Abstract
Increased atmospheric nitrogen (N) deposition is known to alter ecosystem carbon source-sink dynamics through changes in soil CO2 fluxes. However, a limited number of experiments have been conducted to assess the effects of realistic N deposition in the Mediterranean Basin, and none of them have explored the effects of N addition on soil respiration (R s ). To fill this gap, we assessed the effects of N supply on R s dynamics in the following two Mediterranean sites: Capo Caccia (Italy), where 30 kg ha−1 year−1 was supplied for 3 years, and El Regajal (Spain), where plots were treated with 10, 20, or 50 kg N ha−1 year−1 for 8 years. Results show a complex, non-linear response of soil respiration (R s ) to N additions with R s overall increasing at Capo Caccia and decreasing at El Regajal. This suggests that the response of R s to N addition depends on dose and duration of N supply, and the existence of a threshold above which the N introduced in the ecosystem can affect the ecosystem’s functioning. Soil cover and seasonality of precipitations also play a key role in determining the effects of N on R s as shown by the different responses observed across seasons and in bare soil vs. the soil under canopy of the dominant species. These results show how increasing rates of N addition may influence soil C dynamics in semiarid ecosystems in the Mediterranean Basin and represent a valuable contribution for the understanding and the protection of Mediterranean ecosystems.
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References
AEMET.Agencia Española de Meteorología. http://www.aemet.es/es/serviciosclimaticos/datosclimatologicos/valoresclimatologicos?l=3200&k=mad
Ågren G, Bosatta E, Magill A (2001) Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia 128:94–98. doi:10.1007/s004420100646
Allison SD, Czimczik CI, Treseder KK (2008) Microbial activity and soil respiration under nitrogen addition in Alaskan boreal forest. Glob Chang Biol 14:1156–1168. doi:10.1111/j.1365-2486.2008.01549.x
Allison SD, LeBauer DS, Ofrecio MR et al (2009) Low levels of nitrogen addition stimulate decomposition by boreal forest fungi. Soil Biol Biochem 41:293–302. doi:10.1016/j.soilbio.2008.10.032
Almagro M, López J, Querejeta JII, Martínez-Mena M (2009) Temperature dependence of soil CO2 efflux is strongly modulated by seasonal patterns of moisture availability in a Mediterranean ecosystem. Soil Biol Biochem 41:594–605. doi:10.1016/j.soilbio.2008.12.021
Alster CJ, German DP, Lu Y, Allison SD (2013) Microbial enzymatic responses to drought and to nitrogen addition in a Southern California grassland. Soil Biol Biochem 64:68–79. doi:10.1016/j.soilbio.2013.03.034
Barrett JE, Burke IC (2002) Nitrogen retention in semiarid ecosystems across a soil organic-matter gradient. 12:878–890. doi: 10.1007/sl0963-009-9024-4
Bowden RD, Davidson E, Savage K et al (2004) Chronic nitrogen additions reduce total soil respiration and microbial respiration in temperate forest soils at the Harvard forest. For Ecol Manag 196:43–56. doi:10.1016/j.foreco.2004.03.011
Bradford MA, Crowther TW (2013) Commentary: carbon use efficiency and storage in terrestrial ecosystems. New Phytol 199:7–9
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. doi:10.1016/0038-0717(85)90144-0
Correia AC, Minunno F, Caldeira MC et al (2012) Soil water availability strongly modulates soil CO2 efflux in different Mediterranean ecosystems: model calibration using the Bayesian approach. Agric Ecosyst Environ 161:88–100. doi:10.1016/j.agee.2012.07.025
Curiel Yuste J, Janssens IA, Carrara A et al (2003) Interactive effects of temperature and precipitation on soil respiration in a temperate maritime pine forest. Tree Physiol 23:1263–1270. doi:10.1093/treephys/23.18.1263
Curiel Yuste J, Baldocchi DD, Gershenson A et al (2007) Microbial soil respiration and its dependency on carbon inputs, soil temperature and moisture. Glob Chang Biol 13:2018–2035. doi:10.1111/j.1365-2486.2007.01415.x
de Vries W, Solberg S, Dobbertin M et al (2009) The impact of nitrogen deposition on carbon sequestration by European forests and heathlands. For Ecol Manag 258:1814–1823. doi:10.1016/j.foreco.2009.02.034
DeForest JL, Zak DR, Pregitzer KS, Burton AJ (2004) Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Sci Soc Am J 68:132–138
Eberwein JR, Oikawa PY, Allsman LA, Jenerette GD (2015) Carbon availability regulates soil respiration response to nitrogen and temperature. Soil Biol Biochem 88:158–164. doi:10.1016/j.soilbio.2015.05.014
EMEP/2015 EMEP/MSC-W_Reporting. http://www.emep.int/mscw/
Fan H, Wu J, Liu W et al (2014) Nitrogen deposition promotes ecosystem carbon accumulation by reducing soil carbon emission in a subtropical forest. Plant Soil 379:361–371. doi:10.1007/s11104-014-2076-y
Fenn ME, Baron JS, Allen EB et al (2003a) Ecological effects of nitrogen deposition in the western United States. Bioscience 53:404. doi:10.1641/0006-3568(2003)053[0404:EEONDI]2.0.CO;2
Fenn ME, Haeuber R, Tonnesen GS et al (2003b) Nitrogen emissions, deposition, and monitoring in the western United States. Bioscience 53:391. doi:10.1641/0006-3568(2003)053[0391:NEDAMI]2.0.CO;2
Ferretti M, Marchetto A, Arisci S et al (2014) On the tracks of nitrogen deposition effects on temperate forests at their southern European range—an observational study from Italy. Glob Chang Biol 20:3423–3438. doi:10.1111/gcb.12552
Gauss M, Nyíri Á, Benedictow A, Klein H (2016) Transboundary air pollution by main pollutants (S, N, O3) and PM in 2014. Country Reports, Italy and Spain. EMEP/MSC-W Data Note 1/2016. 1–23
Han G, Zhou G, Xu Z et al (2007) Biotic and abiotic factors controlling the spatial and temporal variation of soil respiration in an agricultural ecosystem. Soil Biol Biochem 39:418–425. doi:10.1016/j.soilbio.2006.08.009
Hanson PJ, Edwards NT, Garten CT, Andrews JA (2000) Separating root and soil microbial contributions to soil respiration: a review of methods and observations. Biogeochemistry 48:115–146. doi:10.1023/A:1006244819642
Hasselquist NJ, Metcalfe DB, Högberg P (2012) Contrasting effects of low and high nitrogen additions on soil CO2 flux components and ectomycorrhizal fungal sporocarp production in a boreal forest. Glob Chang Biol 18:3596–3605. doi:10.1111/gcb.12001
He X, Lv G, Qin L et al (2015) Effects of simulated nitrogen deposition on soil respiration in a Populus euphratica community in the Ebinur lake area, a desert ecosystem of northwestern China. PLoS One 10:e0137827. doi:10.1371/journal.pone.0137827
Hungate BA, Dukes JS, Shaw MR, et al (2003) Nitrogen and climate change. Science 302(80-):1512–1513
Janssens IA, Dieleman W, Luyssaert S et al (2010) Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3:315–322. doi:10.1038/ngeo844
Jones D, Willett V (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38:991–999. doi:10.1016/j.soilbio.2005.08.012
Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257
Liang LL, Eberwein JR, Allsman LA et al (2015) Regulation of CO2 and N2O fluxes by coupled carbon and nitrogen availability. Environ Res Lett 10:34008. doi:10.1088/1748-9326/10/3/034008
Litton CMCM, Raich JWJW, Ryan MGMG (2007) Carbon allocation in forest ecosystems. Glob Chang Biol 13:2089–2109. doi:10.1111/j.1365-2486.2007.01420.x
Maestre FT, Cortina J (2003) Small-scale spatial variation in soil CO2 efflux in a Mediterranean semiarid steppe. Appl Soil Ecol 23:199–209. doi:10.1016/S0929-1393(03)00050-7
Manzoni S, Taylor P, Richter A et al (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91. doi:10.1111/j.1469-8137.2012.04225.x
Matteucci M, Gruening C, Goded Ballarin I et al (2015) Components, drivers and temporal dynamics of ecosystem respiration in a Mediterranean pine forest. Soil Biol Biochem 88:224–235. doi:10.1016/j.soilbio.2015.05.017
Morillas L, Bellucco V, Lo Cascio M et al (2017) Contribution of biological crust to soil CO2 efflux in a Mediterranean shrubland ecosystem. Geoderma 289:11–19. doi:10.1016/j.geoderma.2016.11.012
Ochoa-Hueso R, Manrique E (2011) Effects of nitrogen deposition and soil fertility on cover and physiology of Cladonia foliacea (Huds.) Willd., a lichen of biological soil crusts from Mediterranean Spain. Environ Pollut 159:449–457. doi:10.1016/j.envpol.2010.10.021
Ochoa-Hueso R, Hernandez RR, Pueyo JJ, Manrique E (2011) Spatial distribution and physiology of biological soil crusts from semi-arid central Spain are related to soil chemistry and shrub cover. Soil Biol Biochem 43:1894–1901. doi:10.1016/j.soilbio.2011.05.010
Ochoa-Hueso R, Maestre FT, De Los RA et al (2013) Nitrogen deposition alters nitrogen cycling and reduces soil carbon content in low-productivity semiarid Mediterranean ecosystems. Environ Pollut 179:185–193. doi:10.1016/j.envpol.2013.03.060
Phoenix GK, Hicks WK, Cinderby S et al (2006) Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a greater global perspective in assessing N deposition impacts. Glob Chang Biol 12:470–476. doi:10.1111/j.1365-2486.2006.01104.x
Poulter B, Frank D, Ciais P et al (2014) Contribution of semi-arid ecosystems to interannual variability of the global carbon cycle. Nature 509:600–603. doi:10.1038/nature13376
Pregitzer KS, Burton AJ, Zak DR, Talhelm AF (2008) Simulated chronic nitrogen deposition increases carbon storage in northern temperate forests. Glob Chang Biol 14:142–153. doi:10.1111/j.1365-2486.2007.01465.x
Raich JW, Schlesinger WH (1992) The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus B. doi:10.3402/tellusb.v44i2.15428
Reich PB, Hobbie SE, Lee T et al (2006a) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440:922–925. doi:10.1038/nature04486
Reich PB, Hungate BA, Luo Y (2006b) Carbon-nitrogen interactions in terrestrial ecosystems in response to rising atmospheric carbon dioxide. Annu Rev Ecol Evol Syst 37:611–636. doi:10.1146/annurev.ecolsys.37.091305.110039
Rey A, Pegoraro E, Tedeschi V et al (2002) Annual variation in soil respiration and its components in a coppice oak forest in central Italy. Glob Chang Biol 8:851–866. doi:10.1046/j.1365-2486.2002.00521.x
Rodriguez A, Lovett GM, Weathers KC et al (2014) Lability of C in temperate forest soils: assessing the role of nitrogen addition and tree species composition. Soil Biol Biochem 77:129–140. doi:10.1016/j.soilbio.2014.06.025
Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20. doi:10.1023/A:1006247623877
Simpson D, Benedictow A, Berge H et al (2012) The EMEP MSC-W chemical transport model—technical description. Atmos Chem Phys 12:7825–7865. doi:10.5194/acp-12-7825-2012
Sims GK, Ellsworth TR, Mulvaney RL (1995) Microscale determination of inorganic nitrogen in water and soil extracts. Commun Soil Sci Plant Anal 26:303–316. doi:10.1080/00103629509369298
Sinsabaugh RL, Lauber CL, Weintraub MN et al (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264. doi:10.1111/j.1461-0248.2008.01245.x
Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett 16:930–939. doi:10.1111/ele.12113
Soil Survey Staff (1999) Soil taxonomy. a basic system of soil classification for making and interpreting soil surveys. 1975. 754 pp., 12 coloured plates. Agriculture handbook no. 436. Soil conservation service, U.S. Department of Agriculture. From superintendent of documents, U. Geol Mag 114:492. doi:10.1017/S0016756800045489
Sollins P, Glassman C, Paul E et al (1999) Soil carbon and nitrogen: pools and fractions. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P (eds) Standard soil methods for long-term ecological research. Oxford University Pressors, New York, pp 89–105
Ste-Marie C, Paré D (1999) Soil, pH and N availability effects on net nitrification in the forest floors of a range of boreal forest stands. Soil Biol Biochem 31:1579–1589. doi:10.1016/S0038-0717(99)00086-3
Tang J, Baldocchi DD (2005) Spatial–temporal variation in soil respiration in an oak–grass savanna ecosystem in California and its partitioning into autotrophic and heterotrophic components. Biogeochemistry 73:183–207. doi:10.1007/s10533-004-5889-6
Thomas Quinn R, Canham CD, Weathers KC, Goodale CL (2010) Increased tree carbon storage in response to nitrogen deposition in the US. Nat Geosci 3:13–17. doi:10.1038/ngeo721
Treseder KK (2008) Nitrogen additions and microbial biomass: a meta-analysis of ecosystem studies. Ecol Lett 11:1111–1120. doi:10.1111/j.1461-0248.2008.01230.x
Tucker CL, Bell J, Pendall E, Ogle K (2013) Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? Glob Chang Biol 19:252–263. doi:10.1111/gcb.12036
Walkley A, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38. doi:10.1097/00010694-193401000-00003
Welter JR, Fisher SG, Grimm NB (2005) Nitrogen transport and retention in an arid land watershed: influence of storm characteristics on terrestrial–aquatic linkages. Biogeochemistry 76:421–440. doi:10.1007/s10533-005-6997-7
Zhang C, Niu D, Hall SJ et al (2014) Effects of simulated nitrogen deposition on soil respiration components and their temperature sensitivities in a semiarid grassland. Soil Biol Biochem 75:113–123. doi:10.1016/j.soilbio.2014.04.013
Zhou X, Zhang Y (2014) Seasonal pattern of soil respiration and gradual changing effects of nitrogen addition in a soil of the Gurbantunggut desert, northwestern China. Atmos Environ 85:187–194. doi:10.1016/j.atmosenv.2013.12.024
Zhou L, Zhou X, Zhang B et al (2014) Different responses of soil respiration and its components to nitrogen addition among biomes: a meta-analysis. Glob Chang Biol 20:2332–2343. doi:10.1111/gcb.12490
Zhu C, Ma Y, Wu H et al (2016) Divergent effects of nitrogen addition on soil respiration in a semiarid grassland. Sci Rep 6:33541. doi:10.1038/srep33541
Acknowledgments
This research was financially supported by the project “ECO-SCALE” through the Regional Administration of Sardinia, RAS, L.R. 7/2007 “Scientific Research and Technological Innovation in Sardinia.” MLC received funding by PhD grant from the Euro-Mediterranean Centre on Climate Change (CMCC) and received an Erasmus scholarship in collaboration with the Department of Biogeography and Global Change, Spanish National Research Council (CSIC), Madrid, Spain (2014-1-IT02-KA103-000341). This research was also financially supported by a research grant of the Spanish Ministerio de Economía y Competitividad (BIOMOD CGL-2013-44661-R). Comunidad de Madrid also funded this work through REMEDINAL-3 project (S2013/MAE-2719). The authors are very thankful to the owners of “Finca El Regajal” for their kind allowance to work in their property. Special thanks are extended to Iolanda Cocco for helping us with the field and laboratory assistance and to the two anonymous reviewers that provided valuable comments on earlier drafts of the manuscript. SM thanks the Fundação para a Ciência e Tecnologia (FCT) Investigador grant.
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Lo Cascio, M., Morillas, L., Ochoa-Hueso, R. et al. Contrasting effects of nitrogen addition on soil respiration in two Mediterranean ecosystems. Environ Sci Pollut Res 24, 26160–26171 (2017). https://doi.org/10.1007/s11356-017-8852-5
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DOI: https://doi.org/10.1007/s11356-017-8852-5