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Slowing of nitrogen cycling and increasing nitrogen use efficiency following afforestation of semi-arid shrubland

Abstract

Nitrogen (N) and water availability are important factors affecting ecosystem productivity that can be influenced by land-use change. We hypothesized that the observed increase in carbon (C) sequestration associated with afforestation of semi-arid sparse shrubland must also be associated with an increase in N input. We tested this hypothesis by reconstructing the ecosystem N budget of two ecosystems, a semi-arid shrubland and a nearby planted pine forest, using measurements augmented with literature-based estimates. Our findings demonstrate that, contrary to our hypothesis, massive C sequestration by the pine forest could be accounted for without a change in the net N budget (i.e., neither elevated N inputs nor reduced N losses). However, in comparison to the shrubland, the forest showed an almost tripling in aboveground N use efficiency (NUE; 235 vs. 83 kg dry mass kg−1 N) and a doubling in ecosystem level C/N ratio (16 vs. 8, for the forest and shrubland, respectively). Nitrogen cycling slowed in the forest compared to the shrubland: net N mineralization rates in soils decreased by approximately 50%, decomposition rates decreased by approximately 20%, and NOx loss decreased by approximately 64%. These adjustments in N cycling provide a possible basis for increased NUE and subsequent C sequestration without net change in the overall N budget, which should be addressed in future investigations.

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References

  1. Aber JD, Melillo JM, Nadelhoffer KJ, Pastor J, Boone RD (1991) Factors controlling nitrogen cycling and nitrogen saturation in northern temperate forest ecosystems. Ecol Appl 1:303–315

    Article  Google Scholar 

  2. Alcamo J, Moreno JM, Novaky B, Bindi M, Corodov R, Devoy RJN, Giannakopoulos C, Martin E, Olesen JE, Shvidenko A (2007) Europe. Climate change 2007: impacts, adaptation and vulnerability. Contribution of Working Group II to the Fourth Assessment report of the Intergovernmental Panel on Climate Change. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 541–580

    Google Scholar 

  3. Arianoutsou M, Radea C (2000) Litter production and decomposition in Pinus halepesis forests. In: Ne’eman G, Trabaud L (eds) Ecology, biogeography and management of Pinus halepensis and P. brutia forest ecosystems in the Mediterranean Basin, vol 1. Backhuys Publishers, Leiden, pp 183–190

    Google Scholar 

  4. Ariza NCL (2004) Vegetation monitoring in a semi-desert afforestation project. MSc thesis, Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, Beer Sheva

  5. Barkmann J, Schwintzer CR (1998) Rapid N2 fixation in pines? Results of a Maine field study. Ecology 79:1453–1457

    Article  Google Scholar 

  6. Berg B, Laskowski R (2005) Nitrogen dynamics in decomposing litter. In: Berg B, Laskowski R (eds) Advances in ecological research. Litter decomposition: a guide to carbon and nutrient turnover, vol 38. Academic Press, San Diego, pp 157–183

    Google Scholar 

  7. Billings SA (2006) Soil organic matter dynamics and land use change at a grassland/forest ecotone. Soil Biol Biochem 38:2934–2943

    Article  CAS  Google Scholar 

  8. Binkley D, Son Y, Valentine DW (2000) Do forests receive occult inputs of nitrogen? Ecosystems 3:321–331

    Article  CAS  Google Scholar 

  9. Bonneh O (2000) Management of planted pine forests in Israel: past, present and future. In: Ne’eman G, Trabaud L (eds) Ecology, biogeography and management of Pinus halepensis and P. brutia forest ecosystems in the Mediterranean Basin, vol 1. Backhuys Publishers, Leiden, pp 377–390

    Google Scholar 

  10. Borgogno F, D’Odorico P, Laio F, Ridolfi L (2007) Effect of rainfall interannual variability on the stability and resilience of dryland plant ecosystems. Water Resour Res 43:W06411. doi:10.1029/2006WR005314

    Article  Google Scholar 

  11. Brumme R, Khanna PK (2008) Ecological and site historical aspects of N dynamics and current N status in temperate forests. Glob Change Biol 14:125–141. doi:10.1111/j.13652486.2007.01460.x

    Google Scholar 

  12. Bustamante MMC, Medina E, Asner GP, Nardoto GB, Garcia-Montiel DC (2006) Nitrogen cycling in tropical and temperate savannas. Biogeochemistry 79:209–237

    Google Scholar 

  13. Chestnut TJ, Zarin DJ, McDowell WH, Keller M (1999) A nitrogen budget for late-successional hillslope tabonuco forest, Puerto Rico. Biogeochemistry 46:85–108

    CAS  Google Scholar 

  14. Christodoulakis NS, Tsimbani H, Fasseas C (1990) Leaf structural peculiarities in Sarcopoterium spinosum, a seasonally dimorphic subshrub. Ann Bot 65:291–296

    Google Scholar 

  15. Cleveland CC, Townsend AR, Schimel DS, Fisher H, Howarth RW, Hedin LO, Perakis SS, Latty EF, Von Fischer JC, Elseroad A, Wasson MF (1999) Global patterns of terrestrial biological nitrogen (–2) fixation in natural ecosystems. Glob Biogeochem Cycles 13:623–645

  16. Compton J, Hooker T, Perakis S (2007) Ecosystem N distribution and 15N during a century of forest regrowth after agricultural abandonment. Ecosystems 10:1197–1208

    Article  CAS  Google Scholar 

  17. Conrad R (2002) Biological processes involved in trace gas exchange. In: Gasche RP, Rennenberg H (eds) Trace gas exchange in forest ecosystem, vol 3. Kluwer, Dordrecht, pp 3–35

    Google Scholar 

  18. Davidson EA, Hart SC, Firestone MK (1992) Internal cycling of nitrate in soils of a mature coniferous forest. Ecology 73:1148–1156

    Article  Google Scholar 

  19. Evans RD, Belnap J (1999) Long-term consequences of disturbance on nitrogen dynamic in an arid ecosystem. Ecology 80:150–160

    Article  Google Scholar 

  20. Farley KA, Kelly EF (2004) Effects of afforestation of a paramo grassland on soil nutrient status. For Ecol Manag 195:281–290

    Article  Google Scholar 

  21. Fassnacht KS, Gower ST (1999) Comparison of the litterfall and forest floor organic matter and nitrogen dynamics of upland forest ecosystems in north central Wisconsin. Biogeochemistry 45:265–284

    Google Scholar 

  22. Garcia-Pausas J, Casals P, Romanya J (2004) Litter decomposition and faunal activity in Mediterranean forest soils: effects of N content and the moss layer. Soil Biol Biochem 36:989–997

    Article  CAS  Google Scholar 

  23. Gelfand I, Yakir D (2008) Influence of nitrite accumulation in association with seasonal patterns and mineralization of soil nitrogen in a semi-arid pine forest. Soil Biol Biochem 40:415–424

    Article  CAS  Google Scholar 

  24. Gelfand I, Feig G, Meixner FX, Yakir D (2009) Afforestation of semi-arid shrubland reduces biogenic NO emission from soil. Soil Biol Biochem 41:1561–1570

    Article  CAS  Google Scholar 

  25. Grünzweig JM, Körner C (2001) Growth, water and nitrogen relations in grassland model ecosystems of the semi-arid Negev of Israel exposed to elevated CO2. Oecologia 128:251–262

    Article  Google Scholar 

  26. Grünzweig JM, Lin T, Rotenberg E, Schwartz A, Yakir D (2003) Carbon sequestration in arid-land forest. Glob Change Biol 9:791–799

    Article  Google Scholar 

  27. Grünzweig JM, Gelfand I, Fried Y, Yakir D (2007) Biogeochemical mechanisms contributing to enhanced carbon sequestration following afforestation in a semi-arid region. Biogeosciences 4:891–904

    Article  Google Scholar 

  28. Grünzweig JM, Hemming D, Maseyk K, Lin T, Rotenberg E, Raz-Yaseef N, Falloon PD, Yakir D (2009) Water limitation to soil CO2 efflux in a pine forest at the semi-arid ‘timberline’. J Geophys Res 114:G03008

    Article  Google Scholar 

  29. Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization and nitrification. In: Weaver RW (ed) Methods of soil analysis: microbiological and biochemical properties, 3rd edn. Soil Science Society of America, Madison, pp 985–1018

  30. Hooper DU, Johnson L (1999) Nitrogen limitation in dryland ecosystems: Responses to geographical and temporal variation in precipitation. Biogeochemistry 46:247–293

    CAS  Google Scholar 

  31. Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED (1996) A global analysis of root distributions for terrestrial biomes. Oecologia 108:389–411

    Google Scholar 

  32. Jackson RB, Mooney HA, Schulze E-D (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci USA 94:7362–7366

    PubMed  Article  CAS  Google Scholar 

  33. Kelliher FM, Ross DJ, Law BE, Baldocchi DD, Rodda NJ (2004) Limitations to carbon mineralization in litter and mineral soil of young and old ponderosa pine forests. For Ecol Manag 191:201–213

    Google Scholar 

  34. Knops JMH, Bradley KL, Wedin DA (2002) Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol Lett 5:454–466

    Article  Google Scholar 

  35. Krueger-Mangold J, Sheley R, Engel R, Jacobsen J, Svejcar T, Zabinski C (2004) Identification of the limiting resource within a semi-arid plant association. J Arid Environ 58:309–320

    Google Scholar 

  36. Laronne JB, Alexandrov Y, Chocron M, Guertin DP, Goodrich DC (2007) Reducing runoff/soil erosion by afforestation in a semiarid area. Ben Gurion University/USDA/ARS/University of Arizona, Beer Sheva/Tucson

  37. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    PubMed  Article  Google Scholar 

  38. Lovett GM, Traynor MM, Pouyat RV, Carreiro MM, Zhu WX, Baxter JW (2000) Atmospheric deposition to oak forests along an urban–rural gradient. Environ Sci Technol 34:4294–4300

    Google Scholar 

  39. Luo Y, Su QB, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, Mcnurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739

    Google Scholar 

  40. Luo Y, Hui D, Zhang D (2006) Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87:53–63

    PubMed  Article  Google Scholar 

  41. Luyssaert S, Staelens J, De Schrijver A (2005) Does the commonly used estimator of nutrient resorption in tree foliage actually measure what it claims to? Oecologia 144:177–186

    PubMed  Article  Google Scholar 

  42. Maseyk KS (2006) Ecophysiological and phenological aspects of Pinus halepensis in an arid-Mediterranean environment. PhD thesis. Environmental Sciences and Energy Research, Weizmann Institute of Sciences, Rehovot

  43. Maseyk K, Grünzweig JM, Rotenberg E, Yakir D (2008a) Respiration acclimation contributes to high carbon-use efficiency in a seasonally dry pine forest. Glob Change Biol 14:1553–1567

    Article  Google Scholar 

  44. Maseyk KS, Lin T, Rotenberg E, Grunzweig JM, Schwartz A, Yakir D (2008b) Physiology–phenology interactions in a productive semi-arid pine forest. New Phytol 178:603–616. doi:10.1111/j.14698137.2008.02391.x

  45. Maseyk K, Angert A, Hemming D, Leavitt S, Yakir D (2011) The control of temperature and precipitation and CO2 on tree growth and water use efficiency in semi-arid woodland. Oecologia (in press)

  46. Matamala R, Schlesinger WH (2000) Effects of elevated atmospheric CO2 on fine root production and activity in an intact temperate forest ecosystem. Glob Change Biol 6:967–979. doi:10.1046/j.13652486.2000.00374.x

    Article  Google Scholar 

  47. Moro MJ, Domingo F, Escarre A (1996) Organic matter and nitrogen cycles in a pine afforested catchment with a shrub layer of Adenocarpus decorticans and Cistus laurifolius in south-eastern Spain. Ann Bot 78:675–685

    Article  CAS  Google Scholar 

  48. Morris SJ, Bohm S, Haile-Mariam S, Paul EA (2007) Evaluation of carbon accrual in afforested agricultural soils. Glob Change Biol 13:1145–1156

    Article  Google Scholar 

  49. Osem Y, Perevolotsky A, Kigel J (2002) Grazing effect on diversity of annual plant communities in a semi-arid rangeland: interactions with small-scale spatial and temporal variation in primary productivity. J Ecol 90:936–946

    Article  Google Scholar 

  50. Osem Y, Perevolotsky A, Kigel J (2004) Site productivity and plant size explain the response of annual species to grazing exclusion in a Mediterranean semi-arid rangeland. J Ecol 92:297–309

    Article  Google Scholar 

  51. Paavolainen L (1999) Nitrogen transformations in boreal forest soils in response to extreme manipulation treatments. PhD thesis. Faculty of Agriculture and Forestery, University of Helsinki, Helsinki

  52. Parfitt RL, Scott NA, Ross DJ, Salt GJ, Tate KR (2003) Land-use change effects on soil C and N transformations in soils of high N status: comparisons under indigenous forest, pasture and pine plantation. Biogeochemistry 66:203–221

    Google Scholar 

  53. Raz-Yaseef N, Dan Y, Eyal R, Gabriel S, Shabtai C (2010a) Ecohydrology of a semi-arid forest: partitioning among water balance components and its implications for predicted precipitation changes. Ecohydrology 3:143–154

    Google Scholar 

  54. Raz-Yaseef N, Rotenberg E, Yakir D (2010b) Effects of spatial variations in soil evaporation caused by tree shading on water flux partitioning in a semi-arid pine forest. Agric For Meteorol 150:454–462

    Article  Google Scholar 

  55. Reisman-Berman O, Kadmon R, Shachak M (2006) Spatio-temporal scales of dispersal limitation in the recolonization of a semi-arid Mediterranean old-field. Ecography 29:418–426. doi:10.1111/j.2006.09067590.04455.x

    Article  Google Scholar 

  56. Robertson GP, Groffman P (2007) Nitrogen transformations. In: Paul EA (ed) Soil microbiology, ecology, and biochemistry. Elsevier Academic Press, Oxford, pp 341–364

    Google Scholar 

  57. Rotenberg E, Yakir D (2010) Contribution of semi-arid forests to the climate system. Science 327:451–454

    PubMed  Article  CAS  Google Scholar 

  58. Russow R, Veste M, Böhme F (2005) A natural 15N approach to determine the biological fixation of atmospheric nitrogen by biological soil crusts of the Negev desert. Rapid Commun Mass Spectr 19 (23):3451–3456

    Google Scholar 

  59. Santantonio D, Grace JC (1987) Estimating fine-root production and turnover from biomass and decomposition data: a compartment-flow model. Can J For Res 17:900–908

    Article  Google Scholar 

  60. Sanz MJ, Carratala A, Gimeno C, Millan MM (2002) Atmospheric nitrogen deposition on the east coast of Spain: relevance of dry deposition in semi-arid Mediterranean regions. Environ Pollut 118:259–272

    PubMed  Article  CAS  Google Scholar 

  61. Sternberg M, Shoshany M (2001) Influence of slope aspect on Mediterranean woody formations: comparison of a semiarid and an arid site in Israel. Ecol Res 16:335–345

    Article  Google Scholar 

  62. Thomas AD, Dougill AJ (2006) Distribution and characteristics of cyanobacterial soil crusts in the Molopo Basin, South Africa. J Arid Environ 64:270–283

    Google Scholar 

  63. Thompson TL, Zaady E, Huancheng P, Wilson TB, Martens DA (2006) Soil C and N pools in patchy shrublands of the Negev and Chihuahuan deserts. Soil Biol Biochem 38:1943–1955

    Article  CAS  Google Scholar 

  64. van Heerwaarden LM, Toet S, Aerts R (2003) Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: facts and solutions. Oikos 101:664–669

    Article  Google Scholar 

  65. Vitousek PM (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119:553

    Article  Google Scholar 

  66. Vitousek PM, Field CB (2001) Input/output balances and nitrogen limitation in terrestrial ecosystems. In: Schulze ED (ed) Global biogeochemical cycles in the climate system. Academic Press, San Diego, pp 217–225

    Google Scholar 

  67. Vitousek PM, Cassman K, Cleveland CC, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57/58:1–45

    Article  CAS  Google Scholar 

  68. Zaady E (2005) Seasonal change and nitrogen cycling in a patchy Negev desert: a review. Arid Land Res Manag 19:111–124

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to Leon Peters, Uri Shapira, and Nitai Zecharia for technical assistance and help with field sampling, Marcelo Sternberg, Dina Kanas, and Yael Fried-Shaked for information on S. spinosum and pine fine roots biomass, and the KKL for cooperation in the field site. We thank two anonymous reviewers for thoughtful and helpful comments and I. A. Cooper for the editing of the manuscript. This research was supported in part by a grant from the Israeli Ministry of Science and Technology and the German BMBF (GLOWA––Jordan River), the KKL, and JNF-Alberta. The long-term operation of the Yatir Forest Research Field Site is supported by the Cathy Wills and Robert Lewis Program in Environmental Science.

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Correspondence to I. Gelfand or D. Yakir.

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Gelfand, I., Grünzweig, J.M. & Yakir, D. Slowing of nitrogen cycling and increasing nitrogen use efficiency following afforestation of semi-arid shrubland. Oecologia 168, 563–575 (2012). https://doi.org/10.1007/s00442-011-2111-0

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Keywords

  • Mediterranean ecosystem
  • N budget
  • Pinus halepensis
  • Semi-arid climate
  • Land-use change