Abstract
Environmental disturbances define the diversity and assemblage of species, affecting the functioning of ecosystems. Fire is a major disturbance of Mediterranean pine forests. Pines are highly dependent on the ectomycorrhizal (EM) fungal symbiosis, which is critical for tree recruitment under primary succession. To determine the effects of time since fire on the structure and recovery of EM fungal communities, we surveyed the young Pinus pinaster regenerate in three sites differing in the elapsed time after the last fire event. Pine roots were collected, and EM fungi characterized by sequencing the internal transcribed spacer (ITS) and the large subunit (LSU) regions of the nuclear ribosomal (nr)-DNA. The effects of the elapsed time after fire on the EM community structure (richness, presence/absence of fungi, phylogenetic diversity) and on soil properties were analysed.
Fungal richness decreased with the elapsed time since the fire; although, the phylogenetic diversity of the EM community increased. Soil properties were different depending on the elapsed time after fire and particularly, the organic matter, carbon-to-nitrogen (C/N) ratio, nitrogen and iron significantly correlated with the assemblage of fungal species. Ascomycetes, particularly Tuberaceae and Pezizales, were significantly over-represented on saplings in the burned site. On seedlings, a significant over-representation of Rhizopogonaceae and Atheliaceae was observed in the most recently burned site, while other fungi (i.e. Cortinariaceae) were significantly under-represented. Our results are consistent with the hypothesis that fire can act as a selective agent by printing a phylogenetic signal on the EM fungal communities associated with naturally regenerated pines, pointing out to some groups as potential fire-adapted fungi.
Similar content being viewed by others
References
Agerer R (1987–1998) Colour atlas of ectomycorrhizae. Einhirn-Verlag Eduard Dietenberger, Munich
Agerer R (2001) Exploration types of ectomycorrhizae. A proposal to classify extomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114
Anderson TM, Lachance M-A, Starmer WT (2004) The relationship of phylogeny to community structure: the cactus yeast community. Am Nat 164:709–721
Avis PG, McLaughlin DJ, Dentinger BC, Reich PB (2003) Long-term increase in nitrogen supply alters above and below-ground ectomycorrhizal communities and increases the dominance of Russula spp. in a temperate oak savannah. New Phytol 160:239–253
Baar J, Horton TR, Kretzer AM, Bruns TD (1999) Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand-replacing wildfire. New Phytol 143:409–418
Bastias BA, Xu Z, Cairney JWG (2006) Influence of long-term repeated prescribed burning on mycelial communities of ectomycorrhizal fungi. New Phytol 172:149–158
Berbee ML, Taylor JW (1993) Dating the evolutionary radiations of the true fungi. Can J Bot 71:1114–1127
Branco S, Ree RH (2010) Serpentine soils do not limit mycorrhizal fungal diversity. PlosOne 5:1–7
Bruns T, Biartondo MI, Taylor L (2002) Host specificity in ectomycorrhizal communities: what do the exceptions tell us. Integr Comp Biol 42:352–359
Buscardo E, Rodríguez-Echeverría S, Martin MP, de Angelis P, Pereira JS, Freitas H (2010) Impact of wildfire return interval on the ectomycorrhizal resistant propagules communities of a Mediterranean open forest. Fungal Biol 114:628–636
Buscardo E, Freitas H, Pereira JS, de Angelis P (2011) Common environmental factors explain both ectomycorrhizal species diversity and pine regeneration variability in a post-fire Mediterranean forest. Mycorrhiza 21:549–558
Cairney JWG, Bastias BA (2007) Influences of fire on forest soil fungal communities. Can J For Res 37:207–215
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
Certini G (2005) Effects of fire on properties of forest soils: a review. Oecologia 143:1–10
Claridge AW, Trappe JM, Mills DJ, Claridge DL (2009) Diversity and habitat relationships of hypogeous fungi. III. Factors influencing the occurrence of fire-adapted species. Mycol Res 113:792–801
Dahlberg A, Schimmel J, Taylor AFS, Johannesson H (2001) Post-fire legacy of ectomycorrhizal fungal communities in the Swedish boreal forest in relation to fire severity and logging intensity. Biol Conserv 100:151–161
Dickie IA, Dentinger BTM, Avis PG, McLaughlin DJ, Reich PB (2009) Ectomycorrhizal communities of oak savana are distinct from forest communities. Mycologia 101:473–483
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidomycetes: application to identification of mycorrhizae and rusts. Mol Ecol 2:113–118
Grogan P, Baar J, Bruns TD (2000) Below-ground ectomycorrhizal community structure in a recently burned bishop pine forest. J Ecol 88:1051–1062
Hart SC, DeLuca TH, Newman GS, MacKenzie MD, Boyle SI (2005) Post-fire vegetative dynamics as drivers of microbial community structure and function in forest soils. For Ecol Manag 220:166–184
Hibbet DS (2006) A phylogenetic overview of the Agaricomycotina. Mycologia 96:917–925
Horner-Devine MC, Bohannan BJM (2006) Phylogenetic clustering and overdispersion in bacterial communities. Ecology S100-S108
Horton TR, Cazares E, Bruns TD (1998) Ectomycorrhizal, vesicular-arbuscular and dark septate fungal colonization of bishop pine (Pinus muricata) seedlings in the first 5 months of growth after wildfire. Mycorrhiza 8:11–18
James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J et al (2006) Reconstruction the early evolution of fungi using a six gene phylogeny. Nature 443:818–822
Jonsson L, Dahlberg A, Nilsson MC, Zackrisson O, Karen O (1999) Ectomycorrhizal fungal communities in late-successional Swedish boreal forests, and their composition following wildfire. Mol Ecol 8:205–215
Johnson D, Martin F, Cairney JWG, Anderson IC (2012) The importance of individuals: intraspecific diversity on mycorrhizal plants and fungi in ecosystems. New Phytol 194:614–628
Keeley JE, Bond WJ, Bradstock RA, Pausas JG, Rundel PW (2012) Fire in Mediterranean Ecosystems. Ecology, Evolution and Management. Cambridge University Press, NY
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464
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
Kennedy P (2010) Ectomycorrhizal fungi and interspecific competition: species interactions, community structure, coexistence mechanisms and future research directions. New Phytol 187:895–910
Kipfer T, Moser B, Egli S, Wohlgemuth T, Ghazoul J (2011) Ectomycorrhizal succession patterns in Pinus sylvestris forests after stand-replacing fire in the Central Alps. Oecologia 167:219–228
LeDuc SD, Lilleskov EA, Horton TR, Rothstein DE (2012) Ectomycorrhizal fungal succession coincides with shifts in organic nitrogen availability and canopy closure in post-wildfire jack pine forests. Oecologia. doi:10.1007/s00442-012-2471-0
Legendre P, De Cáceres M, Bocard D (2010) Community surveys through space and time: testing the space-time interaction in the absence of replication. Ecology 91:262–272
Lilleskov EA, Hobbie EA, Fahey TJ (2002) Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. New Phytol 154:219–231
Loepfe L, Martinez-Vilalta J, Oliveres J, Piñol J, Lloret F (2010) Feedbacks between fuel reduction and landscape homogenisation determine fire regimes in three Mediterranean areas. For Ecol Manag 259:2366–2374
Longo S, Urcelay C, Nouhra E (2011) Long term effects of fire on ectomycorrhizas and soil properties in Nothofagus pumilio foests in Argentina. For Ecol Manag 262:348–354
Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, USA, Princeton
Maherali H, Klironomos JN (2007) Influence of Phylogeny on Fungal Community Assembly and Ecosystem Functioning. Science 316:1746–1748
McMullan-Fisher SJM, May TW, Robinson RM, Bell TL, Lebel T, Catcheside P, York A (2011) Fungi and fire in Australian ecosystems: a review of current knowledge, management implications and future directions. Aust J Bot 59:70–90
Molina R, Trappe JM, Grubisha LC, Spatafora JW (1999) Rhizopogon. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizal fungi key genera in profile. Springer, Berlin, Germany, pp 129–161
Moncalvo J-M, Nilsson RH, Koster B, Dunham SM, Bernauer T, Matheny PB, McLenon T, Margaritescu S, Wei BM, Garnica S et al (2006) The cantharelloid clade: dealing with incongruent gene trees and phylogenetic reconstruction methods. Mycologia 98:937–948
Nara K (2009) Spores of ectomycorrhizal fungi: ecological strategies for germination and dormancy. New Phytol 181:245–248
Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH (2008) Intraspecific ITS variability in the Kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Informat 4:193–201
Nilsson LO, Wallander H, Gundersen P (2012) Changes in microbial activities and biomasses over a forest floor gradient in C to N ratio. Plant Soil 355:75–86
Oksanen JF, Blanchet G, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2011) Vegan: Community Ecology Package. R package version 2.0-0. http://CRAN.R-project.org/package=vegan
Pausas JG, Verdú M (2010) The jungle of methods for evaluating phenotypic and phylogenetic structure of communities. BioScience 60:614–625
Peay KG, Kennedy PG, Davies SJ, Tan S, Bruns TD (2010) Potential link between plant and fungal distributions in a dipterocarp rainforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytol 185:529–542
Peay KG, Belisle M, Fukami T (2012) Phylogenetic relatedness predicts priority effects in nectar yeast communities. P Roy Soc B 279:749–758
Pereira P, Úbeda X, Martin DA (2012) Fire severity effects on ash chemical composition and water extractable elements. Geoderma 191:105–114
R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.rproject.org/
Rincón AR, Pueyo JJ (2010) Effect of fire severity and site slope on diversity and structure of the ectomycorrhizal fungal community associated with post-fire regenerated Pinus pinaster Ait. seedlings. For Ecol Manag 260:361–369
Rodrigo A, Retana J, Pico FX (2004) Direct regeneration is not the only response of Mediterranean forests to large fires. Ecology 85:716–729
Smith SE, Read DJ (1997) Mycorrhizal Symbiosis. Academic Press, Cambridge, UK
Stendell ER, Horton TR, Bruns TD (1999) Early effects of prescribed fire on the structure of the ectomycorrhizal fungus community in a Sierra Nevada ponderosa pine forest. Mycol Res 103:1353–1359
Schoch CL, Sung GH, Pez-Giraldez FL, Townsend JP, Miadlikowska J, Hofstetter V, Robertse B, Matheny PB, Kauff F, Wang Z et al (2009) The Ascomycota tree of life: a phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Systematic Biol 58:224–239
Sugiyama J, Hosaka K, Suth SO (2006) Early diverging Ascomycota: phylogenetic divergence and related evolutionary enigmas. Mycologia 98:996–1005
Tapias R, Climent J, Pardos JA, Gil L (2004) Life history of Mediterranean pines. Plant Ecol 171:53–68
Taylor DL, Bruns TD (1999) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities. Mol Ecol 8:1837–1850
Tedersoo L, Suvi T, Larsson E, Koljalg U (2006) Diversity and community structure of ectomycorrhizal fungi in a wooded meadow. Mycol Res 110:734–748
Thompson M, Calkin DE (2011) Uncertainty and risk in wild land fire management: a review. J Environ Manage 92:1895–0909
Torres P, Honrubia M (1997) Changes and effects of a natural fire on ectomycorrhizal inoculum potential of soil in a Pinus halepensis forest. For Ecol Manag 96:189–196
Treseder KK, Mack MC, Cross A (2004) Relationships among fires, fungi, and soil dynamics in Alaskan boreal forests. Ecol Appl 14:1824–1838
Tweig BD, Durall DM, Simard SW (2009) Influence of soil nutrients on ectomycorrhizal communities in a chronosequence of mixed temperate forests. Mycorrhiza 19:305–316
Valiente-Banuet A, Verdú M (2007) Facilitation can increase the phylogenetic diversity of plant communities. Ecol Lett 10:1029–1036
Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505
Webb CO, Ackerly DD, Kembel SW (2008) Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 24:2098–2100
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols—A Guide to Methods and Applications. Academic Press, New York, pp 315–322
Acknowledgements
We gratefully acknowledge A Carrillo and R Serrada for the aid in fieldwork, and C Mesa, B Cámara and S Pérez-Ortega for their assistance in molecular and phylogenetic analyses. We thank the editor and the anonymous referees for their constructive comments helping to improve the manuscript. This work was founded by the Empresa de Transformación Agraria (TRAGSA), and grants of the Spanish Ministry of Innovation and Science (CGL2011-29585) and the Comunidad de Madrid (S2009/AMB-1511).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Fig. S1
Map of the study area and location of sampling plots. Two neighbouring areas burned in stand replacing wildfires in the summers of 1994 (Fi-94) (grey plots) and 2005 (Fi-05) (black plots) and an in-between area with a P. pinaster forest unaffected by fire at least in the preceding 60 yr (white plots) were differentiated. Scale 1 cm = 1 km. (PDF 278 kb)
Fig. S2
Phylogenetic tree of the ectomycorrhizal fungi associated with Pinus pinaster seedlings and saplings, in sites differing in the elapsed time since the last fire event: control = > 60 yr after fire (white circles), Fi-94 = 14-yr after fire (squares), and Fi-05 = 3-yr after fire (black triangles). The phylogeny was generated using the 5.8S and 25S LSU sequences of all EM fungal OTUs. The tree was constructed with BEAST programme assuming a general time-reversible model of nucleotide substitution rates, and topological constraints derived from phylogenetic studies of the kingdom Fungi. Black circles point to clades grouping Ascomycetes (up) and Basidiomycetes (down). The scale bar indicates million years. Numbers in parentheses correspond to the identification codes of fungi listed in Table1. (PDF 129 kb)
ESM 1
(PDF 110 kb)
ESM 2
(PDF 57 kb)
Rights and permissions
About this article
Cite this article
Rincón, A., Santamaría, B.P., Ocaña, L. et al. Structure and phylogenetic diversity of post-fire ectomycorrhizal communities of maritime pine. Mycorrhiza 24, 131–141 (2014). https://doi.org/10.1007/s00572-013-0520-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-013-0520-0