Mesozooplankton community in a seasonally hypoxic and highly eutrophic bay
Min-Chul Jang A , Kyoungsoon Shin A , Pung-Guk Jang A , Woo-Jin Lee A and Keun-Hyung Choi B CA Ballast Research Center, South Sea Research Institute, Korea Institute of Ocean Science and Technology, Geoje 656-834, South Korea.
B Department of Oceanography and Ocean Environmental Sciences, Chungnam National University, 99 Daehak-ro, Yuseong-gu, Daejeon 305-764, South Korea.
C Corresponding author. Email: keunhchoi@kiost.ac
Marine and Freshwater Research 66(8) 719-729 https://doi.org/10.1071/MF14036
Submitted: 8 February 2014 Accepted: 16 June 2014 Published: 10 March 2015
Abstract
A 2-year survey of seawater chemistry and mesozooplankton abundance was carried out in Masan Bay, South Korea, one of the most eutrophic coastal ecosystems known. The study aimed to identify the major factors contributing to the seasonally persistent hypoxia in the bay, to characterise the Bay’s mesozooplankton community and to examine the effects of low oxygen on the distribution of mesozooplankton. Hypoxia (<2 mg O2 L–1) was present only in summer, with ultrahypoxia (<0.2 mg O2 L–1) in the bottom waters of the inner bay in both years. Low summer oxygen can be attributed to high summer phytoplankton stocks, together with reduced oxygen solubility at high temperature and stratification of the water column that limits downward diffusion of oxygen. A seasonally and spatially distinct mesozooplankton community was identified in summer when there was greater influence of freshwater discharge in the inner bay. Marine cladocerans were very abundant, with a population outburst of Penilia avirostris in the inner bay (>4000 individuals m–3) during summer. During hypoxic events, the abundance of Penilia avirostris was positively related to oxygen levels in the bottom water, suggesting that hypoxic conditions may cause mortality or have sublethal negative effects on population growth of this filter-feeding cladoceran.
Additional keywords: cladoceran, hypoxia, Masan Bay, Penilia avirostris, stratification.
References
Atienza, D., Calbet, A., Saiz, E., Alcaraz, M., and Trepat, I. (2006). Trophic impact, metabolism, and biogeochemical role of the marine cladoceran Penilia avirostris and the co-dominant copepod Oithona nana in NW Mediterranean coastal waters. Marine Biology 150, 221–235.| Trophic impact, metabolism, and biogeochemical role of the marine cladoceran Penilia avirostris and the co-dominant copepod Oithona nana in NW Mediterranean coastal waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1elsbvP&md5=91409d7904046f2738be782bb9da874dCAS |
Badylak, S., and Phlips, E. J. (2008). Spatial and temporal distributions of zooplankton in Tampa Bay, Florida, including observations during a HAB event. Journal of Plankton Research 30, 449–465.
| Spatial and temporal distributions of zooplankton in Tampa Bay, Florida, including observations during a HAB event.Crossref | GoogleScholarGoogle Scholar |
Bennett, W. A. (2005). Critical assessment of the delta smelt population in the San Francisco Estuary, California. San Francisco Estuary and Watershed Science 3, 1–73.
| Critical assessment of the delta smelt population in the San Francisco Estuary, California.Crossref | GoogleScholarGoogle Scholar |
Calliari, D., Andersen Borg, M. C., Thor, P., Gorokhova, E., and Tiselius, P. (2008). Instantaneous salinity reductions affect the survival and feeding rates of the co-occurring copepods Acartia tonsa Dana and A. clausi Giesbrecht differently. Journal of Experimental Marine Biology and Ecology 362, 18–25.
| Instantaneous salinity reductions affect the survival and feeding rates of the co-occurring copepods Acartia tonsa Dana and A. clausi Giesbrecht differently.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosVOhsbs%3D&md5=3abab189a93b92d74af9c69089fa0f17CAS |
Cervetto, G., Gaudy, R., and Pagano, M. (1999). Influence of salinity on the distribution of Acartia tonsa (Copepoda, Calanoida). Journal of Experimental Marine Biology and Ecology 239, 33–45.
| Influence of salinity on the distribution of Acartia tonsa (Copepoda, Calanoida).Crossref | GoogleScholarGoogle Scholar |
Chang, K.-H., Imai, H., Ayukawa, K., Sugahara, S., Nakano, S.-i., and Seike, Y. (2013). Impact of improved bottom hypoxia on zooplankton community in shallow eutrophic lake. Knowledge and Management of Aquatic Ecosystems 408, 03.
| Impact of improved bottom hypoxia on zooplankton community in shallow eutrophic lake.Crossref | GoogleScholarGoogle Scholar |
Chang, W. K., Ryu, J., Yi, Y., Lee, W., Lee, C., Kang, D., Lee, C., Hong, S., and Nam, J. (2012). Improved water quality in response to pollution control measures at Masan Bay, Korea. Marine Pollution Bulletin 64, 427–435.
| Improved water quality in response to pollution control measures at Masan Bay, Korea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVOnurw%3D&md5=98385094160edc727b338c26268edf3aCAS | 22155120PubMed |
Clark, M. (2013). ‘Generalized Additive Models: Getting Started with Additive Models in R.’ (University of Notre Dame Press: Notre Dame, IN.)
Clarke, K. R. (1993). Nonparametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.
| Nonparametric multivariate analyses of changes in community structure.Crossref | GoogleScholarGoogle Scholar |
Diaz, R. J., and Rosenberg, R. (1995). Marine benthic hypoxia: a review of its ecological effects and the behavioral responses of benthic macrofauna. Oceanography and Marine Biology – an Annual Review 33, 245–303.
Ducklow, H. W., and Shiah, F. K. (1993). Bacterial production in estuaries. In ‘Aquatic Microbiology: an Ecological Approach’. (Ed. T. Ford.) pp. 261–287. (Blackwell Scientific: Boston, MA.)
Ekau, W., Auel, H., Pörtner, H. O., and Gilbert, D. (2010). Impacts of hypoxia on the structure and processes in pelagic communities (zooplankton, macro-invertebrates and fish). Biogeosciences 7, 1669–1699.
| Impacts of hypoxia on the structure and processes in pelagic communities (zooplankton, macro-invertebrates and fish).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtV2rtLjO&md5=c026ae8c16cc7daa4b08835d17ef8df0CAS |
Elliott, D. T., Pierson, J. J., and Roman, M. R. (2013a). Predicting the effects of coastal hypoxia on vital rates of the planktonic copepod Acartia tonsa Dana. PLOS ONE 8, e63987.
| Predicting the effects of coastal hypoxia on vital rates of the planktonic copepod Acartia tonsa Dana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXoslanurw%3D&md5=aa398a9fc8c05fda3b9b2b2461b1b3ddCAS | 23691134PubMed |
Elliott, D. T., Pierson, J. J., and Roman, M. R. (2013b). Copepods and hypoxia in Chesapeake Bay: abundance, vertical position and nonpredatory mortality. Journal of Plankton Research 35, 1027–1034.
| Copepods and hypoxia in Chesapeake Bay: abundance, vertical position and nonpredatory mortality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlGmtrbL&md5=b86d2c62e710e85a00561a007d5fb508CAS |
Froneman, P. W. (2004). Zooplankton community structure and biomass in a southern African temporarily open/closed estuary. Estuarine, Coastal and Shelf Science 60, 125–132.
| Zooplankton community structure and biomass in a southern African temporarily open/closed estuary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtlCjsbc%3D&md5=ce13d64aea0daa2b23b4a52b977e5d97CAS |
Frost, B. W. (1972). Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnology and Oceanography 17, 805–815.
| Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus.Crossref | GoogleScholarGoogle Scholar |
Goto, D., Lindelof, K., Fanslow, D. L., Ludsin, S. A., Pothoven, S. A., Roberts, J. J., Vanderploeg, H. A., Wilson, A. E., and Höök, T. O. (2012). Indirect consequences of hypolimnetic hypoxia on zooplankton growth in a large eutrophic lake. Aquatic Biology 16, 217–227.
| Indirect consequences of hypolimnetic hypoxia on zooplankton growth in a large eutrophic lake.Crossref | GoogleScholarGoogle Scholar |
Hastie, T. J., and Tibshirani, R. J. (1990). ‘Generalized Additive Models.’ (Chapman and Hall: London.)
Hong, J. S., and Lee, J. H. (1983). Effects of the pollution on the benthic macrofauna in Masan Bay, Korea. Journal of Oceanological Society of Korea 18, 169–173.
Jang, M. C., Shin, K., Hyun, B., Lee, T., and Choi, K. H. (2013). Temperature-regulated egg production rate, and seasonal and interannual variations in Paracalanus parvus. Journal of Plankton Research 35, 1035–1045.
| Temperature-regulated egg production rate, and seasonal and interannual variations in Paracalanus parvus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlGmtrbE&md5=ebc7d4cbf471815b541f33a4e814ec8dCAS |
Jang, P. G., Shin, K., Chang, M., and Kim, D. (2011). Spatial and temporal trends in water quality in response to sewage discharge in Masan and Hangam Bays, Korea. Journal of Coastal Research 275, 144–155.
| Spatial and temporal trends in water quality in response to sewage discharge in Masan and Hangam Bays, Korea.Crossref | GoogleScholarGoogle Scholar |
Johns, D. G., Edwards, M., Greve, W., and John, A. W. G. (2005). Increasing prevalence of the marine cladoceran Penilia avirostris (Dana 1852) in the North Sea. Helgoland Marine Research 59, 214–218.
| Increasing prevalence of the marine cladoceran Penilia avirostris (Dana 1852) in the North Sea.Crossref | GoogleScholarGoogle Scholar |
Jung, J. H., Kim, S. J., Lee, T. K., Shim, W. J., Woo, S., Kim, D. J., and Han, C. H. (2008). Biomarker responses in caged rockfish (Sebastes schlegeli) from Masan Bay and Haegeumgang, South Korea. Marine Pollution Bulletin 57, 599–606.
| Biomarker responses in caged rockfish (Sebastes schlegeli) from Masan Bay and Haegeumgang, South Korea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntlGmt74%3D&md5=6c32b3112dc1468fd301618103fadb51CAS | 18234237PubMed |
Kehayias, G., Ramfos, A., Ntzialas, P., Ioannou, S., Bisouki, P., Kyrtzoglou, E., Gianni, A., and Zacharias, I. (2013). Zooplankton diversity and distribution in a deep and anoxic Mediterranean coastal lake. Mediterranean Marine Science 14, 179–192.
| Zooplankton diversity and distribution in a deep and anoxic Mediterranean coastal lake.Crossref | GoogleScholarGoogle Scholar |
Keister, J. E., and Tuttle, L. B. (2013). Effects of bottom-layer hypoxia on spatial distributions and community structure of mesozooplankton in a sub-estuary of Puget Sound, Washington, USA. Limnology and Oceanography 58, 667–680.
| Effects of bottom-layer hypoxia on spatial distributions and community structure of mesozooplankton in a sub-estuary of Puget Sound, Washington, USA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvFyksLw%3D&md5=93485dc615561f5bb758a6bad6be9d2fCAS |
Kim, D., Lee, C. W., Choi, S. H., and Kim, Y. O. (2012). Long-term changes in water quality of Masan Bay, Korea. Journal of Coastal Research 283, 923–929.
| Long-term changes in water quality of Masan Bay, Korea.Crossref | GoogleScholarGoogle Scholar |
Kimmerer, W. J., Burau, J. R., and Bennett, W. A. (1998). Tidally oriented vertical migration and position maintenance of zooplankton in a temperate estuary. Limnology and Oceanography 43, 1697–1709.
| Tidally oriented vertical migration and position maintenance of zooplankton in a temperate estuary.Crossref | GoogleScholarGoogle Scholar |
Lee, C., and Lim, W. (2006). Variation of harmful algal blooms in Masan–Chinhae Bay. ScienceAsia 32, 51–56.
| Variation of harmful algal blooms in Masan–Chinhae Bay.Crossref | GoogleScholarGoogle Scholar |
Lee, C. W., and Min, B. Y. (1990). Pollution in Masan Bay, a matter of concern in South Korea. Marine Pollution Bulletin 21, 226–229.
| Pollution in Masan Bay, a matter of concern in South Korea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXivFOgtg%3D%3D&md5=a7747cfa9254f7dc7137870ba72faf5fCAS |
Lee, H. J., Hong, S. H., Kim, M., Ha, S. Y., An, S. M., and Shim, W. J. (2011). Tracing origins of sewage and organic matter using sterols in Masan and Haengam Bay, Korea. Ocean Science Journal 46, 95–103.
| Tracing origins of sewage and organic matter using sterols in Masan and Haengam Bay, Korea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVKksr7I&md5=0e80fabfaf74be14c844512231a3aa8dCAS |
Lim, H. S., Diaz, R. J., Hong, J. S., and Schaffner, L. C. (2006). Hypoxia and benthic community recovery in Korean coastal waters. Marine Pollution Bulletin 52, 1517–1526.
| Hypoxia and benthic community recovery in Korean coastal waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFOqsrzJ&md5=64abd5378f817606c217ef0e4b8c84e3CAS | 16860829PubMed |
Longhurst, A. R. (1985). The structure and evolution of plankton communities. Progress in Oceanography 15, 1–35.
| The structure and evolution of plankton communities.Crossref | GoogleScholarGoogle Scholar |
Marcus, N. H. (2001). Zooplankton: responses to and consequences of hypoxia. In ‘Coastal Hypoxia: Consequences for Living Resources and Ecosystems’. (Eds N. N. Rabalais and R. E. Turner.) pp. 49–60. (American Geophysical Union: Washington, DC.)
Marques, S. C., Pardal, M. A., Pereira, M. J., Goncalves, F., Marques, J. C., and Azeiteiro, U. M. (2007). Zooplankton distribution and dynamics in a temperate shallow estuary. Hydrobiologia 587, 213–223.
| Zooplankton distribution and dynamics in a temperate shallow estuary.Crossref | GoogleScholarGoogle Scholar |
Mayer, C. M., and Wahl, D. H. (1997). The relationship between prey selectivity and growth and survival in a larval fish. Canadian Journal of Fisheries and Aquatic Sciences 54, 1504–1512.
| The relationship between prey selectivity and growth and survival in a larval fish.Crossref | GoogleScholarGoogle Scholar |
Moon, S. Y., Oh, H. J., and Soh, H. Y. (2010). Seasonal variation of zooplankton communities in the southern coastal waters of Korea. Ocean and Polar Research 32, 411–426.
| Seasonal variation of zooplankton communities in the southern coastal waters of Korea.Crossref | GoogleScholarGoogle Scholar |
Nixon, S. W. (1995). Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41, 199–219.
| Coastal marine eutrophication: a definition, social causes, and future concerns.Crossref | GoogleScholarGoogle Scholar |
Nomura, H., Aihara, K., and Ishimaru, T. (2007). Feeding of the chaetognath Sagitta crassa Tokioka in heavily eutrophicated Tokyo Bay, Japan. Plankton and Benthos Research 2, 120–127.
| Feeding of the chaetognath Sagitta crassa Tokioka in heavily eutrophicated Tokyo Bay, Japan.Crossref | GoogleScholarGoogle Scholar |
Oh, H.-T., Lee, W.-C., Koo, J.-H., Park, S.-E., Hong, S.-J., Jung, R.-H., and Park, J.-S. (2006). Marine ecosystem response to nutrient input reduction in Jinhae Bay, South Korea. Journal of Environmental Sciences 15, 819–827.
| Marine ecosystem response to nutrient input reduction in Jinhae Bay, South Korea.Crossref | GoogleScholarGoogle Scholar |
Pearre, S. (1980). Feeding by chaetognatha: the relation of prey size to predator size in several species. Marine Ecology Progress Series 3, 125–134.
| Feeding by chaetognatha: the relation of prey size to predator size in several species.Crossref | GoogleScholarGoogle Scholar |
Powers, S. P., Harper, D. E., and Rabalais, N. N. (2013). Effect of hypoxia/anoxia on the supply and settlement of benthic invertebrate larvae. In ‘Coastal Hypoxia: Consequences for Living Resources and Ecosystems’. (Eds N. N. Rabalais and R. E. Turner.) pp. 185–210. (American Geophysical Union: Washington, DC.)
Primo, A. L., Azeiteiro, U. M., Marques, S. C., Martinho, F., and Pardal, M. A. (2009). Changes in zooplankton diversity and distribution pattern under varying precipitation regimes in a southern temperate estuary. Estuarine, Coastal and Shelf Science 82, 341–347.
| Changes in zooplankton diversity and distribution pattern under varying precipitation regimes in a southern temperate estuary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjtlOltLs%3D&md5=20ed6cb30b1199311ffd66df0da29ef5CAS |
Ramfos, A., Isari, S., Somarakis, S., Georgopoulos, D., Koutsikopoulos, C., and Fragopoulu, N. (2006). Mesozooplankton community structure in offshore and coastal waters of the Ionian Sea (eastern Mediterranean) during mixed and stratified conditions. Marine Biology 150, 29–44.
| Mesozooplankton community structure in offshore and coastal waters of the Ionian Sea (eastern Mediterranean) during mixed and stratified conditions.Crossref | GoogleScholarGoogle Scholar |
Roman, M., Zhang, X., McGilliard, C., and Boicourt, W. (2005). Seasonal and annual variability in the spatial patterns of plankton biomass in Chesapeake Bay. Limnology and Oceanography 50, 480–492.
| Seasonal and annual variability in the spatial patterns of plankton biomass in Chesapeake Bay.Crossref | GoogleScholarGoogle Scholar |
Roman, M. R., Pierson, J. J., Kimmel, D. G., Boicourt, W. C., and Zhang, X. (2012). Impacts of hypoxia on zooplankton spatial distributions in the northern Gulf of Mexico. Estuaries and Coasts 35, 1261–1269.
| Impacts of hypoxia on zooplankton spatial distributions in the northern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFOhtb3P&md5=bfb707a10efaf28edceb7435673121faCAS |
Selman, M., Greenhalgh, S., Diaz, R., and Sugg, Z. (2008). Eutrophication and hypoxia in coastal areas: a global assessment of the state of knowledge. Water Quality: Eutrophication and Hypoxia Policy Note Series 1, 1–6. World Resources Institute, Washington, DC.
Seo, J. Y., Park, S. H., Lee, J. H., and Choi, J. W. (2012). Structural changes in macrozoobenthic communities due to summer hypoxia in Gamak Bay, Korea. Ocean Science Journal 47, 27–40.
| Structural changes in macrozoobenthic communities due to summer hypoxia in Gamak Bay, Korea.Crossref | GoogleScholarGoogle Scholar |
Shiah, F. K., and Ducklow, H. W. (1994). Temperature regulation of heterotrophic bacterioplankton abundance, production, and specific growth rate in Chesapeake Bay. Limnology and Oceanography 39, 1243–1258.
| Temperature regulation of heterotrophic bacterioplankton abundance, production, and specific growth rate in Chesapeake Bay.Crossref | GoogleScholarGoogle Scholar |
Smith, V. (2003). Eutrophication of freshwater and coastal marine ecosystems a global problem. Environmental Science and Pollution Research International 10, 126–139.
| Eutrophication of freshwater and coastal marine ecosystems a global problem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVCgsrs%3D&md5=c568d8f593e1427b8d4deb2c6ef5fca8CAS | 12729046PubMed |
Soh, H. Y., Lee, I.-T., Yoon, Y. H., Choi, S. D., Lee, S. N., Han, M. I., Kim, B. S., Kang, Y. H., and Lee, W. B. (2002). Species composition and occurrence patterns of zooplankton in Gamag Bay. Korean Journal of Environmental Biology 20, 118–129.
Stalder, L. C., and Marcus, N. H. (1997). Zooplankton responses to hypoxia: behavioral patterns and survival of three species of calanoid copepods. Marine Biology 127, 599–607.
| Zooplankton responses to hypoxia: behavioral patterns and survival of three species of calanoid copepods.Crossref | GoogleScholarGoogle Scholar |
Stoecker, D. K., and Capuzzo, J. M. (1990). Predation on Protozoa: its importance to zooplankton. Journal of Plankton Research 12, 891–908.
| Predation on Protozoa: its importance to zooplankton.Crossref | GoogleScholarGoogle Scholar |
Tett, P., Gilpin, L., Svendsen, H., Erlandsson, C. P., Larsson, U., Kratzer, S., Fouilland, E., Janzen, C., Lee, J., Grenz, C., Newton, A., Ferreira, J. G., Fernandes, T., and Scory, S. (2003). Eutrophication and some European waters of restricted exchange. Continental Shelf Research 23, 1635–1671.
| Eutrophication and some European waters of restricted exchange.Crossref | GoogleScholarGoogle Scholar |
Thompson, A. B., and Harrop, R. T. (1991). Feeding dynamics of fish larvae on Copepoda in the western Irish Sea, with particular reference to cod Gadus morhua. Marine Ecology Progress Series 68, 213–223.
| Feeding dynamics of fish larvae on Copepoda in the western Irish Sea, with particular reference to cod Gadus morhua.Crossref | GoogleScholarGoogle Scholar |
Vieira, L., Azeiteiro, U., Ré, P., Pastorinho, R., Marques, J. C., and Morgado, F. (2003). Zooplankton distribution in a temperate estuary (Mondego estuary southern arm: western Portugal). Acta Oecologica 24, S163–S173.
| Zooplankton distribution in a temperate estuary (Mondego estuary southern arm: western Portugal).Crossref | GoogleScholarGoogle Scholar |
Wood, S. N. (2006). ‘Generalized Additive Models: An Introduction with R.’ (Chapman and Hall: Boca Raton, FL, USA.)
Yim, U. H., Hong, S. H., Shim, W. J., Oh, J. R., and Chang, M. (2005). Spatio-temporal distribution and characteristics of PAHs in sediments from Masan Bay, Korea. Marine Pollution Bulletin 50, 319–326.
| Spatio-temporal distribution and characteristics of PAHs in sediments from Masan Bay, Korea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitF2ns70%3D&md5=83fc37f8019abd56c95ed58ea9a06210CAS | 15757695PubMed |
Yoo, K. I. (1991). Population dynamics of dinoflagellate community in Masan Bay with a note on the impact of environmental parameters. Marine Pollution Bulletin 23, 185–188.
| Population dynamics of dinoflagellate community in Masan Bay with a note on the impact of environmental parameters.Crossref | GoogleScholarGoogle Scholar |
Zettler, M., Bochert, R., and Pollehne, F. (2009). Macrozoobenthos diversity in an oxygen minimum zone off northern Namibia. Marine Biology 156, 1949–1961.
| Macrozoobenthos diversity in an oxygen minimum zone off northern Namibia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosVygtr8%3D&md5=1c2d7f940f6388077b70382cd53c26c7CAS |