Phytoplankton Succession in Recurrently Fluctuating Environments

Coastal marine systems are affected by seasonal variations in biogeochemical and physical processes, sometimes leading to alternating periods of reproductive growth limitation within an annual cycle. Transitions between these periods can be sudden or gradual. Human activities, such as reservoir construction and interbasin water transfers, influence these processes and can affect the type of transition between resource loading conditions. How such human activities might influence phytoplankton succession is largely unknown. Here, we employ a multispecies, multi-nutrient model to explore how nutrient loading switching mode might affect phytoplankton succession. The model is based on the Monod-relationship, predicting an instantaneous reproductive growth rate from ambient inorganic nutrient concentrations whereas the limiting nutrient at any given time was determined by Liebig’s Law of the Minimum. When these relationships are combined with population loss factors, such as hydraulic displacement of cells associated with inflows, a characterization of a species’ niche can be achieved through application of the R* conceptual model, thus enabling an ecological interpretation of modeling results. We found that the mode of reversal in resource supply concentrations had a profound effect. When resource supply reversals were sudden, as expected in systems influenced by pulsed inflows or wind-driven mixing events, phytoplankton were characterized by alternating succession dynamics, a phenomenon documented in inland water bodies of temperate latitudes. When resource supply reversals were gradual, as expected in systems influenced by seasonally developing wet and dry seasons, or annually occurring periods of upwelling, phytoplankton dynamics were characterized by mirror-image succession patterns. This phenomenon has not been reported previously in plankton systems but has been observed in some terrestrial plant systems. These findings suggest that a transition from alternating to “mirror-image” succession patterns might arise with continued coastal zone development, with crucial implications for ecosystems dependent on time-sensitive processes, e.g., spawning events and migration patterns.

[1]  D. Roelke,et al.  Phytoplankton Assemblage Characteristics in Recurrently Fluctuating Environments , 2015, PloS one.

[2]  H. Marshall,et al.  Phytoplankton and nutrient dynamics in a tidally dominated eutrophic estuary: daily variability and controls on bloom formation , 2014 .

[3]  C. Schobess,et al.  Paul Julius Möbius – Ein Schrittmacher in der Geschichte der Neuroophthalmologie , 2014, Klin Monatsbl Augenheilkd.

[4]  A. Long,et al.  Different hydrodynamic processes regulated on water quality (nutrients, dissolved oxygen, and phytoplankton biomass) in three contrasting waters of Hong Kong , 2014, Environmental Monitoring and Assessment.

[5]  Chunyan Li,et al.  Estuarine ecosystem response to three large-scale Mississippi River flood diversion events. , 2013, The Science of the total environment.

[6]  D. Roelke,et al.  Co-occurring and opposing freshwater inflow effects on phytoplankton biomass, productivity and community composition of Galveston Bay, USA , 2013 .

[7]  Yan Bai,et al.  Episodic phytoplankton bloom events in the Bay of Bengal triggered by multiple forcings , 2013 .

[8]  M. Pećarević,et al.  Controlling factors of phytoplankton seasonal succession in oligotrophic Mali Ston Bay (south-eastern Adriatic) , 2013, Environmental Monitoring and Assessment.

[9]  G. Tsirtsis,et al.  Effects of meteorological forcing on coastal eutrophication: modeling with model trees , 2012 .

[10]  L. Morellato,et al.  Reproductive phenology of a northeast Brazilian mangrove community: Environmental and biotic constraints , 2012 .

[11]  A. Lugliè,et al.  Long-term phytoplankton dynamics in a Mediterranean eutrophic lagoon (Cabras Lagoon, Italy) , 2012 .

[12]  C. Davis,et al.  Effects of surface forcing on interannual variability of the fall phytoplankton bloom in the Gulf of Maine revealed using a process-oriented model , 2011 .

[13]  A. Barbosa,et al.  Environmental Forcing of Phytoplankton in a Mediterranean Estuary (Guadiana Estuary, South-western Iberia): A Decadal Study of Anthropogenic and Climatic Influences , 2010 .

[14]  S. G. Marinone,et al.  Spatial Variability of Trace Metals and Inorganic Nutrients in Surface Waters of Todos Santos Bay, México in the Summer of 2005 During a Red Tide Algal Bloom , 2009, Archives of environmental contamination and toxicology.

[15]  Elena Litchman,et al.  Trait-Based Community Ecology of Phytoplankton , 2008 .

[16]  R. Sterner On the Phosphorus Limitation Paradigm for Lakes , 2008 .

[17]  G. Tsirtsis,et al.  Influence of terrestrial runoff on phytoplankton species richness-biomass relationships: A double stress hypothesis , 2008 .

[18]  D. Roelke,et al.  Mixing of Supersaturated Assemblages and the Precipitous Loss of Species , 2007, The American Naturalist.

[19]  T. Andersen,et al.  Seasonal phytoplankton nutrient limitation patterns as revealed by bioassays over Baltic Sea gradients of salinity and eutrophication , 2007 .

[20]  J. Olden,et al.  Homogenization of regional river dynamics by dams and global biodiversity implications , 2007, Proceedings of the National Academy of Sciences.

[21]  Tamar Zohary,et al.  Alternative states in the phytoplankton of Lake Kinneret, Israel (Sea of Galilee) , 2007 .

[22]  P. Montagna,et al.  The effect of freshwater inflow on net ecosystem metabolism in Lavaca Bay, Texas , 2006 .

[23]  C. Reynolds The Ecology of Phytoplankton , 2006 .

[24]  F. Magilligan,et al.  Changes in hydrologic regime by dams , 2005 .

[25]  A. Barbosa,et al.  Nutrients, light and phytoplankton succession in a temperate estuary (the Guadiana, south-western Iberia) , 2005 .

[26]  Ke Yin,et al.  Potential P limitation leads to excess N in the pearl river estuarine coastal plume , 2004 .

[27]  Michael Elliott,et al.  The Estuarine Ecosystem: Ecology, Threats, and Management , 2004 .

[28]  D. Roelke,et al.  Interannual variability in the seasonal plankton succession of a shallow, warm-water lake , 2004, Hydrobiologia.

[29]  Tamiji Yamamoto,et al.  Pulsed nutrient supply as a factor inducing phytoplankton diversity , 2004 .

[30]  T. Abe,et al.  Seasonal changes of floral frequency and composition of flower in two cool temperate secondary forests in Japan , 2003 .

[31]  K. Yin Monsoonal influence on seasonal variations in nutrients and phytoplankton biomass in coastal waters of Hong Kong in the vicinity of the Pearl River estuary , 2002 .

[32]  J. Huisman,et al.  Towards a solution of the plankton paradox : the importance of physiology and life history , 2001 .

[33]  F. Sklar,et al.  Nutrient Dynamics in Vegetated and Unvegetated Areas of a Southern Everglades Mangrove Creek , 2001 .

[34]  S. Interlandi,et al.  LIMITING RESOURCES AND THE REGULATION OF DIVERSITY IN PHYTOPLANKTON COMMUNITIES , 2001 .

[35]  Franz J. Weissing,et al.  Fundamental Unpredictability in Multispecies Competition , 2001, The American Naturalist.

[36]  C. Philippart,et al.  Long‐term phytoplankton‐nutrient interactions in a shallow coastal sea: Algal community structure, nutrient budgets, and denitrification potential , 2000 .

[37]  M. Vernet,et al.  Growth limitation in young Euphausia superba under field conditions , 2000 .

[38]  J. Huisman,et al.  Biodiversity of plankton by species oscillations and chaos , 1999, Nature.

[39]  D. Roelke,et al.  Nutrient and phytoplankton dynamics in a sewage-impacted Gulf coast estuary: A field test of the PEG-model and equilibrium resource competition theory , 1997 .

[40]  T. Vincent,et al.  Trade-Offs and Coexistence in Consumer-Resource Models: It all Depends on what and where you Eat , 1996, The American Naturalist.

[41]  H. Paerl Nuisance phytoplankton blooms in coastal, estuarine, and inland waters1 , 1988 .

[42]  N. Caraco,et al.  Nutrient Limitation of Phytoplankton Growth in Brackish Coastal Ponds , 1987 .

[43]  Ulrich Sommer,et al.  The PEG-model of seasonal succession of planktonic events in fresh waters , 1986, Archiv für Hydrobiologie.

[44]  U. Sommer The paradox of the plankton: Fluctuations of phosphorus availability maintain diversity of phytoplankton in flow-through cultures’ , 2000 .

[45]  R. Cook,et al.  The Major Biogeochemical Cycles and Their Interactions. , 1983 .

[46]  D. Tilman Resource competition and community structure. , 1983, Monographs in population biology.

[47]  J. P. Grime,et al.  A QUANTITATIVE ANALYSIS OF SHOOT PHENOLOGY AND DOMINANCE IN HERBACEOUS VEGETATION , 1977 .

[48]  J. A. León,et al.  Competition between two species for two complementary or substitutable resources. , 1975, Journal of theoretical biology.

[49]  C. E. Morales,et al.  The structure of planktonic communities under variable coastal upwelling conditions off Cape Ghir (31°N) in the Canary Current System (NW Africa) , 2014 .

[50]  R. Pilkaitytė,et al.  Seasonal changes in phytoplankton composition and nutrient limitation in a shallow Baltic lagoon , 2007 .

[51]  W.,et al.  Nutrient limitation of phytoplankton in Chesapeake Bay , 2006 .

[52]  N. Noguer,et al.  Groningen von Liebig ' s Law of the Minimum and Plankton Ecology ( 1899-1991 ) , 2022 .

[53]  R. Sterner,et al.  Algal growth in warm temperate reservoirs: Nutrient-dependent kinetics of individual taxa and seasonal patterns of dominance , 1999 .

[54]  J. Grover Resource Competition , 1997, Population and Community Biology Series.

[55]  de Henricus Baar,et al.  von Liebig's law of the minimum and plankton ecology (1899–1991) , 1994 .

[56]  Ulrich Sommer,et al.  Plankton ecology, succession in plankton communities , 1989 .

[57]  Jacques Monod,et al.  LA TECHNIQUE DE CULTURE CONTINUE THÉORIE ET APPLICATIONS , 1978 .