Biological nitrogen fixation is a fundamental part of ecosystem functioning. Anthropogenic nitrogen deposition and climate change may, however, limit the competitive advantage of nitrogen-fixing plants, leading to reduced relative diversity of nitrogen-fixing plants. Yet, assessments of changes of nitrogen-fixing plant long-term community diversity are rare. Here, we examine temporal trends in the diversity of nitrogen-fixing plants and their relationships with anthropogenic nitrogen deposition while accounting for changes in temperature and aridity. We used forest-floor vegetation resurveys of temperate forests in Europe and the United States spanning multiple decades. Nitrogen-fixer richness declined as nitrogen deposition increased over time but did not respond to changes in climate. Phylogenetic diversity also declined, as distinct lineages of N-fixers were lost between surveys, but the "winners" and "losers" among nitrogen-fixing lineages varied among study sites, suggesting that losses are context dependent. Anthropogenic nitrogen deposition reduces nitrogen-fixing plant diversity in ways that may strongly affect natural nitrogen fixation.

Białowieża Geobotanical Station Faculty of Biology University of Warsaw Sportowa 19 PL 17 230 Warsaw Poland

Center for Computation and Technology Louisiana State University Baton Rouge LA 70803 USA

CIRAD UMR PVBMT 97410 Saint Pierre La Réunion France

Czech University of Life Sciences Prague Kamýcká 129 CZ 16500 Praha Suchdol Czech Republic

Department of Biological Sciences Louisiana State University Baton Rouge LA 70803 USA

Department of Biological Sciences Mississippi State University Mississippi State MS 39762 USA

Department of Biological Sciences University of Bergen Postbox 7803 5020 Bergen Norway

Department of Botany Faculty of Science Palacký University in Olomouc Šlechtitelů 27 CZ 779 00 Olomouc Czech Republic

Department of Botany University of Wisconsin Madison Madison WI 53706 USA

Department of Earth and Environmental Sciences University of West Florida Pensacola FL 32514 USA

Department of Ecology and Evolutionary Biology University of Arizona Tucson AZ 85720 USA

Department of Silviculture and Forest Ecology of the Temperate Zones University of Göttingen Büsgenweg 1 D 37077 Göttingen Germany

ELTE Eötvös Loránd University Department of Plant Systematics Ecology and Theoretical Biology Institute of Biology Pázmány P sétány 1 c H 1117 Budapest Hungary

Faculty of Forestry and Wood Sciences Czech University of Life Sciences Prague Kamýcká 129 CZ 165 21 Praha 6 Suchdol Czech Republic

Faculty of Forestry University of Sopron Bajcsy Zs str 4 H 9400 Sopron Hungary

Florida Museum of Natural History University of Florida Gainesville FL 32611 USA

Forest and Nature Lab Department of Environment Faculty of Bioscience Engineering Ghent University B 9000 Melle Gontrode Belgium

General Botany Institute of Biochemistry and Biology University of Potsdam Maulbeerallee 3 D 14469 Potsdam Germany

German Centre for Integrative Biodiversity Research Halle Jena Leipzig Puschstrasse 4 04103 Leipzig Germany

Independent Researcher PL 50 524 Wrocław Poland

Institute of Biology Biotechnology and Environmental Protection Faculty of Natural Sciences University of Silesia PL 40 032 Katowice Poland

Institute of Botany Czech Academy of Sciences Lidická 25 27 60200 Brno Czech Republic

Institute of Botany Faculty of Biology Jagiellonian University in Kraków Gronostajowa 3 PL 30 387 Kraków Poland

Institute of Botany of the Czech Academy of Sciences Zámek 1 CZ 252 43 Průhonice Czech Republic

Institute of Ecology and Evolution Friedrich Schiller University Jena Dornburger Str 159 D 07743 Jena Germany

Leibniz Centre for Agricultural Landscape Research Eberswalder Strasse 84 D 15374 Muencheberg Germany

MTA DE Lendület Functional and Restoration Ecology Research Group H 4032 Debrecen Hungary

Museum of Natural History Faculty of Biological Sciences University of Wrocław Sienkiewicza 21 PL 50 335 Wrocław Poland

Norwegian Institute of Bioeconomy Research Thormøhlensgate 55 5006 Bergen Norway

Research Institute for Nature and Forest Havenlaan 88 bus 73 B 1000 Brussel Belgium

Southern Swedish Forest Research Centre Swedish University of Agricultural Sciences Box 190 23422 Lomma Sweden

Technical University in Zvolen T G Masaryka 24 SK 96001 Zvolen Slovakia

UMR CNRS 7058 Ecologie et Dynamique des Systèmes Anthropisés Université de Picardie Jules Verne 1 rue des Louvels 80000 Amiens France

Zobrazit více v PubMed

Elser J. J., Bracken M. E., Cleland E. E., Gruner D. S., Harpole W. S., Hillebrand H., Ngai J. T., Seabloom E. W., Shurin J. B., Smith J. E., Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 10, 1135–1142 (2007). PubMed

Treseder K. K., Nitrogen additions and microbial biomass: A meta-analysis of ecosystem studies. Ecol. Lett. 11, 1111–1120 (2008). PubMed

Du E., Terrer C., Pellegrini A. F., Ahlström A., van Lissa C. J., Zhao X., Xia N., Wu X., Jackson R. B., Global patterns of terrestrial nitrogen and phosphorus limitation. Nat. Geosci. 13, 221–226 (2020).

J. I. Sprent, P. Sprent, Nitrogen Fixing Organisms: Pure and Applied Aspects (Springer, 1990).

Sprent J. I., Ardley J., James E. K., Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytol. 215, 40–56 (2017). PubMed

Roy S., Khasa D. P., Greer C. W., Combining alders, frankiae, and mycorrhizae for the revegetation and remediation of contaminated ecosystems. Can. J. Bot. 85, 237–251 (2007).

Zobel M., Davison J., Edwards M. E., Brochmann C., Coissac E., Taberlet P., Willerslev E., Moora M., Ancient environmental DNA reveals shifts in dominant mutualisms during the late Quaternary. Nat. Commun. 9, 139 (2018). PubMed PMC

Suding K. N., Collins S. L., Gough L., Clark C., Cleland E. E., Gross K. L., Milchunas D. G., Pennings S., Functional-and abundance-based mechanisms explain diversity loss due to N fertilization. Proc. Natl. Acad. Sci. U.S.A. 102, 4387–4392 (2005). PubMed PMC

Bassin S., Volk M., Fuhrer J., Species composition of subalpine grassland is sensitive to nitrogen deposition, but not to ozone, after seven years of treatment. Ecosystems 16, 1105–1117 (2013).

Pellegrini A. F., Staver A. C., Hedin L. O., Charles-Dominique T., Tourgee A., Aridity, not fire, favors nitrogen-fixing plants across tropical savanna and forest biomes. Ecology 97, 2177–2183 (2016). PubMed

Liao W., Menge D. N., Lichstein J. W., Ángeles-Pérez G., Global climate change will increase the abundance of symbiotic nitrogen-fixing trees in much of North America. Glob. Chang. Biol. 23, 4777–4787 (2017). PubMed

Doby J. R., Li D., Folk R. A., Siniscalchi C. M., Guralnick R. P., Aridity drives phylogenetic diversity and species richness patterns of nitrogen-fixing plants in North America. Glob. Ecol. Biogeogr. 31, 1630–1642 (2022).

Tian H., Yang J., Lu C., Xu R., Canadell J. G., Jackson R. B., Arneth A., Chang J., Chen G., Ciais P., The global N2O model intercomparison project. Bull. Am. Meteorol. Soc. 99, 1231–1251 (2018).

Ullah S., You Q., Sachindra D. A., Nowosad M., Ullah W., Bhatti A. S., Jin Z., Ali A., Spatiotemporal changes in global aridity in terms of multiple aridity indices: An assessment based on the CRU data. Atmos. Res. 268, 105998 (2022).

K. Calvin, D. Dasgupta, G. Krinner, A. Mukherji, P. W. Thorne, C. Trisos, J. Romero, P. Aldunce, K. Barrett, G. Blanco, W. W. L. Cheung, S. Connors, F. Denton, A. Diongue-Niang, D. Dodman, M. Garschagen, O. Geden, B. Hayward, C. Jones, F. Jotzo, T. Krug, R. Lasco, Y.-Y. Lee, V. Masson-Delmotte, M. Meinshausen, K. Mintenbeck, A. Mokssit, F. E. L. Otto, M. Pathak, A. Pirani, E. Poloczanska, H.-O. Pörtner, A. Revi, D. C. Roberts, J. Roy, A. C. Ruane, J. Skea, P. R. Shukla, R. Slade, A. Slangen, Y. Sokona, A. A. Sörensson, M. Tignor, D. Van Vuuren, Y.-M. Wei, H. Winkler, P. Zhai, Z. Zommers, J.-C. Hourcade, F. X. Johnson, S. Pachauri, N. P. Simpson, C. Singh, A. Thomas, E. Totin, P. Arias, M. Bustamante, I. Elgizouli, G. Flato, M. Howden, C. Méndez-Vallejo, J. J. Pereira, R. Pichs-Madruga, S. K. Rose, Y. Saheb, R. Sánchez Rodríguez, D. Ürge-Vorsatz, C. Xiao, N. Yassaa, A. Alegría, K. Armour, B. Bednar-Friedl, K. Blok, G. Cissé, F. Dentener, S. Eriksen, E. Fischer, G. Garner, C. Guivarch, M. Haasnoot, G. Hansen, M. Hauser, E. Hawkins, T. Hermans, R. Kopp, N. Leprince-Ringuet, J. Lewis, D. Ley, C. Ludden, L. Niamir, Z. Nicholls, S. Some, S. Szopa, B. Trewin, K.-I. Van Der Wijst, G. Winter, M. Witting, A. Birt, M. Ha, J. Romero, J. Kim, E. F. Haites, Y. Jung, R. Stavins, A. Birt, M. Ha, D. J. A. Orendain, L. Ignon, S. Park, Y. Park, A. Reisinger, D. Cammaramo, A. Fischlin, J. S. Fuglestvedt, G. Hansen, C. Ludden, V. Masson-Delmotte, J. B. R. Matthews, K. Mintenbeck, A. Pirani, E. Poloczanska, N. Leprince-Ringuet, C. Péan, “Climate change 2023: Synthesis report” in Contribution of Working Groups I, II and III to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change, H. Lee, J. Romero, Eds. (IPCC, 2023), pp. 1–34.

Ardley J., Sprent J., Evolution and biogeography of actinorhizal plants and legumes: A comparison. J. Ecol. 109, 1098–1121 (2021).

Guinet M., Nicolardot B., Revellin C., Durey V., Carlsson G., Voisin A.-S., Comparative effect of inorganic N on plant growth and N2 fixation of ten legume crops: Towards a better understanding of the differential response among species. Plant Soil 432, 207–227 (2018).

Alon M., Dovrat G., Masci T., Sheffer E., Soil nitrogen regulates symbiotic nitrogen fixation in a legume shrub but does not accumulate under it. Ecosphere 12, e03843 (2021).

Menge D. N., Wolf A. A., Funk J. L., Perakis S. S., Akana P. R., Arkebauer R., Bytnerowicz T. A., Carreras Pereira K., Huddell A. M., Kou-Giesbrecht S., Tree symbioses sustain nitrogen fixation despite excess nitrogen supply. Ecological monographs 93, e1562 (2023).

Midolo G., Alkemade R., Schipper A. M., Benítez-López A., Perring M. P., De Vries W., Impacts of nitrogen addition on plant species richness and abundance: A global meta-analysis. Glob. Ecol. Biogeogr. 28, 398–413 (2019).

Bordeleau L., Prévost D., Nodulation and nitrogen fixation in extreme environments. Plant Soil 161, 115–125 (1994).

Houlton B. Z., Wang Y.-P., Vitousek P. M., Field C. B., A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454, 327–330 (2008). PubMed

Bytnerowicz T. A., Akana P. R., Griffin K. L., Menge D. N., Temperature sensitivity of woody nitrogen fixation across species and growing temperatures. Nat. Plants 8, 209–216 (2022). PubMed

Adams M. A., Turnbull T. L., Sprent J. I., Buchmann N., Legumes are different: Leaf nitrogen, photosynthesis, and water use efficiency. Proc. Natl. Acad. Sci. U.S.A. 113, 4098–4103 (2016). PubMed PMC

Verheyen K., De Frenne P., Baeten L., Waller D. M., Hédl R., Perring M. P., Blondeel H., Brunet J., Chudomelová M., Decocq G., De Lombaerde E., Depauw L., Dirnböck T., Durak T., Eriksson O., Gilliam F., Heinken T., Heinrichs S., Hermy M., Jaroszewicz B., Jenkins M., Johnson S., Kirby K., Kopecký M., Landuyt D., Lenoir J., Li D., Macek M., Maes S., Máliš F., Mitchell F. J. G., Naaf T., Peterken G., Petřík P., Reczyńska K., Rogers D. A., Schei F. H., Schmidt W., Standovár T., Świerkosz K., Ujházy K., Van Calster H., Vellend M., Vild O., Woods K., Wulf M., Bernhardt-Römermann M., Combining biodiversity resurveys across regions to advance global change research. Bioscience 67, 73–83 (2017). PubMed PMC

Govaert S., Vangansbeke P., Blondeel H., Steppe K., Verheyen K., De Frenne P., Rapid thermophilization of understorey plant communities in a 9 year-long temperate forest experiment. J. Ecol. 109, 2434–2447 (2021).

Richard B., Dupouey J., Corcket E., Alard D., Archaux F., Aubert M., Boulanger V., Gillet F., Langlois E., Macé S., Montpied P., Beaufils T., Begeot C., Behr P., Boissier J., Camaret S., Chevalier R., Decocq G., Dumas Y., Eynard-Machet R., Gégout J., Huet S., Malécot V., Margerie P., Mouly A., Paul T., Renaux B., Ruffaldi P., Spicher F., Thirion E., Ulrich E., Nicolas M., Lenoir J., The climatic debt is growing in the understorey of temperate forests: Stand characteristics matter. Glob. Ecol. Biogeogr. 30, 1474–1487 (2021).

Padullés Cubino J., Lenoir J., Li D., Montaño-Centellas F. A., Retana J., Baeten L., Bernhardt-Römermann M., Chudomelová M., Closset D., Decocq G., De Frenne P., Diekmann M., Dirnböck T., Durak T., Hédl R., Heinken T., Jaroszewicz B., Kopecký M., Macek M., Máliš F., Naaf T., Orczewska A., Petřík P., Pielech R., Reczyńska K., Schmidt W., Standovár T., Świerkosz K., Teleki B., Verheyen K., Vild O., Waller D., Wulf M., Chytrý M., Evaluating plant lineage losses and gains in temperate forest understories: A phylogenetic perspective on climate change and nitrogen deposition. New Phytol. 241, 2287–2299 (2024). PubMed

Heath K. D., Stock A., Stinchcombe J., Mutualism variation in the nodulation response to nitrate. J. Evol. Biol. 23, 2494–2500 (2010). PubMed

Peng J., Ma F., Quan Q., Chen X., Wang J., Yan Y., Zhou Q., Niu S., Nitrogen enrichment alters climate sensitivity of biodiversity and productivity differentially and reverses the relationship between them in an alpine meadow. Sci. Total Environ. 835, 155418 (2022). PubMed

Musil C., Kgope B., Chimphango S., Dakora F., Nitrate additions enhance the photosynthetic sensitivity of a nodulated South African Mediterranean-climate legume (Podalyria calyptrata) to elevated UV-B. Environ. Exp. Bot. 50, 197–210 (2003).

Lilleskov E. A., Kuyper T. W., Bidartondo M. I., Hobbie E. A., Atmospheric nitrogen deposition impacts on the structure and function of forest mycorrhizal communities: A review. Environ. Pollut. 246, 148–162 (2019). PubMed

Zhao Y., Yang B., Li M., Xiao R., Rao K., Wang J., Zhang T., Guo J., Community composition, structure and productivity in response to nitrogen and phosphorus additions in a temperate meadow. Sci. Total Environ. 654, 863–871 (2019). PubMed

Afkhami M. E., Mahler D. L., Burns J. H., Weber M. G., Wojciechowski M. F., Sprent J., Strauss S. Y., Symbioses with nitrogen-fixing bacteria: Nodulation and phylogenetic data across legume genera. Ecology 99, 502 (2018). PubMed

Kates H. R., O’Meara B. C., LaFrance R., Stull G. W., James E. K., Liu S.-Y., Tian Q., Yi T.-S., Conde D., Kirst M., Shifts in evolutionary lability underlie independent gains and losses of root-nodule symbiosis in a single clade of plants. Nat. Commun. 15, 4262 (2024). PubMed PMC

Segar J., Pereira H. M., Baeten L., Bernhardt-Römermann M., De Frenne P., Fernández N., Gilliam F. S., Lenoir J., Ortmann-Ajkai A., Verheyen K., Waller D., Teleki B., Brunet J., Chudomelová M., Decocq G., Dirnböck T., Hédl R., Heinken T., Jaroszewicz B., Kopecký M., Macek M., Máliš F., Naaf T., Orczewska A., Reczynska K., Schmidt W., Šebesta J., Stachurska-Swakoń A., Standovár T., Swierkosz K., Vild O., Wulf M., Staude I. R., Divergent roles of herbivory in eutrophying forests. Nat. Commun. 13, 7837 (2022). PubMed PMC

Doxa A., Paracchini M. L., Pointereau P., Devictor V., Jiguet F., Preventing biotic homogenization of farmland bird communities: The role of High Nature Value farmland. Agric. Ecosyst. Environ. 148, 83–88 (2012).

Smith S. A., Brown J. W., Constructing a broadly inclusive seed plant phylogeny. Am. J. Bot. 105, 302–314 (2018). PubMed

Li D., rtrees: An R package to assemble phylogenetic trees from megatrees. Ecography 2023, e06643 (2023).

Li D., Trotta L., Marx H. E., Allen J. M., Sun M., Soltis D. E., Soltis P. S., Guralnick R. P., Baiser B., For common community phylogenetic analyses, go ahead and use synthesis phylogenies. Ecology 100, e02788 (2019). PubMed PMC

Faith D. P., Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10 (1992).

Webb C. O., Ackerly D. D., McPeek M. A., Donoghue M. J., Phylogenies and community ecology. Annu. Rev. Ecol. Evol. Syst. 33, 475–505 (2002).

Paradis E., Claude J., Strimmer K., APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20, 289–290 (2004). PubMed

Tsirogiannis C., Sandel B., PhyloMeasures: A package for computing phylogenetic biodiversity measures and their statistical moments. Ecography 39, 709–714 (2016).

Harris I., Osborn T. J., Jones P., Lister D., Version 4 of the CRU TS monthly high-resolution gridded multivariate climate dataset. Sci. Data 7, 109 (2020). PubMed PMC

R. J. Hijmans, R. Bivand, K. Forner, J. Ooms, E. Pebesma, M. D. Sumner, terra: Spatial Data Analysis, R package, CRAN (2022).

UNEP, World Atlas of Desertification (UNEP, 1992).

J. Pinheiro, D. Bates, S. DebRoy, D. Sarkar, S. Heisterkamp, B. Van Willigen, nlme: Linear and Nonlinear Mixed Effects Models, R package version 3.1.157, CRAN (2017).

Mazalla L., Diekmann M., Regression to the mean in vegetation science. J. Veg. Sci. 33, e13117 (2022).

J. Fox, S. Weisberg, D. Adler, D. M. Bates, G. Baud-bovy, S. Ellison, D. Firth, M. Friendly, G. Gorjanc, S. Graves, R. Heiberger, R. Laboissiere, G. Monette, D. Murdoch, D. Ogle, B. Ripley, W. Venables, car: Companion to Applied Regression, R package version 3.1.1, CRAN (2016).

Zellweger F., Baltensweiler A., Ginzler C., Roth T., Braunisch V., Bugmann H., Bollmann K., Environmental predictors of species richness in forest landscapes: Abiotic factors versus vegetation structure. J. Biogeogr. 43, 1080–1090 (2016).

Pagel M., Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999). PubMed

Revell L. J., phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).