Plant and Soil

, Volume 408, Issue 1–2, pp 343–356 | Cite as

Site-level importance of broadleaf deciduous trees outweighs the legacy of high nitrogen (N) deposition on ecosystem N status of Central Appalachian red spruce forests

  • Kenneth R. SmithEmail author
  • Justin M. Mathias
  • Brenden E. McNeil
  • William T. Peterjohn
  • Richard B. Thomas
Regular Article


Background and aims

Atmospheric nitrogen (N) deposition can influence forest ecosystem N status, and the resilience of forests to the effects of N deposition depends on a number of co-occurring environmental factors that regulate N retention or loss. In this study, we test the idea that N deposition may have important and long-lasting impacts on patterns of N cycling by using field and laboratory techniques to assess N status in seven high-elevation Central Appalachian red spruce (Picea rubens Sarg.) forests located at sites that historically received moderate to high inputs of N atmospheric deposition.


During 2011 and 2012, we measured multiple indices of N availability (e.g. foliar/soil C:N and δ15N, resin ion-exchange, and N transformation rates) that integrate N cycling over seasonal to decadal time scales. Using a model selection approach, we compared the strength of the association between various environmental factors and temporally-integrated indices of N status in a series of regression models.


Site-level differences in the relative importance value of broadleaf deciduous (BD) trees consistently explained most of the observed variation in N status. Soil C:N was significantly lower for sites with greater BD importance (R 2  = 0.67–0.77), and there was a strong positive relationship between BD importance and soil δ15N content (R 2  = 0.64–0.85). Despite a four-fold difference in historic deposition across the seven forest sites, we did not observe any significant relationships between site N status and N deposition.


These findings suggest that potential legacy effects of N deposition were obscured by the influence of BD importance on N status at these sites. Our results add strong support to the idea that predicting the resilience of forests to the effects of N deposition requires detailed knowledge on the contribution of tree species composition to soil N cycling and retention.


Nitrogen N deposition N availability Broadleaf deciduous trees Red spruce 



We would like to thank Amy Hessl, Bradley Breslow, and Benjamin Hedin for assistance with site selection and fieldwork. In addition, we thank the US Forest Service and, in particular, Stephanie Connolly and Kent Karriker for granting us access to these sites to perform fieldwork. Finally we would like to thank Edward Brzostek for his helpful comments and critiques on an earlier draft of this manuscript. This work was supported by the WVU Office of the Dean’s Awards for Research Team Scholarship (ARTS), the WVU Research Corporation’s Program to Stimulate Competitive Research (PSCoR), and in part by the National Science Foundation Research Experience for Undergraduates (NSF-REU) program.

Supplementary material

11104_2016_2940_MOESM1_ESM.pdf (277 kb)
ESM 1 (PDF 276 kb)


  1. Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM (1989) Nitrogen saturation in northern forest ecosystems. Bioscience 39:378–386CrossRefGoogle Scholar
  2. Aber J, McDowell W, Nadelhoffer K et al (1998) Nitrogen saturation in temperate forest ecosystems. Bioscience 48:921–934CrossRefGoogle Scholar
  3. Aber JD, Ollinger SV, Driscoll CT, Likens GE, Holmes RT, Freuder RJ, Goodale CL (2002) Inorganic nitrogen losses from a forested ecosystem in response to physical, chemical, biotic, and climatic perturbations. Ecosystems 5:648–658CrossRefGoogle Scholar
  4. Aber JD, Goodale CL, Ollinger SV et al (2003) Is nitrogen deposition altering the nitrogen status of northeastern forests? Bioscience 53:375–389CrossRefGoogle Scholar
  5. Boggs JL, McNulty SG, Gavazzi MJ, Myers JM (2005) Tree growth, foliar chemistry, and nitrogen cycling across a nitrogen deposition gradient in southern Appalachian deciduous forests. Can J Forest Res 35:1901–1913CrossRefGoogle Scholar
  6. Boggs JL, McNulty SG, Pardo LH (2007) Changes in conifer and deciduous forest foliar and forest floor chemistry and basal area tree growth across a nitrogen (N) deposition gradient in the northeastern US. Environ Pollut 149:303–314CrossRefPubMedGoogle Scholar
  7. Boxman AW, Vandam D, Vandijk HFG, Hogervorst RF, Koopmans CJ (1995) Ecosystem responses to reduced nitrogen and sulfur inputs into two coniferous forest stands in the Netherlands. Forest Ecol Manag 71:7–29CrossRefGoogle Scholar
  8. Boxman AW, van der Ven PJM, Roelefs JGM (1998) Ecosystem recovery after a decrease in nitrogen input to a Scots pine stand at Ysselsteyn, the Netherlands. Forest Ecol Manag 101:155–163CrossRefGoogle Scholar
  9. Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer-VerlagGoogle Scholar
  10. Chen Y, Högberg P (2006) Gross nitrogen mineralization rates still high 14 years after suspension of N input to a N-saturated forest. Soil Biol Biochem 38:2001–2003CrossRefGoogle Scholar
  11. Christ MJ, Peterjohn WT, Cumming JR, Adams MB (2002) Nitrification potentials and landscape, soil and vegetation characteristics in two Central Appalachian watersheds differing in NO3 export. Forest Ecol Manag 159:145–158CrossRefGoogle Scholar
  12. Christenson LM, Lovett GM, Weathers KC, Arthur MA (2009) The influence of tree species, nitrogen fertilization, and soil C to N ratio on gross soil nitrogen transformations. Soil Sci Soc Am J 73:638–646CrossRefGoogle Scholar
  13. Clark CM, Hobbie SE, Venterea R, Tilman D (2009) Long-lasting effects on nitrogen cycling 12 years after treatments cease despite minimal long-term nitrogen retention. Glob Change Biol 15:1755–1766CrossRefGoogle Scholar
  14. Clarkson RB (1964) Tumult on the Mountains: Lumbering in West Virginia 1770–1920. McClain Printing CompanyGoogle Scholar
  15. Corre MD, Lamersdorf NP (2004) Reversal of nitrogen saturation after long-term deposition reduction: impact on soil nitrogen cycling. Ecology 85:3090–3104CrossRefGoogle Scholar
  16. Crowley KF, McNeil BE, Lovett GM et al (2012) Do nutrient limitation patterns shift from nitrogen toward phosphorus with increasing nitrogen deposition across the Northeastern United States? Ecosystems 15:940–957CrossRefGoogle Scholar
  17. DeHayes DH, Schaberg PG, Hawley GJ, Strimbeck GR (1999) Acid rain impacts on calcium nutrition and forest health. Bioscience 49:789–800CrossRefGoogle Scholar
  18. Doane TA, Horwáth WR (2003) Spectrophotometric determination of nitrate with a single reagent. Anal Lett 36:2713–2722CrossRefGoogle Scholar
  19. 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 Ecol Manag 101:9–18CrossRefGoogle Scholar
  20. Finzi AC, Breemen NV, Canham CD (1998) Canopy tree-soil interactions within temperate forests: species effects on soil carbon and nitrogen. Ecol Appl 8:440–446Google Scholar
  21. Foster JR, Reiners WA (1983) Vegetation patterns in a virgin subalpine forest at Crawford Notch, White Mountains, New Hampshire. B Torrey Bot Club 110:141–153CrossRefGoogle Scholar
  22. Galloway JN, Dentener FJ, Capone DG et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  23. Garten CT Jr, Van Miegroet H (1994) Relationships between soil nitrogen dynamics and natural 15N abundance in plant foliage from Great Smoky Mountains National Park. Can J Forest Res 24:1636–1645CrossRefGoogle Scholar
  24. Goodale CL, Aber JD (2001) The long-term effects of land-use history on nitrogen cycling in northern hardwood forests. Ecol Appl 11:253–267CrossRefGoogle Scholar
  25. Goodale CL, Aber JD, McDowell WH (2000) The long-term effects of disturbance on organic and inorganic nitrogen export in the White Mountains, New Hampshire. Ecosystems 3:433–450CrossRefGoogle Scholar
  26. Gundersen P, Callesen I, de Vries W (1998) Nitrate leaching in forest ecosystems is related to forest floor C/N ratios. Environ Pollut 102:403–407CrossRefGoogle Scholar
  27. Hamburg SP, Cogbill CV (1988) Historical decline of red spruce populations and climatic warming. Nature 331:428–431CrossRefGoogle Scholar
  28. Högberg P, Johannisson C (1993) 15N abundance of forests is correlated with losses of nitrogen. Plant Soil 157:147–150CrossRefGoogle Scholar
  29. Hopkins AD (1899) Report on investigations to determine the cause of unhealthy conditions of the spruce and pine from 1880–1893. WV Agricultural Experimental Station. Fairmont Index Steam Print, MorgantownGoogle Scholar
  30. Iverson LR, Prasad AM, Matthews SN, Peters M (2008) Estimating potential habitat for 134 eastern US tree species under six climate scenarios. Forest Ecol Manag 254:390–406CrossRefGoogle Scholar
  31. Johnson AH, McLaughlin SB (1986) In: Gibson J (ed) The nature and timing of the deterioration of red spruce in the northern Appalachian Mountains. National Academy Press, Washington, DC, pp 200–230Google Scholar
  32. Johnson AH, Siccama TG (1983) Acid deposition and forest decline. Environ Sci Technol 17:294A–305ACrossRefPubMedGoogle Scholar
  33. Kelly CN (2010) Carbon and nitrogen cycling in watersheds of contrasting vegetation types in the Fernow Experimental Forest, West Virginia. PhD Dissertation, Virginia TechGoogle Scholar
  34. Kelly CN, Schoenholtz SH, Adams MB (2011) Soil properties associated with net nitrification following watershed conversion from Appalachian hardwoods to Norway spruce. Plant Soil 344:361–376CrossRefGoogle Scholar
  35. Koopmans CJ, Lubrecht WC, Tietema A (1995) Nitrogen transformations in two nitrogen saturated forest ecosystems subjected to an experimental decrease in nitrogen deposition. Plant Soil 175:205–218CrossRefGoogle Scholar
  36. Körner C (1989) The nutritional status of plants from high altitudes. Oecologia 81:379–391CrossRefGoogle Scholar
  37. Lal R (2005) Forest soils and carbon sequestration. Forest Ecol Manag 220:242–258CrossRefGoogle Scholar
  38. Le Quéré C, Peters GP, Andres RJ et al (2013) Global carbon budget 2013. Earth Sys Sci Data Discuss 6:689–760CrossRefGoogle Scholar
  39. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379CrossRefPubMedGoogle Scholar
  40. Lewis RL (1998) Transforming the Appalachian Countryside: railroads, deforestation, and social change in West Virginia, 1880–1990. University of North Carolina PressGoogle Scholar
  41. Lovett GM, Goodale CL (2011) A new conceptual model of nitrogen saturation based on experimental nitrogen addition to an Oak Forest. Ecosystems 14:615–631CrossRefGoogle Scholar
  42. Lovett GM, Rueth H (1999) Soil nitrogen transformations in beech and maple stands along a nitrogen deposition gradient. Ecol Appl 9:1330–1344CrossRefGoogle Scholar
  43. Lovett GM, Weathers KC, Sobczak WV (2000) Nitrogen saturation and retention in forested watersheds of the Catskill Mountains, New York. Ecol Appl 10:73–84CrossRefGoogle Scholar
  44. Lovett GM, Weathers KC, Arthur MA (2002) Control of nitrogen loss from forested watersheds by soil carbon: nitrogen ratio and tree species composition. Ecosystems 5:712–718CrossRefGoogle Scholar
  45. Lovett GM, Weathers KC, Arthur MA, Schultz JC (2004) Nitrogen cycling in a northern hardwood forest: do species matter? Biogeochemistry 67:289–308CrossRefGoogle Scholar
  46. Magill AH, Aber JD, Berntson GM, McDowell WH, Nadelhoffer KJ, Melillo JM, Steudler P (2000) Long-term nitrogen additions and nitrogen saturation in two temperate forests. Ecosystems 3:238–253CrossRefGoogle Scholar
  47. Mariotti A, Germon JC, Hubert P, Kaiser P, Letolle R, Tardieux A, Tardieux P (1981) Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant Soil 62:413–430CrossRefGoogle Scholar
  48. McNeil BE, Read JM, Driscoll CT (2007) Foliar nitrogen responses to elevated atmospheric nitrogen deposition in nine temperate forest canopy species. Environ Sci Technol 41:5191–5197CrossRefPubMedGoogle Scholar
  49. McNeil BE, Read JM, Sullivan TJ, McDonnell TC, Fernandez IJ, Driscoll CT (2008) The spatial pattern of nitrogen cycling in the Adirondack Park, New York. Ecol Appl 18:438–452CrossRefPubMedGoogle Scholar
  50. McNeil BE, Read JM, Driscoll CT (2012) Foliar nitrogen responses to the environmental gradient matrix of the Adirondack Park, New York. Ann Assoc Am Geogr 102:1–16CrossRefGoogle Scholar
  51. McNulty SG, Aber JD, Boone RD (1991) Spatial changes in forest floor and foliar chemistry of spruce-fir forests across New England. Biogeochemistry 14:13–29CrossRefGoogle Scholar
  52. McNulty SG, Boggs J, Aber JD, Rustad L, Magill A (2005) Red spruce ecosystem level changes following 14 years of chronic N fertilization. Forest Ecol Manag 219:279–291CrossRefGoogle Scholar
  53. Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626CrossRefGoogle Scholar
  54. Midgley MG, Phillips RP (2014) Mycorrhizal associations of dominant trees influence nitrate leaching responses to N deposition. Biogeochemistry 117:241–253CrossRefGoogle Scholar
  55. Murdoch PS, Burns DA, Lawrence GB (1998) Relation of climate change to the acidification of surface waters by nitrogen deposition. Environ Sci Technol 32:1642–1647CrossRefGoogle Scholar
  56. Nadelhoffer KJ, Fry B (1994) Nitrogen isotope studies in forest ecosystems. In: Lajtha K, Michener RJ (eds) Stable isotopes in ecology and environmental science, 2nd edn. Blackwell Scientific Publications, Oxford, pp 22–44Google Scholar
  57. Nadelhoffer KJ, Aber JD, Melillo JM (1985) Fine roots, net primary production, and soil nitrogen availability: a new hypothesis. 66:1377–1390Google Scholar
  58. Nadelhoffer KJ, Downs MR, Fry B, Aber JD, Magill AH, Melillo JM (1995) The fate of 15N-labelled nitrate additions to a northern hardwood forest in eastern Maine, USA. Oecologia 103:292–301CrossRefGoogle Scholar
  59. National Atmospheric Deposition Program (2014) Total deposition maps. Version 2014.02. Accessed 19 March 2015
  60. National Atmospheric Deposition Program (2016) NTN Data Access. NADP Program Office, Illinois State Water Survey, University of Illinois, Champaign, Accessed 1 January 2016Google Scholar
  61. Nowacki G, Wendt D (2010) The current distribution, predictive modeling, and restoration potential of red spruce in West Virginia. Proc Confe Ecol Manag High-Elevation Forest Central Southern Appalachian Mountains. USDA-FS Northern Research Station, Slatyfork, WV 163–178Google Scholar
  62. Ollinger SV, Smith ML, Martin ME, Hallett RA, Goodale CL, Aber JD (2002) Regional variation in foliar chemistry and N cycling among forests of diverse history and composition. Ecology 83:339–355Google Scholar
  63. Pan Y, Birdsey RA, Fang J et al (2011) A large and persistent carbon sink in the world’s forests. Science 333:988–993CrossRefPubMedGoogle Scholar
  64. Pardo LH, Schaberg PG, McNulty SG (1998) Response of natural abundance of 15N in spruce foliage to chronic N addition. Proc 83rd Ann Meet Ecol Soc America, Baltimore, MD 105Google Scholar
  65. Pardo LH, Hemond HF, Montoya JP, Fahey TJ, Siccama TG (2002) Response of the natural abundance of 15N in forest soils and foliage to high nitrate loss following clear-cutting. Can J Forest Res 32:1126–1136CrossRefGoogle Scholar
  66. Pardo LH, Templer PH, Goodale CL et al (2006) Regional assessment of N saturation using foliar and root δ15N. Biogeochemistry 80:143–171CrossRefGoogle Scholar
  67. Pardo LH, McNulty SG, Boggs JL, Duke S (2007) Regional patterns in foliar 15N across a gradient of nitrogen deposition in the northeastern US. Environ Pollut 149:293–302CrossRefPubMedGoogle Scholar
  68. Pastor J, Aber JD, McClaugherty CA, Melillo JM (1984) Aboveground production and N and P cycling along a nitrogen mineralization gradient on Blackhawk Island, Wisconsin. Ecology 65:256–268CrossRefGoogle Scholar
  69. Peterjohn WT, Foster CJ, Christ MJ, Adams MB (1999) Patterns of nitrogen availability within a forested watershed exhibiting symptoms of nitrogen saturation. Forest Ecol Manag 119:247–257CrossRefGoogle Scholar
  70. 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 199:41–51CrossRefPubMedGoogle Scholar
  71. Plymale AE, Boerner REJ, Logan TJ (1987) Relative nitrogen mineralization and nitrification in soils of two contrasting hardwood forests: effects of site microclimate and initial soil chemistry. Forest Ecol Manag 21:21–36CrossRefGoogle Scholar
  72. Pollard JH (1971) On distance estimators of density in randomly distributed forests. Biometrics 991–1002Google Scholar
  73. Power SA, Green ER, Barker CG, Bell JNB, Ashmore MR (2006) Ecosystem recovery: Heathland response to a reduction in nitrogen deposition. Glob Change Biol 12:1241–1252CrossRefGoogle Scholar
  74. Prasad AM, Iverson LR, Matthews S, Peters M (2007) A climate change Atlas for 134 forest tree species of the Eastern United States [Database]. Northern Research Station. USDA Forest Service, DelawareGoogle Scholar
  75. Prescott CE (1995) Does nitrogen availability control rates of litter decomposition in forests? In: Nilsson LO, Hüttl RF, Johansson UT (eds) Nutrient uptake and cycling in forest ecosystems. Springer Netherlands, Dordrecht, pp 83–88CrossRefGoogle Scholar
  76. Prescott CE, Taylor BR, Parsons WFJ, Durall DM, Parkinson D (1993) Nutrient release from decomposing litter in Rocky Mountain coniferous forests: influence of nutrient availability. Can J Forest Res 23:1576–1586CrossRefGoogle Scholar
  77. PRISM Climate Group, Oregon State University (2015)
  78. Reich PB, Grigal DF, Aber JD, Gower ST (1997) Nitrogen mineralization and productivity in 50 hardwood and conifer stands on diverse soils. Ecology 78:335–347CrossRefGoogle Scholar
  79. Rhine ED, Mulvaney RL, Pratt EJ, Sims GK (1998) Improving the Berthelot reaction for determining ammonium in soil extracts and water. Soil Sci Soc Am J 62:473–480CrossRefGoogle Scholar
  80. Rinkes ZL, Weintraub MN, DeForest JL, Moorhead DL (2011) Microbial substrate preference and community dynamics during decomposition of Acer saccharum. Fungal Ecol 4:396–407CrossRefGoogle Scholar
  81. Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153–162CrossRefPubMedGoogle Scholar
  82. Robinson CH (2002) Controls on decomposition and soil nitrogen availability at high latitudes. Plant Soil 242:65–81CrossRefGoogle Scholar
  83. Ros GH, Temminghoff EJM, Hoffland E (2011) Nitrogen mineralization: a review and meta-analysis of the predictive value of soil tests. Eur J Soil Sci 62:162–173CrossRefGoogle Scholar
  84. SAS Institute (2003) SAS-JMP version 10.0. SAS Institute, CaryGoogle Scholar
  85. Schaberg PG, DeHayes DH, Hawley GJ, Murakami PF, Strimbeck GR, McNulty SG (2002) Effects of chronic N fertilization on foliar membranes, cold tolerance, and carbon storage in montane red spruce. Can J Forest Res 32:1351–1359CrossRefGoogle Scholar
  86. Scott NA, Binkley D (1997) Foliage litter quality and annual net N mineralization: comparison across North American forest sites. Oecologia 111:151–159CrossRefGoogle Scholar
  87. Scott JT, Siccama TG, Johnson AH, Breisch AR (1984) Decline of red spruce in the Adirondacks, New York. B Torrey Bot Club 111:438–444CrossRefGoogle Scholar
  88. Siccama TG, Bliss M, Vogelmann HW (1982) Decline of red spruce in the Green Mountains of Vermont. B Torrey Bot Club 109:162–168CrossRefGoogle Scholar
  89. Stokes MA, Smiley TL (1996) An introduction to tree-ring dating. University of Arizona Press, TusconGoogle Scholar
  90. Strengbom J, Nordin A, Nasholm T, Ericson L (2001) Slow recovery of boreal forest ecosystem following decreased nitrogen input. Funct Ecol 15:451–457CrossRefGoogle Scholar
  91. Stump LM, Binkley D (1993) Relationships between litter quality and nitrogen availability in Rocky Mountain forests. Can J Forest Res 23:492–502CrossRefGoogle Scholar
  92. Templer P (2003) Soil microbial biomass and nitrogen transformations among five tree species of the Catskill Mountains, New York, USA. Soil Biol Biochem 35:607–613CrossRefGoogle Scholar
  93. Thomas KD, Prescott CE (2000) Nitrogen availability in forest floors of three tree species on the same site: the role of litter quality. Can J Forest Res 30:1698–1706CrossRefGoogle Scholar
  94. US Environmental Protection Agency (2015) National Emissions Inventory (NEI) air pollution emissions. US Environmental Protection Agency, Chicago, Accessed 15 August 2015Google Scholar
  95. Vinton MA, Burke IC (1995) Interactions between individual plant species and soil nutrient status in shortgrass steppe. Ecology 76:1116–1133CrossRefGoogle Scholar
  96. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  97. Yin X (1992) Empirical relationships between temperature and nitrogen availability across North American forests. Can J Forest Res 22:707–712CrossRefGoogle Scholar
  98. Zak DR, Pregitzer KS, Holmes WE, Burton AJ, Zogg GP (2004) Anthropogenic N deposition and the fate of 15NO3 in a northern hardwood ecosystem. Biogeochemistry 69:143–157CrossRefGoogle Scholar
  99. Zogg GP, Zak DR, Pregitzer KS, Burton AJ (2000) Microbial immobilization and the retention of anthropogenic nitrate in a northern hardwood forest. Ecology 81:1858–1866CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Kenneth R. Smith
    • 1
    Email author
  • Justin M. Mathias
    • 1
  • Brenden E. McNeil
    • 2
  • William T. Peterjohn
    • 1
  • Richard B. Thomas
    • 1
  1. 1.Department of BiologyWest Virginia UniversityMorgantownUSA
  2. 2.Department of Geology and GeographyWest Virginia UniversityMorgantownUSA

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