Biogeosciences
www.biogeosciences.net
1726-4170
1726-4189
4
1
2007
10.5194/bg-4-11-2007
http://www.biogeosciences.net/4/11/2007/
http://www.biogeosciences.net/4/11/2007/bg-4-11-2007.html
http://www.biogeosciences.net/4/11/2007/bg-4-11-2007.pdf
11
26
2007-01-11
Nitrogen assimilation and short term retention in a nutrient-rich tidal freshwater marsh – a whole ecosystem <sup>15</sup>N enrichment study
B. Gribsholt
b.gribsholt@nioo.knaw.nl
E. Struyf
A. Tramper
L. De Brabandere
N. Brion
S. van Damme
P. Meire
F. Dehairs
J. J. Middelburg
H. T. S. Boschker
Netherlands Institute of Ecology, Center for Estuarine and Marine Ecology. P.O. Box 140, 4400AC Yerseke, The Netherlands
University of Antwerp, Department of Biology, Environmental Management Research Group, Universiteitsplein 1C, 2610 Wilrijk, Belgium
Vrije Universiteit Brussel, Department of Analytical and Environmental Chemistry, Pleinlaan 2, 1050 Brussel, Belgium
now at: University of Florida, Dept. of Fisheries and Aquatic Sciences, 7922 NW 71st Street, Gainesville FL 32653, USA
An intact tidal freshwater marsh system (3477 m<sup>2</sup>) was labelled by
adding <sup>15</sup>N-ammonium as a tracer to the flood water inundating the
ecosystem. The appearance and retention of <sup>15</sup>N-label in different marsh
components (leaves, roots, sediment, leaf litter and invertebrate fauna) was
followed over 15 days. This allowed us to elucidate the direct assimilation
and dependence on creek-water nitrogen on a relatively short term and
provided an unbiased assessment of the relative importance of the various
compartments within the ecosystem. Two separate experiments were conducted,
one in spring/early summer (May 2002) when plants were young and building up
biomass; the other in late summer (September 2003) when macrophytes were in
a flowering or early senescent state.
<br><br>
Nitrogen assimilation rate (per hour inundated) was >3 times faster in May
compared to September. On both occasions, however, the results clearly
revealed that the less conspicuous compartments such as leaf litter and
ruderal vegetations are more important in nitrogen uptake and retention than
the prominent reed (<i>Phragmites australis</i>) meadows. Moreover, short-term nitrogen retention in
these nutrient rich marshes occurs mainly via microbial pathways associated
with the litter and sediment. Rather than direct uptake by macrophytes, it
is the large reactive surface area provided by the tidal freshwater marsh
vegetation that is most crucial for nitrogen transformation, assimilation
and short term retention in nutrient rich tidal freshwater marshes. Our
results clearly revealed the dominant role of microbes in initial nitrogen
retention in marsh ecosystems.
Ashkenas, L. R., Johnson, S. L., Gregory, S. V., Tank, J. L., and Wollheim, W. M.: A stable isotope tracer study of nitrogen uptake and transformation in an old-growth forest stream, Ecology, 85, 1725–1739, 2004.
Bodelier, P. L. E., Libochant, J. A., Blom, C. W. P. M., and Laanbroek, H. J.: Dynamics of nitrification and denitrification in root-oxygenated sediments and adaptation of ammonia-oxidizing bacteria to low-oxygen or anoxic habitats, Appl. Environ. Microbiol., 62, 4100–4107, 1996.
Bowden, W. B.: Nitrification, nitrate reduction, and nitrogen immobilization in a tidal freshwater marsh sediment, Ecology, 67, 88–99, 1986.
Bowden, W. B., Peterson, B. J., Hobbie, J. E., Steudler, P. A., and Moore III, B: Transport and processing of nitrogen in a tidal freshwater wetland, Water Resour. Res., 27, 389–408, 1991.
Bremner, J.M .: Determination and isotope-ratio analysis of different forms of nitrogen in soils , I, Apparatus and procedures for distillation, and determination of ammonium, Soil Sci. Soc. Am. Proc., 29, 504–507, 1965.
Brix, H.: Do macrophytes play a role in constructed treatment wetlands?, Water Sci. Technol., 35, 11–17, 1997.
Cronk, J. K. and Fennessy, M. S.: Wetland plants, Biology and Ecology, Lewis Publisher, Boca Raton, USA, 2001.
Drake, D. C., Naiman, R. J., and Bechthold, J. S.: Fate of nitrogen in riparian forest soils and trees: An $^15$N tracer study simulating salmon decay, Ecology, 87, 1256–1266, 2006.
Engelhardt, K. M. A. and Ritchie, M. E.: Effects of macrophyte species richness on wetland ecosystem functioning and services, Nature, 411, 687–689, 2001.
Gribsholt, B. and Kristensen, E.: Effects of bioturbation and plant roots on salt marsh bioturbation: a mesocosm study, Mar. Ecol. Prog. Ser., 241, 71–87, 2002.
Gribsholt, B., Boschker, H. T. S., Struyf, E., Andersson, M., Tramper, A., De Brabandere, L., Van Damme, S., Brion, N., Meire, P., Dehairs, F., Middelburg, J. J., and Heip, C.: Nitrogen processing in a tidal freshwater marsh: a whole ecosystem $^15$N labeling study, Limnol. Oceanogr., 50, 1945–1959, 2005.
Gribsholt, B., Struyf, E., Tramper, A., Andersson, M. G. I., Brion, N., De Brabandere, L., Van Damme, S., Meire, P., Middelburg, J.J., Dehairs, F., and Boschker, H. T. S.: Ammonium transformation in a nitrogen-rich tidal freshwater marsh, Biogeochem., 80, 289–298, 2006.
Hamilton, S. K., Tank, J. L., Raikow, D. F., Wollheim, W. M., Peterson, B. J., and Webster, J. R.: Nitrogen uptake and transformation in a midwestern U.S. stream: A stable isotope enrichment study, Biogeochem., 54, 297–340, 2001.
Hansson, L-L., Brönmark, C., Nilsson, P. A., and Åbjörnsson, K.: Conflicting demands on wetland ecosystem services: nutrient retention, biodiversity or both?, Freshw. Biol., 50, 705–714, 2005.
Holmes, R. M., Peterson, B. J., Deegan, L. A., Hughes, J. E., and Fry, B.: Nitrogen biogeochemistry in the oligohaline zone of a New England estuary, Ecology, 81, 416–432, 2000.
Hughes, J. E., Deegan, L. A., Peterson, B. J., Holmes, R. M., and Fry, B.: Nitrogen flow through the food web in the oligohaline zone of a New England estuary, Ecology, 81, 433–452, 2000.
Huttunen, A., Heikkinen, K., and Ihme, R.: Nutrient retention in the vegetation of an overland flow treatment system in northern Finland, Aquat. Bot., 55, 61–73, 1996.
Jeffrey, S. W. and Humphrey, G. F.: New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton, Biochem. Physiol. Pflanzen, 167, 191–194, 1975.
Kling, G. W.: Ecosystem-scale experiments. The use of stable isotopes in fresh waters, in: Environmental Chemistry of lakes and reservoirs, edited by: Baker, L. A., American Chemical Society, 91–120, 1994.
Merrill, J. Z. and Cornwell, J.: The role of oligohaline marshes in estuarine nutrient cycling, in: Concepts and controversies in tidal marsh ecology, edited by: Weinstein, M. P. and Kreeger, D. A., Kluwer Academic Publishers, Dordrecht, The Netherlands, 425–441, 2000.
Meuleman, A. F. M., Beekman, J. P., and Verhoeven, J. T. A: Nutrient retention and nutrient-use efficiency in \textitPhragmites australis stands after wastewater application, Wetlands, 22, 712–721, 2002.
Mitsch, J. M. and Gosselink, J. G.: The value of wetlands: importance of scale and landscape setting, Ecological Economics, 35, 25–33, 2000.
Mulholland, P. J., Tank, J. L., Sanzone, D. M., Wollheim, W. M., Peterson, B. J., Webster, J. R., and Meyer, J. L.: Nitrogen cycling in a forest stream determined by a $^15$N tracer addition, Ecol. Monogr., 70, 471–493, 2000.
Neiman, R. J. and Decamps, H.:, The ecology of interfaces: Riparian zones, Annu. Rev. Ecol. Syst., 28, 621–658, 1997.
Neubauer, S. C., Andersson, I. C., and Neikirk, B. B.: Nitrogen cycling and ecosystem exchange in a Virginia tidal freshwater marsh, Estuaries, 28, 909–922, 2005.
Nieuwenhuize, J., Maas, Y. E. M., and Middelburg, J. J.: Rapid analysis of organic carbon and nitrogen in particulate materials, Mar. Chem., 45, 217–224, 1994.
Odum, W. E.: Comparative ecology of tidal freshwater and salt marshes, Annu. Rev. Ecol. Syst., 19, 147–176, 1988.
Peterson, S. B. and Teal, J. M.: The role of plants in ecologically engineered wastewater treatment systems, Ecol. Eng., 6, 137–148, 1996.
Peterson, B. J., Bahr, M., and Kling, G. W.: A tracer investigation of nitrogen cycling in a pristine tundra river, Can. J. Fish. Aquat. Sci., 54, 2361–2367, 1997.
Rijstenbil, J. W.: Effects of UVB radiation and salt stress on growth, pigments and antioxidative defense of the marine diatom \textitCylindrotheca closterium, Mar. Ecol. Prog. Ser., 254, 37–48, 2003.
Schindler, D. W.: Replication versus realism: the need for ecosystem-scale experiments, Ecosystems, 1, 323–334, 1998.
Soetaert, K., Middelburg, J. J., Heip, C., Meire, P., Van Damme, S., and Maris, T.: Long-term change in dissolved inorganic nutrients in the heterotrophic Scheldt estuary (Belgium, the Netherlands), Limnol. Oceanogr., 51, 409–423, 2006.
Tobias, C. R., Anderson, I. C., Canuel, E. A., and Macko, S. A.: Nitrogen cycling through a fringing marsh-aquifer ecotone, Mar. Ecol. Prog. Ser., 210, 25–39, 2001a.
Tobias, C. R., Macko, S. A, Anderson, I. C., Canuel, E. A., and Harvey J. W.: Tracking the fate of a high concentration groundwater nitrate plume through a fringing marsh: A combined groundwater tracer and an in situ isotope enrichment study, Limnol. Oceanogr., 46, 1977–1989, 2001b.
Tobias, C. R., Cieri, M., Peterson, B. J., Deegan, L. A., Vallino, J., and Hughes, J. E.: Processing watershed-derived nitrogen in a well-flushed New England estuary, Limnol. Oceanogr., 48, 1766–1778, 2003.
Van Damme, S., Struyf, E., Maris, T., Ysebaert, T., Dehairs, F., Tackx , M., Heip, C., and Meire, P.: Spatial and temporal patterns of water quality along the estuarine salinity gradient of the Scheldt estuary (Belgium and The Netherlands): results of an integrated monitoring approach, Hydrobiologia, 540, 29–45, 2005.
Verhoeven, J. T. A. and Van der Toorn, J.: Marsh eutrophication and wastewater treatment, in: Wetlands and Shallow Continental water bodies, edited by: Patten, B. C., Vol 1, SPB Academic Publishing, The Hague, The Netherlands, 571–585,1990.
Veuger, B., Middelburg, J. J., Boschker, H. T. S., and Houtekamer, M.: Analysis of $^15$N incorporation into D-alanine: A new method for tracing nitrogen ubtake by bacteria, Limnol. Oceanogr. Methods, 3, 230–240, 2005.
Verhoeven, J. T. A., Whigham, D. F., van Logtestijn, R., and O'Neill, J.: A comparative study of nitrogen and phosphorous cycling in tidal and non-tidal riverine wetlands, Wetlands, 21, 210–222, 2001.
Webster, J. R., Mulholland, P. J., Tank, J. L., Valett, H. M., Dodds, W. K., Peterson, B. J., Bowden, W. B., Dahm, C. N., Findlay, S., Gregory, S. V., Grimm, N. B., Hamilton, S. K., Johnson, S. L., Marti, E., McDowell, W. H., Meyer, J. L., Morrall, D. D., Thomas, S. A., and Wollheim, W. M.: Factors affecting ammonium uptake in streams - an inter-biome perspective, Freshw. Biol., 48, 1329–1352, 2003.
White, D. S. and Howes, B. L.: Nitrogen incorporation into decomposing litter of \textitSpartina alterniflora, Limnol. Oceanogr., 39, 133–140, 1994a.
White, D. S. and Howes, B. L.: Long-term $^15$N-nitrogen retention in the vegetated sediments of a New England salt marsh, Limnol. Oceanogr., 39, 1878–1892, 1994b.