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Seasonal and regional differences in long-term changes in large mesozooplankton (>505 μm) biomass and abundance in a semi-enclosed subtropical bay

  • Ecology
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Abstract

Obvious spatiotemporal heterogeneity is a distinct characteristic of ecosystems in subtropical bays. To aid targeted management and ecological restoration in long and narrow semi-enclosed subtropical bays, we analyzed seasonal and regional differences in long-term changes (1980–2019) in the biomass and abundance of large mesozooplankton (LMZ; >505 µm) in **angshan Bay, Zhejiang, China. We found spatiotemporal heterogeneity in the historical changes of LMZ. Significant negative trends in LMZ biomass were found in the inner and middle bay during the warm season (summer and autumn), when the nutrient concentration (especially dissolved inorganic nitrogen) and temperature increased simultaneously. Nutrient changes in **angshan Bay began in the late 1980s or early 1990s, coinciding with large-scale fish cage development. A rapid decline in LMZ biomass occurred after 2005 when power plants commenced operation, accelerating the warming trend. Therefore, the joint stress of eutrophication and warming likely precipitated the decline in LMZ biomass. Conversely, a significant increase in LMZ biomass was found in the outer bay in spring. This trend was consistent with the trend of LMZ biomass near the Changjiang (Yangtze) River estuary, which indicates that the pelagic ecosystem in the outer bay was affected by water from the Changjiang River estuary during spring. Based on our results, ecosystem management and restoration in semi-enclosed subtropical bays should focus on internal waters, which have a poor capacity for water exchange. For **angshan Bay, the changes in the Changjiang River estuary ecosystem during the cold season (winter and spring) should also be considered.

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Data Availability Statement

All data generated and/or analyzed during this study are included in this published article and its supplementary information files.

References

  • Bo H P. 1984. Report on zooplankton survey in **angshan Bay. Marine Fisheries, 6(6): 249–253. (in Chinese)

    Google Scholar 

  • Cloern J E. 2018. Why large cells dominate estuarine phytoplankton. Limnology and Oceanography, 63(S1): S392–S409, https://doi.org/10.1002/lno.10749.

    Article  Google Scholar 

  • Daufresne M, Lengfellner K, Sommer U. 2009. Global warming benefits the small in aquatic ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 106(31): 12788–12793, https://doi.org/10.1073/pnas.0902080106.

    Article  Google Scholar 

  • Dong L X, Su J L. 1999. Numerical study of water exchange in **angshangang bay II. model application and water exchange study. Oceanologia et Limnologia Sinica, 30(5): 465–470. (in Chinese with English abstract)

    Google Scholar 

  • Dong Z J, Liu D Y, Keesing J K. 2010. Jellyfish blooms in China: dominant species, causes and consequences. Marine Pollution Bulletin, 60(7): 954–963, https://doi.org/10.1016/j.marpolbul.2010.04.022.

    Article  Google Scholar 

  • Du P, Jiang Z B, Wang Y M, Qian P. 2019. Spatial heterogeneity of the planktonic protistan community in a semi-closed eutrophic bay, China. Journal of Plankton Research, 41(3): 223–239, https://doi.org/10.1093/plankt/fbz012.

    Article  Google Scholar 

  • Du P, Jiang Z B, Zhu Y L, Tang Y B, Liao Y B, Chen Q Z, Zeng J N, Shou L. 2020. What factors control the variations in abundance, biomass, and size of mesozooplankton in a subtropical eutrophic bay? Estuaries and Coasts, 43(8): 2128–2140, https://doi.org/10.1007/s12237-020-00747-8.

    Article  Google Scholar 

  • Du P, Liao Y B, Jiang Z B, Wang K, Zeng J N, Shou L, Xu X Q, Xu X D, Liu J J, Huang W, Zhang D M. 2017. Responses of mesozooplankton communities to different anthropogenic activities in a subtropical semi-enclosed bay. Journal of the Marine Biological Association of the United Kingdom, 98(4): 1–14, https://doi.org/10.1017/S0025315416001995.

    Google Scholar 

  • Du P, Xu X Q, Liu J J, Jiang Z B, Chen Q Z, Zeng J N. 2015. Spatial heterogeneity of macro, and meso-zooplankton in **angshan Bay in spring and summer. Acta Ecologica Sinica, 35(7): 2308–2321, https://doi.org/10.5846/stxb201306091487. (in Chinese with English abstract)

    Google Scholar 

  • Du P. 2018. The Spatio-Temporal Variation and the Driving Factors of Mesozooplankton Community in **angshan Bay. Ningbo University, Ningbo. (in Chinese)

    Google Scholar 

  • Edition Committee of the Bay Chorography in China (ECBCC). 1992. The Bay Chorography in China (5). China Ocean Press, Bei**g, China. p.166–233. (in Chinese)

    Google Scholar 

  • Fan A D, ** X S. 1989. Tidal effect on nutrient exchange in **angshan Bay, China. Marine Chemistry, 27(3–4): 259–281, https://doi.org/10.1016/0304-4203(89)90051-0.

    Google Scholar 

  • Fernández-Urruzola I, Osma N, Packard T T, Gómez M, Postel L. 2014. Distribution of zooplankton biomass and potential metabolic activities across the northern Benguela upwelling system. Journal of Marine Systems, 140: 138–149, https://doi.org/10.1016/j.jmarsys.2014.05.009.

    Article  Google Scholar 

  • Gao S, **e C Q, Feng Y J. 1990. Fine-grained sediment transport and sorting by tidal exchange in **angshan Bay, Zhejiang, China. Estuarine, Coastal and Shelf Science, 31(4): 397–409, https://doi.org/10.1016/0272-7714(90)90034-O.

    Article  Google Scholar 

  • García-Comas C, Stemmann L, Ibanez F, Berline L, Mazzocchi M G, Gasparini S, Picheral M, Gorsky G. 2011. Zooplankton long-term changes in the NW Mediterranean Sea: decadal periodicity forced by winter hydrographic conditions related to large-scale atmospheric changes? Journal of Marine Systems, 87(3–4): 216–226, https://doi.org/10.1016/j.jmarsys.2011.04.003.

    Article  Google Scholar 

  • GB 17378.4-1998/2007. The Specification for Marine Monitoring Part 4: Seawater Analysis. Standards Press, Bei**g, China. 1–162. (in Chinese)

  • Glibert P M. 2010. Long-term changes in nutrient loading and stoichiometry and their relationships with changes in the food web and dominant pelagic fish species in the San Francisco estuary, California. Reviews in Fisheries Science, 18(2): 211–232, https://doi.org/10.1080/10641262.2010.492059.

    Article  Google Scholar 

  • Gu X G, Xu Z L. 1993. Study on the phytoplankton ecology and red tide of middle and western **angshan Bay. Marine Fisheries, 15(5): 199–204. (in Chinese with English abstract)

    Google Scholar 

  • Hao Y J, Tang D L, Boicenco L, Wang S F. 2016. Environmental ecological response to increasing water temperature in the Daya Bay, Southern China in 1982–2012. Natural Resources, 7(4): 184–192, https://doi.org/10.4236/nr.2016.74017.

    Article  Google Scholar 

  • Huang X Q, Ye S F. 2014. Monitoring and Impact Assessment of Temperature Increase Caused by Thermal Discharge from Power Plants in the **angshan Bay. China Ocean Press, Bei**g. p.1–5. (in Chinese)

    Google Scholar 

  • Hughes L. 2000. Biological consequences of global warming: is the signal already apparent? Trends in Ecology & Evolution, 15(2): 56–61, https://doi.org/10.1016/S0169,5347(99)01764-4.

    Article  Google Scholar 

  • Jiang Z B, Du P, Liu J J, Chen Y, Zhu Y L, Shou L, Zeng J N, Chen J F. 2019a. Phytoplankton biomass and size structure in **angshan Bay, China: current state and historical comparison under accelerated eutrophication and warming. Marine Pollution Bulletin, 142: 119–128, https://doi.org/10.1016/j.marpolbul.2019.03.013.

    Article  Google Scholar 

  • Jiang Z B, Gao Y X, Chen Y, Du P, Zhu X Y, Liao Y B, Liu X Y, Zeng J N. 2019b. Spatial heterogeneity of phytoplankton community shaped by a combination of anthropogenic and natural forcings in a long narrow bay in the East China Sea. Estuarine, Coastal and Shelf Science, 217: 250–261, https://doi.org/10.1016/j.ecss.2018.11.028.

    Article  Google Scholar 

  • Jiang Z B, Liu J J, Chen J F, Chen Q Z, Yan X J, Xuan J L, Zeng J N. 2014. Responses of summer phytoplankton community to drastic environmental changes in the Changjiang (Yangtze River) estuary during the past 50 years. Water Research, 54: 1–11. https://doi.org/10.1016/j.watres.2014.01.032.

    Article  Google Scholar 

  • Kideys A E, Kovalev A V, Shulman G, Gordina A, Bingel F. 2000. A review of zooplankton investigations of the Black Sea over the last decade. Journal of Marine Systems, 24(3–4): 355–371, https://doi.org/10.1016/S0924-7963(99)00095-0.

    Article  Google Scholar 

  • Kimmel D G, Boynton W R, Roman M R. 2012. Long-term decline in the calanoid copepod Acartia tonsa in central Chesapeake Bay, USA: an indirect effect of eutrophication? Estuarine, Coastal and Shelf Science, 101: 76–85, https://doi.org/10.1016/j.ecss.2012.02.019.

    Article  Google Scholar 

  • Kong F Z, Xu Z J, Yu R C, Yuan Y Q, Zhou M J. 2016. Distribution patterns of phytoplankton in the Changjiang River estuary and adjacent waters in spring 2009. Chinese Journal of Oceanology and Limnology, 34(5): 902–914, https://doi.org/10.1007/s00343-016-4202-6.

    Article  Google Scholar 

  • Lam-Hoai T, Guiral D, Rougier C. 2006. Seasonal change of community structure and size spectra of zooplankton in the Kaw River estuary (French Guiana). Estuarine, Coastal and Shelf Science, 68(1–2): 47–61, https://doi.org/10.1016/j.ecss.2006.01.009.

    Article  Google Scholar 

  • Lehman P W, Teh S J, Boyer G L, Nobriga M L, Bass E, Hogle C. 2010. Initial impacts of Microcystis aeruginosa blooms on the aquatic food web in the San Francisco Estuary. Hydrobiologia, 637: 229–248, https://doi.org/10.1007/s10750-009-9999-y.

    Article  Google Scholar 

  • Li Y, Li D J, Tang J L, Wang Y M, Liu Z G, He S Q. 2010. Long-term changes in the Changjiang Estuary plankton community related to anthropogenic eutrophication. Aquatic Ecosystem Health & Management, 13(1): 66–72, https://doi.org/10.1080/14634980903579942.

    Article  Google Scholar 

  • Luo X F, Wei H, Wang Y H. 2012. Processes influencing jellyfish particle tracking in the Yellow Sea and East China Sea. Oceanologia et Limnologia Sinica, 43(3): 635–642, https://doi.org/10.11693/hyhz201203034034. (in Chinese with English abstract)

    Google Scholar 

  • Luo X, Zeng J N, Xu X Q, Du P. 2018. Distribution of zooplankton in the **angshan Bay and its changes during longer period. Marine Science Bulletin, 37(1): 74–87, https://doi.org/10.11840/j.issn.1001-6392.2018.01.010.

    Google Scholar 

  • Micheli F. 1999. Eutrophication, fisheries, and consumer, resource dynamics in marine pelagic ecosystems. Science, 285(5432): 1396–1398, https://doi.org/10.1126/science.285.5432.1396.

    Article  Google Scholar 

  • Ning X R, Lin C L, Su J L, Liu C G, Hao Q, Le F F, Tang Q S. 2010. Long-term environmental changes and the responses of the ecosystems in the Bohai Sea during 1960–1996. Deep Sea Research Part II: Topical Studies in Oceanography, 57(11–12): 1079–1091, https://doi.org/10.1016/j.dsr2.2010.02.010.

    Article  Google Scholar 

  • Ning X R, Shi J X, Liu Z L, Cai Y M. 1997. Abundance and distribution of photosynthetic picoplankton and their environmental constraints in **angshan Bay. Acta Oceanologica Sinica, 19(1): 87–95. (in Chinese)

    Google Scholar 

  • Ning X, Lin C, Su J, Liu C, Hao Q, Le F. 2011. Long-term changes of dissolved oxygen, hypoxia, and the responses of the ecosystems in the East China Sea from 1975 to 1995. Journal of Oceanography, 67(1): 59–75, https://doi.org/10.1007/s10872-011-0006-7.

    Article  Google Scholar 

  • Nobre A M, Ferreira J G, Nunes J P, Yan X Y, Bricker S, Corner R, Groom S, Gu H F, Hawkins A J S, Hutson R, Lan D Z, Silva J D L, Pascoe P, Telfer T, Zhang X L, Zhu M Y. 2010. Assessment of coastal management options by means of multilayered ecosystem models. Estuarine, Coastal and Shelf Science, 87(1): 43–62, https://doi.org/10.1016/j.ecss.2009.12.013.

    Article  Google Scholar 

  • Park G S, Marshall H G. 2000. Estuarine relationships between zooplankton community structure and trophic gradients. Journal of Plankton Research, 22(1): 121–136, https://doi.org/10.1093/plankt/22.1.121.

    Article  Google Scholar 

  • Parsons T R, Lalli C M. 2002. Jellyfish population explosions: revisiting a hypothesis of possible causes. La Mer, 40: 111–121.

    Google Scholar 

  • Piontkovski S A, Castellani C. 2009. Long-term declining trend of zooplankton biomass in the Tropical Atlantic. Hydrobiologia, 632: 365–370, https://doi.org/10.1007/s10750-009-9854-1.

    Article  Google Scholar 

  • Salmi T, Määttä A, Anttila P, Ruoho-Airola T, Amnell T. 2002. Detecting Trends of Annual Values of Atmospheric Pollutants by the Mann-Kendall Test and Sen’s Slope Estimates-the Excel Template Application MAKESENS. Publications on Air Quality 31. Finnish Meteorological Institute, Helsinki.

    Google Scholar 

  • Salvador B, Bersano J G F. 2017. Zooplankton variability in the subtropical estuarine system of Paranaguá Bay, Brazil, in 2012 and 2013. Estuarine, Coastal and Shelf Science, 199: 1–13, https://doi.org/10.1016/j.ecss.2017.09.019.

    Article  Google Scholar 

  • Shurin J B, Borer E T, Seabloom E W, Anderson K, Blanchette C A, Broitman B, Cooper S D, Halpern B S. 2002. A cross-ecosystem comparison of the strength of trophic cascades. Ecology Letters, 5(6): 785–791, https://doi.org/10.1046/j.1461-0248.2002.00381.x.

    Article  Google Scholar 

  • Steinberg D K, Lomas M W, Cope J S. 2012. Long-term increase in mesozooplankton biomass in the Sargasso Sea: linkage to climate and implications for food web dynamics and biogeochemical cycling. Global Biogeochemical Cycles, 26(1): 1–16, https://doi.org/10.1029/2010GB004026.

    Article  Google Scholar 

  • Stibor H, Vadstein O, Diehl S, Gelzleichter A, Hansen T, Hantzsche F, Katechakis A, Lippert B, Løseth K, Peters C, Roederer W, Sandow M, Sundt-Hansen L, Olsen Y 2004. Copepods act as a switch between alternative trophic cascades in marine pelagic food webs. Ecology Letters, 7(4): 321–328, https://doi.org/10.1111/j.1461-0248.2004.00580.x.

    Article  Google Scholar 

  • Tang F H, Li L, Liao Y, Wang Y L. 2012. Spatial and temporal distribution on fishery resources of marine pasture demonstration area in **angshan Harbor. Journal of Zhejiang University (Science Edition), 39(6): 696–702, https://doi.org/10.3785/j.issn.1008-9497.2012.06.018. (in Chinese with English abstract)

    Google Scholar 

  • The R Development Core Team. 2020. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

    Google Scholar 

  • Uye S I. 1994. Replacement of large copepods by small ones with eutrophication of embayments: cause and consequence. Hydrobiologia, 292–293(1): 513–519, https://doi.org/10.1007/BF00229979.

    Article  Google Scholar 

  • Valencia B, Landry M R, Décima M, Hannides C C S. 2016. Environmental drivers of mesozooplankton biomass variability in the North Pacific Subtropical Gyre. Journal of Geophysical Research: Biogeosciences, 121(12): 3131–3143, https://doi.org/10.1002/2016JG003544.

    Article  Google Scholar 

  • Wang C S, Liu Z S, He D H. 2003. Seasonal dynamics of zooplankton biomass and abundance in **angshan Bay. Journal of Fisheries of China, 27(6): 595–599, https://doi.org/10.3321/j.issn:1000-0615.2003.06.015. (in Chinese with English abstract)

    Google Scholar 

  • Wang K, Wang R, Zuo T, Gao S W. 2004. Analysis of zooplankton biomass in Changjiang River Estuary and adjacent waters. Oceanologia et Limnologia Sinica, 35(6): 568–576, https://doi.org/10.3321/j.issn:0029-814X.2004.06.014.

    Google Scholar 

  • Wang L, Chen Q W, Han R, Wang B D, Tang X U. 2016a. Zooplankton community in Yangtze River Estuary and adjacent sea areas after the impoundment of the Three Gorges Reservoir. Annales de Limnologie-International Journal of Limnology, 52: 273–284, https://doi.org/10.1051/limn/2016015.

    Article  Google Scholar 

  • Wang L, Wang B D, Chen Q W, Tang X W. 2016b. Characteristics of the zooplankton community and impactfactors in the Yangtze estuary coastal eara after third stage impoundment of the Three Gorges Dam. Acta Ecologica Sinica, 36(9): 2505–2512, https://doi.org/10.5846/stxb201412062423. (in Chinese with English abstract)

    Google Scholar 

  • Wang Y H, Tang R Y, Jiang G C, Dong H L, Lei P F, Lu Y. 1984. Distribution features of the chemical elements in **ang Shan Bay, Zhejiang. Donghai Marine Science, 2(1): 57–62. (in Chinese with English abstract)

    Google Scholar 

  • Wang Y T, Li S F, Yang L L, Yuan X Y, Jiang Y Z, Lin N. 2017. Species composition of larval and juvenile fish in the **angshan Bay in spring and summer. Marine Fisheries, 39(3): 286–295. (in Chinese with English abstract)

    Google Scholar 

  • Wang Y T, Sun S, Wang S W, Wang M X, Zhang G T. 2012. Geographical variations in abundance and size of Aequorea coerulescens in the Yellow and East China Seas in spring 2011. Oceanologia et Limnologia Sinica, 43(6): 1096–1102. (in Chinese with English abstract)

    Google Scholar 

  • Xu Z L. 2006. Dynamics of medusa abundance in the East China Sea. Acta Zoologica Sinica, 52(5): 854–861. (in Chinese with English abstract)

    Google Scholar 

  • Xu Z L. 2009. Water environment adaptability and ecological groups of Hydroidomedusae in East China Sea. Chinese Journal of Applied Ecology, 20(1): 177–184. (in Chinese with English abstract)

    Google Scholar 

  • Ye M Y, Li J L, Shi X L, Jiang Y M, Shi Z Q, Xu L H, He G L, Huang R P, Feng B X. 2017a. Spatial pattern change of the coastline development and utilization in Zhejiang from 1990 to 2015. Geographical Research, 36(6): 1159–1170, https://doi.org/10.11821/dlyj201706013. (in Chinese with English abstract)

    Google Scholar 

  • Ye R, Liu L, Wang Q, Ye X S, Cao W, He Q Y, Cai Y H. 2017b. Identification of coastal water quality by multivariate statistical techniques in two typical bays of northern Zhejiang Province, East China Sea. Acta Oceanologica Sinica, 36(2): 1–10, https://doi.org/10.1007/s13131-017-0981-7.

    Article  Google Scholar 

  • Zeng X M, He R Y, Zong H B. 2017. Variability of Changjiang Diluted Water revealed by a 45-year long-term ocean hindcast and Self-Organizing Maps analysis. Continental Shelf Research, 146: 37–46, https://doi.org/10.1016/j.csr.2017.08.010.

    Article  Google Scholar 

  • Zhong H Y. 1988. Distributional features of chemical factors in the Mid-West part of **ang Shan Bay, Zhejiang. Journal of Zhejiang College of Fisheries, 6(1): 53–61. (in Chinese with English abstract)

    Google Scholar 

  • Zuo T, Wang J, Wu Q, Yuan W, Luan Q S. 2016. Spatial distribution and biomass of large jellyfish in the Yellow Sea and Northern Part of the East China Sea in May 2015. Oceanologia et Limnologia Sinica, 47(1): 195–204. (in Chinese with English abstract)

    Google Scholar 

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Acknowledgment

We are grateful to **aoya LIU, **g**g ZHANG, and **angyu SUN in the SIO, MNR, China for their cooperation with the nutrient analysis. We are also grateful to the anonymous reviewers for improving the quality of the present manuscript.

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Authors and Affiliations

  1. Key Laboratory of Marine Ecosystem Dynamics, Second Institute of Oceanography, Ministry of Natural Resources (MNR), Hangzhou, 310012, China

    ** Du, Zhibing Jiang, Yuanli Zhu, Yibo Liao, Quanzhen Chen, Jiangning Zeng & Lu Shou

  2. Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China

    ** Du & Zhibing Jiang

  3. Key Laboratory of Ocean Space Resource Management Technology, MNR, Hangzhou, 310012, China

    ** Du, Zhibing Jiang & Yibo Liao

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Correspondence to Lu Shou.

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Supported by the National Key Research and Development Program of China (Nos. 2018YFD0900901, 2018YFD0900905), the Long Term Observation and Research Plan in the Changjiang River estuary and the Adjacent East China Sea Project (LORCE) (No. 14282), the National Natural Science Foundation of China (Nos. 41806149, 41806181, 41706125), and the NSFC-Zhejiang Joint Fund, China (No. U1709202)

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Du, P., Jiang, Z., Zhu, Y. et al. Seasonal and regional differences in long-term changes in large mesozooplankton (>505 μm) biomass and abundance in a semi-enclosed subtropical bay. J. Ocean. Limnol. 39, 2281–2294 (2021). https://doi.org/10.1007/s00343-021-0347-z

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