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The inclusion of overlooked lichen microhabitats in standardized forest biodiversity monitoring

Published online by Cambridge University Press:  19 March 2018

Arsen GASPARYAN
Affiliation:
Botanischer Garten und Botanisches Museum, Freie Universität, Berlin, Germany. Email: a.gasparyan@bgbm.org; agasparyan@wwfcaucasus.org WWF-Armenia, Yerevan, Republic of Armenia
Harrie J. M. SIPMAN
Affiliation:
Botanischer Garten und Botanisches Museum, Freie Universität, Berlin, Germany. Email: a.gasparyan@bgbm.org; agasparyan@wwfcaucasus.org
Lorenzo MARINI
Affiliation:
Department of Agronomy, Food, Natural Resources, Animals and the Environment (DAFNAE), University of Padova, Padova, Italy
Juri NASCIMBENE
Affiliation:
Department of Biological, Geological and Environmental Sciences, University of Bologna, Bologna, Italy

Abstract

Epiphytic lichens are increasingly included in forest biodiversity monitoring schemes, but most of the standardized guidelines consider only lichens colonizing a small part of tree trunks (1·0–1·5 m) and overlook other important microhabitats, such as fallen branches and stumps. In this paper, we present results of a small-scale pilot study to evaluate the possible advantage of including four distinct microhabitats in standardized procedures for assessing epiphytic lichen diversity. Trunk bases, trunks between 100 and 150 cm above the ground, stumps, and fallen branches were each sampled with a different standardized sampling method along a forest age gradient in temperate deciduous forests of the Caucasian region. Plot-level species richness was contrasted between the standardized sampling procedures of different substrata and a non-probabilistic floristic sampling. The interactions between sampling procedure and stand age were analysed using linear mixed models, and non-metric multidimensional scaling (NMDS) and multi-response permutation procedures (MRPP) were used for comparing species composition. Overall, 97 species were recorded, their richness increasing with increasing stand age. Results were consistent across the gradient of stand age and demonstrated that the adoption of standardized sampling procedures which include stumps and fallen branches in addition to tree trunks would increase the capability of maximizing species capture. This approach would allow researchers to evaluate lichen patterns by simultaneously considering the response of different communities sensitive to different stand-related factors. Despite the likelihood that a non-probabilistic floristic survey would give a more exhaustive picture of the plot-level lichen diversity, standardized sampling procedures that include tree trunks, fallen branches and stumps are likely to represent a reasonable trade-off between exhaustiveness and cost-effectiveness.

Type
Articles
Copyright
© British Lichen Society, 2018 

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References

Asta, J., Erhardt, W., Ferretti, M., Fornasier, F., Kirschbaum, U., Nimis, P. L., Purvis, O. W., Pirintsos, S., Scheidegger, C., Van Haluwyn, C., et al. (2002) Mapping lichen diversity as an indicator of environmental quality. In Monitoring with Lichens – Monitoring Lichens (P. L. Nimis, C. Scheidegger & P. A. Wolseley, eds): 273279. Dordrecht: Kluwer Academic Publishers.Google Scholar
Blasi, C., Marchetti, M., Chiavetta, U., Aleffi, M., Audisio, P., Azzella, M. M., Brunialti, G., Capotorti, G., Del Vico, E., Lattanzi, E., et al. (2010) Multi-taxon and forest structure sampling for identification of indicators and monitoring of old-growth forest. Plant Biosystems 144: 160170.Google Scholar
Blasy, V. & Ellis, C. J. (2014) Life on deadwood: cut stumps as a model system for the succession and management of lichen diversity. Lichenologist 46: 455469.Google Scholar
Boch, S., Müller, J., Prati, D., Blaser, S. & Fischer, M. (2013) Up in the tree – the overlooked richness of bryophytes and lichens in tree crowns. PLoS ONE 8: e84913.Google Scholar
Cristofolini, F., Brunialti, G., Giordani, P., Nascimbene, J., Cristofori, A., Gottardini, E., Frati, L., Matos, P., Batič, F., Caporale, S., et al. (2014) Towards the adoption of an international standard for biomonitoring with lichens – consistency of assessment performed by experts from six European countries. Ecological Indicators 45: 6367.Google Scholar
Ellis, C. J. (2012) Lichen epiphyte diversity: a species, community and trait-based review. Perspectives in Plant Ecology, Evolution and Systematics 14: 131152.Google Scholar
Fritz, Ö. (2009) Vertical distribution of epiphytic bryophytes and lichens emphasizes the importance of old beeches in conservation. Biodiversity Conservation 18: 289304.Google Scholar
Galloway, D. J. (1992) Biodiversity: a lichenological perspective. Biodiversity Conservation 1: 312323.Google Scholar
Gao, T., Nielsen, A. B. & Hedblom, M. (2015) Reviewing the strength of evidence of biodiversity indicators for forest ecosystems in Europe. Ecological Indicators 57: 420434.Google Scholar
Giordani, P., Brunialti, G., Benesperi, R., Rizzi, G., Frati, L. & Modenesi, P. (2009) Rapid biodiversity assessment in lichen biomonitoring surveys: implications for quality assurance. Journal of Environmental Monitoring 11: 730735.CrossRefGoogle Scholar
Li, S., Liu, W. Y., Li, D. W., Song, L., Shi, X. M. & Lu, H. Z. (2015) Species richness and vertical stratification of epiphytic lichens in subtropical primary and secondary forests in southwest China. Fungal Ecology 17: 3040.Google Scholar
Lie, M. H., 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. Biodiversity Conservation 18: 35793596.Google Scholar
Marmor, L., Tõrra, T., Saag, L., Leppik, E. & Randlane, T. (2013) Lichens on Picea abies and Pinus sylvestris – from tree bottom to the top. Lichenologist 45: 5163.Google Scholar
McCune, B. (2000) Lichen communities as indicators of forest health. Bryologist 103: 353356.Google Scholar
McCune, B. & Grace, J. B. (2002) Analysis of Ecological Communities. Gleneden Beach, Oregon: MjM Software.Google Scholar
McCune, B. & Lesica, P. (1992) The trade-off between species capture and quantitative accuracy in ecological inventory of lichens and bryophytes in forests in Montana. Bryologist 95: 296304.Google Scholar
McCune, B. & Mefford, M. J. (1999) PC-ORD. Multivariate Analysis of Ecological Data. Version 4.0. Gleneden Beach: MjM Software.Google Scholar
McCune, B., Amsberry, K. A., Camacho, F. J., Clery, S., Cole, C., Emerson, C., Felder, G., French, P., Greene, D., Harris, R., et al. (1997) Vertical profile of epiphytes in a Pacific Northwest old-growth forest. Northwest Science 71: 145152.Google Scholar
Ministry of Nature Protection (2008) Management plan of the Noyemberyan forestry. Yerevan, Armenia.Google Scholar
Nascimbene, J. & Marini, L. (2015) Epiphytic lichen diversity along elevational gradients: biological traits reveal a complex response to water and energy. Journal of Biogeography 42: 12221232.Google Scholar
Nascimbene, J., Marini, L., Caniglia, G., Cester, D. & Nimis, P. L. (2008 a) Lichen diversity on stumps in relation to wood decay in subalpine forests of Northern Italy. Biodiversity Conservation 17: 26612670.Google Scholar
Nascimbene, J., Marini, L., Motta, R. & Nimis, P. L. (2008 b) Lichen diversity of coarse woody habitats in a Pinus-Larix stand in the Italian Alps. Lichenologist 40: 153163.Google Scholar
Nascimbene, J., Marini, L., Motta, R. & Nimis, P. L. (2009) Influence of tree age, tree size and crown structure on lichen communities in mature Alpine spruce forests. Biodiversity Conservation 18: 15091522.Google Scholar
Nascimbene, J., Marini, L., Bacaro, G. & Nimis, P. L. (2010) Effect of reduction in sampling effort for monitoring epiphytic lichen diversity in forests. Community Ecology 11: 250256.Google Scholar
Orange, A., James, P. W. & White, F. J. (2010) Microchemical Methods for the Identification of Lichens, 2nd edn. London: British Lichen Society.Google Scholar
Ozanne, C. M. P., Anhuf, D., Boulter, S. L., Keller, M., Kitching, R. L., Körner, C., Meinzer, F. C., Mitchell, A. W., Nakashizuka, T., Silva Dias, P. L., et al. (2003) Biodiversity meets the atmosphere: a global view of forest canopies. Science 30: 183186.Google Scholar
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team (2016) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-127. Available at: http://CRAN.R-project.org/package=nlme.Google Scholar
Puumalainen, J., Kennedy, P. & Folving, S. (2003) Monitoring forest biodiversity: a European perspective with reference to temperate and boreal forest zone. Journal of Environmental Management 67: 514.Google Scholar
R Core Team (2015) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/.Google Scholar
Scheidegger, C., Groner, U., Keller, C. & Stofer, S. (2002) Biodiversity assessment tools — lichens. In Monitoring with Lichens – Monitoring Lichens (P. L. Nimis, C. Scheidegger & P. A. Wolseley, eds):273279. Dordrecht: Kluwer Academic Publishers.Google Scholar
Siitonen, J., Martikainen, P., Punttila, P. & Rauh, J. (2000) Coarse woody debris and stand characteristics in mature managed and old-growth boreal mesic forests in southern Finland. Forest Ecology Management 128: 211225.Google Scholar
Smith, C. W., Aptroot, A., Coppins, B. J., Fletcher, A., Gilbert, O. L., James, P. W. & Wolseley, P. A. (eds) (2009) The Lichens of Great Britain and Ireland. London: British Lichen Society.Google Scholar
Spribille, T., Thor, G., Bunnell, F. L., Goward, T. & Björk, C. R. (2008) Lichens on dead wood: species-substrate relationships in the epiphytic lichen floras of the Pacific Northwest and Fennoscandia. Ecography 31: 741750.Google Scholar
Stofer, S. (2006) Working Report Forest BIOTA ‒ Epiphytic Lichen Monitoring. Available at: http://www.forestbiota.org/docs/report_lichens_20060503.pdf.Google Scholar
Stofer, S., Calatayud, V., Ferretti, M., Fischer, R., Giordani, P., Keller, C., Stapper, N. & Scheidegger, C. (2003) Epiphytic lichen monitoring within the EU/ICP Forests Biodiversity Test-Phase on Level II plots. Available at: www.forestbiota.org.Google Scholar
Stofer, S., Calatayud, V., Giordani, P. & Neville, P. (2012) Assessment of epiphytic lichen diversity. Manual part VII. In Manual on Methods and Criteria for Harmonized Sampling, Assessment, Monitoring and Analysis of the Effects of Air Pollution on Forests. Hamburg: UNECE ICP Forests Programme Co-ordinating Centre. Available at: http://www.icp-forests.org/Manual.htm Google Scholar
Travaglini, D., Barbati, A., Chirici, G., Lombardi, F., Marchetti, M. & Corona, P. (2007) ForestBIOTA data on deadwood monitoring in Europe. Plant Biosystems 2: 222230.Google Scholar
Welsh, H. H. & Droege, S. (2001) A case for using Plethodontid salamanders for monitoring biodiversity and ecosystem integrity of North American forests. Conservation Biology 15: 558569.Google Scholar