Mixotrophy in Heterocapsa rotundata: A mechanism for dominating the winter phytoplankton

Heterocapsa rotundata is a mixotrophic dinoflagellate that can ingest picoplankton, including bacteria, and is known to form large blooms in temperate estuaries during wet winters, particularly when grazing pressure on phytoplankton is low. We hypothesized that phagotrophy gives H. rotundata an advantage over other phytoplankton species during low light conditions. We used laboratory and field experiments to investigate changes in phagotrophy by H. rotundata in response to changes in light availability. Prey removal experiments with a non‐axenic culture of H. rotundata were used to determine changes in H. rotundata's ingestion rates in response to changes in irradiance. Fluorescent microspheres were used to measure in situ ingestion rates of H. rotundata collected on 20 different occasions from the Choptank River during the winter of 2016. In situ H. rotundata ingestion rates were tested for correlation with inorganic nutrient concentrations and irradiance levels. Ingestion rates measured with cultured and in situ H. rotundata followed similar patterns and ingestion rates increased as irradiance decreased. H. rotundata has the potential to obtain nutrients from multiple nutrient sources, switching from phototrophy to partial heterotrophy as irradiance decreases. This response may allow H. rotundata to survive and to potentially form blooms when growth rates of most other estuarine phytoplankton species is low.

[1]  E. Sherr,et al.  Preservation and Storage of Samples for Enumeration of Heterotrophic Protists , 2018 .

[2]  D. Stoecker,et al.  Top-down control by micro- and mesozooplankton on winter dinoflagellate blooms of Heterocapsa rotundata , 2015 .

[3]  S. Balzano,et al.  Seasonal changes in phytoplankton on the north-eastern shelf of Kangaroo Island (South Australia) in 2012 and 2013 , 2015 .

[4]  A. Godhe,et al.  The relationship between variation of phytoplankton species composition and physico-chemical parameters in northern coastal waters of Mumbai, India , 2015 .

[5]  R. Gast,et al.  Physiological Responses of Three Species of Antarctic Mixotrophic Phytoflagellates to Changes in Light and Dissolved Nutrients , 2014, Microbial Ecology.

[6]  J. Göbel,et al.  Effects of nitrogen concentration on the taxonomic and functional structure of phytoplankton communities in the Western Baltic Sea and implications for the European water framework directive , 2014, Hydrobiologia.

[7]  U. Tillmann,et al.  Morphological and molecular characterization of the small armoured dinoflagellate Heterocapsa minima (Peridiniales, Dinophyceae) , 2014 .

[8]  É. Potvin,et al.  Mixotrophy in the newly described dinoflagellate Ansanella granifera: feeding mechanism, prey species, and effect of prey concentration , 2014 .

[9]  Nico Boon,et al.  Routine bacterial analysis with automated flow cytometry. , 2013, Journal of microbiological methods.

[10]  Gary B. Collins,et al.  Vitro Determination of Chlorophyll a and Pheophytin a in Marine and Freshwater Algae by Fluorescence , 2013 .

[11]  R. Gast,et al.  Bacterivory by phototrophic picoplankton and nanoplankton in Arctic waters. , 2012, FEMS microbiology ecology.

[12]  N. Silva,et al.  Importance of mixotrophic nanoplankton in Aysén Fjord (Southern Chile) during austral winter , 2011, CSR 2011.

[13]  H. Jeong,et al.  Mixotrophy in the Newly Described Phototrophic Dinoflagellate Woloszynskia cincta from Western Korean Waters: Feeding Mechanism, Prey Species and Effect of Prey Concentration , 2011, The Journal of eukaryotic microbiology.

[14]  H. Jeong,et al.  Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs , 2010 .

[15]  H. Jeong,et al.  Bacterivory by co-occurring red-tide algae, heterotrophic nanoflagellates, and ciliates , 2006 .

[16]  V. Suriyanon,et al.  IN R , 2006 .

[17]  Michael R. Roman,et al.  Eutrophication of Chesapeake Bay: historical trends and ecological interactions , 2005 .

[18]  J. Lund,et al.  The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting , 1958, Hydrobiologia.

[19]  T. Fisher,et al.  A long-term record of photosynthetically available radiation (PAR) and total solar energy at 38.6°N, 78.2°W , 2003 .

[20]  I. Domaizon,et al.  Taxon-specific and seasonal variations in flagellates grazing on heterotrophic bacteria in the oligotrophic Lake Annecy - importance of mixotrophy. , 2003, FEMS microbiology ecology.

[21]  Roger Harris,et al.  ICES zooplankton methodology manual , 2000 .

[22]  D. Stoecker,et al.  Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications , 1998 .

[23]  G. Hansen.  Analysis of the thecal plate pattern in the dinoflagellate Heterocapsa rotundata (Lohmann) comb. nov. (=Katodinium rotundatum (Lohmann) Loeblich) , 1995 .

[24]  J. Gasol,et al.  Grazing rates on bacteria: the significance of methodology and ecological factors , 1994 .

[25]  Sanghoon Lee.  Measurement of carbon and nitrogen biomass, and biovolume from naturally derived marine bacterioplankton , 1992 .

[26]  A. Ōkubo,et al.  On the use of surrogate food particles to measure protistan ingestion , 1991 .

[27]  K. Sellner,et al.  Importance of a winter dinoflagellate-microflagellate bloom in the Patuxent River estuary , 1991 .

[28]  K. Porter,et al.  Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community , 1989 .

[29]  R. Fallon,et al.  Use of monodispersed, fluorescently labeled bacteria to estimate in situ protozoan bacterivory. , 1987, Applied and environmental microbiology.

[30]  R. Cohen.  Physical processes and the ecology of a winter dinoflagellate bloom of Katodinium rotundatum , 1985 .

[31]  M. Perry,et al.  Photoadaption in marine phytoplankton: Response of the photosynthetic unit , 1981 .

[32]  B. Frost.  EFFECTS OF SIZE AND CONCENTRATION OF FOOD PARTICLES ON THE FEEDING BEHAVIOR OF THE MARINE PLANKTONIC COPEPOD CALANUS PACIFICUS1 , 1972 .