BG Biogeosciences BG 1726-4189 Copernicus GmbH Göttingen, Germany 10.5194/bg-9-1205-2012 Critical loads of nitrogen deposition and critical levels of atmospheric ammonia for semi-natural Mediterranean evergreen woodlands Pinho P. 1 2 Theobald M. R. 3 4 Dias T. 1 Tang Y. S. 4 Cruz C. 1 Martins-Loução M. A. 1 5 Máguas C. 1 Sutton M. 4 Branquinho C. 1 Universidade de Lisboa, Faculdade de Ciências, Centre for Environmental Biology, Lisboa, Portugal Centre for Natural Resources and the Environment, Instituto Superior Técnico, Universidade Técnica de Lisboa, Portugal Dept. Agricultural Chemistry and Analysis, E.T.S.I. Agrónomos, Technical University of Madrid, Spain Centre for Ecology and Hydrology, Edinburgh Research Station, Edinburgh, UK Universidade de Lisboa, Museu Nacional de História Natural, Jardim Botânico, Lisboa, Portugal 28 03 2012 9 3 1205 1215 This is an open-access article ditributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. This article is available from http://www.biogeosciences.net/9/1205/2012/bg-9-1205-2012.html The full text article is available as a PDF file from http://www.biogeosciences.net/9/1205/2012/bg-9-1205-2012.pdf

Nitrogen (N) has emerged in recent years as a key factor associated with global changes, with impacts on biodiversity, ecosystems functioning and human health. In order to ameliorate the effects of excessive N, safety thresholds such as critical loads (deposition fluxes) and levels (concentrations) can be established. Few studies have assessed these thresholds for semi-natural Mediterranean ecosystems. Our objective was therefore to determine the critical loads of N deposition and long-term critical levels of atmospheric ammonia for semi-natural Mediterranean evergreen woodlands. We have considered changes in epiphytic lichen communities, one of the most sensitive comunity indicators of excessive N in the atmosphere. Based on a classification of lichen species according to their tolerance to N we grouped species into response functional groups, which we used as a tool to determine the critical loads and levels. This was done for a Mediterranean climate in evergreen cork-oak woodlands, based on the relation between lichen functional diversity and modelled N deposition for critical loads and measured annual atmospheric ammonia concentrations for critical levels, evaluated downwind from a reduced N source (a cattle barn). Modelling the highly significant relationship between lichen functional groups and annual atmospheric ammonia concentration showed the critical level to be below 1.9 μg m<sup>−3</sup>, in agreement with recent studies for other ecosystems. Modelling the highly significant relationship between lichen functional groups and N deposition showed that the critical load was lower than 26 kg (N) ha<sup>−1</sup> yr<sup>−1</sup>, which is within the upper range established for other semi-natural ecosystems. Taking into account the high sensitivity of lichen communities to excessive N, these values should aid development of policies to protect Mediterranean woodlands from the initial effects of excessive N.

 References Adrizal, A., Patterson, P. H., Hulet, R. M., Bates, R. M., Myers, C. A. B., Martin, G., Shockey, R. L., Van der Grinten, M., Anderson, D. A., and Thompson, J. R.: Vegetative Buffers for Fan Emissions from Poultry Farms: 2. Ammonia, Dust and Foliar Nitrogen, J. Environ. Sci. Health Part B-Pestic. Contam. Agric. Wastes, 43, 96–103, 2008. Aragon, G., Martinez, I., Izquierdo, P., Belinchon, R., and Escudero, A.: Effects of Forest Management on Epiphytic Lichen Diversity in Mediterranean Forests, Appl. Veg. Sci., 13, 183–194, 2010. Asta, J., Erhardt, W., Ferretti, M., Fornasier, F., Kirschbaum, U., Nimis, P.L., Purvis, O. W., Pirintsos, S., Scheidegger, C., van Haluwyn, C., and Wirth, V.: Mapping Lichen Diversity as an Indicator of Environmental Quality, in: Monitoring with Lichens- Monitoring Lichens, edited by: Nimis, P. L., Scheidegger, C., and Wolseley P. A., Kluwer Academic Publisher, 2002. Augusto, S., Maguas, C., Matos, J., Pereira, M. J., Soares, A., and Branquinho, C.: Spatial Modeling of Pahs in Lichens for Fingerprinting of Multisource Atmospheric Pollution, Environ. Sci. Technol., 43, 7762–7769, 2009. Blondel, J. and Aronson, J.: Biology and Wildlife of the Mediterranean Region, Oxford University Press, New York, 1999. Bobbink, R., Hicks, K., Galloway, J., Spranger, T., Alkemade, R., Ashmore, M., Bustamante, M., Cinderby, S., Davidson, E., Dentener, F., Emmett, B., Erisman, J:W., Fenn, M., Gilliam, F., Nordin, A., Pardo, L., and De Vries, W.: Global Assessment of Nitrogen Deposition Effects on Terrestrial Plant Diversity: A Synthesis, Ecol. Appl., 20, 30–59, 2010. Bobbink, R., Braun, S., Nordin, A., Power, S., Schütz, K., Strengbom, J., Weijters, M., and Tomassen, M.: Review and Revision of Empirical Critical Loads and Dose-Response Relationships, Coordination Centre for Effects, National Institute for Public Health and the Environment (RIVM), The Netherlands, 2011. Bonanomi, G., Caporaso, S., and Allegrezza, M.: Short-Term Effects of Nitrogen Enrichment, Litter Removal and Cutting on a Mediterranean Grassland, Acta Oecol.-Int. J. Ecol., 30, 419–425, 2006. Branquinho, C., Gaio-Oliveira, G., Augusto, S., Pinho, P., Maguas, C., and Correia, O.: Biomonitoring Spatial and Temporal Impact of Atmospheric Dust from a Cement Industry, Environ. Pollut., 151, 292–299, 2008. Bugalho, M. N., Caldeira, M. C., Pereira, J. S., Aronson, J., and Pausas, J. G.: Mediterranean cork oak savannas require human use to sustain biodiversity and ecosystem services, Front. Ecol. Environ., 9, 278–286, 2011. Calvo, L., Alonso, I., Fernandez, A. J., and De Luis, E.: Short-Term Study of Effects of Fertilisation and Cutting Treatments on the Vegetation Dynamics of Mountain Heathlands in Spain, Plant Ecol., 179, 181–191, 2005. Cape, J. N., van der Eerden, L. J., Sheppard, L. J., Leith, I. D., and Sutton, M. A.: Evidence for Changing the Critical Level for Ammonia, Environ. Pollut., 157, 1033–1037, 2009. Cruz, C. and Martins-Loução, M. A.: Determination of Ammonium Concentrations in Soils and Plant Extracts, in: Nitrogen in a Sustainable Ecosystem: From the Cell to the Plant, edited by: Martins-Loução M. A. and Lips, S.H., Backhuys Publishers, 2000. Davies, E. D., Moss, D., and Hill, M. O.: Eunis Habitat Classification Revised, European Environment Agency, European topic centre on nature protection and biodiversity, 2004. Dias, T., Malveiro, S., Martins-Loucao, M. A., Sheppard, L. J., and Cruz, C.: Linking N-Driven Biodiversity Changes with Soil N Availability in a Mediterranean Ecosystem, Plant Soil, 341, 125–136, 2011. Dragosits, U., Theobald, M. R., Place, C. J., Lord, E., Webb, J., Hill, J., ApSimon, H. M., and Sutton, M. A.: Ammonia Emission, Deposition and Impact Assessment at the Field Scale: A Case Study of Sub-Grid Spatial Variability, Environ. Pollut., 117, 147–158, 2002. EEA, European Environment Agency: Emep/Corinair Emission Inventory Guidebook, 2007. Erisman, J. W., Sutton, M. A., Galloway, J., Klimont, Z., and Winiwarter, W.: How a Century of Ammonia Synthesis Changed the World, Nat. Geosci., 1, 636–639, 2008. Ellis, E. C.: Anthropogenic transformation of the terrestrial biosphere, Philos. Trans. R. Soc. A-Math. Phys. Eng. Sci. , 369, 1010–1035, 2011. Ellis, E. C. and Ramankutty, N.: Putting people in the map: anthropogenic biomes of the world, Front. Ecol. Environ., 6, 439–447, 2008. Farina, A., Santolini, R., Pagliaro, G., Scozzafava, S., and Schipani, I.: Eco-semiotics: A new field of competence for ecology to overcome the frontier between environmental complexity and human culture in the Mediterranean, Isr. J. Plant Sci., 53, 167–175, 2005. Feest, A. and Spanos, K.: An approach to measuring biodiversity and its use in analysing the effect of nitrogen deposition on woodland butterfly populations in the Netherlands, IForest-biogeosciences and forestry, 2, 46–48, 2009. Fenn, M. E., Geiser, L., Bachman, R., Blubaugh, T. J., and Bytnerowicz, A.: Atmospheric Deposition Inputs and Effects on Lichen Chemistry and Indicator Species in the Columbia River Gorge, Usa, Environ. Pollut., 146, 77–91, 2007. Fenn, M. E., Jovan, S., Yuan, F., Geiser, L., Meixner, T., and Gimeno, B. S.: Empirical and Simulated Critical Loads for Nitrogen Deposition in California Mixed Conifer Forests, Environ. Pollut., 155, 492–511, 2008. Fenn, M. E., Allen, E. B., Weiss, S. B., Jovan, S., Geiser, L. H., Tonnesen, G. S., Johnson, R. F., Rao, L. E., Gimeno, B. S., Yuan, F., Meixner, T., and Bytnerowicz, A.: Nitrogen Critical Loads and Management Alternatives for N-Impacted Ecosystems in California, J. Environ. Manage., 91, 2404–2423, 2010. Flechard, C. R. and Fowler, D.: Atmospheric ammonia at a moorland site. II: Long-term surface-atmosphere micrometeorological flux measurements. Q. J. Roy. Meteorol. Soc., 124, 759–791, 1998. Fowler, D., Pitcairn, C. E. R., Sutton, M. A., Flechard, C., Loubet, B., Coyle, M., and Munro, R. C.: The Mass Budget of Atmospheric Ammonia in Woodland within 1 Km of Livestock Buildings, Environ. Pollut., 102, 343–348, 1998. Frati, L., Santoni, S., Nicolardi, V., Gaggi, C., Brunialti, G., Guttova, A., Gaudino, S., Pati, A., Pirintsos, S. A., and Loppi, S.: Lichen Biomonitoring of Ammonia Emission and Nitrogen Deposition around a Pig Stockfarm, Environ. Pollut., 146, 311–316, 2007. Gaio-Oliveira, G., Dahlman, L., Palmqvist, K., Martins-Loucao, M., and Maguas, C.: Nitrogen Uptake in Relation to Excess Supply and Its Effects on the Lichens Evernia Prunastri (L.) Ach and Xanthoria Parietina (L.) Th. Fr, Planta, 220, 794–803, 2005. Galloway, J. N., Aber, J. D., Erisman, J. W., Seitzinger, S. P., Howarth, R. W., Cowling, E. B., and Cosby, B. J.: The Nitrogen Cascade, Bioscience, 53, 341–356, 2003. Geiser, L., Jovan, S., Glavich, D., and Porter, M.: Lichen based critical loads for atmospheric nitrogen deposition in Western Oregon and Washington Forests,USA. Environ. Pollut., 158, 2412–2421, 2010. Giordani, P.: Is the Diversity of Epiphytic Lichens a Reliable Indicator of Air Pollution? A Case Study from Italy, Environ. Pollut., 146, 317–323, 2007. Giordani, P. and Incerti, G.: The Influence of Climate on the Distribution of Lichens: A Case Study in a Borderline Area (Liguria, Nw Italy), Plant Ecol., 195, 257–272, 2008. Hallsworth, S., Dore, A. J., Bealey, W. I., Dragosits, U., Vieno, M., Hellsten, S., Tang, Y. S., and Sutton, M. A.: The Role of Indicator Choice in Quantifying the Threat of Atmospheric Ammonia to the "Natura 2000" Network, Environ. Sci. Policy, 13, 671–687, 2010. Hao, X. Y., Benke, M. B., Chang, C., Janzen, H. H., Clayton, G. W., and Hill, B. R.: Spatial Pattern of Ammonia Sorption by Soil and Vegetation Downwind of a Beef Feedlot, Agric. Ecosyst. Environ., 132, 39–47, 2009. Hauck, M.: Ammonium and Nitrate Tolerance in Lichens, Environ. Pollut., 158, 1127–1133, 2010. Lavorel, S. and Garnier, E.: Predicting Changes in Community Composition and Ecosystem Functioning from Plant Traits: Revisiting the Holy Grail, Funct. Ecol., 16, 545–556, 2002. Loppi, S. and Pirintsos, S. A.: Effect of Dust on Epiphytic Lichen Vegetation in the Mediterranean Area (Italy and Greece), Isr. J. Plant Sci., 48, 91–95, 2000. Manning, P., Newington, J. E., Robson, H. R., Saunders, M., Eggers, T., Bradford, M. A., Bardgett, R. D., Bonkowski, M., Ellis, R. J., Gange, A. C., Grayston, S. J., Kandeler, E., Marhan, S., Reid, E., Tscherko, D., Godfray, H. C. J., and Rees, M.: Decoupling the Direct and Indirect Effects of Nitrogen Deposition on Ecosystem Function, Ecol. Lett., 9, 1015–1024, 2006. McCulloch, R. B., Few, G. S., Murray, G. C., and Aneja, V. P.: Analysis of Ammonia, Ammonium Aerosols and Acid Gases in the Atmosphere at a Commercial Hog Farm in Eastern North Carolina, Usa, Environ. Pollut., 102, 263–268, 1998. Mittermeier, R. A., Gil, P. R., Hoffman, M., Pilgrim, J., Brooks, T., Cristina Goettsch Mittermeier, Lamoreux, J., and da Fonseca, G. A. B.: Hotspots Revisited - Earth's Biologically Richest and Most Endangered Terrestrial Ecoregions, Conservation International and CEMEX, Mexico City, pp 392, 2005. Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B., and Kent, J.: Biodiversity hotspots for conservation priorities, Nature, 403, 853–858, 2000. Nilsson, J. and Grennfelt, P.: Critical Loads for Sulphur and Nitrogen, in: Report from a Workshop Held at Skokloster, edited by: Nilsson, J. and Grennfelt, P., Sweden, Nordic Council of Ministers, 1988. Nimis, P. L., and Martellos, S.: Italic – the Information System on Italian Lichens V. 4.0, University of Trieste, Dept. of Biology, IN4.0/1, available at:~http://dbiodbs.univ.trieste.it, 2008. Ochoa-Hueso, R., Allen, E. B., Branquinho, C., Cruz, C., Dias, T., Fenn, M. A., Manrique, E., Pérez-Corona, E., Sheppard, L. J., and Stock, W. D.: Nitrogen Deposition Effects on Mediterranean-Type Ecosystems: An Ecological Assessment, Environ. Pollut., 159, 14, http://dx.doi.org/10.1016/j.envpol.2010.12.019doi:10.1016/j.envpol.2010.12.019, 2011. Paoli, L., Pirintsos, S. A., Kotzabasis, K., Pisani, T., Navakoudis, E., and Loppi, S.: Effects of Ammonia from Livestock Farming on Lichen Photosynthesis, Environ. Pollut., 158, 2258–2265, 2010. Paracchini, M. L., Petersen, J. E., Hoogeveen, Y., Bamps, C., Burfield, I., and van-Swaay, C.: 2008. High Nature Value Farmland in Europe – An Estimate of the Distribution Patterns on the Basis of Land Cover and Biodiversity Data, EUR – Scientific and Technical Research series, Joint Research Centre – Institute for Environment and Sustainability, Luxembourg, pp. 87, 2008. Pardo, L. H., Robin-Abbott, M. J., and Driscoll, C. T. (Eds).: Assessment of Nitrogen deposition effects and empirical critical loads of Nitrogen for ecoregions of the United States, Report NRS-80, US Department of Agriculture, Forest Service, Northern Research Station, 2011. Pinho, P., Augusto, S., Branquinho, C., Bio, A., Pereira, M. J., Soares, A., and Catarino, F.: Mapping Lichen Diversity as a First Step for Air Quality Assessment, J. Atmos. Chem., 49, 377–389, 2004. Pinho, P., Augusto, S., Maguas, C., Pereira, M. J., Soares, A., and Branquinho, C.: Impact of Neighbourhood Land-Cover in Epiphytic Lichen Diversity: Analysis of Multiple Factors Working at Different Spatial Scales, Environ. Pollut., 151, 414–422, 2008a. Pinho, P., Augusto, S., Martins-Loucao, M. A., Pereira, M. J., Soares, A., Maguas, C., and Branquinho, C.: Causes of Change in Nitrophytic and Oligotrophic Lichen Species in a Mediterranean Climate: Impact of Land Cover and Atmospheric Pollutants, Environ. Pollut., 154, 380–389, 2008b. Pinho, P., Branquinho, C., Cruz, C., Tang, Y. S., Dias, T., Rosa, A. P., Maguas, C., Martins-Loucao, M. A., and Sutton, M. A.: Assessment of Critical Levels of Atmospheric Ammonia for Lichen Diversity in Cork-Oak Woodland, Portugal, in: Atmospheric Ammonia, edited by: Sutton, M. A., Reis, S., and Baker, S. M. H., Springer, 2009. Pinho, P., Dias, T., Cruz, C., Tang, Y. S., Sutton, M. A., Martins-Loucao, M. A., Maguas, C., and Branquinho, C.: Using Lichen Functional Diversity to Assess the Effects of Atmospheric Ammonia in Mediterranean Woodlands, J. Appl. Ecol., 48, 1107–1116, 2011. Pinho, P., Bergamini, A., Carvalho, P., Branquinho, C., Stofer, S., Scheidegger, C, and Maguas, C.: Lichen Functional Groups as Ecological Indicators of the Effects of Land-Use in Mediterranean Ecosystems, Ecol. Indic., 15, 36–42, 2012. Pitcairn, C. E. R., Leith, I. D., Sheppard, L. J., Sutton, M. A., Fowler, D., Munro, R. C., Tang, S., and Wilson, D.: The Relationship between Nitrogen Deposition, Species Composition and Foliar Nitrogen Concentrations in Woodland Flora in the Vicinity of Livestock Farms, Environ. Pollut., 102, 41–48, 1998. Plieninger, T., Hochtl, F., and Spek, T.: Traditional land-use and nature conservation in European rural landscapes, Environ. Sci. Policy, 9, 317–321, 2006. Reis, S., Pinder, R. W., Zhang, M., Lijie, G., and Sutton, M. A.: Reactive nitrogen in atmospheric emission inventories, Atmos. Chem. Phys., 9, 7657–7677, http://dx.doi.org/10.5194/acp-9-7657-2009doi:10.5194/acp-9-7657-2009, 2009. Rockstrom, J., Steffen, W., Noone, K., Persson, A., Chapin, F. S., Lambin, E. F., Lenton, T. M., Scheffer, M., Folke, C., Schellnhuber, H. J., Nykvist, B., de Wit, C. A., Hughes, T., van der Leeuw, S., Rodhe, H., Sorlin, S., Snyder, P. K., Costanza, R., Svedin, U., Falkenmark, M., Karlberg, L., Corell, R. W., Fabry, V. J., Hansen, J., Walker, B., Liverman, D., Richardson, K., Crutzen, P., and Foley, J. A.: A Safe Operating Space for Humanity, Nature, 461, 472–475, 2009. Roda, F., Avila, A., and Rodrigo, A.: Nitrogen Deposition in Mediterranean Forests, Environ. Pollut., 118, 205–213, 2002. Rogers, P. C., Moore, K. D., and Ryel, R. J.: Aspen Succession and Nitrogen Loading: A Case for Epiphytic Lichens as Bioindicators in the Rocky Mountains, USA, J. Veg. Sci., 20, 498–510, 2009. Ruisi, S., Zucconi, L., Fornasier, F., Paoli, L., Frati, L., and Loppi, S.: Mapping Environmental Effects of Agriculture with Epiphytic Lichens, Isr. J. Plant Sci., 53, 115–124, 2005. Scheffer, M., Bascompte, J., Brock, W. A., Brovkin, V., Carpenter, S. R., Dakos, V., Held, H., van Nes, E. H., Rietkerk, M., and Sugihara, G.: Early-Warning Signals for Critical Transitions, Nature, 461, 53–59, 2009. Simpson, D., Fagerli, H., Jonson, J.E., Tsyro, S., Wind, P., and Tuovinen, J.P.: The Emep Unified Eulerian Model:~model Description, Emep Msc-W Report 1/2003; The Norwegian Meteorological Institute, 2003. Sparrius, L. B.: Response of Epiphytic Lichen Communities to Decreasing Ammonia Air Concentrations in a Moderately Polluted Area of the Netherlands, Environ. Pollut., 146, 375–379, 2007. Spier, L., van Dobben, H., and van Dort, K.: Is Bark Ph More Important Than Tree Species in Determining the Composition of Nitrophytic or Acidophytic Lichen Floras?, Environ. Pollut., 158, 3607–3611, 2010. Stofer, S., Bergamini, A., Aragon, G., Carvalho, P., Coppins, B. J., Davey, S., Dietrich, M., Farkas, E., Karkkainen, K., Keller, C., Lokos, L., Lommi, S., Maguas, C., Mitchell, R., Pinho, P., Rico, V. J., Truscott, A. M., Wolseley, P. A., Watt, A., and Scheidegger, C.: Species Richness of Lichen Functional Groups in Relation to Land Use Intensity, Lichenologist, 38, 331–353, 2006. Sutton, M. A., Milford, C., Dragosits, U., Place, C. J., Singles, R. J., Smith, R. I., Pitcairn, C. E. R., Fowler, D., Hill, J., ApSimon, H. M., Ross, C., Hill, R., Jarvis, S. C., Pain, B. F., Phillips, V. C., Harrison, R., Moss, D., Webb, J., Espenhahn, S. E., Lee, D. S., Hornung, M., Ullyett, J., Bull, K. R., Emmett, B. A., Lowe, J., and Wyers, G. P.: Dispersion, Deposition and Impacts of Atmospheric Ammonia: Quantifying Local Budgets and Spatial Variability, Environ. Pollut., 102, 349–361, 1998. Sutton, M. A., Miners, B., Tang, Y. S., Milford, C., Wyers, G. P., Duyzer, J. H., and Fowler, D.: Comparison of Low Cost Measurement Techniques for Long-Term Monitoring of Atmospheric Ammonia, J. Environ. Monit., 3, 446–453, 2001. Tang, Y. S., Cape, J. N., and Sutton, M.A.: Development and Types of Passive Samplers for Nh3 and No<sub>x</sub>, TheScientificWorld, 1, 513–529, 2001. Theobald, M. R., Dragosits, U., Place, C. J., Smith, J. U., Sozanska, M., Brown, L., Scholefield, D., Del prado, A., Webb, J., Whitehead, P. G., Angus, A., Hodge, I. D., Fowler, D., and Sutton, M. A.: Modelling Nitrogen Fluxes at the Landscape Scale, Water, Air and Soil Pollution: Focus, 4, 135–142, 2004. UNEP: United Nations Environment Programme and WHRC, Woods Hole Research Center: Reactive Nitrogen in the Environment: Too Much or Too Little of a Good Thing, United Nations, 2007. van Herk, C. M.: Bark Ph and Susceptibility to Toxic Air Pollutants as Independent Causes of Changes in Epiphytic Lichen Composition in Space and Time, Lichenologist, 33, 419–441, 2001. Verhagen, R. and van Diggelen, R.: Spatial Variation in Atmospheric Nitrogen Deposition on Low Canopy Vegetation, Environ. Pollut., 144, 826–832, 2006. Vilsholm, R. L., Wolseley, P. A., Sochting, U., and Chimonides, P. J.: Biomonitoring with Lichens on Twigs, Lichenologist, 41, 189–202, 2009. Wolseley, P. A., James, P. W., Theobald, M. R., and Sutton, M. A.: Detecting Changes in Epiphytic Lichen Communities at Sites Affected by Atmospheric Ammonia from Agricultural Sources, Lichenologist, 38, 161–176, 2006.