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Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Resource fluctuation patterns influence emergent properties of phytoplankton assemblages and their resistance to harmful algal blooms

Daniel L. Roelke A B D , Sierra E. Cagle A , Rika M.W. Muhl A , Athanasia Sakavara C and George Tsirtsis C
+ Author Affiliations
- Author Affiliations

A Department of Wildlife and Fisheries Sciences, Texas A&M University, 2258 TAMUS, College Station, TX 77843-2258, USA.

B Department of Oceanography, Texas A&M University, College Station, TX 77843, USA.

C Department of Marine Sciences, University of the Aegean, GR-81100 Mytilene, Greece.

D Corresponding author. Email: droelke@tamu.edu

Marine and Freshwater Research 71(1) 56-67 https://doi.org/10.1071/MF18386
Submitted: 3 October 2018  Accepted: 13 December 2018   Published: 1 February 2019

Abstract

Recent advances in phytoplankton modelling have used species-rich, self-organising assemblages. These models have shown that phytoplankton with complementary life-history traits related to resource exploitation assemble into stable states of lumpy coexistence when resources fluctuate where species’ niches occur in clusters along resource gradients. They have also shown that a high degree of competitive dissimilarity between clusters arises, and that this relates to the incidence of monospecific blooms of allelochemical-producing taxa, i.e. some harmful algal bloom (HAB) species. These findings further suggest that the mode (sudden v. gradual changes) under which limiting resources fluctuate plays an important role in determining the emergent properties of the assemblage. For example, productivity, biodiversity and the number of species clusters (and, therefore, resistance to HABs) are all enhanced when switches in resource supplies are gradual, compared with when they are sudden. These theoretical findings, as well as others discussed herein, are of particular interest in watersheds where human activities, such as dam construction, have the capacity to dramatically alter natural-resource fluctuation patterns.

Additional keywords: competition, HABs, inflows, inorganic nutrients, lumpy coexistence.


References

Abe, T., and Kamo, K. (2003). Seasonal changes in floral frequency and composition of flower in two cool temperate secondary forests in Japan. Forest Ecology and Management 175, 153–162.
Seasonal changes in floral frequency and composition of flower in two cool temperate secondary forests in Japan.Crossref | GoogleScholarGoogle Scholar |

Al-Mufti, M. M., Sydes, C. L., Furnas, S. B., Grime, J. P., and Band, S. R. (1977). A quantitative analysis of shoot phenology and dominance in herbaceous vegetation. Journal of Ecology 65, 759–791.
A quantitative analysis of shoot phenology and dominance in herbaceous vegetation.Crossref | GoogleScholarGoogle Scholar |

Anabalón, V., Arístegui, J., Morales, C. E., Andrade, I., Benavides, M., Correa-Ramírez, M. A., Espino, M., Ettahiri, O., Hormazabal, S., Makaoui, A., Montero, M. F., and Orbi, A. (2014). The structure of planktonic communities under variable coastal upwelling conditions off Cape Ghir (31°N) in the canary current system (NW Africa). Progress in Oceanography 120, 320–339.
The structure of planktonic communities under variable coastal upwelling conditions off Cape Ghir (31°N) in the canary current system (NW Africa).Crossref | GoogleScholarGoogle Scholar |

Anderson, D. M., Glibert, P. M., and Burkholder, J. M. (2002). Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25, 704–726.
Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences.Crossref | GoogleScholarGoogle Scholar |

Bratbak, G., Egge, J. K., and Heldal, M. (1993). Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Marine Ecology Progress Series 93, 39–48.
Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms.Crossref | GoogleScholarGoogle Scholar |

Brook, A. J., and Woodward, W. B. (1956). Some observations on the effects of water inflow and outflow on the plankton of small lakes. Journal of Animal Ecology 25, 22–35.
Some observations on the effects of water inflow and outflow on the plankton of small lakes.Crossref | GoogleScholarGoogle Scholar |

Cardinale, B. J., Wright, J. P., Cadotte, M. W., Carroll, I. T., Hector, A., Srivastava, D. S., Loreau, M., and Weis, J. J. (2007). Impacts of plant diversity on biomass production increase through time because of species complementarity. Proceedings of the National Academy of Sciences of the United States of America 104, 18123–18128.
Impacts of plant diversity on biomass production increase through time because of species complementarity.Crossref | GoogleScholarGoogle Scholar | 17991772PubMed |

Cebrian, J. (1999). Patterns in the fate of production in plant communities. American Naturalist 154, 449–468.
Patterns in the fate of production in plant communities.Crossref | GoogleScholarGoogle Scholar | 10523491PubMed |

Chen, X., Pan, D., Bai, Y., He, X., Chen, C.-T. A., and Hao, Z. (2013). Episodic phytoplankton bloom events in the Bay of Bengal triggered by multiple forcings. Deep-Sea Research 73, 17–30.
Episodic phytoplankton bloom events in the Bay of Bengal triggered by multiple forcings.Crossref | GoogleScholarGoogle Scholar |

Cyr, H., and Pace, M. L. (1993). Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361, 148–150.
Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems.Crossref | GoogleScholarGoogle Scholar |

Davidson, K., Gowen, R. J., Harrison, P. J., Fleming, L. E., Hoagland, P., and Moschonas, G. (2014). Anthropogenic nutrients and harmful algae in coastal waters. Journal of Environmental Management 146, 206–216.
Anthropogenic nutrients and harmful algae in coastal waters.Crossref | GoogleScholarGoogle Scholar | 25173729PubMed |

de Baar, H. J. W. (1994). Von Liebig’s law of the minimum and plankton ecology (1899–1991). Progress in Oceanography 33, 347–386.
Von Liebig’s law of the minimum and plankton ecology (1899–1991).Crossref | GoogleScholarGoogle Scholar |

Drost, M. B., Cuppen, H. P., Van Nieukerken, E. J., and Schreijer, M. (1992). ‘De Waterkevers van Nederland.’ (KNNV Uitgeverij: Utrecht, Netherlands.)

Elser, J. J., and Urabe, J. (1999). The stoichiometry of consumer-driven nutrient cycling: theory, observations, and consequences. Ecology 80, 735–751.
The stoichiometry of consumer-driven nutrient cycling: theory, observations, and consequences.Crossref | GoogleScholarGoogle Scholar |

Elser, J. J., Fagan, W. F., Denno, R. F., Dobberfuhl, D. R., Folarin, A., Huberty, A., Interlandi, S., Kilham, S. S., McCauleyk, E., Schulz, K. L., Siemann, E. H., and Sterner, R. W. (2000). Nutritional constraints in terrestrial and freshwater food webs. Nature 408, 578–580.
Nutritional constraints in terrestrial and freshwater food webs.Crossref | GoogleScholarGoogle Scholar | 11117743PubMed |

Fridley, J. D. (2001). The influence of species diversity on ecosystem productivity: how, where, and why? Oikos 93, 514–526.
The influence of species diversity on ecosystem productivity: how, where, and why?Crossref | GoogleScholarGoogle Scholar |

Fu, F. X., Tatters, A. O., and Hutchins, D. A. (2012). Global change and the future of harmful algal blooms in the ocean. Marine Ecology Progress Series 470, 207–233.
Global change and the future of harmful algal blooms in the ocean.Crossref | GoogleScholarGoogle Scholar |

Fuhrman, J. A. (1999). Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548.
Marine viruses and their biogeochemical and ecological effects.Crossref | GoogleScholarGoogle Scholar | 10376593PubMed |

Gaul, W., and Antia, A. N. (2001). Taxon-specific growth and selective microzooplankton grazing of phytoplankton in the northeast Atlantic. Journal of Marine Systems 30, 241–261.
Taxon-specific growth and selective microzooplankton grazing of phytoplankton in the northeast Atlantic.Crossref | GoogleScholarGoogle Scholar |

Glibert, P. M., and Burkholder, J. M. (2018). Causes of harmful algal blooms. In ‘Harmful Algal Blooms: a Compendium Desk Reference’. (Eds S. E. Shumway, J. M. Burkholder, and S. L. Morton.) pp. 1–38. (Wiley Blackwell: Hoboken, NJ, USA.)

Gobler, C. J., Burkholder, J. M., Davis, T. W., Harke, M. J., Johengen, T., Stow, C. A., and Van de Waal, D. B. (2016). The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae 54, 87–97.
The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms.Crossref | GoogleScholarGoogle Scholar | 28073483PubMed |

Grover, J. P. (1997). ‘Resource Competition.’ (Chapman & Hall: London, UK.)

Grover, J. P., Roelke, D. L., and Brooks, B. W. (2017). Population persistence in flowing-water habitats: conditions where flow-based management of harmful algal blooms works, and where it does not. Ecological Engineering 99, 172–181.
Population persistence in flowing-water habitats: conditions where flow-based management of harmful algal blooms works, and where it does not.Crossref | GoogleScholarGoogle Scholar |

Güsewell, S. (2004). N: P ratios in terrestrial plants: variation and functional significance. New Phytologist 164, 243–266.
N: P ratios in terrestrial plants: variation and functional significance.Crossref | GoogleScholarGoogle Scholar |

Hallegraeff, G. M. (1993). A review of harmful algal blooms and their apparent global increase Phycologia 32, 79–99.
A review of harmful algal blooms and their apparent global increaseCrossref | GoogleScholarGoogle Scholar |

Hardin, G. (1960). The competitive exclusion principle. Science 131, 1292–1297.
The competitive exclusion principle.Crossref | GoogleScholarGoogle Scholar | 14399717PubMed |

Harke, M. J., Berry, D. L., Ammerman, J. W., and Gobler, C. J. (2012). Molecular response of the bloom-forming cyanobacterium, Microcystis aeruginosa, to phosphorus limitation. Microbial Ecology 63, 188–198.
Molecular response of the bloom-forming cyanobacterium, Microcystis aeruginosa, to phosphorus limitation.Crossref | GoogleScholarGoogle Scholar | 21720829PubMed |

Havlicek, T. D., and Carpenter, S. R. (2001). Pelagic species size distributions in lakes, are they discontinuous? Limnology and Oceanography 46, 1021–1033.
Pelagic species size distributions in lakes, are they discontinuous?Crossref | GoogleScholarGoogle Scholar |

Holling, C. S. (1992). Cross-scale morphology, geometry & dynamics of ecosystems. Ecological Monographs 62, 447–502.
Cross-scale morphology, geometry & dynamics of ecosystems.Crossref | GoogleScholarGoogle Scholar |

Hooper, D. U., Chapin, F. S., Ewel, J. J., Hector, A., Inchausti, P., Lavorel, S., Lawton, J. H., Lodge, D. M., Loreau, M., Naeem, S., Schmid, B., Setälä, H., Symstad, A., Vandermeer, J. J., and Wardle, D. A. (2005). Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75, 3–35.
Effects of biodiversity on ecosystem functioning: a consensus of current knowledge.Crossref | GoogleScholarGoogle Scholar |

Hu, S., Chen, C., Ji, R., Townsend, D. W., Tian, R., Beardsley, R. C., and Davis, C. S. (2011). Effects of surface forcing on interannual variability of the fall phytoplankton bloom in the Gulf of Maine revealed using a process-oriented model. Marine Ecology Progress Series 427, 29–49.
Effects of surface forcing on interannual variability of the fall phytoplankton bloom in the Gulf of Maine revealed using a process-oriented model.Crossref | GoogleScholarGoogle Scholar |

Hubbell, S. P. (2001). ‘The Unified Neutral Theory of Biodiversity and Biography.’ (Princeton University Press: Princeton, NJ, USA.)

Hutchinson, G. E. (1961). The paradox of the plankton. American Naturalist 95, 137–145.
The paradox of the plankton.Crossref | GoogleScholarGoogle Scholar |

Katechakis, A., Stibor, H., Sommer, U., and Hansen, T. (2002). Changes in the phytoplankton community and microbial food web of Blanes Bay (Catalan Sea, NW Mediterranean) under prolonged grazing pressure by doliolids (Tunicata), cladocerans or copepods (Crustacea). Marine Ecology Progress Series 234, 55–69.
Changes in the phytoplankton community and microbial food web of Blanes Bay (Catalan Sea, NW Mediterranean) under prolonged grazing pressure by doliolids (Tunicata), cladocerans or copepods (Crustacea).Crossref | GoogleScholarGoogle Scholar |

Ketchum, B. H. (1951). The flushing of tidal estuaries. Sewage and Industrial Wastes 23, 198–209.

Ketchum, B. H. (1954). Relation between circulation and planktonic populations in estuaries. Ecology 35, 191–200.
Relation between circulation and planktonic populations in estuaries.Crossref | GoogleScholarGoogle Scholar |

Kilham, P., and Kilham, S. S. (1980). The evolutionary ecology of phytoplankton. In ‘The Physiological Ecology of Phytoplankton’. (Ed. I. Morris.) pp. 571–597. (Blackwell Scientific: Oxford, UK.)

Kolzau, S., Wiedner, C., Rucker, J., Kohler, J., Kohler, A., and Dolman, A. M. (2014). Seasonal patterns of nitrogen and phosphorus limitation in four German lakes and the predictability of limitation status from ambient nutrient concentrations. PLoS One 9, e96065.
Seasonal patterns of nitrogen and phosphorus limitation in four German lakes and the predictability of limitation status from ambient nutrient concentrations.Crossref | GoogleScholarGoogle Scholar | 24755935PubMed |

Lares, M. L., Marinone, S. G., Rivera-Duarte, I., Beck, A., and Sañudo-Wilhelmy, S. (2009). Spatial variability of trace metals and inorganic nutrients in surface waters of Todos Santos Bay, Mexico in the summer of 2005 during a red tide algal bloom. Archives of Environmental Contamination and Toxicology 56, 707–716.
Spatial variability of trace metals and inorganic nutrients in surface waters of Todos Santos Bay, Mexico in the summer of 2005 during a red tide algal bloom.Crossref | GoogleScholarGoogle Scholar | 18726538PubMed |

Litchman, E., Klausmeier, C. A., Schofield, O. M., and Falkowski, P. G. (2007). The role of phytoplankton functional traits in structuring phytoplankton communities, scaling from cellular to ecosystem level. Ecology Letters 10, 1170–1181.
The role of phytoplankton functional traits in structuring phytoplankton communities, scaling from cellular to ecosystem level.Crossref | GoogleScholarGoogle Scholar | 17927770PubMed |

Lundgren, V. M., Roelke, D. L., Grover, J. P., Brooks, B. W., Prosser, K. N., Scott, W. C., Laws, C. A., and Umphres, G. D. (2013). Interplay between ambient surface water mixing and manipulated hydraulic flushing: Implications for harmful algal bloom mitigation. Ecological Engineering 60, 289–298.
Interplay between ambient surface water mixing and manipulated hydraulic flushing: Implications for harmful algal bloom mitigation.Crossref | GoogleScholarGoogle Scholar |

MacArthur, R. H., and Levins, R. (1967). Limiting similarity, convergence and divergence of coexisting species. American Naturalist 101, 377–385.
Limiting similarity, convergence and divergence of coexisting species.Crossref | GoogleScholarGoogle Scholar |

Magilligan, F. J., and Nislow, K. H. (2005). Changes in hydrologic regime by dams. Geomorphology 71, 61–78.
Changes in hydrologic regime by dams.Crossref | GoogleScholarGoogle Scholar |

Marquard, E., Weigelt, A., Temperton, V. M., Roscher, C., Schumacher, J., Buchmann, N., Fischer, M., Weisser, W. W., and Schmid, B. (2009). Plant species richness and functional composition drive overyielding in a six-year grassland experiment. Ecology 90, 3290–3302.
Plant species richness and functional composition drive overyielding in a six-year grassland experiment.Crossref | GoogleScholarGoogle Scholar | 20120799PubMed |

Marquet, P. A. (2000). Invariants, scaling laws and ecological complexity. Science 289, 1487–1488.
Invariants, scaling laws and ecological complexity.Crossref | GoogleScholarGoogle Scholar | 10991735PubMed |

Maury, O., Shin, Y.-J., Faugeras, B., Ari, T. B., and Marsac, F. (2007). Modeling environmental effects on the size-structured energy flow through marine ecosystems. Part 2, simulations. Progress in Oceanography 74, 500–514.
Modeling environmental effects on the size-structured energy flow through marine ecosystems. Part 2, simulations.Crossref | GoogleScholarGoogle Scholar |

Mayali, X., Franks, P. J. S., and Azam, F. (2008). Cultivation and ecosystem role of a marine Roseobacter clade-affiliated cluster bacterium. Applied and Environmental Microbiology 74, 2595–2603.
Cultivation and ecosystem role of a marine Roseobacter clade-affiliated cluster bacterium.Crossref | GoogleScholarGoogle Scholar | 18326670PubMed |

Mellard, J. P., Yoshiyama, K., Klausmeier, C. A., and Litchman, E. (2012). Experimental test of phytoplankton competition for nutrients and light in poorly mixed water columns. Ecological Monographs 82, 239–256.
Experimental test of phytoplankton competition for nutrients and light in poorly mixed water columns.Crossref | GoogleScholarGoogle Scholar |

Monod, J. (1950). La technique de la culture continue: theorie et applications. Annales de l’Institut Pasteur 79, 390–410.

Morse, R. E., Mulholland, M. R., Egerton, T. A., and Marshall, H. G. (2014). Phytoplankton and nutrient dynamics in a tidally dominated eutrophic estuary: daily variability and controls on bloom formation. Marine Ecology Progress Series 503, 59–74.
Phytoplankton and nutrient dynamics in a tidally dominated eutrophic estuary: daily variability and controls on bloom formation.Crossref | GoogleScholarGoogle Scholar |

Muhl, R. M. W., Roelke, D. L., Zohary, T., Moustaka-Gouni, M., Sommer, U., Borics, G., Gaedke, U., Withrow, F. G., and Bhattacharyya, J. (2018). Resisting annihilation: relationships between functional trait dissimilarity, assemblage competitive power and allelopathy. Ecology Letters 21, 1390–1400.
Resisting annihilation: relationships between functional trait dissimilarity, assemblage competitive power and allelopathy.Crossref | GoogleScholarGoogle Scholar |

Murrell, M. C., Hagy, J. D., Lores, E. M., and Greene, R. M. (2007). Phytoplankton production and nutrient distributions in a subtropical estuary: importance of freshwater flow. Estuaries and Coasts 30, 390–402.
Phytoplankton production and nutrient distributions in a subtropical estuary: importance of freshwater flow.Crossref | GoogleScholarGoogle Scholar |

Nadia, T. L., Morellato, L. P. C., and Machado, I. C. (2012). Reproductive phenology of a northeast Brazilian mangrove community: environmental and biotic constraints. Flora 207, 682–692.
Reproductive phenology of a northeast Brazilian mangrove community: environmental and biotic constraints.Crossref | GoogleScholarGoogle Scholar |

Nordhaus, I., Roelke, D. L., Vaquer-Sunyer, R., and Winter, C. (2018). Coastal systems in transition from a ‘natural’ to an ‘anthropogenically modified’ state. Estuarine, Coastal and Shelf Science 211, 1–5.
Coastal systems in transition from a ‘natural’ to an ‘anthropogenically modified’ state.Crossref | GoogleScholarGoogle Scholar |

Poff, N. L., Olden, J. D., Merritt, D. M., and Pepin, D. M. (2007). Homogenization of regional river dynamics by dams and global biodiversity implications. Proceedings of the National Academy of Sciences of the United States of America 104, 5732–5737.
Homogenization of regional river dynamics by dams and global biodiversity implications.Crossref | GoogleScholarGoogle Scholar | 17360379PubMed |

Ptacnik, R., Solimini, A. G., Andersen, T., Tamminen, T., Brettum, P., Lepisto, L., Willen, E., and Rekolainen, S. (2008). Diversity predicts stability and resource use efficiency in natural phytoplankton communities. Proceedings of the National Academy of Sciences of the United States of America 105, 5134–5138.
Diversity predicts stability and resource use efficiency in natural phytoplankton communities.Crossref | GoogleScholarGoogle Scholar | 18375765PubMed |

Ptacnik, R., Moorthi, S. D., and Hillebrand, H. (2010). Hutchinson reversed, or why there need to be so many species. Advances in Ecological Research 43, 1–43.
Hutchinson reversed, or why there need to be so many species.Crossref | GoogleScholarGoogle Scholar |

Roelke, D. L. (2018). Grazers, pathogens and shelf-shading enhance phytoplankton species richness more and reduce productivity less when environments are less dynamic: a theoretical study. Estuarine, Coastal and Shelf Science 211, 152–165.
Grazers, pathogens and shelf-shading enhance phytoplankton species richness more and reduce productivity less when environments are less dynamic: a theoretical study.Crossref | GoogleScholarGoogle Scholar |

Roelke, D. L., and Eldridge, P. (2008). Mixing of supersaturated assemblages and the precipitous loss of species. American Naturalist 171, 162–175.
Mixing of supersaturated assemblages and the precipitous loss of species.Crossref | GoogleScholarGoogle Scholar | 18197769PubMed |

Roelke, D. L., and Spatharis, S. (2015a). Phytoplankton succession in recurrently fluctuating environments. PLoS One 10, e0121392.
Phytoplankton succession in recurrently fluctuating environments.Crossref | GoogleScholarGoogle Scholar | 26133991PubMed |

Roelke, D. L., and Spatharis, S. (2015b). Phytoplankton assemblage characteristics in recurrently fluctuating environments. PLoS One 10, e0120673.
Phytoplankton assemblage characteristics in recurrently fluctuating environments.Crossref | GoogleScholarGoogle Scholar | 26133991PubMed |

Roelke, D. L., Li, H.-P., Hayden, N. J., Miller, C. J., Davis, S. E., Quigg, A., and Buyukates, Y. (2013). Co-occurring and opposing freshwater inflow effects on phytoplankton biomass, productivity and community composition of Galveston Bay, USA. Marine Ecology Progress Series 477, 61–76.
Co-occurring and opposing freshwater inflow effects on phytoplankton biomass, productivity and community composition of Galveston Bay, USA.Crossref | GoogleScholarGoogle Scholar |

Roy, E. D., White, J. R., Smith, E. A., Bargu, S., and Li, C. (2013). Estuarine ecosystem response to three large-scale Mississippi River flood diversion events. The Science of the Total Environment 458–460, 374–387.
Estuarine ecosystem response to three large-scale Mississippi River flood diversion events.Crossref | GoogleScholarGoogle Scholar | 23685135PubMed |

Sakavara, A., Tsirtsis, G., Roelke, D. L., Mancy, R., and Spatharis, S. (2018). Lumpy species coexistence arises robustly in fluctuating resource environments. Proceedings of the National Academy of Sciences of the United States of America 115, 738–743.
Lumpy species coexistence arises robustly in fluctuating resource environments.Crossref | GoogleScholarGoogle Scholar | 29263095PubMed |

Scheffer, M., and van Nes, E. H. (2006). Self-organized similarity, the evolutionary emergence of groups of similar species. Proceedings of the National Academy of Sciences of the United States of America 103, 6230–6235.
Self-organized similarity, the evolutionary emergence of groups of similar species.Crossref | GoogleScholarGoogle Scholar | 16585519PubMed |

Scheffer, M., van Nes, E. H., and Vergnon, R. (2018). Toward a unifying theory of biodiversity. Proceedings of the National Academy of Sciences of the United States of America 115, 639–641.
Toward a unifying theory of biodiversity.Crossref | GoogleScholarGoogle Scholar | 29326234PubMed |

Schmeller, D. S., Loyau, A., Bao, K. S., Brack, W., Chatzinotas, A., De Vleeschouwer, F., Friesen, J., Gandois, L., Hansson, S. V., Haver, M., Le Roux, G., Shen, J., Teisserenc, R., and Vredenburg, V. T. (2018). People, pollution and pathogens: global change impacts in mountain freshwater ecosystems. The Science of the Total Environment 622–623, 756–763.
People, pollution and pathogens: global change impacts in mountain freshwater ecosystems.Crossref | GoogleScholarGoogle Scholar | 29223902PubMed |

Segura, A. M., Calliari, D., Kruk, C., Conde, D., Bonilla, S., and Fort, H. (2011). Emergent neutrality drives phytoplankton species coexistence. Proceedings. Biological Sciences 278, 2355–2361.
Emergent neutrality drives phytoplankton species coexistence.Crossref | GoogleScholarGoogle Scholar | 21177680PubMed |

Segura, A. M., Kruk, C., Calliari, D., García-Rodriguez, F., Conde, D., Widdicombe, C. E., and Fort, H. (2013). Competition drives clumpy species coexistence in estuarine phytoplankton. Scientific Reports 3, 1037.
Competition drives clumpy species coexistence in estuarine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 23301158PubMed |

Shadrin, N. V., Anufriieva, E. V., Kipriyanova, L. M., Kolesnikova, E. A., Latushkin, A. A., Romanov, R. E., and Sergeeva, N. G. (2018). The political decision caused the drastic ecosystem shift of the Sivash Bay (the Sea of Azov). Quaternary International 475, 4–10.
The political decision caused the drastic ecosystem shift of the Sivash Bay (the Sea of Azov).Crossref | GoogleScholarGoogle Scholar |

Sheriff, D. W., Margolis, H. A., Kaufmann, M. R., and Reich, P. B. (1995). Resource use efficiency. In ‘Resource Physiology of Conifers’. (Eds W. K. Smith and T. M. Hinckley.) pp. 143–178. (Academic Press: New York, NY, USA.)

Smayda, T. J. (1980). Phytoplankton species succession. In ‘The Physiological Ecology of Phytoplankton’. (Ed. I. Morris.) pp. 493–570. (Blackwell Scientific: Oxford, UK.)

Smayda, T. J. (1990). Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic. In ‘Toxic Marine Phytoplankton’. (Eds E. Granéli, B. Sundström, L. Edler, and D. M. Anderson.) pp. 29–40. (Elsevier: New York, NY, USA.)

Smeti, E., Roelke, D. L., Tsirtsis, G., and Spatharis, S. (2018). Species extinctions strengthen the relationship between biodiversity and resource use efficiency. Ecological Modelling 384, 75–86.
Species extinctions strengthen the relationship between biodiversity and resource use efficiency.Crossref | GoogleScholarGoogle Scholar |

Smith, V. H. (1983). Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science 221, 669–671.
Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton.Crossref | GoogleScholarGoogle Scholar | 17787737PubMed |

Smith, V. H. (2002). Effects of resource supply ratios on the structure and function of microbial communities. Antonie van Leeuwenhoek 81, 99–106.
Effects of resource supply ratios on the structure and function of microbial communities.Crossref | GoogleScholarGoogle Scholar | 12448709PubMed |

Sommer, U. (1989). The role of competition for resources in phytoplankton ecology. In ‘Plankton Ecology: Succession in Plankton Communities’. (Ed. U. Sommer.) pp. 57–106. (Springer-Verlag: Berlin, Germany.)

Sommer, U., Gliwicz, Z. M., Lampert, W., and Duncan, A. (1986). The PEG-model of seasonal succession of plankton events in fresh waters. Archiv für Hydrobiologie 106, 436–440.

Sommer, U., Charalampous, E., Genitsaris, S., and Moustaka-Gouni, M. (2017). Benefits, costs and taxonomic distribution of marine phytoplankton body size. Journal of Plankton Research 39, 494–508.

Sterner, R. W., and Elser, J. J. (2002). ‘Ecological Stoichiometry.’ (Princeton University Press: Princeton, NJ, USA.)

Sterner, R. W., and Hessen, D. O. (1994). Algal nutrient limitation and the nutrition of aquatic herbivores. Annual Review of Ecology and Systematics 25, 1–29.
Algal nutrient limitation and the nutrition of aquatic herbivores.Crossref | GoogleScholarGoogle Scholar |

Striebel, M., Behl, S., Diehl, S., and Stibor, H. (2009). Spectral niche complementarity and carbon dynamics in pelagic ecosystems. American Naturalist 174, 141–147.
Spectral niche complementarity and carbon dynamics in pelagic ecosystems.Crossref | GoogleScholarGoogle Scholar | 19456261PubMed |

Strong, D. R. (1992). Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73, 747–754.
Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems.Crossref | GoogleScholarGoogle Scholar |

Sweeney, J. A. (2014). Command-and-control: alternative futures of geoengineering in an age of global weirding. Futures 57, 1–13.
Command-and-control: alternative futures of geoengineering in an age of global weirding.Crossref | GoogleScholarGoogle Scholar |

Tamvakis, A., Miritzis, J., Tsirtsis, G., Spyropoulou, A., and Spatharis, S. (2012). Effects of meteorological forcing on coastal eutrophication: modeling with model trees. Estuarine, Coastal and Shelf Science 115, 210–217.
Effects of meteorological forcing on coastal eutrophication: modeling with model trees.Crossref | GoogleScholarGoogle Scholar |

Thingstad, T. F. (2000). Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnology and Oceanography 45, 1320–1328.
Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems.Crossref | GoogleScholarGoogle Scholar |

Tilman, D. (1977). Resource competition between plankton algae: an experimental and theoretical approach. Ecology 58, 338–348.
Resource competition between plankton algae: an experimental and theoretical approach.Crossref | GoogleScholarGoogle Scholar |

Tilman, D. (1982). ‘Resource Competition and Community Structure.’ (Princeton University Press: Princeton, NJ, USA.)

Tilman, D., Reich, P. B., Knops, J., Wedin, D., Mielke, T., and Lehman, C. (2001). Diversity and productivity in a long-term grassland experiment. Science 294, 843–845.
Diversity and productivity in a long-term grassland experiment.Crossref | GoogleScholarGoogle Scholar | 11679667PubMed |

Townsend, D. W., Cammen, L. M., Holligan, P. M., Campbell, D. E., and Pettigrew, N. R. (1994). Causes and consequences of variability in the timing of spring phytoplankton blooms. 1994. Deep-sea Research – I. Oceanographic Research Papers 41, 747–765.
Causes and consequences of variability in the timing of spring phytoplankton blooms. 1994.Crossref | GoogleScholarGoogle Scholar |

Vahtera, E., Conley, D. J., Gustafsson, B. G., Kuosa, H., Pitkänen, H., Savchuk, O. P., Tamminen, T., Viitasalo, M., Voss, M., Wasmund, N., and Wulff, F. (2007). Internal ecosystem feedbacks enhance nitrogen-fixing cyanobacteria blooms and complicate management in the Baltic Sea. Ambio 36, 186–194.
Internal ecosystem feedbacks enhance nitrogen-fixing cyanobacteria blooms and complicate management in the Baltic Sea.Crossref | GoogleScholarGoogle Scholar | 17520933PubMed |

von Liebig, J. (1855). ‘Principles of Agricultural Chemistry with Special Reference to the Late Researches Made in England.’ (Wiley: New York, NY, USA.)

Weeks, A. R., and Hoffmann, A. A. (2008). Frequency-dependent selection maintains clonal diversity in an asexual organism. Proceedings of the National Academy of Sciences of the United States of America 105, 17872–17877.
Frequency-dependent selection maintains clonal diversity in an asexual organism.Crossref | GoogleScholarGoogle Scholar | 19004792PubMed |

Winder, M., Berger, S. A., Lewandowska, A., Aberle, N., Lengfellner, K., Sommer, U., and Diehl, S. (2012). Spring phenological responses of marine and freshwater plankton to changing temperature and light conditions. Marine Biology 159, 2491–2501.
Spring phenological responses of marine and freshwater plankton to changing temperature and light conditions.Crossref | GoogleScholarGoogle Scholar |

Winemiller, K. O., McIntyre, P. B., Castello, L., Fluet-Chouinard, E., Giarrizzo, T., Nam, S., Baird, I. G., Darwall, W., Lujan, N. K., Harrison, I., Stiassny, M. L. J., Silvano, R. A. M., Fitzgerald, D. B., Pelicice, F. M., Agostinho, A. A., Gomes, L. C., Albert, J. S., Baran, E., Petrere Jr, M., Zarfl, C., Mulligan, M., Sullivan, J. P., Arantes, C. C., Sousa, L. M., Koning, A. A., Hoeinghaus, D. J., Sabaj, M., Lundberg, J. G., Armbruster, J., Thieme, M. L., Petry, P., Zuanon, J., Torrente Vilara, G., Snoeks, J., Ou, C., Rainboth, W., Pavanelli, C. S., Akama, A., van Soesbergen, A., and Sáenz, L. (2016). Balancing hydropower and biodiversity in the Amazon, Congo, and Mekong. Science 351, 128–129.
Balancing hydropower and biodiversity in the Amazon, Congo, and Mekong.Crossref | GoogleScholarGoogle Scholar | 26744397PubMed |

Winter, C., Bouvier, T., Weinbauer, M. G., and Thingstad, T. F. (2010). Trade-offs between competition and defense specialists among unicellular planktonic organisms: the ‘killing the winner’ hypothesis revisited. Microbiology and Molecular Biology Reviews 74, 42–57.
Trade-offs between competition and defense specialists among unicellular planktonic organisms: the ‘killing the winner’ hypothesis revisited.Crossref | GoogleScholarGoogle Scholar | 20197498PubMed |

Zhou, W., Yuan, X., Long, A., Huang, H., and Yue, W. (2014). Different hydrodynamic processes regulated on water quality (nutrients, dissolved oxygen, and phytoplankton biomass) in three contrasting waters of Hong Kong. Environmental Monitoring and Assessment 186, 1705–1718.
Different hydrodynamic processes regulated on water quality (nutrients, dissolved oxygen, and phytoplankton biomass) in three contrasting waters of Hong Kong.Crossref | GoogleScholarGoogle Scholar | 24122158PubMed |