Skip to main content

Advertisement

SpringerLink
Log in

Combined Effects of Drift Macroalgal Bloom and Warming on Occurrence and Intensity of Diel-Cycling Hypoxia in a Eutrophic Coastal Lagoon

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Recently, eutrophication-induced macroalgal bloom and elevating temperature caused by climate change have become major threats to benthic organisms by causing coastal hypoxia. However, combined effects of drift macroalgae and warming on the occurrence and intensity of hypoxia are not well understood, although these anthropogenic stressors have co-occurred. We conducted 10 seasonally replicated 7-day algal enclosure/exclosure experiments at a shallow coastal zone in the eutrophic Nakaumi Lagoon, western Japan, to evaluate the combined effects of drift algae and water warming on occurrence and intensity of diel-cycling hypoxia. Experimental units were 1 × 1 m plots of the sandy bottom fenced within 1 m height with plastic mesh that excluded or included drift algae, with automated dissolved oxygen (DO) sensors deployed at the sediment surface. DO fluctuated over a diel cycle for both algal treatments, and algal presence and elevated temperature additively amplified the diel DO cycle. Algal presence and elevated temperature synergistically increased the occurrence and intensity of diel-cycling hypoxia. The occurrence of hypoxia, including anoxia, increased non-linearly in the presence of algae when mean water temperature exceeded ~ 25 °C, whereas such drastic increase in the hypoxia occurrence was not observed in the absence of algae. Furthermore, the daily minimum DO declined more steeply with warming under algal presence than the absence of algae. These results suggest that coastal areas in the lagoon are now seriously threatened by simultaneous progressions of eutrophication linking to algal bloom and global warming.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arroyo, N.L., and E. Bonsdorff. 2016. The role of drifting algae for marine biodiversity. In Marine macrophytes as foundation species, ed. E. Olafsson, 100–129. London: CRC press, Taylor & Francis group.

    Chapter  Google Scholar 

  • Beck, N.G., and K.W. Bruland. 2000. Diel biogeochemical cycling in a hyperventilating shallow estuarine environment. Estuaries 23 (2): 177–187.

    Article  CAS  Google Scholar 

  • Beck, N.G., A.T. Fisher, and K.W. Bruland. 2001. Modeling water, heat, and oxygen budgets in a tidally dominated estuarine pond. Marine Ecology Progress Series 217: 43–58.

    Article  Google Scholar 

  • Berglund, J., J. Mattila, O. Rönnberg, J. Heikkilä, and E. Bonsdorff. 2003. Seasonal and inter-annual variation in occurrence and biomass of rooted macrophytes and drift algae in shallow bays. Estuarine, Coastal and Shelf Science 56 (5-6): 1167–1175.

    Article  Google Scholar 

  • Boynton, W.R., J.D. Hagy, L. Murray, C. Stokes, and W.M. Kemp. 1996. A comparative analysis of eutrophication patterns in a temperate coastal lagoon. Estuaries 19 (2): 408–421.

    Article  CAS  Google Scholar 

  • Brown, J.H., J.F. Gillooly, A.P. Allen, V.M. Savage, and G.B. West. 2004. Toward a metabolic theory of ecology. Ecology 85 (7): 1771–1789.

    Article  Google Scholar 

  • Burkholder, J.M., D.A. Tomasko, and B.W. Touchette. 2007. Seagrasses and eutrophication. Journal of Experimental Marine Biology and Ecology 350 (1-2): 46–72.

    Article  Google Scholar 

  • Burnham, P.K., and D.R. Anderson. 2002. Models selection and multi-model inference: A practical information—Theoretic approach. New York: Springer–Verlag.

    Google Scholar 

  • Coffin, M.R.S., K.M. Knysh, E.F. Theriault, C.C. Pater, S.C. Courtenay, and M.R. van den Heuvel. 2017. Are floating algal mats a refuge from hypoxia for estuarine invertebrates? PeerJ 5: e3080. https://doi.org/10.7717/peerj.3080.

    Article  Google Scholar 

  • Conley, D.J., J. Carstensen, R. Vaquer-Sunyer, and C.M. Duarte. 2009. Ecosystem thresholds with hypoxia. Hydrobiologia 629 (1): 21–29.

    Article  CAS  Google Scholar 

  • Crain, C.M., K. Kroeker, and B.S. Halpern. 2008. Interactive and cumulative effects of multiple human stressors in marine systems. Ecology Letters 11 (12): 1304–1315.

    Article  Google Scholar 

  • D’ Avanzo, C., and J.N. Kremer. 1994. Diel oxygen dynamics and anoxic events in an eutrophic estuary of Waquoit Bay. Estuaries 18: 131–139.

    Article  Google Scholar 

  • D’ Avanzo, C., J.N. Kremer, and S.C. Wainright. 1996. Ecosystem production and respiration in response to eutrophication in shallow temperate estuaries. Marine Ecology Progress Series 141: 263–274.

  • Diaz, R.J. 2001. Overview of hypoxia around the world. Journal of Environmental Quality 30 (2): 275–281.

    Article  CAS  Google Scholar 

  • Diaz, R.J., and R. Rosenberg. 1995. Marine benthic hypoxia: A review of its ecological effects and the behavioural response of benthic macrofauna. Oceanography and Marine Biology: An Annual Review 33: 245–303.

    Google Scholar 

  • Diaz, R.J., and R. Rosenberg. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321 (5891): 926–929.

    Article  CAS  Google Scholar 

  • Fletcher, R.L. 1996. The occurrence of “green tides”—A review. In Marine benthic vegetation, ed. W. Schramm and P.H. Nienhuis, 7–43. Berlin: Springer–Verlag.

    Chapter  Google Scholar 

  • Fujikawa, Y., T. Mukai, T. Tokiwa, and S. Okita. 2000. Ecological research on fishery organisms (Ruditapes philippinarum and Anadara kagoshimensis). Bulletin of Shimane Prefectural Fishery Experimental Station 2000: 19–27 (in Japanese).

    Google Scholar 

  • Gubelit, Y.I. 2015. Climatic impact on community of filamentous macroalgae in the Neva estuary. Marine Pollution Bulletin 91 (1): 166–172.

    Article  CAS  Google Scholar 

  • Gubelit, Y.I., and N.A. Berezina. 2010. The causes and consequences of algal blooms: The Cladophora glomerata bloom and the Neva estuary (eastern Baltic Sea). Marine Pollution Bulletin 61 (4-6): 183–188.

    Article  CAS  Google Scholar 

  • Halpern, B.S., S. Walbridge, K.A. Selkoe, C.V. Kappel, F. Micheli, C. D'Agrosa, J.F. Bruno, K.S. Casey, C. Ebert, H.E. Fox, R. Fujita, D. Heinemann, H.S. Lenihan, E.M. Madin, M.T. Perry, E.R. Selig, M. Spalding, R. Steneck, and R. Watson. 2008. A global map of human impact on marine ecosystems. Science 319 (5865): 948–952.

    Article  CAS  Google Scholar 

  • Harris, L.A., C.M. Duarte, and S.W. Nixon. 2006. Allometric laws and prediction in estuarine and coastal ecology. Estuaries and Coasts 29 (2): 340–344.

    Article  Google Scholar 

  • Hauxwell, J., and I. Valiela. 2004. Effects of nutrient loading on shallow seagrass-dominated coastal systems: Patterns and processes. In Estuarine nutrient cycling: The influence of primary producers, ed. S.L. Nielsen, G.T. Banta, and M.F. Pedersen, 59–92. Dordrecht: Kluwer Academic Publishers.

    Chapter  Google Scholar 

  • Hauxwell, J., J. Cebrian, C. Furlong, and I. Valiela. 2001. Macroalgal canopies contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystem. Ecology 82 (4): 1007–1022.

    Article  Google Scholar 

  • Höffle, H., T. Wernberg, M.S. Thomsen, and M. Holmer. 2012. Drift algae, an invasive snail and elevated temperature reduce ecological performance of a warm-temperate seagrass, through additive effects. Marine Ecology Progress Series 450: 67–80.

    Article  Google Scholar 

  • Holmer, M., P. Wirachwong, and M.S. Thomsen. 2011. Negative effects of stress-resistant drift algae and high temperature on a small ephemeral seagrass species. Marine Biology 158 (2): 297–309.

    Article  Google Scholar 

  • Hughes, B.B., J.C. Haskins, K. Wasson, and E. Watson. 2011. Identifying factors that influence expression of eutrophication in a central California estuary. Marine Ecology Progress Series 439: 31–43.

    Article  CAS  Google Scholar 

  • Japan Meteorological Agency. 2016. Climate change monitoring report 2015. Tokyo: Japan Meteorological Agency.

    Google Scholar 

  • Katsuki, K., Y. Miyamoto, K. Yamada, H. Takata, K. Yamaguchi, D. Nakayama, H. Coops, H. Kunii, R. Nomura, and B.K. Khim. 2008. Eutrophication-induced changes in Lake Nakaumi, southwest Japan. Journal of Paleolimnology 40 (4): 1115–1125.

    Article  Google Scholar 

  • Kemp, W.M., and W.R. Boyton. 1980. Influence of biological and physical processes on dissolved oxygen dynamics in an estuarine system: Implications for measurement of community metabolism. Estuarine and Coastal Marine Science 11 (4): 407–431.

    Article  Google Scholar 

  • Kemp, W.M., J.M. Testa, D.J. Conley, D. Gilbert, and J.D. Hagy. 2009. Temporal responses of coastal hypoxia to nutrient loading and physical controls. Biogeosciences 6 (12): 2985–3008.

    Article  CAS  Google Scholar 

  • Krause-Jensen, D., K. McGlathery, S. Rysgaard, and P.B. Christensen. 1996. Production within dense mats of the filamentous macroalga Chaetomorpha linum in relation to light and nutrient availability. Marine Ecology Progress Series 134: 207–216.

    Article  Google Scholar 

  • Kunii, H., and K. Minamoto. 2000. Temporal and spatial variation in the macrophyte distribution in coastal lagoon Lake Nakaumi and its neighboring waters. Journal of Sea Research 26: 223–231.

    Google Scholar 

  • Lauringson, V., and J. Kotta. 2006. Influence of the thin drift algal mats on the distribution of macrozoobenthos in Kõiguste Bay, NE Baltic Sea. Hydrobiologia 554 (1): 97–105.

    Article  Google Scholar 

  • Marsden, I.D., and M.J. Bressington. 2009. Effects of macroalgal mats and hypoxia on burrowing depth of the New Zealand cockle (Austrovenus stutchburyi). Estuarine, Coastal and Shelf Science 81 (3): 438–444.

    Article  Google Scholar 

  • Martinetto, P., P. Daleo, M. Escapa, J. Alberti, J.P. Isacch, E. Fanjul, F. Botto, M.L. Piriz, G. Ponce, G. Casas, and O. Iribarne. 2010. High abundance and diversity of consumers associated with eutrophic areas in a semi-desert macrotidal coastal ecosystem in Patagonia, Argentina. Estuarine, Coastal and Shelf Science 88 (3): 357–364.

    Article  CAS  Google Scholar 

  • Miyamoto, Y., and A. Hatsuda. 2007. Horizontal and vertical distribution of macroalgal assemblages in modern Lake Nakaumi, a coastal lagoon. LAGUNA 14: 9–16 (in Japanese with English abstract).

    Google Scholar 

  • Miyamoto, Y., K. Yamada, K. Hatakeyama, and M. Hamaguchi. 2017. Temperature-dependent adverse effects of drifting macroalgae on the survival of Manila clams in a eutrophic coastal lagoon. Plankton and Benthos Research 12 (4): 238–247.

    Article  Google Scholar 

  • Moriwaki, S., and A. Michine. 2007. Catch fluctuations in Nakaumi, estuarine inland-sea, western Japan. Bulletin of Shimane Prefectural Fishery Experimental Station 2007: 41–48 (in Japanese with English abstract).

    Google Scholar 

  • Norkko, A., and E. Bonsdorff. 1996. Population responses of coastal zoobenthos to stress induced by drifting algal mats. Marine Ecology Progress Series 140: 141–151.

    Article  Google Scholar 

  • Reyes, E., and M. Merino. 1991. Diel dissolved oxygen dynamics and eutrophication in a shallow, well-mixed tropical lagoon (Cancun, Mexico). Estuaries 14 (4): 372–381.

    Article  CAS  Google Scholar 

  • Rozan, T.F., M. Taillefert, R.E. Trouwborst, B.T. Glazer, S. Ma, L.M. Herszage, J. Valdes, K.S. Price, and G.W. Luther III. 2002. Iron–sulfur–phosphorus cycling in the sediments of a shallow coastal bay: Implications for sediment nutrient release and benthic macroalgal blooms. Limnology and Oceanography 47 (5): 1346–1354.

    Article  CAS  Google Scholar 

  • Shen, J., T. Wang, J. Herman, P. Mason, and G.L. Arnold. 2008. Hypoxia in a coastal embayment of the Chesapeake Bay: A model diagnostic study of oxygen dynamics. Estuaries and Coasts 31 (4): 652–663.

    Article  CAS  Google Scholar 

  • Smetacek, W., and A. Zingone. 2013. Green and golden seaweed tides on the rise. Nature 504 (7478): 84–88.

    Article  CAS  Google Scholar 

  • Sorokin, Y.I., P.Y. Sorokin, and G. Ravagnan. 1996. On an extremely dense bloom of the dinoflagellate Alexandrium tamarense in lagoons of the Po river delta: Impact on the environment. Journal of Sea Research 35: 251–255.

    Google Scholar 

  • Thamdrup, B., J.W. Hansen, and B.B. Jsrgensen. 1998. Temperature dependence of oxygen respiration in a temperate coastal sediment. FEMS Microbiology Ecology 25 (2): 189–200.

    Article  CAS  Google Scholar 

  • Tyler, R.M., and T.E. Targett. 2007. Juvenile weakfish Cynoscion regalis distribution in relation to diel-cycling dissolved oxygen in an estuarine tributary. Marine Ecology Progress Series 333: 257–269.

    Article  CAS  Google Scholar 

  • Tyler, R.M., D.C. Brady, and T.E. Targett. 2009. Temporal and spatial dynamics of diel-cycling hypoxia in estuarine tributaries. Estuaries and Coasts 32 (1): 123–145.

    Article  CAS  Google Scholar 

  • Valiela, I., J. McClelland, J. Hauxwell, P.J. Behr, D. Hersh, and K. Foreman. 1997. Macroalgal blooms in shallow estuaries: Controls and ecophysiological and ecosystem consequence. Limnology and Oceanography 42 (5part2): 1105–1118.

    Article  Google Scholar 

  • Vaquer-Sunyer, R., and C.M. Duarte. 2008. Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences 105: 15452–15457.

    Article  Google Scholar 

  • Vaquer-Sunyer, R., C.M. Duarte, G. Jordà, and S. Ruiz-Halpern. 2012. Temperature dependence of oxygen dynamics and community metabolism in a shallow Mediterranean macroalgal meadow (Caulerpa prolifera). Estuaries and Coasts 35 (5): 1182–1192.

    Article  CAS  Google Scholar 

  • Wetzel, R.G. 1975. Limnology. Philadelphia, London, and Toronto: W.B. Saunders Co..

    Google Scholar 

  • Yamada, K., Y. Miyamoto, C. Fujii, K. Yamaguchi, and M. Hamaguchi. 2014. Vertical zonation and aggregated distribution of the Manila clam on subtidal sand flats in a coastal brackish lagoon along the Sea of Japan. Marine Ecology 35 (3): 308–318.

    Article  Google Scholar 

  • Yamamuro, M., J. Hiratsuka, Y. Ishitobi, S. Hosokawa, and Y. Nakamura. 2006. Ecosystem shift resulting from loss of eelgrass and other submerged aquatic vegetation in two estuarine lagoons, Lake Nakaumi and Lake Shinji, Japan. Journal of Oceanography 62 (4): 551–558.

    Article  Google Scholar 

  • Ye, N.H., X.W. Zhang, Y.Z. Mao, C.W. Liang, D. Xu, J. Zou, Z.M. Zhuang, and Q.Y. Wang. 2011. Green tides’ are overwhelming the coastline of our blue planet: Taking the world’s largest example. Ecological Research 26 (3): 477–485.

    Article  Google Scholar 

Download references

Acknowledgements

We thank members of the Tottori Environmental Sanitation Research Center for assistance with field work. We also thank the Research Center for Coastal Lagoon Environments of Shimane University for the use of their facilities. Two anonymous reviewers provided valuable comments on preliminary drafts of the manuscript. This research was supported in part by the Center Project in NIES to KY (No. 1112AF001). We dedicate this paper to the memory of Seiji Miyawaki, 1947–2013.

Author information

Authors and Affiliations

  1. Fukui Prefectural Satoyama-Satoumi Research Institute, 122-12-1 Torihama, Wakasa, Mikatakaminaka, Fukui, 919-1331, Japan

    Yasushi Miyamoto

  2. Seikai National Fisheries Research Institute, Fisheries Research Agency, 1551-8 Taira-machi, Nagasaki-shi, Nagasaki, 851-2213, Japan

    Tadashi Nakano

  3. Marine Science Laboratory, Centrer for Water Cycle, Marine Environment and Disaster Management, Kumamoto University, Kurokami 2-39-1, Chuo-ku, Kumamoto, 860-8555, Japan

    Katsumasa Yamada

  4. Environmental Sanitation Research Center, Tottori Prefecture, 526-1 Minamidani, Yurihama, Tottori, 682-0704, Japan

    Keisuke Hatakeyama

  5. National Research Institute of Fisheries and Environment of Inland Sea, Fisheries Research Agency, 2-17-5 Maruishi, Hatsukaichi, Hiroshima, 739-0452, Japan

    Masami Hamaguchi

Authors
  1. Yasushi Miyamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tadashi Nakano
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katsumasa Yamada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Keisuke Hatakeyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Masami Hamaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yasushi Miyamoto.

Additional information

Communicated by Masahiro Nakaoka

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miyamoto, Y., Nakano, T., Yamada, K. et al. Combined Effects of Drift Macroalgal Bloom and Warming on Occurrence and Intensity of Diel-Cycling Hypoxia in a Eutrophic Coastal Lagoon. Estuaries and Coasts 42, 494–503 (2019). https://doi.org/10.1007/s12237-018-0484-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-018-0484-6

Keywords

Search

Navigation