Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe

Nature Communications

Volumn 4, Issue , 2013, Pages

  Peñuelas, Josep ^a,b   Poulter, Benjamin ^c   Sardans, Jordi ^a,b   Ciais, Philippe ^c   Van Der Velde, Marijn ^d   Bopp, Laurent ^c   Boucher, Olivier ^e   Godderis, Yves ^f   Hinsinger, Philippe ^g   Llusia, Joan ^a,b   Nardin, Elise ^f   Vicca, Sara ^h   Obersteiner, Michael ^d   Janssens, Ivan A ^h  

^a CSIC   (Spain)

^b CREAF   (Spain)

^c LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^d INTERNATIONAL INSTITUTE FOR APPLIED SYSTEMS ANALYSIS   (Austria)

^e CNRS   (France)

^f OBSERVATOIRE MIDI PYRÉNÉES   (France)

^g UMR ECO SOLS   (France)

^h UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

NITROGEN; PHOSPHATE FERTILIZER; PHOSPHORUS;

CARBON SEQUESTRATION; CROP YIELD; DEVELOPING WORLD; ECOSYSTEM FUNCTION; ECOSYSTEM STRUCTURE; MASS BALANCE; NITROGEN; PHOSPHORUS; STOICHIOMETRY;

AQUATIC SPECIES; ARTICLE; CARBON CYCLE; CARBON STORAGE; CONTROLLED STUDY; ECOSYSTEM; ENVIRONMENTAL IMPACT; HARVEST; HUMAN; NITROGEN AVAILABILITY; NITROGEN DEPOSITION; PHOSPHORUS CYCLE; STOICHIOMETRY;

CARBON; ECOSYSTEM; EUTROPHICATION; HUMANS; NITROGEN; PHOSPHORUS;

EID: 84890724045     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3934     Document Type: Article

References (70)

1. Galloway, J. N. et al. Nitrogen cycles: past, present, and future. Biogeochemistry 70, 153-226 (2004).
2. UNESCO. Human alteration of the nitrogen cycle. Threats, benefits and opportunities. UNESCO-SCOPE Policy and Benefits 4, 1-6 (2007).
3. Mahowald, N. et al. The global distribution of atmospheric phosphorus deposition and anthropogenic impacts. Global Biogeochem. Cycles 22, GB4026 (2008).
4. Peñuelas, J., Sardans, J., Rivas-Ubach, A. & Janssens, I. A. The human-induced imbalance between C, N and P in Earth's life system. Glob. Change Biol. 189, 5-8 (2012).
5. Foley, J. A. et al. Solutions for a cultivated planet. Nature 478, 337-342 (2011).
6. Lamarque, J. F. et al. Historical (1850-2000) gridded anthropogenic and biomass burning emissions of reactive gases and aerosols: methodology and application. Atmos. Chem. Phys. 10, 7017-7039 (2010).
7. Hungate, B. A., Dukes, J. S., Shaw, M. R., Luo, Y. & Field, C. B. Nitrogen and climate change. Science 302, 1512-1513 (2003). (Pubitemid 37475680)
8. Goll, D. S. et al. Nutrient limitation reduces land carbon uptake in simulations with a model of combined carbon, nitrogen and phosphorus cycling. Biogeosciences 9, 3547-3569 (2012).
9. Zaehle, S. & Dalmonech, D. Carbon-nitrogen interactions on land at global scales: current understanding in modelling climate biosphere feedbacks. Cur. Op. Environ. Sustain 3, 311-320 (2011).
10. Hietz, P. et al. Long-term change in the nitrogen cycle of tropical forests. Science 334, 664-666 (2011).
11. Huang, W. J., Zhou, G. Y. & Liu, J. X. Nitrogen and phosphorus status and their influence on aboveground production under increasing nitrogen deposition in three successional forests. Acta Oecol. 44, 20-27 (2012).
12. Elser, J. J. et al. Shifts in lake N:P stoichiometry and nutrient limitation driven by atmospheric nitrogen deposition. Science 326, 835-837 (2009).
13. Sardans, J., Rivas-Ubach, A. & Peñuelas, J. The C:N:P stoichiometry of organisms and ecosystems in a changing world: a review and perspectives. Persp. Plant Ecol. Evol. Syst. 14, 33-47 (2012b).
14. Turner, R. E., Rabalais, N. N., Justic, D. & Dortch, Q. Global patterns of dissolved N, P and Si in large rivers. Biogeochemistry 64, 297-317 (2003). (Pubitemid 37007874)
15. Hutchins, D. A. et al. CO2 control of Trichodesmium N2 fixation, photosynthesis, growth rates, and elemental ratios: implications for past, present, and future ocean biogeochemistry. Limnol. Oceanogr. 52, 1293-1304 (2007). (Pubitemid 47121544)
16. van der Velde, M. et al. Affordable nutrient solutions for improved food security as evidenced by crop trials. PLoS One 8, e60075 (2013).
17. Cech, P. G., Kuster, T., Edwards, P. J. & Venterink, H. O. Effects of herbivory, fire and N2-fixation on nutrient limitation in a humid African savanna. Ecosystems 11, 991-1004 (2008).
18. Arbuckle, K. E. & Downing, J. A. The influence of watershed land use on lake N:P in a predominantly agricultural landscape. Limnol. Oceanogr. 46, 970-975 (2001). (Pubitemid 32540605)
19. Hall, S. R. Stoichiometrically explicit food webs: feedbacks between resources supply, elemental constrains, and species diversity. Annu. Rev. Ecol. Evol. Syst. 40, 503-528 (2009).
20. Loladze, I. & Elser, J. J. The origins of the Redfield nitrogen-to-phosphorus ratio are in a homeostatic protein-to-rRNA ratio. Ecol. Lett. 14, 244-250 (2011).
21. Rivas-Ubach, A., Sardans, J., Pérez-Trujillo, M., Estiarte, M. & Peñuelas, J. Strong relationship between elemental stoichiometry and metabolome in plants. Proc. Natl Acad. Sci. USA 109, 4181-4186 (2012).
22. Reich, P. B., Oleksyn, J. & Wright, I. J. Leaf phosphorus influences the photosynthesis-nitrogen relation: a cross-biome analysis of 314 species. Oecologia 160, 207-212 (2009).
23. Elser, J. J., Fagan, W. F., Kerkhoff, A. J., Swenson, N. G. & Enquist, B. J. Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol. 186, 593-608 (2010).
24. Güsewell, S. N:P ratios in terrestrial plants: variation and functional significance. New Phytol. 164, 243-266 (2004). (Pubitemid 39393907)
25. Sasaki, T., Yoshihara, Y., Jamsran, U. & Ohkuro, T. Ecological stoichiometry explains larger-scale facilitation processes by shrubs on species coexistence among understory plants. Ecol. Engin. 36, 1070-1075 (2010).
26. Seastedt, T. R. & Vaccaro, L. Plant species richness, productivity, and nitrogen and phosphorus limitations across a snowpack gradient in alpine tundra, Colorado, USA. Artic Antartic Alpine Res. 33, 100-106 (2001). (Pubitemid 32205731)
27. Laliberté, E. et al. How does pedogenesis drive plant diversity? Trends Ecol. Evol. 28, 331-340 (2013).
28. Bobbink, R. et al. Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol. Appl. 20, 30-59 (2010).
29. Wassen, M. J. et al. Endangered plants persist under phosphorus limitation. Nature 437, 547-550 (2005). (Pubitemid 41613551)
30. Moe, S. J. et al. Recent advances in ecological stoichiometry: insights for population and community ecology. Oikos 109, 29-39 (2005). (Pubitemid 40518604)
31. Knorr, M., Frey, S. D. & Curtis, P. S. Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86, 3252-3257 (2005). (Pubitemid 43086900)
32. Yang, X. & Post, W. N. Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method. Biogeosciences 8, 2907-2916 (2011).
33. Elser, J. J., Dobberfuhl, D. R., MacKay, N. A. & Schampel, J. H. Organism size, life history, and N: P stoichiometry. Bioscience 46, 674-684 (1996).
34. Sterner, R. W. & Elser, J. J. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere (Princeton Univ. Press, 2002).
35. Sardans, J., Rivas-Ubach, A. & Peñuelas, J. The elemental stoichiometry of aquatic and terrestrial ecosystems and its relationships with organic lifestyle and ecosystem structure and function: a review and perspectives. Biogeochemistry 111, 1-39 (2012a).
36. Sistla, S. A. & Schimel, J. P. Stoichiometric flexibility as a regulator of carbon and nutrient cycling in terrestrial ecosystems under change. New Phytol. 196, 68-78 (2012).
37. Yu, Q. et al. Linking stoichiometry homeostasis with ecosystem structure, functioning and stability. Ecol. Lett. 13, 1390-1399 (2010).
38. Yu, Q. et al. Stoichiometry homeostasis of vascular plants in the inner Mongolia grassland. Oecologia 166, 1-10 (2011).
39. Vrede, T. et al. Effects of N:P loading ratios on phytoplankton community composition, primary production and N fixation in a eutrophic lake. Freshw. Biol. 54, 331-344 (2009).
40. Mulder, C. & Elser, J. J. Soil acidity, ecological stoichiometry and allometric scaling in grassland food webs. Global Change Biol. 15, 2730-2738 (2009).
41. Hassett, R. P., Cardinale, B., Stabler, L. B. & Elser, J. J. Ecological stoichiometry of N and P in pelagic ecosystems: comparison of lakes and oceans with emphasis on the zooplankton-phytoplankton interaction. Limnol. Oceanogr. 42, 648-662 (1997). (Pubitemid 27468389)
42. Calbet, A., Carlotti, F. & Gaudy, R. The feeding ecology of the copepod Centropagestypicus (Kröyer). Progr. Oceanogr. 72, 137-150 (2007). (Pubitemid 46331087)
43. Dyhrman, S. T., Ammerman, J. W. & Van Mooy, B. A. S. Microbes and the marine phosphorus cycle. Oceanography 20, 110-116 (2007).
44. Martin, R. E., Quigg, A. & Podkovyrov, V. Marine biodiversification in response to evolving phytoplankton stoichiometry. Palaeogeogr. Palaeoclim. Palaeoecol. 258, 277-291 (2008).
45. Ruttenberg, K. C. Treatise in Geochemistry Vol. 8 (ed Schlesinger, W. H.) 585-643 (Elsevier, 2003).
46. Vermeij, G. J. Evolution and Escalation: An Ecological History of Life (Princeton Univ. Press, 1987).
47. Compton, J. S. et al. Marine Authigenesis: From Global To Microbial Society of Sedimentary Geology. (eds Glenn, C. R. et al.) 21-33 (Special Publication Number 66, 2000).
48. Servais, T., Owen, A. W., Harper, D. A. T., Kröger, B. & Munnecke, A. The Great Ordovician Biodiversification Event (GOBE): the palaeoecological dimension. Palaeogeogr. Palaeoclim. Palaeoecol. 294, 99-119 (2010).
49. Planavsky, N. et al. The evolution of the marine phosphate reservoir. Nature 467, 1088-1091 (2010).
50. Aber, J. et al. Nitrogen saturation in temperate forest ecosystems-hypotheses revised. Bioscience 48, 921-934 (1998). (Pubitemid 28494493)
51. Vitousek, P. ,M. & Howarth, R. W. Nitrogen limitation on land and in the sea-how can it occur. Biogeochemistry 13, 87-115 (1991).
52. Tanner, E. V. J., Vitousek, P. M. & Cuevas, E. Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79, 10-22 (1998). (Pubitemid 28397825)
53. Wright, S. J. et al. Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92, 1616-1625 (2011).
54. Marklein, A. R. & Houlton, B. Z. Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol. 193, 696-704 (2012).
55. Tresseder, K. K. & Vitousek, P. M. Effects of soil nutrient availability on investment in acquisition of N and P in Hawaiian rain forests. Ecology 82, 946-954 (2001). (Pubitemid 32333444)
56. Phoenix, G. K. et al. Simulated pollutant nitrogen deposition increases P demand and enhances root-surface phosphatise activities of three plant functional types in a calcareous grassland. New Phytol. 161, 279-289 (2004). (Pubitemid 38047065)
57. Lilleskov, E. A., Fahey, T. J., Horton, T. R. & Lovett, G. M. Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83, 104-115 (2002). (Pubitemid 34067682)
58. Cleveland, C. C. et al. Patterns of new versus recycled primary production in the terrestrial biosphere. Proc. Natl Acad. Sci. USA 110, 12733-12737 (2013).
59. Krishnamurthy, A., Moore, J. K., Mahowald, N., Luo, C. & Zender, C. S. Impacts of atmospheric nutrients inputs on marine biogeochemistry. J. Geophys. Res-Biogeosci. 115, G01006 (2010).
60. Bopp, L. et al. Potential impact of climate change on marine export production. Global Biogeochem. Cycles 15, 81-99 (2001). (Pubitemid 32430732)
61. Doney, S. C. The growing human footprint on coastal and open-ocean biogeochemistry. Science 328, 1512-1516 (2010).
62. McGroddy, M. E., Daufresne, T. & Hedin, L. O. Scaling of C:N:P stoichiometry in forest worldwide: implications of terrestrial Redfield-type ratios. Ecology 85, 2390-2401 (2004). (Pubitemid 39348532)
63. Elser, 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). (Pubitemid 350060402)
64. Friedlingstein, P. et al. Climate-carbon cycle feedback analysis: results from the C4MIP model intercomparison. J. Clim. 19, 3337-3353 (2006). (Pubitemid 44177898)
65. Peters, G. P. et al. Rapid growth in CO2 emissions after the 2008-2009 global financial crisis. Nature Clim. Change 2, 2-4 (2012).
66. Matear, R. J., Wang, Y. P. & Lenton, A. Land and ocean nutrient and carbon cycle interactions. Curr. Opin. Environ. Sust. 2, 258-263 (2010).
67. Regnier, P. et al. Anthropogenic perturbation of the carbon fluxes from land to ocean. Nature Geosci. 6, 597-606 (2013).
68. MacDonald, G. K., Bennett, E. M., Potter, P. A. & Ramankutty, N. Agronomic phosphorus imbalances across the world's croplands. Proc. Natl Acad. Sci. USA 108, 3086-3091 (2011).
69. Le Quéré, C. et al. Trends in the sources and sinks of carbon dioxide. Nature Geosci. 2, 831-836 (2009).
70. Mackenzie, F. T., Ver, L. M. & Lerman, A. Century-scale nitrogen and phosphorus controls of the carbon cycle. Chem. Geol. 190, 13-22 (2002).