Skip to main content
SpringerLink
Log in

Biofilm growth and nitrogen uptake responses to increases in nitrate and ammonium availability

  • Research Article
  • Published:
Aquatic Sciences Aims and scope Submit manuscript

Abstract

Nitrate (NO3 −) and ammonium (NH4 +) are the two major dissolved inorganic nitrogen (DIN) species available in streams. Human activities increase stream DIN concentrations and modify the NO3 −:NH4 + ratio. However, few studies have examined biofilm responses to enrichment of both DIN species. We examined biofilm responses to variation in ambient concentrations and enrichments in either NO3 − or NH4 +. We incubated nutrient diffusing substrata (NDS) bioassays with three treatments (DIN-free, +NO3 − and +NH4 +) in five streams. Biomass-specific uptake rates (U spec ) of NO3 − and NH4 + were then measured using in situ additions of 15N-labeled NO3 − and NH4 +. Biomass (estimated from changes in carbon content) and algal accrual rates, as well as U spec -NO3 − of biofilms in DIN-free treatments varied among the streams in which the NDS had been incubated. Higher ambient DIN concentrations were only correlated with enhanced biofilm growth rates. U spec -NO3 − was one order of magnitude greater and more variable than U spec -NH4 +, however similar relative preference index (RPI) suggested that biofilms did not show a clear preference for either DIN species. Biofilm growth and DIN uptake in DIN-amended NDS (i.e., +NO3 − and +NH4 +) were consistently lower than in DIN-free NDS (i.e., control). Lower values in controls with respect to amended NDS were consistently more pronounced for algal accrual rates and U spec -NO3 − and for the +NH4 + than for the +NO3 − treatments. In particular, enrichment with NH4 + reduced biofilm U spec -NO3 − uptake, which has important implications for N cycling in high NH4 + streams.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

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

  • Battin TJ, Kaplan LA, Newbold JD, Hansen CME (2003) Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426:439–442. doi:10.1038/nature02152

    Article  CAS  PubMed  Google Scholar 

  • Bechtold HA, Marcarelli AM, Baxter CV, Inouye RS (2012) Effects of N, P, and organic carbon on stream biofilm nutrient limitation and uptake in a semi-arid watershed. Limnol Oceanogr 57:1544–1554. doi:10.4319/lo.2012.57.5.1544

    Article  CAS  Google Scholar 

  • Bernhardt ES, Likens GE (2004) Controls on periphyton biomass in heterotrophic streams. Freshw Biol 49:14–27. doi:10.1046/j.1365-2426.2003.01161.x

    Article  Google Scholar 

  • Bernhardt ES, Hall RO, Likens GE (2002) Whole-system estimates of nitrification and nitrate uptake in streams of the Hubbard Brook Experimental Forest. Ecosystems 5:419–430. doi:10.1007/s10021-002-0179-4

    Article  CAS  Google Scholar 

  • Bernot MJ, Tank JL, Royer TV, David MB (2006) Nutrient uptake in streams draining agricultural catchments of the midwestern United States. Freshw Biol 51:499–509. doi:10.1111/j.1365-2427.2006.01508.x

    Article  CAS  Google Scholar 

  • Bunch ND, Bernot MJ (2012) Nitrate and ammonium uptake by natural stream sediment microbial communities in response to nutrient enrichment. Res Microbiol 163:137–141. doi:10.1016/j.resmic.2011.11.004

    Article  CAS  PubMed  Google Scholar 

  • Camargo JA, Alonso A (2006) Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environ Int 32:831–849. doi:10.1016/j.envint.2006.05.002

    Article  CAS  PubMed  Google Scholar 

  • Dodds WK, Welch EB (2000) Establishing nutrient criteria in streams. J N Am Benthol Soc 19:186–196

    Article  Google Scholar 

  • Dodds WK, Lopez AJ, Bowden WB, Gregory S, Grimm NB, Hamilton SK, Hershey AE, Marti E, Mcdowell WH, Meyer JL, Morrall D, Mulholland PJ, Peterson BJ, Tank JL, Valett HM, Webster JR, Wollheim W (2002) N uptake as a function of concentration in streams. J N Am Benthol Soc 21:206–220

    Article  Google Scholar 

  • Dodds WK, Marti E, Tank JL, Pontius J, Hamilton SK, Grimm NB, Bowden WB, Mcdowell WH, Peterson BJ, Valett HM, Webster JR, Gregory S (2004) Carbon and nitrogen stoichiometry and nitrogen cycling rates in streams. Oecologia 140:458–467. doi:10.1007/s00442-004-1599-y

    Article  PubMed  Google Scholar 

  • Domingues RB, Barbosa AB, Sommer U, Galvao HM (2011) Ammonium, nitrate and phytoplankton interactions in a freshwater tidal estuarine zone: potential effects of cultural eutrophication. Aquat Sci 73:331–343. doi:10.1007/s00027-011-0180-0

    Article  CAS  Google Scholar 

  • Dortch Q (1990) The interaction between ammonium and nitrate uptake in phytoplankton. Mar Ecol-Prog Ser 61:183–201. doi:10.3354/meps061183

    Article  CAS  Google Scholar 

  • Dugdale RC, Wilkerson FP, Hogue VE, Marchi A (2007) The role of ammonium and nitrate in spring bloom development in San Francisco Bay Estuar. Coast Shelf Sci 73:17–29. doi:10.1016/j.ecss.2006.12.008

    Article  Google Scholar 

  • Fellows CS, Valett HM, Dahm CN, Mulholland PJ, Thomas SA (2006) Coupling nutrient uptake and energy flow in headwater streams. Ecosystems 9:788–804. doi:10.1007/s10021-006-0005-5

    Article  CAS  Google Scholar 

  • Francoeur SN (2001) Meta-analysis of lotic nutrient amendment experiments: detecting and quantifying subtle responses. J N Am Benthol Soc 20:358–368. doi:10.2307/1468034

    Article  Google Scholar 

  • Geisseler D, Horwath WR, Joergensen RG, Ludwig B (2010) Pathways of nitrogen utilization by soil microorganisms—a review. Soil Biol Biochem 42:2058–2067. doi:10.1016/j.soilbio.2010.08.021

    Article  CAS  Google Scholar 

  • Gonzalez PJ, Correia C, Moura I, Brondino CD, Moura JJG (2006) Bacterial nitrate reductases: molecular and biological aspects of nitrate reduction. J Inorg Biochem 100:1015–1023. doi:10.1016/j.jinorgbio.2005.11.024

    Article  CAS  PubMed  Google Scholar 

  • Gordon ND, McMahon TA, Finlayson BL (1992) Stream hydrology: an introduction for ecologists. Wiley, New York

    Google Scholar 

  • Hill WR, Ryon MG, Schilling EM (1995) Light limitation in a stream ecosystem - responses by primary producers and consumers. Ecology 76:1297–1309. doi:10.2307/1940936

    Article  Google Scholar 

  • Hoellein TJ, Tank JL, Kelly JJ, Rosi-Marshall EJ (2010) Seasonal variation in nutrient limitation of microbial biofilms colonizing organic and inorganic substrata in streams. Hydrobiologia 649:331–345. doi:10.1007/s10750-010-0276-x

    Article  CAS  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. Marine Chem 60:235–243

    Article  CAS  Google Scholar 

  • Johnson LT, Tank JL, Dodds WK (2009) The influence of land use on stream biofilm nutrient limitation across eight North American ecoregions. Can J Fish Aquat Sci 66:1081–1094. doi:10.1139/f09-065

    Article  CAS  Google Scholar 

  • Keck F, Lepori F (2012) Can we predict nutrient limitation in streams and rivers? Freshw Biol 57:1410–1421. doi:10.1111/j.1365-2427.2012.02802.x

    Article  CAS  Google Scholar 

  • Kemp MJ, Dodds WK (2002) 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

    Article  CAS  Google Scholar 

  • King SA, Heffernan JB, Cohen MJ (2014) Nutrient flux, uptake, and autotrophic limitation in streams and rivers. Freshw Sci 33:85–98. doi:10.1086/674383

    Article  Google Scholar 

  • Lassaletta L, Garcia-Gomez H, Gimeno BS, Rovira JV (2009) Agriculture-induced increase in nitrate concentrations in stream waters of a large Mediterranean catchment over 25 years (1981–2005). Sci Total Environ 407:6034–6043. doi:10.1016/j.scitotenv.2009.08.002

    Article  CAS  PubMed  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 33:285–293

    Article  CAS  PubMed  Google Scholar 

  • Martí E, Riera J, Sabater F (2010) Effects of wastewater treatment plants on stream nutrient dynamics under water scarcity conditions. In: Sabater S, Barceló D (eds) Water scarcity in the mediterranean, vol 8. The handbook of environmental chemistry. Springer, Berlin, Heidelberg, pp 173–195. doi:10.1007/698_2009_33

    Google Scholar 

  • McCarty GW (1995) The role of glutamine-synthetase in regulation of nitrogen-metabolism within the soil microbial community. Plant Soil 170:141–147. doi:10.1007/bf02183062

    Article  CAS  Google Scholar 

  • McIntire CD, Gregory SV, Steinman AD, Lamberti GA (1996) Modeling benthic algal communities: an example from stream ecology. Algal Ecol Freshw Benthic Ecosyst. doi:10.1016/b978-012668450-6/50050-3

    Google Scholar 

  • Merbt S, Auguet J-C, Blesa A, Martí E, Casamayor E (2015) Wastewater treatment plant effluents change abundance and composition of ammonia-oxidizing microorganisms in mediterranean urban stream biofilms. Microb Ecol 69:66–74. doi:10.1007/s00248-014-0464-8

    Article  CAS  PubMed  Google Scholar 

  • Naldi M, Wheeler PA (2002) N-15 measurements of ammonium and nitrate uptake by Ulva fenestrata (chlorophyta) and Gracilaria pacifica (rhodophyta): comparison of net nutrient disappearance, release of ammonium and nitrate, and N-15 accumulation in algal tissue. J Phycol 38:135–144. doi:10.1046/j.1529-8817.2002.01070.x

    Article  Google Scholar 

  • Newbold JD, Bott TL, Kaplan LA, Dow CL, Jackson JK, Aufdenkampe AK, Martin LA, Van Horn DJ, De Long AA (2006) Uptake of nutrients and organic C in streams in New York City drinking-water-supply watersheds. J N Am Benthol Soc 25:998–1017

    Article  Google Scholar 

  • O’Brien JM, Dodds WK (2008) Ammonium uptake and mineralization in prairie streams: chamber incubation and short-term nutrient addition experiments. Freshw Biol 53:102–112. doi:10.1111/j.1365-2427.2007.01870.x

    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 84:31–49. doi:10.1007/s10533-007-9073-7

    Article  Google Scholar 

  • Pusch M et al (1998) The role of micro-organisms in the ecological connectivity of running waters. Freshw Biol 40:453–495. doi:10.1046/j.1365-2427.1998.00372.x

    Article  Google Scholar 

  • Ribot M, von Schiller D, Peipoch M, Sabater F, Grimm NB, Marti E (2013) Influence of nitrate and ammonium availability on uptake kinetics of stream biofilms. Freshw Sci 32:1155–1167. doi:10.1899/12-209.1

    Article  Google Scholar 

  • Risgaard-Petersen N, Nicolaisen MH, Revsbech NP, Lomstein BA (2004) Competition between ammonia-oxidizing bacteria and benthic microalgae. Appl Environ Microbiol 70:5528–5537. doi:10.1128/aem.70.9.5528-5537.2004

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sabater F, Butturini A, Marti E, Munoz I, Romani A, Wray J, Sabater S (2000) Effects of riparian vegetation removal on nutrient retention in a Mediterranean stream. J N Am Benthol Soc 19:609–620. doi:10.2307/1468120

    Article  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. Marine Chem 57:227–242

    Article  CAS  Google Scholar 

  • Stanley EH, Maxted JT (2008) Changes in the dissolved nitrogen pool across land cover gradients in Wisconsin streams. Ecol Appl 18:1579–1590. doi:10.1890/07-1379.1

    Article  PubMed  Google Scholar 

  • Steinman AD (1996) Effects of grazers on freshwater benthic algae. Algal Ecol Freshw Benthic Ecosyst. doi:10.1016/b978-012668450-6/50041-2

    Google Scholar 

  • Tank JL, Dodds WK (2003) Nutrient limitation of epilithic and epixylic biofilms in ten North American streams. Freshw Biol 48:1031–1049. doi:10.1046/j.1365-2427.2003.01067.x

    Article  CAS  Google Scholar 

  • von Schiller D, Marti E, Riera JL, Sabater F (2007) Effects of nutrients and light on periphyton biomass and nitrogen uptake in Mediterranean streams with contrasting land uses. Freshw Biol 52:891–906. doi:10.1111/j.1365-2427.2007.01742.x

    Article  Google Scholar 

  • von Schiller D, Marti E, Riera JL, Ribot M, Marks JC, Sabater F (2008) Influence of land use on stream ecosystem function in a Mediterranean catchment. Freshw Biol 53:2600–2612. doi:10.1111/j.1365-2427.2008.02059.x

    Article  Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice-Hall, Upper Saddle River

    Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R (Statistics for biology and health). Springer Science + Business Media, LLC2009

Download references

Acknowledgments

We thank M. Martí and S. Pla for their field and laboratory assistance. We are also grateful to the to the Font del Regàs landowners, Massaneda Garden and the Direcció del Parc Natural del Montseny (Diputació de Barcelona) for allowing access to the study sites during the experiments. This study was funded by the Spanish Ministry of Education and Science through NICON project (ref: CGL2005-7362). MR was supported by a contract with the Spanish Ministry of Science and Innovation through the MED_FORSTREAM project (CGL2011-30590-C02-02). DvS’s work was also funded by a Juan de la Cierva postdoctoral contract (JCI-2010-06397) from the Spanish Ministry of Science and Innovation.

Author information

Authors and Affiliations

  1. Integrative Freshwater Ecology Group, Centre d’Estudis Avançats de Blanes (CEAB-CSIC), Accés a la Cala St. Francesc 14, 17300, Blanes, Spain

    Miquel Ribot & Eugènia Martí

  2. Faculty of Science and Technology, University of the Basque Country, PO Box 644, 48080, Bilbao, Spain

    Daniel von Schiller

  3. Department of Ecology, Faculty of Biology, University of Barcelona, Avinguda Diagonal 645, 08028, Barcelona, Spain

    Francesc Sabater

Authors
  1. Miquel Ribot
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel von Schiller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francesc Sabater
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eugènia Martí
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Miquel Ribot.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ribot, M., von Schiller, D., Sabater, F. et al. Biofilm growth and nitrogen uptake responses to increases in nitrate and ammonium availability. Aquat Sci 77, 695–707 (2015). https://doi.org/10.1007/s00027-015-0412-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00027-015-0412-9

Keywords

Search

Navigation