Skip to main content
SpringerLink
Log in

Macroalgae mitigation potential for fish aquaculture effluents: an approach coupling nitrogen uptake and metabolic pathways using Ulva rigida and Enteromorpha clathrata

  • Combined effects of Environmental Stressors in the Aquatic Environment
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Aquaculture effluents are rich in nitrogen compounds that may enhance local primary productivity, leading to the development of algae blooms. The goal of this study was to assess the potential use of naturally occurring green macroalgae (Ulva and Enteromorpha) as bioremediators for nitrogen-rich effluents from a fish aquaculture plant, by evaluating their respective uptake dynamics under controlled conditions. Ulva and Enteromorpha were incubated separately in aquaculture effluent from a local pilot station. Algae tissue and water samples were collected periodically along 4 h. For each sample, nitrate, nitrite, and ammonia concentrations were quantified in the effluent, while internal algae reserve pools and nitrate reductase activity (NRA) were determined within the algae tissues. Both macroalgae absorbed all dissolved inorganic nitrogen compounds in less than 1 h, favoring ammonia over nitrate. Ulva stored nitrate temporarily as an internal reserve and only used it after ammonia availability decreased, whereas Enteromorpha stored and metabolized ammonia and nitrate simultaneously. These distinct dynamics of ammonia and nitrate uptake supported an increase in NRA during the experiment. This study supports the hypothesis that Ulva or Enteromorpha can be used as bioremediators in aquaculture effluents to mitigate excess of dissolved inorganic nitrogen.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abreu MH, Pereira R, Buschmann AH, Sousa-Pinto I, Yarish C (2011) Nitrogen uptake responses of Gracilaria vermiculophylla (Ohmi) Papenfuss under combined and single addition of nitrate and ammonium. J Exp Mar Biol Ecol 407:190–199. doi:10.1016/j.jembe.2011.06.034

    Article  CAS  Google Scholar 

  • Aníbal J, Rocha C, Sprung M (2007) Mudflat surface morphology as a structuring agent of algae and associated macroepifauna communities: a case study in Ria Formosa. J Sea Res 57:36–46. doi:10.1016/j.seares.2006.07.002

    Article  Google Scholar 

  • Barsanti L, Gualtieri P (2006) Algae: anatomy, biochemistry, and biotechnology. CRC Press, Boca Raton

    Google Scholar 

  • Berges JA (1997) Miniview: algal nitrate reductases. Eur J Phycol 32:3–8. doi:10.1080/09541449710001719315

    Article  Google Scholar 

  • Bird KT, Habig C, DeBusk T (1982) Nitrogen allocation and storage patterns in Gracilaria tikvahiae (Rhodophyta). J Phycol 18:344–348. doi:10.1111/j.1529-8817.1982.tb03194.x

    Article  CAS  Google Scholar 

  • Cabello-Pasini A, Macías-Carranza V, Abdala R, Korbee N, Figueroa FL (2010) Effect of nitrate concentration and UVR on photosynthesis, respiration, nitrate reductase activity, and phenolic compounds in Ulva rigida (Chlorophyta). J Appl Phycol 23:363–369. doi:10.1007/s10811-010-9548-0

    Article  Google Scholar 

  • Cardinale BJ (2011) Biodiversity improves water quality through niche partitioning. Nature 472:86–89. doi:10.1038/nature09904

    Article  CAS  Google Scholar 

  • Cohen RA, Fong P (2005) Experimental evidence supports the use of δ15N content of the opportunistic green macroalga Enteromorpha intestinalis (Chlorophyta) to determine nitrogen sources to estuaries. J Phycol 41:287–293. doi:10.1111/j.1529-8817.2005.04022.x

    Article  CAS  Google Scholar 

  • Chow F, de Oliveira MC, Pedersén M (2004) In vitro assay and light regulation of nitrate reductase in red alga Gracilaria chilensis. J Plant Physiol 161:769–776. doi:10.1016/j.jplph.2004.01.002

    Article  CAS  Google Scholar 

  • Corzo A, Niell FX (1991) Determination of nitrate reductase activity in Ulva rigida C Agardh by the in situ method. J Exp Mar Biol Ecol 146:181–191. doi:10.1016/0022-0981(91)90024-Q

    Article  CAS  Google Scholar 

  • Corzo A, Niell FX (1994) Nitrate-reductase activity and in vivo nitrate-reduction rate in Ulva rigida illuminated by blue light. Mar Biol 120:17–23

    CAS  Google Scholar 

  • Cruz-Suárez LE, León A, Peña-Rodríguez A, Rodríguez-Peña G, Moll B, Ricque-Marie D (2010) Shrimp/Ulva co-culture: a sustainable alternative to diminish the need for artificial feed and improve shrimp quality. Aquaculture 301:64–68. doi:10.1016/j.aquaculture.2010.01.021

    Article  Google Scholar 

  • EEA (2010) The European environment: state and outlook 2010—marine and coastal environment. European Environment Agency, Copenhagen

    Google Scholar 

  • Fei X (2004) Solving the coastal eutrophication problem by large scale seaweed cultivation. Hydrobiologia 512:145–151. doi:10.1023/B:HYDR.0000020320.68331.ce

    Article  Google Scholar 

  • Grasshoff K, Ehrhardt M, Kremling K (1983) Methods of seawater analysis. Chemie, Weinheim

    Google Scholar 

  • Hayden HS, Blomster J, Maggs CA, Silva PC, Stanhope MJ, Waaland JR (2003) Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur J Phycol 38:277–294. doi:10.1080/1364253031000136321

    Article  Google Scholar 

  • He P, Xu S, Zhang H, Wen S, Dai Y, Lin S, Yarish C (2008) Bioremediation efficiency in the removal of dissolved inorganic nutrients by the red seaweed, Porphyra yezoensis, cultivated in the open sea. Water Res 42:1281–1289. doi:10.1016/j.watres.2007.09.023

    Article  CAS  Google Scholar 

  • Hernández I, Tovar A, Vergara JJ (2002) Biofiltering efficiency in removal of dissolved nutrients by three species of estuarine macroalgae cultivated with sea bass (Dicentrarchus labrax) waste waters 2. Ammonium J App Phycol 14:375–384

    Article  Google Scholar 

  • Hong HS, Wang YJ, Wang DZ (2011) Response of phytoplankton to nitrogen addition in the Taiwan strait upwelling region: nitrate reductase and glutamine synthetase activities. Cont Shelf Res 31:S57–S66. doi:10.1016/j.csr.2011.01.018

    Article  Google Scholar 

  • Huo Y, Wu H, Chai Z, Xu S, Han F, Dong L, He P (2012) Bioremediation efficiency of Gracilaria verrucosa for an integrated multi-trophic aquaculture system with Pseudosciaena crocea in Xiangshan harbor, China. Aquaculture 326–329:99–105. doi:10.1016/j.aquaculture.2011.11.002

    Article  Google Scholar 

  • Hurd CL, Berges JA, Osborne J, Harrison PJ (1995) An in vitro nitrate reductase assay for marine macroalgae: optimization and characterization of the enzyme for Fucus gardneri (phaeophyta). J Phycol 31:835–843. doi:10.1111/j.0022-3646.1995.00835.x

    Article  CAS  Google Scholar 

  • Jiménez del Río M, Ramazanov Z, García-Reina G (1996) Ulva rigida (Ulvales, Chlorophyta) tank culture as biofilters for dissolved inorganic nitrogen from fishpond effluents. Hydrobiologia 326(327):61–66. doi:10.1007/BF00047787

    Article  Google Scholar 

  • Jones AB, Dennison WC, Preston NP (2001) Integrated treatment of shrimp effluent by sedimentation, oyster filtration and macroalgal absorption: a laboratory scale study. Aquaculture 193:155–178. doi:10.1016/S0044-8486(00)00486-5

    Article  Google Scholar 

  • Kang YH, Park SR, Chung IK (2011) Biofiltration efficiency and biochemical composition of three seaweed species cultivated in a fish-seaweed integrated culture. Algae 26:97–108. doi:10.4490/algae.2011.26.1.097

    Article  Google Scholar 

  • Kim JK, Kraemer GP, Neefus CD, Chung IK, Yarish C (2007) Effects of temperature and ammonium on growth, pigment production and nitrogen uptake by four species of Porphyra (Bangiales, Rhodophyta) native to the New England coast. J Appl Phycol 19:431–440. doi:10.1007/s10811-006-9150-7

    Article  CAS  Google Scholar 

  • Lartigue J, Sherman TD (2002) Field assays for measuring nitrate reductase activity in Enteromorpha sp. J Phycol 38:971–982. doi:10.1046/j.1529-8817.2002.t01-2-01193.x

    Article  CAS  Google Scholar 

  • Lartigue J, Sherman TD (2005) Response of Enteromorpha sp. (Chlorophyceae) to a nitrate pulse: nitrate uptake, inorganic nitrogen storage and nitrate reductase activity. Mar Ecol Prog Ser 292:147–157. doi:10.3354/meps292147

    Article  CAS  Google Scholar 

  • Liu J, Wang Z, Lin W (2010) De-eutrophication of effluent wastewater from fish aquaculture by using marine green alga Ulva pertusa. Chin J Oceanol Limnol 28:201–208. doi:10.1007/s00343-010-9245-5

    Article  CAS  Google Scholar 

  • Lobban CS, Harrison PJ (1997) Seaweed ecology and physiology. Cambridge University Press, New York

    Google Scholar 

  • Luo MB, Liu F, Xu ZL (2012) Growth and nutrient uptake capacity of two co-occurring species, Ulva prolifera and Ulva linza. Aquat Bot 100:18–24. doi:10.1016/j.aquabot.2012.03.006

    Article  CAS  Google Scholar 

  • Marinho-Soriano E, Nunes SO, Carneiro MAA, Pereira DC (2009a) Nutrients’ removal from aquaculture wastewater using the macroalgae Gracilaria birdiae. Biomass Bioenergy 33:327–331. doi:10.1016/j.biombioe.2008.07.002

    Article  CAS  Google Scholar 

  • Marinho-Soriano E, Panucci RA, Carneiro MAA, Pereira DC (2009b) Evaluation of Gracilaria caudata J. Agardh for bioremediation of nutrients from shrimp farming wastewater. Bioresour Technol 100:6192–6198

    Article  CAS  Google Scholar 

  • Marinho-Soriano E, Azevedo CAA, Trigueiro TG, Pereira DC, Carneiro MAA, Camara MR (2011) Bioremediation of aquaculture wastewater using macroalgae and Artemia. Int Biodeterior Biodegrad 65:253–257. doi:10.1016/j.biortech.2009.06.102

    Article  CAS  Google Scholar 

  • Naldi M, Wheeler PA (2002) 15N 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 15N accumulation in algal tissue. J Phycol 38:135–144. doi:10.1046/j.1529-8817.2002.01070.x

    Article  Google Scholar 

  • de Paula Silva PH, McBride S, de Nys R, Paul NA (2008) Integrating filamentous “green tide” algae into tropical pond-based aquaculture. Aquaculture 284:74–80. doi:10.1016/j.aquaculture.2008.07.035

    Article  Google Scholar 

  • Pregnall AM, Smith RD, Alberte RS (1987) Glutamine synthetase activity and free amino acid pools of eelgrass (Zostera marina L.) roots. J Exp Mar Biol Ecol 106:211–228. doi:10.1016/0022-0981(87)90094-3

    Article  CAS  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Ritz C, Streibig JC (2008) Nonlinear regression with R. Springer, New York

    Google Scholar 

  • Skriptsova AV, Miroshnikova NV (2011) Laboratory experiment to determine the potential of two macroalgae from the Russian Far-East as biofilters for integrated multi-trophic aquaculture (IMTA). Bioresour Technol 102:3149–3154. doi:10.1016/j.biortech.2010.10.093

    Article  CAS  Google Scholar 

  • Teichberg M, Heffner LR, Fox S, Valiela I (2007) Nitrate reductase and glutamine synthetase activity, internal N pools, and growth of Ulva lactuca: responses to long and short-term N supply. Mar Biol 151:1249–1259. doi:10.1007/s00227-006-0561-4

    Article  CAS  Google Scholar 

  • Thomas TE, Harrison PJ (1985) Effect of nitrogen supply on nitrogen uptake, accumulation and assimilation in Porphyra perforata (Rhodophyta). Mar Biol 85:269–278. doi:10.1007/BF00393247

    Article  CAS  Google Scholar 

  • Thompson SM, Valiela I (1999) Effect of nitrogen loading on enzyme activity of macroalgae in estuaries in Waquoit Bay. Bot Mar 42:519–529

    Article  CAS  Google Scholar 

  • Troell M, Halling C, Nilsson A, Buschmann AH, Kautsky N, Kautsky L (1997) Integrated marine cultivation of Gracilaria chilensis (Gracilariales, Rhodophyta) and salmon cages for reduced environmental impact and increased economic output. Aquaculture 156:45–61. doi:10.1016/S0044-8486(97)00080-X

    Article  Google Scholar 

  • Xu D, Gao Z, Zhang X, Qi Z, Meng C, Zhuang Z, Ye N (2011) Evaluation of the potential role of the macroalga Laminaria japonica for alleviating coastal eutrophication. Bioresour Technol 102:9912–9918. doi:10.1016/j.biortech.2011.08.035

    Article  CAS  Google Scholar 

  • Yokoyama H, Ishihi Y (2010) Bioindicator and biofilter function of Ulva spp. (Chlorophyta) for dissolved inorganic nitrogen discharged from a coastal fish farm—potential role in integrated multi-trophic aquaculture. Aquaculture 310:74–83. doi:10.1016/j.aquaculture.2010.10.018

    Article  CAS  Google Scholar 

  • Young EB, Berges JA, Dring MJ (2009) Physiological responses of intertidal marine brown algae to nitrogen deprivation and resupply of nitrate and ammonium. Physiol Plant 135:400–411. doi:10.1111/j.1399-3054.2008.01199.x

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The research leading to these results was primarily funded by the project NITROLINKS–NITROgen loading into the Ria Formosa through Coastal Groundwater Discharge (CGD)—pathways, turnover and LINKS between land and sea in the Coastal Zone (PTDC/MAR/70247/2006) financed by the Portuguese Foundation for Science and Technology (FCT). This research was also partially supported by the European Regional Development Fund (ERDF) through the COMPETE-Operational Competitiveness Programme and national funds through Foundation for Science and Technology (FCT), under the projects “PEst-OE/MAR/UI0350/2011 (CIMA)” and “PEst-C/MAR/LA0015/2011 (CCMAR)”. We also like to thank Dr. Pedro Pousão from EPPO–IPMA for the aquaculture effluents used in the experiments.

Author information

Authors and Affiliations

  1. Centro de Investigação Marinha e Ambiental (CIMA), Universidade do Algarve, Campus de Gambelas, 8005-139, Faro, Portugal

    Jaime Aníbal, Hélder T. Madeira, Liliana F. Carvalho & Cristina Veiga-Pires

  2. Instituto Superior de Engenharia, Universidade do Algarve, Campus da Penha, 8005-139, Faro, Portugal

    Jaime Aníbal, Hélder T. Madeira & Eduardo Esteves

  3. Faculdade de Ciências e Tecnologia, Universidade do Algarve, Campus de Gambelas, 8005-139, Faro, Portugal

    Liliana F. Carvalho & Cristina Veiga-Pires

  4. Centro de Ciências do Mar (CCMAR), Campus de Gambelas, 8005-139, Faro, Portugal

    Eduardo Esteves

  5. Biogeochemistry Research Group, School of Natural Sciences, Trinity College Dublin, Dublin 2, Ireland

    Carlos Rocha

Authors
  1. Jaime Aníbal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hélder T. Madeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liliana F. Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eduardo Esteves
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cristina Veiga-Pires
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Carlos Rocha
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jaime Aníbal.

Additional information

Responsible editor: Hailong Wang

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aníbal, J., Madeira, H.T., Carvalho, L.F. et al. Macroalgae mitigation potential for fish aquaculture effluents: an approach coupling nitrogen uptake and metabolic pathways using Ulva rigida and Enteromorpha clathrata . Environ Sci Pollut Res 21, 13324–13334 (2014). https://doi.org/10.1007/s11356-013-2427-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-2427-x

Keywords

Search

Navigation