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Mycorrhizal associations of dominant trees influence nitrate leaching responses to N deposition

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Abstract

Temperate forests receive some of the highest rates of nitrogen (N) deposition in the world. While numerous studies have investigated the effects of N enrichment on forests, there is little consensus on why some forests become N saturated while others do not. To investigate this, we used a multi-factor meta-analysis to simultaneously estimate the relative importance of several environmental, experimental, and anthropogenic variables on nitrate (NO3 ) leaching in response to experimental N addition. Given that overstory tree species composition and soil C:N ratio influence forest responses to N, we hypothesized that forests dominated by arbuscular mycorrhizal (AM) trees would respond differently than forests dominated by ectomycorrhizal (ECM) trees in the context of forest susceptibility to NO3 leaching. We found that mycorrhizal association is an important predictor of NO3 leaching, and AM-dominated forests leach more NO3 in response to N deposition than ECM forests. Additionally, we found that the amount of total N added, ambient N deposition rates, and the form of N added influenced the magnitude of the NO3 leaching response. Given that the mycorrhizal associations of most temperate trees are known, our results suggest that this functional grouping may be useful in identifying forests that are most susceptible to NO3 leaching.

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References

  • Aber JD, Driscoll CT (1997) Effects of land use, climate variation, and N deposition on N cycling and C storage in northern hardwood forests. Glob Biogeochem Cycles 11(4):639–648

    Article  Google Scholar 

  • Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM (1989) Nitrogen saturation in northern forest ecosystems. Bioscience 39(6):378–386

    Article  Google Scholar 

  • Aber JD, Magill A, McNulty SG, Boone RD, Nadelhoffer KJ, Downs M, Hallett R (1995) Forest biogeochemistry and primary production altered by nitrogen saturation. Water Air Soil Pollut 85(3):1665–1670

    Article  Google Scholar 

  • Aber JD, McDowell W, Nadelhoffer K, Magill A, Berntson G, Kamakea M, McNulty S, Currie W, Rustad L, Fernandez I (1998) Nitrogen saturation in temperate forest ecosystems —hypotheses revisited. Bioscience 48(11):921–934

    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(4):375–389

    Article  Google Scholar 

  • Agren GI, Bosatta E (1988) Nitrogen saturation of terrestrial ecosystems. Environ Pollut 54(3–4):185–197

    Article  Google Scholar 

  • Ahern CR, Baker DE, Aitken RL (1995) Models for relating pH measurements in water and calcium-chloride for a wide-range of pH, soil types and depths. Plant Soil 171(1):47–52

    Article  Google Scholar 

  • Bainard LD, Klironomos JN, Gordon AM (2011) The mycorrhizal status and colonization of 26 tree species growing in urban and rural environments. Mycorrhiza 21(2):91–96

    Article  Google Scholar 

  • Barrios E, Buresh RJ, Sprent JI (1996) Nitrogen mineralization in density fractions of soil organic matter from maize and legume cropping systems. Soil Biol Biochem 28(10–11):1459–1465

    Article  Google Scholar 

  • Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20(1):30–59

    Article  Google Scholar 

  • Brundrett M, Murase G, Kendrick B (1990) Comparative anatomy of roots and mycorrhizae of common Ontario trees. Can J Bot 68(3):551–578

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer-Verlag, New York

    Google Scholar 

  • Campbell JL, Eagar C, McDowell WH, Hornbeck JW (2000) Analysis of nitrogen dynamics in the Lye Brook Wilderness area, Vermont, USA. Water Air Soil Pollut 122(1–2):63–75

    Article  Google Scholar 

  • Castellano MJ, Kaye JP, Lin H, Schmidt JP (2012) Linking carbon saturation concepts to nitrogen saturation and retention. Ecosystems 15(2):175–187

    Article  Google Scholar 

  • Christopher SF, Page BD, Campbell JL, Mitchell MJ (2006) Contrasting stream water NO3− and Ca2+ in two nearly adjacent catchments: the role of soil Ca and forest vegetation. Glob Change Biol 12(2):364–381

    Article  Google Scholar 

  • Cornelissen JHC, Aerts R, Cerabolini B, Werger MJA, van der Heijden MGA (2001) Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia 129(4):611–619

    Article  Google Scholar 

  • De Boer W, Kowalchuk GA (2001) Nitrification in acid soils: micro-organisms and mechanisms. Soil Biol Biochem 33(7–8):853–866

    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

    Article  Google Scholar 

  • Dise NB, Wright RF (1995) Nitrogen leaching from European forests in relation to nitrogen deposition. For Ecol Manag 71(1–2):153–161

    Article  Google Scholar 

  • Dise NB, Matzner E, Forsius M (1998) Evaluation of organic horizon C: n ratio as an indicator of nitrate leaching in conifer forests across Europe. Environ Pollut 102:453–456

    Article  Google Scholar 

  • Dise NB, Rothwell JJ, Gauci V, van der Salm C, de Vries W (2009) Predicting dissolved inorganic nitrogen leaching in European forests using two independent databases. Sci Total Environ 407(5):1798–1808

    Article  Google Scholar 

  • Driscoll CT, Whitall D, Aber J, Boyer E, Castro M, Cronan C, Goodale CL, Groffman P, Hopkinson C, Lambert K, Lawrence G, Ollinger S (2003) Nitrogen pollution in the northeastern United States: sources, effects, and management options. Bioscience 53(4):357–374

    Article  Google Scholar 

  • Elliott EM, Kendall C, Wankel SD, Burns DA, Boyer EW, Harlin K, Bain DJ, Butler TJ (2007) Nitrogen isotopes as indicators of NOx source contributions to atmospheric nitrate deposition across the Midwestern and northeastern United States. Environ Sci Technol 41(22):7661–7667

    Article  Google Scholar 

  • Emmett B (2007) Nitrogen saturation of terrestrial ecosystems: some recent findings and their implications for our conceptual framework. Water Air Soil Pollut Focus 7(1):99–109

    Article  Google Scholar 

  • Finzi AC, Canham CD, Van Breeman N (1998a) Canopy tree-soil interactions within temperate forests: species effects on pH and cations. Ecol Appl 8(3):905

    Google Scholar 

  • Finzi AC, Van Breemen N, Canham CD (1998b) Canopy tree soil interactions within temperate forests: species effects on soil carbon and nitrogen. Ecol Appl 8(2):440–446

    Google Scholar 

  • Frey SD, Knorr M, Parrent J, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in a forest ecosystem. For Ecol Manag 196(1):157–171

    Article  Google Scholar 

  • Galloway JN, Cowling EB (2002) Reactive nitrogen and the world: 200 years of change. Ambio 31(2):64–71

    Google Scholar 

  • Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ (2003) The nitrogen cascade. Bioscience 53(4):341–356

    Article  Google Scholar 

  • Goodale CL, Aber JD (2001) The long-term effects of land-use history on nitrogen cycling in northern hardwood forests. Ecol Appl 11(1):253–267

    Article  Google Scholar 

  • Gundersen P, Callesen I, de Vries W (1998) Nitrate leaching in forest ecosystems is related to forest floor C/N ratios. Environ Pollut 102:403–407

    Article  Google Scholar 

  • Hansen K, Rosenqvist L, Vesterdal L, Gundersen P (2007) Nitrate leaching from three afforestation chronosequences on former arable land in Denmark. Glob Change Biol 13(6):1250–1264

    Article  Google Scholar 

  • Hättenschwiler S, Vitousek PM (2000) The role of polyphenols in terresterial ecosystem nutrient cycling. Trends Ecol Evol 15(6):238–243

    Article  Google Scholar 

  • Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13(3):394–407

    Article  Google Scholar 

  • Högberg P, Fan HB, Quist M, Binkley D, Tamm CO (2006) Tree growth and soil acidification in response to 30 years of experimental nitrogen loading on boreal forest. Glob Change Biol 12(3):489–499

    Article  Google Scholar 

  • Holland EA, Dentener FJ, Braswell BH, Sulzman JM (1999) Contemporary and pre-industrial global reactive nitrogen budgets. Biogeochemistry 46(1–3):7–43

    Google Scholar 

  • Holland EA, Braswell BH, Sulzman J, Lamarque JF (2005) Nitrogen deposition onto the United States and Western Europe: synthesis of observations and models. Ecol Appl 15(1):38–57

    Article  Google Scholar 

  • IBM Corp (2011) IBM SPSS statistics for windows, version 20.0. IBM Corp, Armonk, NY

    Google Scholar 

  • Johnson DW (1992) Nitrogen-retention in forest soils. J Environ Qual 21(1):1–12

    Article  Google Scholar 

  • Kraus TEC, Dahlgren RA, Zasoski RJ (2003) Tannins in nutrient dynamics of forest ecosystems—a review. Plant Soil 256(1):41–66

    Article  Google Scholar 

  • Lajtha K, Jarrell WM, Johnson DW, Sollins P (1999) Collection of soil solution. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P (eds) Standard soil methods for long-term ecological research. Oxford University Press, New York, pp 166–182

    Google Scholar 

  • Langley JA, Hungate BA (2003) Mycorrhizal controls on belowground litter quality. Ecology 84(9):2302–2312

    Article  Google Scholar 

  • Lovett GM, Goodale CL (2011) A new conceptual model of nitrogen saturation based on experimental nitrogen addition to an oak forest. Ecosystems 14(4):615–631

    Article  Google Scholar 

  • Lovett GM, Weathers KC, Sobczak WV (2000) Nitrogen saturation and retention in forested watersheds of the Catskill Mountains, New York. Ecol Appl 10(1):73–84

    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(7):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(3):289–308

    Article  Google Scholar 

  • MacDonald JA, Dise NB, Matzner E, Armbruster M, Gundersen P, Forsius M (2002) Nitrogen input together with ecosystem nitrogen enrichment predict nitrate leaching from European forests. Glob Change Biol 8(10):1028–1033

    Article  Google Scholar 

  • Magill AH, Downs MR, Nadelhoffer KJ, Hallett RA, Aber JD (1996) Forest ecosystem response to four years of chronic nitrate and sulfate additions at Bear Brooks Watershed, Maine, USA. For Ecol Manag 84(1–3):29–37

    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(2):402–415

    Article  Google Scholar 

  • 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(3):238–253

    Article  Google Scholar 

  • Marques R, Ranger J, Gelhaye D, Pollier B, Ponette Q, Goedert O (1996) Comparison of chemical composition of soil solutions collected by zero-tension plate lysimeters with those from ceramic-cup lysimeters in a forest soil. Eur J Soil Sci 47(3):407–417

    Article  Google Scholar 

  • McCormack ML, Adams TS, Smithwick EAH, Eissenstat DM (2012) Predicting fine root lifespan from plant functional traits in temperate trees. New Phytol 195(4):823–831

    Article  Google Scholar 

  • McNulty SG, Aber JD, Newman SD (1996) Nitrogen saturation in a high elevation New England spruce-fir stand. For Ecol Manag 84(1–3):109–121

    Article  Google Scholar 

  • McNulty SG, Boggs J, Aber JD, Rustad L, Magill A (2005) Red spruce ecosystem level changes following 14 years of chronic N fertilization. For Ecol Manag 219(2–3):279–291

    Article  Google Scholar 

  • Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63(3):621–626

    Article  Google Scholar 

  • Mitchell MJ, Foster NW, Shepard JP, Morrison IK (1992) Nutrient cycling in Huntington Forest and Turkey Lakes deciduous stands—nitrogen and sulfur. Can J For Res 22(4):457–464

    Article  Google Scholar 

  • Moorhead DL, Lashermes G, Sinsabaugh RL (2012) A theoretical model of C- and N-acquiring exoenzyme activities, which balances microbial demands during decomposition. Soil Biol Biochem 53:133–141

    Article  Google Scholar 

  • Murdoch PS, Stoddard JL (1992) The role of nitrate in the acidification of streams in the Catskill Mountains of New York. Water Resour Res 28(10):2707–2720

    Article  Google Scholar 

  • Nagakura J, Akama A, Mizoguchi T, Okabe H, Shigenaga H, Yamanaka T (2006) Effects of chronic nitrogen application on the growth and nutrient status of a Japanese cedar (Cryptomeria japonica) stand. J For Res 11(5):299–304

    Article  Google Scholar 

  • Northup RR, Dahlgren RA, McColl JG (1998) Polyphenols as regulators of plant-litter-soil interactions in Northern California’s pygmy forest: a positive feedback? Biogeochemistry 42(1):189–220

    Article  Google Scholar 

  • Pastor J, Post WM (1986) Influence of climate, soil-moisture, and succession on forest carbon and nitrogen cycles. Biogeochemistry 2(1):3–27

    Article  Google Scholar 

  • 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(1):41–51

    Article  Google Scholar 

  • Pinder RW, Appel KW, Dennis RL (2011) Trends in atmospheric reactive nitrogen for the Eastern United States. Environ Pollut 159(10):3138–3141

    Article  Google Scholar 

  • Prosser JI (2011) Soil nitrifiers and nitrification. In: Ward BB, Arp DJ, Klotz MG (eds) Nitrification. ASM Press, Washington, DC, pp 347–383

    Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—A journey towards relevance? New Phytol 157(3):475–492

    Article  Google Scholar 

  • Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101(30):11001–11006

    Article  Google Scholar 

  • Ross DS, Wemple BC, Jamison AE, Fredriksen G, Shanley JB, Lawrence GB, Bailey SW, Campbell JL (2009) A cross-site comparison of factors influencing soil litrification rates in Northeastern USA forested watersheds. Ecosystems 12(1):158–178

    Article  Google Scholar 

  • Ross DS, Shanley JB, Campbell JL, Lawrence GB, Bailey SW, Likens GE, Wemple BC, Fredriksen G, Jamison AE (2012) Spatial patterns of soil nitrification and nitrate export from forested headwaters in the northeastern United States. J Geophys Res 117:G01009

    Google Scholar 

  • Schulze ED, De Vries W, Hauhs M, Rosen K, Rasmussen L, Tamm CO, Nilsson J (1989) Critical loads for nitrogen deposition on forest ecosystems. Water Air Soil Pollut 48(3–4):451–456

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, San Diego

    Google Scholar 

  • Stoddard JL (1994) Long-term changes in watershed retention of nitrogen—its causes and aquatic consequences. Adv Chem Ser 237:223–284

    Article  Google Scholar 

  • Subbarao GV, Ito O, Sahrawat KL, Berry WL, Nakahara K, Ishikawa T, Watanabe T, Suenaga K, Rondon M, Rao IM (2006) Scope and strategies for regulation of nitrification in agricultural systems-challenges and opportunities. Crit Rev Plant Sci 25(4):303–335

    Article  Google Scholar 

  • Sutton MA (2011) The European nitrogen assessment: sources, effects, and policy perspectives. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Talbot JM, Treseder KK (2010) Controls over mycorrhizal uptake of organic nitrogen. Pedobiologia 53(3):169–179

    Article  Google Scholar 

  • Templer PH, Pinder RW, Goodale CL (2012) Effects of nitrogen deposition on greenshouse-gas fluxes for forests and grasslands of North America. Front Ecol Environ 10(10):547–553

    Article  Google Scholar 

  • Thomas RQ, Canham CD, Weathers KC, Goodale CL (2010) Increased tree carbon storage in response to nitrogen deposition in the US. Nat Geosci 3(1):13–17

    Article  Google Scholar 

  • U.S. Department of Agriculture NRCS National soil survey handbook, title 430-VI

  • van der Salm C, de Vries W, Reinds GJ, Dise NB (2007) N leaching across European forests: derivation and validation of empirical relationships using data from intensive monitoring plots. For Ecol Manag 238(1–3):81–91

    Article  Google Scholar 

  • Vesterdal L, Schmidt IK, Callesen I, Nilsson LO, Gundersen P (2008) Carbon and nitrogen in forest floor and mineral soil under six common European tree species. For Ecol Manag 255(1):35–48

    Article  Google Scholar 

  • Viechtbauer W (2010) Conducting meta-analyses in R with the metafor package. J Stat Softw 36(3):1–48

    Google Scholar 

  • Vitousek PM, Reiners WA (1975) Ecosystem succession and nutrient retention—hypothesis. Bioscience 25(6):376–381

    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. For Ecol Manag 243(2–3):210–218

    Article  Google Scholar 

  • Wallenstein MD, McNulty S, Fernandez I, Boggs J, Schlesinger WH (2006) Nitrogen fertilization decreases forest soil funal and bacterial biomass in three long-term N fertilization experiments. For Ecol Manag 222:459–468

    Article  Google Scholar 

  • Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16(5):299–363

    Article  Google Scholar 

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Acknowledgments

This project was supported by grants from the National Science Foundation (DEB, Ecosystem Studies; #1153401), Indiana University’s Center for Research in Environmental Sciences (CRES), and the Indiana Academy of Sciences. We thank Edward Brzostek, Anna Rosling, Zack Brown, Rena Kingery, and Andrew Quebbeman for comments on drafts of this manuscript, Jason Hoeksema, Jim Bever, and Stephanie Dickson for guidance on conducting the meta-analysis, and Wolfgang Viechtbauer for providing model code.

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Correspondence to Meghan G. Midgley.

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Midgley, M.G., Phillips, R.P. Mycorrhizal associations of dominant trees influence nitrate leaching responses to N deposition. Biogeochemistry 117, 241–253 (2014). https://doi.org/10.1007/s10533-013-9931-4

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