Environmental Science and Pollution Research

, Volume 23, Issue 8, pp 7529–7542 | Cite as

Modelling the nitrogen loadings from large yellow croaker (Larimichthys crocea) cage aquaculture

  • Huiwen Cai
  • Lindsay G. Ross
  • Trevor C. Telfer
  • Changwen Wu
  • Aiyi Zhu
  • Sheng Zhao
  • Meiying Xu
Research Article


Large yellow croaker (LYC) cage farming is a rapidly developing industry in the coastal areas of the East China Sea. However, little is known about the environmental nutrient loadings resulting from the current aquaculture practices for this species. In this study, a nitrogenous waste model was developed for LYC based on thermal growth and bioenergetic theories. The growth model produced a good fit with the measured data of the growth trajectory of the fish. The total, dissolved and particulate nitrogen outputs were estimated to be 133, 51 and 82 kg N tonne−1 of fish production, respectively, with daily dissolved and particulate nitrogen outputs varying from 69 to 104 and 106 to 181 mg N fish−1, respectively, during the 2012 operational cycle. Greater than 80 % of the nitrogen input from feed was predicted to be lost to the environment, resulting in low nitrogen retention (<20 %) in the fish tissues. Ammonia contributed the greatest proportion (>85 %) of the dissolved nitrogen generated from cage farming. This nitrogen loading assessment model is the first to address nitrogenous output from LYC farming and could be a valuable tool to examine the effects of management and feeding practices on waste from cage farming. The application of this model could help improve the scientific understanding of offshore fish farming systems. Furthermore, the model predicts that a 63 % reduction in nitrogenous waste production could be achieved by switching from the use of trash fish for feed to the use of pelleted feed.


Dynamic modelling Large yellow croaker Nitrogen loadings Ammonia Urea Cage aquaculture 



This work was funded by National Natural Science Foundation of China (41206088), Ministry of Science and Technology of People’s Republic of China (2012BAB16B02, 2011BAD13B08), State Oceanic Administration (201305009–2, 201305009–3), Natural Science Foundation of Zhejiang Province (LQ12D06001), Bureau of Science and Technology of Zhoushan (2015C41002), PECRE award from Marine Alliance for Science and Technology for Scotland (MASTS) and Youth Teachers’ Program of Zhejiang Ocean University. Some data used are unpublished from EU 6FP INCO SPEAR project (2004–2007). We thank Dr. Kim Jauncey for his constructive comments during this study.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no competing interests.


  1. Ackefors H, Enell M (1990) Discharge of nutrients from Swedish fish farming to adjacent sea areas. Ambio 19(1):28–35Google Scholar
  2. Azevedo PA, Podemskia CL, Hessleina RH, Kasiana SEM, Findlaya DL, Bureau DP (2011) Estimation of waste outputs by a rainbow trout cage farm using a nutritional approach and monitoring of lake water quality. Aquaculture 331:175–186CrossRefGoogle Scholar
  3. Beauchamp DA, Stewart DJ, Thomas GL (1989) Corroboration of a bioenergetics model for sockeye salmon. Trans Am Fish Soc 118(6):597–607CrossRefGoogle Scholar
  4. Beveridge MCM, Philips MJ, Clarke RM (1991) A quantitative and qualitative assessment of wastes from aquatic animal production. In: Brune DE, Tomasso JR (eds) Advances in world aquaculture: aquaculture and water quality. World Aquaculture Society, Baton Rouge, LA, pp 506–527Google Scholar
  5. Boujard T, Labbe' L, Aupe'rin B (2002) Feeding behaviour, energy expenditure and growth of rainbow trout in relation to stocking density and food accessibility. Aquac Res 33:1233–1242CrossRefGoogle Scholar
  6. Boyd D, Thorburn M, Howel T (2001) Recommendations for the operational water quality monitoring at cage culture aquaculture operations. Environmental Monitoring and Reporting Branch Ontario Ministry of the Environment, Rexdale, ON, CanadaGoogle Scholar
  7. Briggs MRP, Funge-Smith SJ (1994) A nutrient budget of some intensive marine shrimp ponds in Thailand. Aquac Res 25:789–811CrossRefGoogle Scholar
  8. Bromley PJ (1987) The effects of food type, meal size and body weight on digestion and gastric evacuation in turbot, Scophthalmus maximus L. J Fish Biol 30(4):501–512CrossRefGoogle Scholar
  9. Bureau DP, Gunther SJ, Cho CY (2003) Chemical composition and preliminary theoretical estimates of waste outputs of rainbow trout reared in commercial cage culture operations in Ontario. N Am J Aquac 65(1):33–38CrossRefGoogle Scholar
  10. Cai LS, Wu TX, Huang XY, Song HY, Li J, Hu L (2006) Apparent digestibility of experimental diets for Miichthys miiuy, Scioenops ocellatus and Preudosciaena crocea. Acta Agric Zhejiangensis 18(4):256–259 (in Chinese)Google Scholar
  11. Carter CG, Bransden MP, van Barneveld RJ, Clarke SM (1999) Alternative methods for nutrition research on the southern bluefin tuna, Thunnus maccoyii: in vitro digestibility. Aquaculture 179(1–4):57–70CrossRefGoogle Scholar
  12. Cho CY, Bureau DP (1997) Reduction of waste output from salmonid aquaculture through feeds and feedings. Prog Fish Cult 59:155–160CrossRefGoogle Scholar
  13. Cho CY, Bureau DP (1998) Development of bioenergetic models and the Fish-PrFEQ software to estimate production, feeding ration and waste output in aquaculture. Aquat Living Resour 11(4):199–210CrossRefGoogle Scholar
  14. Chowdhury MAK, Siddiqui S, Hua K, Bureau DP (2013) Bioenergetics-based factorial model to determine feed requirement and waste output of tilapia produced under commercial conditions. Aquaculture, 138–147Google Scholar
  15. Chu JCW (2002) Environment of mariculture: the effect of feed types on feed waste. P. 103–108. In: APEC/NACA/BOBP/GOI. 2002. Report of the regional workshop on sustainable seafarming and grouper aquaculture, Medan, Indonesia, 17–20 April, 2000. Collaborative APEC Grouper Research and Development Network (FWG 01/99). Network of Aquaculture Centres in Asia-Pacific, Bangkok, Thailand. 224 ppGoogle Scholar
  16. Costa-Pierce BA (2013) Ocean farming and sustainable aquaculture science and technology, an introduction to sustainable food production, 1252–1255Google Scholar
  17. Davies IM, Slaski RJ (2003) Waste production by farmed Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 219:495–502CrossRefGoogle Scholar
  18. Dumas A, France J, Bureau DP (2007) Evidence of three growth stanzas in rainbow trout (Oncorhynchus mykiss) across life stages and adaptation of the thermal-unit growth coefficient. Aquaculture 267:139–146CrossRefGoogle Scholar
  19. Fernandes M, Lauer P, Cheshire A, Angove M (2007) Preliminary model of nitrogen loads from southern bluefin tuna aquaculture. Mar Pollut Bull 54(9):1321–1332CrossRefGoogle Scholar
  20. Ferreira JG, Andersson HC, Corner RA, Esmit XD et al (2008) SPEAR Sustainable options for people, catchment and aquatic resources. Institute of Marine Research, Bergen (Norway)Google Scholar
  21. Fishery Bureau, Ministry of Agriculture, China (2011) Annual report of fishery statistic China. Agriculture Press of China (in Chinese)Google Scholar
  22. Foy RH, Rosell R (1991) Loadings of nitrogen and phosphorus from a northern Ireland fish farm. Aquaculture 96:17–30CrossRefGoogle Scholar
  23. Gordard S (1996) Feed management in intensive aquaculture. Chapman and Hall, LondonCrossRefGoogle Scholar
  24. Guan SJ, Wu RQ, Xie J, Wang GJ, Niu JF (2007) The impact of two types of feed on the growth, digestibility and digestive enzyme activities of largemouth bass. Ind Feed 28(2):32–36 (in Chinese)Google Scholar
  25. Guerin-Ancey O (1976) Effects de la temperature et du poids du corps sur I excretion d’ammoniac et d’uree. Aquaculture 9:71–80CrossRefGoogle Scholar
  26. Hall POJ, Holby O, Kollberg S, Samuelsson MO (1992) Chemical fluxes and mass balances in a marine fish cage farm. IV. Nitrogen. Mar Ecol Prog Ser 89:81–91CrossRefGoogle Scholar
  27. Hasan MR (2001) Nutrition and feeding for sustainable aquaculture development in the third millennium. In: Technical Proceedings of the Conference on Aquaculture in the Third Millennium, Bangkok, Thailand, pp193-219Google Scholar
  28. Jahan P, Watanabe T, Kiron I, Satoh SH (2003) Improved carp diets based on plant protein sources reduce environmental phosphorus loading. Fish Sci, Tokyo 69:219–225CrossRefGoogle Scholar
  29. James AG, Probyn T, Seiderer LJ (1989) Nitrogen excretion and absorption efficiencies of the Cape anchovy Engraulis capensis Gilchrist fed upon a variety of plankton diets. J Exp Mar Biol Ecol 131:101–124CrossRefGoogle Scholar
  30. Jobling M (1994) Fish bioenergetics. Chapman and Hall, LondonGoogle Scholar
  31. Jobling M (2003) The thermal growth coefficient model of fish growth: a cautionary note. Aquac Res 34:581–584CrossRefGoogle Scholar
  32. Kawai Y, Wada A (2007) Diurnal sea surface temperature variation and its impact on the atmosphere and ocean: a review. J Oceanogr 63(5):721–744CrossRefGoogle Scholar
  33. Leung KMY, Chu JCW, Wu RSS (1999a) Effects of body weight, water temperature and ration size on ammonia excretion by the areolated grouper and mangrove snapper (Lutjanus argentimaculatus). Aquaculture 170:215–227CrossRefGoogle Scholar
  34. Leung KMY, Chu JCW, Wu RSS (1999b) Nitrogen budgets for the areolated grouper (Epinephelus areolatus) cultured under laboratory conditions and in open-sea cages. Mar Ecol Prog Ser 186:271–281CrossRefGoogle Scholar
  35. Madenjian CP, O'Connor DV (1999) Laboratory evaluation of a lake trout bioenergetics model. Trans Am Fish Soc 128(5):802–814CrossRefGoogle Scholar
  36. McDonald ME, Tikkanen CA, Axler RP, Larsen CP, Host G (1996) Fish simulation culture model (FIS-C): a bioenergetics based model for aquacultural waste load application. Aquac Eng 15(4):243–259CrossRefGoogle Scholar
  37. Ministry of Agriculture, China (2002) Aquaculture technical specification of Pseudosciaena crocea, National Criteria of Agriculture, NY/T 5061–2002 (in Chinese)Google Scholar
  38. Ney JJ (1993) Bioenergetics modelling today: growing pains on the cutting edge. Trans Am Fish Soc 122(5):736–748CrossRefGoogle Scholar
  39. Paakkonen JPJ, Tikkanen O, Karjalainen J (2003) Development and validation of a bioenergetics model for juvenile and adult burbot. J Fish Biol 63:956–969CrossRefGoogle Scholar
  40. Papatryphon E, Petit J, Van Der Werf HM, Sadasivam KJ, Claver K (2005) Nutrient-balance modeling as a tool for environmental management in aquaculture: the case of trout farming in France. Environ Manag 35(2):161–174CrossRefGoogle Scholar
  41. Ove Arup and Partners, Furano, Hydraulics Research (Asia) and WRc (Asia) (1989) Assessment of the environmental impact of marine fish culture in Hong Kong: final report. Environmental Protection Department, Hong KongGoogle Scholar
  42. Porter CB, Krom MD, Robbins MG, Brickell L, Davidson A (1987) Ammonia excretion and total N budget for gilthead seabream (Sparus aurata) and its effect on water quality condition. Aquaculture 66:287–297CrossRefGoogle Scholar
  43. Rice JA, Cochran PA (1984) Independent evaluation of a bioenergetics model for largemouth bass. Ecology 65:732–739CrossRefGoogle Scholar
  44. Roque D'Orbcastel E, Blancheton JP (2006) The wastes from marine fish production systems: characterization, minimization, treatment and valorization. World Aquacult 31:28–70Google Scholar
  45. Santos JD, Jobling M (1991) Factors affecting gastric evacuation in cod, Gadus morhua L., fed single meals of natural prey. J Fish Biol 38:697–713CrossRefGoogle Scholar
  46. Sayer MDJ, Davenport J (1987) The relative importance of the gills to ammonia and urea excretion in five seawater and one freshwater teleost species. J Fish Biol 31:561–70CrossRefGoogle Scholar
  47. Stigebrandt A (1999) MOM (Monitoring-Ongrowing Fish Farms-Modelling): Turnover of energy and matter by fish: a general model with application to Salmon. HavforskningsinstituttetGoogle Scholar
  48. Strain PM, Hargrave BT (2005) Salmon aquaculture, nutrient fluxes and ecosystem processes in southwestern New Brunswick. In: Hargrave B (ed) The handbook of environmental chemistry, vol. 5, Part M: Environmental effects of marine finfish aquaculture. Springer, Berlin, pp 29–57CrossRefGoogle Scholar
  49. Sun Z, Yu FP, Yao HF, Jin CX (2004) Oxygen consumption and ammonia excretion of Pseudosciaena crocea and Sciaenops ocellatus in cage farming. Journal of Zhejiang Ocean University 23(3): 207–217 (in Chinese)Google Scholar
  50. Wang K, Yan XJ (2008) Study on expression of ammonia excretion rate of large yellow croaker. (in Chinese)
  51. Whitledge GW, Bajer PG, Hayward RS (2006) Improvement of bioenergetics model predictions for fish undergoing compensatory growth. Trans Am Fish Soc 135:49–54CrossRefGoogle Scholar
  52. Wright PA, Anderson P (2001) Fish physiology: nitrogen excretion, 1st ed. Academic PressGoogle Scholar
  53. Zhang B, Zhang M, Dai FQ, Jin XS (2008) The biochemical compositions and energy content of 16 important resource species in the central and southern Yellow Sea. Mar Fish Res 29(5):11–18Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Huiwen Cai
    • 1
    • 3
  • Lindsay G. Ross
    • 2
  • Trevor C. Telfer
    • 2
  • Changwen Wu
    • 1
  • Aiyi Zhu
    • 1
  • Sheng Zhao
    • 1
  • Meiying Xu
    • 1
  1. 1.National Engineering Research Centre of Marine Facilities AquacultureZhejiang Ocean UniversityZhoushanPeople’s Republic of China
  2. 2.Institute of AquacultureUniversity of StirlingStirlingUK
  3. 3.ZhoushanPeople’s Republic of China

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