Abstract
We conducted a 7-year field study at two oak-dominated forest sites which differ in their atmospheric N deposition to test the hypothesis that red oak regeneration failure in the upper Midwestern US forests, at least in part, results from increased N load. The sites are located in Swallow Cliffs (SC) in Cook County, Illinois, and Indiana Dunes National Lakeshore (IDNL) in Porter County, Indiana. Annual wet NO3 − deposition for the 22 years immediately prior to the experiments was significantly higher in IDNL than in the SC site. Results from common garden experiments showed that oak seedling biomass was 60 % lower at IDNL compared with SC, but there was little site effect on growth of maple seedlings. Experimental N addition also resulted in a 45 % decrease in the total biomass of the oak seedlings at SC, but had no significant effect on the biomass at IDNL. Maple seedlings responded little to experimental fertilization. The growth rate of mature oak trees was also lower at IDNL but to a much smaller extent than that of seedlings. Maple trees did not significantly differ between sites. We conclude that: (1) chronic N load adversely affects seedling performance of red oak, but not sugar maple, in these temperate forests; and (2) the seedling establishment phase rather than the adult tree is the likely target stage for this adverse effect of N loading. The exact mechanisms for the differential effects of N on these co-occurring species are not clear, but different plasticity in fractional biomass and N allocation to the leaves might be involved.
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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. 10.1029/97GB01366 ISSN:0886–6236
Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM (1989) Nitrogen saturation in northern forest ecosystems. Bioscience 39(6):378–386
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
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
Abrahamson W, Caswell H (1982) On the comparative allocation of biomass, energy and nutrients in plants. Ecology 63:982–991
Abrams MD (2003) Where has all the white oak gone? Bioscience 53:927–939
Aldrich PR, Parker GR, Romero-Severson J, Michler CH (2005) Confirmation of oak recruitment failure in Indiana old-growth forest: 75 years of data. For Sci 51:406–416
Alexander HD, Arthur MA (2009) Foliar morphology and chemistry of upland oaks, red maple, and sassafras seedlings in response to single and repeated prescribed fires. Can J For Res 39:740–754. doi:10.1139/x09-007
Alexander HD, Arthur MA, Loftis DL, Green SR (2008) Survival and growth of upland oak and co-occurring competitor seedlings following single and repeated prescribed fires. For Ecol Manage 256:1021–1030. doi:10.1016/j.foreco.2008.06.004
Avis PG, Mueller GM, Lussenhop J (2008) Ectomycorrhizal fungal communities in two North American oak forests respond to nitrogen addition. New Phytol 179:472–483
Baxter J, Pickett STA, Carreiro MM, Dighton J (1999) Ectomycorrhizal diversity and community structure in oak forest stands exposed to contrasting anthropogenic impacts. Can J Bot 77:771–782
Bazzaz FA (1997) Allocation of resources in plants: state-of-the-science and critical questions. In: Bazzaz FA, Grace J (eds) Plant resource allocation. Physiological Ecology Series of Academic Press, San Diego, pp 14–37
Bedison JE, McNeil BE (2009) Is the growth of temperate forest trees enhanced along an ambient nitrogen deposition gradient? Ecology 90(7):1736–1742
Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman J-W, 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 20:30–59. doi:10.1890/08-1140.1
Borden KK (2007) Seasonal dynamics of soil nitrogen in temperate forests affected by anthropogenic nitrogen deposition. Master thesis, University of Illinois at Chicago, Chicago, IL, USA
Boudsocq S, Niboyet A, Lata JC, Raynaud X, Loeuille N, Mathieu J, Blouin M, Abbadie L, Barot S (2012) Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? Am Nat 180:60–69
Bowles ML, Jones MD (2008) Chronological change in old-growth forests of the Chicago region. Report to the Illinois department of natural resources and the Chicago wilderness. The Morton Arboretum, Lisle, Illinois, US
Bowles ML, Jones M, McBride J, Bell T, Dunn C (2000) Structural composition and species richness indices for upland forests of the Chicago region. Erigenia 18:30–57
Bowles ML, Jones M, Dunn C, McBride J, Bushey C, Moran R (2003) Twenty-year woody vegetation changes in northern flatwoods and mesic forest at Ryerson conservation area, Lake County, Illinois. Erigenia 18:30–57
Bowles ML, Jones M, McBride J, Bell T, Dunn C (2005) Temporal instability in Chicago’s upland old growth forests. Chicago Wilderness J 3(2):5–6. http://www.chicagowilderness
Britto DT, Kronzucker HJ (2013) Ecological significance and complexity of N-source preference in plants. Ann Bot 112:957–963
Brouwer R (1983) Functional equilibrium: sense or nonsense? Neth J Agric Sci 31:335–348
Canham CD, Berkowitz AR, Kelly VR, Lovett GM, Ollinger SV, Schnurr J (1996) Biomass allocation and multiple resource limitation in tree seedlings. Can J For Res 26:1521–1530. doi:10.1139/x26-171
Catovsky S, Bazzaz FA (2002a) Feedbacks between canopy composition and seedlings regeneration in mixed conifer broadleaved forests. Oikos 98:403–420
Catovsky S, Bazzaz FA (2002b) Nitrogen availability influences regeneration of temperate tree species in the understory seedling bank. Ecol Appl 12:1056–1070. doi:10.2307/3061036
Catovsky S, Bradford MA, Hector A (2002) Biodiversity and ecosystem productivity: implications for carbon storage. Oikos 97:443–448. doi:10.1034/j.1600-0706.2002.970315.x
Cha DH, Appel HM, Frost CJ, Schultz JC, Steiner KC (2010) Red oak responses to nitrogen addition depend on herbivory type, tree family, and site. Forest Ecol and Manag 259:1930–1937. doi:10.1016/j.foreco.2010.02.004
Clark FB (1993) An historical perspective of oak regeneration. In: Proceedings oak regeneration: serious problems practical recommendations, Knoxville, Tenn, pp 3–13
Clark CM, Tilman D (2008) Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451:712–715
Clark CM, Morefield PE, Gilliam FS, Pard LH (2013) Estimated losses of plant biodiversity in the United States from historical N deposition (1985–2010). Ecology 94:1441–1448
Cox F, Barsoum N, Lilleskov EA, Bidartondo M (2010) Nitrogen availability is a primary determinant of conifer mycorrhizas across complex environmental gradients. Ecol Lett 13:1103–1113
Dickie IA, Schnitzer SA, Reich PB, Hobbie SE (2007) Is oak establishment in old-fields and savanna openings context dependent? J Ecol 95:309–320. doi:10.1111/j.1365-2745.01202x
Dighton J, Tuininga AR, Gray DM, Huskins RE, Belton T (2004) Impacts of atmospheric deposition on New Jersey pine barrens forest soils and communities of ectomycorrhizal. For Ecol Manage 201:131–144
Dirnböck T, Grandin U, Bernhardt-Römermann M, Beudert B, Canullo R, Forsius M, Grabner M-T, Holmberg M, Kleemola S, Lundin L, Mirtl M, Neumann M, Pompei E, Salemaa M, Starlinger F, Staszewski T, Uziębło AK (2014) Forest floor vegetation response to nitrogen deposition in Europe. Glob Change Biol 20:429–440. doi:10.1111/gcb.12440
Downs MR, Nadelhoffer KJ, Melillo JM, Aber JD (1993) Foliar and fine root nitrate reductase activity in seedlings of four forest tree species in relation to nitrogen availability. Trees Struct Funct 7:233–236
Edwards IP, Cripliver JL, Gillespie AR, Johnsen KH, Scholler M, Turco RF (2004) Nitrogen availability alters macrofungal basidiomycete community structure in optimally fertilized loblolly pine forests. New Phytol 162:755–770
Elvir JA, Wiersma GB, White A, Fernandez I (2003) Effects of chronic ammonium sulfate treatment on basal area increment in red spruce and sugar maple at the Bear Brook watershed in Maine. Can J For Res 33:862–869
Elvir JA, Wiersma GB, Day ME, Greenwood MS, Fernandez IJ (2006) Effects of enhanced nitrogen deposition on foliar chemistry and physiological processes of forest trees at the Bear Brook Watershed in Maine. For Ecol Manage 221:207–214
Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19
Falxa-Raymond N, Patterson AE, Schuster WS, Griffin KL (2012) Oak loss increases foliar nitrogen, δ15 N and growth rates of Betula lentain in a northern temperate deciduous forest. Tree Physiol 32:1092–1101
Fei S, Steiner KC (2008) Relationships between advance oak regeneration and biotic and abiotic factors. Tree Physiol 28:1111–1119
Ferretti M, Marchetto A, Arisci S, Bussotti F, Calderisi M, Carnicelli S, Cecchini G, Fabbio G, Bertini G, Matteucci G, Cinti B, Salvati L, Pompei E (2014) On the tracks of nitrogen deposition effects on temperate forests at their southern European range—an observational study from Italy. Glob Change Biol. doi:10.1111/gcb.12552
Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, New York, pp 25–54
Francis R, Read DJ (1994) The contributions of mycorrhizal fungi to the determination of plant community structure. Plant Soil 159:11–25
Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby J (2003) The nitrogen cascade. Bioscience 53:341–356
Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vöosmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226. doi:10.1007/s10533-004-0370-0
Gilliam FS (2006) Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J Ecol 94:1176–1191. doi:10.1111/j.1365-2745.2006.01155.x
Gilliam FS (2007) The ecological significance of the herbaceous layer in temperate forest ecosystems. Bioscience 57:845–858
Gilliam FS, Yurish BM, Adams MB (2001) Temporal and spatial variation of nitrogen transformations in nitrogen saturated soils of a Central Appalachian hardwood forest. Can J For 31:1768–1785
Gutschick VP, Kay LE (1995) Nutrient-limited growth rates: quantitative benefits of stress responses and some aspects of regulation. J Exp Bot 46:995–1009
Holland E, Braswell B, Sulzman J, Lamarque JF (2005) Nitrogen deposition onto the United States and Western Europe: synthesis of observations and models. Ecol Appl 15:38–57
Isbell F, Tilman D, Polasky S, Binder S, Hawthorne P (2013) Low biodiversity state persists two decades after cessation of nutrient enrichment. Ecol Lett 16:454–460
Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647
Jonsson L, Anders D, Tor-Erik B (2000) Spatiotemporal distribution of an ectomycorrhizal community in an oligotrophic Swedish Picea abies forest subjected to experimental nitrogen addition: above- and below-ground views. For Ecol Manage 132:143–156
Jonsson LM, Nilsson MC, Wardle DA, Zackrisson O (2001) Context dependent effects of ectomycorrhizal species richness on tree seedling productivity. Oikos 93:353–364
Karen O, Hogberg N, Dahlberg A, Jonsson L, Nylund JE (1997) Inter- and intraspecific variation in the ITS region of rDNA of ectomycorrhizal fungi in Fennoscandia as detected by endonuclease analysis. New Phytol 136:313–325
Klironomos JN, Zobel M, Tibbett M, Stock WD, Rillig MC, Parrent JL, Moora M, Kock AM, Facelli JM, Dickie IA, Bever JD (2011) Forces that structure plant communities: quantifying the importance of the mycorrhizal symbiosis. New Phytol 189:366–370
Loftis DL, McGee CE, ed. (1993) Oak regeneration: serious problems, practical recommendations; symposium proceedings, Knoxville, Tennessee, September 1992. General technical report SE-84. USDA Forest Service, Southeastern Forest Experiment Station
Lorimer CG (1993) Causes of the oak regeneration problem. USDA For Serv Gen Tech Report SE SE–84
Lovett GM, Mitchell MJ (2004) Sugar maple and nitrogen cycling in the forests of eastern North America. Front Ecol Environ 2:81–88. doi:10.2307/3868214
Lovett GM, Rueth H (1999) Soil nitrogen transformations in beech and maple stands along a nitrogen deposition gradient. Ecol Appl 9:1330–1344. doi:10.2307/2641400
Lovett GM, Weathers KC, Sobczak W (2000) Nitrogen saturation and retention in forested watersheds of the Catskill Mountains, New York. Ecol Appl 10:73–84
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 7:402–415
Matson P, Lohse KA, Hall SJ (2002) The globalization of nitrogen deposition: consequences for terrestrial ecosystems. Ambio 31:113–119. doi:10.1639/0044-7447(2002)031[0113:tgondc]2.0.co;2
McNeil BE, Martel RE, Read JM (2006) GIS and biogeochemical models for examining the legacy of forest disturbance in the Adirondack Park, NY, USA. Ecol Model 195:281–295
McNulty SG, Aber JD, Newman SD (1996) Nitrogen saturation in a high elevation New England spruce-fir stand. For Ecol Manage 84:109–121
Mendivelso HA, Camarero JJ, Obregon OR, Guitierrez E, Toledo M (2013) Differential growth responses to water balance of coexisting deciduous tree species are linked to wood density in a Bolivian tropical dry forest. PLoS One 8(10):e73855. doi:10.1371/journal.pone.073855
Newingham BA, Callaway RM, BassiriRad H (2007) Allocating nitrogen away from a herbivore: a novel compensatory response to root herbivory. Oecologia 153:913–920. doi:10.1007/s00442-007-0791-2
Norby RJ (1998) Nitrogen deposition: a component of global change analyses. New Phytol 139:189–200
Patterson SL, Zak DR, Burton AJ, Talhelm AF, Pregitzer KS (2012) Simulated N deposition negatively impacts sugar maple regeneration in a northern hardwood ecosystem. J Appl Ecol 49:155–163. doi:10.1111/j.1365-2664.2011.02090.x
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 199:41–51
Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Aust J Plant Physiol 27:595–607
Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391
Reynolds HL, D’Antonio C (1996) The ecological significance of plasticity in root weight ratio in response to nitrogen: opinion. Plant Soil 185:75–97
Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774
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
Southon GE, Field C, Caporn SJM, Britton AJ, Power SA (2013) Nitrogen deposition reduces plant diversity and alters ecosystem functioning: field-scale evidence from a nationwide survey of UK heathlands. PLoS One 8(4):e59031. doi:10.1371/journal.pone.0059031
Stanturf JA, Stone EL Jr, McKittrick RC (1989) Effects of added nitrogen on growth of hardwood trees in southern New York. Can J For Res 19:279–284
Stevens CJ, Dise NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879
Stevens CJ, Dise NB, Gowing DJG, Mountford JO (2006) Loss of forb diversity in relation to nitrogen deposition in the UK: regional trends and potential controls. Glob Change Biol 12:1823–1833. doi:10.1111/j.1365-2486.2006.01217.x
Stevens C, Duprè C, Gaudnik C, Dorland E, Dise N, Gowing D, Bleeker A, Alard D, Bobbink R, Fowler D, Vandvik V, Corcket E, Mountford JO, Aarrestad PA, Muller S, Diekmann M (2011) Changes in species composition of European acid grasslands observed along a gradient of nitrogen deposition. J Veg Sci 22:207–215. doi:10.1111/j.1654-1103.2010.01254.x
Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL, Milchunas DG, Pennings S (2005) Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proc Natl Acad Sci USA 102:4387–4392
Talhelm AF, Burton AJ, Pregitzer KS, Campione MA (2013) Chronic nitrogen deposition reduces the abundance of dominant forest understory and groundcover species. For Ecol Manage 293:39–48
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. doi:10.1023/b:plso.0000037047.16616.98
Thomas FM, Hilker C (2000) Nitrate reduction in leaves and roots of young pedunculate oaks (Quercus robur) growing on different nitrate concentrations. Environ Exp Bot 43:19–32. doi:10.1016/s0098-8472(99)00040-4
Thomas FM, Blank R, Hartmann G (2002) Abiotic and biotic factors and their interactions as causes of oak decline in Central Europe. For Pathol 32:277–307. doi:10.1046/j.1439-0329.2002.00291.x
Thomas RQ, Canham CD, Weathers KC, Goodale CL (2010) Increased tree carbon storage in response to nitrogen deposition in the US. Nat Geosci 3:13–17. doi:10.1038/ngeo721
Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University Press, Princeton
Truax B, Gagnon D, Chevrier N (1994) Nitrate reductase activity in relation to growth and soil N-forms in red oak and red ash planted in 3 different environments-forest, clear-cut and field. For Ecol Manage 64:71–82. doi:10.1016/0378-1127(94)90128-7
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:72–75
van der Heijden MG, Bardgett RD, van Straalen NM (2008a) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11(3):296–310
van der Heijden MGA, Bardgett RD, van Straalen NM (2008b) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310
Vitousek PM, Aber J, 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 7:737–750
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 Manage 243:210–218. doi:10.1016/j.foreco.2007.02.015
Zaccherio MT, Finzi AC (2007) Atmospheric deposition may affect northern hardwood forest composition by altering soil nutrient supply. Ecol Appl 17:1929–1941
Zerihun A, Bassirirad H (2001) Interspecies variation in nitrogen uptake kinetic responses of temperate forest species to elevated CO2: potential causes and consequences. Glob Chang Biol 7:211–222
Acknowledgments
We thank M. Jorgensen, W. Gaswick, P. Orland, P. Patel, and J. Zayner who were instrumental in transplanting, harvesting, processing and data analyses. We also thank B. Tsang and S. Harrison for their editorial comments on an earlier version of the manuscript. M. Bowles and R. Fahey of the Morton Arboretum have intimate knowledge of the community ecology dynamics of oak and maples in these regionally important forests. We benefited immensely from their insights and feedbacks on various aspects of this project. Valuable comments from J. Lichstein and two anonymous reviewers helped improved various aspects of this manuscript. Support for this work was provided by the National Science Foundation.
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BassiriRad, H., Lussenhop, J.F., Sehtiya, H.L. et al. Nitrogen deposition potentially contributes to oak regeneration failure in the Midwestern temperate forests of the USA. Oecologia 177, 53–63 (2015). https://doi.org/10.1007/s00442-014-3119-z
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DOI: https://doi.org/10.1007/s00442-014-3119-z