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Unwinding a Tangled Web: a Fine-Scale Approach towards Understanding the Drivers of Harmful Algal Bloom Species in a Eutrophic South African Estuary

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Abstract

A permanently eutrophic South African estuary provided an ideal model ecosystem from which to unravel the drivers of recurrent accumulations of harmful algal bloom (HAB) species. Designed to encapsulate broad- to fine-scale variations, seasonal in situ bihourly monitoring of abiotic and phytoplankton components took place at a fixed location over a 24-h period on four sampling occasions. Four known HAB species were recorded at bloom concentrations (> 20 μg Chl-a L−1) during the study, including Heterosigma akashiwo, Heterocapsa rotundata, Mesodinium rubrum, and Karenia cf. mikimotoi. Model results identified temperature as a key driver, with distinct community shifts between winter (~H. rotundata and M. rubrum) and spring/summer (~H. akashiwo and K. cf. mikimotoi) conditions. Evidence of niche overlap between all four HAB taxa was highlighted by their predilection for elevated nitrate levels, a vertically stratified water column and mesohaline (ca. 10) surface waters. As such, internal biotic processes such as plasticity of diel vertical migration patterns, reliance of M. rubrum on suitable ‘prey’ resources, and the suppressive pressure of H. akashiwo on co-occurring taxa-explained phytoplankton community dynamics beyond the influence of physico-chemical variability. These findings provide novel insight regarding the ecology of HAB taxa and how they have adapted to thrive in anthropogenically manipulated environments.

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References

  • Anderson, D.M. 2009. Approaches to monitoring, control and management of harmful algal blooms (HABs). Ocean & Coastal Management 52 (7): 342–347.

    Article  Google Scholar 

  • Barnosky, A.D., E.A. Hadly, J. Bascompte, E.L. Berlow, J.H. Brown, M. Fortelius, W.M. Getz, J. Harte, A. Hastings, P.A. Marquet, N.D. Martinez, A. Mooers, P. Roopnarine, G. Vermeij, J.W. Williams, R. Gillespie, J. Kitzes, C. Marshall, N. Matzke, D.P. Mindell, E. Revilla, and A.B. Smith. 2012. Approaching a state shift in Earth’s biosphere. Nature 486 (7401): 52–58.

    Article  CAS  Google Scholar 

  • Barton, K. 2013. MuMIn: multi-model inference. In: R package version 2.15.1.

  • Bate, G.C., and B.V. Heelas. 1975. Studies on the nitrate nutrition of two indigenous Rhodesian grasses. Journal of Applied Ecology 12 (3): 941–952.

    Article  CAS  Google Scholar 

  • Brand, L.E., L. Campbell, and E. Bresnan. 2012. Karenia: the biology and ecology of a toxic genus. Harmful Algae 14: 156–178.

    Article  Google Scholar 

  • Cloern, J.E., and A.D. Jassby. 2010. Patterns and scales of phytoplankton variability in estuarine-coastal ecosystems. Estuaries and Coasts 33 (2): 230–241.

    Article  CAS  Google Scholar 

  • Coulon, C., and V. Alexander. 1972. A sliding-chamber phytoplankton settling technique for making permanent quantitative slides with applications in fluorescent microscopy and autoradiography. Limnology and Oceanography 17 (1): 149–152.

    Article  Google Scholar 

  • Crawford, D.W., D.A. Purdie, A.P.M. Lockwood, and P. Weissman. 1997. Recurrent red-tides in the Southampton Water Estuary caused by the phototrophic ciliate Mesodinium rubrum. Estuarine, Coastal and Shelf Science 45 (6): 799–812.

    Article  CAS  Google Scholar 

  • Dugdale, R.C., F.P. Wilkerson, V.E. Hogue, and A. Marchi. 2007. The role of ammonium and nitrate in spring bloom development in San Francisco Bay. Estuarine, Coastal and Shelf Science 73 (1-2): 17–29.

    Article  Google Scholar 

  • Fenchel, T., and P.J. Hansen. 2006. Motile behaviour of the bloom-forming ciliate Mesodinium rubrum. Marine Biology Research 2 (1): 33–40.

    Article  Google Scholar 

  • Glibert, P.M., J.I. Allen, A.F. Bouwman, C.W. Brown, K.J. Flynn, A.J. Lewitus, and C.J. Madden. 2010. Modeling of HABs and eutrophication: status, advances, challenges. Journal of Marine Systems 83 (3-4): 262–275.

    Article  Google Scholar 

  • Gobler, C.J., O.M. Doherty, T.K. Hattenrath-Lehmann, A.W. Griffith, Y. Kang, and R.W. Litaker. 2017. Ocean warming since 1982 has expanded the niche of toxic algal blooms in the North Atlantic and North Pacific oceans. PNAS 114 (19): 4975–4980.

    Article  CAS  Google Scholar 

  • Gustafson, D.E., D.K. Stoecker, M.D. Johnson, W.F. van Heukelem, and K. Sneider. 2000. Cryptophyte algae are robbed of their organelles by the marine ciliate Mesodinium rubrum. Nature 405 (6790): 1049–1052.

    Article  CAS  Google Scholar 

  • Hall, N.S., A.C. Whipple, and H.W. Paerl. 2015. Vertical spatio-temporal patterns of phytoplankton due to migration behaviors in two shallow, microtidal estuaries: influence on phytoplankton function and structure. Estuarine, Coastal and Shelf Science 162: 7–21.

    Article  Google Scholar 

  • Handy, S.M., K.J. Coyne, K.J. Portune, E. Demir, M.A. Doblin, C.E. Hare, S.C. Cary, and D.A. Hutchins. 2005. Evaluating vertical migration behavior of harmful raphidophytes in the Delaware Inland Bays utilizing quantitative real-time PCR. Aquatic Microbial Ecology 40: 121–132.

    Article  Google Scholar 

  • Hansen, P.J., L.T. Nielsen, M. Johnson, T. Berge, and K.J. Flynn. 2013. Acquired phototrophy in Mesodinium and Dinophysis—a review of cellular organization, prey selectivity, nutrient uptake and bioenergetics. Harmful Algae 28: 126–139.

    Article  CAS  Google Scholar 

  • Hilmer, T., and G.C. Bate. 1991. Vertical migration of a flagellate-dominated bloom in a shallow South African estuary. Botanica Marina 34: 113–121.

    Article  Google Scholar 

  • Johnson, M.D., D.K. Stoecker, and H.G. Marshall. 2013. Seasonal dynamics of Mesodinium rubrum in Chesapeake Bay. Journal of Plankton Research 35 (4): 877–893.

    Article  Google Scholar 

  • Lemley, D.A., J.B. Adams, and S. Taljaard. 2017. Comparative assessment of two agriculturally-influenced estuaries: similar pressure, different response. Marine Pollution Bulletin 117: 135–146.

    Article  CAS  Google Scholar 

  • Levin, S.A. 1992. The problem of pattern and scale in ecology. Ecology 73 (6): 1943–1967.

    Article  Google Scholar 

  • Millette, N.C., J.J. Pierson, A. Aceves, and D.K. Stoecker. 2017. Mixotrophy in Heterocapsa rotundata: a mechanism for dominating the winter phytoplankton. Limnology and Oceanography 62 (2): 836–845.

    Article  CAS  Google Scholar 

  • Murphy, R.R., W.M. Kemp, and W.P. Ball. 2011. Long-term trends in Chesapeake Bay seasonal hypoxia, stratification, and nutrient loading. Estuaries and Coasts 34 (6): 1293–1309.

    Article  CAS  Google Scholar 

  • Nusch, E.A. 1980. Comparison of different methods for chlorophyll and phaeopigment determination. Archiv für Hydrobiologie 14: 14–36.

    CAS  Google Scholar 

  • O’Boyle, S., G. McDermott, J. Silke, and C. Cusack. 2016. Potential impact of an exceptional bloom of Karenia mikimotoi on dissolved oxygen levels in waters off western Ireland. Harmful Algae 53: 77–85.

    Article  Google Scholar 

  • Paerl, H.W., and J.T. Scott. 2010. Throwing fuel on the fire: synergistic effects of excessive nitrogen inputs and global warming on harmful algal blooms. Environmental Science & Technology 44 (20): 7756–7758.

    Article  CAS  Google Scholar 

  • Parsons, T.R., Y. Maita, and C.M. Lalli. 1984. A manual of chemical and biological methods for seawater analysis. New York: Pergamon Press 173 pp.

    Google Scholar 

  • Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar, and R Core Team. 2016. nlme: Linear and nonlinear mixed effects models. In: R package version 3.1–128.

  • Poloczanska, E.S., C.J. Brown, W.J. Sydeman, W. Kiessling, D.S. Schoeman, P.J. Moore, K. Brander, J.F. Bruno, L.B. Buckley, M.T. Burrows, C.M. Duarte, B.S. Halpern, J. Holding, C.V. Kappel, M.I. O'Connor, J.M. Pandolfi, C. Parmesan, F. Schwing, S.A. Thompson, and A.J. Richardson. 2013. Global imprint of climate change on marine life. Nature Climate Change 3 (10): 919–925.

    Article  Google Scholar 

  • Qin, Q., and J. Shen. 2017. The contribution of local and transport processes to phytoplankton biomass variability over different timescales in the Upper James River, Virginia. Estuarine, Coastal and Shelf Science 196: 123–133.

    Article  CAS  Google Scholar 

  • R Core Team. 2017. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Sellner, K.G., G.J. Doucette, and G.J. Kirkpatrick. 2003. Harmful algal blooms: causes, impacts and detection. Journal of Industrial Microbiology and Biotechnology 30 (7): 383–406.

    Article  CAS  Google Scholar 

  • Snow, G.C., G.C. Bate, and J.B. Adams. 2000. The effects of a single freshwater release into the Kromme Estuary. 2: microalgal response. Water SA 26 (3): 301–310.

    CAS  Google Scholar 

  • Wang, Y., U. Naumann, S.T. Wright, and D.I. Warton. 2012. Mvabund—an R package for model-based analysis of multivariate abundance data. Methods in Ecology and Evolution 3 (3): 471–474.

    Article  Google Scholar 

  • Warton, D.I., S.T. Wright, and Y. Wang. 2012. Distance-based multivariate analyses confound location and dispersion effects. Methods in Ecology and Evolution 3 (1): 89–101.

    Article  Google Scholar 

  • Warton, D.I., S.D. Foster, G. De’ath, J. Stoklosa, and P.K. Dunstan. 2015. Model-based thinking for community ecology. Plant Ecology 216 (5): 669–682.

    Article  Google Scholar 

  • Wilkerson, F.P., and G. Grunseich. 1990. Formation of blooms by the symbiotic ciliate Mesodinium rubrum: the significance of nitrogen uptake. Journal of Plankton Research 12 (5): 973–989.

    Article  Google Scholar 

  • Wilkerson, F.P., R.C. Dugdale, A.E. Parker, S.B. Blaser, and A. Pimenta. 2015. Nutrient uptake and primary productivity in an urban estuary: sing rate measurements to evaluate phytoplankton response to different hydrological and nutrient conditions. Aquatic Ecology 49 (2): 211–233.

    Article  CAS  Google Scholar 

  • Yamochi, S., and T. Abe. 1984. Mechanisms to initiate a Heterosigma akashiwo red tide in Osaka Bay. II. Diel vertical migration. Marine Biology 83 (3): 255–261.

    Article  Google Scholar 

  • Zhang, Y., F. Fu, E. Whereat, K.J. Coyne, and D.A. Hutchins. 2006. Bottom-up controls on a mixed-species HAB assemblage: a comparison of sympatric Chattonella subsalsa and Heterosigma akashiwo (Raphidophyceae) isolates from the Delaware Inland Bays, USA. Harmful Algae 5 (3): 310–320.

    Article  CAS  Google Scholar 

  • Zuur, A.F., E.N. Ieno, N.J. Walker, A.A. Saveliev, and G.M. Smith. 2009. Mixed effects models and extensions in ecology with R. New York: Springer.

    Book  Google Scholar 

  • Zuur, A.F., E.N. Ieno, and C.S. Elphick. 2010. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1 (1): 3–14.

    Article  Google Scholar 

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Acknowledgments

The authors would like to thank Mrs. Patricia Smailes for her assistance with the microalgal counts and identification. A special thank you to the reviewers for their invaluable input on the manuscript.

Funding

The lead author, Dr. Daniel A. Lemley received funding from the Joint In-Country German Academic Exchange Service (DAAD) and the National Research Foundation (NRF) scholarship (Unique Grant ID: 94261), as well as the Ernst and Ethel Eriksen Trust. The Claude Leon Foundation is also thanked for providing a postdoctoral fellowship to co-author, Dr. Gavin M. Rishworth.

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Authors and Affiliations

  1. Botany Department and the Institute for Coastal and Marine Research, Nelson Mandela University, Port Elizabeth, 6031, South Africa

    Daniel A. Lemley & Janine B. Adams

  2. DST/NRF Research Chair in Shallow Water Ecosystems, Nelson Mandela University, Port Elizabeth, 6031, South Africa

    Gavin M. Rishworth

Authors
  1. Daniel A. Lemley
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  2. Janine B. Adams
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  3. Gavin M. Rishworth
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Correspondence to Daniel A. Lemley.

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Communicated by James L. Pinckney

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Lemley, D.A., Adams, J.B. & Rishworth, G.M. Unwinding a Tangled Web: a Fine-Scale Approach towards Understanding the Drivers of Harmful Algal Bloom Species in a Eutrophic South African Estuary. Estuaries and Coasts 41, 1356–1369 (2018). https://doi.org/10.1007/s12237-018-0380-0

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  • DOI: https://doi.org/10.1007/s12237-018-0380-0

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