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Bryophyte-cyanobacterial associations as a key factor in N2-fixation across the Canadian Arctic

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Abstract

Nitrogen inputs via biological N2-fixation are important in arctic environments where N often limits plant productivity. An understanding of the direct and indirect theoretical causal relationships between key intercorrelated variables that drive the process of N2-fixation is essential to understanding N input. An exploratory multi-group Structural Equation Modeling (SEM) approach was used to examine the direct and indirect effects of soil moisture, plant community functional composition, and bryophyte and lichen abundance on rates of nitrogen fixation at a low arctic ecosystem, two high arctic oases and a high arctic polar desert in the Canadian Arctic. Increasing soil moisture was strongly associated with an increasing presence of bryophytes and increasing bryophyte abundance was a major factor determining higher N2-fixation rates at all sites. Shrubs had a negative effect on bryophyte abundance at all sites with the exception of the polar desert site at Alexandra Fjord highland. The importance of competition from vascular plants appears to be greater in more productive sites and may increase at lower latitudes. Moisture availability may have an indirect effect on ecosystem development by affecting N input into the system with bryophyte-cyanobacterial associations playing an important intermediary role in the process.

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References

  • Arft AM, Walker MD, Gurevitch J, Alatalo JM, Bret-Harte MS, Dale M, Diemer M, Gugerli F, Henry GHR, Jones MH, Hollister RD, Jonsdottir IS, Laine K, Levesque E, Marion GM, Molau U, Molgaard P, Nordenhall U, Raszhivin V, Robinson CH, Starr G, Stenstrom A, Stenstrom M, Totland O, Turner PL, Walker LJ, Webber PJ, Welker JM, Wookey PA (1999) Responses of tundra plants to experimental warming: Meta-analysis of the International Tundra Experiment. Ecol Monogr 69:491–511

    Google Scholar 

  • Alexander V, Schell DM (1973) Seasonal and spatial variation of nitrogen fixation in the Barrow, Alaska, Tundra. Arct Alp Res 5:77–88

    Article  CAS  Google Scholar 

  • Alexander V (1974) A synthesies of the IBP tundra biome circumpolar study of nitrogen fixation. In: Holding AJ, Heal OW, MacLean SF, Flanagan PW (eds) Soil Organisms and Decomposition in Tundra. Biome Steering Committee, Stockholm, pp 109–121

    Google Scholar 

  • Alexander VM, Billington M, Schell DM (1978) Nitrogen fixation in arctic and alpine tundra. In: Tieszen LL (ed) Vegetation and Production Ecology of an Alaskan Arctic Tundra. Springer, New York, pp 539–558

    Google Scholar 

  • Anderson DC, Harper KT, Holmgren RC (1982) Factors influencing development of cryptogamic soil crusts in Utah deserts. J Range Manag 35:180–185

    Article  Google Scholar 

  • Arndal MF, Illeris L, Michelsen A, Albert K, Tamstorf M, Hansen BU (2009) Seasonal variation in gross ecosystem production, plant biomass, and carbon and nitrogen pools in five high arctic vegetation types. Arct Antarct Alp Res 41:164–173

    Article  Google Scholar 

  • Basilier K, Granhall U (1978) Nitrogen fixation in wet minerotrophic moss communities of a subarctic mire. Oikos 31:236–246

    Article  CAS  Google Scholar 

  • Batten DS, Svoboda J (1994) Plant communities on the uplands in the vicinity of the Alexandra Fiord Lowland. In: Svoboda J, Freedman B (eds) Ecology of a Polar Oasis: Alexandra Fiord Ellesmere Island. Captus University Publications, Toronto, pp 97–112

    Google Scholar 

  • Belnap J, Büdel B, Lange OL (2001) Biological soil crusts: Characteristics and distribution. In: Belnap J, Lange OL (eds) Biological Soil Crusts: Structure, Function, and Management. Springer, New York, pp 3–30

    Chapter  Google Scholar 

  • Belnap J (2002) Nitrogen fixation in biological soil crusts from southeast Utah, USA. Biol Fertil Soils 35:128–135

    Article  CAS  Google Scholar 

  • Bliss LC (1987) Truelove Lowland. A high arctic ecosystem. University of Alberta Press, Edmonton Devon Island, Canada

    Google Scholar 

  • Bliss LC, Gold WG (1994) The patterning of plant communities and edaphic factors along a high arctic coastline: Implications for succession. Can J Bot 72:1095–1107

    Article  Google Scholar 

  • Bliss LC, Henry GHR, Svoboda J, Bliss DI (1994) Patterns of plant distribution within two polar desert landscapes. Arct Alpin Res 26:46–55

    Article  Google Scholar 

  • Bliss LC, Gold WG (1999) Vascular plant reproduction, establishment, and growth and the effects of cryptogamic crusts within a polar desert ecosystem, Devon Island, N.W.T., Canada. Can J Bot 77:623–636

    Google Scholar 

  • Breen K, Lévesque E (2008) The influence of biological soil crusts on soil characteristic along a high arctic glacier foreland, Nunavut, Canada. Arct Antarct Alp Res 40:287–297

    Article  Google Scholar 

  • Chapin DM, Bliss LC, Bledsoe LJ (1991) Environmental regulation of nitrogen fixation in a high arctic lowland ecosystem. Can J Bot 69:2744–2755

    Article  Google Scholar 

  • Chapin FS III, Shaver GR, Giblin AE, Nadelhoffer KJ, Laundre JA (1995) Responses of Arctic Tundra to experimental and observed changes in climate. Ecol 76:694–711

    Article  Google Scholar 

  • Chapin DM, Bledsoe C (1992) Nitrogen fixation in arctic plant communities. In: Chapin FS III, Jefferies RL, Reynolds JF, Shaver GR, Svoboda J (eds) Arctic Ecosystems in a Changing Climate: An Ecophysiological Perspective. Academic, New York, pp 301–319

    Google Scholar 

  • Convey P, Smith RIL (2006) Responses of terrestrial Antarctic ecosystems in climate change. Plant Ecol 182:1–10

    Google Scholar 

  • Cornelissen JHC, Callaghan TV, Alatalo JM, Michelsen A, Graglia E, Hartley AE, Hik DS, Hobbie SE, Press MC, Robinson CH, Henry GHR, Shaver GR, Phoenix GK, Jones GD, Jonasson S, Chapin FS III, Molau U, Neil C, Lee JA, Mellillo JM, Sveinbjornsson B, Aerts R (2001) Global change and arctic ecosystems: Is lichen decline a function of increases in vascular plant biomass. J Ecol 89:984–994

    Article  Google Scholar 

  • Coxson DS, Kershaw KA (1983) Rehydration response of nitrogenase activity in terrestrial Nostoc commune from Stipa-Bouteloa grassland. Can J Bot 61:2658–2668

    Article  CAS  Google Scholar 

  • Crittenden PD, Kershaw KA (1978) Discovering the role of lichens in the nitrogen cycle in the Boreal-Arctic ecosystem. Bryol 81:258–267

    Article  CAS  Google Scholar 

  • Crittenden PD, Kershaw KA (1979) Studies on lichen-dominated systems. XXII. The environmental control of nitrogenase activity in Stereocaulon paschale in spruce-lichen woodland. Can J Bot 57:236–254

    Article  CAS  Google Scholar 

  • Crocker RL, Major J (1955) Soil development in relation to vegetation and surface age at Glacier Bay, Alaska. J Ecol 43:425–448

    Google Scholar 

  • Davey A (1983) Effects of abiotic factors on nitrogen fixation by blue-green algae in Antarctica. Polar Biol 2:95–100

    Article  CAS  Google Scholar 

  • Davidson DW, Bowker M, George D, Philips SL, Belnap J (2002) Treatment effects on performance of N-fixing lichens in disturbed soil crusts of the Colorado plateau. Ecol Appl 12:1391–1405

    Article  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

    Article  PubMed  CAS  Google Scholar 

  • DeLuca TH, Zackrisson O (2007) Enhanced soil fertility under Juniperus communis in arctic ecosystems. Plant Soil 294:157–155

    Article  Google Scholar 

  • DeLuca TH, Zackrisson O, Francesco G, Sellstedt A, Nilsson M-C (2007) Ecosystem controls on nitrogen fixation in boreal feather moss communities. Oecologia 152:121–130

    Article  PubMed  Google Scholar 

  • Dickson LG (2000) Constraints to nitrogen fixation by cryptogamic crusts in a polar desert ecosystem, Devon Island, N.W.T., Canada. Arct Alp Res 32:40–45

    Article  Google Scholar 

  • Foster DR (1985) Vegetation development following fire in Picea mariana (black spruce)-Pleurozium forest of south-eastern Labrador, Canada. J Ecol 73:517–534

    Article  Google Scholar 

  • George DB, Davidson DW, Schleip KC, Patrell-Kim LJ (2000) Microtopography of microbiotic crusts on the Colorado Plateau, and the distribution of component organisms. West N Am Nat 60:343–354

    Google Scholar 

  • Goetz SJ, Bunn AJ, Fiske GJ, Houghton RA (2005) Satellite observed photosynthetic trends across boreal North America associated with climate and fire disturbance. Proc National Acad of Sci 102:13521–13525

    Article  CAS  Google Scholar 

  • Gold WG, Glew KA, Dickson LG (2001) Functional influences of cryptobiotic surface crusts in an alpine tundra basin of the Olympic Mountains, Washington, U.S.A. Northwest Sci 75:315–326

    Google Scholar 

  • Gold WG, Bliss LC (1995a) The nature of water limitations for plants in a high arctic polar desert. In: Callaghan T (ed) Global Change and Arctic Terrestrial Ecosystems. European Commission, Luxembourg, pp 149–155

    Google Scholar 

  • Gold WG, Bliss LC (1995b) Water limitations and plant community development in a high arctic polar desert. Ecol 76:1558–1568

    Article  Google Scholar 

  • Grace JB (2006) Structural Equation Modeling and Natural Systems. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Granhall U, Lid-Torsvik V (1975) Nitrogen fixation by bacteria and free-living blue-green algae in tundra areas. In: Wielgolaske FE (ed) Fennoscandian Tundra Ecosystems, part 1. Springer, New York, pp 306–315

    Google Scholar 

  • Gundale MJ, Gustafsson H, Nilsson M-C (2009) The sensitivity of nitrogen fixation by a feathermoss-cyanobacteria association to litter and moisture variability in young and old boreal forests. Can J For Res 39:2542–2549

    Article  CAS  Google Scholar 

  • Gunther AJ (1989) Nitrogen fixation by lichens in a subarctic Alaskan watershed. Bryol 92:202–208

    Article  Google Scholar 

  • Harper KT, Belnap J (2001) The influence of biological soil crusts on mineral uptake by associated vascular plants. J Arid Environ 47:347–357

    Article  Google Scholar 

  • Hartley AE, Schlesinger WH (2002) Potential environmental controls on nitrogenase activity in biological crusts of northern Chihuahuan Desert. J Arid Environ 52:293–304

    Article  Google Scholar 

  • Henry GHR, Svoboda J (1986) Dinitrogen fixation (acetylene reduction) in high arctic sedge meadow communities. Arct Antarct Alp Res 18:181–187

    Google Scholar 

  • Hobara S, McCalley C, Koba K, Giblin AE, Weiss MS, Gettel GM, Shaver GR (2006) Nitrogen fixation in surface soils and vegetation in an Arctic tundra watershed: A key source of atmospheric nitrogen. Arct Antarct Alp Res 38:363–372

    Article  Google Scholar 

  • Houle D, Bilodeau Gauthier S, Paquet S, Planas D, Warren A (2006) Identification of two genera of N2-fixing cyanobacteria growing on three feather moss species in boreal forest of Quebec, Canada. Can J Bot 84:1025–1029

    Article  Google Scholar 

  • Kallio S, Kallio P (1975) Nitrogen fixation in lichens at Kevo, North Finland. In: Wielgolaske FE (ed) Fennoscandian Tundra Ecosystems, part 1. Springer, New York, pp 292–304

    Google Scholar 

  • Kershaw KA (1976) Studies on lichen-dominated systems. XX An examination of some aspects of the northern boreal lichen woodlands in Canada. Can J Bot 55:393–410

    Article  Google Scholar 

  • Kleiner EF, Harper KT (1977) Soil properties in relation to cryptogamic groundcover in Canyonlands National Park. J Range Manag 30:202–205

    Article  CAS  Google Scholar 

  • Kurina LM, Vitousek PM (1999) Controls over the accumulation and decline of a nitrogen-fixing lichen, Stereocaulon vulcani, on young Hawaiian lava flows. J Ecol 87:784–799

    Article  Google Scholar 

  • Labine C (1994) Meteorology and climatology of the Alexandra Fiord Lowland. In: Svoboda J, Freedman B (eds) Ecology of a Polar Oasis: Alexandra Fiord Ellesmere Island. Captus University Publications, Toronto, pp 23–40

    Google Scholar 

  • Lafleur PM, Humphreys ER (2008) Spring warming and carbon dioxide exchange over low arctic tundra in central Canada. Glob Chang Biol 14:1–17

    Google Scholar 

  • Lagerström A, Nilsson MC, Zackrisson O, Wardle DA (2007) Ecosystem input of nitrogen through biological fixation in feather mosses during ecosystem retrogression. Funct Ecol 21:1027–1033

    Article  Google Scholar 

  • Liengen T, Olsen RA (1997) Seasonal and site-specific variations in nitrogen fixation in a high Arctic area, Ny-Alesund, Spitsbergen. Can J Microbiol 43:759–769

    Article  CAS  Google Scholar 

  • Liengen T (1999) Environmental factors influencing the nitrogen fixation activity of free-living terrestrial cyanobacteria from a high arctic area, Spitsberg. Can J Microbiol 45:573–581

    Article  CAS  Google Scholar 

  • Line MA (1992) Nitrogen fixation in the sub-Antarctic Macquarie Island. Polar Biol 11:601–606

    Article  Google Scholar 

  • Muc M, Bliss LC (1987) Plant communities of Truelove Lowland. In: Bliss LC (ed) Truelove Lowland, Devon Island, Canada: A high arctic ecosystem. University of Alberta Press, Edmonton, pp 143–154

    Google Scholar 

  • Muc M, Freedman B, Svoboda J (1989) Vascular plant communities of a polar oasis at Alexandra Fiord (79oN), Ellesmere Island, Canada. Can J Bot 67:1126–1136

    Google Scholar 

  • Nash TH III, Olafsen AG (1995) Climate change and the ecophysiological response of Arctic lichens. Lichenol 27:559–565

    Article  Google Scholar 

  • Oberbauer SF, Dawson TE (1992) Water relations of arctic vascular plants. In: Chapin FS III, Jefferies RL, Reynolds JF, Shaver GR, Svoboda J (eds) Arctic Ecosystems in a Changing Climate: An Ecophysiological Perspective. Academic, New York, pp 259–275

    Google Scholar 

  • Obst J (2008) Classification of land cover, vegetation communities, ecosystems and habitats in East Daring Lake Basin, Northwest Territories. Prepared for Department of Environment and Natural Resources, Wildlife Division Government of the Northwest Territories and Environment and Conservation Division. Indian and Northern Affairs Canada, Yellowknife, NT

  • Ponzetti JM, McCune BP (2001) Biotic soil crusts of Oregon's shrub steppe: Community composition in relation to soil chemistry, climate, and livestock activity. Bryol 104:212–225

    Article  Google Scholar 

  • Schell DM, Alexander V (1973) Nitrogen fixation in Arctic coastal tundra in relation to vegetation and micro-Relief. Arct 26:130–137

    Google Scholar 

  • Shipley B (2000) Cause and Correlation in Biology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Smith JL, Halvorson JJ, Bolton H Jr (2002) Soil properties and microbial activity across a 500 m elevation gradient in a semi-arid environment. Soil Biol Biochem 34:1749–1757

    Article  CAS  Google Scholar 

  • Sohlberg EH, Bliss LC (1984) Microscale pattern of vascular plant distribution in two high arctic plant communities. Can J Bot 62:2033–2042

    Article  Google Scholar 

  • Soil Classification Working Group (1998) The Canadian System of Soil Classification. 3rd ed. Agric. and Agri-Food Can. Publ. 1646, Ottawa, pp. 187.

  • Solheim B, Endal A, Vigstad H (1996) Nitrogen fixation in Arctic vegetation and soils from Svalbard, Norway. Polar Biology 16:35–40

    Google Scholar 

  • Solheim B, Zielke M, Bjerke JW, Rozema J (2006) Effects of enhanced UV-B radiation on nitrogen fixation in arctic ecosystems. Plant Ecol 182:109–118

    Google Scholar 

  • Sorensen PL, Jonasson S, Michelsen A (2006) Nitrogen fixation, denitrification, and ecosystem nitrogen pools in relation to vegetation development in the subarctic. Arct, Antarct Alp Res 38:263–272

    Article  Google Scholar 

  • Stewart WDP, Fritzgerald GP, Burris RH (1967) In situ studies on N2 fixation using the acetylene reduction technique. Proceed Natl Acad Sci USA 58:2071–2078

    Article  CAS  Google Scholar 

  • Sturm M, Racine C, Tape K (2001) Climate change—Increasing shrub abundance in the Arctic. Nature 411:546–547

    Article  PubMed  CAS  Google Scholar 

  • Turetsky MR (2003) The role of bryophytes in carbon and nitrogen cycling. Bryol 106:395–409

    Article  Google Scholar 

  • Verrecchia E, Yair A, Kidron GW, Verrecchia K (1995) Physical properties of the psammophile crptogamic crust and their consequences to the water regime of sandy soils, north-western Negev Desert, Israel. J Arid Environ 29:427–437

    Article  Google Scholar 

  • Vitousek PM, Cassman K, Cleveland C, Crewes T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochem 57(58):1–45

    Article  Google Scholar 

  • Walker DA, Binnian E, Evans BM, Lederer ND, Nordstrand E, Webber PJ (1989) Terrain, vegetation and landscape evolution of the R4D research site, Brooks Range Foothills Alaska. Holarct Ecol 12:238–261

    Google Scholar 

  • Walker DA (2000) Hierarchical subdivision of arctic tundra based on vegetation response to climate, parent material, and topography. Glob Chang Biol 6:19–34

    Article  Google Scholar 

  • Walker MD, Wahren CH, Hollister RD, Henry GHR, Ahlquist LE, Alatalo JM, Bret-Harte MS, Calef MP, Callaghan TV, Carroll AB, Epstein HE, Jonsdottir IS, Klein JA, Magnusson B, Molau U, Oberbauer SF, Rew SP, Robinson CH, Shaver GR, Suding KN, Thompson CC, Tolvanen A, Totland O, Turner PL, Tweedie CE, Webber PJ, Wookey PA (2006) Plant community responses to experimental warming across the tundra biome. Proceed Natl Acad Sci USA 103:1342–1346

    Article  CAS  Google Scholar 

  • Webber PJ (1978) Spatial and temporal variation of the vegetation and its production. In: Tieszen LL (ed) Vegetation and Production Ecology of an Alaskan Arctic Tundra. Springer, New York, pp 37–112

    Google Scholar 

  • Wierenga PJ, Hendricx JM, Nash MH, Ludwig J, Daugherty LA (1987) Variation of soil and vegetation with distance along a transect in the Chihuahuan Desert. J Arid Environ 13:53–63

    Google Scholar 

  • Zackrisson O, DeLuca TH, Nilson M-C, Selstedt A, Berglund LM (2004) Nitrogen fixation increases with successional age in boreal forests. Ecol 85:3327–3334

    Article  Google Scholar 

  • Zackrisson O, DeLuca TH, Gentili F, Selstedt A, Jäderland A (2009) Nitrogen fixation in mixed Hylocomium splendens moss communities. Oecologia 160:309–319

    Article  PubMed  CAS  Google Scholar 

  • Zielke M, Ekker AS, Olsen RA, Spjelkavik S, Solheim B (2002) The influence of abiotic factors on biological nitrogen fixation in different types of vegetation in the high arctic, Svalbard. Arct Antarct Alp Res 34:293–299

    Article  Google Scholar 

  • Zielke M, Solheim B, Spjelkavik S, Olsen RA (2005) Nitrogen fixation in the high arctic: Role of vegetation and environmental conditions. Arct Antarct Alp Res 37:372–378

    Article  Google Scholar 

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Acknowledgements

We thank Ian Snape, Greg Henry, Alanna DeBusschere and Rebecca Carmichael for assistance in the field and lab. This study was supported by the International Polar Year 2007–2008 in collaboration with Climate Change Impacts on Canadian Arctic Tundra (CiCAT) project and an NSERC post-doctoral fellowship to E.G.L.

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Correspondence to Katherine J. Stewart.

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Description of variables included in the structural equation model and full model results including direct and indirect effects and unstandardized path coefficients. (DOC 240 kb)

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Stewart, K.J., Lamb, E.G., Coxson, D.S. et al. Bryophyte-cyanobacterial associations as a key factor in N2-fixation across the Canadian Arctic. Plant Soil 344, 335–346 (2011). https://doi.org/10.1007/s11104-011-0750-x

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