Abstract
Purpose
Old-growth forests in the Pacific Northwest host a variety of epiphytes on their branches and stem. Given the common and often large epiphytic biomass associated with Acer macrophyllum (Pursh) in this region, we evaluated how seasonal weather changes and urbanization (metal and nitrogen deposition), affect canopy epiphytic N2 fixation in the Hoh Rainforest of the Olympic Peninsula and in urban parks and forests in Seattle.
Methods
We collected Isothecium stoloniferum (Brid.) samples from both the Hoh Rainforest and Seattle at four periods from April 2016 through January 2017. Moss-associated N2 fixation rates were measured in the laboratory using the acetylene reduction assay and trace metal concentrations in the moss were analyzed using NO3 + H2O2 digestion.
Results
We found levels of N2 fixation were highest during the spring sampling period. Elevated levels of heavy metals were observed in I. stoloniferum samples collected in the urban canopies in Seattle where N2 fixation rates were low, suggesting N2 fixation is sensitive to the bioaccumulation of heavy metals. In A. macrophyllum canopies, I. stoloniferum was found to yield 0.1130 g N m−2 yr−1 in canopy branches within the Hoh Rainforest and only 0.0009 g N m−2 yr−1 on branches in Seattle.
Conclusions
These results highlight a rarely explored source of biological N2-fixation in temperate rainforests and suggest that epiphytic N2-fixation may contribute bio-available nitrogen in A. macrophyllum stands. N2-fixation in canopy bryophytes was found to be highly sensitive to urban pollution, possibly due to bioaccumulation of heavy metals in bryophyte tissue.
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Data availability
The datasets generated during and analyzed during the current study are available at DRYAD entry DOI.
References
Ackermann K, Zackrisson O, Rousk J, Jones DL, DeLuca TH (2012) N2 fixation in feather mosses is a sensitive indicator of N deposition in boreal forests. Ecosystems 15(6):986–998
Aldous AR (2002) Nitrogen translocation in Sphagnum mosses: effects of atmospheric nitrogen deposition. New Phytol 156(2):241–253
Alexander V, Schell DM (1973) Seasonal and spatial variation of nitrogen fixation in the Barrow, Alaska, tundra. Arct Alp Res 5(2):77–88
Basilier K, Granhall U, Stenström TA (1978) Nitrogen fixation in wet minerotrophic moss communities of a subarctic mire. Oikos 31(2):236–246
Basiliko N, Yavitt JB (2001) Influence of Ni Co, Fe, and Na additions on methane production in Sphagnum-dominated Northern American peatlands. Biogeochemistry 52(2):133–153
Bates JW (1992) Mineral nutrient acquisition and retention by bryophytes. J Bryol 17(2):223–240
Bengtsson C, Folkeson L, Göransson A (1982) Growth reduction and branching frequency in Hylocomium splendens near a foundry emitting copper and zinc. Lindbergia 8:129–138
Berg B, McClaugherty C (2008) Plant litter. Decomposition, humus formation, carbon sequestration, 2nd edn. Springer, Berlin, 2008
Berg T, Steinnes E (1997) Recent trends in atmospheric deposition of trace elements in Norway as evident from the 1995 moss survey. Sci Total Environ 208(3):197–206
Berg T, Røyset O, Steinnes E (1995) Moss (Hylocomium splendens) used as biomonitor of atmospheric trace element deposition: estimation of uptake efficiencies. Atmos Environ 29(3):353–360
Bidwell AL, Callahan ST, Tobin PC, Nelson BK, DeLuca TH (2019) Quantifying the elemental composition of mosses in western Washington USA. Sci Total Environ 693:133404
Binkley D, Graham RL (1981) Biomass, production, and nutrient cycling of mosses in an old-growth Douglas-fir forest. Ecology 62(5):1387–1389
Brady NC, Weil RR (2000) Elements of the nature and properties of soils. Prentice Hall, Upper Saddle River, pp 463–471
Chapin FS (1991) Integrated responses of plants to stress. Bioscience 41(1):29–36
Cornelissen JHC, Land SI, Soudzilovskaia NA, During HJ (2007) Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Ann Bot 99:987–1001
Davey A, Marchant HJ (1983) Seasonal variation in nitrogen fixation by Nostoc commune Vaucher at the Vestfold Hills, Antarctica. Phycologia 22(4):377–385
Decina SM, Hutyra LR, Templer PH (2020) Hotspots of nitrogen deposition in the world’s urban areas: a global data synthesis. Front Ecol Environ 18(2):92–100
DeLuca TH, Zackrisson O, Nilsson MC, Sellstedt A (2002) Quantifying nitrogen-fixation in feather moss carpets of boreal forests. Nature 419(6910):917–920
DeLuca TH, Zackrisson O, Gundale MJ, Nilsson MC (2008) Ecosystem feedbacks and nitrogen fixation in boreal forests. Science 320(5880):1181–1181
DeLuca TH, Zackrisson O, Nilsson M-C, Sun S, Arróniz-Crespo M (2022) Long-term fate of nitrogen fixation in Pleurozium schreberi Brid (mit.) moss carpets in boreal forests. Appl Soil Ecol 169:104215
Erisman JW, Bleeker A, Galloway J, Sutton MS (2007) Reduced nitrogen in ecology and the environment. Environ Pollut 150(1):140–149
Fenn ME, Ross CS, Schilling SL, Baccus WD, Larrabee MA, Lofgren RA (2013) Atmospheric deposition of nitrogen and sulfur and preferential canopy consumption of nitrate in forests of the Pacific Northwest, USA. For Ecol Manage 302:240–253
Gentili F, Nilsson MC, Zackrisson O, DeLuca TH, Sellstedt A (2005) Physiological and molecular diversity of feather moss associative N2-fixing cyanobacteria. J Exp Bot 56(422):3121–3127
Gjengedal E, Steinnes E (1990) Uptake of metal ions in moss from artificial precipitation. Environ Monit Assess 14(1):77–87
González AG, Pokrovsky OS (2014) Metal adsorption on mosses: toward a universal adsorption model. J Colloid Interface Sci 415:169–178
Gotsch SG, Nadkarni N, Amici A (2016) The functional roles of epiphytes and arboreal soils in tropical montane cloud forests. J Trop Ecol 32(5):455–468
Gundale MJ, Gustafsson H, Nilsson MC (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(12):2542–2549
Gundale MJ, DeLuca TH, Nordin A (2011) Bryophytes attenuate anthropogenic nitrogen inputs in boreal forests. Glob Change Biol 17(8):2743–2753
Gundale MJ, Nilsson M, Bansal S, Jäderlund A (2012) The interactive effects of temperature and light on biological nitrogen fixation in boreal forests. New Phytol 194(2):453–463
Haristoy CT, Zabowski D, Nadkarni N (2014) Canopy soils of Sitka spruce and bigleaf maple in the Queets River Watershed, Washington. Soil Sci Soc Am J 78(S1):S118–S124
Harmens H, Norris DA, Koerber GR, Buse A, Steinnes E, Rühling Å (2008) Temporal trends (1990–2000) in the concentration of cadmium, lead and mercury in mosses across Europe. Environ Pollut 151(2):368–376
Hart GE, Parent DR (1974) Chemistry of throughfall under Douglas-fir and Rocky Mountain juniper. Am Midl Nat 92:191–201
Kenkel NC, Bradfield GE (1986) Epiphytic vegetation on Acer macrophyllum: a multivariate study of species-habitat relationships. Plant Ecol 68(1):43–53
Kershaw KA (1985) Physiological ecology of lichens. Cambridge University Press, London, p 304
Klopatek JM, Barry MJ, Johnson DW (2006) Potential canopy interception of nitrogen in the Pacific Northwest, USA. For Ecol Manage 234(1):344–354
Legendre P, Legendre L (1998) Numerical Ecology. Elsevier
Lennihan R, Chapin DM, Dickson LG (1994) Nitrogen fixation and photosynthesis in high arctic forms of Nostoc commune. Can J Bot 72(7):940–945
Liengen T, Olsen RA (1997) Seasonal and site-specific variations in nitrogen fixation in a high arctic area, Ny-Ålesund, Spitsbergen. Can J Microbiol 43(8):759–769
Lindo Z, Whiteley JA (2011) Old trees contribute bio-available nitrogen through canopy bryophytes. Plant Soil 342(1–2):141–148
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(11):2957–2966
Meeks JC (1998) Symbiosis between Nitrogen-Fixing Cyanobacteria and Plants The establishment of symbiosis causes dramatic morphological and physiological changes in the cyanobacterium. Bioscience 48(4):266–276
Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5(1):62–71
Mulvaney RL (1996) Nitrogen—inorganic forms. In: Sparks DL (ed) Methods of soil analysis Part 3: Chemical methods. SSSA Book Series 5. Soil Science Society of America, Madison, pp 1123–1184
Nadkarni NM (1984) Biomass and mineral capital of epiphytes in an Acer macrophyllum community of a temperate moist coniferous forest, Olympic Peninsula, Washington State. Can J Bot 62(11):2223–2228
Nadkarni NM (1994) Diversity of species and interactions in the upper tree canopy of forest ecosystems. American Zoologist 34:70–78
Nadkarni NM, Matelson TJ (1992) Biomass and nutrient dynamics of fine litter of terrestrially rooted material in an Neotropical Montane Forest, Costa Rica. Biotropica 24(2):113–120
NOWData (2017) NOAA Online Weather Data: https://www.weather.gov/wrh/climate?wfo=lbf. National Oceanic and Atmospheric Administration. Accessed 14 Mar 2017
Oechel WC, Van Cleve K (1986) The role of bryophytes in nutrient cycling in the taiga. In: Van Cleve K, Chapin FS, Flanagan PW, Viereck LA, Dyrness CT (eds) Forest ecosystems in the Alaskan taiga: a synthesis of structure and function. Springer, New York, pp 121–137
Pearson J, Wells DM, Seller KJ, Bennett A, Soares A, Woodall J, Ingrouille MJ (2000) Traffic exposure increases natural 15N and heavy metal concentrations in mosses. New Phytol 147(2):317–326
Perez-Quezada JF, Pérez CA, Brito CE, Fuentes JP, Gaxiola A, Aguilera-Riquelme D, Lopatin J (2021) Biotic and abiotic drivers of carbon, nitrogen and phosphorus stocks in a temperate rainforest. For Ecol Manage 494:119341
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(4):680–699
Pott U, Turpin DH (1998) Assessment of atmospheric heavy metals by moss monitoring with Isothecium stoloniferum Brid. in the Fraser Valley, BC, Canada. Water Air Soil Pollut 101(1):25–44
Proctor M (2001) Patterns of desiccation tolerance and recovery in bryophytes. Plant Growth Regul 35(2):147–156
Puget Sound Regional Council (2020) Vision 2050: A Plan for the Central Puget Sound Region. PSR Council, Seattle
Pypker TG, Unsworth MH, Bond BJ (2006) The role of epiphytes in rainfall interception by forests in the Pacific Northwest. II. Field measurements at the branch and canopy scale. Can J For Res 36(4):819–832
Raymond BA, Pott U (2003) Atmospheric contaminants in biota of forested watersheds near Vancouver, BC: Environment Canada. Georgia Basin Ecosystem Initiative
Raymond BA, Bassingthwaighte T (2010) Measuring nitrogen and sulphur deposition in the Georgia Basin, British Columbia, using lichens and moss. J Limnol 69(1s):22–32
Reimann C, Niskavaara H, Kashulina G, Filzmoser P, Boyd R, Volden T, Tomilina O, Bogatyrev I (2001) Critical remarks on the use of terrestrial moss (Hylocomium splendens and Pleurozium schreberi) for monitoring of airborne pollution. Environ Pollut 113(1):41–57
Rousk K, Jones DL, DeLuca TH (2014) Exposure to nitrogen does not eliminate N2 fixation in the feather moss Pleurozium schreberi (Brid.) Mitt. Plant Soil 374(1–2):513–521
Rousk K, Pedersen PA, Dyrnum K, Michelsen A (2017) The interactive effects of temperature and moisture on nitrogen fixation in two temperate-arctic mosses. Theor Exp Plant Physiol 29(1):25–36
RStudio Team (2020) RStudio: Integrated Development for R. RStudio, PBC, Boston. http://www.rstudio.com/
Schöllhorn R, Burris RH (1967) Acetylene as a competitive inhibitor of N-2 fixation. Proc Natl Acad Sci 58(1):213–216
Scott D, Bradley RL, Bellenger J-P, Houle D, Gundale M, Rousk K, DeLuca TH (2018) Anthropogenic deposition of heavy metals and phosphorus may reduce biological N2 fixation in boreal forest mosses. Sci Total Environ 630(1):303–310
Shi XM, Song L, Liu WY, Lu HZ, Qi JH, Li S, Chen X, Wu JF, Liu S, Wu CS (2017) Epiphytic bryophytes as bio-indicators of atmospheric nitrogen deposition in a subtropical montane cloud forest: Response patterns, mechanism, and critical load. Environ Pollut 229:932–941
Solheim B, Johanson U, Callaghan TV, Lee JA, Gwynn-Jones D, Björn LO (2002) The nitrogen fixation potential of arctic cryptogram species is influenced by enhanced UV-B radiation. Oecologia 133(1):90–93
Spearing AM (1972) Cation-exchange capacity and galacturonic acid content of several species of Sphagnum in Sandy Ridge Bog, Central New York State. Bryologist 75(2):154–158
Susfalk RB, Johnson DW (2002) Ion exchange resin based soil solution lysimeters and snowmelt solution collectors. Commun Soil Sci Plant Anal 33(7–8):1261–1275
Tejo CF, Zabowski D, Nadkarni NM (2015) Total and epiphytic litter under the canopy of Acer macrophyllum in an old-growth temperate rainforest, Washington State, USA. Can J For Res 45(11):1654–1661
Tyler G (1990) Bryophytes and heavy metals: a literature review. Bot J Linn Soc 104(1–3):231–253
Van Langenhove L, Depaepe T, Verryckt LT, Fuchslueger L, Donald J, Leroy C, Moorthy SMK, Gargallo-Garriga A, Ellwood MDF, Verbeeck H, Van Der Straeten D, Peñuelas J, Janssens IA (2021) Comparable canopy and soil free-living nitrogen fixation rates in a lowland tropical forest. Sci Total Environ 754:142202
Van Stan JT, Pypker TG (2015) A review and evaluation of forest canopy epiphyte roles in the partitioning and chemical alteration of precipitation. Sci Total Environ 536:813–824
Zackrisson O, DeLuca TH, Nilsson MC, Sellstedt A, Berglund LM (2004) Nitrogen fixation increases with successional age in boreal forests. Ecology 85(12):3327–3334
Zackrisson O, DeLuca TH, Gentili F, Sellstedt A, Jäderlund A (2009) Nitrogen fixation in mixed Hylocomium splendens moss communities. Oecologia 160(2):309
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. Arctic Antarctic Alpine Res 34(3):293–299
Acknowledgements
This work was supported by the USDA National Institute of Food and Agriculture, McIntire-Stennis Cooperative Forestry Program (Project #1006427 to THD and PCT). The contents are solely the responsibility of the authors and do not necessarily represent the official views of the USDA. The authors would like to thank Sean Callahan, Jake Betzen, and Constance Lin for their hard work in the field, and Si Gao for her help in the lab. This research was conducted under Hoh River Trust general use permit, and the City of Seattle Department of Parks and Recreation special use permit. This research was conducted by ALB in partial fulfillment of the requirements for the M.S. degree from the University of Washington.
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Amanda L. Bidwell: Conceptualization, Data Curation, Analysis, Methodology, Visualization, Writing (Original draft preparation, Reviewing & Editing), Funding Acquisition. Patrick C. Tobin: Conceptualization, Methodology, Writing (Original draft preparation, Reviewing & Editing), Funding Acquisition. Thomas H. DeLuca: Conceptualization, Methodology, Writing (Original draft preparation, Reviewing & Editing), Supervision, Project Administration, Funding Acquisition.
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Bidwell, A.L., Tobin, P.C. & DeLuca, T.H. Nitrogen-fixation in Acer macrophyllum canopy bryophytes in the Pacific Northwest, USA. Plant Soil 490, 387–399 (2023). https://doi.org/10.1007/s11104-023-06082-8
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DOI: https://doi.org/10.1007/s11104-023-06082-8