Abstract
Nitrogen (N) fertilization has enhanced the forest land carbon (C) sink by increasing the amount of C stored in soils, possibly through reductions in decomposition. Established differences in nutrient acquisition strategies between trees that associate with arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) fungi have been shown to influence the magnitude of this N effect on decomposition and soil C stocks. However, N deposition is declining across many temperate North American forests and little is known about how mycorrhizal-associated strategies in trees may impact short-term recovery. To examine divergent nutrient acquisition responses to N between AM and ECM systems, we developed a conceptual framework based on the idea that N fertilization reduces the C cost of N acquisition. In this framework, under N fertilization, ECM trees shift from N mining to N foraging and AM trees shift from mycorrhizal foraging to root foraging. We expanded on this framework by hypothesizing that initial recovery occurs across a spectrum, where nutrient foraging strategies either (1) persist in their N fertilized state, (2) return to the ambient state, or (3) shift to a new steady state. We tested this framework by examining fine root biomass and morphology, mycorrhizal colonization, and soil enzyme activities in organic horizon, bulk mineral, and rhizosphere mineral soils in AM and ECM dominated plots during the last year of a ~ 30 year N fertilization experiment and 1-year after fertilization ceased at Bear Brook Watershed, in Maine USA. Overall, our results indicate that N fertilization disrupted the organic N mining nutrient economy of ECM trees by reducing fine root biomass and mycorrhizal colonization and altering root morphology to improve N foraging. In contrast, AM trees appeared to shift from mycorrhizal foraging toward root foraging by reducing mycorrhizal colonization while maintaining root biomass. While AM and ECM mycorrhizal colonization in the fertilized plots remained lower than the ambient plots during the year after fertilization ceased, the rapid recovery of roots in fertilized ECM soils back to a level similar to those of the control soils was mirrored by ECM rhizosphere and organic horizon enzyme recovery. The ECM bulk mineral and all of the AM soil enzymes activities remained at their N fertilized levels. Although these are short-term recovery responses, our results suggest that the recovery of enzyme activities in the majority of ECM soil fractions, but not the AM soils may destabilize stored soil C in ECM stands that decades of N deposition have enhanced.
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The data that support the findings of this study are openly available in the Environmental Data Initiative repository at https://portal.edirepository.org/nis/mapbrowse?scope=edi&identifier=912&revision=1 and https://portal.edirepository.org/nis/mapbrowse?scope=edi&identifier=913&revision=1.
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References
Allen CD, Macalady AK, Chenchouni H et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manage 259:660–684. https://doi.org/10.1016/j.foreco.2009.09.001
Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944. https://doi.org/10.1016/j.soilbio.2004.09.014
Allison SD, Wallenstein MD, Bradford MA (2010) Soil-carbon response to warming dependent on microbial physiology. Nat Geosci 3:336–340. https://doi.org/10.1038/ngeo846
Averill C, Turner BL, Finzi AC (2014) Mycorrhiza-mediated competition between plants and decomposers drives soil carbon storage. Nature 505:543–545. https://doi.org/10.1038/nature12901
Averill C, Dietze MC, Bhatnagar JM (2018) Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks. Glob Chang Biol 24:4544–4553. https://doi.org/10.1111/gcb.14368
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a pracrtical and powerful approach to multiple testing. J R Stat Soc Ser B 57(1):289–300. https://doi.org/10.2307/2346101
Boxman AW, van Dam D, van Dijk HFG et al (1995) Ecosystem responses to reduced nitrogen and sulphur inputs into two coniferous forest stands in the Netherlands. For Ecol Manage 71:7–29. https://doi.org/10.1016/0378-1127(94)06081-S
Boxman AW, Blanck K, Brandrud TE et al (1998) Vegetation and soil biota response to experimentally-changed nitrogen inputs in coniferous forest ecosystems of the NITREX project. For Ecol Manage 101:65–79. https://doi.org/10.1016/S0378-1127(97)00126-6
Brzostek ER, Blair JM, Dukes JS et al (2012) The effect of experimental warming and precipitation change on proteolytic enzyme activity: positive feedbacks to nitrogen availability are not universal. Glob Chang Biol 18:2617–2625. https://doi.org/10.1111/j.1365-2486.2012.02685.x
Brzostek ER, Greco A, Drake JE, Finzi AC (2013) Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils. Biogeochemistry 115:65–76. https://doi.org/10.1007/s10533-012-9818-9
Brzostek ER, Dragoni D, Brown ZA, Phillips RP (2015) Mycorrhizal type determines the magnitude and direction of root-induced changes in decomposition in a temperate forest. New Phytol 206:1274–1282. https://doi.org/10.1111/nph.13303
Bzdyk RM, Olchowik J, Studnicki M et al (2019) Ectomycorrhizal colonisation in declining oak stands on the Krotoszyn Plateau. Forests, Poland. https://doi.org/10.3390/f10010030
Carrara JE, Walter CA, Hawkins JS et al (2018) Interactions among plants, bacteria, and fungi reduce extracellular enzyme activities under long-term N fertilization. Glob Chang Biol 24:2721–2734. https://doi.org/10.1111/gcb.14081
Carrara JE, Walter CA, Freedman ZB et al (2021) Differences in microbial community response to nitrogen fertilization result in unique enzyme shifts between arbuscular and ectomycorrhizal dominated soils. Glob Chang Biol. https://doi.org/10.1111/gcb.15523
Chen W, Koide RT, Adams TS et al (2016) Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees. Proc Natl Acad Sci USA 113:8741–8746. https://doi.org/10.1073/pnas.1601006113
Chen W, Koide RT, Eissenstat DM (2018a) Nutrient foraging by mycorrhizas: From species functional traits to ecosystem processes. Funct Ecol 32:858–869. https://doi.org/10.1111/1365-2435.13041
Chen W, Koide RT, Eissenstat DM (2018b) Root morphology and mycorrhizal type strongly influence root production in nutrient hot spots of mixed forests. J Ecol 106:148–156. https://doi.org/10.1111/1365-2745.12800
Choat B, Jansen S, Brodribb TJ et al (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755. https://doi.org/10.1038/nature11688
Cleveland CC, Liptzin D (2007) C: N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85(3):235–252
Comas LH, Callahan HS, Midford PE (2014) Patterns in root traits of woody species hosting arbuscular and ectomycorrhizas: implications for the evolution of belowground strategies. Ecol Evol 4:2979–2990. https://doi.org/10.1002/ece3.1147
Contosta AR, Frey SD, Cooper AB (2011) Seasonal dynamics of soil respiration and N mineralization in chronically warmed and fertilized soils. Ecosphere 2:1–21. https://doi.org/10.1890/ES10-00133.1
Eastman BA, Adams MB, Brzostek ER et al (2021) Altered plant carbon partitioning enhanced forest ecosystem carbon storage after 25 years of nitrogen additions. New Phytol 230:1435–1448. https://doi.org/10.1111/nph.17256
Entwistle EM, Zak DR, Argiroff WA (2018) Anthropogenic N deposition increases soil C storage by reducing the relative abundance of lignolytic fungi. Ecol Monogr 88:225–244. https://doi.org/10.1002/ecm.1288
Fatemi FR, Fernandez IJ, Simon KS, Dail DB (2016) Nitrogen and phosphorus regulation of soil enzyme activities in acid forest soils. Soil Biol Biochem 98:171–179. https://doi.org/10.1016/j.soilbio.2016.02.017
Fellbaum CR, Gachomo EW, Beesetty Y et al (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 109:2666–2671. https://doi.org/10.1073/pnas.1118650109
Fernandez IJ, Rustad LE, Norton SA et al (2003) Experimental acidification causes soil base-cation depletion at the bear brook watershed in maine. Soil Sci Soc Am J 67:1909–1919. https://doi.org/10.2136/sssaj2003.1909
Fernandez IJ, Karem JE, Norton SA, Rustad LE (2007) Temperature, soil moisture, and streamflow at the Bear Brook Watershed in Maine (BBWM)
Finzi AC, Abramoff RZ, Spiller KS et al (2015) Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Glob Chang Biol 21:2082–2094. https://doi.org/10.1111/gcb.12816
Firestone MK, Killham K, McColl JG (1983) Fungal toxicity of mobilized soil aluminum and manganese. Appl Environ Microbiol 46:758–761. https://doi.org/10.1128/aem.46.3.758-761.1983
Freedman ZB, Romanowicz KJ, Upchurch RA, Zak DR (2015) Differential responses of total and active soil microbial communities to long-term experimental N deposition. Soil Biol Biochem 90:275–282. https://doi.org/10.1016/j.soilbio.2015.08.014
Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manage 196:159–171. https://doi.org/10.1016/j.foreco.2004.03.018
Frey SD, Ollinger S, Nadelhoffer K et al (2014) Chronic nitrogen additions suppress decomposition and sequester soil carbon in temperate forests. Biogeochemistry 121:305–316. https://doi.org/10.1007/s10533-014-0004-0
Galloway JN, Dentener FJ, Capone DG et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226. https://doi.org/10.1007/s10533-004-0370-0
Galloway JN, Townsend AR, Erisman JW et al (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892. https://doi.org/10.1126/science.1136674
Gilliam FS, Burns DA, Driscoll CT et al (2019) Decreased atmospheric nitrogen deposition in eastern North America: predicted responses of forest ecosystems. Environ Pollut 244:560–574. https://doi.org/10.1016/j.envpol.2018.09.135
Gilliam FS, Adams MB, Peterjohn WT (2020) Response of soil fertility to 25 years of experimental acidification in a temperate hardwood forest. J Environ Qual 49:961–972. https://doi.org/10.1002/jeq2.20113
Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Govindarajulu M, Pfeffer PE, Jin H et al (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823. https://doi.org/10.1038/nature03610
Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci USA 107:13754–13759. https://doi.org/10.1073/pnas.1005874107
Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299. https://doi.org/10.1038/35095041
Hurlbert SH (1984) Psuedoreplication and the design of ecological experiments. Ecol Monogr 54:187–211
Janssens IA et al (2010) Reduction of forest soil respiration in response to nitrogen deposition. Nat Geosci 3:315–322. https://doi.org/10.1038/ngeo844
Jefts S, Fernandez IJ, Rustad LE, Dail DB (2004) Decadal responses in soil N dynamics at the Bear Brook Watershed in Maine, USA. For Ecol Manage 189:189–205. https://doi.org/10.1016/j.foreco.2003.08.011
Lambers H, Raven JA, Shaver GR, Smith SE (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103. https://doi.org/10.1016/j.tree.2007.10.008
Lawrence GB, Hazlett PW, Fernandez IJ et al (2015) Declining acidic deposition begins reversal of forest–soil acidification in the Northeastern U.S. and Eastern Canada. Environ Sci Technol 49:13103–13111. https://doi.org/10.1021/acs.est.5b02904
Marschener H (1998) Role of root growth, arbuscular mycorrhiza, and root exudates for the efficiency in nutrient acquisition. Field Crop Res 56:203–207. https://doi.org/10.1016/S0378-4290(97)00131-7
McGonigle TP, Miller MH, Evans DG et al (1990) A new method which gives an objective measure of colonization of roots by vesicular–arbuscular mycorrhizal fungi. New Phytol 115:495–501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x
Meier IC, Pritchard SG, Brzostek ER et al (2015) The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO2. New Phytol 205:1164–1174. https://doi.org/10.1111/nph.13122
Midgley MG, Phillips RP (2014) Mycorrhizal associations of dominant trees influence nitrate leaching responses to N deposition. Biochemistry 117:241–253. https://doi.org/10.1007/s10533-013-9931-4
Midgley MG, Phillips RP (2016) Resource stoichiometry and the biogeochemical consequences of nitrogen deposition in a mixed deciduous forest. Ecology 97:3369–3377. https://doi.org/10.1002/ecy.1595
Morrison EW, Frey SD, Sadowsky JJ et al (2016) Chronic nitrogen additions fundamentally restructure the soil fungal community in a temperate forest. Fungal Ecol 23:48–57. https://doi.org/10.1016/j.funeco.2016.05.011
Norton S, Kahl J, Fernandez I et al (1999) The Bear Brook Watershed, Maine (BBWM), USA. Environ Monit Assess 55:7–51. https://doi.org/10.1023/A:1006115011381
Ostonen I, Rosenvald K, Helmisaari HS et al (2013) Morphological plasticity of ectomycorrhizal short roots in Betula sp and Picea abies forests across climate and forest succession gradients: Its role in changing environments. Front Plant Sci 4:1–10. https://doi.org/10.3389/fpls.2013.00335
Patel KF, Fernandez IJ, Nelson SJ et al (2019) Forest N dynamics after 25 years of whole watershed n enrichment: the Bear Brook Watershed in Maine. Soil Sci Soc Am J. https://doi.org/10.2136/sssaj2018.09.0348
Persson H, Ahlström K, Clemensson-Lindell A (1998) Fine-root response to nitrogen addition and removal at Gårdsjön—results from ingrowth cores. Root Demogr Their Effic Sustain Agric Grasslands for Ecosyst. https://doi.org/10.1007/978-94-011-5270-9_35
Phillips RP, Fahey TJ (2005) Patterns of rhizosphere carbon flux in sugar maple (Acer saccharum) and yellow birch (Betula allegheniensis) saplings. Glob Chang Biol 11:983–995. https://doi.org/10.1111/j.1365-2486.2005.00959.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. https://doi.org/10.1111/nph.12221
Pregitzer KS, Burton AJ, Zak DR, Talhelm AF (2008) Simulated chronic nitrogen deposition increases carbon storage in Northern Temperate forests. Glob Chang Biol 14:142–153. https://doi.org/10.1111/j.1365-2486.2007.01465.x
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492
Rennenberg H, Loreto F, Polle A et al (2006) Physiological responses of forest trees to heat and drought. Plant Biol 8:556–571. https://doi.org/10.1055/s-2006-924084
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. https://doi.org/10.1016/S0038-0717(02)00074-3
Sanclements MD, Fernandez IJ, Norton SA (2010) Soil chemical and physical properties at the Bear Brook Watershed in Maine, USA. Environ Monit Assess 171:111–128. https://doi.org/10.1007/s10661-010-1531-3
Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563. https://doi.org/10.1016/S0038-0717(03)00015-4
Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24. https://doi.org/10.1023/A:1016541114786
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250. https://doi.org/10.1146/annurev-arplant-042110-103846
Strengbom J, Nordin A, Näsholm T, Ericson L (2001) Slow recovery of boreal forest ecosystem following decreased nitrogen input. Funct Ecol 15:451–457. https://doi.org/10.1046/j.0269-8463.2001.00538.x
Terrer C, Vicca S, Hungate BA et al (2016) Mycorrhizal association as a primary control of the CO2 fertilization effect. Science 353:72–74. https://doi.org/10.1126/science.aaf4610
Terrer C, Phillips RP, Hungate BA et al (2021) A trade-off between plant and soil carbon storage under elevated CO2. Nature 591:599–603. https://doi.org/10.1038/s41586-021-03306-8
Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355. https://doi.org/10.1111/j.1469-8137.2004.01159.x
Waldrop MP, Zak DR, Sinsabaugh RL et al (2004) Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol Appl 14:1172–1177
Wallenstein MD, McNulty S, Fernandez IJ et al (2006) Nitrogen fertilization decreases forest soil fungal and bacterial biomass in three long-term experiments. For Ecol Manage 222:459–468. https://doi.org/10.1016/j.foreco.2005.11.002
Wang Z, Fernandez I (1999) Soil type and forest vegetation influences on forest floor nitrogen dynamics at the Bear Brook Watershed in Maine (BBWM). Environ Monit Assess 55:221–234. https://doi.org/10.1023/A:1006134120951
Yin H, Wheeler E, Phillips RP (2014) Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biol Biochem 78:213–221. https://doi.org/10.1016/j.soilbio.2014.07.022
Zak DR, Argiroff WA, Freedman ZB et al (2019) Anthropogenic N deposition, fungal gene expression, and an increasing soil carbon sink in the Northern Hemisphere. Ecology 100:1–8. https://doi.org/10.1002/ecy.2804
Acknowledgements
We thank Christopher A. Walter, Jason T. Rothman, Farrah Fatemi, Nanette Raczka, Lacy Smith, Jessica Reis, Rachel McCoy, Nathan Williams, Nathan Sheldon, Francesca Basil, Jacob Carrara, and Jennifer Mangano for assistance in the field and in the lab. This work was supported by the National Science Foundation Graduate Research Fellowship to Joseph Carrara under Grant No. DGE-1102689 and by the Long-Term Research in Environmental Biology (LTREB) program at the National Science Foundation under Grant No. DEB-1119709 to Ivan Fernandez.
Funding
This work was supported by the National Science Foundation Graduate Research Fellowship to Joseph Carrara under Grant No. DGE-1102689 and by the Long-Term Research in Environmental Biology (LTREB) program at the National Science Foundation under Grant No. DEB-1119709 to Ivan Fernandez.
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Carrara, J.E., Fernandez, I.J. & Brzostek, E.R. Mycorrhizal type determines root–microbial responses to nitrogen fertilization and recovery. Biogeochemistry 157, 245–258 (2022). https://doi.org/10.1007/s10533-021-00871-y
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DOI: https://doi.org/10.1007/s10533-021-00871-y