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Contrasts among macrophyte riparian species in their use of stream water nitrate and ammonium: insights from 15N natural abundance

Aquatic Sciences volume 76, pages 203–215 (2014)Cite this article

Abstract

We examined the relevance of dissolved inorganic nitrogen (DIN) forms (nitrate and ammonium) in stream water as N sources for different macrophyte species. To do this, we investigated the variability and relationships between 15N natural abundance of DIN forms and of four different macrophyte species in five different streams influenced by inputs from wastewater treatment plants and over time within one of these streams. Results showed that 15N signatures were similar in species of submersed and amphibious macrophytes and in stream water DIN, whereas 15N signatures of the riparian species were not. 15N signatures of macrophytes were generally closer to 15N signatures of nitrate, regardless of the species considered. Our results showed significant relationships between 15N signatures of DIN and those of submersed Callitriche stagnalis and amphibious Veronica beccabunga and Apium nodiflorum, suggesting stream water DIN as a relevant N source for these two functional groups. Moreover, results from a mixing model suggested that stream water DIN taken up by the submersed and amphibious species was mostly in the form of nitrate. Together, these results suggest different contribution to in-stream N uptake among the spatially-segregated species of macrophytes. While submersed and amphibious species can contribute to in-stream N uptake by assimilation of DIN, macrophyte species located at stream channel edges do not seem to rely on stream water DIN as an N source. Ultimately, these results add a functional dimension to the current use of macrophytes for the restoration of stream channel morphology, indicating that they can also contribute to reduce excess DIN in streams.

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References

  • Acuña V, Vilches C, Giorgi A (2011) As productive and slow as a stream can be-the metabolism of a Pampean stream. J N Am Benthol Soc 30(1):71–83. doi:10.1899/09-082.1

    Article  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26(1):32–46. doi:10.1111/j.1442-9993.2001.01070.pp.x

    Google Scholar 

  • APHA (1995) Standard methods for the examination of water and wastewater, 19th edn. American Publishers Health Association, Washington

    Google Scholar 

  • Benson ER, O’Neil JM, Dennison WC (2008) Using the aquatic macrophyte Vallisneria americana (wild celery) as a nutrient bioindicator. Hydrobiologia 596:187–196. doi:10.1007/s10750-007-9095-0

    Article  CAS  Google Scholar 

  • Biggs J, Williams P, Whitfield M, Nicolet P, Weatherby A (2005) 15 years of pond assessment in Britain: results and lessons learned from the work of Pond Conservation. Aquat Conserv Mar Freshw Ecosyst 15(6):693–714. doi:10.1002/aqc.745

    Article  Google Scholar 

  • Blom CWPM, Voesenek LACJ (1996) Flooding: the survival strategies of plants. Trends Ecol Evol 11(7):290–295

    Article  CAS  PubMed  Google Scholar 

  • Bolker, R Development Core Team (2012). bbmle: tools for general maximum likelihood estimation. R package version 1.0.5.2. http://CRAN.R-project.org/package=bbmle

  • Bowden WB, Glime JM, Riis T (2007) Macrophytes and bryophytes. In: Hauer FR, Lamberti GA (eds) Methods in stream ecology. Elsevier, Oxford

    Google Scholar 

  • Brooker RW, Callaghan TV, Jonasson S (1999) Nitrogen uptake by rhizomes of the clonal sedge Carex bigelowii: a previously overlooked nutritional benefit of rhizomatous growth. New Phytol 142(1):35–48. doi:10.1046/j.1469-8137.1999.00384.x

    Article  Google Scholar 

  • Caille F, Riera JLL, Rosell-Melé A (2012) Modelling nitrogen and phosphorus loads in a Mediterranean river catchment (La Tordera, NE Spain). Hydrol Earth Syst Sci 16(8):2417–2435

    Article  CAS  Google Scholar 

  • Carr GM, Chambers PA (1998) Macrophyte growth and sediment phosphorus and nitrogen in a Canadian prairie river. Freshw Biol 39(3):525–536. doi:10.1046/j.1365-2427.1998.00300.x

    Article  CAS  Google Scholar 

  • Cedergreen N, Madsen TV (2002) Nitrogen uptake by the floating macrophyte Lemna minor. New Phytol 155:285–292

    Article  Google Scholar 

  • Clarke SJ (2002) Vegetation growth in rivers: influences upon sediment and nutrient dynamics. Prog Phys Geogr 26(2):159–172. doi:10.1191/0309133302pp324ra

    Article  Google Scholar 

  • Clarke RT, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Cohen RA, Bradham AM (2010) Uptake of stable N isotopes by Myriophyllum spicatum is not selective. Aquat Bot 92(4):227–232

    Article  CAS  Google Scholar 

  • Cole ML, Kroeger KD, McClelland JW, Valiela I (2005) Macrophytes as indicators of land-derived wastewater: application of a delta N-15 method in aquatic systems. Water Resour Res 41(1):W01014

    Google Scholar 

  • Costanzo SD, O’Donohue MJ, Dennison WC, Loneragan NR, Thomas M (2001) A new approach for detecting and mapping sewage impacts. Mar Pollut Bull 42:149–156

    Article  CAS  PubMed  Google Scholar 

  • De Brabandere L, Frazer TK, Montoya JP (2007) Stable nitrogen isotope ratios of macrophytes and associated periphyton along a nitrate gradient in two subtropical, spring-fed streams. Freshw Biol 52(8):1564–1575. doi:10.1111/j.1365-2427.2007.01788.x

    Article  Google Scholar 

  • Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6(3):121–126

    Article  CAS  PubMed  Google Scholar 

  • Evans RD, Bloom AJ, Sukrapanna SS, Ehleringer JR (1996) Nitrogen isotope composition of tomato (Lycopersicon esculentum Mill. cv. T-5) grown under ammonium or nitrate nutrition. Plant Cell Environ 19(11):1317–1323. doi:10.1111/j.1365-3040.1996.tb00010.x

    Article  Google Scholar 

  • Feijoo C, Giorgi A, Ferreiro N (2011) Phosphate uptake in a macrophytes-rich Pampean stream. Limnologica 41(2011):285–289

    Article  CAS  Google Scholar 

  • Finlay JC, Kendall C (2007) Stable isotope tracing of temporal and spatial variability in organic matter sources to freshwater ecosystems. In: Michener RH, Lajtha k (eds) Stable isotopes in ecology and environmental science, 2nd edn. Blackwell Publishing, Malden, pp 283–333

  • Fry B (2008) Stable isotope ecology, 3rd edn. Springer, New York

    Google Scholar 

  • Gacia E, Ballesteros E, Camarero L, Delgado O, Palau A, Riera JL, Catalan J (1994) Macrophytes from lakes in the eastern pyrenees—community composition and ordination in relation to environmental factors. Freshw Biol 32(1):73–81. doi:10.1111/j.1365-2427.1994.tb00867.x

    Article  Google Scholar 

  • Gammons CH, Babcock JN, Parker SR, Poulson SR (2010) Diel cycling and stable isotopes of dissolved oxygen, dissolved inorganic carbon, and nitrogenous species in a stream receiving treated municipal sewage. Chem Geol 283(1–2):44–55

    Google Scholar 

  • Gherardi LA, Sala OE, Yahdjian L (2013) Preference for different inorganic nitrogen forms among plant functional types and species of the Patagonian steppe. Oecologia. doi:10.1007/s00442-013-2687-7

    PubMed  Google Scholar 

  • Giorgi A, Feijoo C, Tell G (2005) Primary producers in a Pampean stream: temporal variation and structuring role. Biodivers Conserv 14(7):1699–1718. doi:10.1007/s10531-004-0694-z

    Article  Google Scholar 

  • Gordon N, Mcmahon TA, Finlayson BL, Gippel CJ, Nathan RJ (2004) Stream hydrology. An introduction for ecologists. Wiley, Chichester

    Google Scholar 

  • Gucker B, Brauns M, Pusch MT (2006) Effects of wastewater treatment plant discharge on ecosystem structure and function of lowland streams. J N Am Benthol Soc 25(2):313–329. doi:10.1899/0887-3593(2006)25[313:eowtpd]2.0.co;2

    Article  Google Scholar 

  • Handley LL, Austin AT, Robinson D, Scrimgeour CM, Raven JA, Heaton THE, Schmidt S, Stewart GR (1999) The N-15 natural abundance (delta N-15) of ecosystem samples reflects measures of water availability. Aust J Plant Physiol 26(2):185–199

    Article  Google Scholar 

  • Harrison SSC, Pretty JL, Shepherd D, Hildrew AG, Smith C, Hey RD (2004) The effect of instream rehabilitation structures on macroinvertebrates in lowland rivers. J Appl Ecol 41(6):1140–1154. doi:10.1111/j.0021-8901.2004.00958.x

    Article  Google Scholar 

  • Holmes RM, McClelland JW, Sigman DM, Fry B, Peterson BJ (1998) Measuring N-15-NH4+ in marine, estuarine and fresh waters: an adaptation of the ammonia diffusion method for samples with low ammonium concentrations. Mar Chem 60(3–4):235–243. doi:10.1016/s0304-4203(97)00099-6

    Article  CAS  Google Scholar 

  • Kohzu A, Miyajima T, Tayasu I, Yoshimizu C, Hyodo F, Matsui K, Nakano T, Wada E, Fujita N, Nagata T (2008) Use of stable nitrogen isotope signatures of riparian macrophytes as an indicator of anthropogenic N inputs to river ecosystems. Environ Sci Technol 42(21):7837–7841. doi:10.1021/es801113k

    Article  CAS  PubMed  Google Scholar 

  • Larned ST, Suren AM, Flanagan M, Biggs BJF, Riis T (2006) Macrophytes in urban stream rehabilitation: establishment, ecological effects, and public perception. Restor Ecol 14(3):429–440. doi:10.1111/j.1526-100X.2006.00151.x

    Article  Google Scholar 

  • Madsen TV, Cedergreen N (2002) Sources of nutrients to rooted submerged macrophytes growing in a nutrient-rich stream. Freshw Biol 47(2):283–291. doi:10.1046/j.1365-2427.2002.00802.x

    Article  Google Scholar 

  • Marion L, Paillisson JM (2003) A mass balance assessment of the contribution of floating-leaved macrophytes in nutrient stocks in an eutrophic macrophyte-dominated lake. Aquat Bot 75(3):249–260. doi:10.1016/s0304-3770(02)00177-8

    Article  Google Scholar 

  • Mariotti A, Germon JC, Leclerc A (1982) Nitrogen isotope fractionation associated with the NO2–N2O step of denitrification in soils. Can J Soil Sci 62(2):227–241

    Article  CAS  Google Scholar 

  • Marti E, Aumatell J, Gode L, Poch M, Sabater F (2004) Nutrient retention efficiency in streams receiving inputs from wastewater treatment plants. J Environ Qual 33(1):285–293

    Article  CAS  PubMed  Google Scholar 

  • Melzer A (1999) Aquatic macrophytes as tools for lake management. Hydrobiologia 395:181–190

    Article  Google Scholar 

  • Merbt SN, Auguet JC, Casamayor EO, Marti E (2011) Biofilm recovery in a wastewater treatment plant-influenced stream and spatial segregation of ammonia-oxidizing microbial populations. Limnol Oceanogr 56:1054–1064

    Article  CAS  Google Scholar 

  • Merseburger GC, Marti E, Sabater F (2005) Net changes in nutrient concentrations below a point source input in two streams draining catchments with contrasting land uses. Sci Total Environ 347(1–3):217–229. doi:10.1016/j.scitotenv.2004.12.022

    Article  CAS  PubMed  Google Scholar 

  • Nichols DS, Keeney DR (1976) Nitrogen nutrition of myriophyllum spicatum—uptake and translocation of N-15 by shoots and roots. Freshw Biol 6(2):145–154. doi:10.1111/j.1365-2427.1976.tb01598.x

    Article  CAS  Google Scholar 

  • O’Brien JM, Dodds WK, Wilson KC, Murdock JN, Eichmiller J (2007) The saturation of N cycling in central plains streams: N-15 experiments across a broad gradient of nitrate concentrations. Biogeochemistry 84(1):31–49. doi:10.1007/s10533-007-9073-7

    Article  Google Scholar 

  • Pastor A, Peipoch M, Canas L, Chappuis E, Ribot M, Gacia E, Riera JLL, Marti E, Sabater F (2013) Nitrogen stable isotopes in primary utake compartments across streams differing in nutrient availability. Environ Sci Technol. doi:10.1021/es400726e

  • Peipoch M, Marti E, Gacia E (2012) Variability in delta N-15 natural abundance of basal resources in fluvial ecosystems: a meta-analysis. Freshw Sci 31(3):1003–1015. doi:10.1899/11-157.1

    Article  Google Scholar 

  • Pelton DK, Levine SN, Braner M (1998) Measurements of phosphorus uptake by macrophytes and epiphytes from the LaPlatte river (VT) using P-32 in stream microcosms. Freshw Biol 39(2):285–299. doi:10.1046/j.1365-2427.1998.00281.x

    Article  Google Scholar 

  • Ribot M, Marti E, Von Schiller D, Sabater F, Daims H, Battin TJ (2012) Nitrogen processing and the role of epilithic biofilms downstream of a wastewater treatment plant. Freshw Sci 31(4):1057–1069

    Article  Google Scholar 

  • Riis T, Biggs BJF (2003) Hydrologic and hydraulic control of macrophyte establishment and performance in streams. Limnol Oceanogr 48(4):1488–1497

    Article  Google Scholar 

  • Riis T, Dodds WK, Kristensen PB, Baisner AJ (2012) Nitrogen cycling and dynamics in a macrophyte-rich stream as determined by a N15-NH4+ release. Freshw Biol 57(8):1579–1591. doi:10.1111/j.1365-2427.2012.02819.x

    Article  CAS  Google Scholar 

  • Sand-Jensen K, Mebus JR (1996) Fine-scale patterns of water velocity within macrophyte patches in streams. Oikos 76(1):169–180. doi:10.2307/3545759

    Article  Google Scholar 

  • Sand-Jensen K, Pedersen O (1999) Velocity gradients and turbulence around macrophyte stands in streams. Freshw Biol 42(2):315–328. doi:10.1046/j.1365-2427.1999.444495.x

    Article  Google Scholar 

  • Schulz M, Kozerski HP, Pluntke T, Rinke K (2003) The influence of macrophytes on sedimentation and nutrient retention in the lower River Spree (Germany). Water Res 37(3):569–578. doi:10.1016/s0043-1354(02)00276-2

    Article  CAS  PubMed  Google Scholar 

  • Sigman DM, Altabet MA, Michener R, McCorkle DC, Fry B, Holmes RM (1997) Natural abundance-level measurement of the nitrogen isotopic composition of oceanic nitrate: an adaptation of the ammonia diffusion method. Mar Chem 57(3–4):227–242. doi:10.1016/s0304-4203(97)00009-1

    Article  CAS  Google Scholar 

  • Simon KS, Niyogi DK, Frew RD, Townsend CR (2007) Nitrogen dynamics in grassland streams along a gradient of agricultural development. Limnol Oceanogr 52(3):1246–1257

    Article  CAS  Google Scholar 

  • Suren AM (2009) Using macrophytes in urban stream rehabilitation: a cautionary tale. Restor Ecol 17(6):873–883. doi:10.1111/j.1526-100X.2008.00446.x

    Article  Google Scholar 

  • Svendsen LM, Kronvang B (1993) Retention of nitrogen and phosphorous in a Danish lowland river system: implications for the export from the watrershed. Hydrobiologia 251:123–135

    Article  CAS  Google Scholar 

  • Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sunderland (USA)

  • Toda H, Uemura Y, Okino T, Kawanishi T, Kawashima H (2001) Use of nitrogen stable isotope ratio of periphyton for monitoring nitrogen sources in a river system. In: IWA Asia-Pacific regional conference, Fukuoka, Japan, Sep 12–15 2001. I W a Publishing, pp 431–435

  • Udy JW, Fellows CS, Bartkow ME, Bunn SE, Clapcott JE, Harch BD (2006) Measures of nutrient processes as indicators of stream ecosystem health. Hydrobiologia 572:89–102

    Article  CAS  Google Scholar 

  • Von Schiller D, Marti E, Riera JL, Ribot M, Argerich A, Fonolla P, Sabater F (2008) Inter-annual, annual, and seasonal variation of P and N retention in a perennial and an intermittent stream. Ecosystems 11(5):670–687. doi:10.1007/s10021-008-9150-3

    Article  Google Scholar 

  • Von Schiller D, Marti E, Riera JL (2009) Nitrate retention and removal in Mediterranean streams bordered by contrasting land uses: a N-15 tracer study. Biogeosciences 6(2):181–196

    Article  Google Scholar 

  • Yoneyama T, Matsumaru T, Usui K, Engelaar WMHG (2001) Discrimantion of nitrogen isotopes during absorption of ammonium and nitrate at different nitrogen concentrations by rice (oryza sativa L.) plants. Plant Cell Environ 24:131–139

    Article  Google Scholar 

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Acknowledgments

The authors would like to thank the town council of Santa Maria de Palautordera for granting access to the field location, and the Institute of Marine Sciences (ICM-CSIC) for the nutrient samples analysis. We also thank two anonymous reviewers for their useful comments and suggestions on the manuscript. Financial support was provided by the Spanish Ministry of Science and Innovation through the ISONEF (ref: CGL2008-05504-C02-02/BOS) and MED_FORESTREAM (ref: CGL2011-30590-C02-02) projects and by the European Science Foundation project COMIX (EuroDiversity Collaborative Research program, ref: 05_EDIV_FP065-COMIX). M. Peipoch and M. Ribot were funded through a FPI PhD fellowship and a technical training contract, respectively, from the Spanish Ministry of Science and Innovation through the ISONEF project. A. Blesa was granted a FPI PhD fellowship associated to grant BIO2010-18875 from the Spanish Ministry of Science and Innovation.

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  1. Integrative Freshwater Ecology Group, Centre d’Estudis Avançats de Blanes, Consejo Superior de Investigaciones Científicas (CEAB-CSIC), Accés a la Cala Sant Francesc 14, 17300, Blanes, Girona, Spain

    Marc Peipoch, Esperança Gacia, Miquel Ribot & Eugènia Martí

  2. Consejo Superior de Investigaciones Científicas. Center of Molecular Biology “Severo Ochoa”, Autonomous University of Madrid, C/Nicolás Cabrera 1, Campus de la Universidad Autónoma de Madrid, 28049, Madrid, Spain

    Alba Blesa

  3. Department of Ecology, University of Barcelona (UB), Diagonal 643, 08028, Barcelona, Spain

    Joan L. Riera

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  1. Marc Peipoch
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  2. Esperança Gacia
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  3. Alba Blesa
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Correspondence to Marc Peipoch.

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Peipoch, M., Gacia, E., Blesa, A. et al. Contrasts among macrophyte riparian species in their use of stream water nitrate and ammonium: insights from 15N natural abundance. Aquat Sci 76, 203–215 (2014). https://doi.org/10.1007/s00027-013-0330-7

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  • DOI: https://doi.org/10.1007/s00027-013-0330-7

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