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Ecological consequences of the expansion of N2-fixing plants in cold biomes

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Abstract

Research in warm-climate biomes has shown that invasion by symbiotic dinitrogen (N2)-fixing plants can transform ecosystems in ways analogous to the transformations observed as a consequence of anthropogenic, atmospheric nitrogen (N) deposition: declines in biodiversity, soil acidification, and alterations to carbon and nutrient cycling, including increased N losses through nitrate leaching and emissions of the powerful greenhouse gas nitrous oxide (N2O). Here, we used literature review and case study approaches to assess the evidence for similar transformations in cold-climate ecosystems of the boreal, subarctic and upper montane-temperate life zones. Our assessment focuses on the plant genera Lupinus and Alnus, which have become invasive largely as a consequence of deliberate introductions and/or reduced land management. These cold biomes are commonly located in remote areas with low anthropogenic N inputs, and the environmental impacts of N2-fixer invasion appear to be as severe as those from anthropogenic N deposition in highly N polluted areas. Hence, inputs of N from N2 fixation can affect ecosystems as dramatically or even more strongly than N inputs from atmospheric deposition, and biomes in cold climates represent no exception with regard to the risk of being invaded by N2-fixing species. In particular, the cold biomes studied here show both a strong potential to be transformed by N2-fixing plants and a rapid subsequent saturation in the ecosystem’s capacity to retain N. Therefore, analogous to increases in N deposition, N2-fixing plant invasions must be deemed significant threats to biodiversity and to environmental quality.

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References

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

    Google Scholar 

  • Anthelme F, Grossi JL, Brun JJ, Didier L (2001) Consequences of green alder expansion on vegetation changes and arthropod communities removal in the northern French Alps. For Ecol Manage 145:57–65

    Google Scholar 

  • Anthelme F, Villaret J, Brun J (2007) Shrub encroachment in the Alps gives rise to the convergence of sub-alpine communities on a regional scale. J Veg Sci 18:355–362

    Google Scholar 

  • Aradóttir ÁL and Halldórsson G (eds.) (2011) Vistheimt á Íslandi [Restoration in Iceland]. Agricult Univ. Iceland and the Icelandic Soil Conserv Ser, p 172

  • Arnalds Ó, Gudbergsson G, Gudmundsson J (2000) Carbon sequestration and reclamation of severely degraded soils in Iceland. Icelandic Agric Sci 13:87–97

    Google Scholar 

  • BAFU/BFS (2011) Umwelt Schweiz 2011, (Hrsg.) Bundesamt für Umwelt BAFU Bern und Bundesamt für Statistik BFS Neuchâtel, p 101

  • Belnap J, Lange O (2003) Biological soil crusts: structure, function, and management. Springer, Berlin

    Google Scholar 

  • Benecke U (1970) Nitrogen fixation by Alnus viridis (Chaix) DC. Plant Soil 33:30–48

    Google Scholar 

  • Benson DR, Brooks JM, Huang Y, Bickhart DM, Mastronunzio JE (2011) The biology of Frankia sp. strains in the post-genome era. Mol Plant Microbe Interact 24:1310–1316

    CAS  PubMed  Google Scholar 

  • Binkley D (2003) Seven decades of stand development in mixed and pure stands of conifers and nitrogen-fixing red alder. Can J For Res 33:2274–2279

    Google Scholar 

  • Binkley D, Greene S (1983) Production in mixtures of conifers and red alder: the importance of site fertility and stand age. IUFRO symposium, forest site and continuous productivity. U.S. Dept. of Agriculture, Forest Service, General technical report PNW-163, pp 112–117

  • Binkley D, Sollins P, Bell R, Sachs D, Myrold D (1992) Biogeochemistry of adjacent conifer and alder-conifer stands. Ecology 73:2022–2033

    CAS  Google Scholar 

  • Binkley D, Cromack K Jr, Baker DD (1994) Nitrogen fixation by red alder: biology, rates and controls. In: Hibbs DE, DeBell DS, Tarrant RF (eds) The biology and management of red alder. Oregon State University Press, Corvallis, pp 57–72

    Google Scholar 

  • Bischof N (1984) Pflanzensoziologische Untersuchungen von Sukzessionen aus gemähten Magerrasen in der subalpinen Stufe der Zentralalpen. Beitr. Gebot. Landesaufahme der Schweiz, Heft 60, p 128

  • Björnsson H (2007) Fertilization of Nootka lupin (Lupinus nootkatensis) for biomass production and carbon sequestration. Icelandic Agric Sci 20:81–92

    Google Scholar 

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

    CAS  Google Scholar 

  • Bormann BT, Cromack K Jr, Russell WO III (1994) The influences of red alder on soils and long-term ecosystem productivity. In: Hibbs DE, DeBell DS, Tarrant RF (eds) The biology and management of red alder. Oregon State University Press, Corvallis, pp 47–56

    Google Scholar 

  • Brändli UB (ed) (2010) Schweizerisches Landesforstinventar. Ergebnisse der dritten Erhebung 2004–2006. Birmensdorf, Eidgenössische Forschungsanstalt für Wald, Schnee und Landschaft WSL. Bern, Bundesamt für Umwelt, BAFU, p 312

  • Brookshire ENJ, Valett HM, Thomas SA, Webster JR (2007) Atmospheric N deposition increases organic N loss from temperate forests. Ecosystems 10:252–262

    CAS  Google Scholar 

  • Bühlmann T, Hiltbrunner E, Körner C(2013) Die Verbuschung des Alpenraums durch die Grünerle. FactSheet Swiss Academies of Arts and Sciences (Bern), p 4

  • Butterbach-Bahl K, Gundersen P (2011) Nitrogen processes in terrestrial ecosystems. In: Sutton MA et al (eds) The European nitrogen assessment: sources effects, and policy perspectives. Cambridge University Press, Cambridge, pp 99–125

    Google Scholar 

  • Caprez R (2012) Ecosystem carbon balance of temperate forests differing in elevation and nitrogen elevation. PhD Thesis, University of Basel, p 61

  • Caviezel C, Hunziker M, Schaffner M, Kuhn NJ (2014) Soil-vegetation interaction on slopes with bush encroachment in the central Alps—adapting slope stability measurements to shifting process domains. Earth Surf Process Landf 39:509–521

    Google Scholar 

  • Chaia EE, Myrold DD (2010) Variation of 15N natural abundance in leaves and nodules of actinorhizal shrubs in Northwest Patagonia. Symbiosis 50:97–105

    CAS  Google Scholar 

  • Chapin FS III (2002) Principles of terrestrial ecosystem ecology. Springer, New York

    Google Scholar 

  • Cleveland CC, Townsen AR, Schimel DS, Fisher H, Howarth RW, Hedin OL, Perakis SS, Latty EF, Von Fischer JC, Elseroad AE, Wasson MF (1999) Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global Biochem Cy 13:623–645

    CAS  Google Scholar 

  • Colautti RI, MacIsaac HI (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10:135–141

    Google Scholar 

  • Cole DW, Compton JE, Edmonds RL, Homann PS, Van Miegroet J (1995) Comparison of carbon accumulation in Douglas fir and red alder forests. In: McFee WW, Kelly JM (eds) Carbon forms and functions in forest soils. Soil Sci Soc Am, Madison, pp 527–546

    Google Scholar 

  • Compton JE, Church MR, Larned ST, Hogsett WE (2003) Nitrogen export from forested watersheds in the Oregon coast range: the role of N2-fixing red alder. Ecosystems 6:773–785

    CAS  Google Scholar 

  • Cools N, Vesterdal L, De Vos B, Vanguelova E, Hansen K (2014) Tree species is the major factor explaining C: N ratios in European forests. For Eco Manage 311:3–16

    Google Scholar 

  • Crews TE, Kurina LM, Vitousek PM (2001) Organic matter and nitrogen accumulation and nitrogen fixation during early ecosystem development in Hawaii. Biogeochemistry 52:259–279

    CAS  Google Scholar 

  • Cromack K Jr, Miller RE, Helgerson O, Smith RB, Anderson HW (1999) Soil Carbon and nutrients in a coastal Oregon Douglas-fir plantation with red alder. Soil Sci Soc Am J 63:232–239

    CAS  Google Scholar 

  • David F (2010) Expansion of green alder (Alnus alnobetula Ehrh K. Koch) in the northern French Alps: a palaeoecological point of view. C R Biol 333:424–428

    PubMed  Google Scholar 

  • Davidsdottir B (2013) The effect of vegetation reclamation on birds and invertebrates. A comparative study of barren land, restored heathland and land revegetated by Nootka lupin. M.Sc. thesis, Agricultural University of Iceland, p 39

  • De Vries W, Solberg S, Dobbertin M, Sterba H, Laubhann D, Reinds GJ, Nabuurs GJ, Gundersen P, Sutton MA (2008) Ecologically implausible carbon response? Nature 451:E1–E3

    PubMed  Google Scholar 

  • De Vries W, Solberg S, Dobbertin M, Sterba H, Laubhann D, van Oijen M, Evans C, Gundersen P, Kros J, Wamelink GWW, Reinds GJ, Sutton MA (2009) The impact of nitrogen deposition on carbon sequestration by European forests and heathlands. For Ecol Manage 258:1814–1823

    Google Scholar 

  • DeLuca TH, Zackrisson O, Nilsson M-C, Sellstedt A (2002) Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419:917–920

    CAS  PubMed  Google Scholar 

  • Eriksson Hägg H, Humborg C, Swaney DP, Mörth C-M (2012) Riverine nitrogen export in Swedish catchments dominated by atmospheric inputs. Biogeochemistry 111:203–217

    Google Scholar 

  • Fremstad E (2010) NOBANIS–Invasive alien species fact sheet—Lupinus polyphyllus–From: Online Database of the European Network on Invasive Alien Species–NOBANIS www.nobanis.org. Accessed 15 Nov 2012

  • Frost GV, Epstein HE (2014) Tall shrub and tree expansion in Siberian tundra ecotones since the 1960s. Glob Change Biol 20:1264–1277

    Google Scholar 

  • Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland C, Green P, Holland E, Karl DM, Michaels AF, Porter JH, Townsend A, Vörösmarty C (2004) Nitrogen cycles: past, present and future. Biogeochemistry 70:153–226

    CAS  Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions and potential solutions. Science 320:889–892

    CAS  PubMed  Google Scholar 

  • Gerzabek MH, Haberhauer G, Stemmer M, Klepsch S, Haunold E (2004) Long-term behaviour of 15N in an alpine grassland ecosystem. Biogeochemistry 70:59–69

    CAS  Google Scholar 

  • Gigon A, Weber E (2005) Invasive Neophyten in der Schweiz: Lagebericht und Handlungsbedarf. Geobotanisches Institut, ETH Zentrum, 8092 Zürich Bericht Zu Handen des Bundesamtes für Umwelt, Wald und Landschaft in Bern, p 40

  • Gíslason SR, Arnórsson S, Ármannsson H (1996) Chemical weathering of basalt in southwest Iceland: effects of runoff, age of rocks and vegetative/glacial cover. Am J Sci 296:837–907

    Google Scholar 

  • Goulson D, Rotheray EL (2012) Population dynamics of the invasive weed Lupinus arboreus in Tasmania, and interactions with two non-native pollinators. Weed Res 52:535–541

    Google Scholar 

  • Gunnarsson TG, Indridadottir GH (2009) Effects of sandplain revegetation on avian abundance and diversity at Skogasandur and Myrdalssandur, South-Iceland. Conserv Evid 6:98–104

    Google Scholar 

  • Gutschick VP (1978) Energy and nitrogen fixation. Bioscience 28:571–575

  • Hart SC, Binkley D, Perry DA (1997) Influence of red alder on soil nitrogen transformations in two conifer forests of contrasting productivity. Soil Biol Biochem 29:1111–1123

    CAS  Google Scholar 

  • Harvey IC, Seyb AM, Warren AJF, van den Ende H (1996) The biological control of Russel lupin in riverbeds with endemic plant pathogens. In: Proc 49th NZ Plant Protection Conf 1996, pp 119–125

  • Herbst M, Eschenbach C, Kappen L (1999) Water use in neighbouring stands of beech (Fagus sylvatica L.) and black alder (Alnus glutinosa (L.) Gaertn.). Ann For Sci 56:107–120

    Google Scholar 

  • Hietz P, Turner BL, Wanek W, Richter A, Nock CA, Wright SJ (2011) Long-term change in the nitrogen cycle of tropical forests. Science 334:664–666

    CAS  PubMed  Google Scholar 

  • Hoekstra NJ, Finn JA, Lüscher A (2013) Nutrient uptake in soil niches affected by plant species and drought stress. In: Helgadottir A, Hopkins A (eds) The role of grasslands in a green future, vol 18. European Grassland Federation EGF, Grassland Science in Europe, pp 135–137

    Google Scholar 

  • Holtgrieve GW, Schindler DE, Hobbs WO, Leavitt PR, Ward EJ, Bunting L, Chen GJ, Finney BP, Gregory-Eaves I, Holmgren S, Lisac MJ, Lisi PJ, Nydick K, Rogers LA, Saros JE, Selbie DT, Shapley MD, Walsh PB, Wolfe AP (2011) A coherent signature of anthropogenic nitrogen deposition to remote watersheds of the northern hemisphere. Science 334:1545–1548

    CAS  PubMed  Google Scholar 

  • Hong B, Swaney DP, Howarth RW (2011) A toolbox for calculating net anthropogenic nitrogen inputs (NANI). Environ Model Softw 26:623–633

    Google Scholar 

  • Hong B, Swaney DP, Mörth C-M, Smedberg E, Eriksson Hägg H, Humborg C, Howarth RW, Bouraoui F (2012) Evaluating regional variation of net anthropogenic nitrogen and phosphorus inputs (NANI/NAPI), major drivers, nutrient retention pattern and management implications in the multinational areas of Baltic Sea basin. Ecol Model 227:117–135

    CAS  Google Scholar 

  • Houlton BZ, Wang Y-P, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330

    CAS  PubMed  Google Scholar 

  • Howarth RW, Swaney DP, Billen G, Garnier J, Hong B, Humborg C, Johnes P, Mörth C-M, Marino RM (2012) Nitrogen fluxes from large watersheds to coastal ecosystems controlled by net anthropogenic nitrogen inputs and climate. Front Ecol Environ 10:37–43

    Google Scholar 

  • Huber B, Frehner M (2012) Forschungsprojekt Grünerle. Abenis AG Chur und Forstingenieurbüro Monika Frehner, Sargans, Bericht erstellt im Auftrag des Bundesamtes für Umwelt (BAFU), p 198

    Google Scholar 

  • Huss-Danell K (1986) Growth and the production of leaf litter nitrogen by Alnus incana in response to liming and fertilization on degenerated forest soil. Can J For Res 16:847–853

    Google Scholar 

  • Huss-Danell K, Lundmark J-E (1988) Growth of nitrogen-fixing Alnus incana and Lupinus spp. for restoration of degenerated forest soil in northern Sweden. Studia Forestalia Suecica 181:1–20

    Google Scholar 

  • Isermann M, Diekmann M, Heemann S (2007) Effects of the expansion by Hippophaë rhamnoides on plant species richness in coastal dunes. App Veg Sci 10:33–42

    Google Scholar 

  • Jacot KA, Lüscher A, Nösberger J, Hartwig UA (2000a) Symbiotic N2 fixation of various legume species along an altitudinal gradient in the Swiss Alps. Soil Biol Biochem 32:1043–1052

    CAS  Google Scholar 

  • Jacot KA, Lüscher A, Nösberger J, Hartwig UA (2000b) The relative contribution of symbiotic N2 fixation and other nitrogen sources to grassland ecosystems along an altitudinal gradient in the Alps. Plant Soil 225:201–211

    CAS  Google Scholar 

  • Johnson DW (1992) Effects of forest management on soil carbon storage. Water Air Soil Pollut 64:83–120

    CAS  Google Scholar 

  • Johnson DW, Curtis PS (2001) Effects of forest management on soil C and N storage: meta analysis. For Ecol Manag 140:227–238

    Google Scholar 

  • Johnson DA, Rumbaugh MD (1986) Field nodulation and acetylene reduction activity of high-altitude legumes in the western United States. Arctic Alp Res 18:171–179

    Google Scholar 

  • Kardjilov MI, Gisladottir G, Gislason SR (2006) Land degradation in northeastern Iceland: present and past carbon fluxes. Land Degrad Dev 17:401–417

    Google Scholar 

  • Kershaw KA (1985) Physiological ecology of lichens. Cambridge studies in ecology. Cambridge University Press, Cambridge

    Google Scholar 

  • Kopacek J, Hejzlar J, Posch M (2013) Factors controlling the export of nitrogen from agricultural land in a large central European catchment during 1900−2010. Environ Sci Technol 47:6400–6407

    CAS  PubMed  Google Scholar 

  • Körner C (2003) Alpine plant life, 2nd edn. Springer, Berlin, p 344

    Google Scholar 

  • Körner C (2012) Alpine Treelines. Functional ecology of the global high elevation tree limits. Springer, Basel, p 220

    Google Scholar 

  • Körner C (2013a) Growth controls photosynthesis—mostly. Nova Acta Leopold 114:273–283

    Google Scholar 

  • Körner C (2013b) Plant-environment interactions. In: Bresinsky A, Körner C, Joachim W, Kadereit JW, Neuhaus G, Sonnewald U (eds) Strasburger’s plant sciences, including prokaryotes and fungi. Springer, Berlin, pp 1056–1166

    Google Scholar 

  • Körner C, Hilscher H (1978) Wachstumsdynamik von Grünerlen auf ehemaligen Almflächen an der zentralalpinen Waldgrenze. In: Cernusca A (ed) Ökologische Analysen von Almflächen im Gasteiner Tal. Veröff Oesterr MaB-Hochgebirgsprogramm Hohe Tauern, vol 2. Universitätsverlag Wagner, Innsbruck, pp 187–193

    Google Scholar 

  • Körner C, Jussel U, Schiffer K (1978) Transpiration, Diffusionswiderstand und Wasserpotential in verschiedenen Schichten eines Grünerlenbestandes. In: Cernusca A (ed) Ökologische Analysen von Almflächen im Gasteiner Tal. Veröff Oesterr MaB-Hochgebirgsprogramm Hohe Tauern, vol 2. Universitätsverlag Wagner, Innsbruck, pp 81–98

    Google Scholar 

  • Lantz TC, Gerge SE, Henry GHR (2010) Response of green alder (Alnus viridis subsp. fruticosa) patch dynamics and plant community composition to fire and regional temperature in north-western Canada. J Biogeogr 37:1597–1610

    Google Scholar 

  • Lantz TC, Marsh P, Kokelj SV (2012) Recent shrub proliferation in the Mackenzie Delta Uplands and microclimatic implications. Ecosystems 16:47–59

    Google Scholar 

  • Lavery JM, Comeau PG, Prescott CE (2004) The influence of red alder patches on light, litterfall, and soil nutrients in adjacent conifer stands. Can J For Res 34:56–64

    Google Scholar 

  • Laws MT, Graves WR (2005) Nitrogen inhibits nodulation and reversibly suppresses nitrogen fixation in nodules of Alnus maritima. J Am Soc Hortic Sci 130:496–499

    Google Scholar 

  • Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology, 2nd edn. Wiley-Blackwell, New York, p 466

    Google Scholar 

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

    Google Scholar 

  • Magesan GN, Wang H, Clinton PW (2012) Nitrogen cycling in gorse-dominated ecosystems in New Zealand. N Z J Ecol 36:21–28

    Google Scholar 

  • Magill AH, Aber JD, Currie WS, Nadelhoffer KJ, Martin ME, McDowell WH, Melillo JM, Steudler P (2004) Ecosystem response to 15 years of chronic N additions at the Harvard forest LTER, Massachusetts USA. For Ecol Manage 196:7–28

    Google Scholar 

  • Magnusson B (2010) NOBANIS–Invasive alien species fact sheet–Lupinus nootkatensis–From: Online database of the European Network on invasive alien species–www.nobanis.org. Accessed 15 Nov 2012

  • Magnússon B (ed) (1995) Biological studies of Nootka lupin (Lupinus nootkatensis) in Iceland. Rala Report 178, Agricult Res Inst, Reykjavik, p 82

  • Magnússon B, Magnússon SH, Sigurdsson BD (2001) Gródurframvinda í lúpínubreidum [Vegetation succession in areas colonized by the introduced Nootka lupin (Lupinus nootkatensis) in Iceland] Rala Report 207. Agricultural Research Institute, Reykjavik, p 100

    Google Scholar 

  • Magnússon B, Magnússon SH, Sigurdsson BD (2003) Áhrif alaskalúpínu á gródurfar [Effects of introduced Nootka lupin, Lupinus nootkatensis) on plant succession in Iceland]. Náttúrufrædingurinn 71:14–27

    Google Scholar 

  • Magnússon B, Magnússon SH, Sigurðsson BD (2004) Plant succession in areas colonized by the introduced Nootka lupin in Iceland. In: van Santen E, Hill GD (eds) Wild and cultivated lupins from the tropics to the poles. Proc 10th Int Lupin Conf, Iceland, 2002. Publ Int Lupin Assoc, Canterbury, pp 170–177

    Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London, p 889

    Google Scholar 

  • McGinley M (2012) Invasive species In: Cleveland JC (ed) Encyclopedia of Earth, Environmental information coalition, National Council for Science and Environment. First published in The Encyclopedia of Earth 25 July 2012, Last revised 8 Apr 2011

  • McQueen JC, Tozer WC, Clarkson BD (2006) Consequences of alien N2-fixers on vegetation succession in New Zealand. In: Allen RB, Lee WG (eds) Biological invasions in New Zealand. Ecol Stud, vol 186. Springer, Berlin, pp 27–58

    Google Scholar 

  • Menge DNL, Hedin LO (2009) Nitrogen fixation in different biogeochemical niches along a 120 000 year chronosequence in New Zealand. Ecology 90:2190–2201

    PubMed  Google Scholar 

  • Menge DNL, Levin SA, Hedin LO (2009) Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences. Am Nat 174:465–477

    PubMed  Google Scholar 

  • Menge DNL, DeNoyer JL, Lichstein JW (2010) Phylogenetic constraints do not explain the rarity of nitrogen-fixing trees in late-successional temperate forests. PLoS One 5:e12056

    PubMed Central  PubMed  Google Scholar 

  • Miller RE, Murray MD (1978) The effects of red alder on Douglas-fir growth. In: Briggs DG, DeBell DS, Atkinson WA (eds) Utilization and management of alder. Forest Service US Dept of Agricult, Portland, pp 283–306

    Google Scholar 

  • Myers-Smith IH, Forbes BC, Wilmking M, Hallinger M, Lantz T, Blok D, Tape KD, Macias-Fauria M, Sass-Klaassen U, Lévesque E, Boudreau S, Ropars P, Hermanutz L, Trant A, Collier LS, Weijers S, Rozema J, Rayback SA, Schmidt NM, Schaepman-Strub G, Wipf S, Rixen C, Ménard CB, Venn S, Goetz S, Andreu-Hayles L, Elmendorf S, Ravolainen V, Welker J, Grogan P, Epstein HE, Hik DS (2011) Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ Res Lett 6:045509

    Google Scholar 

  • Myrold DD, Huss-Danell K (2003) Alder and lupine enhance nitrogen cycling in a degraded forest soil in Northern Sweden. Plant Soil 254:47–56

    CAS  Google Scholar 

  • Nadelhoffer KJ, Emmett BA, Gundersen P, Kjønaas OJ, Koopmans CJ, Schleppi P, Tietema A, Wright RF (1999) Nitrogen deposition makes a minor contribution to carbon sequestration in temperate forests. Nature 398:145–148

    CAS  Google Scholar 

  • Oechslin M (1927) Die Wald- und Wirtschaftsverhältnisse im Kanton Uri Beiträge zur geobotanischen Landesaufnahme Band 14, Schweizerische Naturforschende Gesellschaft/Geobotanische KommissionVerlag Huber, p 209

  • Olsen SL, Sandvik SM, Totland O (2013) Influence of two N-fixing legumes on plant community properties and soil nutrient levels in an alpine ecosystem. Arct Antarct Alp Res 45:363–371

    Google Scholar 

  • Otte A, Maul P (2005) Verbreitungsschwerpunkte und strukturelle Einnischung der Stauden-Lupine (Lupinus polyphyllus Lindl.) in Bergwiesen der Rhön. Tuexenia 25:151–182

    Google Scholar 

  • Pallardy SG (2008) Physiology of Woody Plants, 3rd edn. Academic Press, London, p 454

    Google Scholar 

  • Pálmason F, Gudmundsson J, Sverrisson H (2009) Níturnám úr lofti í belgjurtum og tveimur trjátegundum [Nitrogen fixing by legumous plants]. Rit Fraedathings landbúnadarins 9:213–218 (In Icelandic)

    Google Scholar 

  • Pardo LH, Fenn MF, Goodale CL, Geiser LH, Driscoll CT, Allen EB, Baron JS, Bobbink R, Bowman WD, Clark CM, Emmett B, Gilliam FS, Greaver TL, Hall SJ, Lilleskov EA, Liu L, Lynch JA, Nadelhoffer KJ, Perakis SS, Robin-Abbott MJ, Stoddard JL, Weathers KC, Dennis RL (2011) Effects of nitrogen deposition and empirical nitrogen critical loads for ecoregions of the United States. Ecol Appl 21:3049–3082

    Google Scholar 

  • Parsons R, Stanforth A, Raven JA, Sprent JI (1993) Nodule growth and activity may be regulated by a feedback mechanism involving phloem nitrogen. Plant Cell Environ 16:125–136

    CAS  Google Scholar 

  • Pawlowski K, Sprent J (2008) Comparison between actinorhizal and legume symbiosis. In: Pawlowski K, Newton WE (eds) Nitrogen-fixing actinorhizal symbioses. Springer, Dordrecht, p 261l

    Google Scholar 

  • Podrazskya VV, Ulbrichova I (2003) Soil chemistry changes in green alder [Alnus alnobetula (Ehrh.) C. Koch] stands in mountain areas. J For Sci 49:104–107

    Google Scholar 

  • Radosevich SR, Hibbs DE, Ghersa CM (2006) Effects of species mixtures on growth and stand development of Douglas-fir and red alder. Can J For Res 36:768–782

    Google Scholar 

  • Reed SC, Cleveland CC, Townsend AR (2011) Functional ecology of free-living nitrogen fixation: a contemporary perspective. Ann Rev Ecol Evol Syst 42:489–512

    Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmanek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93

    CAS  PubMed  Google Scholar 

  • Richter C (2005) Agrikulturchemie und Pflanzenernährung. Margraf Publishers, Germany 426 p

    Google Scholar 

  • Rhoades CC, Oskarsson H, Binkley D, Stottlemer R (2001) Alder (Alnus crispa) effects on soils in ecosystems of the Agashashok River valley, northwest Alaska. Ecoscience 8:89–95

  • Rohrs-Richey JK, Mulder CPH, Winton LM, Stanosz G (2011) Physiological performance of an Alaskan shrub (Alnus fruticosa) in response to disease (Valsa melanodiscus) and water stress. New Phytol 189:295–307

    PubMed  Google Scholar 

  • Rothe A, Cromack K Jr, Resh SC, Makineci E, Son Y (2002) Soil carbon and nitrogen changes under Douglas-fir with and without red alder. Soil Sci Soc Am J 66:1988–1995

    CAS  Google Scholar 

  • Schaeffer SM, Sharp E, Schimel SP, Welker JM (2013) Soil-plant N processes in a High Arctic ecosystem, NW Greenland are altered by long-term experimental warming and higher rainfall. Glob Change Biol 19:3529–3539

    Google Scholar 

  • Scherer-Lorenzen M, Olde Venterink H, Buschmann H (2007) Nitrogen enrichment and plant invasions: the importance of nitrogen-fixing plants and anthropogenic eutrophication. In: Nentwig W (ed) Biological invasions. Ecol Stud, vol 193. Springer, Berlin, pp 163–180

    Google Scholar 

  • Shaftel RS, King RS, Back JA (2012) Alder cover drives nitrogen availability in Kenai lowland headwater streams, Alaska. Biogeochemistry 107:135–148

    CAS  Google Scholar 

  • Sigurdsson BD, Magnússon B (2004) Seed ecology of the Nootka lupin (Lupinus nootkatensis) in Iceland. In: van Santen E, Hill GD (eds) Wild and cultivated lupins from the tropics to the poles. Proc 10th Int Lupin Conf, Iceland, 2002. Publ Int Lupin Assoc, Canterbury, pp 195–198

    Google Scholar 

  • Sprent JI (2009) Legume nodulation: a global perspective. Wiley-Blackwell, New York

    Google Scholar 

  • Stevens CJ, Diese NB, Mountford JO, Gowing DJ (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879

    CAS  PubMed  Google Scholar 

  • Streeter J (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. Crit Rev Plant Sci 7:1–23

    CAS  Google Scholar 

  • Sutton MA, Howard CM, Erisman JW, Billen G, Bleeker A, Grennfelt P, van Grinsven H, Grizzetti B (eds) (2011) The European nitrogen assessment. Sources, effects and policy perspectives, 1st edn. Cambridge University Press

  • Svensson JS, Jeglum JK (2003) Spatio-temporal properties of tree-species belts during primary succession on rising Gulf of Bothnia coastlines. Ann Bot Fenn 40:265–282

    Google Scholar 

  • Swensen SM, Benson DR (2008) Evolution of actinorhizal host plants and Frankia endosymbionts. In: Pawlowski K, Newton WE (eds) Nitrogen fixing actinorhizal symbioses. Springer, Dordrecht, pp 73–104

    Google Scholar 

  • Tape KD, Hallinger M, Welker JM, Ruess RW (2012) Landscape heterogeneity of shrub expansion in arctic Alaska. Ecosystems 15:711–724

    CAS  Google Scholar 

  • Tarrant RF, Miller RE (1963) Accumulation of organic matter and soil nitrogen beneath a plantation of red alder and Douglas-fir. Soil Sci Soc Am Proc 27:231–234

    Google Scholar 

  • Thimonier A, Graf Pannatier E, Schmitt M, Waldner P, Walthert L, Schleppi P, Dobbertin M, Kräuchi N (2010) Does exceeding the critical loads for nitrogen alter nitrate leaching, the nutrient status of trees and their crown condition at Swiss long-term forest ecosystem research (LWF) sites? Eur J For Res 129:443–461

    CAS  Google Scholar 

  • Thomas RB, Van Bloem SJ, Schlesinger WH (2006) Climate change and symbiotic nitrogen fixation in agroecosystems. In: Newton PCD, Carran RA, Edwards GR, Niklaus PA (eds) Agroecosystems in a changing climate. CRC Press Taylor & Francis, London, pp 85–116

    Google Scholar 

  • Thompson K, Hodgson JG, Rich TCG (1995) Native and alien invasive plants: more of the same? Ecography 18:390–402

    Google Scholar 

  • Uhlig M, Dorn S, Bachofen C, Vogel J, Mody K (2011) Green alder as an important habitat of subalpine rove beetles(Coleoptera: Staphylinidae) in the Urseren valley (canton Uri, Switzerland). Mitt Schw Entomol Ges 84:141–149

    Google Scholar 

  • Uliassi DD, Ruess RW (2002) Limitations to symbiotic nitrogen fixation in primary succession on the Tanana river floodplain. Ecology 83:88–103

    Google Scholar 

  • Uri V, Lõhmus K, Mander Ü, Ostonen I, Aosaar J, Maddison M, Helmisaari H-S, Augustin J (2011) Long-term effects on the nitrogen budget of a short-rotation grey alder (Alnus incana (L.) Moench) forest on abandoned agricultural land. Ecol Eng 37:920–930

    Google Scholar 

  • van Miegroet H, Cole DW (1984) Impact of nitrification on soil acidification and cation leaching in a red alder ecosystem. J Environ Qual 13:586–590

    Google Scholar 

  • Vessey JK, John Waterer J (1992) In search of the mechanism of nitrate inhibition of nitrogenase activity in legume nodules: recent developments. Physiol Plant 84:171–176

    CAS  Google Scholar 

  • Vitousek PM (1994) Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238:802–804

  • Vitousek PM, Walker LR, Whiteaker LD, Mueller-Dombois D, Matson PA (1987) Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238:802–804

    CAS  PubMed  Google Scholar 

  • Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of earth’s ecosystems. Science 277:494–499

    CAS  Google Scholar 

  • Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns, and ecological controls in terrestrial ecosystems. Philos Trans R Soc Lond B Biol Sci. doi:10.1098/rstb.2013.0119

    Google Scholar 

  • Volz H (2003) Ursachen und Auswirkungen der Ausbreitung von Lupinus polyphyllus Lindl. im Bergwiesenökosystem der Rhön und Maßnahmen zu seiner Regulierung. Dissertation Justus-Liebig-Universität Gießen, p 157

  • Volz H, Otte A (2001) Occurrence and spreading ability of Lupinus polyphyllus Lindl in the Hochrhön area (central Germany). In: Kowarik I, Starfinger U (eds) Biological invasions in Germany—a challenge to act? Bundesamt für Naturschutz-Skripten, vol 32, pp 97–98

  • Walker TW, Syers JK (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19

    CAS  Google Scholar 

  • Weedon JT, Kowalchuk GA, Aerts R, van Hal J, van Logtestijn R, Tas N, Röling WFM, van Bodegom PM (2012) Summer warming accelerates sub-arctic peatland nitrogen cycling without changing enzyme pools or microbial community structure. Glob Change Biol 18:138–150

    Google Scholar 

  • Wettstein S (1999) Grünerlengebüsch in den Schweizer Alpen. Ein Simulationsmodell aufgrund abiotischer Faktoren und Untersuchungen über morphologische und strukturelle Variabilität. Diplomarbeit, University of Berne

  • Wiedmer E, Senn-Irlet B (2006) Biomass and primary productivity of an Alnus viridis stand—a case study from the Schächental valley, Switzerland. Bot Helv 116:55–64

    Google Scholar 

  • Wunderli R (2010) Landwirtschaftlicher Strukturwandel und Pflanzendiversität im Urserntal (UR). Bauhinia 22:17–32

    Google Scholar 

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Acknowledgments

This article synthesizes and expands the results from a workshop on ‘N-fixing plant invasion into cold climates’ which was held in the Swiss central Alps in September 2012 as part of the ClimMani research network activity under European Science Foundation (ESF). We are grateful to all participants of this workshop for the valuable discussions and contributions. We greatly acknowledge the generous funding for the workshop from the European Science Foundation, and funding received by the Swiss National Science Foundation (project VALUrsern, CR30I3-124809/1) and Mercator Foundation Switzerland for advancing this topic. Any use of trade names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Correspondence to Erika Hiltbrunner.

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Communicated by Pascal A. Niklaus.

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Hiltbrunner, E., Aerts, R., Bühlmann, T. et al. Ecological consequences of the expansion of N2-fixing plants in cold biomes. Oecologia 176, 11–24 (2014). https://doi.org/10.1007/s00442-014-2991-x

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