Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations

Abstract

In field populations of the mixotrophic dinoflagellate Ceratium furca, feeding on microzooplankton is commonly observed and is influenced by inorganic nutrient concentrations and ratios. Using batch and 'semi-continuous' laboratory cultures, we examined in more detail the nutrient conditions that trigger feeding in C. furca. Cultures were maintained at a range of nitrogen (N) and phosphorus (P) concentrations for 31 to 36 d. Several parameters were determined at regular intervals, including inorganic nutrient concentrations of the medium, C. furca abundance and size, cellular chlorophyll a (chl a), C, N, and P contents and densities, photosynthetic rates, and ingestion of ciliate prey. We detected significant differences between treatments in all cellular parameters measured. Most notably, feeding only occurred in cultures that had been growing under N-or P-deplete conditions for 11 to 16 d, whereas nutrient-replete cells did not ingest prey. Feeding increased markedly as cellular C:N:P ratios deviated farther from those found under optimum growth conditions. Specifically, feeding in P-deplete cultures increased at C:P ratios >130 and at N:P ratios >19, whereas N-deplete cultures required a C:N ratio of ~10 and an N:P ratio < 7 to commence feeding. Growth and photosynthetic rates were reduced compared to those of nutrient-replete cells regardless of the limiting nutrient. In N-limited cultures, cell size and chl a density decreased compared to nutrientreplete cells, whereas the size of P-limited cells significantly increased. This change in average cell size was caused by the development of a bimodal size distribution under N-and P-reduced conditions, raising the possibility of sexual reproduction in C. furca. Changes in cellular parameters were reversible upon nutrient addition, and feeding decreased or ceased within hours to days. The findings presented here indicate that cellular nutrient quotas and ratios are more critical than absolute inorganic nutrient concentrations in regulating feeding behavior of C. furca.

Influence of inorganic nutrients, irradiance, and time of day on food uptake by the mixotrophic dinoflagellate Neoceratium furca

“…Mixotrophy in laboratory cultures of Neoceratium furca (= Ceratium furca) is strongly influenced by nutrient concentrations, with feeding increasing drastically when cells become nutrient limited (Smalley et al 2003). In the present study, we document a similar effect of inorganic nutrients on field populations of N. furca.…”

“…Feeding was determined over a 6 h period. Different letters indicate significant differences between means (p < 0.05) trations in regulating feeding behavior, especially when inorganic nutrient concentrations are changing rapidly (Smalley et al 2003). In P-depleted laboratory cultures of Neoceratium furca (= Ceratium furca), feeding was induced above a cellular N:P ratio of 19, while N-depleted cultures required a cellular N:P ratio below 7 to commence feeding.…”

“…In the laboratory, feeding in N. furca was strongly influenced by dissolved inorganic nutrient concentrations and cellular carbon (C), nitrogen (N), and phosphorus (P) content (Smalley et al 2003), suggesting that N. furca may be a Type IIA mixotroph. In the present study, we examined the relationship between feeding and nutrients in field populations of N. furca.…”

The functional role of planktonic mixotrophs in altering seston stoichiometry

“…Several studies have investigated concentrations of particular nutrients in mixotrophic flagellates, but most of them focused more on the effect of light, temperature and dissolved nutrient conditions on phagotrophic feeding and its contribution to C and nutrient budgets (Caron et al 1993, Li et al 2000, Skovgaard et al 2000, Smalley et al 2003, Carvalho & Granéli 2010, Simonds et al 2010, Brutemark & Granéli 2011, Wilken et al 2014, Johnson 2015 or on the relationship of internal nutrient concentrations and toxin production in different harmful dinoflagel-lates (Johnsen et al 1999, John & Flynn 2000, Van de Waal et al 2013, Pérez Blanco et al 2015. We are aware of only 2 empirical studies that have specifically addressed the balance of intracellular nutrients in particular mixotrophs and its dependence on environmental factors and potential differences in their nutrient stoichiometry compared to purely phototrophic or heterotrophic organisms.…”

Palynomorph Assemblages Dominated by Heterotrophic Marine Palynomorphs in Tropical Coastal Shallow-water Sediments from the Southern Myanmar Coast

“…This species has usually been regarded as autotrophic because it possesses many chloroplasts. However, C. furca can also consume ciliates as prey organisms (Bockstahler & Coasts 1993, Smalley et al 2003 and is thus a phagotrophic species (Stoecker 1999). C. furca can reproduce under non-photosynthetically suitable yet unfavorable environmental conditions, such as low light irradiance and nutrient depletion, by switching to an exordial nutrition ratio mixotrophic mode capability and preying on other organisms like bacteria (Stoecker 1999, Jeon et al 2010.…”