Nitrogen (N) deposition is predicted to impact on the structure and functioning of Mediterranean ecosystems. In this study, we measured plant species composition, production and root phosphatase activity in a field experiment in which N (0, 10, 20 and 50 kg N ha−1 year−1) was added since October 2007 to a semiarid shrubland in central Spain. The characteristically dominant annual forb element responded negatively to N after ~2.5 and ~3.5 years. In contrast, the nitrophilous element (mainly crucifers) increased with N after ~2.5 and ~5.5 years, a response controlled by between-year variations in rainfall and the heterogeneous distribution of P availability. We also described a hierarchy of factors driving the structure and composition of the plant community: soil fertility was the most important driver, whereas calcareousness/acidity of soils and shrub cover played a secondary role; finally, N deposition contributed to explain a smaller fraction of the total variance, and its effects were predominantly negative, which was attributed to ammonium toxicity. Root phosphatase activity of three species was not responsive to N after ~2.5 years but there was a negative relationship with soil P in two of them. We conclude that increased N deposition in semiarid Mediterranean ecosystems of Europe can contribute to cause a shift in plant communities associated with an increase in the nitrophilous element and with a decline in abundance of various forb species adapted to the local conditions.
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Aber, J. D., Goodale, C. L., Ollinger, S. V., Smith, M.-L., Magill, A. H., Martin, M. E., Hallett, A., & Stoddard, J. L. (2003). Is nitrogen deposition altering the nitrogen status of Northeastern forests? Bioscience, 53, 375–389.
Allen, E. B., Padgett, P. E., Bytnerowicz, A., & Minnich, R. A. (1998). Nitrogen deposition effects on coastal sage vegetation of southern California (pp. 131–140). In: Proceedings of the International Symposium on Air Pollution and Climate Change Effects on Forest Ecosystems. US Department of Agriculture Forest Service Pacific Southwest Research Station, Riverside, California, USA.
Bobbink, R., Hicks, K., Galloway, J., Spranger, T., Alkemade, R., Ashmore, M., Bustamante, M., Cinderby, S., Davidson, E., Dentener, F., Emmet, B., Erisman, J.-W., Fenn, M., Gilliam, F., Nordin, A., Pardo, L., & De Vries, W. (2010). Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl, 20, 30–59.
Bonanomi, G., Caporaso, S., & Allegrezza, M. (2006). Short-term effects of nitrogen enrichment litter removal and cutting on a Mediterranean grassland. Acta Oecol, 30, 419–425.
Boudsocq, S., Niboyet, A., Lata, J. C., Raynaud, X., Loeuille, N., Mathieu, J., et al. (2012) Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning?. The American Naturalist 180(1), 60–69.
Carfrae, J. A., Sheppard, L. J., Raven, J. A., Leith, I. D., & Crossley, A. (2007). Potassium and phosphorus additions modify the response of Sphagnum capillifolium growing on a Scottish ombrotrophic bog to enhanced nitrogen deposition. Appl Geochem, 22, 1111–1121.
Ceulemans, T., Merckx, R., Hens, M., & Honnay, O. (2013). Plant species loss from European semi natural grasslands following nutrient enrichment–is it nitrogen or is it phosphorus?. Global Ecology and Biogeography, 22(1), 73–82.
Cox, R. D., & Allen, E. B. (2008). Composition of soil seed banks in southern California coastal sage scrub and adjacent exotic grassland. Plant Ecol, 198, 37–46.
Cruz, C., Bio, A. M. F., Jullioti, A., Tavares, A., Dias, T., & Martins-Loução, M. A. (2008). Heterogeneity of soil surface ammonium concentration and other characteristics related to plant specific variability in a Mediterranean-type ecosystem. Environ Pollut. doi:10.1016/jenvpol200712071–10.
Dias, T., Malveiro, S., Martins-Loução, M. A., Sheppard, L. J., & Cruz, C. (2011). Linking N-driven biodiversity changes with soil N availability in a Mediterranean ecosystem. Plant and soil, 341(1-2), 125–136.
Egerton-Warburton, L. M., & Allen, E. B. (2000). Shifts in arbuscular mycorrhizal communities along an anthropogenic nitrogen deposition gradient. Ecological Applications, 10(2), 484–496.
Emmett, B. A. (2007). Nitrogen saturation of terrestrial ecosystems: some recent findings and their implications for our conceptual framework. Water Air Soil Pollut: Focus, 7(1–3), 99–109.
Fanelli, G., Lestini, M., & Sauli, A. S. (2008). Floristic gradients of herbaceous vegetation and P/N ratio in soil in a Mediterranean area. Plant Ecol, 194, 231–242.
Fenn, M. E., Baron, J. S., Allen, E. B., Rueth, H. M., Nydick, K. R., Geiser, L., Bowman, W. D., Sickman, J. O., Meixner, T., Johnson, D. W., & Neitlich, P. (2003). Ecological effects of nitrogen deposition in the Western United States. Bioscience, 53, 404–420.
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., & Bytnerowicz, A. (2010). J Environ Manag, 91, 2404–2423.
Fisher, J., Lorenagan, W. A., Dixon, K., & Veneklaas, E. J. (2009). Soil seed bank compositional change constrains biodiversity in an invaded species-rich woodland. Biol Conserv, 142, 256–29.
Gallardo, A., Rodríguez-Saucedo, J. J., Covelo, F., & Fernández-Alés, R. (2000). Soil nitrogen heterogeneity in a Dehesa ecosystem. Plant Soil, 222, 71–82.
Gutknecht, J. L., Field, C. B., & Balser, T. C. (2012). Microbial communities and their responses to simulated global change fluctuate greatly over multiple years. Global Change Biology, 18(7), 2256–2269.
Hobbs, R. J., & Richardson, D. M. (1995). Mediterranean-type ecosystems: opportunities and constraints for studying the function of biodiversity (pp. 1–42). In: Davis, G.W., & Richardson, D. Mediterranean-type ecosystems. The function of biodiversity. Springer-Verlag, Berlin, Heidelberg.
Horswill, P., O’Sullivan, O., Phoenix, G. K., Lee, J. A., & Leake, J. R. (2008). Base cation depletion eutrophication and acidification of species-rich grasslands in response to long-term simulated nitrogen deposition. Environ Pollut, 155, 336–349.
Johnson, D., Leake, J. R., & Lee, J. A. (1999). The effects of quantity and duration of simulated pollutant nitrogen deposition on root-surface phosphatase activities in calcareous and acid grasslands: a bioassay. New Phytol, 141, 433–442.
Kritzler, U. H., & Johnson, D. (2010). Mineralisation of carbon and plant uptake of phosphorus from microbially-derived organic matter in response to 19 years of simulated nitrogen deposition. Plant Soil, 326, 311–319.
Ladwig, L. M., Collins, S. L., Swann, A. L., Xia, Y., Allen, M. F., & Allen, E. B. (2012). Above-and belowground responses to nitrogen addition in a Chihuahuan Desert grassland. Oecologia, 169(1), 177–185.
Ochoa-Hueso, R., & Manrique, E. (2010). Nitrogen fertilization and water supply affect germination and plant establishment of the soil seed bank present in a semi-arid Mediterranean scrubland. Plant Ecol, 210, 263–273.
Ochoa-Hueso, R., & Manrique, E. (2011). Effects of nitrogen deposition and soil fertility on cover and physiology of Cladonia foliacea (Huds) Willd a lichen of biological soil crusts from Mediterranean Spain. Environ Pollut, 159, 449–457.
Ochoa‐Hueso, R., & Manrique, E. (2014). Impacts of altered precipitation, nitrogen deposition and plant competition on a Mediterranean seed bank. J Veg Sci. doi:10.1111/jvs.12183.
Ochoa-Hueso, R., Allen, E. B., Branquinho, C., Cruz, C., Dias, T., Fenn, M. E., Manrique, E., Pérez-Corona, M. E., Sheppard, L. J., & Stock, W. D. (2011a). Nitrogen deposition effects on Mediterranean-type ecosystems: an ecological assessment. Environ Pollut. doi:10.1016/j.envpol.2010.12.019.
Ochoa-Hueso, R., Hernandez, R. R., Pueyo, J. J., & Manrique, E. (2011b). Spatial distribution and physiology of biological soil crusts from semi-arid central Spain are related to soil chemistry and shrub cover. Soil Biol Biochem. doi:10.1016/j.soilbio.2011.05.010.
Ochoa-Hueso, R., Pérez-Corona, M. E., & Manrique, E. (2013a). Impacts of simulated N deposition on plants and mycorrhizae from Spanish semiarid Mediterranean shrublands. Ecosystems, 16, 838–851.
Ochoa-Hueso, R., Stevens, C. J., Ortiz-Llorente, M. J., & Manrique, E. (2013b). Soil chemistry and fertility alterations in response to N application in a semiarid Mediterranean shrubland. Sci Total Environ, 452–453, 78–86.
Ochoa-Hueso, R., Arróniz-Crespo, M., Bowker, M. A., Maestre, F. T., Pérez-Corona, M. E., Theobald, M. R., Vivanco, M. G., & Manrique, E. (2014). Biogeochemical indicators of elevated nitrogen deposition in semiarid Mediterranean ecosystems. Environ Monit Assess, 186, 5831–5842.
Phoenix, G. K., Booth, R. E., Leake, J. R., Read, D. R., Grime, J. P., & Lee, J. A. (2003). Simulated pollutant nitrogen deposition increases P demand and enhances root-surface phosphatase activities of three plant functional types in a calcareous grassland. New Phytol, 161, 279–289.
Phoenix, G. K., Hicks, W. K., Cinderby, S., Kuylenstierna, J. C. I., Stock, W. D., Dentener, F. J., Giller, K. E., Austin, A. T., Lefroy, R. D. B., Gimeno, B. S., Ashmore, M. S., & Ineson, P. (2006). Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a greater global perspective in assessing N deposition impacts. Glob Chang Biol, 12, 470–476.
Pilkington, M. G., Caporn, S. J. M., Carroll, J. A., Cresswell, N., Lee, J. A., Ashenden, T. W., Brittain, S. A., & Turner, B. L. (2008). Resource partitioning for soil phosphorus: a hypothesis. J Ecol, 96, 698–702.
Rao, L. E., Parker, D. R., Bytnerowicz, A., & Allen, E. B. (2009). Nitrogen mineralization across an atmospheric nitrogen deposition gradient in Southern California deserts. Journal of arid environments, 73(10), 920–930.
Rivas-Martínez, S. (1987) Memoria del mapa de series de vegetación de España. ICONA, Madrid.
Southon, G. E., Field, C., Caporn, S. J., Britton, A. J., & Power, S. A. (2013). Nitrogen deposition reduces plant diversity and alters ecosystem functioning: field-scale evidence from a nationwide survey of UK heathlands. PLoS one,8(4), e59031.
Stevens, C. J., Duprè, C., Dorland, E., Gaudnik, C., Gowing, D. J., Bleeker, A., et al. (2011). The impact of nitrogen deposition on acid grasslands in the Atlantic region of Europe. Environmental Pollution, 159(10), 2243–2250.
Turner, B. L. (2008). Resource partitioning for soil phosphorus: a hypothesis. Journal of Ecology, 96(4), 698–702.
Vourlitis, G. L., & Pasquini, S. C. (2009). Experimental dry-season N deposition alters species composition in southern Californian Mediterranean-type shrublands. Ecology, 90, 2183–2189.
Witkowski, E. F. T. (1989). Response to nutrient additions by the plant growth forms of sand-plain lowland fynbos South Africa. Vegetatio, 79, 89–97.
This research was financially supported by the Spanish Ministerio de Educación y Ciencia (CGL-2009-11015 and REMEDINAL-2 S2009/AMB-1783). ROH was also funded by an FPU fellowship (AP2006-04638). CJS was funded by a Leverhulme Early Career Fellowship, the European Science Foundation Nitrogen in Europe programme and the Percy Sladen Memorial Fund. We are very thankful to Octavio Cedenilla, Daniel de la Puente, Cristina Paradela and Christopher Long for helping with the lab and field work. Prof. Alfredo Polo and Dr. J.C. García-Gil are thanked for kindly allowing us to use their spectrophotometer and enzyme substrates. Dr. Jason Kaye provided helpful comments on an earlier version of the manuscript. Finally, we want to specially mention Prof. Esteban Manrique and Dr. M. Esther Pérez-Corona for their personal involvement within this project.
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Ochoa-Hueso, R., Stevens, C.J. European Semiarid Mediterranean Ecosystems are Sensitive to Nitrogen Deposition: Impacts on Plant Communities and Root Phosphatase Activity. Water Air Soil Pollut 226, 5 (2015). https://doi.org/10.1007/s11270-014-2278-1
- Inorganic N
- Local forbs
- Mediterranean ecosystems
- N deposition
- Nitrophilous plants
- Phosphorus availability
- Shrub cover
- Soil fertility