Using lichen functional diversity to assess the effects of atmospheric ammonia in Mediterranean woodlands

1. Atmospheric ammonia (NH3) is one of the main drivers for ecosystem changes world-wide, including biodiversity loss. Modelling its deposition to evaluate its impact on ecosystems has been the focus of many studies. For that, universal indicators are needed to determine and compare the early effects of NH3 across ecosystems. 2. We evaluate the effects of atmospheric NH3 in ecosystems using lichens, which are one of the most sensitive communities at the ecosystem level. Rather than measuring total diversity, we use a functional diversity approach because this is potentially a more universal tool. 3. We evaluated the spatial and temporal patterns of atmospheric NH3 concentrations ([NH3]atm) emitted from a point-source over a 1-year period in a cork oak Mediterranean woodland. We observed a temporal pattern of [NH3]atm, with maximum concentrations during autumn. 4. The distribution of lichen species was c. 90% explained by [NH3]atm. The tolerance of lichen species to atmospheric NH3, based on expert knowledge from literature, was tested for the first time against direct measurements of atmospheric NH3. Most species were well classified, with the exception of Lecanora albella and Chrysothrix candelaris, which were more tolerant than expected. Our updated lichen classification can be used to establish lichen functional groups that respond to atmospheric NH3, and these can be used in other Mediterranean countries. 5. Increasing [NH3]atm led to a complete replacement of oligotrophic by nitrophytic species within 65 m of the NH3 source. The geostatistical analysis of functional diversity variables yielded a spatial model with low non-spatial variance, indicating that these variables can cope robustly with high spatial variation in NH3. 6. Synthesis and applications. Our results support the use of functional diversity variables, such as a lichen diversity value, as accurate and robust indicators of the effects of atmospheric NH3 on ecosystems. The spatial modelling of these indicators can provide information with high spatial resolution about the effects of atmospheric NH3 around point- and diffuse sources. As this methodology is based on functional groups, it can be applied to monitor both the impact of atmospheric NH3 and the success of mitigation strategies.

[1]  J. Webb,et al.  Dispersion, deposition and impacts of atmospheric ammonia: quantifying local budgets and spatial variability , 1998 .

[2]  J. Cape,et al.  A study of the epiphytic communities of Atlantic oak woods along an atmospheric nitrogen deposition gradient , 2005 .

[3]  K. Kreutzer,et al.  Three years of continuous measurements of atmospheric ammonia concentrations over a forest stand at the Höglwald site in southern Bavaria , 2002, Plant and Soil.

[4]  Marie-Josée Fortin,et al.  Spatial Analysis: A Guide for Ecologists 1st edition , 2005 .

[5]  D. Hawksworth,et al.  Qualitative Scale for estimating Sulphur Dioxide Air Pollution in England and Wales using Epiphytic Lichens , 1970, Nature.

[6]  Erin E. Dooley,et al.  European Pollutant Emission Register , 2004 .

[7]  S. Loppi,et al.  EFFECT OF DUST ON EPIPHYTIC LICHEN VEGETATION IN THE MEDITERRANEAN AREA (ITALY AND GREECE) , 2000 .

[8]  K. Gross,et al.  Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[9]  W. Robarge,et al.  Atmospheric concentrations of ammonia and ammonium at an agricultural site in the southeast United States , 2002 .

[10]  C. Braak,et al.  Ranking of Epiphytic Lichen Sensitivity to Air Pollution Using Survey Data: A Comparison of Indicator Scales , 1999, The Lichenologist.

[11]  B. Gimeno,et al.  Empirical and simulated critical loads for nitrogen deposition in California mixed conifer forests. , 2008, Environmental pollution.

[12]  P. Pinho,et al.  Causes of change in nitrophytic and oligotrophic lichen species in a Mediterranean climate: impact of land cover and atmospheric pollutants. , 2008, Environmental pollution.

[13]  A. Cropper Convention on Biological Diversity , 1993, Environmental Conservation.

[14]  John D Simmons,et al.  Ammonia emissions from swine houses in the southeastern United States. , 2004, Journal of environmental quality.

[15]  M. Sutton,et al.  Assessment of Critical Levels of Atmospheric Ammonia for Lichen Diversity in Cork-Oak Woodland, Portugal , 2009 .

[16]  J. Olesen,et al.  Processes controlling ammonia emission from livestock slurry in the field , 2003 .

[17]  M. Sutton,et al.  Detecting changes in epiphytic lichen communities at sites affected by atmospheric ammonia from agricultural sources , 2006, The Lichenologist.

[18]  T. K. Mandal,et al.  Study on concentration of ambient NH3 and interactions with some other ambient trace gases , 2010, Environmental monitoring and assessment.

[19]  J. Cape,et al.  The influence of nitrogen in stemflow and precipitation on epiphytic bryophytes, Isothecium myosuroides Brid., Dicranum scoparium Hewd. and Thuidium tamariscinum (Hewd.) Schimp of Atlantic oakwoods. , 2008, Environmental pollution.

[20]  David Svoboda Evaluation of the European method for mapping lichen diversity (LDV) as an indicator of environmental stress in the Czech Republic , 2007, Biologia.

[21]  M. Fortin,et al.  Spatial Analysis: A Guide for Ecologists 1st edition , 2005 .

[22]  C. Stevens,et al.  Nitrogen deposition and loss of biological diversity : agricultural land retirement as a policy response. , 2008 .

[23]  G. P. Wyers,et al.  Comparison of low cost measurement techniques for long-term monitoring of atmospheric ammonia. , 2001, Journal of environmental monitoring : JEM.

[24]  V. Nicolardi,et al.  Lichen biomonitoring of ammonia emission and nitrogen deposition around a pig stockfarm. , 2007, Environmental pollution.

[25]  R. Ryel,et al.  Aspen succession and nitrogen loading: a case for epiphytic lichens as bioindicators in the Rocky Mountains, USA , 2009 .

[26]  Mark R. Theobald,et al.  The potential for spatial planning at the landscape level to mitigate the effects of atmospheric ammonia deposition , 2006 .

[27]  D. Fowler,et al.  Bioindicators of enhanced nitrogen deposition. , 2003, Environmental pollution.

[28]  E. Davidson,et al.  Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. , 2010, Ecological applications : a publication of the Ecological Society of America.

[29]  J. Cape,et al.  Reassessment of Critical Levels for Atmospheric Ammonia , 2009 .

[30]  J. Cape,et al.  Development and Types of Passive Samplers for Monitoring Atmospheric NO2 and NH3 Concentrations , 2001, TheScientificWorldJournal.

[31]  M. Sutton,et al.  The European perspective on nitrogen emission and deposition. , 2003, Environment international.

[32]  S. S. Srivastava,et al.  Simultaneous measurements of SO2, NO2, HNO3 and NH3 : seasonal and spatial variations , 2004 .

[33]  O. W. Purvis,et al.  MAPPING LICHEN DIVERSITY AS AN INDICATOR OF ENVIRONMENTAL QUALITY , 2002 .

[34]  A. Truscott,et al.  Variation of lichen communities with landuse in Aberdeenshire, UK , 2006, The Lichenologist.

[35]  O. W. Purvis,et al.  Lichen and bryophyte distribution on oak in London in relation to air pollution and bark acidity. , 2007, Environmental pollution.

[36]  D. Fowler,et al.  The relationship between nitrogen deposition, species composition and foliar nitrogen concentrations in woodland flora in the vicinity of livestock farms , 1998 .

[37]  C. Branquinho,et al.  Understanding the performance of different lichen species as biomonitors of atmospheric dioxins and furans: potential for intercalibration , 2009, Ecotoxicology.

[38]  L. Zucconi,et al.  Mapping environmental effects of agriculture with epiphytic lichens , 2005 .

[39]  J. Cape,et al.  Evidence for changing the critical level for ammonia. , 2009, Environmental pollution.

[40]  A. Bytnerowicz,et al.  Atmospheric deposition inputs and effects on lichen chemistry and indicator species in the Columbia River Gorge, USA. , 2007, Environmental pollution.

[41]  U. Dämmgen Atmospheric nitrogen dynamics in Hesse, Germany: Creating the data base : 3. Monitoring of atmospheric concentrations of ammonia using passive samplers , 2007 .

[42]  E. Cowling,et al.  The Nitrogen Cascade , 2003 .

[43]  F. Chapin,et al.  A safe operating space for humanity , 2009, Nature.

[44]  P. Pinho,et al.  Mapping Lichen Diversity as a First Step for Air Quality Assessment , 2004 .

[45]  P. Pinho,et al.  Impact of neighbourhood land-cover in epiphytic lichen diversity: analysis of multiple factors working at different spatial scales. , 2008, Environmental pollution.

[46]  P. Giordani,et al.  Effects of atmospheric pollution on lichen biodiversity (LB) in a Mediterranean region (Liguria, northwest Italy). , 2002, Environmental pollution.

[47]  C. Branquinho,et al.  Improving the use of lichens as biomonitors of atmospheric metal pollution. , 1999, The Science of the total environment.

[48]  C. M. V. Herk Mapping of Ammonia Pollution with Epiphytic Lichens in the Netherlands , 1999, The Lichenologist.

[49]  C.J.F. ter Braak,et al.  Effects of atmospheric NH3 on epiphytic lichens in the Netherlands : The pitfalls of biological monitoring , 1998 .

[50]  S. Wanless,et al.  Temporal variation in atmospheric ammonia concentrations above seabird colonies , 2008 .

[51]  P. Nimis,et al.  Lichens, air pollution and lung cancer , 1997, Nature.

[52]  Gerald J. Niemi,et al.  Application of Ecological Indicators , 2004 .

[53]  P. Giordani Is the diversity of epiphytic lichens a reliable indicator of air pollution? A case study from Italy. , 2007, Environmental pollution.

[54]  C. Gaggi,et al.  Effects of NO2 and NH3 from road traffic on epiphytic lichens. , 2006, Environmental pollution.