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Plant function and evolutionary biology
RESEARCH ARTICLE

Short-term 15N uptake kinetics and nitrogen nutrition of bryophytes in a lowland rainforest, Costa Rica

Wolfgang Wanek A B and Katja Pörtl A
+ Author Affiliations
- Author Affiliations

A Department of Chemical Ecology and Ecosystem Research, Vienna Ecology Center, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria.

B Corresponding author. Email: wolfgang.wanek@univie.ac.at

Functional Plant Biology 35(1) 51-62 https://doi.org/10.1071/FP07191
Submitted: 2 August 2007  Accepted: 19 November 2007   Published: 25 January 2008

Abstract

Though bryophytes can markedly affect the hydrological and biogeochemical cycles of tropical rainforests, virtually nothing is known on their nutritional requirements. Here, short-term 15N uptake kinetics of NO3, NH4+ and glycine were studied in nine species of bryophytes in a lowland wet tropical forest, Costa Rica. Net uptake of all three N forms obeyed to saturation (Michaelis-Menten) kinetics between 1 and 500 µmol L–1. Mean Km (Vmax) values ranged between 21 µm (6.6 µmol g–1 DW h–1, nitrate), 94 µm (43.5 µmol g–1 DW h–1, ammonium) and 126 µm (37.6 µmol g–1 DW h–1, glycine). No significant differences were evident between epiphyllous and epiphytic bryophytes. Concentrations of nitrogenous solutes of external sources ranged between 1.7 and 35.9 µm. External nitrogen concentrations and kinetic constants of the bryophyte species allowed estimation of net uptake rates in the field. The mean uptake rates were 1.8 µmol g–1 DW h–1 for nitrate, 3.6 µmol g–1 DW h–1 for ammonium, and 3.4 µmol g–1 DW h–1 for glycine, indicating that amino acids significantly contribute to bryophyte nutrition.

Additional keywords: ammonium, glycine, transport system, nitrate.


Acknowledgements

We are indebted to the University of Vienna for providing travel funds to W.W. and K.P. Robbert S. Gradstein and Ingo Holz (Georg-August–University Göttingen) and Andrea Bernecker-Lücking (Universidad de Costa Rica, San José) helped with species determination.


References


Aerts R, Wallén B, Malmer N (1992) Growth-limiting nutrients in Sphagnum-dominated bogs subject to low and high atmospheric nitrogen supply. Journal of Ecology 80, 131–140.
Crossref | GoogleScholarGoogle Scholar | open url image1

Amato M, Ladd JN (1988) Assay for microbial biomass based on ninhydrin-reactive nitrogen in extracts of fumigated soil. Soil Biology & Biochemistry 20, 107–114.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bates JW (2000) Mineral nutrition, substratum ecology, and pollution. In ‘Bryophyte biology’. (Eds AJ Shaw, B Goffinet) pp. 248–311. (Cambridge University Press: Cambridge)

Bernecker-Lücking A (1995) Diversität und Mikrohabitatspräferenzen epiphyller Moose in einem tropischen Regenwald in Costa Rica unter besonderer Berücksichtigung der Familie Lejeuneaceae. Dissertation thesis, Fakultät für Naturwissenschaften der Universität Ulm.

Bloom AJ, Sukrapanna SS, Warner RL (1992) Root respiration associated with ammonium and nitrate absorption and assimilation by barley. Plant Physiology 99, 1294–1301.
PubMed |
open url image1

Britto DT, Kronzucker HJ (2006) Futile cycling at the plasma membrane: a hallmark of low-affinity nutrient transport. Trends in Plant Science 11, 529–534.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ (2001) Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proceedings of the National Academy of Sciences of the United States of America 98, 4255–4258.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Burkholder PR (1959) Organic nutrition of some mosses growing in pure culture. The Bryologist 62, 6–15. open url image1

Büscher P, Koedam N, van Spreybroeck D (1990) Cation-exchange properties and adaptation to soil acidity in bryophytes. The New Phytologist 115, 177–186.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chalot M, Brun A (1998) Physiology of organic nitrogen acquisition by ectomycorrhizal fungi and ectomycorrhizas. FEMS Microbiology Reviews 22, 21–44.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chapin FS, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen for growth by a non-mycorrhizal arctic sedge. Nature 361, 150–153.
Crossref | GoogleScholarGoogle Scholar | open url image1

Clark 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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Coxson DS (1991) Nutrient release from epiphytic bryophytes in tropical montane rain forest (Guadeloupe). Canadian Journal of Botany 69, 2122–2129.
Crossref |
open url image1

Dahlman L, Persson J, Palmqvist K, Näsholm T (2004) Organic and inorganic nitrogen uptake in lichens. Planta 219, 459–467.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Falkengren-Grerup U, Mansson KF, Olsson MO (2000) Uptake capacity of amino acids by ten grasses and forbs in relation to soil acidity and nitrogen availability. Environmental and Experimental Botany 44, 207–219.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Filoso S, Williams MR, Melack JM (1999) Composition and deposition of throughfall in a flooded forest archipelago (Negro River, Brazil). Biogeochemistry 45, 169–195. open url image1

Forsum A, Dahlman L, Näsholm T, Nordin A (2006) Nitrogen utilization by Hylocomium splendens in a boreal forest fertilization experiment. Functional Ecology 20, 421–426.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gjengedal E, Steinnes E (1990) Uptake of metal ions in moss from artificial precipitation. Environmental Monitoring and Assessment 14, 77–87.
Crossref | GoogleScholarGoogle Scholar | open url image1

Glass ADM, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ , et al. (2002) The regulation of nitrate and ammonium transport systems in plants. Journal of Experimental Botany 53, 855–864.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gradstein SR , Churchill SP , Salazar Allen N (2001) ‘Guide to the bryophytes of tropical America.’ (The New York Botanical Garden Press: New York)

Grubb PJ, Flint OP, Gregory SC (1969) Preliminary observations on the mineral nutrition of epiphytic mosses. Transactions of the British Bryological Society 5, 802–817. open url image1

Holscher D, Kohler L, van Dijk A, Bruijnzeel LA (2004) The importance of epiphytes to total rainfall interception by a tropical montane rain forest in Costa Rica. Journal of Hydrology 292, 308–322.
Crossref | GoogleScholarGoogle Scholar | open url image1

Inselsbacher E, Cambui CA, Richter A, Stange CF, Mercier H, Wanek W (2007) Microbial activities and foliar uptake of nitrogen in the epiphytic bromeliad Vriesea gigantea. The New Phytologist 175, 311–320.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jauhiainen J, Wallén B, Malmer N (1998) Potential NH4+ and NO3– uptake in seven Sphagnum species. The New Phytologist 138, 287–293.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jones DL, Healey JR, Willett VB, Farrar JF, Hodge A (2005) Dissolved organic nitrogen uptake by plants – an important N uptake pathway? Soil Biology & Biochemistry 37, 413–423.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biology and Fertility of Soils 6, 68–72.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kielland K (1994) Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75, 2373–2383.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kielland K (1995) Landscape patterns of free amino acids in arctic tundra soils. Biogeochemistry 31, 85–98.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kielland K (1997) Role of free amino acids in the nitrogen economy of arctic cryptogams. Ecoscience 4, 75–79. open url image1

Knight AH, Crooke WM, Inkson RHE (1961) Cation-exchange capacities of tissues of higher and lower plants and their related uronic acid contents. Nature 192, 142–143.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lee JA, Baxter JW, Emes MJ (1990) Responses of Spagnum species to atmospheric nitrogen and sulphur deposition. Botanical Journal of the Linnean Society 104, 255–265. open url image1

Lesica P, Antibus RK (1991) Canopy soils and epiphyte richness. National Geographic Research and Exploration 7, 156–165. open url image1

Leskovac V (2003) ‘Comprehensive enzyme kinetics.’ (Springer: Netherlands)

Lipson D, Nasholm T (2001) The unexpected versatility of plants: organic nitrogen use and availability in terrestrial ecosystems. Oecologia 128, 305–316.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lipson DA, Raab TK, Schmidt SK, Monson RK (1999) Variation in competitive abilities of plants and microbes for specific amino acids. Biology and Fertility of Soils 29, 257–261.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lüttge U, Bauer K (1968) Die Kinetik der Ionenaufnahme durch junge und alte Sprosse von Mnium cuspidatum. Planta 78, 310–320.
Crossref | GoogleScholarGoogle Scholar | open url image1

Markus M, Hess B, Ottaway JH, Cornish-Bowden A (1976) The analysis of kinetic data in biochemistry. A critical evaluation of methods. FEBS Letters 63, 225–230.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB , et al. (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415, 68–71.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Michelsen A, Quarmby C, Sleep D, Jonasson S (1998) Vascular plant 15N natural abundance in heath and forest tundra ecosystems is closely correlated with presence and type of mycorrhizal fungi in roots. Oecologia 115, 406–418.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nadkarni NM (1986) The nutritional effects of epiphytes on host trees with special reference to alteration of precipitation chemistry. Selbyana 9, 44–51. open url image1

Nasholm T, Ekblad A, Nordin A, Giesler R, Hogberg M, Hogberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392, 914–916.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nasholm T, Huss-Danell K, Hogberg P (2000) Uptake of organic nitrogen in the field by four agriculturally important plant species. Ecology 81, 1155–1161. open url image1

Olarinmoye SO (1974) Ecology of epiphyllous liverworts: growth in three natural habitats in Western Nigeria. Journal of Bryology 8, 275–289. open url image1

Owen AG, Jones DL (2001) Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biology & Biochemistry 33, 651–657.
Crossref | GoogleScholarGoogle Scholar | open url image1

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. The New Phytologist 147, 317–326.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pócs T (1980) The epiphytic biomass and its effect on the water balance of two rain forest types in the Uluguru Mountains (Tanzania, East Africa). Acta Botanica Academiae Scientiarium Hungaricae 26, 143–167. open url image1

Pócs T (1982) Tropical forest bryophytes. In ‘Bryophyte ecology’. (Ed. AJE Smith) pp. 59–104. (Chapman and Hall: London)

Putz FE, Holbrook NM (1989) Strangler fig rooting habits and nutrient relations in the llanos of Venezuela. American Journal of Botany 76, 781–788.
Crossref | GoogleScholarGoogle Scholar | open url image1

Richards PW (1984) The ecology of tropical forest bryophytes. In ‘New manual of bryology’. (Ed. RM Schuster) pp. 1233–1270. (Hattori Botanical Laboratory: Nichinan)

Schmidt S, Stewart GR (1999) Glycine metabolism by plant roots and its occurrence in Australian plant communities. Australian Journal of Plant Physiology 26, 253–264. open url image1

Soares A, Pearson J (1997) Short-term physiological response of mosses to atmospheric ammonium and nitrate. Water, Air, and Soil Pollution 93, 225–242. open url image1

Thornton B, Robinson D (2005) Uptake and assimilation of nitrogen from solutions containing multiple N sources. Plant, Cell & Environment 28, 813–821.
Crossref | GoogleScholarGoogle Scholar | open url image1

Veneklaas EJ, Zagt RJ, Van Leerdam A, van Ek R, Broekhoven AJ, Van Genderen M (1990) Hydrological properties of the epiphytic biomass of a montane tropical rainforest, Colombia. Vegetatio 89, 183–192.
Crossref | GoogleScholarGoogle Scholar | open url image1

von Wiren N, Gazzarrini S, Gojon A, Frommer WB (2000) The molecular physiology of ammonium uptake and retrieval. Current Opinion in Plant Biology 3, 254–261.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wanek W, Arndt SK, Huber W, Popp M (2002) Nitrogen nutrition during ontogeny of hemiepiphytic Clusia species. Functional Plant Biology 29, 733–740.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wanek W, Pörtl K (2005) Phyllosphere nitrogen relations: reciprocal transfer of nitrogen between epiphyllous liverworts and host plants in the understorey of a lowland tropical wet forest in Costa Rica. The New Phytologist 166, 577–588.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wania R, Hietz P, Wanek W (2002) Natural 15N abundance of epiphytes depends on the position within the forest canopy: source signals and isotope fractionation. Plant, Cell & Environment 25, 581–589.
Crossref | GoogleScholarGoogle Scholar | open url image1

Warren CR (2006) Potential organic and inorganic N uptake by six Eucalyptus species. Functional Plant Biology 33, 653–660.
Crossref | GoogleScholarGoogle Scholar | open url image1

Weber A , Huber W , Weissenhofer A , Zamora N , Zimmermann G (2001) ‘An introductory field guide to the flowering plants of the Golfo Dulce rain forests, Costa Rica.’ (Biologiezentrum des OÖ Landesmuseums: Linz, Austria)

Wilcke W, Yasin S, Valarezo C, Zech W (2001) Change in water quality during the passage through a tropical montane rain forest in Ecuador. Biogeochemistry 55, 45–72.
Crossref | GoogleScholarGoogle Scholar | open url image1

Winkler S (1967) Die epiphyllen Moose der Nebelwälder von El Salvador. Revue Bryologique et Lichenologique 35, 303–369. open url image1

Zotz G, Budel B, Meyer A, Zellner H, Lange OL (1997) Water relations and CO2 exchange of tropical bryophytes in a lower montane rain forest in Panama. Botanica Acta 110, 9–17. open url image1