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Inhibition of Nitrification Alters Carbon Turnover in the Patagonian Steppe

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Abstract

Human activities are altering biodiversity and the nitrogen (N) cycle, affecting terrestrial carbon (C) cycling globally. Only a few specialized bacteria carry out nitrification—the transformation of ammonium (NH +4 ) to nitrate (NO −3 ), in terrestrial ecosystems, which determines the form and mobility of inorganic N in soils. However, the control of nitrification on C cycling in natural ecosystems is poorly understood. In an ecosystem experiment in the Patagonian steppe, we inhibited autotrophic nitrification and measured its effects on C and N cycling. Decreased net nitrification increased total mineral N and NH +4 and reduced NO −3 in the soil. Plant cover (P < 0.05) and decomposition (P < 0.0001) decreased with inhibition of nitrification, in spite of increases in NH +4 availability. There were significant changes in the natural abundance of δ15N in the dominant vegetation when nitrification was inhibited suggesting that a switch occurred in the form of N (from NO −3 to NH +4 ) taken up by plants. Results from a controlled-condition experiment supported the field results by showing that the dominant plant species of the Patagonian steppe have a marked preference for nitrate. Our results indicate that nitrifying bacteria exert a major control on ecosystem functioning, and that the inhibition of nitrification results in significant alteration of the C cycle. The interactions between the C and N cycles suggest that rates of C cycling are affected not just by the amount of available N, but also by the relative availability for plant uptake of NH +4 and NO −3 .

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References

  • Aber JD, Magill A, Boone RD. 1993. Plant and soil responses to chronic nitrogen additions at the Harvard forest. Ecol Appl 3:156–66

    Google Scholar 

  • Aerts R, Berendse F. 1988. The effect of increased nutrient availability on vegetation dynamics in wet heathlands. Vegetatio 76:63–9

    Google Scholar 

  • Ågren G, Bosatta E, Magill AH. 2001. Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia 128:94–8

    Article  Google Scholar 

  • Austin AT, Sala OE. 2002. Carbon and nitrogen dynamics across a natural gradient of precipitation in Patagonia, Argentina. J Veg Sci 13:351–60

    Article  Google Scholar 

  • Carreiro M, Sinsabaugh RL, Repert DA, Parkhurst DF. 2000. Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–65

    Article  Google Scholar 

  • Chapin FS III, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, et al. 2000. Consequences of changing biodiversity. Nature 405:234–42

    Article  PubMed  CAS  Google Scholar 

  • Crawford DM, Chalk PM. 1992. Mineralization and immobilization of soil and fertilizer nitrogen with nitrification inhibitors and solvents. Soil Biol Biochem 24:559–68

    Article  CAS  Google Scholar 

  • Falkengren-Grerup U, Michelsen A, Olsson MO, Sleep D, Quarmby C. 2004. Plant nitrate use in deciduous woodland: the relationship between leaf N, 15N natural abundance of forbs and soil N mineralisation. Soil Biol Biochem 36:1885–91

    Article  CAS  Google Scholar 

  • Fernández RJ, Sala OE, Golluscio RA. 1991. Woody and herbaceous aboveground production of a Patagonian steppe. J Range Manage 44:434–7

    Google Scholar 

  • Galloway JN, Cowling EB. 2002. Reactive nitrogen and the world: 200 years of change. Ambio 31:64–71

    PubMed  Google Scholar 

  • Gill RA, Polley HW, Johnson HB, Anderson LJ, Maherali H, Jackson RB. 2002. Nonlinear grassland response to past and future atmospheric CO2. Nature 417:279–82

    Article  PubMed  CAS  Google Scholar 

  • Golluscio RA, Sala OE. 1993. Plant functional types and ecological strategies in Patagonian forbs. J Veg Sci 4:839–46

    Article  Google Scholar 

  • Goring CAI. 1962. Control of nitrification by 2-chloro-6-(trichloromethyl) pyridine. Soil Sci 93:211–8

    Article  CAS  Google Scholar 

  • Greig-Smith P. 1983. Quantitative plant ecology. Oxford (UK): Blackwell Scientific. 359 p

    Google Scholar 

  • Gundersen P, Emmett BA, Kjonaas OJ, Koopmans CJ, Tietema A. 1998. Impact of nitrogen deposition on nitrogen cycling in forests: a synthesis of NITREX data. For Ecol Manage 101:37–55

    Article  Google Scholar 

  • Handley LL, Raven JA. 1992. The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant Cell Environ 15:965–85

    Article  CAS  Google Scholar 

  • Handley LL, Austin AT, Robinson D, Scrimegour CM, Raven JA, Heaton THE, Schmidt S, et al. 1999. The 15-N natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Aust J Plant Physiol 26:185–199

    Article  Google Scholar 

  • Hart SC, Nason GE, Myrold DD, Perry DA. 1994. Dynamics of gross nitrogen transformations in an old-growth forest: the carbon connection. Ecology 75:880–91

    Article  Google Scholar 

  • Haynes RJ, Goh KM. 1978. Ammonium and nitrate nutrition of plants. Biol Rev 53:465–510

    Article  CAS  Google Scholar 

  • Hobbie SE. 2000. Interactions between litter lignin and soil nitrogen availability during leaf litter decomposition in a Hawaiian montane forest. Ecosystems 3:484–94

    Article  CAS  Google Scholar 

  • Hu S, Chapin FS III, Firestone MK, Field CB, Chiariello NR. 2001. Nitrogen limitation of microbial decomposition in a grassland under elevated CO2. Nature 409:188–191

    Article  PubMed  CAS  Google Scholar 

  • Jackson LE, Schimel JP, Firestone MK. 1989. Short-term partitioning of ammonium and nitrate between plants and microbes in an annual grassland. Soil Biol Biochem 21:409–15

    Article  Google Scholar 

  • Jobbágy EG, Sala OE. 2000. Controls on grass and shrub aboveground production in the Patagonian steppe. Ecol Appl 10:541–9

    Google Scholar 

  • Kholdebarin B, Mozafar A, Frossard E. 1998. Differential inhibition of nitrification by three metabolic inhibitors. J Plant Nutr 21:929–36

    CAS  Google Scholar 

  • Kronzucker HJ, Glass ADM, Siddiqi MY. 1999. Inhibition of nitrate uptake by ammonium in barley: analysis of component fluxes. Plant Physiol 120:283–91

    Article  PubMed  CAS  Google Scholar 

  • Lambers H, Chapin FS III, Pons TL. 1998. Plant physiological ecology. New York: Springer-Verlag

    Google Scholar 

  • Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C. 2006. Archaea perdominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  PubMed  CAS  Google Scholar 

  • López NI, Austin AT, Sala OE, Méndez B. 2003. Controls on nitrification in a water-limited ecosystem: experimental inhibition of ammonia-oxidizing bacteria in the Patagonian steppe. Soil Biol Biochem 35:1609–13

    Article  CAS  Google Scholar 

  • Magill AH, Aber JD. 1998. Long-term effects of experimental nitrogen additions on foliar litter decay and humus formation in forest ecosystems. Plant Soil 203:301–11

    Article  CAS  Google Scholar 

  • Mariotti A, Pierre D, Vedy JC, Bruckert S, Guillemot J. 1981. Experimental determinations of nitrogen kinetic isotope fractionations: some principles. Illustration for the denitrification and nitrification process. Plant Soil 62:413–30

    Article  CAS  Google Scholar 

  • McCarty GW. 1999. Modes of action of nitrification inhibitors. Biol Fertil Soil 29:1–9

    Article  CAS  Google Scholar 

  • McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, et al. 2002. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71

    Article  PubMed  CAS  Google Scholar 

  • Nadelhoffer KJ, Emmett BA, Gundersen P, Kjonaas OJ, Koopmans CJ, Schleppi P, Tietema A, et al. 1999. Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–8

    Article  CAS  Google Scholar 

  • Neff JC, Townsend AR, Gleixner G, Lehman SJ, Turnbull J, Bowman WD. 2002. Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419:915–7

    Article  PubMed  CAS  Google Scholar 

  • Nordin A, Högberg P, Näsholm T. 2001. Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia 129:125–32

    Article  Google Scholar 

  • Paul EA, Clark FE. 1996. Soil microbiology and biochemistry. San Diego (CA): Academic Press. 340 p

    Google Scholar 

  • Reich PB, Knops J, Tilman D, Craine J, Ellsworth D, Tjoelker M, Lee T, et al. 2001. Plant diversity enhances ecosystem responses to elevated CO2 and nitrogen deposition. Nature 410:809–11

    Article  PubMed  CAS  Google Scholar 

  • Robertson GP, Paul EA. 2000. Decomposition and soil organic matter dynamics. In: Sala OE, Jackson RB, Mooney HA, Howarth RW, editors. Methods in ecosystem science. New York: Springer. p 104–16

    Google Scholar 

  • Sahrawat KL. 1989. Effects of nitrification inhibitors on nitrogen transformations, other than nitrification, in soils. Adv Agron 42:279–309

    Article  CAS  Google Scholar 

  • Sala OE, Golluscio RA, Lauenroth WK, Soriano A. 1989. Resource partitioning between shrubs and grasses in the Patagonian steppe. Oecologia 81:501–5

    Article  Google Scholar 

  • Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, et al. 2000. Global biodiversity scenarios for the year 2100. Science 287:1770–4

    Article  PubMed  CAS  Google Scholar 

  • Schlesinger WH. 1997. Biogeochemistry: an analysis of global change. San Diego (CA): Academic Press. 443 p

    Google Scholar 

  • Schlesinger WH, Lichter J. 2001. Limited carbon storage in soil and litter of experimental forest plots under increased atmospheric CO2. Nature 411:466–9

    Article  PubMed  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ. 1995. Biometry. New York: WH Freeman. 887 p

    Google Scholar 

  • Soriano A, Sala OE. 1983. Ecological strategies in a Patagonian arid steppe. Vegetatio 56:9–15

    Article  Google Scholar 

  • Soriano A, Sala OE, Perelman SB. 1994. Patch structure and dynamics in a Patagonian arid steppe. Vegetatio 111:127–35

    Article  Google Scholar 

  • Stark JM, Hart SC. 1997. High rates of nitrification and nitrate turnover in undisturbed conifer forests. Nature 385:61–4

    Article  CAS  Google Scholar 

  • Tilman D. 1993. Species richness of experimental productivity gradients: how important is colonization limitation? Ecology 74:2179–91

    Article  Google Scholar 

  • Valle HFD. 1998. Patagonian soils: a regional synthesis. Ecol Aust 8:103–24

    Google Scholar 

  • Van Soest PJ. 1963. Use of detergents in analysis of fibrous feeds. II. A rapid method for the determination of fiber and lignin. Assoc Off Analy Chem 46:829–35

    Google Scholar 

  • Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, et al. 1997a. Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–50

    Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM. 1997b. Human domination of Earth’s ecosystems. Science 277:494–9

    Article  CAS  Google Scholar 

  • Wedin DA, Tilman D. 1996. Influence of nitrogen loading and species composition on the carbon balance of grasslands. Science 274:1720–3

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The research was supported by a grant from the Inter-American Institute for Global Change Research (CRN-012), the Fondo para la Investigación Científica y Tecnológica (FONCyT), and the University of Buenos Aires; additional institutional support was provided by IFEVA. A.T.A. was supported by a National Science Foundation International Research Fellowship and a grant from Fundación Antorchas of Argentina. We thank Jerry Huffman of DowElanco for his expertise and the donation of N-serve 24E for use in our experiment. J. Vrsalovic, L. Vivanco, P. Flombaum, N. Sala, J. Rotundo, R. Pera, P. Roset, and S. Veron provided field assistance, and M. Tagliazucchi, A. Sala, I. Montoya, and W. Cook provided laboratory assistance. L. Gherardi assisted with the greenhouse experiment. T. Loynachan, D. Mengel, G. Malzer, A. Mosier and P. Vitousek supplied us with information about nitrification inhibitors. We are especially grateful to R. Sanchez, J. Stark, and W. Schlesinger for their comments on the experiment.

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  1. Instituto de Investigaciones Fisiológicas y Ecológicas Vinculadas a la Agricultura (IFEVA), Facultad de Agronomía, CONICET and Universidad de Buenos Aires, Avenida San Martín 4453, Buenos Aires, C1417DSE, Argentina

    Amy T. Austin & Osvaldo E. Sala

  2. Department of Biology and Nicholas School of the Environment, Duke University, Durham, North Carolina, 27708, USA

    Robert B. Jackson

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  1. Amy T. Austin
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  2. Osvaldo E. Sala
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Correspondence to Amy T. Austin.

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Austin, A.T., Sala, O.E. & Jackson, R.B. Inhibition of Nitrification Alters Carbon Turnover in the Patagonian Steppe. Ecosystems 9, 1257–1265 (2006). https://doi.org/10.1007/s10021-005-0039-0

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