Advertisement

Oecologia

, Volume 191, Issue 4, pp 971–981 | Cite as

Assessing tree ring δ15N of four temperate deciduous species as an indicator of N availability using independent long-term records at the Fernow Experimental Forest, WV

  • Mark B. BurnhamEmail author
  • Mary Beth Adams
  • William T. Peterjohn
Ecosystem ecology – original research

Abstract

Nitrogen deposition in the northeastern US changed N availability in the latter part of the twentieth century, with potential legacy effects. However, long-term N cycle measurements are scarce. N isotopes in tree rings have been used as an indicator of N availability through time, but there is little verification of whether species differ in the strength of this signal. Using long-term records at the Fernow Experimental Forest in West Virginia, we examined the relationship between soil conditions, including net nitrification rates, and wood δ15N in 2014, and tested the strength of correlation between tree ring δ15N of four species and stream water NO3 loss from 1971 to 2000. Higher soil NO3 was weakly associated with higher wood δ15N across species, and higher soil net nitrification rates were associated with higher δ15N for Quercus rubra only. The δ15N of Liriodendron tulipifera and Q. rubra, but neither Fagus grandifolia nor Prunus serotina, was correlated with stream water NO3. L. tulipifera tree ring δ15N had a stronger association with stream water NO3 than Q. rubra. Overall, we found only limited evidence of a relationship between soil N cycling and tree ring δ15N, with a strong correlation between the wood δ15N and NO3 leaching loss through time for one of four species. Tree species differ in their ability to preserve legacies of N cycling in tree ring δ15N, and given the weak relationships between contemporary wood δ15N and soil N cycle measurements, caution is warranted when using wood δ15N to infer changes in the N cycle.

Keywords

Dendroisotope Wood δ15Nitrogen deposition Watershed Fernow Experimental Forest 

Notes

Acknowledgements

The authors thank Chris Walter, Rachel Arrick, Jessica Graham, Hoff Lindberg, Hannah Hedrick, and Leah Baldinger for their field and laboratory assistance on this study. We also acknowledge the USDA Forest Service staff at the Fernow Experimental Forest for long-term management of the site and support of this project. This work was supported by the Long-Term Research in Environmental Biology (LTREB) program at the National Science Foundation (Grant nos. DEB-0417678 and DEB-1019522) and the WVU Department of Biology and Eberly College of Arts and Sciences.

Author contribution statement

MBB and WTP conceived the idea. MBA maintained and processed long-term N data, and MBB and WTP performed field core and soil collection and laboratory analyses. MBA provided editorial advice, and MBB and WTP analyzed the data and wrote the manuscript.

Supplementary material

442_2019_4528_MOESM1_ESM.pdf (483 kb)
Supplementary material 1 (PDF 482 kb)

References

  1. Aber J, McDowell W, Nadelhoffer K et al (1998) Nitrogen saturation in temperate forest ecosystems. Bioscience 48:921–934CrossRefGoogle Scholar
  2. Bahr A, Ellström M, Akselsson C et al (2013) Growth of ectomycorrhizal fungal mycelium along a Norway spruce forest nitrogen deposition gradient and its effect on nitrogen leakage. Soil Biol Biochem 59:38–48.  https://doi.org/10.1016/j.soilbio.2013.01.004 CrossRefGoogle Scholar
  3. Bazot S, Fresneau C, Damesin C, Barthes L (2016) Contribution of previous year’s leaf N and soil N uptake to current year’s leaf growth in sessile oak. Biogeosciences 13:3475–3484.  https://doi.org/10.5194/bg-13-3475-2016 CrossRefGoogle Scholar
  4. 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 41:1331–1338CrossRefGoogle Scholar
  5. Bunn AG (2010) Statistical and visual crossdating in R using the dplR library. Dendrochronologia 28:251–258.  https://doi.org/10.1016/j.dendro.2009.12.001 CrossRefGoogle Scholar
  6. Bunn AG, Helfield JM, Gerdts JR et al (2017) A solvent-based extraction fails to remove mobile nitrogen from western redcedar (Thuja plicata). Dendrochronologia 44:19–21.  https://doi.org/10.1016/j.dendro.2017.03.001 CrossRefGoogle Scholar
  7. Burnham MB, McNeil BE, Adams MB, Peterjohn WT (2016) The response of tree ring δ15N to whole-watershed urea fertilization at the Fernow Experimental Forest, WV. Biogeochemistry 130:133–145.  https://doi.org/10.1007/s10533-016-0248-y CrossRefGoogle Scholar
  8. Burnham MB, Cumming JR, Adams MB, Peterjohn WT (2017) Soluble soil aluminum alters the relative uptake of mineral nitrogen forms by six mature temperate broadleaf tree species: possible implications for watershed nitrate retention. Oecologia.  https://doi.org/10.1007/s00442-017-3955-8 CrossRefPubMedGoogle Scholar
  9. Caceres MLL, 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.  https://doi.org/10.1002/rcm.5227 CrossRefPubMedGoogle Scholar
  10. Campbell JL, Hornbeck JW, Mitchell MJ et al (2004) Input-output budgets of inorganic nitrogen for 24 forest watersheds in the northeastern United States: a review. Water Air Soil Pollut 151:373–396CrossRefGoogle Scholar
  11. Crowley KF, Lovett GM (2017) Effects of nitrogen deposition on nitrate leaching from forests of the northeastern United States will change with tree species composition. Can J For Res 47:997–1009.  https://doi.org/10.1139/cjfr-2016-0529 CrossRefGoogle Scholar
  12. Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Peñuelas J, Reich PB, Schuur EAG, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ (2009) Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183(4):980–992CrossRefGoogle Scholar
  13. Del Arco JM, Escudero A, Garrido MV (1991) Effects of site characteristics on nitrogen retranslocation from senescing leaves. Ecology 72:701–708.  https://doi.org/10.2307/2937209 CrossRefGoogle Scholar
  14. Edwards P, Helvey J (1991) Long-term ionic increases from a Central Appalachian forested watershed. J Environ Qual 20:250–255CrossRefGoogle Scholar
  15. El Zein R, Maillard P, Bréda N et al (2011) Seasonal changes of C and N non-structural compounds in the stem sapwood of adult sessile oak and beech trees. Tree Physiol 31:843–854.  https://doi.org/10.1093/treephys/tpr074 CrossRefPubMedGoogle Scholar
  16. Elhani S, Lema B, Zeller B et al (2003) Inter-annual mobility of nitrogen between beech rings: a labelling experiment. Ann For Sci 60:503–508.  https://doi.org/10.1051/forest CrossRefGoogle Scholar
  17. Elhani S, Guehl J-M, Nys C et al (2005) Impact of fertilization on tree-ring δ15N and δ13C in beech stands: a retrospective analysis. Tree Physiol 25:1437–1446CrossRefGoogle Scholar
  18. Elliott EM, Kendall C, Wankel SD et al (2007) Nitrogen isotopes as indicators of NOx source contributions to atmospheric nitrate deposition across the midwestern and northeastern United States. Environ Sci Technol 41:7661–7667CrossRefGoogle Scholar
  19. Elmore AJ, Nelson DM, Craine JM (2016) Earlier springs are causing reduced nitrogen availability in North American eastern deciduous forests. Nat Plants 2:16133.  https://doi.org/10.1038/nplants.2016.133 CrossRefPubMedGoogle Scholar
  20. Falxa-Raymond N, Patterson AE, Schuster WSF, Griffin KL (2012) Oak loss increases foliar nitrogen, δ15N and growth rates of Betula lenta in a northern temperate deciduous forest. Tree Physiol 32:1092–1101.  https://doi.org/10.1093/treephys/tps068 CrossRefPubMedGoogle Scholar
  21. Galloway J, Dentener F, Capone D et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  22. Garten C (1993) Variation in foliar 15N abundance and the availability of soil nitrogen on Walker Branch Watershed. Ecology 74:2098–2113CrossRefGoogle Scholar
  23. Gerhart LM, McLauchlan KK (2014) Reconstructing terrestrial nutrient cycling using stable nitrogen isotopes in wood. Biogeochemistry 120:1–21.  https://doi.org/10.1007/s10533-014-9988-8 CrossRefGoogle Scholar
  24. Gilliam FS, Adams MB (2011) Effects of nitrogen on temporal and spatial patterns of nitrate in streams and soil solution of a central hardwood forest. ISRN Ecol 2011:1–9CrossRefGoogle Scholar
  25. Gilliam FS, Adams MB, Yurish BM (1996) Ecosystem nutrient responses to chronic nitrogen inputs at Fernow Experimental Forest, West Virginia. Can J For Res 26:196–205CrossRefGoogle Scholar
  26. Gilliam FS, Yurish BM, Adams MB (2001) Temporal and spatial variation of nitrogen transformations in nitrogen-saturated soils of a central Appalachian hardwood forest. Can J For Res 31:1768–1785.  https://doi.org/10.1139/cjfr-31-10-1768 CrossRefGoogle Scholar
  27. Gilliam FS, Welch NT, Phillips AH et al (2016) Twenty-five-year response of the herbaceous layer of a temperate hardwood forest to elevated nitrogen deposition. Ecosphere 7:e01250.  https://doi.org/10.1002/ecs2.1250 CrossRefGoogle Scholar
  28. Gilliam FS, Walter CA, Adams MB, Peterjohn WT (2018) Nitrogen (N) dynamics in the mineral soil of a Central Appalachian hardwood forest during a quarter century of whole-watershed N additions. Ecosystems 21:1489–1504.  https://doi.org/10.1007/s10021-018-0234-4 CrossRefGoogle Scholar
  29. Goodale CL (2017) Multiyear fate of a 15N tracer in a mixed deciduous forest: retention, redistribution, and differences by mycorrhizal association. Glob Change Biol 23:867–880.  https://doi.org/10.1111/gcb.13483 CrossRefGoogle Scholar
  30. Handley LL, Raven JA (1992) The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant Cell Environ 15:965–985.  https://doi.org/10.1111/j.1365-3040.1992.tb01650.x CrossRefGoogle Scholar
  31. Härdtle W, Niemeyer T, Assmann T et al (2013) Long-term trends in tree-ring width and isotope signatures (δ13C, δ15N) of Fagus sylvatica L. on soils with contrasting water supply. Ecosystems 16:1413–1428.  https://doi.org/10.1007/s10021-013-9692-x CrossRefGoogle Scholar
  32. Hart SC, Classen AT (2003) Potential for assessing long-term dynamics in soil nitrogen availability from variations in δ15N of tree rings. Isotopes Environ Health Stud 39:15–28.  https://doi.org/10.1080/1025601031000102206 CrossRefPubMedGoogle Scholar
  33. Heaton THE (1990) 15N/14N ratios of NOx from vehicle engines and coal-fired power stations. Tellus 42:304–307.  https://doi.org/10.3402/tellusb.v42i3.15223 CrossRefGoogle Scholar
  34. 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(6056):664–666CrossRefGoogle Scholar
  35. Hobbie EA, Högberg P (2012) Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol 196:367–382.  https://doi.org/10.1111/j.1469-8137.2012.04300.x CrossRefPubMedGoogle Scholar
  36. Hobbie EA, Ouimette AP (2009) Controls of nitrogen isotope patterns in soil profiles. Biogeochemistry 95:355–371.  https://doi.org/10.1007/s10533-009-9328-6 CrossRefGoogle Scholar
  37. Högberg P, Johannisson C (1993) 15N abundance of forests is correlated with losses of nitrogen. Plant Soil 157:147–150CrossRefGoogle Scholar
  38. Högberg P, Johannisson C, Högberg MN (2014) Is the high 15N natural abundance of trees in N-loaded forests caused by an internal ecosystem N isotope redistribution or a change in the ecosystem N isotope mass balance? Biogeochemistry 117:351–358.  https://doi.org/10.1007/s10533-013-9873-x CrossRefGoogle Scholar
  39. Kjøller R, Nilsson L, Hansen K et al (2012) Dramatic changes in ectomycorrhizal community composition, root tip abundance and mycelial production along a stand-scale nitrogen deposition gradient. New Phytol 194:278–286CrossRefGoogle Scholar
  40. Kochenderfer JN (2006) Fernow and the Appalachian Hardwood Region. In: Adams M, DeWalle D, Hom J (eds) The Fernow Watershed acidification study. Springer, Dordrecht, pp 17–39CrossRefGoogle Scholar
  41. Kranabetter JM, Meeds JA (2017) Tree ring δ15N as validation of space-for-time substitution in disturbance studies of forest nitrogen status. Biogeochemistry 134:201–215.  https://doi.org/10.1007/s10533-017-0355-4 CrossRefGoogle Scholar
  42. Kranabetter JM, Saunders S, MacKinnon JA et al (2013) An assessment of contemporary and historic nitrogen availability in contrasting coastal Douglas-fir forests through δ15N of tree rings. Ecosystems 116:111–122.  https://doi.org/10.1007/s10021-012-9598-z CrossRefGoogle Scholar
  43. Lin G, Mccormack ML, Ma C, Guo D (2017) Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests. New Phytol 213:1440–1451.  https://doi.org/10.1111/nph.14206 CrossRefPubMedGoogle Scholar
  44. Lovett GM, Goodale CL (2011) A new conceptual model of nitrogen saturation based on experimental nitrogen addition to an oak forest. Ecosystems 14:615–631.  https://doi.org/10.1007/s10021-011-9432-z CrossRefGoogle Scholar
  45. Lovett GM, Weathers KC, Arthur MA (2002) Control of nitrogen loss from forested watersheds by soil carbon:nitrogen ratio and tree species composition. Ecosystems 5:712–718.  https://doi.org/10.1007/s10021-002-0153-1 CrossRefGoogle Scholar
  46. Lovett GM, Weathers KC, Arthur MA, Schultz JC (2004) Nitrogen cycling in a northern hardwood forest: do species matter? Biogeochemistry 67:289–308.  https://doi.org/10.1023/B:BIOG.0000015786.65466.f5 CrossRefGoogle Scholar
  47. Lovett GM, Goodale CL, Ollinger SV et al (2018) Nutrient retention during ecosystem succession: a revised conceptual model. Front Ecol Environ 16:1–7.  https://doi.org/10.1002/fee.1949 CrossRefGoogle Scholar
  48. Martinelli LA, Piccolo MC, Townsend AR et al (1999) Nitrogen stable isotopic composition of leaves and soil: tropical versus temperate forests. Biogeochemistry 46:45–65Google Scholar
  49. May JD, Burdette SB, Gilliam FS, Adams MB (2005) Interspecific divergence in foliar nutrient dynamics and stem growth in a temperate forest in response to chronic nitrogen inputs. Can J For Res 35:1023–1030.  https://doi.org/10.1139/x05-036 CrossRefGoogle Scholar
  50. McLauchlan KK, Craine JM (2012) Species-specific trajectories of nitrogen isotopes in Indiana hardwood forests, USA. Biogeosciences 9:867–874.  https://doi.org/10.5194/bg-9-867-2012 CrossRefGoogle Scholar
  51. McLauchlan KK, Craine JM, Oswald WW et al (2007) Changes in nitrogen cycling during the past century in a northern hardwood forest. Proc Natl Acad Sci USA 104:7466–7470.  https://doi.org/10.1073/pnas.0701779104 CrossRefPubMedGoogle Scholar
  52. McLauchlan KK, Gerhart LM, Battles JJ et al (2017) Centennial-scale reductions in nitrogen availability in temperate forests of the United States. Sci Rep 7:7856.  https://doi.org/10.1038/s41598-017-08170-z CrossRefPubMedPubMedCentralGoogle Scholar
  53. Millard P, Grelet GA (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095.  https://doi.org/10.1093/treephys/tpq042 CrossRefPubMedGoogle Scholar
  54. National Atmospheric Deposition Program (NADP) (2016) NADP Program Office, Wisconsin State Laboratory of Hygiene, 465 Henry Mall, Madison, WI 53706Google Scholar
  55. Pardo LH, Nadelhoffer KJ (2012) Using nitrogen isotope ratios to assess terrestrial ecosystems at regional and global scales. In: West JB, Bowen GJ, Dawson TE, Tu KP (eds) Isoscapes. Springer, Dordrecht, pp 221–249Google Scholar
  56. Pardo LH, Templer PH, Goodale CL et al (2006) Regional assessment of N saturation using foliar and root δ15N. Biogeochemistry 80:143–171.  https://doi.org/10.1007/s10533-006-9015-9 CrossRefGoogle Scholar
  57. Peterjohn WT, Adams MB, Gilliam FS (1996) Symptoms of nitrogen saturation in two central Appalachian hardwood forest ecosystems. Biogeochemistry 35:507–522CrossRefGoogle Scholar
  58. Peterjohn WT, Harlacher MA, Christ MJ, Adams MB (2015) Testing associations between tree species and nitrate availability: do consistent patterns exist across spatial scales? For Ecol Manag 358:335–343.  https://doi.org/10.1016/j.foreco.2015.09.018 CrossRefGoogle Scholar
  59. Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests. New Phytol 199:41–51.  https://doi.org/10.1111/nph.12221 CrossRefPubMedGoogle Scholar
  60. Piatek KB, Munasinghe P, Peterjohn WT et al (2009) Oak contribution to litter nutrient dynamics in an Appalachian forest receiving elevated nitrogen and dolomite. Can J For Res 39:936–944.  https://doi.org/10.1139/X09-028 CrossRefGoogle Scholar
  61. 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.  https://doi.org/10.1016/0009-2541(95)00097-6 CrossRefGoogle Scholar
  62. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  63. Reimchen TE, Arbellay E (2018) Intra-annual variability in isotopic and total nitrogen in tree rings of old growth Sitka spruce from coastal British Columbia. Botany 96:851–857CrossRefGoogle Scholar
  64. Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153–162CrossRefGoogle Scholar
  65. Rose LA, Elliott EM, Adams MB (2015) Triple nitrate Isotopes indicate differing nitrate source contributions to streams across a nitrogen saturation gradient. Ecosystems 18:1209–1223.  https://doi.org/10.1007/s10021-015-9891-8 CrossRefGoogle Scholar
  66. Saurer M, Cherubini P, Ammann M et al (2004) First detection of nitrogen from NOx in tree rings: a 15 N/14 N study near a motorway. Atmos Environ 38:2779–2787.  https://doi.org/10.1016/j.atmosenv.2004.02.037 CrossRefGoogle Scholar
  67. Savard MM, Bégin C, Smirnoff A et al (2009) Tree-ring nitrogen isotopes reflect anthropogenic NOx emissions and climatic effects. Environ Sci Technol 43:604–609CrossRefGoogle Scholar
  68. Schuler T, Gillespie A (2000) Temporal patterns of woody species diversity in a central Appalachian forest from 1856 to 1997. J Torrey Bot Soc 127:149–161CrossRefGoogle Scholar
  69. 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.  https://doi.org/10.1023/B:PLSO.0000037047.16616.98 CrossRefGoogle Scholar
  70. Templer PH, Arthur MA, Lovett GM, Weathers KC (2007) Plant and soil natural abundance δ15N: indicators of relative rates of nitrogen cycling in temperate forest ecosystems. Oecologia 153:399–406.  https://doi.org/10.1007/s00442-007-0746-7 CrossRefPubMedGoogle Scholar
  71. Tomlinson G, Siegwolf R, Buchmann N et al (2014) The mobility of nitrogen across tree-rings of Norway spruce (Picea abies L.) and the effect of extraction method on tree-ring δ15N and δ13C values. Rapid Commun Mass Spectrom 28:1–7.  https://doi.org/10.1002/rcm.6897 CrossRefGoogle Scholar
  72. Tomlinson G, Buchmann N, Siegwolf R et al (2016) Can tree-ring δ15N be used as a proxy for foliar δ15N in European beech and Norway spruce? Trees Struct Funct 30:627–638.  https://doi.org/10.1007/s00468-015-1305-1 CrossRefGoogle Scholar
  73. Vitousek PM, Reiners WA (1975) Ecosystem succession and nutrient retention: a hypothesis. Bioscience 25:376–381CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Center for Advanced Bioenergy and Bioproducts InnovationUniversity of Illinois Urbana-ChampaignUrbanaUSA
  2. 2.USDA Forest Service Northern Research StationMorgantownUSA
  3. 3.Department of BiologyWest Virginia UniversityMorgantownUSA

Personalised recommendations