Biodiversity and Conservation

, Volume 23, Issue 9, pp 2155–2172 | Cite as

Disturbance and diversity of wood-inhabiting fungi: effects of canopy gaps and downed woody debris

  • Nicholas J. Brazee
  • Daniel L. Lindner
  • Anthony W. D’Amato
  • Shawn Fraver
  • Jodi A. Forrester
  • David J. Mladenoff
Original Paper

Abstract

Experimental canopy gap formation and additions of coarse woody debris (CWD) are techniques intended to mimic the disturbance regime and accelerate the development of northern hardwood forests. The effects of these techniques on biodiversity and ecosystem functioning were investigated by surveying the abundance and diversity of wood-inhabiting fungi in six treatments: (i) unharvested control, (ii) control + fenced to exclude deer, (iii) gap creation + fenced to exclude deer, (iv) gap creation, (v) gap creation + CWD addition, and (vi) CWD addition under closed-canopy. A total of 1,885 fungal occurrences (polyporoid and corticoid fruiting bodies) representing 130 species were recorded on 11 tree species, with eight fungal species accounting for 52 % of all observations. A linear mixed model demonstrated significant differences in the abundance and diversity of wood-inhabiting fungi by treatment, with the gap creation + CWD addition treatment supporting the highest abundance and richness of fungal species. Non-metric multidimensional scaling demonstrated that stumps, sugar maple substrates, medium (20 to <25 cm) and large-diameter (>40 cm) substrates most strongly influenced fungal species occurrences. Rarefaction curves indicated that smaller diameter substrates (<20 cm) supported a rich fungal community, yet substrates in the largest diameter class (>40 cm) supported nearly 25 % of all fungal species detected. Rarefaction curves also highlighted the importance of well-decayed substrates and minor host tree species. A subset of fungal species was significantly more abundant in gap treatments. The results indicate that wood-inhabiting fungi are responsive to forest management intended to promote the structural attributes of old-growth northern hardwood forests.

Keywords

Biodiversity Decay fungi Gap-phase Northern hardwoods Sugar maple Restoration 

Supplementary material

10531_2014_710_MOESM1_ESM.docx (54 kb)
Supplementary material 1 (DOCX 48 kb)

References

  1. Abrego N, Salcedo I (2013) Variety of woody debris as the factor influencing wood-inhabiting fungal richness and assemblages: Is it a question of quantity or quality? For Ecol Manage 291:377–385Google Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Ahang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bader P, Jansson S, Jonsson BG (1995) Wood-inhabiting fungi and substratum decline in selectively logged boreal spruce forests. Biol Conserv 72:355–362CrossRefGoogle Scholar
  4. Bässler C, Müller J, Svoboda M, Lepšová A, Hahn C, Holzer H, Pouska V (2012) Diversity of wood-decaying fungi under different disturbance regimes: a case study from spruce mountain forests. Biodivers Conserv 21:33–49CrossRefGoogle Scholar
  5. Berglund H, Jönsson MT, Penttilä R, Vanha-Majamaa I (2011) The effects of burning and dead-wood creation on the diversity of pioneer wood-inhabiting fungi in managed boreal spruce forests. For Ecol Manag 261:1293–1305CrossRefGoogle Scholar
  6. Brazee NJ, Lindner DL, Fraver S, D’Amato AW, Milo AM (2012) Wood-inhabiting, polyporoid fungi in aspen-dominated forests managed for biomass in the U.S. Lake States. Fungal Ecol 5:600–609CrossRefGoogle Scholar
  7. Bressette JW, Beck H, Beauchamp VB (2012) Beyond the browse line: complex cascade effects mediated by white-tailed deer. Oikos 121:1749–1760CrossRefGoogle Scholar
  8. Brualdi RA, Sanderson JG (1999) Nested species subsets, gaps, and discrepancy. Oecologia 119:256–264CrossRefGoogle Scholar
  9. Burke DJ, Weintraub MN, Hewins CR, Kalisz S (2011) Relationship between soil enzyme activities, nutrient cycling and soil fungal communities in a northern hardwood forest. Soil Biol Biochem 43:795–803CrossRefGoogle Scholar
  10. Carlile MJ, Watkinson SC, Gooday GW (2006) The fungi, 2nd edn. Elsevier Academic Press, LondonGoogle Scholar
  11. Crockatt ME (2012) Are there edge effects on forest fungi and if so do they matter? Fun Biol Rev 26:94–101CrossRefGoogle Scholar
  12. Czederpiltz DLL (2001) Forest management and the diversity of wood-inhabiting polyporoid and corticioid fungi. Dissertation, University of Wisconsin, MadisonGoogle Scholar
  13. Dahlberg A, Genney DR, Heilmann-Clausen J (2010) Developing a comprehensive strategy for fungal conservation in Europe: current status and future needs. Fungal Ecol 3:50–64CrossRefGoogle Scholar
  14. D’Amato AW, Orwig DA (2008) Stand landscape-level disturbance dynamics in old-growth forests in western Massachusetts. Ecol Monogr 78:507–522CrossRefGoogle Scholar
  15. Dyer JH, Gower ST, Forrester JA, Lorimer CG, Mladenoff DJ, Burton JI (2010) Effects of selective tree harvests on aboveground biomass and net primary productivity of a second-growth northern hardwood forest. Can J For Res 40:2360–2369CrossRefGoogle Scholar
  16. Edman M, Jonsson BG (2001) Spatial pattern of downed logs and wood-decaying fungi in an old-growth Picea abies forest. J Veg Sci 12:609–620CrossRefGoogle Scholar
  17. Edman M, Kruys N, Jonsson BG (2004) Local dispersal sources strongly affect colonization patterns of wood-inhabiting fungi on spruce logs. Ecol Appl 14:893–901CrossRefGoogle Scholar
  18. Eyre FH (1980) Forest Cover types of the United States and Canada. Society of American Foresters, Washington DCGoogle Scholar
  19. Forrester JA, Mladenoff DJ, Gower ST, Stoffel JL (2012) Interactions of temperature and moisture with respiration from coarse woody debris in experimental forest canopy gaps. For Ecol Manag 265:124–132CrossRefGoogle Scholar
  20. Frelich LE, Lorimer CG (1991) Natural disturbance regimes in hemlock-hardwood forests of the Upper Great Lakes region. Ecol Monogr 61:145–164CrossRefGoogle Scholar
  21. Goodburn JM, Lorimer CG (1998) Cavity trees and coarse woody debris in old-growth and managed northern hardwood forests in Wisconsin and Michigan. Can J For Res 28:427–438Google Scholar
  22. Gore JA, Patterson WA III (1986) Mass of downed wood in northern hardwood forests in New Hampshire: potential effects of forest management. Can J For Res 16:335–339CrossRefGoogle Scholar
  23. Halme P, Kotiaho JS, Ylisirniö A-L, Hottola J, Junninen K, Kouki J, Lindgren M, Mönkkönen M, Penttilä R, Renvall P, Siitonen J, Similä M (2009) Perennial polypores as indicators of annual and red-listed polypores. Ecol Indic 9:256–266CrossRefGoogle Scholar
  24. Halme P, Ódor P, Christensen M, Piltaver A, Veerkamp M, Walleyn R, Siller I, Heilmann-Clausen J (2013) The effect of habitat degradation on metacommunity structure of wood-inhabiting fungi in European beech forests. Biol Conserv 168:24–30CrossRefGoogle Scholar
  25. Hanson JJ, Lorimer CG (2007) Forest structure and light regimes following moderate wind storms: implications for multi-cohort management. Ecol Appl 17:1325–1340PubMedCrossRefGoogle Scholar
  26. Heilmann-Clausen J, Christensen M (2004) Does size matter? On the importance of various dead wood fractions for fungal diversity in Danish beech forests. For Ecol Manage 201:105–117CrossRefGoogle Scholar
  27. Heilmann-Clausen J, Christensen M (2005) Wood-inhabiting macrofungi in Danish beech-forests: conflicting diversity patterns and their implications in a conservation perspective. Biol Conserv 122:633–642CrossRefGoogle Scholar
  28. Heilmann-Clausen J, Aude E, Christensen M (2005) Cryptogam communities on decaying deciduous wood: does tree species diversity matter? Biodivers Conserv 14:2061–2078CrossRefGoogle Scholar
  29. Hennon PE (1995) Are heart rot fungi major factors of disturbance in gap-dynamic forests? Northwest Sci 69:284–293Google Scholar
  30. Hepting GH (1971) Diseases of forest and shade trees of the United States. USDA Agricultural Handbook No. 386, Washington DCGoogle Scholar
  31. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  32. Horsley SB, Stout SL, deCalesta DS (2003) White-tailed deer impact on the vegetation dynamics of a northern hardwood forest. Ecol Appl 13:98–118CrossRefGoogle Scholar
  33. Hurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586CrossRefGoogle Scholar
  34. Jacobs JM, Work TM (2012) Linking deadwood-associated beetles and fungi with wood decomposition rates in managed black spruce forests. Can J For Res 42:1477–1490CrossRefGoogle Scholar
  35. Jonsson BG (2001) A null model for randomization tests of nestedness in species assemblages. Oecologia 127:309–313CrossRefGoogle Scholar
  36. Jönsson MT, Edman M, Jonsson BG (2008) Colonization and extinction patterns of wood-decaying fungi in a boreal old-growth Picea abies forest. J Ecol 96:1065–1075CrossRefGoogle Scholar
  37. Junninen K, Similä M, Kouki J, Kotiranta H (2006) Assemblages of wood-inhabiting fungi along the gradients of succession and naturalness in boreal pine-dominated forests in Fennoscandia. Ecography 29:75–83CrossRefGoogle Scholar
  38. Junninen K, Penttilä R, Martikainen P (2007) Fallen retention aspen trees on clear-cuts can be important habitats for red-listed polypores: a case study in Finland. Biodivers Conserv 16:475–490CrossRefGoogle Scholar
  39. Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bionform 9:286–298CrossRefGoogle Scholar
  40. Kebli H, Brais S, Kernaghan G, Drouin P (2012) Impact of harvesting intensity on wood-inhabiting fungi in boreal aspen forests of Eastern Canada. For Ecol Manag 279:45–54CrossRefGoogle Scholar
  41. Kruys N, Jonsson BG (1999) Fine woody debris is important for species richness on logs in managed boreal spruce forests of northern Sweden. Can J For Res 29:1295–1299CrossRefGoogle Scholar
  42. Küffer N, Senn-Irlet B (2005) Influence of forest management on the species richness and composition of wood-inhabiting basidiomycetes in Swiss forests. Biodivers Conserv 14:2419–2435CrossRefGoogle Scholar
  43. Larkin BG, Hunt LS, Ramsey PW (2012) Foliar nutrients shape fungal endophyte communities in Western white pine (Pinus monticola) with implications for white-tailed deer herbivory. Fungal Ecol 5:252–260CrossRefGoogle Scholar
  44. Lessard J-P, Reynolds WN, Bunn WA, Genung MA, Cregger MA, Felker-Quinn E, Barrios-Garcia MN, Stevenson ML, Lawton RM, Brown CB, Patrick M, Rock JH, Jenkins MA, Bailey JK, Schweitzer JA (2012) Equivalence in the strength of deer herbivory on above and below ground communities. Basic Appl Ecol 13:59–66CrossRefGoogle Scholar
  45. Lindhe A, Asenblad N, Torenson H-G (2004) Cut logs and high stumps of spruce, birch, aspen and oak—nine years of saproxylic fungi succession. Biol Cons 119:443–454CrossRefGoogle Scholar
  46. Lindner DL, Banik MT (2009) Effects of cloning and root-tip size on observations of fungal ITS sequences from Picea glauca roots. Mycologia 101:157–165PubMedCrossRefGoogle Scholar
  47. Lindner DL, Burdsall HH, Stanosz GR (2006) Species diversity of polyporoid and corticioid fungi in northern hardwood forests with differing management histories. Mycologia 98:195–217PubMedCrossRefGoogle Scholar
  48. Lonsdale D, Pautasso M, Holdenreider O (2008) Wood-decaying fungi in the forest: conservation needs and management options. Eur J For Res 127:1–22CrossRefGoogle Scholar
  49. Lorimer CG, White AS (2003) Scale and frequency of natural disturbances in the northeastern US: implications for early successional forest habitats and regional age distributions. For Ecol Manag 185:41–64CrossRefGoogle Scholar
  50. Marchant R (2002) Do rare species have any place in multivariate analysis for bioassessment? J N Am Benthol Soc 21:311–313CrossRefGoogle Scholar
  51. Maser C, Anderson RG, Cromack K, Williams JT, Martin RE (1979) Dead and down woody material In: Thomas JW (ed) Wildlife habitats in managed forests of the Blue Mountains of Oregon and Washington. USDA Forest Service Agricultural Handbook 553, Washington DC, pp 78–95Google Scholar
  52. McCune B, Mefford MJ (2011) PC-ORD. Multivariate analysis of ecological data. Version 6.0. MjM Software, Gleneden Beach, ORGoogle Scholar
  53. McGee GG, Leopold DJ, Nyland RD (1999) Structural characteristics of old-growth, maturing, and partially cut northern hardwood forests. Ecol Appl 9:1316–1329CrossRefGoogle Scholar
  54. Müller J, Engel H, Blaschke M (2007) Assemblages of wood-inhabiting fungi related to silvicultural management intensity in beech forests in southern Germany. Eur J For Res 126:513–527CrossRefGoogle Scholar
  55. Nordén B, Ryberg M, Götmark F, Olausson B (2004) Relative importance of coarse and fine woody debris for the diversity of wood-inhabiting fungi in temperate broadleaf forests. Biol Conserv 117:1–10CrossRefGoogle Scholar
  56. Nordén B, Gotmark F, Ryberg M, Paltto H, Allmer J (2008) Partial cutting reduces species richness of fungi on woody debris in oak-rich forests. Can J For Res 38:1807–1816CrossRefGoogle Scholar
  57. Nordén B, Penttilá R, Siitonen J, Tomppo E, Ovaskainen O (2013) Specialist species of wood-inhabiting fungi struggle while generalists thrive in fragmented boreal forests. J Ecol 101:701–712CrossRefGoogle Scholar
  58. Olsson J, Jonsson BG, Hjalten J, Ericson L (2011) Addition of coarse woody debris—the early fungal succession on Picea abies logs in managed forests and reserves. Biol Conserv 144:1100–1110CrossRefGoogle Scholar
  59. Pasanen H, Junninen K, Kouki J (2014) Restoring dead wood in forests diversifies wood-decaying fungal assemblages but does not quickly benefit red-listed species. For Ecol Manag 312:92–100CrossRefGoogle Scholar
  60. Poos MS, Jackson DA (2012) Addressing the removal of rare species in multivariate bioassessments: the impact of methodological choices. Ecol Indic 18:82–90CrossRefGoogle Scholar
  61. Rhemtulla JM, Mladenoff DJ, Clayton MK (2007) Regional land-cover conversion in the U.S. upper Midwest: magnitude of change and limited recovery (1850–1935–1993). Landscape Ecol 22:57–75CrossRefGoogle Scholar
  62. Robert V, Stegehuis G, Stalpers J (2005) The MycoBank engine and related databases. http://www.mycobank.org. Accessed 10 July 2013
  63. Rooney TP, Waller DM (2003) Direct and indirect effects of white-tailed deer in forest ecosystems. For Ecol Manag 181:165–176CrossRefGoogle Scholar
  64. Runkle JR (1982) Patterns of disturbance in some old-growth mesic forests of eastern North America. Ecology 63:1533–1546CrossRefGoogle Scholar
  65. Rydin H, Diekmann M, Hallingback T (1997) Biological characteristics, habitat associations, and distribution of macrofungi in Sweden. Conserv Biol 11:628–640CrossRefGoogle Scholar
  66. Sanders HL (1968) Marine benthic diversity: a comparative study. Am Nat 102:243–282CrossRefGoogle Scholar
  67. Sippola AL, Lehesvirta T, Renvall P (2001) Effects of selective logging on coarse woody debris and diversity of wood-decaying polypores in eastern Finland. Ecol Bull 49:243–254Google Scholar
  68. Stokland J, Kauserud H (2004) Phellinus nigrolimitatus—a wood-decomposing fungus highly influenced by forestry. For Ecol Manag 187:333–343CrossRefGoogle Scholar
  69. Stokland JN, Larsson K-H (2011) Legacies from natural forest dynamics: different effects of forest management on wood-inhabiting fungi in pine and spruce forests. For Ecol Manag 261:1707–1721CrossRefGoogle Scholar
  70. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRefGoogle Scholar
  71. Taylor FH (1956) Variation in sugar content of maple sap. University of Vermont and State Agricultural College Experiment Station: Bulletin 587Google Scholar
  72. Toivanen T, Markkanen A, Kotiaho JS, Halme P (2012) The effect of forest fuel harvesting on the fungal diversity of clear-cuts. Biomass Bioenergy 39:84–93CrossRefGoogle Scholar
  73. Van Sickle J, Larsen DP, Hawkins CP (2007) Exclusion of rare taxa affects performance of the O/E index in bioassessments. J N Am Benthol Soc 26:319–331CrossRefGoogle Scholar
  74. Worrall JJ, Lee TD, Harrington TC (2005) Forest dynamics and agents that initiate and expand canopy gaps in Picea-Abies forests of Crawford Notch, New Hampshire, USA. J Ecol 93:178–190CrossRefGoogle Scholar
  75. Ylisirnio A-L, Pentilla R, Berglund H, Hallikainen V, Isaeva L, Hauhanen H, Koivula M, Mikkola K (2012) Dead wood and polypore diversity in natural post-fire succession forests and managed stands: lessons for biodiversity management in boreal forests. For Ecol Manag 286:16–27CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht (out side the USA) 2014

Authors and Affiliations

  • Nicholas J. Brazee
    • 1
  • Daniel L. Lindner
    • 2
  • Anthony W. D’Amato
    • 3
  • Shawn Fraver
    • 4
  • Jodi A. Forrester
    • 5
  • David J. Mladenoff
    • 5
  1. 1.Center for AgricultureUniversity of MassachusettsAmherstUSA
  2. 2.USDA Forest Service, Northern Research StationCenter for Forest Mycology ResearchMadisonUSA
  3. 3.Department of Forest ResourcesUniversity of MinnesotaSt. PaulUSA
  4. 4.School of Forest ResourcesUniversity of MaineOronoUSA
  5. 5.Department of Forest and Wildlife EcologyUniversity of WisconsinMadisonUSA

Personalised recommendations