Skip to main content
Log in

The phosphorus status of northern hardwoods differs by species but is unaffected by nitrogen fertilization

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Northern hardwood forests in the eastern US exhibit species-specific influences on nitrogen (N) cycling, suggesting that their phosphorus (P) cycling characteristics may also vary by species. These characteristics are increasingly important to understand in light of evidence suggesting that atmospheric N deposition has increased N availability in the region, potentially leading to phosphorus limitation. We examined how P characteristics differ among tree species and whether these characteristics respond to simulated N deposition (fertilization). We added NH4NO3 fertilizer (50 kg ha−1 year−1) to single-species plots of red oak (Quercus rubra L.), sugar maple (Acer saccharum Marsh.), eastern hemlock (Tsuga canadensis (L.) Carr.), American beech (Fagus grandifolia Ehrh.), and yellow birch (Betula alleghaniensis Britt.), in the Catskill Mountains, New York from 1997 to 2007. Species differences were observed in foliar, litter and root P concentrations, but all were unaffected by a cumulative N fertilization of 550 kg/ha. Similarly, measures of soil P availability and biotic P sufficiency differed by species but were unaffected by N fertilization. Results suggest species exhibit unique relationships to P as well as N cycles. We found little evidence that N fertilization leads to increased P limitation in these northern hardwood forests. However, species such as sugar maple and red oak may be sufficient in P, whereas beech and hemlock may be less sufficient and therefore potentially more sensitive to future N-stimulated P limitation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM (1989) Nitrogen saturation in northern forest ecosystems. BioScience 39:378–386

    Article  Google Scholar 

  • Aber JD, Goodale CL, Ollinger SV, Smith ML, Magill AH, Martin ME, Hallett RA, Stoddard JL (2003) Is nitrogen deposition altering the nitrogen status of northeastern forests? BioScience 53:375–389

    Article  Google Scholar 

  • Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608

    Article  Google Scholar 

  • Binkley D (1995) The influence of tree species on forest soils—processes and patterns. In: Mead DJ, Cornforth IS (eds) Proceedings of the trees and soil workshop. Agronomy society of New Zealand special publication #10. Lincoln University Press, Canterbury

    Google Scholar 

  • Blum JD, Klaue A, Nezat CA, Driscoll CT, Johnson CE, Siccama TG, Eagar C, Fahey TJ, Likens GE (2002) Mycorrhizal weathering of apatite as an important calcium source in base-poor forest ecosystems. Nature 417:729–731

    Article  Google Scholar 

  • Boerner REJ, Koslowsky SD (1989) Microsite variations in soil chemistry and nitrogen mineralization in a beech-maple forest. Soil Biol Biochem 21:795–801

    Article  Google Scholar 

  • 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 149:303–314

    Article  Google Scholar 

  • Braun EL (1950) Deciduous forests of eastern North America. Blakiston, Philadelphia

    Google Scholar 

  • Carreira JA, Garcia-Ruiz R, Lietor J, Harrison AF (2000) Changes in soil phosphatase activity and P transformation rates induced by application of N- and S-containing acid-mist to a forest canopy. Soil Biol Biochem 32:1857–1865

    Article  Google Scholar 

  • Cross AF, Schlesinger WH (1995) A literature review and evaluation of the Hedley fractionation—applications to the biogeochemical cycle of soil-phosphorus in natural ecosystems. Geoderma 64:197–214

    Article  Google Scholar 

  • D’Angelo E, Crutchfield J, Vandiviere M (2001) Rapid, sensitive, microscale determination of phosphate in water and soil. J Environ Qual 30:2206–2209

    Google Scholar 

  • Dancer WS, Eliason R, Lekhakul S (1998) Microwave assisted soil and waste dissolution for estimation of total phosphorus. Commun Soil Sci Plant Anal 29:1997–2006

    Article  Google Scholar 

  • DeForest JL, Zak DR, Pregitzer KS, Burton AJ (2004) Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Sci Soc Am J 68:132–138

    Google Scholar 

  • Dighton J (1983) Phosphatase production by mycorrhizal fungi. Plant Soil 71:455–462

    Article  Google Scholar 

  • Dise NB, Wright RF (1995) Nitrogen leaching from European forests in relation to nitrogen deposition. Forest Ecol Manag 71:153–161

    Article  Google Scholar 

  • Eickmeier WG (1982) Fall phosphorus resorption by Quercus prinus L. and Acer saccharum Marsh in central Tennessee. Am Midl Nat 107:196–198

    Article  Google Scholar 

  • Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142

    Article  Google Scholar 

  • Fabio ES, Arthur MA, Rhoades CC (2009) Influence of moisture regime and tree species composition on nitrogen cycling dynamics in hardwood forests of Mammoth Cave National Park, Kentucky, USA. Can J For Res-Rev Can Rech For 39:330–341

    Article  Google Scholar 

  • Fenn ME, Poth MA, Aber JD, Baron JS, Bormann BT, Johnson DW, Lemly AD, McNulty SG, Ryan DE, Stottlemyer R (1998) Nitrogen excess in North American ecosystems: predisposing factors, ecosystem responses, and management strategies. Ecol Appl 8:706–733

    Article  Google Scholar 

  • Finzi AC (2009) Decades of atmospheric deposition have not resulted in widespread phosphorus limitation or saturation of tree demand for nitrogen in southern New England. Biogeochemistry 92:217–229

    Article  Google Scholar 

  • Finzi AC, Van Breemen N, Canham CD (1998) Canopy tree soil interactions within temperate forests: species effects on soil carbon and nitrogen. Ecol Appl 8:440–446

    Google Scholar 

  • Fiorentino I, Fahey TJ, Groffman PM, Driscoll CT, Eagar C, Siccama TG (2003) Initial responses of phosphorus biogeochemistry to calcium addition in a northern hardwood forest ecosystem. Can J For Res-Rev Can Rech For 33:1864–1873

    Article  Google Scholar 

  • Fisk MC, Fahey TJ (2001) Microbial biomass and nitrogen cycling responses to fertilization and litter removal in young northern hardwood forests. Biogeochemistry 53:201–223

    Article  Google Scholar 

  • Fiske CH, Subbarow Y (1925) The colorimetric determination of phosphorus. J Biol Chem 66:375–400

    Google Scholar 

  • Galloway JN, Schlesinger WH, Levy H, Michaels A, Schnoor JL (1995) Nitrogen-fixation—anthropogenic enhancement-environmental response. Global Biogeochem Cycles 9:235–252

    Article  Google Scholar 

  • Gower ST, Son Y (1992) Differences in soil and leaf litterfall nitrogen dynamics for 5 forest plantations. Soil Sci Soc Am 56:1959–1966

    Article  Google Scholar 

  • Gradowski T, Thomas SC (2006) Phosphorus limitation of sugar maple growth in central Ontario. Forest Ecol Manag 226:104–109

    Article  Google Scholar 

  • Gress SE, Nichols TD, Northcraft CC, Peterjohn WT (2007) Nutrient limitation in soils exhibiting differing nitrogen availabilities: what lies beyond nitrogen saturation? Ecology 88:119–130

    Article  Google Scholar 

  • Griffin JM, Lovett GM, Arthur MA, Weathers KC (2003) The distribution and severity of beech bark disease in the Catskill Mountains, NY. Can J For Res-Rev Can Rech For 33:1754–1760

    Article  Google Scholar 

  • Hendershot WH, Lalande H, Duquette M (1993) Soil reaction and exchangeable acidity. In: Carter MR (ed) Soil sampling and methods of analysis. Canadian Society of Soil Science. Lewis Publishers, Boca Raton, pp 141–159

    Google Scholar 

  • Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–334

    Article  Google Scholar 

  • Jeannotte R, Sommerville DW, Hamel C, Whalen JK (2004) A microplate assay to measure soil microbial biomass phosphorus. Biol Fertility Soils 40:201–205

    Article  Google Scholar 

  • Johnson D, Leake JR, Lee JA, Campbell CD (1998) Changes in soil microbial biomass and microbial activities in response to 7 years simulated pollutant nitrogen deposition on a heathland and two grasslands. Environ Pollut 103:239–250

    Article  Google Scholar 

  • Johnson AH, Frizano J, Vann DR (2003) Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure. Oecologia 135:487–499

    Google Scholar 

  • Juice SM, Fahey TJ, Siccama TG, Driscoll CT, Denny EG, Eagar C, Cleavitt NL, Minocha R, Richardson AD (2006) Response of sugar maple to calcium addition to Northern Hardwood Forest. Ecology 87:1267–1280

    Article  Google Scholar 

  • Kamei J, Pandey HN, Barik SK (2009) Tree species distribution and its impact on soil properties, and nitrogen and phosphorus mineralization in a humid subtropical forest ecosystem of northeastern India. Can J For Res-Rev Can Rech For 39:36–47

    Article  Google Scholar 

  • Killingbeck KT (1996) Nutrients in senesced leaves: Keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727

    Article  Google Scholar 

  • Lovett GM, Rueth H (1999) Soil nitrogen transformations in beech and maple stands along a nitrogen deposition gradient. Ecol Appl 9:1330–1344

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lovett GM, Weathers KC, Arthur MA, Schultz JC (2004) Nitrogen cycling in a northern hardwood forest: do species matter? Biogeochemistry 67:289–308

    Article  Google Scholar 

  • Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD (2006) Forest ecosystem responses to exotic pests and pathogens in eastern North America. BioScience 56:395–405

    Article  Google Scholar 

  • McIntosh RP (1972) Forests of the Catskill Mountains, New York. Ecol Monogr 42:143–161

    Article  Google Scholar 

  • Mohren GMJ, Vandenburg J, Burger FW (1986) Phosphorus deficiency induced by nitrogen input in Douglas-fir in the Netherlands. Plant Soil 95:191–200

    Article  Google Scholar 

  • Myers RG, Thien SJ, Pierzynski GM (1999) Using an ion sink to extract microbial phosphorus from soil. Soil Sci Soc Am J 63:1229–1237

    Article  Google Scholar 

  • Myers RG, Sharpley AN, Thien SJ, Pierzynski GM (2005) Ion-sink phosphorus extraction methods applied on 24 soils from the continental USA. Soil Sci Soc Am J 69:511–521

    Google Scholar 

  • Norton SA, Fernandez IJ, Kahl JS, Reinhardt RL (2004) Acidification trends and the evolution of neutralization mechanisms through time at the Bear Brook Watershed in Maine (BBWM), USA. Water Air Soil Pollut Focus 4:289–310

    Article  Google Scholar 

  • Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activity by N and P availability. Biogeochemistry 49:175–190

    Article  Google Scholar 

  • Pare D, Bernier B (1989a) Origin of the phosphorus deficiency observed in declining sugar maple stands in the Quebec Appalachians. Can J For Res-Rev Can Rech For 19:24–34

    Article  Google Scholar 

  • Pare D, Bernier B (1989b) Phosphorus-fixing potential of Ah-horizons and H-horizons subjected to acidification. Can J For Res-Rev Can Rech For 19:132–134

    Article  Google Scholar 

  • Perring MP, Hedin LO, Levin SA, McGroddy M, de Mazancourt C (2008) Increased plant growth from nitrogen addition should conserve phosphorus in terrestrial ecosystems. Proc Natl Acad Sci 105:1971–1976

    Article  Google Scholar 

  • Phoenix GK, Booth RE, Leake JR, Read DJ, Grime JP, Lee JA (2004) Simulated pollutant nitrogen deposition increases P demand and enhances root-surface phosphatase activities of three plant functional types in a calcareous grassland. New Phytol 161:279–289

    Article  Google Scholar 

  • Polyakova O, Billor N (2007) Impact of deciduous tree species on litterfall quality, decomposition rates and nutrient circulation in pine stands. Forest Ecol Manag 253:11–18

    Article  Google Scholar 

  • Pontius JA, Hallett RA, Jenkins JC (2006) Foliar chemistry linked to infestation and susceptibility to hemlock woolly adelgid (Homoptera : Adelgidae). Environ Entomol 35:112–120

    Article  Google Scholar 

  • Psenner R, Bostrom B, Dinka M, Pettersson K, Pucsko R, Sager M (1988) Fractionation of phosphorus in suspended matter and sediment. Arch Hydrobiol 30:98–103

    Google Scholar 

  • Rich JL (1934) Glacial geology of the Catskill Mountains. NY State Museum Bull 299:1–180

    Google Scholar 

  • Rubaek GH, Sibbesen E (1993) Resin extraction of labile, soil organic phosphorus. J Soil Sci 44:467–478

    Article  Google Scholar 

  • Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315

    Article  Google Scholar 

  • Sherman J, Fernandez IJ, Norton SA, Ohno T, Rustad LE (2006) Soil aluminum, iron, and phosphorus dynamics in response to long-term experimental nitrogen and sulfur additions at the Bear Brook watershed in Maine. USA Environ Monit Assess 121:421–429

    Google Scholar 

  • Sinsabaugh RL, Gallo ME, Lauber C, Waldrop MP, Zak DR (2005) Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75:201–215

    Article  Google Scholar 

  • Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    Google Scholar 

  • Spiers GA, McGill WB (1979) Effects of phosphorus addition and energy supply on acid phosphatase production and activity in soils. Soil Biol Biochem 11:3–8

    Article  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Stoddard JL, Murdoch PS (1991) Catskill Mountains. In: Charles DF (ed) Acidic deposition and aquatic ecosystems: regional case studies. Springer-Verlag, New York, pp 237–271

    Google Scholar 

  • Templer P (2005) Tree species effects on nitrogen cycling and retention: a synthesis of studies using 15 N tracers. In: Binkley D, Menyailo O (eds) Tree species effects on soils: implications for global change. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Templer P, Findlay S, Lovett G (2003) Soil microbial biomass and nitrogen transformations among five tree species of the Catskill Mountains, New York, USA. Soil Biol Biochem 35:607–613

    Article  Google Scholar 

  • Templer PH, Lovett GM, Weathers KC, Findlay SE, Dawson TE (2005) Influence of tree species on forest nitrogen retention in the Catskill Mountains, New York, USA. Ecosystems 8:1–16

    Article  Google Scholar 

  • Tessier JT, Raynal DJ (2003) Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. J Appl Ecol 40:523–534

    Article  Google Scholar 

  • van Heerwaarden LM, Toet S, Aerts R (2003) Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: facts and solutions. Oikos 101:664–669

    Article  Google Scholar 

  • Vaz MDR, Edwards AC, Shand CA, Cresser MS (1993) Phosphorus fractions in soil solution—influence of soil acidity and fertilizer additions. Plant Soil 148:175–183

    Article  Google Scholar 

  • Walbridge MR, Richardson CJ, Swank WT (1991) Vertical distribution of biological and geochemical phosphorus subcycles in 2 southern Appalachian forest soils. Biogeochemistry 13:61–85

    Article  Google Scholar 

  • Wallace ZP, Lovett GM, Hart JE, Machona B (2007) Effects of nitrogen saturation on tree growth and death in a mixed-oak forest. Forest Ecol Manag 243:210–218

    Article  Google Scholar 

  • Wallander H, Fossum A, Rosengren U, Jones H (2005) Ectomycorrhizal fungal biomass in roots and uptake of P from apatite by Pinus sylvestris seedlings growing in forest soil with and without wood ash amendment. Mycorrhiza 15:143–148

    Article  Google Scholar 

  • Weathers KC, Lovett GM, Likens GE, Lathrop R (2000) The effect of landscape features on deposition to Hunter Mountain, Catskill Mountains, New York. Ecol Appl 10:528–540

    Article  Google Scholar 

  • Wood TE (1980) Biological and chemical control of phosphorus cycling in a northern hardwood forest. Yale University, New Haven

    Google Scholar 

  • Wood T, Bormann FH, Voigt GK (1984) Phosphorus cycling in a northern hardwood forest—biological and chemical control. Science 223:391–393

    Article  Google Scholar 

  • Zou XM, Binkley D, Caldwell BA (1995) Effects of dinitrogen fixing trees on phosphorus biogeochemical cycling in contrasting forests. Soil Sci Soc Am J 59:1452–1458

    Google Scholar 

Download references

Acknowledgments

We thank the National Science Foundation (grants DEB 9981503 and DEB 0444895) for financial support for this work. We are grateful to Chris Barton, Noah Beck, Margaret Carreiro, Jim Crutchfield, Ivan Fernandez, Stuart Findlay, David Fischer, Jake Griffin, Millie Hamilton, Amy Herberg, Rob Keefe, Brent Mellen, Jen Peters, Rachel Ruppel, Maggie Ward, and other employees and students at the Cary Institute and the University of Kentucky who helped with the sample collection and analysis. We thank the University of Kentucky’s Regulatory Services Soil Testing Laboratory for P analyses on plant and soil material. This is a publication of the Kentucky Agricultural Experiment Station (09-09-016) and a contribution to the program of the Cary Institute of Ecosystem Studies.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Matthew P. Weand.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Weand, M.P., Arthur, M.A., Lovett, G.M. et al. The phosphorus status of northern hardwoods differs by species but is unaffected by nitrogen fertilization. Biogeochemistry 97, 159–181 (2010). https://doi.org/10.1007/s10533-009-9364-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-009-9364-2

Keywords

Navigation