Abstract
Symbiotic cyanobacteria—bryophyte associations on the forest floor are shown to contribute significantly to stand-level nitrogen budgets through the process of biological nitrogen fixation (BNF), but few studies have considered the role of canopy bryophytes. Given the high biomass of epiphytic bryophytes in many tree species of the North American temperate rain forest, we suggest that canopy bryophytes may contribute substantially to stand-level N dynamics. We confirm the presence of cyanobacteria and measure rates of BNF at three heights (0, 15 and 30 m) in Sitka spruce trees across three watershed estuaries of Clayoquot Sound, British Columbia, Canada. This study is the first to report BNF by cyanobacteria associated with epiphytic and forest floor bryophytes in the coastal temperate rain forest of North America. Cyanobacteria density was significantly greater in epiphytic bryophytes compared to mosses on the forest floor, and rates of BNF were highest at 30 m in the canopy. The majority of total stand-level BNF (0.76 kg N · ha-1 · yr-1) occurs in the canopy, rather than on the forest floor (0.26 kg N · ha-1 · yr-1). We suggest that BNF by cyanobacterial-bryophyte associations in the canopy of coastal temperate rain forests is a unique source of ecosystem N, which is dependent on large, old trees with high epiphytic bryophyte biomass.
Similar content being viewed by others
References
Adams DG, Duggan PS (2008) Cyanobacteria—bryophyte symbioses. J Exp Bot 59:1047–1058
Antoine ME (2004) An ecophysiological approach to quantifying nitrogen fixation by Lobaria oregana. Bryologist 107:82–87
Bentley BL, Carpenter EJ (1984) Direct transfer of newly-fixed nitrogen from free-living epiphyllous microorganisms to their host plant. Oecologia 63:52–56
Blevins LL, Prescott CE, Niejenhuis AV (2006) The roles of nitrogen and phosphorous in increasing productivity of western redcedar plantations on Northern Vancouver Island. For Ecol Manag 234:116–122
Burgoyne TA, DeLuca TH (2009) Short-term effects of forest restoration management on non-symbiotic nitrogen-fixation in western Montana. For Ecol Manag 258:1369–1375
Brunner A, Kimmins JP (2003) Nitrogen fixation in coarse woody debris of Thuja plicata and Tsuga heterophylla forests on northern Vancouver Island. Can J For Res 33:1670–1682
Carey EV, Sala A, Keane R, Callaway RM (2001) Are old forests underestimated as global carbon sinks? Glob Change Biol 7:339–344
Clarke DL, Nadkarni NM, Gholz HL (1998) Growth, net production, litter decomposition, and net nitrogen accumulation by epiphytic bryophytes in a tropical montane forest. Biotropica 30:12–23
Clement JP, Shaw DC (1999) Crown structure and the distribution of epiphyte functional group biomass in old-growth Pseudotsuga menziesii trees. Ecoscience 6:243–254
Cleveland CC, Townsend AR, Schimel DS, Fisher H, Howarth RW, Hedin LO, Perakis SS, Latty EF, Von Fischer JC, Elseroad A, Wasson MF (1999) Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Glob Biogeochem Cycles 13:623–645
DeLuca TH, Zackrisson O, Gundale MJ, Nilsson M-C (2008) Ecosystem feedbacks and nitrogen fixation in boreal forests. Science 320:1181
DeLuca TH, Zackrisson O, Nilsson M-C, Sellstedt A (2002) Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419:917–920
Diaz IA, Sieving KE, Peña-Foxon ME, Larraín J, Armesto JJ (2010) Epiphyte diversity and biomass loads of canopy emergent trees in Chilean temperate rain forests: a neglected functional component. For Ecol Manag 259:1490–1501
Edmonds RL, Thomas TB, Rhodes JJ (1991) Canopy and soil modification of precipitation chemistry in a temperate rain forest. Soil Sci Soc Am J 55:1685–1693
Ellyson WJT, Sillett SC (2003) Epiphyte communities on Sitka spruce in an old-growth redwood forest. Bryologist 106:197–211
Favilli F, Messini A (1990) Nitrogen fixation at phyllospheric level in coniferous plants in Italy. Plant Soil 128:91–95
Footen PW, Harrison RB, Strahm BD (2009) Long-term effects of nitrogen fertilization on the productivity of subsequent stands of Douglas-fir in the Pacific Northwest. For Ecol Manag 258:2194–2198
Gavazov KS, Soudzilovskaia NA, van Logtestijn RSP, Braster M, Cornelissen JHC (2010) Isotopic analysis of cyanobacterial nitrogen fixation associated with subarctic lichen and bryophyte species. Plant Soil 333:507–517
Gentili F, Nilsson M-C, Zackrisson O, DeLuca TH, Sellstedt A (2005) Physiological and molecular diversity of feather moss associative N2-fixing cyanobacteria. J Exp Bot 56:3121–3127
Gower ST, McMurtrie RE, Murty D (1996) Aboveground net primary production decline with stand age: potential causes. TREE 11:378–382
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
Hardy RWF, Holsten RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for N2 fixation, laboratory and field evaluation. Plant Physiol 43:1185–1207
Hazell P, Gustafsson L (1999) Retention of trees at final harvest—evaluation of a conservation technique using epiphytic bryophyte and lichen transplants. Biol Conserv 90:133–142
Heitz P, Wanek W, Wania R, Nadkarni NM (2002) Nitrogen-15 natural abundance in a montane cloud forest canopy as an indicator of nitrogen cycling and epiphyte nutrition. Oecologia 131:350–355
Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330
Hsu C-C, Horng F-W, Kuo C-M (2002) Epiphyte biomass and nutrient capital of a moist subtropical forest in north-eastern Taiwan. J Trop Ecol 18:659–670
Jones K (1982) Nitrogen fixation in the canopy of temperate forest trees: a re-examination. Ann Bot 50:329–334
Komárek J, Kling H, Komárková J (2003) Filamentous cyanobacteria. In: Wehr JD, Sheath RG (eds) Freshwater algae of North America: ecology and classification. Academic, San Diego, pp 117–196
Lagerström A, Nilsson M-C, Zackrisson O, Wardle DA (2007) Ecosystem input of nitrogen through biological fixation in feather mosses during ecosystem retrogression. Funct Ecol 21:1365–2435
Lefsky MA (2010) A global forest canopy height map from the moderate resolution imaging spectroradiometer and the geoscience laser altimeter system. Geophys Res Lett 37:L15401
Liengen T (1999) Environmental factors influencing the nitrogen fixation activity of free-living terrestrial cyanobacteria from a high arctic area, Spitsbergen. Can J Microbio 45:573–581
Lindo Z (2010) Communities of Oribatida associated with litter input in western redcedar tree crowns: are moss mats ‘magic carpets’ for oribatid mite dispersal? In: Sabelis MW, Bruin J (eds) Trends in acarology: Proceedings 12th International Congress of Acarology, pp 143–148.
Lindo Z, Gonzalez A (2010) The bryosphere: an integral and influential component of the Earth’s biosphere. Ecosystems 13:612–627
Lindo Z, Winchester NN (2007) Oribatid mite communities and foliar litter decomposition in canopy suspended soils and forest floor habitats of western redcedar forests, Vancouver Island, Canada. Soil Biol Biochem 39:2957–2966
Lindo Z, Winchester NN (2009) Spatial and environmental factors contributing to patterns in arboreal and terrestrial oribatid mite diversity across spatial scales. Oecologia 160:817–825
Luyssaert S, Schulz E-D, Börner A, Knohl A, Hessenmöllen D, Law BE, Ciais P, Grace J (2008) Old-growth forests as global carbon sinks. Nature 455:213–215
Marshall WA, Chalmers MO (1997) Airborne dispersal of Antarctic terrestrial algae and cyanobacteria. Ecography 20:585–594
McCune B (1993) Gradients in epiphytic biomass in three Pseudotsuga-Tsuga forests of different ages in Western Oregon and Washington. Bryologist 96:405–411
McCune B, Amsberry KA, Camacho FJ, Clery S, Ciole C, Emerson C, Felder G, French P, Greene D, Harris R, Hutten M, Larson B, Lesko M, Majors S, Markwell T, Parker GG, Pendergrass K, Peterson EB, Peterson ET, Platt J, Proctor J, Rambo T, Rosso A, Shaw D, Turner R, Widmer M (1997) Vertical profile of epiphytes in a Pacific Northwest old-growth forest. Northwest Sci 71:145–151
Menge DNL, Hedin LO (2009) Nitrogen fixation in different biogeochemical niches along a 120 000-year chronosequence in New Zealand. Ecology 90:2190–2201
Ministry of Forests (2001) Mensuration data from the provincial ecology program. For. Sci. Prog. B.C. Min. For. Victoria, BC, Work. Pap. 62/2001. URL: http//www.for.gov.bc.ca/hfd/pubs/Docs/Wp/Wp62.htm.
Murty D, McMurtrie RE, Ryan MG (1996) Declining forest productivity in aging forest stands: a modeling analysis of alternative hypotheses. Tree Physiol 16:187–200
Nadkarni NM (1994) Factors affecting the initiation and growth of aboveground adventitious roots in a tropical cloud forest tree: an experimental approach. Oecologia 100:94–97
Nadkarni NM, Matelson TJ (1991) Fine litter dynamics within the tree canopy of a tropical cloud forest. Ecology 72:2071–2082
Nadkarni NM, Schaefer D, Matelson TJ, Solano R (2002) Comparison of arboreal and terrestrial soil characteristics in a lower montane forest, Monteverde, Costa Rica. Pedobiologia 46:24–33
Newmaster SG, Belland RJ, Arsenault A, Vitt DH (2003) Patterns of bryophyte diversity in humid coastal and inland cedar-hemlock forests of British Columbia. Environ Rev 11:S159–S185
Perez CA, Carmona MR, Armesto JJ (2010) Non-symbiotic nitrogen fixation during leaf litter decomposition in an old-growth temperate rain forest of Chiloé Island, southern chilie: effects of single versus mixed species litter. Austral Ecol 35:148–156
Pike LH (1978) The importance of epiphytic lichens in mineral cycling. Bryologist 8:247–257
Pike LH, Rydell RA, Denison WC (1977) A 400-year-old Douglas fir tree and its epiphytes: biomass, surface area, and their distributions. Can J For Res 7:680–699
Prescott CE, McDonald MA, Weetman GF (1993) Availability of N and P in the forest floors of adjacent stands of western red cedar—western hemlock and western hemlock-amabilis fir on northern Vancouver Island. Can J For Res 23:605–610
Prescott CE, Vesterdal L, Pratt J, Venner KH, de Montigny LM, Trofymow JA (2000) Nutrient concentrations and nitrogen mineralization in forest floors of single species conifer plantations in coastal British Columbia. Can J For Res 30:1341–1352
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
Rosso AL, Muir PS, Rambo TR (2001) Using transplants to measure accumulation rates of epiphytic bryophytes in forests of western Oregon. Bryologist 104:430–439
Ryan MG, Binkely D, Fownes JH (1997) Age-related decline in forest productivity: pattern and process. Adv Ecol Res 27:214–252
Sillett SC (1995) Branch epiphyte assemblages in the forest interior and on the clearcut edge of a 700-year-old forest canopy in western Oregon. Bryologist 98:301–312
Sillett SC, Bailey MG (2003) Effects of tree crown structure on biomass of the epiphytic fern Polypodium scouleri (Polypodiaceae) in redwood forests. Am J Bot 90:255–261
Sillett SC, Rambo TR (2000) Vertical distribution of dominant epiphytes in Douglas-fir forests of the central Oregon cascades. Northwest Sci 74:44–49
Smith VH (1992) Effects of nitrogen: phosphorus supply ratios on nitrogen fixation in agricultural and pastoral ecosystems. Biogeochemistry 18:19–35
Solheim B, Zielke M (2002) Associations between cyanobacteria and mosses. In: Rai AN, Bergman B, Rasmussen U (eds) Cyanobacteria in symbiosis. Kluwer Academic Publishers, Dordrecht, pp 137–152
Stal LJ (2006) Physiological ecology of cyanobacteria in microbial mats and other communities. New Phytol 131:1–32
Turetsky MR (2003) The role of bryophytes in carbon and nitrogen cycling. Bryologist 106:395–409
Twieg BD, Durall DM, Simard SW, Jones MD (2009) Influence of soil nutrients on ectomycorrhizal communities in a chronosequence of mixed temperate forests. Mycorrhiza 19:305–316
Van Tuyl S, Law BE, TurnerDP GAI (2005) Variability in net primary production and carbon storage in biomass across Oregon forests—an assessment integrating data from forest inventories, intensive sites, and remote sensing. For Ecol Manage 209:273–291
Vance ED, Nadkarni NM (1990) Microbial biomass and activity in canopy organic matter and the forest floor of a tropical cloud forest. Soil Biol Biochem 22:677–684
Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115
Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45
Zackrisson O, DeLuca TH, Nilsson M-C, Sellstedt A, Berglund LM (2004) Nitrogen fixation increases with successional age in boreal forests. Ecology 85:3327–3334
Zehr JP, Montoya J (2007) Measuring N2 fixation in the field. In: Bothe H, Ferguson SJ, Newton EW (eds) Biology of the nitrogen cycle. Elsevier, Amsterdam, pp 193–205
Acknowledgements
This research was funded by a grant from the Natural Sciences and Engineering Research Council of Canada to Z. Lindo. A grant from Clayoquot Biosphere Trust to N. Winchester provided site access. We thank K. Jordan for logistical help in the field, A. MacKinnon, A. Gonzalez, T. DeLuca, J. Campbell, C. Prescott, M. Gundale, and anonymous reviewers for helpful comments on previous versions of this manuscript. A. Gonzalez provided laboratory space and equipment. Z. Lindo and J. Whiteley designed the experiment, Z. Lindo conducted the sampling, sample processing and data analyses. Z. Lindo and J. Whiteley wrote the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Euan K. James.
Rights and permissions
About this article
Cite this article
Lindo, Z., Whiteley, J.A. Old trees contribute bio-available nitrogen through canopy bryophytes. Plant Soil 342, 141–148 (2011). https://doi.org/10.1007/s11104-010-0678-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-010-0678-6