Forestry impacts on the hidden fungal biodiversity associated with bryophytes

FEMS Microbiology Ecology

Volumn 90, Issue 1, 2014, Pages 313-325

  Davey, Marie L ^a,b   Kauserud, Håvard ^a   Ohlson, Mikael ^b  

^a UNIVERSITY OF OSLO   (Norway)

^b NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

Author keywords

Bryophilous fungi; Clear cut; Disturbance; Next generation sequencing; Old growth forest

Indexed keywords

BRYOPHYTES; FUNGI;

BIODIVERSITY; CLASSIFICATION; FOREST; FORESTRY; FUNGUS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOSS;

BIODIVERSITY; BRYOPHYTA; FORESTRY; FORESTS; FUNGI;

EID: 84907879770     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/1574-6941.12386     Document Type: Article

References (94)

1. Amend AS, Seifert KA & Bruns TD (2010) Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol Ecol 19: 5555-5565.
2. Bainbridge EL & Strong WL (2005) Pinus contorta understory vegetation dynamics following clear cutting in west-central Alberta, Canada. For Ecol Manage 213: 133-150.
3. Berg A, Ehnström B, Gustafsson L, Hallingbäck T, Jonsell M & Weslin J (1994) Threatened plant, animal, and fungus species in Swedish forests: distribution and habitat associations. Conserv Biol 8: 718-731.
4. Berry D, ben Mahfoudh K, Wagner M & Loy A (2011) Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl Environ Microbiol 77: 7846-7849.
5. Bonan GB & Shugart HH (1989) Environmental factors and ecological processes in boreal forests. Annu Rev Ecol Syst 20: 1-28.
6. Caporaso JG, Kuczynski J, Stombaugh J et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
7. Carleton TJ & Read DJ (1991) Ectomycorrhizas and nutrient transfer in conifer-feather moss ecosystems. Can J Bot 69: 778-785.
8. Carlsen T, Aas AB, Lindner D, Vrålstad T, Schumacher T & Kauserud H (2012) Don't make a mista(g)ke: Is tag switching an overlooked source of error in amplicon pyrosequencing studies? Fungal Ecol 5: 747-749.
9. Colwell RK (2009) EstimateS: Statistical estimation of species richness and shared species from samples. Version 8.2. User's Guide and application published at: http://purl.oclc.org/estimates.
10. Cronberg N (2002) Colonization and dynamics of the clonal moss Hylocomium splendens on islands in a Baltic land uplift area: reproduction, genet distribution and genetic variation. J Ecol 90: 925-935.
11. Davey ML & Currah RS (2006) Interactions between mosses (Bryophyta) and fungi. Can J Bot 84: 1509-1519.
12. Davey ML, Nybakken L, Kauserud H & Ohlson M (2009) Fungal biomass in the phyllosphere of bryophytes and vascular plants. Mycol Res 113: 1254-1260.
13. Davey ML, Tsuneda A & Currah RS (2010) Saprobic and parasitic interactions of Coniochaeta velutina with mosses. Botany 88: 258-265.
14. Davey ML, Heegard E, Halvorsen R, Ohlson M & Kauserud H (2012) Seasonal trends in the biomass and structure of bryophyte-associated fungal communities explored by 454 pyrosequencing. New Phytol 195: 844-856.
15. Davey ML, Heegaard E, Halvorsen R, Kauserud H & Ohlson M (2013a) Amplicon pyrosequencing based detection of compositional shifts in bryophyte-associated fungal communities along an elevation gradient. Mol Ecol 22: 368-383.
16. Davey ML, Heimdal R, Ohlson M & Kauserud H (2013b) Host- and tissue-specificity of moss-associated Galerina and Mycena determined from amplicon pyrosequencing data. Fungal Ecol 6: 179-186.
17. de Caceres M & Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90: 3566-3574.
18. Diggle PJ & Ribeiro PJ Jr (2007) Model Based Geostatistics. Springer, New York, NY.
19. Döbbeler P (2002) Microniches occupied by brophilous ascomycetes. Nova Hedwigia 75: 275-306.
20. Durall DM, Gamiet S, Simard SW, Kudrna L & Sakakibara SM (2006) Effects of clear cut logging and tree species composition on the diversity and community composition of epigeous fruit bodies formed by ectomycorrhizal fungi. Can J Bot 84: 966-980.
21. Dynesius M & Hylander K (2007) Resilience of bryophyte communities to clear-cutting of boreal stream-side forests. Biol Conserv 135: 423-434.
22. Edgar RC (2010) Search and clustering orders of magnitude faster than blast. Bioinformatics 26: 2460-2461.
23. Frivold LH (1999) Skoghistorie i Norge. Skogs- och lantbrukshistoriska meddelanden 22: 207-236 (in Norwegian).
24. Gamfeldt L, Snäll T, Bagchi R et al. (2013) Higher levels of multiple ecosystem services are found in forests with more species. Nat Commun 4: Article Number 1340.
25. Gardes M & Bruns T (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2: 113-118.
26. Gauslaa Y, Ohlson M & Rolstad J (1998) Fine-scale distribution of the epiphytic lichen Usnea longissima on two even-aged neighbouring Picea abies trees. J Veg Sci 9: 95-102.
27. Gauslaa Y, Lie M, Solhaug KA & Ohlson M (2006) Growth and ecophysiological acclimation of the foliose lichen Lobaria pulmonaria in forests with contrasting light climates. Oecologia 147: 406-416.
28. Gauslaa Y, Palmqvist K, Solhaug KA, Holien H, Hilmo O, Nybakken L, Myhre LC & Ohlson M (2007) Growth of epiphytic old forest lichens across climatic and successional gradients. Can J For Res 37: 1832-1845.
29. Gjerde I, Brandsrud TE, Ohlson M & Ødegaard F (2010) Woodland. Environmental Conditions and Impacts for Red List Species (Kålås JA, Henriksen S, Skjelseth S & Viken Å, eds), pp. 67-78. Norwegian Biodiversity Information Centre, Trondheim, Norway.
30. Gower ST (2003) Patterns and mechanisms of the forest carbon cycle. Annu Rev Environ Resour 28: 169-204.
31. Halpern CB & Spies TA (1995) Plant species diversity in natural and managed forests of the Pacific Northwest. Ecol Appl 5: 913-934.
32. Hellberg E, Josefsson T & Östlund L (2009) The transformation of a Norway spruce dominated landscape since pre-industrial times in northern Sweden: the influence of modern forest management on forest structure. Silva Fennica 43: 783-797.
33. Helle P (1985) Effects of forest regeneration on the structure of bird communities in northern Finland. Ecography 8: 120-132.
34. Hill MO (1979) DECORANA - A FORTRAN Program for Detrended Correspondence Analysis and Reciprocal Averaging. Cornell University, New York, NY, USA.
35. Hill MO & Gauch HG Jr (1980) Detrended correspondence analysis: an improved ordination technique. Vegetatio 42: 47-58.
36. Hobbie SE, Schimel JP, Trumbore SE & Randerson JR (2000) Controls over carbon storage in high-latitude soils. Glob Change Biol 6: S196-S210.
37. Hylander K & Jonsson BG (2002) Evaluating buffer strips along boreal streams using bryophytes as indicators. Ecol Appl 12: 797-806.
38. Hynes HM & Germida JJ (2012) A chronosequential approach to investigating microbial community shifts following clearcutting in Boreal Plain forest soils. Can J For Res 42: 2078-2089.
39. Jones MD, Durall DM & Cairney JWG (2003) Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytol 157: 399-422.
40. Jonsell M, Nitterus K & Stighäll K (2004) Saproxylic beetles in natural and man-made deciduous high stumps retained for conservation. Biol Conserv 118: 163-173.
41. Josefsson T, Olsson J & Östlund L (2010) Linking forest history and conservation efforts: long-term impact of low-intensity timber harvest on forest structure and wood-inhabiting fungi in northern Sweden. Biol Conserv 143: 1803-1811.
42. Kålås JA, Viken Å, Henriksen S & Skjelseth S (2010) The 2010 Norwegian Red List for Species. Norwegian Biodiversity Information Center, Trondheim, Norway.
43. Kauserud H, Lie M, Stensrud Ø & Ohlson M (2005) Molecular characterisation of airborne fungal spores in boreal forests of contrasting human disturbance. Mycologia 97: 1215-1224.
44. Kauserud H, Mathiesen C & Ohlson M (2008) High diversity of fungi associated with living parts of boreal forest bryophytes. Botany 86: 1326-1333.
45. Koivula M, Kukkonen J & Niemelä J (2002) Boreal carabid-beetle (Coleoptera, Carabidae) assemblages along the clear-cut originated succession gradient. Biodivers Conserv 11: 1269-1288.
46. Kruskal JB (1964a) Multidimensional scaling optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29: 1-27.
47. Kruskal JB (1964b) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29: 115-129.
48. Kuuluvainen T, Tahvonen O & Aakala T (2012) Even-aged and uneven-aged forest management in boreal Fennoscandia: a review. Ambio 41: 720-737.
49. Larsson JY & Hylen G (2007) Statistics of Forest Conditions and Forest Resources in Norway. Viten fra Skog og landskap 1/07 Norwegian Forest and Landscape Institute, Ås, Norway.
50. Lie MH, Arup U, Grytnes J-A & Ohlson M (2009) The importance of host tree age, size and growth rate as determinants of epiphytic lichen diversity in boreal spruce forests. Biodivers Conserv 18: 3579-3596.
51. Lie MH, Josefsson T, Storaunet KO & Ohlson M (2012) A refined view on the "Green lie": forest structure and composition succeeding early twentieth century selective logging in SE Norway. Scand J For Res 27: 270-284.
52. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J & Finlay RD (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173: 611-620.
53. Liu HY, Økland T, Halvorsen R, Gao JX, Liu QR, Eilertsen O & Bratli H (2008) Gradient analyses of forests ground vegetation and its relationships to environmental variables in five subtropical forest areas, S and SW China. Sommerfeltia 32: 1-196.
54. Lõhmus A (2011) Silviculture as a disturbance regime: the effects of clear-cutting, planting, and thinning on polypore communities in mixed forests. J For Res 16: 194-202.
55. Lundmark H, Josefsson T & Östlund L (2013) The history of clear-cutting in northern Sweden - driving forces and myths in boreal silviculture. For Ecol Manage 307: 112-122.
56. Lundström J, Öhman K, Perhans K, Rönnqvist M & Gustafsson L (2011) Cost-effective age structure and geographical distribution of boreal forest reserves. J Appl Ecol 48: 133-142.
57. Minchin PR (1987) An evaluation of the relative robustness of techniques for ecological ordination. Vegetatio 69: 89-107.
58. Moore-Kucera J & Dick RP (2008) PLFA profiling of microbial community structure and seasonal shifts in soils of a Douglas-fir chronosequence. Microb Ecol 55: 500-511.
59. Murray M & Thompson W (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8: 4321.
60. Niemelä J, Langor D & Spence JR (1993) Effects of clear-cut harvesting on boreal ground-beetle assemblages (Coleoptera: Carabidae) in Western Canada. Conserv Biol 7: 551-561.
61. Ohlson M & Tryterud E (1999) Long-term spruce forest continuity - a challenge for a sustainable Scandinavian forestry. For Ecol Manage 124: 27-34.
62. Ohlson M, Söderström L, Hörnberg G, Zackrisson O & Hermansson J (1997) Habitat qualities versus long-term continuity as determinants of biodiversity in old-growth boreal swamp forests. Biol Conserv 81: 221-231.
63. Ohlson M, Brown KJ, Birks HJB, Grytnes J-A, Hörnberg G, Niklasson M, Seppä H & Bradshaw RHW (2011) Invasion of Norway spruce diversifies the fire regime in boreal European forests. J Ecol 99: 395-403.
64. Økland RH (1990) Vegetation ecology: theory, methods and applications with reference to Fennoscandia. Sommerfeltia (Suppl 1): S1-S233.
65. Økland B (1994) Mycetophilidae (Diptera), an insect group vulnerable to forestry practices - a comparison of clear-cut, managed and seminatural spruce forests in southern Norway. Biodivers Conserv 3: 68-85.
66. Økland RH (1995) Population biology of the clonal moss Hylocomium splendens in Norwegian boreal spruce forests. 1. Demography. J Ecol 83: 697-712.
67. Økland RH (1996a) Are ordination and constrained ordination alternative or complementary strategies in general ecological studies? J Veg Sci 7: 289-292.
68. Økland T (1996b) Vegetation-environment relationships of boreal spruce forest in ten monitoring reference areas in Norway. Sommerfeltia 22: 1-349.
69. Økland RH & Eilertsen O (1993) Vegetation-environment relationships of boreal coniferous forests in the Solhomfjell area, Gjerstad, S Norway. Sommerfeltia 16: 1-254.
70. Økland B, Bakke A, Hågvar S & Kvamme T (1996) What factors influence the diversity of saproxylic beetles? A multiscaled study from a spruce forest in southern Norway. Biodivers Conserv 5: 75-100.
71. Oksanen J, Blanchet FG, 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.
72. Östlund L, Zackrisson O & Axelsson L (1997) The history and transformation of a Scandinavian boreal forest landscape since the 19th century. Can J For Res 27: 1198-1206.
73. Paillet Y, Berges L & Hjalten J et al. (2010) Biodiversity differences between managed and unmanged forests: meta-analysis of species richness in Europe. Conserv Biol 24: 101-112.
74. Palvainen M, Finer L, Mannerkoski H, Piirainen S & Starr M (2005) Responses of vegetation species to clear-cutting in a boreal forest: aboveground biomass and nutrient contents during the first 7 years. Ecol Res 20: 652-660.
75. Pykälä J (2007) Implementation of forest act habitats in Finland: does it protect the right habitats for threatened species? For Ecol Manage 242: 281-287.
76. R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.
77. Reeder J & Knight R (2010) Rapidly denoising pyrosequencing amplicon reads by exploiting rank-abundance distributions. Nat Methods 7: 668-669.
78. Ribeiro PJ Jr & Diggle PJ (2001) geoR: a package for geostatistical analysis. R-NEWS 1: 15-18.
79. Rolstad J, Rolstad E & Groven R (1996) Nordens eldste gran? Blyttia 54: 7-8 (in Norwegian).
80. Rydgren K, de Kroon H, Økland RH & van Groenendael J (2001) Effects of fine-scale disturbances on the demography of and population dynamics of the clonal moss Hylocomium splendens. J Ecol 89: 395-405.
81. Sato T, Watanabe K, Fukushima K & Tokuchi N (2014) Parasites and forest chronosequence: long-term recovery of nematomorph parasites after clear-cut logging. For Ecol Manage 314: 166-171.
82. Schloss PD, Westcott SL, Ryabin T et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541.
83. Schmiegelow FKA & Mönkkönen M (2002) Habitat loss and fragmentation in dynamic landscapes: avian perspectives from the boreal forest. Ecol Appl 12: 375-389.
84. Söderström L (1988) Occurrence of epixylic bryophyte and lichen species in an old natural and managed forest stand in northeast Sweden. Biol Conserv 45: 169-178.
85. Storaunet KO, Rolstad J, Gjerde I & Gundersen VS (2005) Historical logging, productivity, and structural characteristics of boreal coniferous forests in Norway. Silva Fennica 39: 429-442.
86. Tedersoo L, Nilsson RH, Abarenkov K, Jairus T, Sadam A, Saar I, Bahram M, Bechem E, Chuyuong G & Kõljalg U (2010) 454 Pyrosequencing and Sanger sequencing of tropical mycorrhizal fungi provide similar results but reveal substantial methodological biases. New Phytol 188: 291-301.
87. ter Braak CFJ (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67: 1167-1179.
88. Timonen J, Gustafsson L, Kotiaho JS & Mönkkönen M (2011) Hotspots in cold climate: conservation value of woodland key habitats in boreal forests. Biol Conserv 144: 2061-2067.
89. Tryterud E (2003) Forest fire in Norway: from fire-disturbed pine forests to fire-free spruce forests. Ecography 26: 161-170.
90. Turetsky MR (2003) The role of bryophytes in carbon and nitrogen cycling. Bryologist 106: 395-409.
91. Tveite S (1961) Engelsk-norsk Trelasthandel 1640-1710. Universitetsforlaget, Oslo (in Norwegian with English summary).
92. Walker LR, Wardle DA, Bardgett RD & Clarkson BD (2010) The use of chronosequences in studies of ecological succession and soil development. J Ecol 98: 725-736.
93. White TJ, Bruns T, Lee S & Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications (Innis MA, Gelfand DH, Sninsky JJ & White TJ, eds), pp. 315-322, Academic Press Inc., New York, USA.
94. Zackrisson O (1977) Influence of forest fires on the North Swedish boreal forest. Oikos 29: 22-32.