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Hypoxia and nutrient dynamics affected by marine aquaculture in a monsoon-regulated tropical coastal lagoon

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Abstract

The Laoyehai (lagoon) is located at the east coast of Hainan Island in the South China Sea and has been subject to perturbations from human activities, notably marine aquaculture, and has eutrophic surface and hypoxic near-bottom waters. A lack of knowledge of hydrodynamic and biogeochemical processes is a challenge to the sustainable management of lagoon at the ecosystem level in science. Five field campaigns, including three during the southwest monsoon and two in the northeast monsoon periods, were carried out at the Laoyehai in 2008–2011. The aim of this study is to investigate the impacts of dynamic processes of hydrography and human activities on nutrient geochemistry and their relationships to the system eutrophication and hypoxia in the lagoon. In this coastal system, high levels of ammonium relative to nitrate are found, elevated phosphate skews the DIN/DIP relative to the Redfield ratio, and the dissolved silicate concentration is high because of submarine groundwater discharge. The organic fraction in the Laoyehai accounts for a large proportion of the total nutrients associated with the release of wastes from marine aquaculture. The hypoxia of near-bottom waters in the Laoyehai is created and maintained by heterotrophic processes that are fueled by organic matter, which are exacerbated by poor water exchange as a consequence of the geomorphology and weak tidal circulation.

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References

  • Bricker, S. B., Ferreira, J. G., & Simas, T. (2003). An integrated methodology for assessment of estuarine trophic status. Ecological Modelling, 169, 39–60.

    Article  CAS  Google Scholar 

  • Cao, L., Wang, W. M., Yang, Y., Yang, C. T., Yuan, Z. H., Xiong, S. B., & Diana, J. (2007). Environmental impact of aquaculture and counter measures to aquaculture pollution in China. Environmental Science and Pollution Research, 14, 452–462.

    Article  CAS  Google Scholar 

  • Cobelo-García, A., Bernárdez, P., Leira, M., López-Sánchez, D. E., Santos-Echeandía, J., Prego, R., & Pérez-Arlucea, M. (2012). Temporal and diel cycling of nutrients in a barrier–lagoon complex: implications for phytoplankton abundance and composition. Estuarine, Coastal and Shelf Science, 110, 69–76.

    Article  Google Scholar 

  • Daniele, N., David, T. W., Elisa Anna, F., & Pierluigi, V. (2006). Impact of clam and mussel farming on benthic metabolism and nitrogen cycling, with emphasis on nitrate reduction pathways. Marine Ecology Progress Series, 315, 151–165.

    Article  Google Scholar 

  • Diaz, R. J., & Rosenberg, R. (2008). Spreading dead zones and consequences of marine ecosystems. Science, 321, 926–929.

    Article  CAS  Google Scholar 

  • Fang, J. G., Zhang, J., Xiao, T., Huang, D. J., & Liu, S. M. (2016). Integrated multi-trophic aquaculture (IMTA) in Sanggou Bay, China. Aquaculture Environment Interactions, 8, 201–205.

    Article  Google Scholar 

  • FAO (2012) The state of world fisheries and aquaculture 2012. Rome, 209 p.

  • FAO (2016) FAO yearbook: fishery and aquaculture statistics 2014. Rome, 105 p.

  • Grasshoff K., Kremling K. and Ehrhardt M. (1999) Methods of seawater analysis. 3rd edition, Wiley-VCH, Weinheim, 600 p.

  • Hargrave, B. T., Phillips, G. A., Doucette, L. I., White, M. J., Milligan, T. G., Wildish, D. J., & Granston, R. E. (1997). Assessing benthic impacts of organic enrichment from marine aquaculture. Water, Air, and Soil Pollution, 99, 641–650.

    CAS  Google Scholar 

  • Herbeck, L. S., Unger, D., Wu, Y., & Jennerjahn, T. (2013). Effluent, nutrient and organic matter export from shrimp and fish ponds causing eutrofication in coastal and back-reef waters of NE Hainan, tropical China. Continental Shelf Research, 57, 92–104.

    Article  Google Scholar 

  • HNMDDI (2011) On the evolution of morphology and environmental capacity of the Laoyehai coastal lagoon. Hainan Marine Development Designing Institute (HNMDDI), Haikou, 43 p (in Chinese).

  • Hwang, D. W., Kim, G. B., Lee, W. C., & Oh, H. T. (2010). The role of submarine groundwater discharge (SGD) in nutrient budgets of Gamak Bay, a shellfish farming bay in Korea. Journal of Sea Research, 64, 224–230.

    Article  CAS  Google Scholar 

  • Jensen, M., Kuypers, M., Lavik, G., & Thamdrup, B. (2008). Rates and regulation of anaerobic ammonium oxidation and denitrification in the Black Sea. Limnology and Oceanography, 53, 23–36.

    Article  CAS  Google Scholar 

  • Jensen, M., Petersen, J., Dalsgaard, T., & Thamdrup, B. (2009). Pathways, rates, and regulation of N2 production in the chemocline of an anoxic basin, Mariager Fjord, Denmark. Marine Chemistry, 113, 102–113.

    Article  CAS  Google Scholar 

  • Ji, T., Du, J. Z., Moore, W. S., Zhang, G. S., Su, N., & Zhang, J. (2013). Nutrient inputs to a lagoon through submarine groundwater discharge: the case of Laoye Lagoon, Hainan. China. Journal of Marine Systems, 111-112, 253–262.

    Article  Google Scholar 

  • Jiang, Z. B., Chen, Q. Z., Zeng, J. N., Liao, Y. B., Shou, L., & Liu, J. (2012). Phytoplankton community distribution in relation to environmental parameters in three aquaculture systems in a Chinese subtropical eutrophic bay. Marine Ecology Progress Series, 446, 73–89.

    Article  CAS  Google Scholar 

  • Jiang, Z., Li, J., Qiao, X., Wang, G., Bian, D., Jiang, X., Liu, Y., Huang, D., Wang, W., & Fang, J. (2015). The budget of dissolved inorganic carbon in the shellfish and seaweed integrated mariculture area of Sanggou Bay, Shandong, China. Aquaculture, 446, 167–174.

    Article  CAS  Google Scholar 

  • Lee, Y. G., Jeong, D. U., Lee, J. S., Choi, Y. H., & Lee, M. O. (2016). Effects of hypoxia caused by mussel farming on benthic foraminifera in semi-closed Gamak Bay, South Korea. Marine Pollution Bulletin, 109, 566–581.

    Article  CAS  Google Scholar 

  • Levin, L. A., Ekau, W., Gooday, A. J., Jorissen, F., Middelburg, J. J., Naqvi, S. W. A., Neira, C., Rabalais, N. N., & Zhang, J. (2009). Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences, 6, 2063–2098.

    Article  CAS  Google Scholar 

  • Li, R. H., Liu, S. M., Li, Y. W., Zhang, G. L., Ren, J. L., & Zhang, J. (2014a). Nutrient dynamics in tropical rivers, lagoons, and coastal ecosystems of eastern Hainan Island, South China Sea. Biogeosciences, 11, 481–506.

    Article  Google Scholar 

  • Li, Y., Zhang, J., Deng, H., Wang, D. R., & Zhu, Z. Y. (2014b). Response of bottom hypoxia in Laoyehai Lagoon to the South China Sea monsoon climate rhythm. Oceanologica Limnolgy Sinica, 45(4), 719–733 (in Chinese).

    Google Scholar 

  • Liu, S. M., Li, R. H., Zhang, G. L., Wang, D. R., Du, J. Z., Herbeck, L. S., Zhang, J., & Ren, J. L. (2011). The impact of anthropogenic activities on nutrient dynamics in the tropical Wenchanghe and Wenjiaohe estuary and lagoon system in East Hainan, China. Marine Chemistry, 125, 49–68.

    Article  CAS  Google Scholar 

  • Mahmood, T., Fang, J., Jiang, Z., & Zhang, J. (2016). Seasonal nutrient chemistry in an integrated multi-trophic aquaculture region: case study of Sanggou Bay from North China. Chemistry and Ecology, 32, 149–168.

    Article  CAS  Google Scholar 

  • Martins, C. I. M., Eding, E. H., Verdegem, M. C. J., Heinsbroek, L. T. N., Schneider, O., Blancheton, J. P., d’Orbcastel, E. R., & Verreth, J. A. J. (2010). New developments in recirculating aquaculture systems in Europe: a perspective on environmental sustainability. Aquacultural Engineering, 43, 83–93.

    Article  Google Scholar 

  • McCarthy, M. J., Carini, S. A., Liu, Z., Ostrom, N. E., & Gardner, W. S. (2013). Oxygen consumption in the water column and sediments of the northern Gulf of Mexico hypoxic zone. Estuarine, Coastal and Shelf Science, 123, 46–53.

    Article  CAS  Google Scholar 

  • McCoy, C., Viso, R., Peterson, R. N., Libes, S., Lewis, B., Ledoux, J., Voulgaris, G., Smith, E., & Sanger, D. (2011). Radon as an indicator of limited cross-shelf mixing of submarine groundwater discharge along an open ocean beach in the South Atlantic Bight during observed hypoxia. Continental Shelf Research, 31, 1306–1317.

    Article  Google Scholar 

  • MEMCHN (2005) Report of water quality for the Laoyehai fishery: 2001-2004. Marine Environmental Monitoring Center of Hainan (MEMCHN), Haikou, 30 p (in Chinese).

  • Mirto, S., Gristina, M., Sinopoli, M., Maricchiolo, G., Genovese, L., Vizzini, S., & Mazzola, A. (2012). Meiofauna as an indicator for assessing the impact of fish farming at an exposed marine site. Ecological Indicators, 18, 468–476.

    Article  Google Scholar 

  • Pawar, V., Matsuda, O., Yamamoto, T., Hashimoto, T., & Rajendran, N. (2001). Spatial and temporal variations of sediment quality in and around fish cage farms: a case study of aquaculture in the Seto Inland Sea, Japan. Fisheries Science, 67, 619–627.

    Article  CAS  Google Scholar 

  • Rabalais, N. N., Diaz, R. J., Levin, L. A., Turner, R. E., Gilbert, D., & Zhang, J. (2010). Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences, 7, 585–619.

    Article  CAS  Google Scholar 

  • Rodellas, V., Garcia-Orellana, J., Masque, P., Feldman, M., & Weinstein, Y. (2015). Submarine groundwater discharge as major source of nutrients to the Mediterranean Sea. PNAS, 112, 3926–3930. https://doi.org/10.1073/pnas.1419049112.

    Article  CAS  Google Scholar 

  • SCSIO (2006) Report on the water research and remediation of the Laoyehai from the “Shenzhou” Peninsula. South China Sea Institute of Oceanology (SCSIO), Guangzhou, 123 p (in Chinese).

  • STAP (2011) Hypoxia and nutrient reduction in the coastal zone. Advice for prevention, remediation and research. A STAP Advisory Document. Global Environment Facility, Washington DC, 88 p.

  • Sutherland, T. F., Levings, C. D., Petersen, S. A., Poon, P., & Piercey, B. (2007). The use of meiofauna as an indicator of benthic organic enrichment associated with salmonid aquaculture. Marine Pollution Bulletin, 54, 1249–1261.

    Article  CAS  Google Scholar 

  • Valdemarsen, T., Hansen, P. K., Ervik, A., & Bannister, R. J. (2015). Impact of deep-water fish farms on benthic macrofauna communities under different hydrodynamic conditions. Marine Pollution Bulletin, 101, 776–783.

    Article  CAS  Google Scholar 

  • Vignes, F., Barbone, E., Breber, P., D'Adamo, R., Leonilde, R., Ungaro, N., Facoardi, S., Renzi, M., & Basset, A. (2009). Spatial and temporal description of the dystrophic crisis in Lesina lagoon during summer 2008. Transitional Waters Bull., 3, 47–62.

    Google Scholar 

  • Wang, X. L., & Du, J. Z. (2016). Submarine groundwater discharge into typical tropical lagoons: a case study in eastern Hainan Island, China. Geochemistry, Geophysics, Geosystems, 17, 4366–4382.

    Article  Google Scholar 

  • Wang, X. L., Du, J. Z., Ji, T., Wen, T. Y., Liu, S. M., & Zhang, J. (2014). An estimation of nutrient fluxes via submarine groundwater discharge in the Sanggou Bay—a typical multi-species culture ecosystem in China. Marine Chemistry, 167, 113–122.

    Article  CAS  Google Scholar 

  • Xiao, Y. J., Ferreira, J. G., Bricker, S. B., Nunes, J. P., Zhu, M. Y., & Zhang, X. L. (2007). Trophic assessment in Chinese coastal systems—review of methods and application to the Changjiang (Yangtze River) Estuary and Jiaozhou Bay. Estuaries and Coasts, 30, 901–918.

    Article  Google Scholar 

  • Yamamuro, M. (2012). Herbicide-induced macrophyte-to-phytoplankton shifts in Japanese lagoons during the last 50 years: consequences for ecosystem services and fisheries. Hydrobiologia, 699, 5–19.

    Article  CAS  Google Scholar 

  • Zapata, M., & Garrido, J. L. (1991). Influence of injection conditions in reversed-phase high-performance liquid chromatography of chlorophylls and carotenoids. Chromatographia, 31, 589–594.

    Article  CAS  Google Scholar 

  • Zapata, M., Rodríguez, F., & Garrido, J. L. (2000). Separation of chlorophylls and carotenoids from marine phytoplankton: a new HPLC method using a reversed phase C8 column and phridine containing mobile phases. Marine Ecology Progress Series, 195, 29–45.

    Article  CAS  Google Scholar 

  • Zhang Y.L., Baptista A.M. and Myers III E.P. (2004) A cross-scale model for 3-D baroclinic circulation in estuary-plume-shelf systems: I. Formulation and skill assessment. Continental Shelf Research, 24: 2187–2214.

    Article  Google Scholar 

  • Zhang, J., Gilbert, D., Gooday, A. J., Levin, L., Naqvi, S. W. A., Middelburg, J. J., Scranton, M., Ekau, W., Pena, A., Dewitte, B., Oguz, T., Monteiro, P. M. S., Urban, E., Rabalais, N. N., Ittekkot, V., Kemp, W. M., Ulloa, O., Elmgren, R., Escobar-Briones, E., & Van der Plas, A. K. (2010). Natural and human-induced hypoxia and consequences for coastal areas: synthesis and future development. Biogeosciences, 7, 1443–1467.

    Article  CAS  Google Scholar 

  • Zhu, Z. Y., Zhang, J., Wu, Y., Zhang, Y. Y., Lin, J., & Liu, S. M. (2011). Hypoxia off the Changjiang (Yangtze River) Estuary: Oxygen depletion and organic matter decomposition. Marine Chemistry, 125, 108–116.

    Article  CAS  Google Scholar 

  • Zhu, Z. Y., Liu, S. M., Wu, Y., Li, Y., Zhang, J., & Hu, J. (2015). Phytoplankton dynamics and its further implication for particulate organic carbon in surface waters of a tropical/subtropical estuary. Estuaries and Coasts, 38, 905–916.

    Article  CAS  Google Scholar 

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Acknowledgements

We express our gratitude to colleagues from the Ocean University of China, the Hainan Provincial Marine Development Plan and Design Research Institute, and the East China Normal University for their support in the field observations and laboratory work. Dr. J.A. Elvir and two anonymous reviewers are acknowledged; their constructive comments and suggestions improve the original manuscript.

Funding

The research project was implemented in 2008–2011 with the financial support from the Natural Science Foundation of China (Contract No. 40830850) and the Ministry of Science and Technology of China (Contract No. 2007DFB20380).

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Correspondence to Jing Zhang.

Appendix 1. Numerical model simulation for the Laoyehai

Appendix 1. Numerical model simulation for the Laoyehai

The 3-D ELCIRC hydrodynamic model solves for the free surface elevation, water velocity, and distribution of hydrographic parameters (e.g., salinity and temperature), using a set of six hydrostatic equations based on the Boussinesq approximation, which represent mass conservation in both 3-D and depth-integrated forms (Zhang and Baptista 2004). The governing equations are given below (A1–A4):

$$ \frac{\partial u}{\partial x}+\frac{\partial v}{\partial y}+\frac{\partial w}{\partial z}=0 $$
(A1)
$$ \frac{\partial \eta }{\partial t}+\frac{\partial }{\partial x}{\int}_{H_{R-\eta}}^{H_{R+\eta }} udz+\frac{\partial }{\partial y}{\int}_{H_{R-\eta}}^{H_{R+\eta }} udz=0 $$
(A2)
$$ \frac{Du}{Dt}= fv-\frac{\partial }{\partial x}\left\{g\left(\eta -\alpha \overset{\frown }{\psi}\right)+\frac{P_a}{\rho_0}\right\}-\frac{g}{\rho_0}{\int}_z^{H_{R+\eta }}\frac{\partial \rho }{\partial x} dz+\frac{\partial }{\partial z}\left({K}_{mv}\frac{\partial u}{\partial z}\right)+{F}_{mx} $$
(A3)
$$ \frac{Dv}{Dt}=- fu-\frac{\partial }{\partial y}\left\{g\left(n-\alpha \overset{\frown }{\psi}\right)+\frac{P_a}{\rho_0}\right\}-\frac{g}{\rho_0}{\int}_z^{H_{R+\eta }}\frac{\partial \rho }{\partial y} dz+\frac{\partial }{\partial z}\left({K}_{mv}\frac{\partial v}{\partial z}\right)+{F}_{my} $$
(A4)

where (x, y) are the horizontal Cartesian coordinates (m), ϕ, λ are the latitude and longitude, z is the vertical coordinate with upward being positive (m), t is time (s), HR is the z-coordinate at the reference level (i.e., mean sea level, MSL), η(x, y, t) is the free surface elevation (m), and h(x, y) is the bathymetric depth (m); \( \overrightarrow{u}\left(\overrightarrow{x},t\right) \) is the water velocity at \( \overrightarrow{x}\left(x,y,z\right) \), having Cartesian components (u, v, and w), in m/s; f is the Coriolis factor (per s), G is the acceleration under gravity (m/s), ψ(ϕ, λ) is the tidal potential (m), and α is the effective Earth elasticity factor; \( \rho \left(\overrightarrow{x},t\right) \) is the water density, for which the default reference value ρ0 is 1025 kg/m3; and Pa(x, y, t) is the atmospheric pressure at the free surface (N/m), Kmv is the vertical eddy viscosity (m2/s), and Fmx, Fmy is the horizontal diffusion for momentum and transport equations.

The differential system for the six primary variables (η, u, v, w, T, S) in Eqs. A1, A2, A3, and A4 is closed with the equation of state, the definition of the tidal potential and the Coriolis factor, parameterizations for vertical mixing, and initial and boundary conditions. Initial conditions require problem-dependent specification of pre-simulation fields for all primary variables and for any turbulence parameters required by the vertical mixing parameterization (Zhang and Baptista 2004).

In implementation, the model was firstly validated by time-series data of tidal level, current and hydrographic parameters (e.g., salinity and temperature) from anchor stations of 26 h for both spring and neap tides and the simulation results were compared to the section profiles of hydrography in different seasons (cf. HNMDDI 2011). Then the numerical simulations were applied to understand the hydrodynamic processes of Laoyehai using Lagrangian particles as passive tracer.

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Zhang, J., Zhu, Z., Mo, W.Y. et al. Hypoxia and nutrient dynamics affected by marine aquaculture in a monsoon-regulated tropical coastal lagoon. Environ Monit Assess 190, 656 (2018). https://doi.org/10.1007/s10661-018-7001-z

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