Abstract
Although recent anthropogenic effects on the global nitrogen (N) cycle have been significant, the consequences of increased anthropogenic N on terrestrial ecosystems are unclear. Studies of the impact of increased reactive N on forest ecosystems—impacts on hydrologic and gaseous loss pathways, retention capacity, and even net primary productivity—have been particularly limited by a lack of long-term baseline biogeochemical data. Stable nitrogen isotope analysis (ratio of 15N to 14N, termed δ15N) of wood chronologies offers the potential to address changes in ecosystem N cycling on millennial timescales and across broad geographic regions. Currently, nearly 50 studies have been published utilizing wood δ15N records; however, there are significant differences in study design and data interpretation. Here, we identify four categories of wood δ15N studies, summarize the common themes and primary findings of each category, identify gaps in the spatial and temporal scope of current wood δ15N chronologies, and synthesize methodological frameworks for future research by presenting eight suggestions for common methodological approaches and enhanced integration across studies. Wood δ15N records have the potential to provide valuable information for interpreting modern biogeochemical cycling. This review serves to advance the utility of this technique for long-term biogeochemical reconstructions.
References
Ammann M, Siegwolf R, Pichlmayer F, Suter M, Saurer M, Brunold C (1999) Estimating the uptake of traffic-derived NO2 from 15N abundance in Norway spruce needles. Oecologia 118:124–131
Argerich A, Johnson SL, Sebestyen SD, Rhoades CC, Greathouse E, Knoepp JD, Adams MB, Likens GE Campbell JL, McDowell WH, Scatena FN, Ice GG (2013) Trends in stream nitrogen concentrations for forested reference catchments across the USA. Environ Res Lett 8:014039
Bai E, Houlton BZ, Wang YP (2012) Isotopic identification of nitrogen hotspots across natural terrestrial ecosystems. Biogeosciences 9:3287–3304
Balster NJ, Marshall JD, Clayton M (2009) Coupling tree-ring δ13C and δ15N to test the effect of fertilization on mature Douglas-fir (Pseudotsuga menziesii var. glauca) stands across the Interior northwest, USA. Tree Physiol 29:1491–1501
Bao W, O’Malley DM, Sederoff RR (1992) Wood contains a cell-wall structural protein. Proc Natl Acad Sci USA 89:6604–6608
Batterman SA, Hedin LO, van Breugel M, Ransijn J, Craven DJ, Hall JS (2013) Key role of symbiotic dinitrogen fixation in tropical forest secondary succession. Nature 502:224–227
Battipaglia G, Marzaioli F, Lubritto C, ALtieri S, Strumia S, Cherubini P, Cotrufo MF (2010) Traffic pollution affects tree-ring width and isotopic composition of Pinus pinea. Sci Total Environ 408:586–593
Beghin R, Cherubini P, Battipaglia G, Siegwolf R, Saurer M, Bovio G (2011) Tree-ring growth and stable isotopes (δ13C and δ15N) detect effects of wildfires on tree physiological processes in Pinus sylvestris L. Trees 25:627–636
Bernal S, Hedin LO, Likens GE, Gerber S, Buso DC (2012) Complex response of the forest nitrogen cycle to climate change. Proc Natl Acad Sci USA 109:3406–3411
Bukata AR, Kyser TK (2005) Response of the nitrogen isotopic composition of tree-rings following tree-clearing and land-use change. Environ Sci Technol 39:7777–7783
Bukata AR, Kyser TK (2007) Carbon and nitrogen isotope variations in tree-rings as records of perturbations in regional carbon and nitrogen cycles. Environ Sci Technol 41:1331–1338
Chapin FS, Matson PA, Vitousek P, Chapin MC (2011) Principles of terrestrial ecosystem ecology. Springer-Verlag, New York
Choi W-J, Lee S-M, Chang SX, Ro H-M (2005) Variation of δ13C and δ15N in Pinus densiflora tree-rings and their relationship to environmental changes in Eastern Korea. Water Air Soil Poll 164:173–187
Choi W-J, Chang SX, Bhatti JS (2007) Drainage affects tree growth and C and N dynamics in a minerotrophic peatland. Ecology 88:443–453
Craine JM et al (2009) Global patterns of oliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations and nitrogen availability. New Phytol 183:980–992
Craine JM et al (2014) Convergence of terrestrial nitrogen loss patterns across global climate gradients. Nat Geosci, in review (Personal communication)
Cuoto-Vázquez A, González-Prieto SJ (2010) Effects of climate, tree age, dominance and growth on δ15N in young pinewoods. Trees 24:507–514
Doucet A, Savard MM, Bégin C, Smirnoff A (2011) Is wood pre-treatment essential for tree-ring nitrogen concentration and isotope analysis? Rapid Commun Mass Sp 25:469–475
Doucet A, Savard MM, Bégin C, Smirnoff A (2012) Tree-ring δ15N values to infer air quality changes at regional scale. Chem Geol 320–321:9–16
Drake DC, Sheppard PJ, Naiman RJ (2011) Relationships between salmon abundance and tree ring δ15N: three objective tests. Can J For Res 41:2423–2432
Elhani S, Lema BF, Zeller B, Bréchet C, Guehl J-M, Dupouey J-L (2003) Inter-annual mobility of nitrogen between beech rings: a labelling experiment. Ann For Sci 60:503–508
Elhani S, Guehl J-M, Nys C, PIcard J-F, Dupouey J-L (2005) Impact of fertilization on tree-ring δ15N and δ13C in beech stands: a retrospective analysis. Tree Physiol 25:1437–1446
Elliott EM, Kendall C, Wankel SD, Burns DA, Boyer EW, Harlin K, Bain DJ, Butler TJ (2007) Nitrogen isotopes as indicators of NOx source contributions to atmospheric nitrate deposition across the midwestern and northeastern United States. Environ Sci Technol 41:7661–7667
Elliott EM, Kendall C, Boyer E, Burns DA, Lear GG, Golden HE, Harlin K, Bytnerowicz A, Butler TJ, Glatz R (2009) Dual nitrate isotopes in dry deposition: utility for partitioning NOx source contributions to landscape nitrogen deposition. J Geophys Res 114:G04020
Emmett BA, Kjønaas OJ, Gundersen P, Koopmans C, Tietema A, Sleep D (1998) Natural abundance of 15N in forests across a nitrogen deposition gradient. Forest Ecology and Management 101:9–18
Eronen M, Zetterberg P, Briffa KR, Lindholm M, Meriläinen J, Timonen M (2002) The supra-long Scots pine tree-ring record for Finnish Lapland: part 1, chronology construction and initial inferences. Holocene 12:673–680
Felix JD, Elliott EM, Shaw SL (2012) Nitrogen isotopic composition of coal-fired power plant NOx: influence of emission controls and implications for global emissions inventories. Environ Sci Technol 46:3528–3535
Ferguson CW (1968) Bristlecone pine: science and esthetics A 7100-year tree-ring chronology aids scientists; old trees draw visitors to California mountains. Science 159:839–846
Freyer HD, Kely D, Volz-Thomas A, Kobel K (1993) On the interaction of isotopic exchange processes with photochemical reactions in atmospheric oxides of nitrogen. J Geophys Res 98:14791–14796
Galloway J, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892
Gerhart LM, Harris JM, Nippert JB, Sandquist DR, Ward JK (2012) Glacial trees from the La Brea tar pits show physiological constraints of low CO2. New Phytol 194:63–69
Guerrieri MR, Saurer M, Siegwolf RTW, Waldner P, Cherubini P (2006) Impatto del traffico veicolare su δ15N, δ13C e δ18O di aghi ed anelli annuali di abete rosso (Picea abies L.) presso un’autostrada in Svizzera. Forest@ 3:437–445
Guerrieri MR, Siegwolf RTW, Saurer M, Jäggi M, Cherubini P, Ripullone F, Borghetti M (2009) Impact of different nitrogen emission sources on tree physiology as assessed by a triple stable isotope approach. Atmos Environ 43:410–418
Guerrieri MR, Siegwolf R, Saurer M, Ripullone F, Mencuccini M, Borghetti M (2010) Anthropogenic NOx emissions alter the intrinsic water-use efficiency (WUEi) for Quercus cerris stands under Mediterranean climate conditions. Environ Pollut 158:2841–2847
Guerrieri MR, Mencuccini M, Sheppard LJ, Saurer M, Perks MP, Levy P, Sutton MA, Borghetti M, Grace J (2011) The legacy of enhanced N and S deposition as revealed by the combined analysis of δ13C, δ18O and δ15N in tree rings. Glob Change Biol 17:1946–1962
Härdtle W et al (2013) Long-term trends in tree-ring width and isotope signatures (δ13C, δ15N) of Fagus sylvatics L. on soils with contrasting water supply. Ecosystems 16:1413
Hart SC, Classen AT (2003) Potential for assessing long-term dynamics in soil nitrogen availability from variations in δ15N of tree rings. Isot Environ Health Stud 39:15–28
Hastings MG, Casciotti KL, Elliott EM (2013) Stable isotopes as tracers of anthropogenic nitrogen sources, deposition, and impacts. Elements 9:339–344
Heaton THE (1990) 15N/14N ratios of NOx from vehicle engines and coal-fired power stations. Tellus 42B:304–307
Hietz P, Dünisch O, Wanek W (2010) Long-term trends in nitrogen isotope composition and nitrogen concentration in Brazilian rainforest trees suggest changes in nitrogen cycle. Environ Sci Technol 44:1191–1196
Hietz P, Turner BL, Wanek W, Richter A, Nock CA, Wright SJ (2011) Long-term change in the nitrogen cycle of tropical forests. Science 334:664–666
Hobbie EA, Högberg P (2012) Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol 196:367–382
Högberg P (1997) Tansley review no. 95 15N natural abundance in soil-plant systems. New Phytol 137:179–203
Holdaway RN, Hawke DJ, Hyatt OM, Wood GC (2007) Stable isotopic (δ15N, δ13C) analysis of wood in trees growing in past and present colonies of burrow-nesting seabirds in New Zealand. I. δ15N in two species of conifer (Podocarpaceae) from a mainland colony of Westland petrels (Procellaria westlandica), Punakaiki, South Island. J R Soc N Z 37:75–84
Holland EA, Braswell BH, Sulzman J, Lamarque J-F (2005) Nitrogen deposition onto the United States and western Europe: synthesis of observations and models. Ecol Appl 15:38–57
Houlton BZ, Sigman DM, Hedin LO (2006) Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc Natl Acad Sci USA 103:8745–8750
Houlton BZ, Boyer E, Finzi A, Galloway J, Leach A, Liptzin D, Melillo JM, Rosenstock TS, Sobota D, Townsend AR (2013) Intentional versus unintentional nitrogen use in the United States: trends, efficiency and implications. Biogeochemistry 114:11–23
Jai G, Chen F (2010) Monthly variations in nitrogen isotopes of ammonium and nitrate in wet deposition at Guangzhou, south China. Atmos Environ 44:2309–2315
Jardine TD, Cunjack RA (2005) Analytical error in stable isotope ecology. Oecologia 144:528–533
Jung K, Choi W-J, Chang SX, Arshad MA (2013) Soil and tree ring chemistry of Pinus banksiana and Populus tremuloides stands as indicators of changes in atmospheric environments in the oil sands region of Alberta, Canada. Ecol Indic 25:256–265
Koopmans CJ, Tietema A, Boxman AW (1996) The fate of 15N enriched throughfall in two coniferous forest stands at different nitrogen deposition levels. Biogeochemistry 34:19–44
Kranabetter JM, Saunders S, MacKinnon JA, Klassen H, Spittlehouse DL (2013) As assessment of contemporary and historic nitrogen availability in contrasting coastal Douglas-fir forests through δ15N of tree rings. Ecosystems 16:111–122
Kundu S, Kawamura K, Lee M (2010) Seasonal variation of the concentrations of nitrogenous species and their nitrogen isotopic ratios in aerosols at Gosan, Jeju Island: implications for atmospheric processing and source changes of aerosols. J Geophys Res 115:D20305
Kwak J-H, Lim S-S, Park H-J, Lee S-I, Lee K-H, Kim H-Y, Chang SX, Lee S-M, Ro H-M, Choi W-J (2009) Relating tree ring chemistry of Pinus densiflora to precipitation acidity in an industrial area of South Korea. Water Air Soil Pollut 199:95–106
Kwak J-H, Lim S-S, Chang SX, Lee K-H, Choi W-J (2011) Potential use of δ13C, δ15N, N concentration, and Ca/Al of PInus densiflora tree rings in estimating historical precipitation pH. J Soils Sediments 11:709–721
Larry L, Chitoshi M, Mizota C, Yamanaka T, Nobori Y (2010) Temporal changes in tree-ring nitrogen of Pinus thunbergii trees exposed to black-tailed gull (Larus crassirostris) breeding colonies. Appl Geochem 25:1699–1702
Larry L, Chitoshi M, Mizota C, Yamanaka T, Nobori Y (2011) Effects of pre-treatment on the nitrogen isotope composition of Japanese black pine (Pinus thunbergii) tree-rings as affected by high N input. Rapid Commun Mass Spectrom 25:3298–3302
Leavitt SW, Danzer SR (1993) Method for batch processing small wood samples to holocellulose for stable-carbon isotope analysis. Anal Chem 55:87–89
Leavitt SW, Long A (1986) Stable-carbon isotope variability in tree foliage and wood. Ecology 67:1002–1010
Leonelli G, Battipaglia G, Siegwolf RTW, Saurer M, Morra di Cella U, Cherubini P, Pelfini M (2012) Climatic isotope signals in tree rings masked by air pollution: a case study conducted along the Mont Blanc Tunnel access road (Western Alps, Italy). Atmos Environ 61:169–179
Lovett GM, Weathers KC, Arthur MA, Schultz JC (2004) Nitrogen cycling in a northern hardwood forest: do species matter? Biogeochemistry 67:289–308
Mara P, Mihalopoulos N, Gogou A, Daehnke K, Schlarbaum T, Emeis K-C, Krom M (2009) Isotopic composition of nitrate in wet and dry atmospheric deposition on Crete in the eastern Mediterranean Sea. Glob Biogeochem Cycles 23:GB4002
McLauchlan KK, Craine JM (2012) Species-specific trajectories of nitrogen isotopes in Indiana hardwood forests, USA. Biogeosciences 9:867–874
McLauchlan KK, Craine JM, Oswalkd WW, Leavitt PR, Likens GE (2007) Changes in nitrogen cycling during the past century in a northern hardwood forest. Proc Natl Acad Sci USA 104:7466–7470
Mead DJ, Preston CM (1994) Distribution and retranslocation of 15N in lodgepole pine over eight growing seasons. Tree Physiol 14:389–402
Merrill W, Cowling EB (1966) Role of nitrogen in wood deterioration: amounts and distribution of nitrogen in tree stems. Can J Bot 44:1555–1579
Mizota C, MLL C, Yamanaka T, Nobori Y (2011) Differential response of two Pinus spp. to avian nitrogen input as revealed by nitrogen isotope analysis for tree rings. Isot Environ Health Stud 47:62–70
Nadelhoffer KJ, Colman BP, Currie WS, Magill AH, Aber JD (2004) Decadal-scale fates of 15N tracers added to oak and pine stands under ambient and elevated N inputs at the Harvard Forest (USA). Forest Ecol Manag 196:89–107
Nadelhoffer KJ, Downs MR, Fry B, Aber JD, Magill AH, Melillo JM (1995) The fate of 15N-labeled nitrate additions to a northern hardwood forest in eastern Maine, USA. Oecologia 103:292–301
Nadelhoffer KJ, Downs MR, Fry B (1999a) Sinks for 15N-enriched additions to an oak forest and a red pine plantation. Ecol Appl 9:72–86
Nadelhoffer KJ, Emmett BA, Gundersen P, Kjønaas OJ, Koopmans C, Schleppi P, Tietema A, Wright RF (1999b) Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–148
National Atmospheric Deposition Program (NRSP-3). 2007. NADP Program Office, Illinois State Water Survey, 2204 Griffith Dr., Champaign, IL 61820
Nommik H (1966) The uptake and translocation of fertilizer N15 in young trees of Scots pine and Norway spruce. Stueia For Suec 35:1–18
Park M, Randel WJ, Kinnison DE, Garcia RR, Choi W (2004) Seasonal variation o fmethane, water vapor, and nitrogen oxides near the tropopause: satellite observations and model simulations. J Geophys Res 109:D03302
Peñuelas J, Estiarte M (1997) Trends in plant carbon concentration and plant demand for N throughout this century. Oecologia 109:69–73
Poulson SR, Chamberlain CP, Friedland AJ (1995) Nitrogen isotope variation of tree rings as a potential indicator of environmental change. Chem Geol 125:307–315
Reimchen TE, Mathewson D, Hocking MD, Moran J (2002) Isotopic evidence for enrichment of salmon-derived nutrients in vegetation, soil, and insects in riparian zones in coastal British Columbia. In: Stockner J (ed) Nutrients in salmonid ecosystems: sustaining production and diversity, vol 34. American Fisheries Society Symposium, Bethesda, pp 59–69
Roden JS, Ehleringer JR (2000) Hydrogen and oxygen isotope ratios of tree ring cellulose for field-grown riparian trees. Oecologia 123:481–489
Rolff C, Elmgren R, Voss M (2008) Deposition of nitrogen and phosphorus on the Baltic Sea: seasonal patterns and nitrogen isotope composition. Biogeosciences 5:1657–1667
Saurer M, Cherubini P, Ammann M, Cinti BD, Siegwolf R (2004) First detection of nitrogen from NOx in tree rings: a 15N/14N study near a motorway. Atmos Environ 38:2779–2787
Savard MM (2010) Tree-ring stable isotopes and historical perspectives on pollution. Environ Pollut 158:2007–2013
Savard MM, Begin C, Smirnoff A, Marion J, Rioux-Paquette E (2009) Tree-ring nitrogen isotopes reflect anthropogenic NOx emissions and climatic effects. Environ Sci Technol 43:604–609
Schaub D, Weiss AK, Kaiser JW, Petritoli A, Richter A, Buchmann B, Burrows JP (2005) A transboundary transport episode of nitrogen dioxide as observed from GOME an its impact in the Alpine region. Atmos Chem Phys 5:23–37
Schleppi P, Bucher-Wallin I, Siegwolf R, Saurer M, Muller N, Bucher JB (1999) Simulation of increased nitrogen deposition to a montane forest ecosystem: partitioning of the added 15N. Water Air Soil Pollut 116:129–134
Schulze B, Wirth C, Linke P, Brand WA, Kuhlmann I, Horna V, Schulze E-D (2004) Laser ablation-combustion-GC-IRMS—a new method for online analysis of intra-annual variation of δ13C in tree rings. Tree Physiol 24:1193–1201
Sheppard PR, Thompson TL (2000) Effect of extraction on radial variation of nitrogen concentration in tree rings. J Environ Qual 29:2037–2042
Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23
Stock WD, Bourke L, Foend RH (2012) Dendroecological indicators of historical responses of pines to water and nutrient availability on a superficial aquifer in south-western Australia. For Ecol Manage 264:108–114
Sun F, Kuang Y, Wen D, Xu Z, Li J, Zuo W, Hou E (2010) Long-term tree growth rate, water use efficiency, and tree ring nitrogen isotope composition of Pinus massoniana L. in response to global climate change and local nitrogen deposition in Southern China. J Soils Sediments 10:1453–1465
Templer PH, Dawson TE (2004) Nitrogen uptake by four tree species of the Catskill Mountains, New York: implications for forest N dynamics. Plant Soil 262:251–261
Templer PH et al (2012) Sinks for nitrogen inputs in terrestrial ecosystem: a meta-analysis of 15N tracer field studies. Ecology 93:1816–1829
Vines TH, Albert AYK, Andrew RL, Débarre F, Bock DG, Franklin MT, Gilbert KJ, Moore J-S, Renaut S, Rennison DJ (2013) The availability of research data declines rapidly with article age. Curr Biol 24:94–97
Vitousek PM, Matson PA, van Cleve K (1989) Nitrogen availability and nitrification during succession: primary, secondary, and old-field seres. Plant Soil 115:229–239
Weber P, Bol R, Dixon L, Bardgett RD (2008) Large old trees influence patterns of δ13C and δ15N in forests. Rapid Commun Mass Spectrom 22:1627–1630
Wolfe AP, Hobbs WO, Birks HH, Briner JP, Holmgren SU, Ingólfsson Ó, Kaushal SS, Miller GH, Pagani M, Saros JE, Vinebrooke RD (2013) Stratigraphic expressions of the Holocene-Anthropocene transition revealed in sediments from remote lakes. Earth-Sci Rev 116:17–34
Wolkovich EM, Regetz J, O’Connor MI (2012) Advances in global change research require open science by individual researchers. Glob Change Biol 18:2102–2110
Acknowledgments
This work was funded in part by the National Science Foundation under grant NSF-DEB 1145815 to K.M. We thank members of the Novus Network for helpful discussions, and Joe Craine and Julie Commerford for technical assistance.
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Gerhart, L.M., McLauchlan, K.K. Reconstructing terrestrial nutrient cycling using stable nitrogen isotopes in wood. Biogeochemistry 120, 1–21 (2014). https://doi.org/10.1007/s10533-014-9988-8
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DOI: https://doi.org/10.1007/s10533-014-9988-8