100-108.
37. Green J, Bohannan BJM. 2006. Spatial scaling of microbial biodiversity. Trends In Ecology & Evolution 21: 501-507.
38. Hanson CA, Fuhrman JA, Horner-Devine MC, Martiny JB. 2012. Beyond biogeographic patterns: processes shaping the microbial landscape. Nature reviews. Microbiology 10: 497-506.
39. Howe HF, Smallwood J. 1982. Ecology of seed dispersal. Annual Review Of Ecology Evolution And Systematics 13: 201-228.
40. Hubbell SP. 2001. The unified neutral theory of biodiversity and biogeography. Princeton, NJ, USA: Princeton University Press.
41. Hutchinson GE. 1959. Homage to Santa-Rosalia or why are there so many kinds of animals. American Naturalist 93: 145-159.
42. Hutchinson GE. 1961. The paradox of the plankton. The American Naturalist 95: 137-145.
43. Ishida TA, 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.
44. Janzen DH. 1970. Herbivores and the number of tree species in tropical forests. American Naturalist 104: 501-528.
45. Kauserud H, Heegaard E, Halvorsen R, Boddy L, Hoiland K, Stenseth NC. 2010a. Mushroom's spore size and time of fruiting are strongly related: is moisture important? Biology Letters 7: 273-276.
46. Kauserud H, Heegaard E, Semenov MA, Boddy L, Halvorsen R, Stige LC, Sparks TH, Gange AC, Stenseth NC. 2010b. Climate change and spring-fruiting fungi. Proceedings of the Royal Society B-Biological Sciences 277: 1169-1177.
47. Kauserud H, Stige LC, Vik JO, Okland RH, Hoiland K, Stenseth NC. 2008. Mushroom fruiting and climate change. Proceedings of the National Academy of Sciences, USA 105: 3811-3814.
48. Kennedy P, Hortal S, Bergemann S, Bruns T. 2007. Competitive interactions among three ectomycorrhizal fungi and their relation to host plant performance. Journal of Ecology 95: 1338-1345.
49. Kennedy PG, Higgins LM, Rogers RH, Weber MG. 2011. Colonization-competition tradeoffs as a mechanism driving successional dynamics in ectomycorrhizal fungal communities. PLoS ONE 6: e25126.
50. Kennedy PG, Peay KG, Bruns TD. 2009. Root tip competition among ectomycorrhizal fungi: are priority effects a rule or an exception? Ecology 90: 2098-2107.
51. Knight R, Reeder J. 2010. Denoising pyrosequencing reads by flowgram clustering. Nature Methods 7: 668-669.
52. Kuznetsova A, Brockhoff PB, Christensen RHB. 2014. lmerTest: Tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). R package version 2.0-6.: [WWW document] URL http://Cran.r-project.org/package=lmerTest [accessed 23 June 2014].
53. Last FT, Dighton J, Mason PA. 1987. Successsions of sheathing mycorrhizal fungi. Trends in Ecology and Evolution 2: 157-161.
54. Legendre P, Gallagher E. 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271-280.
55. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D et al. 2004. The metacommunity concept: a framework for multi-scale community ecology. Ecology Letters 7: 601-613.
56. Levine JM, Murrell DJ. 2003. The community-level consequences of seed dispersal patterns. Annual Review Of Ecology Evolution And Systematics 34: 549-574.
57. Lomolino MV, Riddle BR, Brown JH. 2006. Biogeography. Sunderland, MA, USA: Sinauer.
58. Mangan SA, Schnitzer SA, Herre EA, Mack KML, Valencia MC, Sanchez EI, Bever JD. 2010. Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466: 752-755.
59. McMurdie PJ, Holmes S. 2013. Waste not, want not: why rarefying microbiome data is inadmissible. arXiv 1310.0424.
60. Moles AT, Ackerly DD, Webb CO, Tweddle JC, Dickie JB, Westoby M. 2005. A brief history of seed size. Science 307: 576-580.
61. Nara K, Nakaya H, Hogetsu T. 2003. Ectomycorrhizal sporocarp succession and production during early primary succession on Mount Fuji. New Phytologist 158: 193-206.
62. Nathan R, Muller-Landau HC. 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology & Evolution 15: 278-285.
63. Norros V, Penttilä R, Suominen M, Ovaskainen O. 2012. Dispersal may limit the occurrence of specialist wood decay fungi already at small spatial scales. Oikos 121: 961-974.
64. Oksanen J, Kindt R, Legendre P, O'Hara B, Simpson GL, Solymos P, Henry M, Stevens H, Wagner H. 2008. vegan: Community Ecology Package. R package version 1.15-1. [WWW document] http://cran.r-project.org/, http://vegan.r-forge.r-project.org/ [accessed 23 June 2014].
65. Packer A, Clay K. 2000. Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404: 278-281.
66. Peay KG, Bidartondo MI, Arnold AE. 2010b. Not every fungus is everywhere: scaling to the biogeography of fungal-plant interactions across roots, shoots and ecosystems. New Phytologist 185: 878-882.
67. Peay KG, Bruns TD, Kennedy PG, Bergemann SE, Garbelotto M. 2007. A strong species-area relationship for eukaryotic soil microbes: island size matters for ectomycorrhizal fungi. Ecology Letters 10: 470-480.
68. Peay KG, Dickie IA, Wardle DA, Bellingham PJ, Fukami T. 2012a. Rat invasion of islands alters fungal community structure, but not wood decomposition rates. Oikos 122: 258-264.
69. Peay KG, Garbelotto M, Bruns TD. 2010a. Evidence of dispersal limitation in soil microorganisms: isolation reduces species richness on mycorrhizal tree islands. Ecology 91: 3631-3640.
70. Peay KG, Kennedy PG, Bruns TD. 2008. Fungal community ecology: a hybrid beast with a molecular master. BioScience 58: 799-810.
71. Peay KG, Schubert MG, Nguyen N, Bruns TD. 2012b. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Molecular Ecology 16: 4122-4136.
72. Pinheiro J, Bates D, Sarkar D, R Development Core Team. 2013. nlme: linear and nonlinear mixed effects models. R package version 3.1-111. URL http://cran.r-project.org/web/packages/nlme/nlme.pdf [accessed 23 June 2014].
73. Robertson LD, Brandys R. 2011. A multi-laboratory comparative study of spore trap analyses. Mycologia 103: 226-231.
74. Sato H, Morimoto S, Hattori T. 2012. A thirty-year survey reveals that ecosystem function of fungi predicts phenology of mushroom fruiting. PLoS ONE 7: e49777.
75. Silver WL, Miya RK. 2001. Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129: 407-419.
76. Smith DP, Peay KG. 2014. Sequence depth, not PCR replication, improves ecological inference from Next Generation DNA Sequencing. PLoS ONE 92: e90234.
77. Straatsma G, Ayer F, Egli S. 2001. Species richness, abundance, and phenology of fungal fruit bodies over 21 years in a Swiss forest plot. Mycological Research 105: 515-523.
78. Talbot JM, Bruns TD, Taylor JW, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Liao HL, Smith ME et al. 2014. Endemism and functional convergence across the North American soil mycobiome. Proceedings of the National Academy of Sciences, USA. doi:10.1073/pnas.1402584111.
79. Taylor DL, Herriott IC, Stone KE, McFarland JW, Booth MG, Leigh MB. 2010. Structure and resilience of fungal communities in Alaskan boreal forest soils. Canadian Journal of Forest Research 40: 1288-1301.
80. Tedersoo L, May TW, Smith ME. 2010a. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20: 217-263.
81. Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, Bahram M, Bechem E, Chuyong G, Koljalg U. 2010b. 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytologist 188: 291-301.
82. Terborgh J. 2012. Enemies maintain hyperdiverse tropical forests. American Naturalist 179: 303-314.
83. Terwilliger J, Pastor J. 1999. Small mammals, ectomycorrhizae, and conifer succession in beaver meadows. Oikos 85: 83-94.
84. Thompson JN. 1988. Variation in interspecific interactions. Annual Review of Ecology and Systematics 19: 65-87.
85. Tilman D. 1994. Competition and biodiversity in spatially structured habitats. Ecology 75: 2-16.
86. Visser S. 1995. Ectomycorrhizal fungal succession in Jack Pine stands following wildfire. New Phytologist 129: 389-401.
87. Weber A, Karst J, Gilbert B, Kimmins JP. 2005. Thuja plicata exclusion in ectomycorrhiza-dominated forests: testing the role of inoculum potential of arbuscular mycorrhizal fungi. Oecologia 143: 148-156.
88. Whittaker RH. 1956. Vegetation of the Great Smoky Mountains. Ecological Monographs 26: 1-80.
89. Wiens JA. 1976. Population responses to patchy environments. Annual Review of Ecology and Systematics 7: 81-120.