Skip to main content
SpringerLink
Log in

Bryophyte and lichen biomass and nitrogen fixation in a high elevation cloud forest in Cerro de La Muerte, Costa Rica

  • Ecosystem ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Cloud forests have been found to lose more nitrogen in stream discharge than they gain from atmospheric deposition. They also support a large diversity and biomass of tree epiphytes, predominately composed of cryptogams. Since cryptogam epiphytes harbor nitrogen fixing cyanobacteria, they may help make up for the nitrogen loss from ecosystems. We assessed cryptogam biomass on the ground, boles and branches in Quercus costaricensis dominated stands near the tree line in the Cordillera de Talamanca, Costa Rica. Nitrogen fixation was assayed using 15N2 uptake. Total cryptogam biomass was 2 977 kg ha−1, with 67% being found on the lower branches. Bryophytes and chlorolichens made up 53% and 44%, respectively, of the biomass. Half of the bryophyte mass was composed of the liverwort Plagiochila heterophylla, and 66% of the chlorolichen of Lobariella pallida. There were no significant differences in nitrogen fixation rates between the cryptogam species, with a mean rate of 5.04 µg N g−1 day−1 during the predominantly wet condition in the forest. The overall nitrogen input from fixation was 6.1 kg N ha−1 year−1, of which 78% came from bryophytes, 18% from chlorolichens, and 4% from cyanolichens. Only 2.0% of the fixation occurred in cryptogams on the ground, whereas 67%, 24%, and 7% occurred on the lower branches, boles, and upper branches, respectively. These results show that tree epiphytes constitute a significant source of nitrogen for these forests, due to the trees’ large surface area, and can make up for the nitrogen lost from these ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Adams DG, Duggan PS (2008) Cyanobacteria–bryophyte symbioses. J Exp Bot 59:1047–1058

    Article  CAS  PubMed  Google Scholar 

  • Andrews M, James EK, Sprent J, Boddy RM, Gross E, Bueno do Reis Jr. F (2011) Nitrogen fixation in legumes and actinorhizal plants in natural ecosystems: values obtained using 15N natural abundance. Plant Ecol Diversity 4:131–140

    Article  Google Scholar 

  • Asplund J, Wardle DA (2017) How lichens impact on terrestrial community and ecosystem properties. Biol Rev 92:1720–1738

    Article  PubMed  Google Scholar 

  • Benner JW, Conroy S, Lunch CK, Toyoda N, Vitousek P (2007) Phosphorus fertilization increases the abundance and nitrogenase activity of the cyanolichen Pseudocyphellaria crocata in Hawaiian montane forest. Biotropica 39:400–405

    Article  Google Scholar 

  • Bergeron Y, Fenton NJ (2012) Boreal forests of eastern Canada revisited: old growth, non fire disturbances, forest succession and biodiversity. Botany 2012:509–523

    Article  Google Scholar 

  • Blukacz EA, Sprules WG, Brunner J (2005) Use of the bootstrap for error propagation in estimating zooplankton production. Ecology 86:2223–2231

    Article  Google Scholar 

  • Brodo IM, Sharnoff SD, Sharnoff S (2001) Lichens of North America. Yale University Press, New Haven

    Google Scholar 

  • Brookshire ENJ, Hedin LO, Newbold JD, Sigman DM, Jackson JK (2012) Sustained losses of bioavailable nitrogen from montane tropical forests. Nat Geosci 5:123–126

    Article  CAS  Google Scholar 

  • Bruijnzeel LA, Scatena FN, Hamilton LS (2010) Tropical Montane cloud forests: science for conservation and management. Cambridge University Press, Cambridge

    Google Scholar 

  • Cavelier J, Tanner E, Santamaria J (2000) Effect of water, temperature and fertilizers on soil nitrogen net transformations and tree growth in an elfin cloud forest of Colombia. J Trop Ecol 16:83–99

    Article  Google Scholar 

  • Chen L, Liu W, Wang G (2010) Estimation of epiphytic biomass and nutrient pools in the subtropical montane cloud forest in the Ailao Mountains, south-western China. Ecol Res 25:315–325

    Article  Google Scholar 

  • Coxson DS, Nadkarni NM (1995) Ecological roles of epiphytes in nutrient cycles of forest ecosystems. In: Lowman M, Nadkarni NM (eds) Forest canopies. Academic Press, San Diego, pp 495–543

    Google Scholar 

  • Cusack DF, Silver WL, McDowell WH (2009) Biological nitrogen fixation in two tropical forests: ecosystem-level patterns and effects of nitrogen fertilization. Ecosystems 12:1299–1315

    Article  CAS  Google Scholar 

  • Darnajoux R et al (2017) Biological nitrogen fixation by alternative nitrogenases in boreal cyanolichens: importance of molybdenum availability and implications for current biological nitrogen fixation estimates. New Phytol 213:680–689

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Diocares R, Morey T, Holguin G (2006) Producing and dispensing small quantities of 15N2 gas at atmospheric pressure. Anal Biochem 352:302–304

    Article  CAS  PubMed  Google Scholar 

  • Ellyson WJT, Sillett SC (2003) Epiphyte communities on sitka spruce in an old-growth redwood forest. The Bryologist 106:197–211

    Article  Google Scholar 

  • Favilli F, Messini A (1990) Nitrogen fixation at phyllospheric level in coniferous plants in Italy. Plant Soil 128:91–95

    Article  CAS  Google Scholar 

  • Forman RTT (1975) Lichens with blue-green algae: a nitrogen source in a Colombian rain forest. Ecology 56:1176–1184

    Article  Google Scholar 

  • Francisco TM, Couto DR, Garbin ML, Muylaert RL, Ruiz-Miranda CR (2019) Low modularity and specialization in a commensalistic epiphyte–phorophyte network in a tropical cloud forest. Biotropica 51:509–518

    Article  Google Scholar 

  • Freiberg M, Freiberg E (2000) Epiphyte diversity and biomass in the canopy of lowland and montane forests in Ecuador. J Trop Ecol 16:673–688

    Article  Google Scholar 

  • Fürnkranz M, Wanek W, Richter A, Abell G, Rasche F, Sessitsch A (2008) Nitrogen fixation by phyllosphere bacteria associated with higher plants and their colonizing epiphytes of a tropical lowland rainforest of Costa Rica. ISME J 2:5612–5570

    Article  Google Scholar 

  • Galloway JN, Dentener FJ, Capone DG (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226

    Article  CAS  Google Scholar 

  • Gavazov K, 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

    Article  CAS  Google Scholar 

  • Gundale MJ, Wardle DA, Nilsson M-C (2012) The effect of altered macroclimate on N-fixation by boreal feather mosses. Glob Change Biol 8:805–808

    Google Scholar 

  • Henskens FL, Green TGA, Wilkins A (2012) Cyanolichens can have both cyanobacteria and green algae in a common layer as major contributors to photosynthesis. Ann Bot 110:555–563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holz I, Gradstein R (2005) Cryptogamic Epiphytes in primary and recovering upper montane oak forests of Costa Rica. Plant Ecol 178:89–109

    Article  Google Scholar 

  • Holz I, Gradstein R, Heinrichs J, Kappelle M (2002) Bryophyte diversity, microhabitat differentiation, and distribution of life forms in Costa Rican upper montane Quercus forest. The Bryologist 105:334–348

    Article  Google Scholar 

  • Köhler L, Tobon C, Furmau KF, Bruijnzeel LA (2007) Biomass and water storage dynamics of epiphytes in old-growth and secondary montane cloud forest stands in Costa Rica. Plant Ecol 193:171–184

    Article  Google Scholar 

  • 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 21:1027–1033

    Article  Google Scholar 

  • Lindo Z, Whiteley JA (2010) Old trees contribute bio-available nitrogen through canopy bryophytes. Plant Soil 342:141–148

    Article  Google Scholar 

  • Liu W, Fox JED, Xu Z (2002) Nutrient fluxes in bulk precipitation, throughfall and stemflow in montane subtropical moist forest on Ailao Mountains in Yunnan, south-west China. J Trop Ecol 18:527–548

    Article  Google Scholar 

  • Liu S et al (2017) Dry-hot stress significantly reduced the nitrogenase activity of epiphytic cyanolichen. Sci Total Env 2017:619–620

    Google Scholar 

  • Markham JH (2009) Variation in moss associated nitrogen fixation in boreal forest stands. Oecologia 161:353–359

    Article  PubMed  Google Scholar 

  • Marrs RH, Proctor J, Heaney A, Mountford MD (1988) Changes in soil nitrogen-mineralization and nitrification along an altitudinal transect in tropical rain forest in Costa Rica. J Ecol 76:466–482

    Article  Google Scholar 

  • Matzek V, Vitousek P (2003) Nitrogen fixation in bryophytes, lichens, and decaying wood along a soil-age gradient in Hawaiian montane rain forest. Biotropica 35:12–19

    Google Scholar 

  • McCune B (1990) Estimation of abundance of epiphytes on branches. The Bryologist 93:39–43

    Article  Google Scholar 

  • Millbank JW, Olsen JD (1986) The assessment of nitrogen fixation and throughput by lichens IV. Nitrogen losses from Peltigera membranacea (Ach.) Nyl. in autumn, winter and spring. New Phytol 104:643–651

    Article  Google Scholar 

  • Montoya JP, Voss M, Kähler P, Capone DG (1996) A simple, high precision, high sensitivity tracer assay for N2 fixation. Appl Environ Microbiol 62:986–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nadkarni NM, Schaefer D, Matelson TJ, Solano R (2004) Biomass and nutrient pools of canopy and terrestrial components in a primary and a secondary montane cloud forest, Costa Rica. For Ecol Manage 198:223–236

    Article  Google Scholar 

  • Pérez CA, Carmona MR, Armestro JJ (2010) Non-symbiotic nitrogen fixation during leaf litter decomposition in an old-growth temperate rain forest of Chiloé Island, southern Chile: effects of single versus mixed species litter. Austral Ecol 35:148–156

    Article  Google Scholar 

  • Sheridan RP (1991) Nitrogenase activity by Hapalosiphon flexosus associated with Sphagnum erythrocalyx mats in cloud forest on the volcano La Soufriére, Guadeloupe, French West Indies. Biotropica 23:134–140

    Article  Google Scholar 

  • Sim-Sim M et al (2011) Epiphytic bryophyte diversity on Madeira Island: effects of tree species on bryophyte species richness and composition. The Bryologist 114:142–154

    Article  Google Scholar 

  • Stanton DE, Batterman SA, Von Fisher JC, Hedin LO (2019) Rapid nitrogen fixation by canopy microbiome in tropical forest determined by both phosphorus and molybdenum. Ecology 100:e02795

    Article  PubMed  Google Scholar 

  • Still CJ, Foster PN, Schneider SH (1999) Simulating the effects of climate change on tropical montane cloud forests. Nature 398:608–610

    Article  CAS  Google Scholar 

  • Sullivan BW et al (2014) Spatially robust estimates of biological nitrogen (N) fixation imply substantial human alteration of the tropical N cycle. PNAS 111:8101–8106

    Article  CAS  PubMed  Google Scholar 

  • Tamm CO (1991) Nitrogen in terrestrial ecosystems. Springer, Berlin

    Book  Google Scholar 

  • Torrey JG (1978) Nitrogen fixation by actinomycete-nodulated angiosperms. Bioscience 28:586–592

    Article  Google Scholar 

  • Vitousek PM et al (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57(58):1–45

    Article  Google Scholar 

  • Werner FA, Homeier J, Oesker M, Boy J (2012) Epiphytic biomass of a tropical montane forest varies with topography. J Trop Ecol 28:23–31

    Article  Google Scholar 

  • Wolf JHD (1993) Diversity Patterns and biomass of epiphytic bryophytes and lichens along an altitudinal gradient in the Northern Andes. Ann Mo Bot Gard 80:928–960

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by an NSERC discovery grant to JM and by the Vicerrectoría de Investigación from the University of Costa Rica. Thanks to Michelle Piercey Normore and María Isabel Morales Zurcher for help identifying the cryptogams. Thanks to Federico Valverde at Los Nímbulos Field station. The Instituto Meteorológico Nacional de Costa Rica provided part of the weather data used in this study.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Manitoba, Winnipeg, MB, R3T 2N2, Canada

    John Markham

  2. Research Center for Biodiversity and Tropical Ecology (CIBET), and School of Biology, University of Costa Rica, San Pedro, San Jose, 11501-2060, Costa Rica

    Mauricio Fernández Otárola

Authors
  1. John Markham
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mauricio Fernández Otárola
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JM and MFO conceived and designed and performed the experiments. JM performed the data analysis. JM and MFO wrote the manuscript.

Corresponding author

Correspondence to John Markham.

Additional information

Communicated by Duncan Menge.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 313 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Markham, J., Fernández Otárola, M. Bryophyte and lichen biomass and nitrogen fixation in a high elevation cloud forest in Cerro de La Muerte, Costa Rica. Oecologia 195, 489–497 (2021). https://doi.org/10.1007/s00442-020-04840-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-020-04840-4

Keywords

Search

Navigation