Biodiversity and Conservation

, Volume 26, Issue 11, pp 2547–2567 | Cite as

Will forest conservation areas protect functionally important diversity of fungi and lichens over time?

  • Mari T. JönssonEmail author
  • Alejandro Ruete
  • Olle Kellner
  • Urban Gunnarsson
  • Tord Snäll
Original Paper


Incorporating functional values in biodiversity monitoring systems could add novel perspectives of the status of biodiversity in conservation areas. Stable frequencies of large foliose nitrogen-fixing cyanolichens likely have positive effects on the nitrogen budget of forests and provide food, material and shelter for invertebrates, gastropods and birds. Stable volumes of deadwood and frequencies of associated fungi provide an important supporting function for ecosystem services such as nutrient cycling, carbon storage and soil formation. Based on regional monitoring data from boreal old-growth forest nature reserves and key habitats, we tested for changes in the frequency of various functionally important substrates and species over time. We detected significant reductions in the frequency of indicator cyanolichens occurring on deciduous trees already after 10 years in key habitats, despite non-significant changes in their host substrates. Frequencies of indicator pendulous lichens Alectoria sarmentosa and Bryoria nadvornikiana had also decreased in key habitats, despite overall stable volumes of large conifer host trees. Lichen reductions were more pronounced in the smaller key habitats compared to the larger formally protected nature reserves, likely due to degrading fragmentation and isolation effects. In contrast to these lichens, the average frequencies of old-growth forest indicator fungi decaying coniferous deadwood and common fungi on deciduous trees (Fomes fomentarius) and coniferous trees (Fomitopsis pinicola) remained unchanged. The studied cyanolichens and fruiting fungi generally had similar extinction rates over 10 years, whilst only cyanolichens had substantially lower colonization rates. Amid a severely fragmented landscape, conservation areas seem to struggle in preserving some of the basic old-growth forest values.


Biomonitoring Cryptogams Ecosystem function Functional groups Indicator species Protected areas 



Many thanks to all that have participated in the field work: Annika Forsslund, Stefan Henriksson, Anders Johansson, Fredrik Jonsson, Sebastian Kirppu, Ulrika Nordin, Elin Hultman and Ville Pokela. We are grateful to Bengt-Gunnar Jonsson, Anders Dahlberg, Håkan Berglund, Panu Halme, and one anonymous reviewer whose comments helped us improve the manuscript. The study was funded by the Swedish Forest Society (Skogssällskapet), the Swedish Environmental Protection Agency (Naturvårdsverket), and the Faculty of Natural Resources and Agricultural Sciences, SLU.

Supplementary material

10531_2015_1035_MOESM1_ESM.docx (40 kb)
Supplementary material 1 (DOCX 41 kb)


  1. Akçakaya HR, Sjögren-Gulve P (2000) Population viability analysis in conservation planning: an overview. Ecol Bull 48:9–21Google Scholar
  2. Antoine ME (2004) An ecophysiological approach to quantifying nitrogen fixation by Lobaria oregano. Bryologist 107:82–87CrossRefGoogle Scholar
  3. Armstrong RA, Welch AR (2007) Competition in lichen communities. Symbiosis 43:1–12Google Scholar
  4. Artdatabanken (2015) Rödlistade arter i Sverige 2015. Artdatabanken SLU, UppsalaGoogle Scholar
  5. Asplund J, Larsson P, Vatne S et al (2010) Gastropod grazing shapes the vertical distribution of epiphytic lichens in forest canopies. J Ecol 98:218–225CrossRefGoogle Scholar
  6. Aune K, Jonsson BG, Moen J (2005) Isolation and edge effects among woodland key habitats in Sweden: is forest policy promoting fragmentation? Biol Conserv 124:89–95CrossRefGoogle Scholar
  7. Balvanera P, Pfisterer AB, Buchmann N et al (2006) Quantifying the evidence for forest biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156CrossRefPubMedGoogle Scholar
  8. Berglund H, Jonsson BG (2005) Verifying an extinction debt among lichens and fungi in northern Swedish boreal forests. Conserv Biol 19:338–348CrossRefGoogle Scholar
  9. Brooks TM, Bakarr MI, Boucher T et al (2004) Coverage provided by the global protected-area system: is it enough? Bioscience 54:1081–1091CrossRefGoogle Scholar
  10. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer Verlag, New YorkGoogle Scholar
  11. Butchart SHM, Walpole M, Collen B et al (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168CrossRefPubMedGoogle Scholar
  12. Cardinale BJ, Matulich KL, Hooper DU et al (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:572–592CrossRefPubMedGoogle Scholar
  13. Chan KMA, Shaw MR, Cameron DR et al (2006) Conservation planning for ecosystem services. PLoS Biol 4:2138–2152Google Scholar
  14. 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
  15. De Bello F, Lavorel S, Díaz S et al (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893CrossRefGoogle Scholar
  16. Diaz S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655CrossRefGoogle Scholar
  17. Edman M, Jönsson M, Jonsson BG (2007) Small-scale fungal- and wind-mediated disturbances strongly influence the temporal availability of logs in an old-growth Picea abies forest. Ecol Appl 170:482–490CrossRefGoogle Scholar
  18. Egoh B, Rouget M, Reyers B, Knight AT, Cowling RM et al (2007) Integrating ecosystem services into conservation assessments: a review. Ecol Econ 63:714–721CrossRefGoogle Scholar
  19. Ellis CJ (2012) Lichen epiphyte diversity: a species, community and trait-based review. Perspect Plant Ecol 14:131–152CrossRefGoogle Scholar
  20. Ellis CJ, Coppins BJ (2007) Changing climate and historic-woodland structure interact to control species diversity of the ‘Lobarion’ epiphyte community in Scotland. J Veg Sci 18:725–734CrossRefGoogle Scholar
  21. Esseen PA, Renhorn KE (1998) Mass loss of epiphytic lichen litter in a boreal forest. Ann Bot Fenn 35:211–217Google Scholar
  22. Esseen PA, Renhorn KE, Petersson RB (1996) Epiphytic lichen biomass in managed and old-growth boreal forests: effect of branch quality. Ecol Appl 6:228–238CrossRefGoogle Scholar
  23. Essen PA (2006) Edge influence on the old-growth forest indicator lichen Alectoria sarmentosa in natural ecotones. J Veg Sci 17:185–194Google Scholar
  24. Fedrowitz K, Kuusinen M, Snäll T (2012) Metapopulation dynamics and future persistence of epiphytic cyanolichens in a European boreal forest ecosystem. J Appl Ecol 49:493–502CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gamfeldt L, Snäll T, Bagchi R, Jonsson M, Gustafsson L, Kjellander P, Ruiz-Jaen MC, Fröberg M, Stendahl J, Philipson CD, Mikusiński G, Andersson E, Westerlund B, Andrén H, Moberg F, Moen J, Bengtsson J (2013) Higher levels of multiple ecosystem services are found in forests with more tree species. Nat Commun 4:1340CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gärdenfors U (2010) The 2010 red list of Swedish species. Swedish Species Information Centre in Cooperation with Swedish Environmental Protection Agency, UppsalaGoogle Scholar
  27. Gauslaa Y, Palmqvist K, Solhaug KA et al (2007) Growth of epiphytic old forest lichens at regional and successional scales. Can J For Res 37:1832–1845CrossRefGoogle Scholar
  28. Geldmann J, Barnes M, Coad L et al (2013) Effectiveness of terrestrial protected areas in reducing habitat loss and population declines. Biol Conserv 161:230–238CrossRefGoogle Scholar
  29. Gunnarsson B, Hake M, Hultengren S (2004) A functional relationship between species richness of spiders and lichens in spruce. Biodivers Conserv 13:685–693CrossRefGoogle Scholar
  30. Halme P, Mönkkönen M, Kotiaho JS et al (2009) Quantifying the indicator power of an indicator species. Conserv Biol 23:1008–1016CrossRefPubMedGoogle Scholar
  31. Hansen K, Malmaeus M, Lindblad M (2014) Ekosystemtjänster i svenska skogar. IVL Rapport B2190Google Scholar
  32. Hedwall P-O, Mikusiński G (2015) Structural changes in protected forests in Sweden: implications for conservation functionality. Can J For Res 45:1–10CrossRefGoogle Scholar
  33. Heilmann-Clausen J, Barron ES, Boddy L et al (2015) A fungal perspective on conservation biology. Conserv Biol 29:61–68CrossRefPubMedGoogle Scholar
  34. Jacobs JM, Work TT (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. Janisch JE, Harmon ME (2002) Successional changes in live and dead wood carbon stores: implications for net ecosystem productivity. Tree Physiol 22:77–89CrossRefPubMedGoogle Scholar
  36. Jenkins CN, Joppa L (2009) Expansion of the global terrestrial protected area system. Biol Conserv 142:2166–2174CrossRefGoogle Scholar
  37. Jönsson MT, Fraver S, Jonsson BG (2009) Forest history and the development of old-growth characteristics in fragmented boreal forests. J Veg Sci 20:91–106CrossRefGoogle Scholar
  38. Junninen K, Komonen A (2011) Conservation ecology of boreal polypores: a review. Biol Conserv 144:11–20CrossRefGoogle Scholar
  39. Jüriado I, Liira J, Paal J et al (2009) Tree and stand level variables influencing diversity of lichens on temperate broad-leaved trees in boreo-nemoral floodplain forests. Biodivers Conserv 18:105–125CrossRefGoogle Scholar
  40. Kivinen S, Moen J, Berg A et al (2010) Effects of modern forest management on winter grazing resources for reindeer in Sweden. Ambio 39:269–278CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kouki J, Arnold K, Martikainen P (2004) Long-term persistence of aspen—a key host for many threatened species—is endangered in old-growth conservation areas in Finland. J Nat Conserv 12:41–52CrossRefGoogle Scholar
  42. Kuusinen M (1994) Epiphytic lichen diversity on Salix caprea in old-growth southern and middle boreal forests of Finland. Ann Bot Fenn 31:77–92Google Scholar
  43. Larsson P, Gauslaa Y (2011) Rapid juvenile development in old forest lichens. Botany 89:65–72CrossRefGoogle Scholar
  44. Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol 16:545–556CrossRefGoogle Scholar
  45. Lie MH, Arup U, Grytnes JA et al (2009) The importance of host tree age, size and growth rate as determinants of epiphytic lichen diversity in boreal forests. Biodivers Conserv 18:3579–3596CrossRefGoogle Scholar
  46. Lindenmayer DB, Laurance WF, Franklin JF (2012) Global decline in large old trees. Science 338:1305–1306CrossRefPubMedGoogle Scholar
  47. Lindenmayer DB, Laurance WF, Franklin JF et al (2014) New policies for old trees: averting a global crisis in a keystone ecological structure. Conserv Lett 7:61–69CrossRefGoogle Scholar
  48. Löbel S, Snäll T, Rydin H (2006) Species richness patterns and metapopulation processes—evidence from epiphyte communities in boreo-nemoral forests. Ecography 29:169–182CrossRefGoogle Scholar
  49. Marmor L, Tõrra T, Saag L et al (2012) Species richness of epiphytic lichens in coniferous forests: the effect of canopy openness. Ann Bot Fenn 49:352–358CrossRefGoogle Scholar
  50. McCarthy J (2001) Gap dynamics of forest trees: a review with particular attention to boreal forests. Environ Rev 9:1–59CrossRefGoogle Scholar
  51. McCune B, Rosentreter R, Ponzetti JM et al (2000) Epiphyte habitats in an old conifer forest in western Washington, U.S.A. Bryologist 103:417–427CrossRefGoogle Scholar
  52. Millennium Ecosystem Assessment (2005) Ecosystems and human well-being: synthesis. In: Reid WV (ed). Island Press, Washington, DCGoogle Scholar
  53. Moning C, Werth S, Dziock F et al (2009) Lichen diversity in temperate montane forests is influenced by forest structure more than climate. For Ecol Manag 258:745–751CrossRefGoogle Scholar
  54. Nitare J (2000) Indicator species for assessing the nature conservation value of woodland sites—a flora of selected cryptogams. Skogsstyrelsen, Jönköping (In Swedish with English summary) Google Scholar
  55. Nitare J (2011) Barrskogar - Nyckelbiotoper i Sverige. Skogsstyrelsen, Jönköping (In Swedish)Google Scholar
  56. Nordén B, Paltto H, Claesson C et al (2012) Partial cutting can enhance epiphyte conservation in temperate oak-rich forests. For Ecol Manag 270:35–44CrossRefGoogle Scholar
  57. Nordén J, Penttilä R, Siitonen J et al (2013) Specialist species of wood-inhabiting fungi struggle while generalists thrive in fragmented boreal forests. J Ecol 101:701–712CrossRefGoogle Scholar
  58. Norén M, Hultgren B, Nitare J et al (1995) Instruktion för datainsamling vid inventering av nyckelbiotoper. Skogsstyrelsen, Jönköping (In Swedish) Google Scholar
  59. Öckinger E, Nilsson SG (2010) Local population extinction and vitality of an epiphytic lichen in old-growth forest fragments. Ecology 91:2100–2109CrossRefPubMedGoogle Scholar
  60. Ottosson E, Nordén J, Dahlberg A et al (2014) Species associations during the succession of wood-inhabiting fungal communities. Fungal Ecol 11:17–28CrossRefGoogle Scholar
  61. Perhans K, Gustafsson L, Jonsson F et al (2007) Bryophytes and lichens in different types of forest set-asides in boreal Sweden. For Ecol Manag 242:374–390CrossRefGoogle Scholar
  62. Pettersson RB, Ball JP, Renhorn KE et al (1995) Invertebrate communities in boreal forest canopies as influenced by forestry and lichens with implications for passerine birds. Biol Conserv 74:57–63CrossRefGoogle Scholar
  63. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  64. Roberge JM, Bengtsson SBK, Wulff S et al (2011) Edge creation and tree dieback influence the patch-tracking metapopulation dynamics of a red-listed epiphytic bryophyte. J Ecol 48:650–658Google Scholar
  65. Rodrigues ASL (2006) Are global conservation efforts successful? Science 313:1051–1052CrossRefPubMedGoogle Scholar
  66. Rudolphi J, Jönsson MT, Gustafsson L (2014) Biological legacies buffer local species extinction after logging. J Appl Ecol 51:53–62CrossRefPubMedGoogle Scholar
  67. Siitonen J (2001) Forest management, coarse woody debris and saproxylic organisms: fennoscandian boreal forests as an example. Ecol Bull 49:11–41Google Scholar
  68. Sillett SC, Antoine ME (2004) Lichens and bryophytes in forest canopies. In: Lowman MD, Rinker HB (eds) Forest canopies, 2nd edn. Academic Press, San Diego, pp 151–174CrossRefGoogle Scholar
  69. Sillett SC, McCune B, Peck JE et al (2000) Dispersal limitations of epiphytic lichens result in species dependent on old-growth forests. Ecol Appl 10:789–799CrossRefGoogle Scholar
  70. Smalian L (1837) Beitrag zur Holzmesskunst. Stralsund, GermanyGoogle Scholar
  71. Snäll T, Jonsson BG (2001) Edge effects on six polyporous fungi used as old-growth indicatorsin Swedish boreal forest. Ecol Bull 49:255–262Google Scholar
  72. Snäll T, Ehrlén J, Rydin H (2005) Modelling epiphyte metapopulation dynamics in a dynamic forest landscape. Oikos 109:209–222CrossRefGoogle Scholar
  73. Söderberg U (1992) Funktioner för skogsindelning. Höjd, formhöjd och barktjocklek för enskilda träd. Rapport nr. 52. Institutionen för skogstaxering. Sveriges Lantbruksuniversitet. (In Swedish)Google Scholar
  74. Stokland JN, Siitonen J, Jonsson BG (2012) Biodiversity in dead wood. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  75. Tilman D (2001) Functional diversity. In: Levin SA (ed) Encyclopedia of biodiversity, 3rd edn. Academic Press, San Diego, pp 109–120CrossRefGoogle Scholar
  76. Tilman D, May RM, Lehman CL et al (1994) Habitat destruction and the extinction debt. Nature 371:65–66CrossRefGoogle Scholar
  77. Timonen J, Siitonen J, Gustafsson L et al (2010) Woodland key habitats in northern Europe: concepts, inventory and protection. Scand J For Res 25:309–324CrossRefGoogle Scholar
  78. Timonen J, Gustafsson L, Kotiaho JS et al (2011) Hotspots in cold climate: conservation value of woodland key habitats in boreal forests. Biol Conserv 144:2061–2067CrossRefGoogle Scholar
  79. Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892CrossRefGoogle Scholar
  80. Wardle DA, Jonsson M (2010) Biodiversity effects in real ecosystems—a response to Duffy. Front Ecol Environ 8:10–11CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Mari T. Jönsson
    • 1
    Email author
  • Alejandro Ruete
    • 1
  • Olle Kellner
    • 2
  • Urban Gunnarsson
    • 3
  • Tord Snäll
    • 1
  1. 1.Swedish Species Information CentreSwedish University of Agricultural Sciences (SLU)UppsalaSweden
  2. 2.County Administrative Board of GävleborgGävleSweden
  3. 3.County Administrative Board of DalarnaFalunSweden

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