Biogeosciences www.biogeosciences.net 1726-4170 1726-4189 6 2 2009 10.5194/bg-6-181-2009 http://www.biogeosciences.net/6/181/2009/ http://www.biogeosciences.net/6/181/2009/bg-6-181-2009.html http://www.biogeosciences.net/6/181/2009/bg-6-181-2009.pdf 181 196 2009-02-11 Nitrate retention and removal in Mediterranean streams bordered by contrasting land uses: a 15N tracer study D. von Schiller schiller@ceab.csic.es E. Martí J. L. Riera Limnology Group, Centre d'Estudis Avançats de Blanes, Consejo Superior de Investigaciones Científicas, 17300 Blanes, Spain Departament d'Ecologia, Facultat de Biología, Universitat de Barcelona, 08028 Barcelona, Spain now at: Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 301, 12561 Berlin, Germany We used 15N-labelled nitrate (NO3−) additions to investigate pathways of nitrogen (N) cycling at the whole-reach scale in three stream reaches with adjacent forested, urban and agricultural land areas. Our aim was to explore among-stream differences in: (i) the magnitude and relative importance of NO3− retention (i.e. assimilatory uptake) and removal (i.e. denitrification), (ii) the relative contribution of the different primary uptake compartments to NO3− retention, and (iii) the regeneration, transformation and export pathways of the retained N. Streams varied strongly in NO3− concentration, which was highest in the agricultural stream and lowest in the forested stream. The agricultural stream also showed the lowest dissolved oxygen (DO) concentration and discharge. Standing stocks of primary uptake compartments were similar among streams and dominated by detritus compartments (i.e. fine and coarse benthic organic matter). Metabolism was net heterotrophic in all streams, although the degree of heterotrophy was highest in the agricultural stream. The NO3− uptake length was shortest in the agricultural stream, intermediate in the urban stream, and longest in the forested stream. Conversely, the NO3− mass-transfer velocity and the areal NO3− uptake rate were highest in the urban stream. Denitrification was not detectable in the forested stream, but accounted for 9% and 68% of total NO3− uptake in the urban and the agricultural stream, respectively. The relative contribution of detritus compartments to NO3− assimilatory uptake was greatest in the forested and lowest in the agricultural stream. In all streams, the retained N was rapidly regenerated back to the water column. Due to a strong coupling between regeneration and nitrification, most retained N was exported from the experimental reaches in the form of NO3−. This study provides evidence of fast in-stream N cycling, although the relative importance of N retention and removal varied considerably among streams. Results suggest that permanent NO3− removal via denitrification may be enhanced over temporary NO3− retention via assimilatory uptake in heterotrophic human-altered streams characterized by high NO3− and low DO concentrations. Alexander R. B., Smith R. A., and Schwarz, G. E.: Effect of stream channel size on the delivery of nitrogen to the Gulf of Mexico, Nature, 403, 758–761, 2000. Allan, J. D.: Stream ecology: structure and function of running waters, Kluwer Academic Publishers, Dordrecht, The Netherlands, 388 pp., 1995. Alvarez-Cobelas, M., Rojo, C., and Angeler D. G.: Mediterranean limnology: current status, gaps and the future, J. Limnol., 64, 13–29, 2005. APHA: Standard methods for the examination of water and wastewater, American Public Health Association, Washington, USA, 1995. Ashkenas, L. R., Johnson, S. l., Gregory, S. V., Tank, J. L., and Wollheim, W. M.: A stable isotope study of nitrogen uptake and transformation in an old growth forest stream, Ecology, 85, 1725–1739, 2004. Beaulieu, J. J.,~Arango, C. P., Hamilton, S. K., and Tank, J. L.: The production and emission of nitrous oxide from headwater streams in the Midwestern United States, Glob. Change Biol., 14, 878–894, 2008. Bernot, M. J. and Dodds, W. K.: Nitrogen retention, removal, and saturation in lotic ecosystems, Ecosystems, 8, 442–453, 2005. Bernot, M. J., Tank, J. L., Royer, T. V., and David, M. B.: Nutrient uptake in streams draining agricultural catchments of the Midwestern United States, Freshw. Biol., 51, 499–509, 2006. Böhlke,~J. K., Harvey, J. W., and Voytek, M. A.: Reach-scale isotope tracer experiment to quantify denitrification and related processes in a nitrate-rich stream, midcontinent United States, Limnol. Oceanogr., 49,~821–838, 2004. Bott T. L.: Primary productivity and community respiration, in: Methods in stream ecology, edited by: Hauer, F. R., and Lamberti, G. A., Academic Press, San Diego, CA, USA, 663–690, 2006. Burgin A. J. and Hamilton S. K.: Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways, Front. Ecol. Environ., 5, 89–96, 2007. Butturini, A. and Sabater F.: Ammonium and phosphate retention in a Mediterranean stream: hydrological versus temperature control, Can. J. Fish. Aquat. Sci., 55, 1938–1945, 1998. Butturini, A., Bernal, S., Sabater, S., and Sabater, F.: The influence of the riparian-hyporheic zone on the hydrological responses in an intermittent stream, Hydrol. Earth Syst. Sci., 6, 515–525, 2002. Camargo, J. A. and Alonso, A.: Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment, Environ. Int., 32, 831–849, 2006. Christensen, P. B., Nielsen, L. P., Sorensen, J., and Revsbech, N. P.: Denitrification in nitrate-rich streams: diurnal and seasonal variation related to benthic oxygen metabolism, Limnol. Oceanogr., 35, 640–651, 1990. Davis, J. C. and Minshall, G. W.: Nitrogen and phosphorus uptake in two Idaho (USA) headwater wilderness streams, Oecologia, 119, 247–255, 1999. Dodds, W. K., Evans-White, M. A., Gerlanc, N. M., Gray, L., Gudder, D. A., Kemp, M. J., López, A. L., Stagliano, D., Strauss, E. A., Tank, J. L., Whiles, M. R., and Wollheim, W. M. Quantification of the Nitrogen Cycle in a Prairie Stream, Ecosystems, 3, 574–589, 2000. Dodds, K. D., López, A. L., Bowden, W. D., Gregory, S. V., Grimm, N. B., Hamilton, S. K., Hershey, A. E., Martí, E., McDowell, W. H., Meyer, J. L., Morrall, D., Mulholland, P. J., Peterson, B. J., Tank, J. L., Valett, H. M., Webster, J. R., and Wollheim, W. M.: N uptake as a function of concentration in streams. J. North Am. Benthol. Soc., 21, 206–220, 2002. Earl, S. R., Valett, H. M., and Webster J. R.: Nitrogen saturation in stream ecosystems, Ecology, 87, 3140–3151, 2006. Ensign, S. H. and Doyle M. W.: In-channel transient storage and associated nutrient retention: evidence from experimental manipulations. Limnol. Oceanogr., 50, 1740–1751, 2005. Fellows, C. S., Valett, H. M., Dahm,C. N., Mulholland, P. J., and Thomas, S. A..: Coupling nutrient uptake and energy flow in headwater streams, Ecosystems, 9, 788–804, 2006. Fowler, J. and Cohen, L.: Practical statistics for field biology, Wiley & Sons, Chichester, UK, 1990. Genereux, D. P. and Hemond, H. F.: Determination of gas exchange rates for a small stream on Walker Branch Watershed, Tenessee, Water Resour. Res., 28, 2365–2374, 1992. Grimm, N. B., Sheibley, R. W., Crenshaw, C. L., Dahm, C. N., Roach, W. J., and Zeglin, L. H.: N retention and transformation in urban streams, J. North Am. Benthol. Soc., 24, 626–642, 2005. Gücker, B. and Pusch, M. T.: Regulation of nutrient uptake in eutrophic lowland streams, Limnol. Oceanogr., 51, 1443–1453, 2006. Hall, R. O., Peterson, B. J., and Meyer, J. L.: Testing a nitrogen-cycling model of a forest stream by using a nitrogen-15 tracer addition, Ecosystems, 1, 283–298, 1998. Hall, R. O., Bernhardt, E. S., and Likens G. E.: Relating nutrient uptake with transient storage in forested mountain streams, Limnol. Oceanogr. 47, 255–265, 2002. Hamilton, S. K. and Ostrom, N. E.: Measurement of the stable isotope ratio of dissolved N2 in 15N tracer experiments, Limnol. Oceanogr. Meth., 5, 233–240, 2007. Hoellein, T. J., Tank, J. L., Rosi-Marshall, E. J., Entrekin, S. A., and Lamberti, G. A.: Controls on spatial and temporal variation of nutrient uptake in three Michigan headwater streams, Limnol. Oceanogr., 52, 1964–-1977, 2007. Holmes, R. M., Jones, J. B.. Fisher, S. G, and Grimm, N. B.: Denitrification in a nitrogen-limited stream ecosystem, Biogeochem., 33, 125–146, 1996. Holmes, R. M., McClelland, J. W., Sigman, D. M., Fry, B., and Peterson, B. J.: Measuring $^15$N-NH$_4^+$ in marine, estuarine and fresh waters: an adaptation of the ammonia diffusion method for samples with low ammonium concentrations, Mar. Chem., 60, 235–243, 1998. Inwood, S. E., Tank, J. L., and Bernot, M. J.: Patterns of denitrification associated with land use in 9 midwestern headwater streams, J. North Am. Benthol. Soc., 24, 227–245. 2005. Kaplan, L. A. and Bott, T. L.: Diel fluctuations in bacterial activity on streambed substrata during vernal algal blooms: effects of temperature, water chemistry, and habitat, Limnol. Oceanogr., 34, 718–733, 1989. Kemp, M. J. and Dodds, W. K.: The Influence of ammonium, nitrate, and dissolved oxygen concentrations on uptake, nitrification, and denitrification rates associated with prairie stream substrata, Limnol. Oceanogr., 47, 1380–1393, 2002. Merriam, J. L., McDowell, W. H., Tank, J. L., Wollheim, W. M., Crenshaw, C. L., and Johnson, S. L.: Characterizing nitrogen dynamics, retention and transport in a tropical rainforest stream using an in situ $^15$N addition. Freshw. Biol., 47, 143–160, 2002. 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. Mulholland, P. J., Tank, J. L., Webster, J. R., Bowden, W. D., Dodds, K. D., Gregory, S. V., Grimm, N. B., Hamilton, S. K., Johnson, S. L., Martí, E., McDowell, W. H., Merriam, J. L., Meyer, J. L., Peterson, B. J., Valett, H. M., and Wollheim, W. M.: Can uptake length in streams be determined by nutrient addition experiments? Results from an interbiome comparison study, J. North Am. Benthol. Soc., 21, 544–560, 2002. Mulholland, P. J., Valett H. M., Webster, J. R. Thomas, S. A., Cooper, L. W., Hamilton, S. K., and Peterson, B. J.: Stream denitrification and total nitrate uptake rates measured using a field $^15$N tracer addition approach, Limnol. Oceaonogr., 49, 809–820, 2004. Mulholland, P. J., Thomas S. A., Valett H. M., Webster, J. R., and Beaulieu, J. J.: Effects of light on NO$_3^-$ uptake in small forested streams: diurnal and day-to-day variations. J. North Am. Benthol. Soc., 25, 583–595, 2006. Mulholland, P.J., Helton, A. M., Poole, G. C., Hall, R. O., Hamilton, S. K., Peterson, B. J., Tank, J. L., Ashkenas, L. R., Cooper, L. W., Dahm, C. N., Dodds, W. K., Findlay, S. E., Gregory, S. V., Grimm, N. B., Johnson, S. L., Mcdowell, W. H., Meyer, J. L., Valett, H. M., Webster, J. R., Arango, C. P., Beaulieu, J. J., Bernot, M. J., Burgin, A. J., Crenshaw, C. L., Johnson, L. T., Niederlehner, B. R., O'Brien, J. M., Potter, J. D., Sheibley, R. W., Sobota, D. J., and Thomas, S. M.: Stream denitrification across biomes and its response to anthropogenic nitrate loading, Nature, 452, 202–205, 2008. Naiman, R. J. and Decamps, H.: The ecology of interfaces: riparian zones, Annu. Rev. Ecol. Syst., 28, 621–658, 1997. Newbold, J. D.: Cycles and spirals of nutrients, in: River flows and channel forms, edited by: Petts, G, and Calow C., Blackwell, Oxford, UK, 130–159, 1996. O'Brien, J. M., Dodds, W. K., Wilson, K. C., Murdock, J. N., and Eichmiller, J.: The saturation of N cycling in Central Plains streams: $^15$N experiments across a broad gradient of nitrate concentrations, Biogeochem., 84, 31–49, 2007. Owens, M.: Measurements on non-isolated natural communities in running waters, in: A manual on Methods for measuring primary production in aquatic environments, edited by: Vollenweider, R. A., Blackwell, Oxford, UK, 111–119, 1974. 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. Peterson, B. J., Wollheim, W. M., Mulholland, P. J., Webster, J. R., Meyer, J. L., Tank, J. L., Martí, E., Bowden, W. D., Valett H. M., Hershey, A. E., McDowell, W. H., Dodds, K. D., Hamilton, S. K., Gregory, S. V., and Morrall, D.: Control of nitrogen export from watersheds by headwater streams, Science, 292, 86–90, 2001. Piña-Ochoa, E. and Álvarez-Cobelas, M.: Denitrification in aquatic environments: a cross-system analysis, Biogeochem., 81, 11–130, 2006. Ruggiero, A., Solimini, A. G., and Carchini, G.: Effects of a wastewater treatment plant on organic matter dynamics and ecosystem functioning in a Mediterranean stream, Annal. Limnol., 42, 97–107, 2006. Runkel, R. L.: One dimensional transport with inflow and storage (OTIS): a solute transport model for streams and rivers. Water Resources Investigations Report 98-4018, US Geological Survey, Denver, USA, 1998. Sabater, S., Bernal, S., Butturini, A., Nin, E., and Sabater, F.: Wood and leaf debris input in a Mediterranean stream: the influence of riparian vegetation, Arch. Hydrobiol., 153, 91–102, 2001. Schade, J. D., Welter, J. R., Martí, E., and Grimm, N. B.: Hydrologic exchange and N uptake by riparian vegetation in an arid-land stream. J. North Am. Benthol. Soc., 24, 19–28, 2005. Seitzinger, S. P.: Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance, Limnol. Oceanogr., 33, 702–724, 1988. Sigman, D. M., Altabet, M. A., Michener, R., McCorkle, D. C., Fry, B., and Holmes, R. M.: Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: an adaptation of the ammonia diffusion method, Mar. Chem., 57, 227–242, 1997. Simon, K. S., Townsend, C. R., Biggs, B. J., and Bowden, W. D.: Temporal variation of N and P uptake in 2 New Zealand streams, J. North Am. Benthol. Soc., 24, 1–18, 2005. Simon, K. S., Niyogi, D. K., Frew, R. D. and Townsend, C. R.: Nitrogen dynamics in grassland streams along a gradient of agricultural development, Limnol. Oceanogr., 52, 1246–1257, 2007. Stream Solute Workshop: Concepts and methods for assessing solute dynamics in stream ecosystems, J. North Am. Benthol. Soc., 9, 95–119, 1990. Tank, J. L., Meyer, J. L., Sanzone, D. M., Mulholland, P. J., Webster, J. R., Peterson, B. J., Wollheim, W. M., and Leonard, N. E.: Analysis of nitrogen cycling in a forest stream during autumn using a $^15$N-tracer addition, Limnol. and Oceanogr., 45, 1013–1029, 2000. von Schiller, D., Martí, E., Riera, J. L., and Sabater, F.: Effects of nutrients and light on periphyton biomass and nitrogen uptake in Mediterranean streams with contrasting land uses, Freshw. Biol., 52, 891–906, 2007. von Schiller, D., Martí, E., Riera, J. L., Ribot, M., Marks, J. C., and Sabater, F.: Influence of land use on stream ecosystem function in a Mediterranean catchment, Freshw. Biol., 53, 2600–2612, 2008. Wagner, B. J. and Harvey, J. W.: Experimental design for estimating parameters of rate-limited mass transfer: analysis of stream transfer studies, Water Resour. Res., 33, 1731–1741, 1997. Webster, J. R. and Valett, H. M.: Solute dynamics, in: Methods in stream ecology, edited by: Hauer, F. R. and Lamberti, G. A., Academic Press, San Diego, CA, USA, 169–185, 2006.