Skip to main content

Advertisement

Log in

Dispersal ecology of the endangered woodland lichen Lobaria pulmonaria in managed hemiboreal forest landscape

  • Original paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Changes in the forest management practices have strongly influenced the distribution of species inhabiting old-growth forests. The epiphytic woodland lichen Lobaria pulmonaria is frequently used as a model species to study the factors affecting the population biology of lichens. We sampled 252 L. pulmonaria individuals from 12 populations representing three woodland types differing in their ecological continuity and management intensity in Estonia. We used eight mycobiont-specific microsatellite loci to quantify genetic diversity among the populations. We calculated the Sørensen distance to estimate genetic dissimilarity among individuals within populations. We revealed that L. pulmonaria populations have significantly higher genetic diversity in old-growth forests than in managed forests and wooded meadows. We detected a significant woodland-type-specific pattern of genetic dissimilarity among neighbouring L. pulmonaria individuals, which suggests that in wooded meadows and managed forests dominating is vegetative reproduction. The vegetative dispersal distance between the host trees of L. pulmonaria was found to be only 15–30 m. Genetic dissimilarity among individuals was also dependent on tree species and trunk diameter. Lobaria pulmonaria populations in managed forests included less juveniles compared to old-growth forests and wooded meadows, indicating that forest management influences life stage structure within populations. We conclude that as intensive stand management reduces the genetic diversity of threatened species in woodland habitats, particular attention should be paid to the preservation of remnant populations in old-growth habitats. Within managed habitats, conservation management should target on maintenance of the stand’s structural diversity and availability of potential host trees.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

NE:

Northeast

SW:

Southwest

References

  • Adermann V (2008) Estonian forests 2007. The estimation of forest sources by statistical sampling methodology. Metsakaitse- ja Metsauuenduskeskus, Tallinn

    Google Scholar 

  • Andersson L, Appelqvist T (1987) Lobaria pulmonaria and Gyalecta ulmi as indicators of deciduous woodland with high nature qualities. Svensk Bot Tidskr 81:185–194

    Google Scholar 

  • Andersson L, Martverk R, Külvik M et al (2003) Woodland key habitat inventory in Estonia 1999–2002. Regio Publishing, Tartu

    Google Scholar 

  • Arnaud-Haond S, Belkhir K (2007) GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Mol Ecol Notes 7:15–17

    Article  CAS  Google Scholar 

  • Asplund J, Gauslaa Y (2008) Mollusc grazing limits growth and early development of the old forest lichen Lobaria pulmonaria in broadleaved deciduous forests. Oecologia 155:93–99

    Article  PubMed  Google Scholar 

  • Belinchón R, Martínez I, Otálora MAG et al (2009) Fragment quality and matrix affect epiphytic performance in a Mediterranean forest landscape. Am J Bot 96:1974–1982

    Article  PubMed  Google Scholar 

  • Büdel B, Scheidegger C (2008) Thallus morphology and anatomy. In: Nash TH (ed) Lichen biology. University Press, Cambridge, pp 40–68

    Chapter  Google Scholar 

  • Campbell J, Fredeen AL (2004) Lobaria pulmonaria abundance as an indicator of macrolichen diversity in Interior Cedar-Hemlock forests of east-central British Columbia. Can J Bot 82:970–982

    Article  Google Scholar 

  • Carlsson R, Nilsson K (2009) Status of the red-listed lichen Lobaria pulmonaria on the Åland Islands, SW Finland. Ann Bot Fennici 46:549–554

    Google Scholar 

  • Edman M, Eriksson A-M, Villard M-A (2008) Effects of selection cutting on the abundance and fertility of indicator lichens Lobaria pulmonaria and Lobaria quercizans. J Appl Ecol 45:26–33

    Article  Google Scholar 

  • Etverk I, Sein H (1995) Forests and their management. In: Raukas A (ed) Estonian nature. Valgus and Eesti Entsüklopeediakirjastus, Tallinn, pp 402–416

    Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  • Gaggiotti OE (1996) Population genetic models of source–sink metapopulations. Theor Pop Biol 50:178–208

    Article  Google Scholar 

  • Gauslaa Y (1985) The ecology of Lobarion pulmonariae and Parmelion caperatae in Quercus dominated forests in south-west Norway. Lichenologist 17:117–140

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Gu WD, Kuusinen M, Konttinen T et al (2001) Spatial pattern in the occurrence of the lichen Lobaria pulmonaria in managed and virgin boreal forests. Ecography 24:139–150

    Article  Google Scholar 

  • Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer Associates, Sunderland

    Google Scholar 

  • James PW, Hawksworth DL, Rose F (1977) Lichen communities in the British Isles: a preliminary conspectus. In: Seaward MRD (ed) Lichen ecology. Academic, London, pp 295–413

    Google Scholar 

  • Jüriado I, Liira J (2009) Distribution and habitat ecology of the threatened forest lichen Lobaria pulmonaria in Estonia. Folia Cryptog Estonica 46:55–65

    Google Scholar 

  • Jüriado I, Liira J (2010) Threatened forest lichen Lobaria pulmonaria—its past, present and future in Estonia. For Stud 53:15–24

    Google Scholar 

  • Kalwij JM, Wagner HH, Scheidegger C (2005) Effects of stand-level disturbance events on the spatial distribution of a lichen indicator of forest conservation value. Ecol Appl 15:2015–2024

    Article  Google Scholar 

  • Kohv K, Liira J (2005) Anthropogenic disturbances, structural changes and indicators in the boreal forest. Scan J For Res 20:122–134

    Article  Google Scholar 

  • Kukk T, Kull K (1997) Wooded meadows. Estonia Marit 2:1–249

    Google Scholar 

  • Kukk T, Sammul M (2006) Area of seminatural Natura 2000 habitat types in Estonia. In: Sammul M (ed) Year-book of the Estonian Naturalists’ Society. Estonian Naturalists’ Society, Tartu, pp 114–158

    Google Scholar 

  • Laasimer L (1965) Vegetation of the Estonian S.S.R. Valgus, Tallinn

    Google Scholar 

  • Laasimer L, Masing V (1995) Flora and plant cover. In: Raukas A (ed) Estonian nature. Valgus and Eesti Entsüklopeediakirjastus, Tallinn, pp 364–401

    Google Scholar 

  • Leppik E, Jüriado I (2008) Factors important for epiphytic lichen communities in wooded meadows of Estonia. Folia Cryptog Estonica 44:75–87

    Google Scholar 

  • Leppik E, Jüriado I, Liira J (2011) Changes in stand structure due to the cessation of traditional land use in wooded meadows impoverish epiphytic lichen communities. Lichenologist 43:257–274

    Article  Google Scholar 

  • Liira J, Sepp T (2009) Indicators of structural and habitat natural quality in boreo-nemoral forests along the management gradient. Ann Bot Fennici 46:308–325

    Google Scholar 

  • McCune B, Mefford MJ (1999) PC-ORD. Multivariate analysis of ecological data, version 4. MjM Software Design, Gleneden Beach

    Google Scholar 

  • Nascimbene J, Caniglia G, Nicli M et al (2006) Populations of Lobaria pulmonaria (L.) Hoffm. in the Cansiglio Regional Forest (Veneto, Pre-Alps, north-east Italy): distribution, diversity and conservation issues. Plant Biosyst 140:34–42

    Article  Google Scholar 

  • Nascimbene J, Brunialti G, Ravera S et al (2010) Testing Lobaria pulmonaria (L.) Hoffm. as an indicator of lichen conservation importance of Italian forests. Ecol Indicat 10:353–360

    Article  Google Scholar 

  • Nilsson S, Arup U, Baranowski R et al (1995) Tree-dependent lichens and beetles as indicators in conservation forests. Conserv Biol 9:1208–1215

    Article  Google Scholar 

  • Öckinger E, Nilsson SG (2010) Local population extinction and vitality of an epiphytic lichen in fragmented old-growth forest. Ecology 91:2100–2109

    Article  PubMed  Google Scholar 

  • Öckinger E, Niklasson M, Nilsson SG (2005) Is local distribution of the epiphytic lichen Lobaria pulmonaria limited by dispersal capacity or habitat quality? Biodiv Conserv 14:759–773

    Article  Google Scholar 

  • Otálora MAG, Martínez I, Belinchón R et al (2011) Remnant fragments preserve genetic diversity of the old forest lichen Lobaria pulmonaria in a fragmented Mediterranean mountain forest. Biodivers Conserv. doi:10.1007/s10531-011-0025-0

  • Päretel M, Helm A, Roosaluste E, Zobel M (2007) Biological diversity of Estonian semi-natural grassland ecosystems. In: Punning J-M (ed) Problems of contemporary environmental studies, vol 10. Tallinna Ülikooli Ökoloogia Instituut, Tallinn, pp 223–302

  • Peakall R, Smouse PE (2005) GenAlEx 6: genetic analysis in excel. Population genetic software for teaching and research. The Australian National University, Canberra

    Google Scholar 

  • Richardson DHS, Cameron RP (2004) Cyanolichens: their response to pollution and possible management strategies for their conservation in northeastern North America. Northeast Nat 11:1–22

    Article  Google Scholar 

  • Riiali A, Penttinen A, Kuusinen M (2001) Bayesian mapping of lichens growing on trees. Biom J 43:717–736

    Article  Google Scholar 

  • Rose F (1976) Lichenological indicators of age and environmental continuity in woodlands. In: Brown DH, Hawksworth DL, Bailey RH (eds) Lichenology: progress and problems. Academic, London, pp 279–307

    Google Scholar 

  • Scheidegger C (1995) Early development of transplanted isidioid soredia of Lobaria pulmonaria in an endangered population. Lichenologist 27:361–374

    Google Scholar 

  • Scheidegger C, Goward T (2002) Monitoring lichens for conservation: red lists and conservation action plans. In: Nimis PL, Scheidegger C, Wolseley PA (eds) Monitoring with lichens—monitoring lichens, Nato Science Series. IV. Earth and environmental sciences. Kluwer Academic Publishers, Dordrecht, pp 163–181

    Google Scholar 

  • Scheidegger C, Werth S (2009) Conservation strategies for lichens: insights from population biology. Fungal Biol Rev 23:55–66

    Article  Google Scholar 

  • Scheidegger C, Frey B, Zoller S (1995) Transplantation of symbiotic propagules and thallus fragments: methods for the conservation of threatened epiphytic lichen populations. Mitteilungen der Eidgenössishen Forschungsanstalt für Wald, Schnee und Landschaft 70:41–62

    Google Scholar 

  • Scheidegger C, Frey B, Walser J C (1998) Reintroduction and augmentation of populations of the endangered Lobaria pulmonaria: methods and concepts. In: Kondratyuk SJ, Coppins B (eds) Lobarion lichens as indicators of the primeval forests of the Eastern Carpathians (Darwin International Workshop, 25–30 May 1998, Kostrino, Ukraine). Phytosociocentre, Kiev, pp 33–52

  • StatSoft Inc (2005) Statistica for Windows, ver 8.1. StatSoft, Inc, Tulsa

    Google Scholar 

  • Wagner HH, Werth S, Kalwij JM et al (2006) Modelling forest recolonization by an epiphytic lichen using a landscape genetic approach. Landsc Ecol 21:849–865

    Article  Google Scholar 

  • Walser J-C (2004) Molecular evidence for limited dispersal of vegetative propagules in the epiphytic lichen Lobaria pulmonaria. Am J Bot 91:1273–1276

    Article  Google Scholar 

  • Walser J-C, Sperisen C, Soliva M et al (2003) Fungus-specific microsatellite primers of lichens: application for the assessment of genetic variation on different spatial scales in Lobaria pulmonaria. Fungal Genet Biol 40:72–82

    Article  PubMed  CAS  Google Scholar 

  • Walser J-C, Gugerli F, Holderegger R et al (2004) Recombination and clonal propagation in different populations of the lichen Lobaria pulmonaria. Heredity 93:322–329

    Article  PubMed  CAS  Google Scholar 

  • Werth S (2010a) Optimal sample sizes and allelic diversity in studies of the genetic variability of mycobiont and photobiont populations. Lichenologist 43:73–81

    Article  Google Scholar 

  • Werth S (2010b) Population genetics of lichen-forming fungi—a review. Lichenologist 42:499–519

    Article  Google Scholar 

  • Werth S, Wagner HH, Gugerli F et al (2006a) Quantifying dispersal and establishment limitation in a population of epiphytic lichen. Ecology 87:2037–2046

    Article  PubMed  Google Scholar 

  • Werth S, Wagner HH, Holderegger R et al (2006b) Effect of disturbances on the genetic diversity of an old-forest associated lichen. Mol Ecol 15:911–921

    Article  PubMed  CAS  Google Scholar 

  • Werth S, Gugerli F, Holderegger R et al (2007) Landscape-level gene flow in Lobaria pulmonaria, an epiphytic lichen. Mol Ecol 16:2807–2815

    Article  PubMed  Google Scholar 

  • Widmer I, Dal Grande F, Cornejo C et al (2010) Highly variable microsatellite markers for the fungal and algal symbionts of the lichen Lobaria pulmonaria and challenges in developing biont-specific molecular markers for fungal associations. Fungal Biol 114:538–544

    Article  PubMed  CAS  Google Scholar 

  • Wolseley P, James P (2000) Factors affecting changes in species of Lobaria in sites across Britain 1986–1998. For Snow Landsc Res 75:319–338

    Google Scholar 

  • Yoshimura I (1998) Lung lichens and their vegetation in Japan and the other regions. In: Kondratyuk SJ, Coppins B (eds) Lobarion lichens as indicators of the primeval forests of the Eastern Carpathians (Darwin International Workshop, 25–30 May 1998, Kostrino, Ukraine). Phytosociocentre, Kiev, pp 53–63

  • Zoller S, Lutzoni F, Scheidegger C (1999) Genetic variation within and among populations of the threatened lichen Lobaria pulmonaria in Switzerland and implications for its conservation. Mol Ecol 8:2049–2059

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors are thankful to the administration of the Nigula Nature Reserve for kind help during field work. The Genetic Diversity Centre of ETH Zürich (GDC) provided facilities for data collection. We are grateful to Asko Lõhmus and the anonymous reviewers for valuable comments on the manuscript. Ester Jaigma is acknowledged for revising the English text of the manuscript. Financial support was received from the Swiss National Science Foundation (SNF 3100A0-10583 to CS), the Estonian Science Foundation (grants 7878 and 7816), the Ministry of Education and Research of Estonia (targeted financing SF0180012s09 and SF0180153s08), the EEA Financial Mechanism (grant EMP9, 08066N) and the European Union through the European Regional Development Fund (FIBIR Centre of Excellence).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Inga Jüriado.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jüriado, I., Liira, J., Csencsics, D. et al. Dispersal ecology of the endangered woodland lichen Lobaria pulmonaria in managed hemiboreal forest landscape. Biodivers Conserv 20, 1803–1819 (2011). https://doi.org/10.1007/s10531-011-0062-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-011-0062-8

Keywords

Navigation