Pulse feeding and pulse growth: a highly adaptive strategy of heterotrophic dinoflagellates Oxyrrhis marina

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Pulse feeding and growth of the Black Sea strain of dinof lagellates Oxyrrhis marina (Dujardin, 1841) (OXY–IBSS), equivalent spherical diameter (ESD) (23.5 ± 3.1 mm) have been studied under experimental conditions simulating phytoplankton blooms. Microalgae Phaeodactylum tricornutum (P, ESD 3.4 ±0.3 mm), Isochrysis galbana (I, ESD 3.7 ± 0.4 mm), Tetraselmis suecica (T, ESD 6.1 ± 0.9 mm), and Rhodomonas salina (R, 7.4 ± 0.7 µm) were used as food objects in a one-component and three-component suspensions. Microalgae concentrations (~106 cells/mL for T and R; up to ~4 × 106 cells/mL for P and I) were chosen to ensure their equal total carbon biomass ~0.02 mg C/mL in the food mixtures at the beginning of the experiment. Under ad libitum conditions, the maximum clearance rates of the OXY–IBSS reached 0.1–0.5 mL ind./day, and the grazing rate of microalgae was 34–44 cells/(ind h) for P and I, and 2–11 cells/(ind. h) for R and T, respectively. The grazing rate of microalgae in carbon units was significantly higher when feeding on I (3.9 ng C/(ind. day)) and significantly less when fed with a mixture of microalgae TRP (1.5 ng C/(ind. day)). Maximum abundance of OXY–IBSS, achieved within 3 or 4 days (by the time the microalgae concentration decreased below threshold), varied from 19 × 103 ind./mL (P) to 43 × 103 ind./mL (I). In the absence of food, dinof lagellates O. marina turned to cannibalism, and within 4 days the oscillating f luctuations (within 50%) in their number took place. Although the specific population growth rate (m, day-1) of OXY–IBSS was higher when feeding on small cells (~2 days–1 on I), the gross growth efficiency (GGE) of OXY–IBSS was significantly higher when fed on large (T and R) microalgae (26–29% vs. 14–15%). At lower daily rations (DRs) when fed with the mixture TRP, the GGE of OXY–IBSS was significantly higher (41%) when compared to other nutritional conditions. The feeding strategy of opportunistic predator O. marina on diverse (in terms of size and chemotaxonomic characteristics) mixtures of prey lay in a f lexible choice between high specific population growth rate, or high gross growth efficiency, that obviously gives the populations of this species the advantages over other protists under conditions of the pulsed phytoplankton blooms.

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Sobre autores

A. Khanaychenko

Institute of Biology of the South Seas

Autor responsável pela correspondência
Email: a.khanaychenko@gmail.com
Rússia, Sevastopol

L. Aganesova

Institute of Biology of the South Seas

Email: a.khanaychenko@gmail.com
Rússia, Sevastopol

V. Mukhanov

Institute of Biology of the South Seas

Email: a.khanaychenko@gmail.com
Rússia, Sevastopol

Bibliografia

  1. Бегун А.А., Орлова Т.Ю., Селина М.С. 2004. Случай “цветения” воды в Амурском заливе Японского моря, вызванный динофитовой водорослью Oxyrrhis marina Dujardin, 1841 // Биология моря. T. 30. № 1. С. 68.
  2. Заика В.Е. 1972. Удельная продукция водных беспозвоночных. Киев: Наук. думка.
  3. Романова Н.Д., Мазей Ю.А., Тихоненков Д.В. и др. 2013. Сообщества гетеротрофных микроорганизмов на границе “вода–дно” в Карском море // Океанология. Т. 53. Вып. 3. С. 375. https://doi.org/10.7868/s0030157413030106
  4. Стельмах Л.В., Мансурова И.М. 2021. Физиологический механизм выживания динофитовых водорослей в условиях биогенного лимитирования // Биология внутр. вод. № 2. С. 1987. https://doi.org/10.31857/S0320965221020157.
  5. Anderson S.R., Menden-Deuer S. 2017. Growth, grazing, and starvation survival in three heterotrophic dinoflagellate species // J. Eukaryotic Microbiol. V. 64. № 2. P. 213. https://doi.org/10.1111/jeu.12353
  6. Calbet A., Isari S., Martínez R.A. et al. 2013. Adaptations to feast and famine in different strains of the marine heterotrophic dinoflagellates Gyrodinium dominans and Oxyrrhis marina // Mar. Ecol. Prog. Ser. V. 483. P. 67. https://doi.org/10.3354/meps10291
  7. Cucci T.L., Shumway S.E., Brown W.S., Newell C.R. 1989. Using phytoplankton and flow cytometry to analyze grazing by marine organisms // Cytometry: The Journal of the International Society for Analytical Cytology. V. 10. № 5. P. 659. https://doi.org/10.1002/cyto.990100523
  8. Droop M.R. 1959. Water-soluble factors in the nutrition of Oxyrrhis marina // J. Mar. Biol. Assoc. U K. V. 38. № 3. P. 605. https://doi.org/10.1017/s0025315400007037
  9. Frost B.W. 1972. Effects of size and concentration of food particles on the feeding behavior of the Marine planktonic copepod Calanus pacificus // Limnol., Oceanogr. V. 6. P. 805. https://doi.org/10.4319/lo.1972.17.6.0805
  10. Goldman J.C., Dennett M.R., Gordin H. 1989. Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina // J. Plankton Res. V. 11. № 2. P. 391. https://doi.org/10.1093/plankt/11.2.391
  11. Jeong H.J., You J.H., Lee K.H. et al. 2018. Feeding by common heterotrophic protists on the mixotrophic alga Gymnodinium smaydae (Dinophyceae), one of the fastest growing dinoflagellates // J. Phycol. V. 54. № 5. P. 734. https://doi.org/10.1111/jpy.12775
  12. Khanaychenko A., Mukhanov V., Aganesova L. et al. 2018. Grazing and feeding selectivity of Oithona davisae in the Black Sea: importance of cryptophytes // Turkish J. Fish and Aquat. Sci. V. 18. № 8. P. 937. http://doi.org/10.4194/1303-2712-v18_8_02
  13. Khanaychenko A.N., Telesh I.V., Skarlato S.O. 2019. Bloom-forming potentially toxic dinoflagellates Prorocentrum cordatum in marine plankton food webs // Protistology. V. 13. P. 95. https://doi.org/10.21685/1680-0826-2019-13-3-1
  14. Menden-Deuer S., Lessard E.J. 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton // Limnol., Oceanogr. V. 45. № 3. P. 569. https://doi.org/10.4319/lo.2000.45.3.0569
  15. Meunier C.L., Hantzsche F.M., Cunha-Dupont A.Ö. et al. 2012. Intraspecific selectivity, compensatory feeding and flexible homeostasis in the phagotrophic flagellate Oxyrrhis marina: three ways to handle food quality fluctuations // Hydrobiologia. V. 680. № 1. P. 53. https://doi.org/10.1007/s10750-011-0900-4
  16. Olson R.J., Zettler E.R., DuRand M.D. 1993. Phytoplankton analysis using flow cytometry // Handbook of methods in aquatic microbial ecology. Publishers, Boca Raton, FL. P. 175. https://doi.org/10.1201/9780203752746-23
  17. Parrish C.C., French V.M., Whiticar M.J. 2012. Lipid class and fatty acid composition of copepods (Calanus finmarchicus, C. glacialis, Pseudocalanus sp., Tisbe furcata and Nitokra lacustris) fed various combinations of autotrophic and heterotrophic protists // J. Plankton Res. V. 1. № 34(5). P. 356. https://doi.org/10.1093/plankt/fbs003
  18. Roberts E.C., Wootton E.C., Davidson K. et al. 2011. Feeding in the dinoflagellate Oxyrrhis marina: Linking behaviour with mechanisms // J. Plankton Res. V. 33. P. 603. https://doi.org/10.1093/plankt/fbq118
  19. Telesh I., Schubert H., Skarlato S. 2021. Abiotic stability promotes dinoflagellate blooms in marine coastal ecosystems // Estuarine Coastal Shelf Sci. V. 251. P. 107239. https://doi.org/10.1016/j.ecss.2021.107239
  20. Vanderploeg A.H., Scavia D. 1979. Two electivity indices for feeding with special reference to zooplankton grazing // J. Fish Res. Board Can. V. 36. P. 362. https://doi.org/10.1139/f79-055

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2. Fig. 1. Micrographs of the original cells: a — living cells of Tetraselmis sp. from the microcenosis of a temporary splash pond (Tetraselmis sp. + Oxyrrhis marina); b — living cells of Tetraselmis sp. and O. marina from a natural pond; c — an O. marina cell with Tetraselmis sp. inside and free Tetraselmis sp. cells after fixation with Lugol's solution; d — a living O. marina cell from a laboratory culture.

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3. Fig. 2. Gating of microalgae from three-component mixtures of TRI (a, b) and TRP (c, d) on two-parameter cytograms of direct light scattering (FS) and autofluorescence in the red (FL4, chlorophyll a) and orange (FL2, phycoerythrin) regions of the spectrum: I — Isochrysis galbana, P — Phaeodactylum tricornutum, T — Tetraselmis suecica, R — Rhodomonas salina.

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4. Fig. 3. Dynamics of changes in the cell number (N, cells/ml) of microalgae and Oxyrrhis marina in single-component suspensions: a — with Isochrysis galbana (I); b — with Phaeodactylum tricornutum (P); c — with Rhodomonas salina (R); d — with Tetraselmis suecica (T). O–P, O–I, O–T, O–R — the number of O. marina when feeding on the corresponding microalgae.

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5. Fig. 4. Dynamics of changes in the cell number (cells/ml) of microalgae in three-component mixtures of TRI (a) and TRP (b); dynamics of changes in the cell number of Oxyrrhis marina (cells/ml) in TRI and TRP mixtures and in the absence of microalgae (O-O) (c); dynamics of changes in the carbon equivalent of O. marina biomass in TRI and TRP mixtures and in the absence of microalgae (O-O) (d). Here and in Figs. 5, 6: I — Isochrysis galbana; N — abundance; O — Oxyrrhis marina, P –Phaeodactylum tricornutum, R — Rhodomonas salina, T — Tetraselmis suecica.

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6. Fig. 5. Filtration rates (F, nl/(specimen day)) and consumption rates of microalgae cells (Gi, cells/(specimen day)) and the carbon equivalent of their biomass (Gc, pg C/(specimen day)) by dinoflagellates from ad libitum to threshold concentrations in single-component suspensions.

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7. Fig. 6. Selectivity indices (Ei) of microalgae cells from three-component mixtures TRI (a, c) and TRP (b, d) on the 1st day of the experiment (a, b) and for 3 days in total (c, d).

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8. Fig. 7. Efficiency of carbon use from consumed microalgae on the increase in the carbon equivalent of biomass of heterotrophic dinoflagellates O. marina (GGE, %) when fed in one-component mixtures (O–P — Phaeodactylum tricornutum; O–R — Rhodomonas salina; O–T — Tetraselmis suecica; O–I — Isochrysis galbana) and in three-component mixtures of microalgae (O–TRI — Tetraselmis suecica, Rhodomonas salina, Isochrysis galbana and O–TRP — Tetraselmis suecica, Rhodomonas salina, Phaeodactylum tricornutum).

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