Abstract
Climate change and anthropogenic nitrogen deposition are both important ecological threats. Evaluating their cumulative effects provides a more holistic view of ecosystem vulnerability to human activities, which would better inform policy decisions aimed to protect the sustainability of ecosystems. Our knowledge of the cumulative effects of these stressors is growing, but we lack an integrated understanding. In this Review, we describe how climate change alters key processes in terrestrial and freshwater ecosystems related to nitrogen cycling and availability, and the response of ecosystems to nitrogen addition in terms of carbon cycling, acidification and biodiversity.
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References
Schlesinger, W. H. On the fate of anthropogenic nitrogen. Proc. Natl Acad Sci. USA 106, 203–208 (2009).
Compton, J. E. et al. Ecosystem services altered by human changes in the nitrogen cycle: a new perspective for US decision making. Ecol. Lett. 14, 804–815 (2011).
Röckstrom, J. et al. A safe operating space for humanity. Nature 461, 472–475 (2009).
Collins, M. et al. in Climate Change 2013: The Physical Science Basis (eds Stocker, T. F. et al.) Ch. 12 (IPCC, Cambridge Univ. Press, 2013).
Pinder, R. W. et al. Climate change impacts of US reactive nitrogen. Proc. Natl Acad Sci. USA 109, 7671–7675 (2012).
Engardt, M. & Langner, J. Simulations of future sulphur and nitrogen deposition over Europe using meteorological data from three regional climate projections. Tellus B 65, 20348 (2013).
Tagaris, E. et al. Impacts of future climate change and emissions reductions on nitrogen and sulfur deposition over the United States. Geophys. Res. Lett. 35, L08811 (2008).
Baron, J. S. et al. The interactive effects of excess reactive nitrogen and climate change on aquatic ecosystems and water resources of the United States. Biogeochemistry 114, 71–92 (2013).
Borken, W. & Matzner, E. Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Glob. Change Biol. 15, 808–824 (2009).
Rustad, L. E., Campbell, J. L. & Marion, G. M. A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming. Oecol. 126, 543–562 (2001).
Jiménez Cisneros, B. E. et al. in Climate Change 2014: Impacts, Adaptation, and Vulnerability (eds Field, C. B. et al.) Ch. 3 (IPCC, Cambridge Univ. Press, 2014).
Morse, J. L., Duran, J. & Groffman, P. M. Soil denitrification fluxes in a northern hardwood forest: the importance of snowmelt and implications for ecosystem N budgets. Ecosyst. 18, 520–532 (2015).
Vitousek, P. M., Menge, D. N. L., Reed, S. C. & Cleveland, C. C. Biological nitrogen fixation: rates, patterns and ecological controls in terrestrial ecosystems. Phil. Trans. R. Soc. B 368, 20130119 (2013).
Welter, J. R. et al. Does N-2 fixation amplify the temperature dependence of ecosystem metabolism? Ecology 96, 603–610 (2015).
Billen, G., Garnier, J. & Lassaletta, L. The nitrogen cascade from agricultural soils to the sea: modelling nitrogen transfers at regional watershed and global scales. Phil. Trans. R. Soc. B 368, 20130123 (2013).
Band, L. E., Tague, C. L., Groffman, P. & Belt, K. Forest ecosystem processes at the watershed scale: hydrological and ecological controls of nitrogen export. Hydrol. Process. 15, 2013–2028 (2001).
Boulton, A. J. Hyporheic rehabilitation in rivers: restoring vertical connectivity. Freshwater Biol. 52, 632–650 (2007).
Whitehead, P. G., Wilby, R. L., Battarbee, R. W., Kernan, M. & Wade, A. J. A review of the potential impacts of climate change on surface water quality. Hydrol. Sci. J. 54, 101–123 (2009).
Goodridge, B. M. & Melack, J. M. Land use control of stream nitrate concentrations in mountainous coastal California watersheds. J. Geophys. Res. Biogeosci. 117, G02005 (2012).
Kaushal, S. S. et al. Interaction between urbanization and climate variability amplifies watershed nitrate export in Maryland. Environ. Sci. Technol. 42, 5872–5878 (2008).
Lamersdorf, N. P. et al. Effect of drought experiments using roof installations on acidification/nitrification of soils. Forest Ecol. Manag. 101, 95–109 (1998).
Van Metre, P. C. et al. High nitrate concentrations in some Midwest United States streams in 2013 after the 2012 drought. J. Environ. Qual. http://dx.doi.org/10.2134/jeq2015.12.0591 (2016).
Bayley, S. E., Schindler, D. W., Parker, B. R., Stainton, M. P. & Beaty, K. G. Effects of forest-fire and drought on acidity of a base-poor boreal forest stream — similarities between climatic warming and acidic precipitation. Biogeochemistry 17, 191–204 (1992).
Kaushal, S. S. et al. Land use and climate variability amplify carbon, nutrient, and contaminant pulses: a review with management implications. J. Am. Wat. Res. Assoc. 50, 585–614 (2014).
Casson, N. J., Eimers, M. C. & Watmough, S. A. Impact of winter warming on the timing of nutrient export from forested catchments. Hydrol. Process. 26, 2546–2554 (2012).
Baron, J. S., Schmidt, T. M. & Hartman, M. D. Climate-induced changes in high elevation stream nitrate dynamics. Glob. Change Biol. 15, 1777–1789 (2009).
Weier, K. L., Doran, J. W., Power, J. F. & Walters, D. T. Denitrification and the dinitrogen/nitrous oxide ratio as affected by soil water, available carbon, and nitrate. Soil Sci. Soc. Am. J. 51, 66–72 (1993).
Anderson, T. R., Groffman, P. M. & Walter, M. T. Using a soil topographic index to distribute denitrification fluxes across a northeastern headwater catchment. J. Hydrol. 522, 123–134 (2015).
Duncan, J. M., Groffman, P. M. & Band, L. E. Towards closing the watershed nitrogen budget: apatial and temporal scaling of denitrification. J. Geophys. Res. Biogeosci. 118, 1105–1119 (2013).
Thomas, R. Q., Canham, C. D., Weathers, K. C. & Goodale, C. L. Increased tree carbon storage in response to nitrogen deposition in the US. Nature Geosci. 3, 13–17 (2010).
Liu, L. & Greaver, T. L. A review of nitrogen enrichment effects on three biogenic GHGs: the CO2 sink may be largely offset by stimulated N2O and CH4 emission. Ecol. Lett. 12, 1103–1117 (2009).
de Vries, W., Du, E. Z. & Butterbach-Bahl, K. Short and long-term impacts of nitrogen deposition on carbon sequestration by forest ecosystems. Curr. Opin. Env. Sust. 9–10, 90–104 (2014).
Chu, C. et al. Does climate directly influence NPP globally? Glob. Change Biol. 22, 12–24 (2015).
Lu, M. et al. Responses of ecosystem carbon cycle to experimental warming: a meta-analysis. Ecology 94, 726–738 (2013).
Bachelet, D., Neilson, R. P., Lenihan, J. M. & Drapek, R. J. Climate change effects on vegetation distribution and carbon budget in the United States. Ecosystems 4, 164–185 (2001).
Liu, L. L. & Greaver, T. L. A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol. Lett. 13, 819–828 (2010).
Xia, J. Y. & Wan, S. Q. Global response patterns of terrestrial plant species to nitrogen addition. New Phytol. 179, 428–439 (2008).
Treseder, K. K. A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol. 164, 347–355 (2004).
Bond-Lamberty, B. & Thomson, A. Temperature-associated increases in the global soil respiration record. Nature 464, 579–582 (2010).
Churkina, G. et al. Interactions between nitrogen deposition, land cover conversion, and climate change determine the contemporary carbon balance of Europe. Biogeosci. 7, 2749–2764 (2010).
Emmett, B. A. et al. The response of soil processes to climate change: results from manipulation studies of shrublands across an environmental gradient. Ecosystems 7, 625–637 (2004).
Burd, A. et al. Terrestrial and marine perspectives on modeling organic matter and degredation pathways. Glob. Change Biol. 22, 121–136 (2015).
Gerber, S., Hedin, L. O., Oppenheimer, M., Pacala, S. W. & Shevliakova, E. Nitrogen cycling and feedbacks in a global dynamic land model. Glob. Biogeochem. Cy. 24, GB1001 (2010).
Janssens, I. A. et al. Reduction of forest soil respiration in response to nitrogen deposition. Nature Geosci. 3, 315–322 (2010).
Conant, R. T. et al. Temperature and soil organic matter decomposition rates — synthesis of current knowledge and a way forward. Glob. Change Biol. 17, 3392–3404 (2011).
Xiang, S. R., Doyle, A., Holden, P. A. & Schimel, J. P. Drying and rewetting effects on C and N mineralization and microbial activity in surface and subsurface California grassland soils. Soil Biol. Biochem. 40, 2281–2289 (2008).
Laudon, H. et al. Cross-regional prediction of long-term trajectory of stream water DOC response to climate change. Geophys. Res. Lett. 39, L18404 (2012).
Wu, Z., Koch, G. W., Dijkstra, P., Bowker, M. A. & Hungate, B. A. Responses of ecosystem carbon cycling to climate change treatments along an elevation gradient. Ecosystems 14, 1066–1080 (2011).
Elser, J. J. et al. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 10, 1135–1142 (2007).
Cole, J. J. et al. Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10, 171–184 (2007).
Kastowski, M., Hinderer, M. & Vecsei, A. Long-term carbon burial in European lakes: analysis and estimate. Glob. Biogeochem. Cy. 25, GB3019 (2011).
Gudasz, C. et al. Temperature-controlled organic carbon mineralization in lake sediments. 466, 478–481 (2010).
Schaberg, P. G. et al. Effects of chronic N fertilization on foliar membranes, cold tolerance, and carbon storage in montane red spruce. Can. J. For. Res. 32, 1351–1359 (2002).
McNulty, S. G., Cohen, E. C., Myers, J. A. M., Sullivan, T. J. & Li, H. Estimates of critical acid loads and exceedances for forest soils across the conterminous United States. Environ. Poll. 149, 281–292 (2007).
Driscoll, C. T. et al. Acidic deposition in the northeastern United States: sources and inputs, ecosystem effects, and management strategies. BioScience 51, 180–198 (2001).
Aber, J. et al. Nitrogen saturation in temperate forest ecosystems — hypotheses revisited. BioScience 48, 921–934 (1998).
Burns, D. A., Lynch, J. A., Cosby, B. J., Fenn, M. E., Baron, J. S. National Acid Precipitation Assessment Program Report to Congress 2011: An Integrated Assessment (National Science and Technology Council, 2011).
Mosley, L. M. Drought impacts on the water quality of freshwater systems; review and integration. Earth Sci. Rev. 140, 203–214 (2015).
Kowalik, R. A., Cooper, D. M., Evans, C. D. & Ormerod, S. J. Acidic episodes retard the biological recovery of upland British streams from chronic acidification. Glob. Change Biol. 13, 2439–2452 (2007).
Wright, R. F. & Schindler, D. W. Interaction of acid rain and global changes: effects on terrestrial and aquatic ecosystems. Wat. Air Soil Poll. 85, 89–99 (1995).
Evans, C. et al. Does elevated nitrogen deposition or ecosystem recovery from acidification drive increased dissolved organic carbon loss from upland soil? A review of evidence from field nitrogen addition experiments. Biogeochemistry 91, 13–35 (2008).
Booth, M. S., Stark, J. M. & Rastetter, E. Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol. Monogr. 75, 139–157 (2005).
Murdoch, P. S., Burns, D. A. & Lawrence, G. B. Relation of climate change to the acidification of surface waters by nitrogen deposition. Environ. Sci. Technol. 32, 1642–1647 (1998).
Fernandez, I. J., Rustad, L. E., Norton, S. A., Kahl, J. S. & Cosby, B. J. Experimental acidification causes soil base-cation depletion at the Bear Brook Watershed in Maine. Soil Sci. Soc. Am. J. 67, 1909–1919 (2003).
Li, H. & McNulty, S. G. Uncertainty analysis on simple mass balance model to calculate critical loads for soil acidity. Environ. Poll. 149, 315–326 (2007).
Roberto, H. G. & Broecker, W. S. The separate and combined effects of temperature, soil p CO2, and organic acidity on silicate weathering in the soil environment: formulation of a model and results. Glob. Biogeochem. Cy. 8, 141–155 (1994).
Belyazid, S., Kurz, D., Braun, S., Sverdrup, H., Rihm, B., Hettelingh J. P. A dynamic modelling approach for estimating critical loads of nitrogen based on plant community changes under a changing climate. Environ. Poll. 159, 789–801 (2011).
Wu, W. & Driscoll, C. T. Impact of climate change on three-dimensional dynamic critical load functions. Environ. Sci. Technol. 44, 720–726 (2010).
Poleo, A. B. S. & Muniz, I. P. The effect of aluminum in soft-water at low pH and different temperatures on mortality, ventilation frequency and water-balance in smoltifying Atlantic Salmon, Salmo-salar. Environ. Biol. Fish 36, 193–203 (1993).
Bobbink, R. et al. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol. Appl. 20, 30–59 (2010).
Howarth, R. et al. Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Front. Ecol. Environ. 9, 18–26 (2011).
Roem, W. J., Klees, H. & Berendse, F. Effects of nutrient addition and acidification on plant species diversity and seed germination in heathland. J. Appl. Ecol. 39, 937–948 (2002).
Sullivan, T. J. et al. Effects of acidic deposition and soil acidification on sugar maple trees in the adirondack mountains, New York. Environ. Sci. Technol. 47, 12687–12694 (2013).
Greaver, T. L. et al. Ecological effects of nitrogen and sulfur air pollution in the US: what do we know? Front. Ecol. Environ. 10, 365–372 (2012).
de Sassi, C., Lewis, O. T. & Tylianakis, J. M. Plant-mediated and nonadditive effects of two global change drivers on an insect herbivore community. Ecology 93, 1892–1901 (2012).
Dise, N. et al. in The European Nitrogen Assessment (ed. Mark A. Sutton) Ch. 21 (Cambridge Univ. Press, 2011).
Zavaleta, E. S., Shaw, M. R., Chiariello, N. R., Mooney, H. A. & Field, C. B. Additive effects of simulated climate changes, elevated CO2, and nitrogen deposition on grassland diversity. Proc. Natl Acad Sci. USA 100, 7650–7654 (2003).
Reich, P. B., Hobbie, S. E. & Lee, T. D. Plant growth enhancement by elevated CO2 eliminated by joint water and nitrogen limitation. Nature Geosci. 7, 920–924 (2014).
Reich, P. B. Elevated CO2 reduces losses of plant diversity caused by nitrogen deposition. Science 326, 1399–14020 (2009).
Clark, C. M. & Tilman, D. Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451, 712–715 (2008).
Elser, J. J. et al. Shifts in lake N:P stoichiometry and nutrient limitation driven by atmospheric nitrogen deposition. Science 326, 835–837 (2009).
Hobbs, W. O. et al. Quantifying recent ecological changes in remote lakes of North America and greenland using sediment diatom assemblages. Plos One http://doi.org/cj89hf (2010).
Jeppesen, E. et al. Climate change impacts on lakes: an integrated ecological perspective based on a multi-faceted approach, with special focus on shallow lakes. J. Limnol. 73, 88–111 (2014).
Kangur, K. et al. Long-term effects of extreme weather events and eutrophication on the fish community of shallow lake Peipsi (Estonia/Russia). J. Limnol. 72, 376–387 (2013).
Winfield, I. J. et al. Population trends of Arctic charr (Salvelinus alpinus) in the UK: assessing the evidence for a widespread decline in response to climate change. Hydrobiol. 650, 55–65 (2010).
Jeppesen, E. et al. Impacts of climate warming on the long-term dynamics of key fish species in 24 European lakes. Hydrobiol. 694, 1–39 (2012).
Burgmer, T., Hillebrand, H. & Pfenninger, M. Effects of climate-driven temperature changes on the diversity of freshwater macroinvertebrates. Oecol. 151, 93–103 (2007).
Ozen, A. et al. Long-term effects of warming and nutrients on microbes and other plankton in mesocosms. Freshwater Biol. 58, 483–493 (2013).
Kosten, S. et al. Warmer climates boost cyanobacterial dominance in shallow lakes. Glob. Change Biol. 18, 118–126 (2012).
Williamson, T. J. et al. Warming alters coupled carbon and nutrient cycles in experimental streams. Glob. Change Biol. 22, 2152–2164 (2016).
Meerhoff, M. et al. Environmental warming in shallow lakes: a review of potential changes in community structure as evidenced from space-for-time substitution approaches. Adv. Ecol. Res. 46, 259–349 (2012).
Feuchtmayr, H. et al. Global warming and eutrophication: effects on water chemistry and autotrophic communities in experimental hypertrophic shallow lake mesocosms. J. Appl. Ecol. 46, 713–723 (2009).
Williams, W. D. Anthropogenic salinisation of inland waters. Hydrobiol. 466, 329–337 (2001).
Jeppesen, E. et al. Restoration of shallow lakes by nutrient control and biomanipulation-the successful strategy varies with lake size and climate. Hydrobiol. 581, 269–285 (2007).
Paerl, H. W. et al. Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Res. 45, 1973–1983 (2011).
Hernández, D. L. et al. Nitrogen pollution is linked to US listed species declines. BioScience 66, 213–222 (2016).
LeBauer, D. S. & Treseder, K. K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379 (2008).
Knorr, M., Frey, S. D. & Curtis, P. S. Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86, 3252–3257 (2005).
Dieleman, W. I. J. et al. Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature. Glob. Change Biol. 18, 2681–2693 (2012).
Liu, L. et al. A cross-biome synthesis of soil respiration and its determinants under simulated precipitation changes. Glob Change Biol. 22, 1394–1405 (2015).
Acknowledgements
The authors thank the participants of the Environmental Protection Agency sponsored workshop: 'Interacting Effects of Climate and Nitrogen on Ecosystems and Their Services: Workshop to Review Current Science and Inform Policy-Driven Scientific Needs' for their contributions. We also thank Meredith Lassiter and Ellen Cooter for technical comments to improve the manuscript. The views expressed in this abstract are those of the authors and do not necessarily represent the views or policies of the US EPA.
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C.M.C., J.E.C., R.A.H. and T.L.G conceived the paper. T.L.G., C.M.C., J.E.C., D.V., A.F.T. and C.P.W. led the writing, with contributions from L.L., E.F., E.A.D, C.L.G., J.A.L., L.E.B., C.L.T., J.S.B., J.D.H. and K.J.N.
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Greaver, T., Clark, C., Compton, J. et al. Key ecological responses to nitrogen are altered by climate change. Nature Clim Change 6, 836–843 (2016). https://doi.org/10.1038/nclimate3088
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DOI: https://doi.org/10.1038/nclimate3088
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