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Effects of Reduced and Oxidised Nitrogen on Rich-Fen Mosses: a 4-Year Field Experiment

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Abstract

Dutch fens, subjected to high nitrogen (N) deposition levels with reduced N (NHy) highly dominating over oxidised N (NOx), have since the second half of the past century seen a significant decline of Scorpidium and other characteristic brown moss species, while several Sphagnum species have increased rapidly. This promotes acidification and the transition from rich to poor fens. In line with the outcomes of previous short-term water culture experiments, we hypothesised that Scorpidium growth is negatively affected by NHy due to ammonium toxicity, but not by NOx deposition, and that Sphagnum grows equally well on both N forms. To test this hypothesis under field conditions, we carried out a 4-year N addition experiment (5.0 g N m−2 year−1, applied either as NO3 -N or as NH4 +-N) on natural mixed Scorpidium revolvensSphagnum contortum stands in a rich fen with relatively low background N deposition. After 4 years, ammonium addition had significantly reduced Scorpidium growth, while Sphagnum had not significantly been affected by N additions. Increased ammonium levels were directly toxic to Scorpidium, while Sphagnum was not affected. Furthermore, N addition (in particular nitrate) also indirectly influenced moss growth through promoting vascular plants. Our study confirms that it is ecologically relevant to consider the specific form in which N enrichment occurs, i.e. the ratio of NHy vs. NOx. We conclude that in rich fens, the risk of rapid transition of the moss layer to dominance of poor-fen species is strongly promoted by increased deposition of reduced N.

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References

  • Aerts, R., & Chapin, F. S., III. (2000). The mineral nutrition of wild plants revisited: a reevaluation of processes and patterns. Advances in Ecological Research, 30, 1–67.

    Article  CAS  Google Scholar 

  • Aherne, J., & Farrell, E. P. (2002). Deposition of sulphur, nitrogen and acidity in precipitation over Ireland: chemistry, spatial distribution and long-term trends. Atmospheric Environment, 36, 1379–1389.

    Article  CAS  Google Scholar 

  • Bakker, S. A., Van den Berg, N. J., & Speleers, B. P. (1994). Vegetation transitions of floating wetlands in a complex of turbaries between 1937 and 1989 as determined from aerial photographs with GIS. Vegetatio, 114, 161–167.

    Google Scholar 

  • Bakker, S. A., Jasperse, C., & Verhoeven, J. T. A. (1997). Accumulation rates of organic matter associated with different successional stages from open water to carr forest in former turbaries. Plant Ecology, 129, 113–120.

    Article  Google Scholar 

  • Bates, J. W. (2000). Mineral nutrition, substratum ecology, and pollution. In A. J. Shaw & B. Goffinet (Eds.), Bryophyte biology (pp. 248–311). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Beltman, B., Van den Broek, T., & Bloemen, S. (1995). Restoration of acidified rich-fen ecosystems in the Vechtplassen area: successes and failures. In B. D. Wheeler, S. C. Shaw, W. Fojt, & R. A. Robertson (Eds.), Restoration of temperate wetlands (pp. 273–286). Chichester: John Wiley & Sons.

    Google Scholar 

  • Beltman, B., Dorland, E., & Van Vliet, B. (2002). The role of a buffer zone on species composition and nutrient status of fens in Ireland: a case study in Scragh Bog, Co. Westmeath. Irish Naturalists’ Journal, 27, 19–32.

    Google Scholar 

  • Bergamini, A., & Pauli, D. (2001). Effects of increased nutrient supply on bryophytes in montane calcareous fens. Journal of Bryology, 23, 331–339.

    Article  Google Scholar 

  • Bobbink, R., & Hettelingh, J. P. (Eds.). (2011). Review and revision of empirical critical loads and dose–response relationships. Bilthoven: Coordination Centre for Effects, National Institute for Public Health and the Environment (RIVM). URL: http://www.rivm.nl/cce.

    Google Scholar 

  • Bobbink, R., Ashmore, M., Braun, S., Flückiger, W., & Van den Wyngaert, I. J. J. (2003). Empirical nitrogen critical loads for natural and semi-natural ecosystems: 2002 update. In B. Achermann & R. Bobbink (Eds.), Empirical critical loads for nitrogen—proceedings (pp. 43–170). Berne: SAEFL.

    Google Scholar 

  • 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., & De Vries, W. (2010). Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecological Applications, 20(1), 30–59.

    Article  CAS  Google Scholar 

  • Bremner, J. M., & Mulvaney, C. S. (1982). Salicylic acid-thiosulphate modification of Kjeldahl method to include nitrate and nitrite. In A. C. Page, R. H. Miller, & D. R. Keeney (Eds.), Agronomy 9: methods of soil analyses. Part 2. Chemical and microbiological properties (pp. 621–622). Soil Science Society of America: Madison.

    Google Scholar 

  • Christmas, M., & Whitton, B. A. (1998). Phosphorus and aquatic bryophytes in the Swale-Ouse river system, north-east England. 1. Relationship between ambient phosphate, internal N:P ratio and surface phosphatase activity. Science of the Total Environment, 210(211), 389–399.

    Article  Google Scholar 

  • Cusell, C., Lamers, L. P. M., Van Wirdum, G., & Kooijman, A. (2013). Impacts of water level fluctuation on mesotrophic rich fens: acidification vs. eutrophication. Journal of Applied Ecology, 50, 998–1009.

    Article  CAS  Google Scholar 

  • De Graaf, M. C. C., Bobbink, R., Roelofs, J. G. M., & Verbeek, P. J. M. (1998). Differential effects of ammonium and nitrate on three heathland species. Plant Ecology, 135, 185–196.

    Article  Google Scholar 

  • Dias, T., Clemente, A., Martins-Loução, M. A., Sheppard, L., Bobbink, R., & Cruz, C. (2014). Ammonium as a driving force of plant diversity and ecosystem functioning: observations based on 5 years’ manipulation of N dose and form in a Mediterranean ecosystem. PLoS ONE, 9(4), e92517.

    Article  CAS  Google Scholar 

  • Dorland, E., Stevens, C. J., Gaudnik, C., Corcket, E., Rotthier, S., Wotherspoon, K., Jokerud, M., Vandvik, V., Soons, M. B., Hefting, M. M., Aarrestad, P. A., Alard, D., Diekmann, M., Duprè, C., Dise, N. B., Gowing, D. J. G., & Bobbink, R. (2013). Differential effects of oxidised and reduced nitrogen on vegetation and soil chemistry of species-rich acidic grasslands. Water, Air, and Soil Pollution, 224, 1664. doi:10.1007/s11270-013-1664-4.

    Article  CAS  Google Scholar 

  • Eckstein, R. L., & Karlsson, P. S. (1999). Recycling of nitrogen among segments of Hylocomium splendens as compared with Polytrichum commune—implications for clonal integration in an ectohydric bryophyte. Oikos, 86, 87–96.

    Article  Google Scholar 

  • Eerens, H. C., Van Dam, J. D., Beck, J. P., Dolmans, J. H. J., Van Pul, W. A. J., Sluyter, R. B. C., Van Velze, K., & Vissenberg, H. A. (2001). Grootschalige luchtverontreiniging en depositie in de Nationale Milieuverkenning 5 (RIVM report 408129 016 / 2001). Bilthoven: RIVM.

    Google Scholar 

  • European Environment Agency (2004). EUNIS – European Nature Information System. URL: http://eunis.eea.europa.eu/.

  • Fagerli, H., & Aas, W. (2008). Trends of nitrogen in air and precipitation: model results and observations at EMEP sites in Europe, 1980–2003. Environmental Pollution, 154, 448–461.

    Article  CAS  Google Scholar 

  • Galloway, J. N. (1995). Acid deposition: perspectives in time and space. Water, Air, and Soil Pollution, 86, 15–24.

    Article  Google Scholar 

  • Galloway, J. N., Townsend, A. R., Erisman, J. W., Bekunda, M., Cai, Z., Freney, J. R., Martinelli, L. A., Seitzinger, S. P., & Sutton, M. A. (2008). Transformation of the nitrogen cycle: recent trends, questions and potential solutions. Science, 320, 889–892.

    Article  CAS  Google Scholar 

  • Gorham, E., Janssens, J. A., Wheeler, G. A., & Glaser, P. H. (1987). The natural and anthropogenic acidification of peatlands. In T. C. Hutchinson & K. M. Meema (Eds.), Effects of atmospheric pollutants on forests, wetlands and agricultural ecosystems (NATO ASI series, Vol. G16, pp. 493–512). Berlin: Springer.

    Chapter  Google Scholar 

  • Jonasson, S. (1988). Evaluation of the point intercept method for the estimation of plant biomass. Oikos, 52, 101–106.

    Article  Google Scholar 

  • Jones, M. L. M., Oxley, E. R. B., & Ashenden, T. W. (2002). The influence of nitrogen deposition, competition and desiccation on growth and regeneration of Racomitrium lanuginosum (Hedw.) Brid. Environmental Pollution, 120, 371–378.

    Article  CAS  Google Scholar 

  • Koerselman, W., Bakker, S. A., & Blom, M. (1990). Nitrogen, phosphorus and potassium budgets for two small fens surrounded by heavily fertilized pastures. Journal of Ecology, 78, 428–442.

    Article  Google Scholar 

  • Kooijman, A. M. (1992). The decrease of rich fen bryophytes in the Netherlands. Biological Conservation, 35, 139–143.

    Article  Google Scholar 

  • Kooijman, A. M., & Bakker, C. (1995). Species replacement in the bryophyte layer in mires: the role of water type, nutrient supply and interspecific interactions. Journal of Ecology, 83, 1–8.

    Article  Google Scholar 

  • Kooijman, A. M., & Paulissen, M. P. C. P. (2006). Higher acidification rates in fens with phosphorus enrichment. Applied Vegetation Science, 9(2), 205–212.

    Article  Google Scholar 

  • Lamers, L. P. M., Bobbink, R., & Roelofs, J. G. M. (2000). Natural nitrogen filter fails in polluted raised bogs. Global Change Biology, 6, 583–586.

    Article  Google Scholar 

  • Limpens, J., & Berendse, F. (2003). Growth reduction of Sphagnum magellanicum subjected to high N deposition: the role of amino acid N concentration. Oecologia, 135, 339–345.

    Article  CAS  Google Scholar 

  • Limpens, J., Berendse, F., & Klees, H. (2003). N deposition affects N availability in interstitial water, growth of Sphagnum and invasion of vascular plants in bog vegetation. New Phytologist, 157, 339–347.

    Article  Google Scholar 

  • Lövblad, G., & Erisman, J. W. (1992). Deposition of nitrogen in Europe. In P. Grennfelt & E. Thörnelof (Eds.), Critical loads for nitrogen—a workshop report (pp. 239–285). Copenhagen: Nordic Council of Ministers.

    Google Scholar 

  • Lucassen, E. C. H. E. T., Bobbink, R., Smolders, A. J. P., Van der Ven, P. J. M., Lamers, L. P. M., & Roelofs, J. G. M. (2003). Interactive effects of low pH and high ammonium levels responsible for the decline of Cirsium dissectum (L.) Hill. Plant Ecology, 165, 45–52.

    Article  Google Scholar 

  • Mäkipää, R. (1998). Sensitivity of understorey vegetation to nitrogen and sulphur deposition in a spruce stand. Ecological Engineering, 10, 87–95.

    Article  Google Scholar 

  • Nordin, A., & Gunnarsson, U. (2000). Amino acid accumulation and growth of Sphagnum under different levels of N deposition. Ecoscience, 7(4), 474–480.

    Google Scholar 

  • O’Connell, M. (1980). The developmental history of Scragh Bog, Co. Westmeath and the vegetational history of its hinterland. New Phytologist, 85, 301–319.

    Article  Google Scholar 

  • O’Connell, M. (1981). The phytosociology and ecology of Scragh Bog, Co. Westmeath. New Phytologist, 87, 139–187.

    Article  Google Scholar 

  • Paulissen, M. P. C. P. (2004). Effects of nitrogen enrichment on bryophytes in fens. PhD thesis, Utrecht University, the Netherlands.

  • Paulissen, M. P. C. P., Van der Ven, P. J. M., Dees, A. J., & Bobbink, R. (2004). Differential effects of nitrate and ammonium on three fen bryophyte species in relation to pollutant nitrogen input. New Phytologist, 164, 451–458.

    Article  Google Scholar 

  • Paulissen, M. P. C. P., Espasa Besalú, L., De Bruijn, H., Van der Ven, P. J. M., & Bobbink, R. (2005). Contrasting effects of ammonium enrichment on fen bryophytes. Journal of Bryology, 27, 109–117.

    Article  Google Scholar 

  • Paulissen, M. P. C. P., Schaminée, J. H. J., During, H. J., Wamelink, G. W. W., & Verhoeven, J. T. A. (2014). Expansion of acidophytic late-successional bryophytes in Dutch fens between 1940 and 2000. Journal of Vegetation Science, 25, 525–533.

    Article  Google Scholar 

  • Pearce, I. S. K., Woodin, S. J., & Van der Wal, R. (2003). Physiological and growth responses of the montane bryophyte Racomitrium lanuginosum to atmospheric nitrogen deposition. New Phytologist, 160, 145–155.

    Article  CAS  Google Scholar 

  • Phoenix, G. K., Booth, R. E., Leake, J. R., Read, D. J., 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 Phytologist, 161, 279–289.

    Article  CAS  Google Scholar 

  • Press, M. C., & Lee, J. A. (1983). Acid phosphatase activity in Sphagnum species in relation to phosphate nutrition. New Phytologist, 93, 567–573.

    Article  CAS  Google Scholar 

  • Proctor, M. C. F. (2000). Physiological ecology. In A. J. Shaw & B. Goffinet (Eds.), Bryophyte biology (pp. 225–247). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Roelofs, J. G. M. (1986). The effect of air-borne sulphur and nitrogen deposition on aquatic and terrestrial heathland vegetation. Experientia, 42, 372–377.

    Article  CAS  Google Scholar 

  • Rydin, H., & Clymo, R. S. (1989). Transport of carbon and phosphorus compounds about Sphagnum. Proceedings of the Royal Society of London B, 237, 63–84.

    Article  CAS  Google Scholar 

  • Schaminée, J. H. J., Weeda, E. J., & Westhoff, V. (1995). De vegetatie van Nederland 2. Plantengemeenschappen van wateren, moerassen en heiden. Uppsala: Opulus Press.

    Google Scholar 

  • Sjörs, H. (1950). On the relation between vegetation and electrolytes in north Swedish mire waters. Oikos, 2, 241–258.

    Article  Google Scholar 

  • Soares, A., & Pearson, J. (1997). Short-term physiological responses of mosses to atmospheric ammonium and nitrate. Water, Air, and Soil Pollution, 93, 225–242.

    CAS  Google Scholar 

  • Stevens, C. J., Manning, P., Van den Berg, L. J. L., De Graaf, M. C. C., Wamelink, G. W. W., Boxman, A. W., Bleeker, A., Vergeer, P., Arroniz-Crespo, M., Limpens, J., Lamers, L. P. M., Bobbink, R., & Dorland, E. (2011). Ecosystem responses to reduced and oxidised nitrogen inputs in European terrestrial habitats. Environmental Pollution, 159, 665–676.

    Article  CAS  Google Scholar 

  • Tomassen, H. B. M., Smolders, A. J. P., Lamers, L. P. M., & Roelofs, J. G. M. (2003). Stimulated growth of Betula pubescens and Molinia caerulea on ombrotrophic bogs: role of high levels of atmospheric nitrogen deposition. Journal of Ecology, 91, 357–370.

    Article  Google Scholar 

  • Turner, B. L., Baxter, R., Ellwood, N. T. W., & Whitton, B. A. (2001). Characterization of the phosphatase activities of mosses in relation to their environment. Plant, Cell and Environment, 24, 1165–1176.

    Article  CAS  Google Scholar 

  • Turner, B. L., Baxter, R., Ellwood, N. T. W., & Whitton, B. A. (2003). Seasonal phosphatase activities of mosses from Upper Teesdale, northern England. Journal of Bryology, 25, 189–200.

    Article  Google Scholar 

  • Van Baaren, M., During, H., & Leltz, G. (1988). Bryophyte communities in mesotrophic fens in the Netherlands. Holarctic Ecology, 11, 32–40.

    Google Scholar 

  • Van den Berg, L. J. L., Dorland, E., Vergeer, P., Hart, M. A. C., Bobbink, R., & Roelofs, J. G. M. (2005). Decline of acid-sensitive plant species in heathland can be attributed to ammonium toxicity in combination with low pH. New Phytologist, 166, 551–564.

    Article  CAS  Google Scholar 

  • Van den Berg, L. J. L., Peters, C. J. H., Ashmore, M. R., & Roelofs, J. G. M. (2008). Reduced nitrogen has a greater effect than oxidised nitrogen on dry heathland vegetation. Environmental Pollution, 154, 359–369.

    Article  CAS  Google Scholar 

  • Van Diggelen, R., Molenaar, W. J., & Kooijman, A. M. (1996). Vegetation succession in a floating mire in relation to management and hydrology. Journal of Vegetation Science, 7, 809–820.

    Article  Google Scholar 

  • Van Dijk, H. F. G., & Roelofs, J. G. M. (1988). Effects of excessive ammonium deposition on the nutritional status and condition of pine needles. Physiologia Plantarum, 73, 494–501.

    Article  Google Scholar 

  • Van Wirdum, G., Den Held, A. J., & Schmitz, M. (1992). Terrestrializing fen vegetation in former turbaries in the Netherlands. In J. T. A. Verhoeven (Ed.), Fens and bogs in the Netherlands: vegetation, history, nutrient dynamics and conservation (pp. 323–360). Dordrecht: Kluwer.

    Chapter  Google Scholar 

  • Verhoeven, J. T. A., & Bobbink, R. (2001). Plant diversity of fen landscapes in the Netherlands. In B. Gopal, W. J. Junk, & J. A. Davis (Eds.), Biodiversity in wetlands: assessment, function and conservation (Vol. 2, pp. 65–87). Leiden: Backhuys.

    Google Scholar 

  • Verhoeven, J. T. A., Beltman, B., Dorland, E., Robat, S. A., & Bobbink, R. (2011). Differential effects of ammonium and nitrate deposition on fen phanerogams and bryophytes. Applied Vegetation Science, 14, 149–157.

    Article  Google Scholar 

  • Vitt, D. H. (2000). Peatlands: ecosystems dominated by bryophytes. In A. J. Shaw & B. Goffinet (Eds.), Bryophyte biology (pp. 312–343). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

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Acknowledgments

The fieldwork and report of the results was financially supported by the Schure-Beijerinck-Popping Fund (Royal Netherlands Academy of Arts and Sciences) and the Dutch Ministry of Economic Affairs (ref. BO-11 Nature and Biodiversity, HD3574), respectively. The authors also express their thanks to Dúchas (now National Parks and Wildlife Service of Ireland) for permission to carry out the field experiment in Scragh Bog, to the Wallace family (Portnashangan, County Westmeath, Ireland) for permission of access to the site, and to Emer Colleran and Sean Pender (Microbiology Department, National University of Ireland, Galway) for enabling us to carry out the phosphatase assays at their lab. Boudewijn Beltman, Albert Dees, Marion van Gellekom and Isabel Van den Wyngaert helped during fieldwork. Paul van der Ven assisted in the field and during laboratory analyses. Edwin Martens (Centre for Biostatistics, Utrecht University) and Saskia Burgers (Biometris, Wageningen University & Research Centre) provided statistical advice. Furthermore, we thank Rien van der Gaag and the staff of the Department of Environmental Biology for enabling us to carry out the amino acid analyses at the Radboud University of Nijmegen. Finally, we are grateful to Dick Bal (Dutch Ministry of Economic Affairs) for his comments on an earlier version of the manuscript.

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Paulissen, M.P.C.P., Bobbink, R., Robat, S.A. et al. Effects of Reduced and Oxidised Nitrogen on Rich-Fen Mosses: a 4-Year Field Experiment. Water Air Soil Pollut 227, 18 (2016). https://doi.org/10.1007/s11270-015-2713-y

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