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Changes in Canopy Processes Following Whole-Forest Canopy Nitrogen Fertilization of a Mature Spruce-Hemlock Forest

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Abstract

Most experimental additions of nitrogen to forest ecosystems apply the N to the forest floor, bypassing important processes taking place in the canopy, including canopy retention of N and/or conversion of N from one form to another. To quantify these processes, we carried out a large-scale experiment and determined the fate of nitrogen applied directly to a mature coniferous forest canopy in central Maine (18–20 kg N ha−1 y−1 as NH4NO3 applied as a mist using a helicopter). In 2003 and 2004 we measured NO3 −, NH4 +, and total dissolved N (TDN) in canopy throughfall (TF) and stemflow (SF) events after each of two growing season applications. Dissolved organic N (DON) was greater than 80% of the TDN under ambient inputs; however NO3 − accounted for more than 50% of TF N in the treated plots, followed by NH4 + (35%) and DON (15%). Although NO3 − was slightly more efficiently retained by the canopy under ambient inputs, canopy retention of NH4 +as a percent of inputs increased markedly under fertilization. Recovery of less than 30% of the fertilizer N in TF suggested that the forest canopy retained more than 70% of the applied N (>80% when corrected for N which bypassed tree surfaces at the time of fertilizer addition). Results from plots receiving 15N enriched NO3 − and NH4 + confirmed bulk N estimations that more NO3 − than NH4 + was washed from the canopy by wet deposition. The isotope data did not show evidence of canopy nitrification, as has been reported in other spruce forests receiving much higher N inputs. Conversions of fertilizer-N to DON were observed in TF for both 15NH4 + and 15NO3 − additions, and occurred within days of the application. Subsequent rain events were not significantly enriched in 15N, suggesting that canopy DON formation was a rapid process related to recent N inputs to the canopy. We speculate that DON may arise from lichen and/or microbial N cycling rather than assimilation and re-release by tree tissues in this forest. Canopy retention of experimentally added N may meet and exceed calculated annual forest tree demand, although we do not know what fraction of retained N was actually physiologically assimilated by the plants. The observed retention and transformation of DIN within the canopy demonstrate that the fate and ecosystem consequences of N inputs from atmospheric deposition are likely influenced by forest canopy processes, which should be considered in N addition studies.

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References

  • Aber JD, Nadelhoffer KJ, Steudler P, Melillo PM. 1989. Nitrogen saturation in northern forest ecosystems. BioScience 39:378–86

    Article  Google Scholar 

  • Balestrini R, Tagliaferri A. 2001. Atmospheric deposition and canopy exchange processes in alpine forest ecosystems (northern Italy). Atmos Environ 35:6421–33

    Article  CAS  Google Scholar 

  • Beier C, Hansen K, Gundersen P. 1993. Spatial variability of throughfall fluxes in a spruce forest. Environ Pollut 81:257–67

    Article  PubMed  CAS  Google Scholar 

  • Bowden RD, Geballe GT, Bowden WB. 1989. Foliar uptake of 15N from simulated cloud water by red spruce (Picea rubens) seedlings. Can J For Res 19:382–6

    Google Scholar 

  • Boyce RL, Friedland AJ, Chamberlain CP, Poulson SR. 1996. Direct canopy nitrogen uptake from 15N-labeled wet deposition by mature red spruce. Can J For Res 26:1539–47

    Google Scholar 

  • Brooks PD, Stark JM, McInteer BB, Preston T. 1989. A diffusion method to prepare soil extracts for automated nitrogen-15 analysis. Soil Sci Soci Am 53:1707–11

    Article  CAS  Google Scholar 

  • Cabrera ML, Beare MH. 1993. Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soci Am 57:1007–12

    Article  CAS  Google Scholar 

  • Calanni JE, Berg M, Wood D, Mangis R, Boyce W, Weathers H, Sievering H. 1999. Atmospheric nitrogen deposition at a conifer forest: response of free amino acids in Engelmann spruce needles. Environ Pollut 105:79–89

    Article  CAS  Google Scholar 

  • Cape JN, Dunster A, Crossley A, Sheppard LJ, Harvey FJ. 2001. Throughfall chemistry in a Sitka spruce plantation in response to six different simulated polluted mist treatments. Water Air Soil Pollut 130:619–24

    Article  Google Scholar 

  • Carlisle A, Brown AH, White EJ. 1966 The organic matter and nutrient elements in the precipitation beneath a sessile oak (Quercus petraea) canopy. J Ecol 54:87–98

    Article  Google Scholar 

  • Carroll GC. 1980. Forest canopies: complex and independent subsystems. In: Waring RH, Ed. Forests: fresh perspectives from ecosystem analysis. Proceedings of the 40th Annual Biology Colloquium. Oregon State University Press. pp 87–107

  • Chen CW, Hudson RJ, Gherini SA, Dean JD, Goldstein RA. 1983. Acid rain model: canopy module. J Environ Eng 109:585–603

    Article  CAS  Google Scholar 

  • Chiwa M, Crossley A, Sheppard LJ, Sakugawa H, Cape JN. 2004. Throughfall chemistry and canopy interactions in a Sitka spruce plantation sprayed with six different simulated polluted mist treatments. Environ Pollut 127:57–64

    Article  PubMed  CAS  Google Scholar 

  • Coudhury D. 1988. Herbivory induced changes in leaf-litter resource quality: a neglected aspect of herbivory in ecosystem nutrient dynamics. Oikos 51:389–93

    Article  Google Scholar 

  • Cole D, Rapp M. 1981. Elemental cycling in forest ecosystems. In: Reichle D (ed) Dynamic properties of forest ecosystems. Cambridge University Press. International Biological Programme 23:341–409

  • Dail DB, Hollinger D, Davidson E, Fernandez I, Scott N, Goltz S, Sievering H, Lee JT. 2007. Fate of 15N additions to a mature Spruce-Hemlock canopy. Oecologia (in review)

  • D’Elia CF, Steudler PA, Corwin N. 1977. Determination of total nitrogen in aqueous samples using persulfate digestion. Limnol Oceanogr 22:760–4

    CAS  Google Scholar 

  • Eilers JR, Brumme R, Matzner E. 1992. Above-ground N-uptake from wet deposition by Norway spruce (Picea abies Karst.). For Ecol Manag 51:239–249

    Article  Google Scholar 

  • Fernandez IJ, Lawrence GB, Richards KJ. 1990. Characteristics of foliar chemistry in a commercial spruce-fir stand of northern New England USA. Plant Soil 125:288–292

    Article  CAS  Google Scholar 

  • Friedland AJ, Miller EK, Battles JJ, Thorne JF. 1991. Nitrogen deposition, distribution and cycling in a sub-alpine spruce-fir forest in the Adirondacks, New York, U.S.A. Biogeochemistry 14:31–55

    Article  CAS  Google Scholar 

  • Galloway JN, Cowling EB. 2002. Reactive nitrogen and the world: 200 years of change. Ambio 31:64–71

    Article  PubMed  Google Scholar 

  • Hansen K. 1996. In-canopy throughfall measurements of ion fluxes in Norway spruce. Atmos Environ 30:4065–76

    Article  CAS  Google Scholar 

  • Hollinger DY. Aber J, Dail B, Davidson EA, Goltz SM, Hughes H, Leclerc MY, Lee JT, Richardson AD, Rodrigues C, Scott NA, Achuatavarier D, Walsh J. 2004. Spatial and temporal variability in forest–atmosphere CO2 exchange. 2004 Global Change Biol 10:1–18

    Article  Google Scholar 

  • Hollinger DY, Goltz SM, Davidson EA, Lee JT, Tu K, Valentine HT. 1999. Seasonal patterns and environmental control of carbon dioxide and water vapor exchange in an ecotonal boreal forest. Global Change Biol 5:891–902

    Article  Google Scholar 

  • Kinkel LL. 1997. Microbial population dynamics on leaves. Ann Rev Phytopath 35:327–47

    Article  CAS  Google Scholar 

  • Kristensen HL, Gundersen P, Callesen I, Reinds G. 2004. Atmospheric N deposition influences soil nitrate concentration differently in European Coniferous and Deciduous Forests. Ecosystems 7: 180–92

    Article  CAS  Google Scholar 

  • Lawrence GB, Fernandez IJ. 1991. Biogeochemical effects of acidic deposition on a low elevation spruce-fir stand in Howland, Maine. Can J For Res 21:867–75

    Article  CAS  Google Scholar 

  • Lawrence GB, Fernandez IJ. 1993. A reassessment of areal variability of throughfall deposition measurements. Ecol Appl 3:473–80

    Article  Google Scholar 

  • Lewis J. 2003. Stemflow estimation in a redwood forest using model-based stratified random sampling. Environmetrics 14:559–71

    Article  Google Scholar 

  • Liechty HO, Mroz GD, Reed DD. 1993. Cation and anion fluxes in northern hardwood throughfall along an acidic deposition gradient. Can J For Res 23:457–67

    Article  CAS  Google Scholar 

  • Lovett GM. 1992. Atmospheric deposition and forest nutrient cycling: a synthesis of the integrated forest study. Ecol. Stud. 91, In: Johnson D, Lindberg S, New York: Springer, pp 634–55

  • Lovett GM, Lindberg SE. 1993. Atmospheric deposition and canopy interactions of nitrogen in forests. Can J For Res 23:1603–16

    Article  CAS  Google Scholar 

  • Lovett GM, Nolan SS, Driscoll CT, Fahey TJ. 1996. Factors regulating thoughfall flux in a New Hampshire forested landscape. Can J For Res 26:2134–44

    Article  Google Scholar 

  • Magill AH, Aber JD, Hendricks JJ, Bowden RD, Melillo JM, Steudler PA. 1997. Biogeochemical response of forest ecosystems to simulated chronic nitrogen deposition. Ecol Appl 7:402–15

    Article  Google Scholar 

  • McLaughlin JW, Fernandez IJ, Richards K. 1996. Atmospheric deposition to a low-elevation spruce-fir forest, Maine, USA. J Environ Qual 25:248–59

    Article  CAS  Google Scholar 

  • McNulty SG, Aber JD, Newman SD. 1996. Nitrogen saturation in a high elevation New England spruce-fir stand. For Ecol Manag 84:109–21

    Article  Google Scholar 

  • Nadelhoffer K, Emmett B, Gundersen P, Tietema A, Wright R. 1999. Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–47

    Article  CAS  Google Scholar 

  • Nadelhoffer KJ, Johnson LC, Laundre JA, Giblin AE, Shaver GR. 2002. Fine root production and nutrient content in wet and moist arctic tundras as influenced by chronic fertilization. Plant Soil 242:107–13

    Article  CAS  Google Scholar 

  • Papen H, Geßler A, Zumbusch E, Rennenberg H. 2002. Chemolithoautotrophic nitrifiers in the phyllosphere of a spruce ecosystem receiving high atmospheric nitrogen input. Curr Microbiol 44:56–60

    Article  PubMed  CAS  Google Scholar 

  • Parker GG. 1983. Advances in ecological research. New York: Academic, pp 58–135

    Google Scholar 

  • Pizzicannella F, Nirel P, Landry J-C. 1995. Mise au point d’une méthode de détermination de l’azote organique dissous. Arch Sci Genève 49:59–68

    Google Scholar 

  • Potter CS, Ragsdale HL, Swank WT. 1991. Atmospheric deposition and foliar leaching in a regenerating southern Appalachian forest canopy. J Ecol 79:97–115

    Article  Google Scholar 

  • Scott NA, Rodrigues CA, Hughes H, Lee JT, Davidson EA, Dail DB, Malerba P, Hollinger DY. 2004. Changes in carbon storage and net carbon exchange one year after an initial shelterwood harvest at Howland Forest. ME Env Manage 33 (Suppl. 1):S9–22

    Google Scholar 

  • Sievering H, Fernandez I, Lee J, Hom J, Rustad L. 2000. Forest canopy uptake of atmospheric nitrogen deposition at eastern U.S. conifer sites: carbon storage implications? Global Biogechem Cycles 14:1153–9

    Article  CAS  Google Scholar 

  • Shearer G, Kohl DH. 1993. Natural abundance of 15N: fractional contribution of two sources to a common sink and use of isotope discrimination. In: Knowles, R, Blackburn TH, Eds. Nitrogen isotope techniques. San Diego: Academic

  • Solórzano L, Sharp JH. 1980. Determination of total dissolved nitrogen in natural waters. Limnol Oceanogr 25:751–4

    Google Scholar 

  • Sørensen P, Jensen ES. 1991. Sequential diffusion of ammonium and nitrate from soil extracts to a polytetrafluoroethylene trap for 15N determination. Anal Chim Acta. 252:201–3

    Article  Google Scholar 

  • Stadler B, Michalzik B. 1998. Aphid infested Norway spruce are “hot spots” in throughfall carbon chemistry in coniferous forests. Can J Fort Res 28:1717–22

    Article  Google Scholar 

  • Stadler B, Michalzik B, Muller T. 1998. Linking aphid ecology with nutrient fluxes in a coniferous forest. Ecology 79:1514–25

    Article  Google Scholar 

  • Stark JM, Hart SC. 1996. Diffusion technique for preparing salt solutions, kjeldahl digests and persulfate digests for nitrogen-15 analysis. Soil Sci Soc Am J 60:1846–55

    Article  CAS  Google Scholar 

  • Swan HSD. 1971. Woodlands report WR/34. Pulp and Paper Resources Institute of Canada, p 27

  • Tietema A, Emmet BA, Gundersen P, Kjønaas OJ, Koopmans CJ. 1998. The fate of 15N labeled nitrogen deposition in coniferous forest ecosystems. For Ecol Manage 101:19–27

    Article  Google Scholar 

  • Tomaszewski T, Boyce RL, Sievering H. 2003. Canopy uptake of atmospheric nitrogen and new growth nitrogen requirement at a Colorado subalpine forest. Can J For Res/Rev Can Res 33(11):2221–7

    Article  Google Scholar 

  • Townsend AR, Braswell BH, Holland EA, Penner JE. 1996. Spatial and temporal patterns in terrestrial carbon storage due to deposition of fossil fuel nitrogen. Ecol Appl 6:806–14

    Article  Google Scholar 

  • U.S. Department of Agriculture, Forest Service. 2002. Forest inventory and analysis national core field guide; volume II: field data collection procedures for phase 3 plots, version 1.6, Sect. 14, pp 265–298

  • USEPA. 2004. Howland, ME (HOW132). Clean Air Status and Trends Network. “http://www.epa.gov/castnet/sites/how132.html” (10 September 04)

  • Vitousek PM. 1982. Nutrient cycling and nutrient use efficiency. Am Nat 119:553–72

    Article  Google Scholar 

  • Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–50

    Google Scholar 

  • Wright RF, Rasmussen L. 1998. Introduction to the NITREX and EXMAN projects. For Ecol Manage 101:1–7

    Article  Google Scholar 

  • Young HE, Ribe JH, Wainwright K. 1980. Weight tables for tree and shrub species in Maine. Univ of Maine Life Sci and Agric. Exp. Stn. Misc. Rep. 230. University of Maine, Orono, ME. 84 pp

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Acknowledgments

We thank the International Paper Company, Ltd., and GMO, LLC for providing access to the research site in Howland, Maine. We also thank our technical support staff; Mr. John Lee, Ms. Holly Hughes and Mr. Charles Rodrigues and undergraduates; Mr. David Dunston, Ms. Nell Burger and Ms. Gretchen Miles; Department of Energy SURE program interns who worked on this project. This research was supported by the Office of Science (BER), U.S. Department of Energy, through the Northeast Regional Center of the National Institute for Global Environmental Change under Cooperative Agreement Nos. DE-FC02-03ER63613, DE-FC-03-90ER61010, and DE-FG02-00ER63002; DOE-NICCR agreement No, DE-FG02-06ER64157 and NSF award No. 0223188. Financial support does not constitute an endorsement by DOE or NSF of the views expressed in this article. We also thank several anonymous reviewers. This is Maine Agriculture and Forestry Experiment Station publication #2964.

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Authors and Affiliations

  1. Department of Plant, Soil, and Environmental Sciences, University of Maine, 5722 Deering Hall, Orono, Maine, 04469-5722, USA

    E. Gaige, D. B. Dail & I. J. Fernandez

  2. US Forest Service, Northern Region Research Station, 271 Mast Road, Durham, New Hampshire, 03824, USA

    D. Y. Hollinger

  3. Woods Hole Research Center, 149 Woods Hole Road, Falmouth, Massachusetts, 02540-1644, USA

    E. A. Davidson

  4. Geography and Environmental Sciences, University of Colorado-Denver, Campus Box 172, P.O. Box 173364, Denver, Colorado, 80217-3364, USA

    H. Sievering

  5. Forest Ecosystem Science, School of Forest Resources, University of Maine, 5755 Nutting Hall, Orono, Maine, 04469-5755, USA

    A. White

  6. Math and Statistics, University of Maine, 5752 Neville Hall, Orono, Maine, 04469-5752, USA

    W. Halteman

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  1. E. Gaige
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  2. D. B. Dail
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Correspondence to D. B. Dail.

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Fig4

Areal spraying of Howland Forest: Dissolved ammonium nitrate (18 kg N/ha/growing season) was applied to the canopy in 5 equally spaced doses from May to September.

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Gaige, E., Dail, D.B., Hollinger, D.Y. et al. Changes in Canopy Processes Following Whole-Forest Canopy Nitrogen Fertilization of a Mature Spruce-Hemlock Forest. Ecosystems 10, 1133–1147 (2007). https://doi.org/10.1007/s10021-007-9081-4

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