Skip to main content
Log in

European Semiarid Mediterranean Ecosystems are Sensitive to Nitrogen Deposition: Impacts on Plant Communities and Root Phosphatase Activity

Water, Air, & Soil Pollution Aims and scope Submit manuscript

Cite this article


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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3


  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Gallardo, A., Rodríguez-Saucedo, J. J., Covelo, F., & Fernández-Alés, R. (2000). Soil nitrogen heterogeneity in a Dehesa ecosystem. Plant Soil, 222, 71–82.

    Article  CAS  Google Scholar 

  • 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.

    Book  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

Download references


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.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Raúl Ochoa-Hueso.

Electronic supplementary material

Below is the link to the electronic supplementary material.


(DOCX 15 kb)


(DOCX 21 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: