Abstract
We tested the relationship between Sphagnum growth and the amount of nitrogen stored in free amino acids in a fertilisation experiment with intact peat monoliths in an open greenhouse in The Netherlands. Three nitrogen deposition scenarios were used: no nitrogen deposition, field conditions and a doubling of the latter, corresponding to 0, 40 and 80 kg N ha−1 year−1. Growth of Sphagnum as expressed by height increment was reduced in the 80 kg N treatment, but showed no correlation with the total nitrogen tissue concentration or with the concentration of individual or pooled free amino acids. The amount of nitrogen stored in free amino acids increased concomitantly with deposition, although it lagged more and more behind the total nitrogen concentration, the latter pointing to the accumulation of unmeasured nitrogen compounds. Asparagine clearly acted as the major storage compound for nitrogen in Sphagnum stem tissue, whereas arginine fulfilled this function to a lesser extent in the capitulum. It appears that nitrogen-induced growth inhibition of Sphagnum is related to acclimation rather than to certain threshold concentrations of amino nitrogen or total nitrogen. We propose that when Sphagnum is exposed to a step increase of nitrogen, its nitrogen metabolism does not adapt fast enough to keep up with the enhanced uptake rate. This imbalance between nitrogen uptake and assimilation may lead to an accumulation of toxic NH4 + in the cell and a subsequent reduction in growth.
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References
Aerts R, Wallén B, Malmer N (1992) Growth-limiting nutrients in Sphagnum-dominated bogs subject to low and high atmospheric nitrogen supply. J Ecol 80:131–140
Baxter R, Emes MJ, Lee DS (1992) Effects of an experimentally applied increase in ammonium on growth and amino-acid metabolism of Sphagnum cuspidatum Ehrh. ex. Hoffm. from differently polluted areas. New Phytol 120:265–274
Berendse F, Van Breemen N, Rydin H, Buttler A, Heijmans MMPD, Hoosbeek MR, Lee JA, Mitchell E, Saarinen T, Vasander H, Wallén B (2001) Raised atmospheric CO2 levels and increased N deposition cause shifts in plant species composition and production in Sphagnum bogs. Global Change Biol 7:591–598
Bieleski RL, Turner NA (1966) Separation and estimation of amino acids in crude plant extracts by thin-layer electrophoresis and chromatography. Anal Biochem 17:278–293
Calanni J, Berg E, Wood M, Mangis D, Boyce R, Weathers W, Sievering H (1999) Atmospheric nitrogen deposition at a conifer forest: response of free amino acids in Engelmann spruce needles. Environ Poll 105:79–89
Clymo RS, Hayward H (1982) The ecology of Sphagnum. In: Smith AJE (ed) Bryophyte ecology. Chapman and Hall, London, pp 229-289
Fangmeier A, Hadwiger-Fangmeier A, Van der Eerden L, Jager HJ (1994) Effects of atmospheric ammonia on vegetation. A review. Environ Poll 86:43–82
Garrels RM, Christ CL (1965) Solutions, minerals and equilibria. Harper and Row, New York
Gerendas J, Zhu Z, Bendixen R, Ratcliffe RG, Sattelmacher B, Zhu ZJ (1997) Physiological and biochemical processes related to ammonium toxicity in higher plants. Z Pflanzenernähr Bodenkd 160:3-251
Gunnarsson U, Rydin H (2000) Nitrogen fertilization reduces Sphagnum production in bog communities. New Phytol 147:527–537
Heeschen V, Gerendas J, Richter CP, Rudolph H (1997) Glutamate dehydrogenase of Sphagnum. Phytochemistry 45: 881–887
Heijmans MMPD, Berendse F, Arp WJ, Masselink AK, Klees H, De Visser W, Van Breemen N (2001) Effects of elevated carbon dioxide and increased nitrogen deposition on bog vegetation in the Netherlands. J Ecol 89:268–279
Jauhiainen J, Vasander H, Silvola J (1994) Response of Sphagnum fuscum to N deposition and increased CO2. J Bryol 18:83–95
Jauhiainen J, Wallén B, Malmer N (1998) Potential NH4 + and NO3 - uptake in seven Sphagnum species. New Phytol 138:287–293
Jauhiainen J, Silvola J, Vasander H (1999) The effects of increased nitrogen deposition and CO2 on Sphagnum angustifolium and S. warnstorfii. Ann Bot Fenn 35:247–256
Kahl S, Gerendas J, Heeschen V, Ratcliffe RG, Rudolph H (1997) Ammonium assimilation in bryophytes. L-glutamine synthetase from Sphagnum fallax. Physiol Plant 101:86–92
Karisto M, Kitunen V, Vasander H (1996) The effects of N deposition on free amino acid concentrations in two Sphagnum mosses. In: Laiho R, Laine J, Vasander H (eds) Northern peatlands in global change. Academy of Finland, Helsinki, Finland, pp 23–29
Lamers LPM, Bobbink R, Roelofs JGM (2000) Natural nitrogen filter fails in polluted raised bogs. Global Change Biol 6:583–586
Lea PJ, Miflin BJ (1980) Amino Acids and Derivatives. In: Miflin BJ (ed) The Biochemistry of Plants, vol 5. Academic Press, London, pp 569–604
Limpens J, Berendse F, Klees H (2003) N deposition affects N availability in interstitial water, growth of Sphagnum and invasion of vascular plants in bog vegetation. New Phytol 157:339–347
Morgan SM, Lee JA, Ashenden TW (1992) Effects of nitrogen oxides on nitrate assimilation in bryophytes. New Phytol 120:89–97
Näsholm T, Edvast A, Ericsson A, Norden L (1994) Accumulation of amino acids in some boreal forest plants in response to increased nitrogen availability. New Phytol 126:137–143
Nordin A, Gunnarsson U (2000) Amino acid accumulation and growth of Sphagnum under different levels of N deposition. Ecoscience 7:474–480
Press MC, Lee JA (1982) Nitrate reductase activity of Sphagnum species in the south Pennines. New Phytol 92: 487–494
Press MC, Woodin S, Lee JA (1986) The potential importance of an increased atmospheric nitrogen supply to the growth of ombrotrophic Sphagnum species. New Phytol 103:45–55
Risager M (1998) Growth response of two Sphagnum spp., S. fallax and S. magellanicum, to nitrogen. In: Impacts of nitrogen on Sphagnum dominated bogs, thesis at the Department of Plant Ecology, University of Copenhagen, pp 81–105
RIVM (1999) Luchtkwaliteit, Jaaroverzicht 1997. RIVM report 725301 001. RIVM Bilthoven
Rudolph H, Voigt JU (1986) Effects of NH4 +-N and NO3 --N on growth and metabolism of Sphagnum magellanicum. Physiol Plant 66:339–343
Rudolph H, Hohlfeld J, Jacubowski S, von der Lage P, Matlok H, Schmidt H (1993) Nitrogen metabolism of Sphagnum. Adv Bryol 5:79–105
Smolders AJP, van Riel MC, Roelofs JGM (2000) Accumulation of free amino acids as an early indicator for physiological stress (nitrogen overload) due to elevated ammonium levels in vital Stratiotes aloides L. stands. Arch Hydrobiol 150:169–175
Thönes S, Rudolph H (1983) Investigation of free amino acids and content of nitrogen in Sphagnum magellanicum. Telma 13:201–210
Tomassen HBM, Smolders AJP, Lamers LPM, Roelofs JGM (2000) Conservation of ombotrophic bog vegetations: the effects of high atmospheric nitrogen deposition. In: Rochefort L, Daigle J-Y (eds.) Sustaining our peatlands. Proceedings of the 11th International Peat Congress, Quebec City, pp 253–261
Twenhöven FL (1992a) Competition between two Sphagnum species under different deposition levels. J Bryol 17:71–80
Twenhöven FL (1992b) Untersuchungen zur Wirkung stickstoffhaltiger Niederschläge auf die Vegetation von Hochmooren (thesis). Mitteilungen der Arbeitsgemeinschaft Geobotanik in Schleswig-Holstein und Hamburg 44:1-172
Van der Heijden E, Verbeek SK, Kuiper PJC (2000) Elevated atmospheric CO2 and increased nitrogen deposition: effects on C and N metabolism and growth of peat moss Sphagnum recurvum P. Beauv. var. mucronatum (Russ.) Warnst. Global Change Biol 6:201–212
Van Katwijk MM, Vergeer LHT, Schmitz GHW, Roelofs JGM (1997) Ammonium toxicity in eelgrass Zostera marina. Mar Ecol Prog Ser 16:159–173
Williams BL, Buttler A, Grosvernier P, Francez AJ, Gilbert D, Ilomets M, Jauhiainen J, Matthey Y, Silcock DJ, Vasander H (1999a) The fate of NH4NO3 added to Sphagnum magellanicum carpets at five European mire sites. Biogeochemistry 45:73–93
Williams BL, Silcock D, Young M (1999b) Seasonal dynamics of N in two Sphagnum moss species and the underlying peat treated with 15NH4 15NO3. Biogeochemistry 45:285–302
Woodin SJ, Lee JA (1987) The effects of nitrate, ammonium and temperature on nitrate reductase activity in Sphagnum species. New Phytol 105:103–115
Woodin SJ, Press MC, Lee JA (1985) Nitrate reductase activity in Sphagnum fuscum in relation to wet deposition of nitrate from the atmosphere. New Phytol 99:381–388
Acknowledgements
This research was supported by the Ministry of Agriculture, Nature Management and Fisheries of the Netherlands. We are indebted to Harry Jonker (Plant Research International) for help with the amino acid analysis and Monique Heijmans for valuable comments on the manuscript. The authors' editor was Joy Burrough.
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Limpens, J., Berendse, F. Growth reduction of Sphagnum magellanicum subjected to high nitrogen deposition: the role of amino acid nitrogen concentration. Oecologia 135, 339–345 (2003). https://doi.org/10.1007/s00442-003-1224-5
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DOI: https://doi.org/10.1007/s00442-003-1224-5