, Volume 169, Issue 4, pp 915–925 | Cite as

Variation in foliar nitrogen and albedo in response to nitrogen fertilization and elevated CO2

  • Haley F. WickleinEmail author
  • Scott V. Ollinger
  • Mary E. Martin
  • David Y. Hollinger
  • Lucie C. Lepine
  • Michelle C. Day
  • Megan K. Bartlett
  • Andrew D. Richardson
  • Richard J. Norby
Physiological ecology - Original research


Foliar nitrogen has been shown to be positively correlated with midsummer canopy albedo and canopy near infrared (NIR) reflectance over a broad range of plant functional types (e.g., forests, grasslands, and agricultural lands). To date, the mechanism(s) driving the nitrogen–albedo relationship have not been established, and it is unknown whether factors affecting nitrogen availability will also influence albedo. To address these questions, we examined variation in foliar nitrogen in relation to leaf spectral properties, leaf mass per unit area, and leaf water content for three deciduous species subjected to either nitrogen (Harvard Forest, MA, and Oak Ridge, TN) or CO2 fertilization (Oak Ridge, TN). At Oak Ridge, we also obtained canopy reflectance data from the airborne visible/infrared imaging spectrometer (AVIRIS) to examine whether canopy-level spectral responses were consistent with leaf-level results. At the leaf level, results showed no differences in reflectance or transmittance between CO2 or nitrogen treatments, despite significant changes in foliar nitrogen. Contrary to our expectations, there was a significant, but negative, relationship between foliar nitrogen and leaf albedo, a relationship that held for both full spectrum leaf albedo as well as leaf albedo in the NIR region alone. In contrast, remote sensing data indicated an increase in canopy NIR reflectance with nitrogen fertilization. Collectively, these results suggest that altered nitrogen availability can affect canopy albedo, albeit by mechanisms that involve canopy-level processes rather than changes in leaf-level reflectance.


Albedo Nitrogen Leaf structure Nitrogen fertilization Free air CO2 enrichment 



We thank G. James Collatz for helpful comments on a draft of this manuscript, Rob Braswell for providing the SAIL-2 model code, and Richard Norby, Colleen Iversen, and Jeffery Warren for support at ORNL. We are indebted to Michael Eastwood, ER-2 pilots Denis Steel, Tim Williams, and the rest of the AVIRIS team for aircraft data acquisition. This work was funded by a grant from the North American Carbon Program (NACP) NASA’s Terrestrial Ecology and Carbon Cycle Science Programs and a graduate fellowship provided by the Research and Discover program. The ORNL FACE experiment was supported by the US Department of Energy, Office of Science, Biological and Environmental Research Program. A.D.R. and M.K.B. acknowledge support, through the Harvard Forest REU program, from the National Science Foundation (Grant DBI-04-52254).


  1. Andrieu B, Baret F, Jacquemoud S, Malthus T, Steven M (1997) Evaluation of an improved version of SAIL model for simulating bidirectional reflectance of sugar beet canopies. Remote Sens Environ 60:247–257CrossRefGoogle Scholar
  2. Asner GP (1998) Biophysical and biochemical sources of variability in canopy reflectance. Remote Sens Environ 64:234–253CrossRefGoogle Scholar
  3. Braswell BH, Schimel DS, Privette JL, Moore B III, Emery WJ, Sulzman EW, Hudak AT (1996) Extracting ecological and biophysical information from AVHRR optical data: an integrated algorithm based on inverse modeling. J Geophys Res 101:23335–23348CrossRefGoogle Scholar
  4. Brooks TJ, Wall GW, Pinter PJ Jr, Kimball BA, LaMorte RL, Leavitt SW, Matthias AD, Adamsen FJ, Hunsaker DJ, Webber AN (2000) Acclimation response of spring wheat in a free-air CO2 enrichment (FACE) atmosphere with variable soil nitrogen regimes. 3. Canopy architecture and gas exchange. Photosynth Res 66:97–108PubMedCrossRefGoogle Scholar
  5. Castro-Esau KL, Sanchez-Azofeifa GA, Rivard B, Wright AJ, Quesada M (2006) Variability in leaf optical properties of Mesoamerican trees and the potential for species classification. Am J Bot 94:517–530CrossRefGoogle Scholar
  6. Chen JM, Cihlar J (1995) Quantifying the effect of canopy architecture on optical measurements of leaf area index using two gap size analysis methods. IEEE Transact Geosci Remote Sens 33:777–787CrossRefGoogle Scholar
  7. Close DC, Beadle CL (2006) Leaf angle responds to nitrogen supply in eucalypt seedlings. Is it a photoprotective mechanism? Tree Physiol 26:743–748PubMedCrossRefGoogle Scholar
  8. Daughtry CST, Walthall CL, Kim MS, Brown de Colstoun E, McMurtrey JE III (2000) Estimating corn leaf chlorophyll concentration from leaf and canopy reflectance. Remote Sens Environ 74:229–239CrossRefGoogle Scholar
  9. Ellsworth DS, Reich PB, Naumburg ES, Koch GW, Kubiske ME, Smith SD (2004) Photosythesis, carboxilation and leaf nitrogen responses of 16 species to elevated pCO2 across four free-air CO2 enrichment experiments in forest, grassland and desert. Glob Change Biol 10:2121–2138CrossRefGoogle Scholar
  10. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19CrossRefGoogle Scholar
  11. Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givinsh TI (ed) On the economy of form and function. Cambridge University Press, Cambridge, pp 25–55Google Scholar
  12. Gates DM, Keegan HJ, Schleter JC, Weidner VR (1965) Spectral properties of plants. Appl Opt 4:11–20CrossRefGoogle Scholar
  13. Gausman HW, Allen WA, Cardenas R, Richardson AJ (1970) Relation of light reflectance to historical and physical evaluations of cotton leaf maturity. Appl Opt 9:545–552PubMedCrossRefGoogle Scholar
  14. Gausman HW, Allen WA, Escobar DE (1974) Refractive index of plant cell walls. Appl Opt 13:109–111PubMedCrossRefGoogle Scholar
  15. Gueymard C (2004) The sun’s total and spectral irradiance for solar energy applications and solar radiation models. Sol Energy 76:423–453CrossRefGoogle Scholar
  16. Hollinger DY, Ollinger SV, Richardson AD, Meyers TP, Dail DB, Martin ME, Scott NA, Arkebauer TJ, Baldocchi DD, Clark KL, Curtis PS, Davis KJ, Desai AR, Dragoni D, Goulden ML, Gu L, Katul GG, Pallardy SG, Paw UKT, Schmid HP, Stoy PC, Suyker AE, Verma SB (2010) Albedo estimates for land surface models and support for a new paradigm based on foliage nitrogen concentration. Glob Change Biol 16:696–710CrossRefGoogle Scholar
  17. Huemmrich KF, Goward SN (1997) Vegetation canopy PAR absorptance and NDVI: an assessment for ten tree species with the SAIL model. Remote Sens Environ 61:254–269CrossRefGoogle Scholar
  18. Iversen CM, Norby RJ (2008) Nitrogen limitation in a sweetgum plantation: implications for carbon allocation and storage. Can J For Res 38:1021–1032CrossRefGoogle Scholar
  19. Jacquemoud S, Verhoef W, Baret F, Bacour C, Zarco-Tejada PJ, Asner GP, François C, Ustin SL (2009) PROSPECT + SAIL models: a review of use for vegetation characterization. Remote Sens Environ 113:S56–S66CrossRefGoogle Scholar
  20. Johnson DW, Cheng W, Joslin JD, Norby RJ, Edwards NT, Todd DE Jr (2004) Effects of elevated CO2 on nutrient cycling in a sweetgum plantation. Biogeochemistry 69:379–403CrossRefGoogle Scholar
  21. Knapp AK, Carter GA (1998) Variability in leaf optical properties among 26 species from a broad range of habitats. Am J Bot 85:940–946PubMedCrossRefGoogle Scholar
  22. Longstreth DJ, Bolaños JA, Goddard RH (1985) Photosynthetic rate and mesophyll surface area in expanding leaves of Alternanthera philoxeroides grown at two light levels. Am J Bot 72:14–19CrossRefGoogle Scholar
  23. Magill AH, Aber JD, Currie WS, Nadelhoffer KJ, Martin ME, McDowell WH, Melillo JM, Steudler P (2004) Ecosystem response to 15 years of chronic nitrogen additions at the Havard Forest LTER, Massachusetts, USA. For Ecol Manag 196:7–28CrossRefGoogle Scholar
  24. Malenovský Z, Martin E, Homolová L, Gastellu-Etchegorry J-P, Zurita-Milla R, Schaepman ME, Pokorný R, Clevers JGPW, Cudlín P (2008) Influence of woody elements of a Norway spruce canopy on nadir reflectance simulated by the DART model at very high spatial resolution. Remote Sens Environ 112:1–18CrossRefGoogle Scholar
  25. Niinemets U (1999) Research review: components of leaf dry mass per area-thickness and density-alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol 144:35–47CrossRefGoogle Scholar
  26. Niinemets U (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82:453–469CrossRefGoogle Scholar
  27. Nobel PS, Zaragoza LJ, Smith WK (1975) Relation between mesophyll surface area, photosynthetic rate, and illumination level during development for leaves of Plectranthus parviflorus Henckel. Plant Physiol 55:1067–1070PubMedCrossRefGoogle Scholar
  28. Norby RJ, Iversen CM (2006) Nitrogen uptake, ditribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest. Ecology 87:5–14PubMedCrossRefGoogle Scholar
  29. Norby RJ, Todd DE, Fults J, Johnson DW (2001) Allometric determination of tree growth in a CO2-enriched sweetgum stand. New Phytol 150:477–487CrossRefGoogle Scholar
  30. Norby RJ, Sholtis JD, Gunderson CA, Jawdy SS (2003) Leaf dynamics of a deciduous forest canopy: no response to elevated CO2. Oecologia 136:574–584PubMedCrossRefGoogle Scholar
  31. Ollinger SV (2011) Sources of variability in canopy reflectance and the convergent properties of plants. New Phytol 189:375–394PubMedCrossRefGoogle Scholar
  32. Ollinger SV, Aber JD, Lovett GM, Millham SE, Lathrop RG, Ellis JE (1993) A spatial model of atmospheric deposition for the Northeastern US. Ecol Appl 3:459–472CrossRefGoogle Scholar
  33. Ollinger SV, Richardson AD, Martin ME, Hollinger DY, Frolking S, Reich PB, Plourde LC, Katul GG, Munger JW, Oren R, Smith ML, Paw UKT, Bolstad PV, Cook BD, Day MC, Martin TA, Monson RK, Schmid HP (2008) Canopy nitrogen, carbon assimilation and albedo in temperate and boreal forests: functional relations and potential climate feedbacks. Proc Nat Acad Sci 105:19335–19340CrossRefGoogle Scholar
  34. Oren R, Ellsworth DS, Johnsen KH, Phillips N, Ewers BE, Maier C, Schäfer KVR, McCarthy H, Hendrey G, McNulty SG, Katul GG (2001) Soil fertility limits carbon sequestration by forest ecosystems in a CO2-enriched atmosphere. Nature 411:469–472PubMedCrossRefGoogle Scholar
  35. Rademacher IF, Nelson CJ (2001) Nitrogen effects on leaf anatomy within the intercalary meristems of tall fescue leaf blades. Ann Bot 88:893–903CrossRefGoogle Scholar
  36. Rautiainen M, Stenberg P, Nilson T, Kuusk A (2004) The effect of crown shape on the reflectance of coniferous stands. Remote Sens Environ 89:41–52CrossRefGoogle Scholar
  37. Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Nat Acad Sci 94:13730–13734PubMedCrossRefGoogle Scholar
  38. Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf train relationships: a test across six biomes. Ecology 80:1955–1969CrossRefGoogle Scholar
  39. Riggs JS, Tharp ML, Norby RJ (2009) ORNL FACE CO2 data. carbon dioxide information analysis center, Oak Ridge, TN, USA. Accessed 15-July-2010
  40. Sánchez J, Canton MP (1999) Space imaging processing. CRC Press LLC, Boca RatonGoogle Scholar
  41. Slaton MR, Hunt ER, Smith WK (2001) Estimating near-infrared leaf reflectance from leaf structural characteristics. Am J Bot 88:278–284PubMedCrossRefGoogle Scholar
  42. Smolander S, Stenberg P (2003) A method to account for shoot scale clumping in coniferous canopy reflectance models. Remote Sens Environ 88:363–373CrossRefGoogle Scholar
  43. Tari DB, Gazanchian A, Pirdashti HA, Nasiri M (2009) Flag leaf morphophysiological response to different agronomical treatments in a promising line of rice (Oryza sativa L.). Am-Euras J Agric Environ Sci 5:403–408Google Scholar
  44. Verhoef W (1984) Light scattering by leaf layers with application to canopy reflectance modeling: the SAIL model. Remote Sens Environ 16:125–141CrossRefGoogle Scholar
  45. Woolley JT (1971) Reflectance and transmittance of light by leaves. Plant Physiol 47:656–662PubMedCrossRefGoogle Scholar
  46. Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M-L, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827PubMedCrossRefGoogle Scholar
  47. Zhang Q, Xiao X, Braswell BH, Linder E, Ollinger S, Smith ML, Jenkins JP, Baret F, Richardson AD, Moore B III, Minocha R (2006) Characterization of seasonal variation of forest canopy in a temperate deciduous broadleaf forest, using daily MODIS data. Remote Sens Environ 105:189–203CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Haley F. Wicklein
    • 1
    Email author
  • Scott V. Ollinger
    • 1
  • Mary E. Martin
    • 1
  • David Y. Hollinger
    • 2
  • Lucie C. Lepine
    • 1
  • Michelle C. Day
    • 1
  • Megan K. Bartlett
    • 3
  • Andrew D. Richardson
    • 4
  • Richard J. Norby
    • 5
  1. 1.Complex Systems Research Center, Morse Hall, Institute for the Study of Earth, Oceans, and SpaceUniversity of New HampshireDurhamUSA
  2. 2.Northern Research StationUS Department of Agriculture Forest ServiceDurhamUSA
  3. 3.Department of Environmental Science, Policy, and ManagementUniversity of CaliforniaBerkeleyUSA
  4. 4.Department of Organismic and Evolutionary Biology, Harvard University HerbariumHarvard UniversityCambridgeUSA
  5. 5.Environmental Sciences DivisionOak Ridge National LaboratoryOak RidgeUSA

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