Skip to main content

Advertisement

Log in

Bioremediation efficiencies of Gracilaria verrucosa cultivated in an enclosed sea area of Hangzhou Bay, China

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Due to the discharge of nutrients into the East China Sea, severe eutrophication has appeared in Hangzhou Bay. Therefore, we cultivated Gracilaria verrucosa on a large scale in the Jinshan enclosed sea with an area of 1.72 km2 in the northern part of Hangzhou Bay to perform bioremediation. The Fengxian enclosed sea with an area of 2.3 km2 and 50 km far from Jinshan was used as the control. The results showed that the Hangzhou Bay was severely eutrophicated before G. verrucosa cultivation. During the period of cultivation between August 2006 and July 2007, the annual growth rate of G. verrucosa was 9.42% day−1, and the sea water quality was improved from worse than grade IV to grades II–III, with the concentration of dissolved inorganic nitrogen (DIN) and PO4-P significantly lower than that in the Fengxian enclosed sea (p < 0.01). The concentration of NH4-N, NO3-N, NO2-N, and PO4-P after G. verrucosa cultivation was decreased by 54.12%, 75.54%, 49.81%, and 49.00%, respectively. The density of phytoplankton in the Jinshan enclosed sea with cultivation of G. verrucosa was 6.90 –126.53 × 104 cells m−3, which was significantly lower than that in the Fengxian enclosed sea. In addition, species diversity, richness, and evenness was significantly increased after cultivation of G. verrucosa in the Jinshan enclosed sea compared with that in the Fengxian enclosed sea. The density of Skeletonema costatum, Prorocentrum micans, and Prorocentrum donghaiense, which were the usual species of red tides at the coastal sea of China, in the Jinshan enclosed sea with cultivation of G. verrucosa was significantly lower. Based on these results, if the water quality in the Jinshan enclosed sea were to be maintained at grade I (DIN ≤0.20 mg  L−1) or II (DIN ≤0.30 mg  L−1), 21.8 t or 18.0 t fresh weight of G. verrucosa need to be cultivated, respectively. These results indicated that large-scale cultivation of G. verrucosa could play a significant role in the bioremediation of Hangzhou Bay.

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

Access this article

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

  • Anderson RJ, Smit AJ, Levitt GJ (1999) Upwelling and fishfactory waste as nitrogen sources for suspended cultivation of Gracilaria gracilis in Saldanha Bay, South Africa. Hydrobiologia 398/399:455–462

    Article  Google Scholar 

  • Bonsdorff E, Römberg C, Aarnio K (2002) Some ecological properties in relation to eutrophication in the Baltic Sea. Hydrobiologia 475/476:371–377

    Article  Google Scholar 

  • Buschmann AH, Westermeier R, Retamales CA (1995) Cultivation of Gracilaria on the sea-bottom in southern Chile: a review. J Appl Phycol 7:291–301

    Article  Google Scholar 

  • Buschmann AH, Troell M, Kautsky N, Kautsky L (1996) Integrated cultivation of salmonids and Gracilaria chilensis (Gracilariales, Rhodophyta). Hydrobiologia 326/327:75–82

    Article  Google Scholar 

  • Buschmann AH, Correa JA, Westermeier R, Hernandez-Gonzalez MC, Norambuena R (2001) Red algal farming in Chile: a review. Aquaculture 194:203–220

    Article  Google Scholar 

  • Capriulo GM, Smith G, Troy R, Wikfors G, Pellet J, Yarish C (2002) The planktonic food web structure of a temperate zone estuary, and its alteration due to eutrophication. Hydrobiologia 475/476:263–333

    Article  Google Scholar 

  • Carmona R, Kraemer GP, Yarish C (2006) Exploring northeast American and Asian species of Porphyra for use in an integrated finfish—algal aquaculture system. Aquaculture 252:54–65

    Article  Google Scholar 

  • Chen JY, Chen SL (2003) Environmental changes of Yangtze river and opinions on estuary improvement. Water Resour Hydropower Eng 34:19–25, in Chinese with English abstract

    CAS  Google Scholar 

  • Chopin T, Yarish C (1999) Aquaculture does not only mean fin-fish monoculture….seaweeds must be a significant component for an integrated ecosystem approach. Bull Aquacult Assoc Can 99:35–37

    Google Scholar 

  • Chopin T, Yarish C, Wilkes R, Belyea E, Lu S, Mathieson A (1999) Developing Porphyra/salmon integrated aquaculture for bioremediation and diversification of the aquaculture industry. J Appl Phycol 11:463–472

    Article  Google Scholar 

  • Chopin T, Bastarache S, Belyea E, Haya K, Sephton D, Martin JL, Eddy S, Stewart I (2003) Development of the cultivation of Laminaria saccharina as the extractive inorganic component of an integrated aquaculture system and monitoring of therapeutants and phycotoxins. J Phycol 39(S1):10

    Article  Google Scholar 

  • Chung I, Kang YH, Yarish C, Kraemer G, Lee J (2002) Application of seaweed cultivation to the bioremediation of nutrient-rich effluent. Algae 17:187–194

    Article  Google Scholar 

  • Cuomo V, Merrill J, Palomba I, Perretti A (1993) Systematic collection of Ulva and mariculture of Porphyra: biotechnology against eutrophication in the Venice Lagoon. Int J Environ Stud 43:141–149

    Article  Google Scholar 

  • Fei XG (2004) Solving the coastal eutrophication problem by large scale seaweed cultivation. Hydrobiologia 512:145–151

    Article  Google Scholar 

  • Fei XG, Lu S, Bao Y, Wilkes R, Yarish C (1998) Seaweed cultivation in China. World Aquac 29:22–24

    Google Scholar 

  • Fei XG, Bao Y, Lu S (1999) Seaweed cultivation: traditional way and its reformation. Chin J Oceanol Limnol 7:193–199

    Google Scholar 

  • Guildford SJ, Hecky RE (2000) Total nitrogen, total phosphorus, and nutrient limitation in lakes and oceans: is there a common relationship? Limnol Oceanogr 45:1213–1223

    Article  CAS  Google Scholar 

  • He PM, Xu SN, Zhang HY, Wen SS, Dai YJ, Lin SJ, 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

    Article  PubMed  CAS  Google Scholar 

  • Hernández I, Pérez-Pastor A, Vergara JJ, Martínez-Aragón JF, Fernández-Engo MÁ, Pérez-Lloréns JL (2006) Studies on the biofiltration capacity of Gracilariopsis longissima: from microscale to macroscale. Aquaculture 252:43–53

    Article  CAS  Google Scholar 

  • Ji HH, Ye SF, Wang JH, Huang XQ (2004) Variation and assessment of nutrients in the sea area of Jinshan three-islands marine ecological natural reserve. Mar Environ Sci 23:38–39, in Chinese with English abstract

    Google Scholar 

  • Jia HL, Wen YM, Xie J (2005) Self-pollution status of cage culture in Yaling Bay. Mar Environ Sci 24(2):5–8, in Chinese with English abstract

    CAS  Google Scholar 

  • Jiang ZJ, Fang JG, Mao YZ, Wang W (2010) Eutrophication assessment and bioremediation strategy in a marine fish cage culture area in Nansha Bay, China. J Appl Phycol 22:421–426

    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

    Article  Google Scholar 

  • Kraemer GP, Carmona R, Chopin T, Neefus C, Tang XR, 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 16:489–497

    Article  CAS  Google Scholar 

  • Makoto K (1984) The concept of tidal exchange and the tidal exchange ratio. J Oceanol Soc Jpn 40:135–147

    Article  Google Scholar 

  • Mao YZ, Yang HS, Zhou Y, Ye NH, Fang JG (2009) Potential of the seaweed Gracilaria lemaneiformis for integrated multi-trophic aquaculture with scallop Chlamys farreri in North China. J Appl Phycol 21:649–656

    Article  Google Scholar 

  • Margalef DR (1968) Perspectives in ecological theory. University of Chicago Press, Chicago, pp 1–111

    Google Scholar 

  • Mariachiara N, Pierluigi V (2002) Nitrate uptake and storage in the seaweed Ulva rigida C. Agardh in relation to nitrate availability and thallus nitrate content in a eutrophic coastal lagoon (Sacca di Goro, Po River Delta, Italy). J Exp Mar Biol Ecol 269:65–83

    Article  Google Scholar 

  • Mclachlan J, Bird CJ (1986) Gracilaria (Gigartinales, Rhodophyta) and productivity. Aquat Bot 26:27–49

    Article  Google Scholar 

  • McVey JP, Stickney R, Yarish C, Chopin T (2002) Aquatic polyculture and balanced ecosystem management: new paradigms for seafood production. In: Stickney RR, McVey JP (eds) Responsible aquaculture. CAB International, Oxon, pp 91–104

    Chapter  Google Scholar 

  • Naylor RL, Goldburg RJ, Primavera JH, Kautsky N, Beveridge MCM, Clay J, Folke C, Lubchenco J, Mooney H, Troell M (2000) Effect of aquaculture on world fish supplies. Nature 405:1017–1024

    Article  PubMed  CAS  Google Scholar 

  • Neori A, Ragg NLC, Shpigel M (1998) The integrated culture of seaweed, abalone, fish and clams in modular intensive land-based system: II. Performance and nitrogen partitioning within an abalone (Haliotis tuberculata) and macroalgae culture system. Aquac Eng 17:215–239

    Article  Google Scholar 

  • Neto CC (1987) Seaweed culture in Rio Grande do Norte, Brazil. Hydrobiologia 151/152:363–367

    Article  Google Scholar 

  • Parsons TR, Maita Y, Lalli GM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon, pp 101–122

  • 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 252:66–78

    Article  CAS  Google Scholar 

  • Pielou EC (1975) Ecological diversity. Wiley, New York, pp 16–51

    Google Scholar 

  • S.O.A. (2004–2008) Marine environment quality bulletin of China. State Oceanic Administration, China. http://www.soa.gov.cn/hyjww/hygb/hyhjzlgb/A020707index_1.htm. Accessed 12 Feb 2009

  • Schramm W (1999) Factors influencing seaweed responses to eutrophication: some results from EU-project EUMAC. J Appl Phycol 11:69–78

    Article  Google Scholar 

  • Schramm W, Lotze H, Schories D (1996) Eutrophication and macroalgal blooms in inshore waters of the German Baltic coasts: the Schlei Fjord, a case study. In: Rijstenbil JW, Kamermans P, Nienhuis PH (eds) EUMAC Synthesis Report and Proceedings of the second EUMAC Workshop. Sete, France, pp 18–73

    Google Scholar 

  • Sfriso A, Pavoni B, Marcomini A (1992) Macroalgae, nutrient cycles and pollutants in the Lagoon of Venice. Estuaries 15:517–528

    Article  CAS  Google Scholar 

  • Shannon CE, Weaver W (1963) The mathematical theory of communication. University of Illinois Press, Urbana, pp 1–117

    Google Scholar 

  • Suzuki Y, Kametani T, Maruyama T (2005) Removal of heavy metals from aqueous solution by nonliving Ulva seaweed as biosorbent. Water Res 39:1803–1808

    Article  PubMed  CAS  Google Scholar 

  • Tang KX, You XP, Lin YS, Chen ME, Shen DL, Lin SB (2005) A study on bioremediation of eutrophication of mariculture waters by Gracilaria lemaneaformis. Acta Ecol Sin 25(11):3044–3051, in Chinese with English abstract

    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

    Article  Google Scholar 

  • Tseng CK (2001) Algal biotechnology industry and research activities in China. J Appl Phycol 13:375–380

    Article  Google Scholar 

  • Victor ND, Elliott M, Orive E (2002) Causes, historical development, effects and future challenges of a common environmental problem: eutrophication. Hydrobiologia 475/476:1–19

    Google Scholar 

  • Wakibia JG, Anderson RJ, Keats DW (2001) Growth rates and agar properties of three gracilarioids in suspended open-water cultivation in St. Helena Bay, South Africa. J Appl Phycol 13:195–207

    Article  CAS  Google Scholar 

  • Wang YL, Yuan J, Shen XQ (2005) Ecological character of phytoplankton in spring in the Yangtze River estuary and adjacent water. J Fish Sci China 12:300–306, in Chinese with English abstract

    Google Scholar 

  • Xu SN, He PM (2006) Analysis of phenomena for frequent occurrence of red tides and bioremediation by seaweed cultivation. J Fish China 30(4):554–561, in Chinese with English abstract

    CAS  Google Scholar 

  • Xu SN, Chen ZZ, He PM (2007) Influencing analysis of human activities on frequency of red tides (HABs) in Zhejiang Sea Area. Mar Environ Sci 26:232–236, in Chinese with English abstract

    CAS  Google Scholar 

  • Xu SN, Wen SS, Wu WX, He PM (2008a) Bioremediation of caged fish aquaculture by the red alga Gracilaria verrucosa in an integrated multi-trophic aquaculture system. Acta Ecol Sinica 28:1467–1475, in Chinese with English abstract

    Google Scholar 

  • Xu YJ, Fang JG, Wei W (2008b) Application of Gracilaria lichenoides (Rhodophyta) for alleviating excess nutrients in aquaculture. J Appl Phycol 20:199–203

    Article  Google Scholar 

  • Yang YF, Fei XG (2003) Prospects for bioremediation of cultivation of large-sized seaweed in eutrophic mariculture areas. J Ocean U Qingdao 33:53–57, in Chinese with English abstract

    Google Scholar 

  • Yang YF, Li CH, Nie XP, Tang DL, Chung IK (2004) Development of mariculture and its impacts in Chinese coastal waters. Rev Fish Biol Fish 14:1–10

    Article  Google Scholar 

  • Yang HS, Zhou Y, Mao YZ, Li XX, Liu Y, Zhang FS (2005) Growth characters and photosynthetic capacity of Gracilaria lemaneiformis as a biofilter in a shellfish farming area in Sanggou Bay, China. J Appl Phycol 17:199–206

    Article  Google Scholar 

  • Yang YF, Fei XG, Song JM, Hu HY, Wang GC, Chung IK (2006) Growth of Gracilaria lemaneiformis under different cultivation conditions and its effects on nutrient removal in Chinese coastal waters. Aquaculture 254:248–255

    Article  Google Scholar 

  • Ye Y, Xu JL, Ying QL, Wei DY, Chen QZ, Ning XR (2002) Changes of nutrient in net aquaculture area of Xiangshan Harbor. Mar Environ Sci 21(1):39–41, in Chinese with English abstract

    CAS  Google Scholar 

  • Zhang GS, Chen HT, Zhang J, Liu SM (2003) Nutrient elements in the atmospheric wet deposition in Changjiang River estuary. Chin J Appl Ecol 14:1107–1111

    CAS  Google Scholar 

  • Zhou Y, Yang HS, Hu HY, Liu Y, Mao YZ, Zhou H, Xu XL, Zhang FS (2006) Bioremediation potential of the macroalga Gracilaria lemaneiformis (Rhodophyta) integrated into fed fish culture in coastal waters of north China. Aquaculture 252:264–276

    Article  Google Scholar 

Download references

Acknowledgment

This study was supported by National Natural Science Foundation (30371101), the Project for Excellence Disciplines Leader (08XD14037), International Cooperation Project (08540702600), Pujiang Project (05PJ14086), in Shanghai Science Commission, and Superiority Subject Sponsored Projects in Shanghai Municipal Education Commission (S30701). Thanks are due also to two anonymous reviewers for their valuable comments and suggestions on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pei Min He.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huo, Y.Z., Xu, S.N., Wang, Y.Y. et al. Bioremediation efficiencies of Gracilaria verrucosa cultivated in an enclosed sea area of Hangzhou Bay, China. J Appl Phycol 23, 173–182 (2011). https://doi.org/10.1007/s10811-010-9584-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-010-9584-9

Keywords

Navigation