Journal of Applied Phycology

, Volume 26, Issue 2, pp 947–955 | Cite as

Nitrogen biofiltration capacities and photosynthetic activity of Pyropia yezoensis Ueda (Bangiales, Rhodophyta): groundwork to validate its potential in integrated multi-trophic aquaculture (IMTA)

  • Yun Hee Kang
  • Sangil Kim
  • Joon-Baek Lee
  • Ik Kyo Chung
  • Sang Rul Park


Porphyra spp. (currently Porphyra and Pyropia) are major sources of seafood globally. In this study, we investigated the effects of ammonium concentration, water temperature, and thallus stocking density on N-ammonium uptake rate (NUR), tissue nutrients content, N–NH4 + filtration efficiency (NUE: nitrogen uptake efficiency %) of Pyropia yezoensis at a laboratory scale and in a mesoscale to evaluate the potential of this species as a biofilter. Additionally, photosynthetic activity was examined using Diving-PAM fluorometer to evaluate the health status. At a laboratory scale, the NUR and tissue nitrogen (N) content of P. yezoensis increased with increasing NH4 + concentrations in the medium. The NUR at thallus stocking densities of 5 and 10 g fresh weight (FW) L–1 were significantly higher than that at 20 g FW L–1. Effective quantum yield (∆ F/F m ) and tissue N content was significantly higher at all stocking densities than that at the beginning of experiment. The NUE was over 90 % at 10 and 17 °C, while all thalli cultured at 25 °C died after 5 days. In a mesoscale, the NUE at a thallus stocking density of 10.0 g FW L–1 was significantly higher than that at a stocking density of 5.0 g FW L–1. No differences in the NUE occurred between 10 °C and 17 °C. Photosynthetic activity (∆F/Fm and rETRmax) of P. yezoensis at optimal culture condition (10–12 °C and 10 g FW L–1) increased over time through the experiment. This indicates that thallus was healthy during culture and chlorophyll a fluorescence can be as a monitoring tool for evaluating the physiological status of seaweeds in an integrated multi-trophic aquaculture.


Nitrogen biofiltration IMTA Pyropia yezoensis Photosynthetic activity Stocking density Temperature 



We would like to thank Dr. M S Hwang for her kind help. This work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT & Future Planning (2012R1A1A1012429), and the Jeju Sea Grant College Program funded by the Ministry of Oceans and Fisheries of Korea.


  1. 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 407:190–199CrossRefGoogle Scholar
  2. Barr NG, Kloeppel A, Rees TAV, Scherer C, Taylor RB, Wenzel A (2008) Wave surge increases rates of growth and nutrient uptake in the green seaweed Ulva pertusa maintained at low bulk flow velocities. Aquat Biol 3:179–186CrossRefGoogle Scholar
  3. Buschmann AH, Troell M, Kautsky N (2001) Integrated algal farming: a review. Cah Biol Mar 42:83–90Google Scholar
  4. Carmona R, Kraemer GP, Yarish C (2006) Exploring Northeast American and Asian species of Porphyra for use in an integrated finfish–alga aquaculture system. Aquaculture 252:54–65CrossRefGoogle Scholar
  5. Chopin T, Yarish C, Wilkes R, Belyea E, Lu S, Mathieson A (1999) Developing Porphyra yezoensis/salmon integrated aquaculture for bioremediation and diversification of the aquaculture industry. J Appl Phycol 11:463–472CrossRefGoogle Scholar
  6. Chopin T, Buschmann AH, Halling C, Troell M, Kautsky N, Neori A, Kraemer GP, Zertuche-González JA, Yarish C, Neefus C (2001) Integrating seaweeds into marine aquaculture systems: a key toward sustainability. J Phycol 37:975–986CrossRefGoogle Scholar
  7. Chung IK, Kang YH, Yarish C, Kraemer GP, Lee JA (2002) Application of seaweed cultivation to the bioremediation of nutrient-rich effluent. Algae 17:187–194CrossRefGoogle Scholar
  8. Durako MJ, Kunzelman JI, Kenworthy WJ, Hammerstrom KK (2003) Depth-related variability in the photobiology of two populations of Halophila johnsonii and Halophila decipiens. Mar Biol 142:1219–1228Google Scholar
  9. Figueroa FL, Santos R, Conde-Álvarez R, Mata L, Gómez-Pinchetti L, Matos J, Huovinen P, Schuenhoff A, Silva J (2006) The use of chlorophyll fluorescence for monitoring photosynthetic condition of two tank-cultivated red macroalgae using fishpond effluents. Bot Mar 49:275–282CrossRefGoogle Scholar
  10. Food and Agriculture Organization of the United Nations (2012) Fisheries and aquaculture statistics 2010. Rome, ItalyGoogle Scholar
  11. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 900:87–92CrossRefGoogle Scholar
  12. Gómez I, Figueroa FL, Sousa-Pinto I, Viñegla B, Pérez-Rodríguez E, Maestre C, Coelho S, Felga A, Pereira R (2001) Effects of UV radiation and temperature on photosynthesis as measured by PAM fluorescence in the red alga Gelidium pulchellum (Turner) Kützing. Bot Mar 44:9–16CrossRefGoogle Scholar
  13. Gómez-Pinchetti JLG, Fernández EC, Díez PM, Reina GG (1998) Nitrogen availability influences the biochemical composition and photosynthesis of tank-cultivated Ulva rigida (Chlorophyta). J Appl Phycol 10:383–389CrossRefGoogle Scholar
  14. Greer DH, Berry JA, Bjorman O (1986) Photoinhibition of photosynthesis in intact bean leaves: role of temperature, and requirement for chloroplast-protein synthesis during recovery. Planta 168:253–260PubMedGoogle Scholar
  15. Hanisak MD, Harlin MM (1978) Uptake of inorganic nitrogen by Codium fragile subsp. tomentosoides (Chlorophyta). J Phycol 14:450–454CrossRefGoogle Scholar
  16. 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 42:1281–1289PubMedCrossRefGoogle Scholar
  17. Henley WJ, Ramus J (1989) Photoacclimation of Ulva rotundata (Chlorophyta) under natural irradiance. Mar Biol 103:261–266CrossRefGoogle Scholar
  18. Hernández I, Fernández-Engo MA, Pérez-Lloréns JL, Vergara JJ (2005) Integrated outdoor culture of two estuarine macroalgae as biofilters for dissolved nutrients from Sparus aurata waste waters. J Appl Phycol 17:557–567CrossRefGoogle Scholar
  19. Hernández I, Pérez-Pastor A, Vergara JJ, Martínez-Aragόn JF, Fernández-Engo MÁ, Pérez-Lloréns L (2006) Studies on the biofiltration capacity of Gracilariopsis longissima: from microscale to macroscale. Aquaculture 252:43–53CrossRefGoogle Scholar
  20. Hitchock GL (1980) Influence of temperature on the growth rate of Skeletonema costatum in response to variations in daily light intensity. Mar Biol 57:261–269CrossRefGoogle Scholar
  21. Kang YH, Shin JA, Kim MS, Chung IK (2008) A preliminary study of the bioremediation potential of Codium fragile applied to seaweed integrated multi-trophic aquaculture (IMTA) during the summer. J Appl Phycol 20:183–190CrossRefGoogle Scholar
  22. Kang YH, Park SR, Oak JH, Seo TH, Shin JA, Chang IK (2009) Physiological responses of Porphyra yezoensis Ueda (Bangiales, Rhodophyta) exposed to high ammonium effluent in a seaweed-based integrated aquaculture system. J Fish Sci Technol 12:70–77CrossRefGoogle Scholar
  23. Kang YH, Park SR, Chung IK (2011) Biofiltration efficiency and biochemical composition of seaweed on intertidal rocky surfaces. Algae 26:97–108CrossRefGoogle Scholar
  24. Kang YH, Hwang JR, Chung IK, Park SR (2013) Development of a seaweed species-selection index for successful culture in a seaweed-based integrated aquaculture system. J Ocean Univ China 12:125–133CrossRefGoogle Scholar
  25. Kim NG, Won YI, Shon CH (1989) Morphology of utricles and maturing period in Codium fragile (Suringar) Hariot. J Aquacult 2:33–41Google Scholar
  26. Kim JG, Karemer 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 19:431–440CrossRefGoogle Scholar
  27. Kraemer GP, Carmona R, Chopin T, Neefus C, Tang X, Yarish C (2004) Evaluation of the bioremediatory potential of several species of the red alga Porphyra using short-term measurements of nitrogen uptake as a rapid bioassay. J Appl Phycol 16:489–497CrossRefGoogle Scholar
  28. Neori A, Chopin T, Troell M, Buschmann AH, Kraemer GP, Halling C, Shpigel M, Yarish C (2004) Integrated aquaculture: rational, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture 231:361–391CrossRefGoogle Scholar
  29. Neori A, Troell M, Chopin T, Yarish C, Critchley A, Buschmann AH (2007) The need for a balanced ecosystem approach to blue revolution aquaculture. Environment 49:36–43CrossRefGoogle Scholar
  30. Noda H (1993) Health benefits and nutritional properties of nori. J Appl Phycol 5:255–258CrossRefGoogle Scholar
  31. Park CS, Sohn CH (1992) Effects of light and temperature on morphogenesis of Codium fragile (Suringar) Hariot in laboratory culture. Korean J Phycol 7:213–223Google Scholar
  32. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, New York, pp 14–17CrossRefGoogle Scholar
  33. Pedersen A (1994) Transient ammonium uptake in the macroalgae Ulva lactuca (Chlorophyta), nature, regulation, and the consequences for choice of measuring technique. J Phycol 30:980–986CrossRefGoogle Scholar
  34. Pedersen A, Kraemer G, Yarish C (2004) The effects of temperature and nutrient concentrations on nitrate and phosphate uptake in different species of Porphyra from Long Island Sound (USA). J Exp Mar Biol Ecol 312:235–252CrossRefGoogle Scholar
  35. Pereira R, Yarish C (2010) The role of Porphyra in sustainable culture system: physiology and application. In: Israel A, Einav R, Seckbach J (eds) Seaweed and their role in globally changing environments. Springer, Dordrecht, pp 339–354CrossRefGoogle Scholar
  36. Pereira R, Yarish C, Sousa-Pinto I (2006) The influence of stocking density, light and temperature on the growth, production and nutrient removal capacity of Porphyra dioica (Bangiales, Rhodophyta). Aquaculture 252:66–78CrossRefGoogle Scholar
  37. Pereira R, Kraemer G, Yarish C, Sousa-Pinto I (2008) Nitrogen uptake by gametophytes of Porphyra dioica (Bangiales, Rhodophyta) under controlled-culture conditions. Eur J Phycol 43:107–118CrossRefGoogle Scholar
  38. Platt T, Gallegos DL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701Google Scholar
  39. Read P, Fernandes T (2003) Management of environmental impacts of marine aquaculture in Europe. Aquaculture 226:139–163CrossRefGoogle Scholar
  40. Sutherland JE, Lindstrom SC, Nelson WA, Brodie J, Lynch MDJ, Hwang MS, Choi HG (2011) A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J Phycol 47:1131–1151CrossRefGoogle Scholar
  41. Tidwell JH, Allen GL (2001) Fish as food: aquaculture’s contribution. Ecological and economic impacts and contributions of fish farming and capture fisheries. EMBO Rep 2:958–963PubMedCentralPubMedCrossRefGoogle Scholar
  42. Troell M, Kautsky N, Folke C (1999) Applicability of integrated coastal aquaculture systems. Ocean Coast Manag 42:63–69CrossRefGoogle Scholar
  43. Troell M, Halling C, Neori A, Choin T, Bushmann AH, Kautsky N, Yarish C (2003) Integrated mariculture: asking the right questions. Aquaculture 226:69–90CrossRefGoogle Scholar
  44. Wu CY, Zhang YX, Li RZ, Penc ZS, Zhang YF, Liu QC, Zhang JP, Fan X (1984) Utilization of ammonium-nitrogen by Porphyra yezoensis and Gracilaria verrucosa. Hydrobiologia 116/117:475–477Google Scholar
  45. Zhou Y, Yang H, Hu H, Liu Y, Mao Y, Zhou H, Xu X, Zhang F (2006) Bioremediation potential of the macroalga Gracilaria lemaneiformis (Rhodophyta) integrated into fed fish culture in coastal waters of north China. Aquaculture 252:264–276CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of Marine Life SciencesJeju National UniversityJejuSouth Korea
  2. 2.Department of Earth and Marine SciencesJeju National UniversityJejuSouth Korea
  3. 3.Department of OceanographyPusan National UniversityPusanSouth Korea

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