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Spatial scales of variation in lichens: implications for sampling design in biomonitoring surveys

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Abstract

The variability of biological data is a main constraint affecting the quality and reliability of lichen biomonitoring surveys for estimation of the effects of atmospheric pollution. Although most epiphytic lichen bioindication surveys focus on between-site differences at the landscape level, associated with the large scale effects of atmospheric pollution, current protocols are based on multilevel sampling, thus adding further sources of variation and affecting the error budget. We test the hypothesis that assemblages of lichen communities vary at each spatial scale examined, in order to determine what scales should be included in future monitoring studies. We compared four sites in Italy, along gradients of atmospheric pollution and climate, to test the partitioning of the variance components of lichen diversity across spatial scales (from trunks to landscapes). Despite environmental heterogeneity, we observed comparable spatial variance. However, residuals often overcame between-plot variability, leading to biased estimation of atmospheric pollution effects.

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References

  • Anderson, M. J. (2001a). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32–46.

    Google Scholar 

  • Anderson, M. J. (2001b). Permutation tests for univariate or multivariate analysis of variance and regression. Canadian Journal of Fisheries and Aquatic Sciences, 58, 626–639.

    Article  Google Scholar 

  • Anderson, M. J., & ter Braak, C. J. F. (2003). Permutation tests for multi-factorial analysis of variance. Journal of Statistical Computation and Simulation, 73, 85–113.

    Article  Google Scholar 

  • ANPA. (2001). I.B.L.: Indice di Biodiversità Lichenica. Serie Manuali e Linee Guida, 2/2001. Roma: ANPA.

    Google Scholar 

  • Asta, J., Erhardt, W., Ferretti, M., Fornasier, F., Kirschbaum, U., Nimis, P. L., et al. (2002). Mapping lichen diversity as an indicator of environmental quality. In P. L. Nimis, C. Scheidegger, & P. Wolseley (Eds.), Monitoring with lichens—monitoring lichens (pp. 273–279). Dordrecht: Kluwer.

    Chapter  Google Scholar 

  • Balata, D., Bertocci, I., Piazzi, L., & Nesti, U. (2008). Comparison between epiphyte assemblages of leaves and rhizomes of the seagrass Posidonia oceanica subjected to different levels of anthropogenic eutrophication. Estuarine, Coastal and Shelf Science, 79, 533–540.

    Article  Google Scholar 

  • Balestri, E., Cinelli, F. & Lardicci, C. (2003). Spatial variation in Poseidonia oceanica structural, morphological and dynamic features in a northwestern Mediterranean coastal area: a multi-scale analysis. Marine Ecology Progress Series, 250, 51–60.

    Google Scholar 

  • Botkin, D. B. (1990). Discordant harmonies: a new ecology for the twenty-first century. Oxford: Oxford University Press.

    Google Scholar 

  • Branquinho, C., Gaio-Oliveira, G., Augusto, S., Pinho, P., Maguas, C., & Correia, O. (2008). Biomonitoring spatial and temporal impact of atmospheric dust from a cement industry. Environmental Pollution, 151, 292–299.

    Article  CAS  Google Scholar 

  • Brunialti, G., & Giordani, P. (2003). Variability of lichen diversity in a climatically heterogeneous area (Liguria, NW Italy). The Lichenologist, 35, 55–69.

    Article  Google Scholar 

  • Brunialti, G., Frati, L., Incerti, G., Rizzi, G., Vinci, M., & Giordani, P. (2009). Lichen biomonitoring of air pollution: issues for applications in complex environments. In G. C. Romano & A. G. Conti (Eds.), Air quality in the 21st century (pp. 211–259). Hauppauge: Nova.

    Google Scholar 

  • Cao, Y., Bark, A. W., & Williams, P. (1997). A comparison of clustering methods for river benthic community analysis. Hydrobiologia, 347, 25–40.

    Article  CAS  Google Scholar 

  • Cristofolini, F., Giordani, P., Gottardini, E., & Modenesi, P. (2008). The response of epiphytic lichens to air pollution and subsets of ecological predictors: a case study from the Italian Prealps. Environmental Pollution, 151, 308–317.

    Article  CAS  Google Scholar 

  • Davies, L., Bates, J. W., Bell, J. N. B., James, P. W., & Purvis, O. W. (2007). Diversity and sensitivity of epiphytes to oxides of nitrogen in London. Environmental Pollution, 146, 299–310.

    Article  CAS  Google Scholar 

  • Dungan, J. L., Perry, J. N., Dale, M. R. T., Legendre, P., Citron-Pousty, S., Fortin, M. J., et al. (2002). A balanced view of scale in spatial statistical analysis. Ecography, 25, 626–640.

    Article  Google Scholar 

  • Ellis, C. J. (2011). Lichen epiphyte diversity: a species, community and trait-based review. Perspectives in Plant Ecology, Evolution and Systematics. doi:10.1016/j.ppees.2011.10.001

  • Ferretti, M., & Erhardt, W. (2002). Key issues in designing biomonitoring programs. Monitoring scenarios, sampling strategies and quality assurance. In P. L. Nimis, C. Scheidegger, & P. Wolseley (Eds.), Monitoring with lichens—monitoring lichens (pp. 111–139). London: Kluwer.

    Chapter  Google Scholar 

  • Ferretti, M., Brambilla, E., Brunialti, G., Fornasier, F., Mazzali, C., Giordani, P., et al. (2004). Reliability of different sampling densities for estimating and mapping lichen diversity in biomonitoring studies. Environmental Pollution, 127, 249–256.

    Article  CAS  Google Scholar 

  • Frati, L., & Brunialti, G. (2006). Long-term biomonitoring with lichens: comparing data from different sampling procedures. Environmental Monitoring and Assessment, 119, 391–404.

    Article  CAS  Google Scholar 

  • Frati, L., Santoni, S., Nicolardi, V., Gaggi, C., Brunialti, G., Guttova, A., et al. (2007). Lichen biomonitoring of ammonia emission and nitrogen deposition around a pig stockfarm. Environmental Pollution, 146, 311–316.

    Article  CAS  Google Scholar 

  • Gaston, K. J. (2000). Global patterns in biodiversity. Nature, 405, 220–227.

    Article  CAS  Google Scholar 

  • Geiser, L. H., & Neitlich, P. N. (2007). Pollution and climate gradients in western Oregon and Washington indicated by epiphytic macrolichens. Environmental Pollution, 145, 203–218.

    Article  CAS  Google Scholar 

  • Giordani, P. (2006). Variables influencing the distribution of epiphytic lichens in heterogeneous areas: a case study for Liguria, NW Italy. Journal of Vegetation Science, 17, 195–206.

    Article  Google Scholar 

  • Giordani, P. (2012). Assessing the effects of forest management on epiphytic lichens in coppiced forests using different indicators. Plant Biosystems. doi:10.1080/11263504.2011.654136

  • Giordani, P., Brunialti, G., & Alleteo, D. (2002). Effects of atmospheric pollution on lichen biodiversity (LB) in a Mediterranean region (Liguria, northwest Italy). Environmental Pollution, 118, 53–64.

    Article  CAS  Google Scholar 

  • Giordani, P., Calatayud, V., Stofer, S., Granke, O. (2011). Epiphytic lichen diversity in relation to atmospheric deposition. In Fischer R, Lorenz M (eds.). 2011: forest condition in Europe, 2011 Technical Report of ICP Forests and FutMon. Work Report of the Institute for World Forestry 2011/1. ICP Forests, Hamburg, 2011, 212 pp

  • Gunnar, J. B., & Moen, J. (1998). Patterns in species associations in plant communities: the importance of scale. Journal of Vegetation Science, 9, 327–332.

    Google Scholar 

  • ISPRA (2008). BRACE. Dati e Metadati di Qualità dell’aria. ISPRA

  • Jovan, S., & McCune, B. (2005). Air-quality bioindication in the greater central valley of California, with epiphytic macrolichen communities. Ecological Applications, 15, 1712–1726.

    Article  Google Scholar 

  • Jovan, S., & McCune, B. (2006). Using epiphytic macrolichen communities for biomonitoring ammonia in forests of the greater Sierra Nevada, California. Water, Air, and Soil Pollution, 170, 69–93.

    Article  CAS  Google Scholar 

  • Levin, S. A. (1992). The problem of pattern and scale in ecology. Ecology, 73, 1943–1967.

    Article  Google Scholar 

  • McArdle, B. H., & Anderson, M. J. (2001). Fitting multivariate models to semi-metric distances: a comment on distance-based redundancy analysis. Ecology, 82, 290–297.

    Article  Google Scholar 

  • Nascimbene, J., Nimis, P. L., & Marini, L. (2007). Testing indicators of epiphytic lichen diversity: a case study in N Italy. Biodiversity and Conservation, 16, 3377–3386.

    Article  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, 250–256.

    Article  Google Scholar 

  • Nimis, P. L. & Martellos, S. (2008). ITALIC—the information system on Italian Lichens. Version 4.0.

  • Nimis, P. L., Scheidegger, C., & Wolseley, P. A. (2002). Monitoring with lichens—monitoring lichens. Dordrecht: Kluwer. Published in association with the NATO Scientific Affairs Division.

    Book  Google Scholar 

  • Palmer, M. W. (1990). Spatial scale and patterns of vegetation, flora and species richness in hardwood forests of the north Carolina Piedmont. Coenoses, 5, 89–96.

  • Pinho, P., Augusto, S., Branquinho, C., Bio, A., Pereira, M. J., Soares, A., & Catarino, F. (2004). Mapping lichen diversity as a first step for air quality assessment. Journal of Atmospheric Chemistry, 49, 377–389.

    Article  CAS  Google Scholar 

  • Pinho, P., Augusto, S., Maguas, C., Pereira, M. J., Soares, A., & Branquinho, C. (2008). Impact of neighbourhood land-cover in epiphytic lichen diversity: analysis of multiple factors working at different spatial scales. Environmental Pollution, 151, 414–422.

    Article  CAS  Google Scholar 

  • Pirintsos, S. A., Diamantopoulos, J., & Stamou, G. P. (1993). Analysis of the vertical distribution of epiphytic lichens on Pinus nigra. Vegetatio, 109, 63–70.

    Article  Google Scholar 

  • Pirintsos, S. A., Diamantopoulos, J., & Stamou, G. P. (1995). Analysis of the distribution of epiphytic lichens within homogeneous Fagus sylvatica stands along an altitudinal gradient (Mount Olympos, Greece). Vegetatio, 116, 33–40.

    Google Scholar 

  • Purvis, A., & Hector, A. (2000). Getting the measure of biodiversity. Nature, 405, 212–219.

    Article  CAS  Google Scholar 

  • Purvis, O. W., Chimonides, P. J., Joness, G. C., Mikhailova, I. N., Spiro, B., Weiss, D. J., et al. (2004). Lichen biomonitoring near Karabash Smelter Town, Ural Mountains, Russia, one of the most polluted areas in the world. Proceedings of the Royal Society B: Biological Sciences, 271, 221–226.

    Article  Google Scholar 

  • Saipunkaew, W., Wolseley, P. A., Chimonides, P. J., & Boonpragob, K. (2007). Epiphytic macrolichens as indicators of environmental alteration in northern Thailand. Environmental Pollution, 146, 366–374.

    Article  CAS  Google Scholar 

  • Seaward, M. R. D., & Letrouit-Galinou, M. A. (1991). Lichen recolonization of trees in the Jardin du Luxembourg, Paris. The Lichenologist, 23, 181–186.

    Article  Google Scholar 

  • Stofer, S., Bergamini, A., Aragon, G., Carvalho, P., Coppins, B. J., Davey, S., et al. (2006). Species richness of lichen functional groups in relation to land use intensity. The Lichenologist, 38, 331–353.

    Article  Google Scholar 

  • Tarrassón, L. & Nyíri, À. (Eds.) (2008). Transboundary Acidification, Eutrophication and Ground Level Ozone. in Europe in 2006. EMEP Status Report 2008/1. ISSN 1504-6109.

  • Underwood, A. J., & Chapman, M. G. (1996). Scales of spatial patterns of distribution of intertidal invertebrates. Oecologia, 107, 212–224.

    Article  Google Scholar 

  • Underwood, A.J., Chapman, M.G. & Connell, S.D. (2000). Observations in ecology: you can’t make progress on processes without understanding the patterns. Journal of Experimental Marine Biology and Ecology, 250, 97–115.

    Google Scholar 

  • Van Dobben, H. F., & Ter Braak, C. J. F. (1998). Effects of atmospheric NH3 on epiphytic lichens in the Netherlands: the pitfalls of biological monitoring. Atmospheric Environment, 32, 551–557.

    Article  Google Scholar 

  • van Dobben, H. F., Wolterbeek, H. T., Wamelink, G. W. W., & Ter Braak, C. J. F. (2001). Relationship between epiphytic lichens, trace elements and gaseous atmospheric pollutants. Environmental Pollution, 112, 163–169.

    Article  Google Scholar 

  • van Herk, C. M. (1999). Mapping of ammonia pollution with epiphytic lichens in The Netherlands. The Lichenologist, 31, 9–20.

    Article  Google Scholar 

  • van Herk, C. M., Mathijssen-Spiekman, A. M. E., & de Zwart, D. (2003). Long distance nitrogen air pollution effects on lichens in Europe. The Lichenologist, 35, 347–359.

    Article  Google Scholar 

  • Will-Wolf, S., Geiser, L. H., Neitlich, P., & Reis, A. H. (2006). Forest lichen communities and environment—how consistent are relationships across scales? Journal of Vegetation Science, 17, 171–184.

    Google Scholar 

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Acknowledgments

This study was partially funded by CESI S.p.A. and Edipower S.p.A. We are grateful to Dr. Maurizio Perotti and Dr. Francesca Deperis for technical support and data management.

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Correspondence to Paolo Giordani.

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Giordani, P., Brunialti, G., Frati, L. et al. Spatial scales of variation in lichens: implications for sampling design in biomonitoring surveys. Environ Monit Assess 185, 1567–1576 (2013). https://doi.org/10.1007/s10661-012-2651-8

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