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Abstract
The state art of dinoflagellate heterotrophy are reviewed in this paper. Heterotrophic dinoflagellates are widespreadly in dinoflagellates, only few species are living on autotrophic mechanism sensu stricto (autotrophic amphitrophy) alone. Nearly half of the dinoflagellate species are apochlorotic, and the rest dinoflagellate species have organic nutritional needs even if they have chloroplasts, called mixotrophy. These mixotrophy dinoflagellates do not necessarily uptake organic compounds as the major carbon sources, but vitamins, biotin and so on for growth and reproduction. The mixotrophy dinoflagellates can live not only on actively uptaking dissovled organic matters (osmotrophy) and extracellular digestion of food with subsequent uptake of the dissolved products (saprotrophy), but also parasitic (parasitism) and symbiotic (symbiosis) way to support their growth. Most apochlorotic dinoflagellates live on organic matters as their only carbon source, called heterotrophic amphitrophy sensu stricto, or organotrophy, which are the majority of heterotrophic dinoflagellates. There are three types of organotrophy, parasitic organotrophy, symbiosis organotrophy and phagotrophy. This article discusses the three kinds of phagotrophy in detail: phagotrophic feeding, peduncle feeding and pallium feeding. Phagotrophic feeding is commonly found in either thecate or athecate apochlorotic dinoflagellates, phagotrophic dinoflagellates mainly feed through the junction of the flagellar grooves in sulcus or the bottom of the hypotheca for the prey, but through the apical hole and suture are also found. Peduncle feeding dinoflagellates feed by means of an extinsible, tube-like "peduncle/ phagopod", by which attached to unicellular algae, ciliates and even small metazoans, pierce through their prey cytoplasmic membrane and suck their cytoplasma to get the nutrition. Peduncle feeding is the majority of phagotrophy in dinoflagellates. Pallium feeding only is found in Protoperidinium and Diplopsalis, feeding on other plankton with a pallium (sac) extruded from a microtubular basket outside the cell, wrapping and digesting the prey in pallium. The sizes of dinoflagellates prey have a wide range, from a few microns to hundreds of microns. Some dinoflagellates feed selectively. They locate and feed on special prey by chemical sensing, and consequently increase the biovolume and ecdysis. Other types of heterotrophic feeding by dinoflagellates, such as filter/ interception feeding, pseudopodial feeding, stompopd feeding, tentacle/ piston feeding etc., is briefly introduced in this article. The methodology of dinoflagellate heterotroph study, an attempt to understand the evolutionary meaning of these heterotrophic manifestations, their implications on the marine ecosystem, and future research topics are also briefly discussed.
... Species identification, individual counting, and linear parameter measurement were performed under a microscope (Motic Panthera L) at a magnification of 100-400X. For the species identification of MZP, we assumed that they were mainly heterotrophic, given that no chloroplasts were observed in the dinoflagellates group, purely autotrophic types of dinoflagellates are rare (Lessard and Swift, 1985), and heterotrophic or mixotrophic types are present in almost exclusively all dinoflagellates (Sun and Guo, 2011). This procedure has been adopted in many studies (Paterson et al., 2007;Jyothibabu et al., 2008b;Stoecker et al., 2014b;Yong et al., 2022). ...
Microzooplankton (MZP) are an important part of the microbial food web and play a pivotal role in connecting the classic food chain with the microbial loop in the marine ecosystem. They may play a more important role than mesozooplankton in the lower latitudes and oligotrophic oceans. In this article, we studied the species composition, dominant species, abundance, and carbon biomass of MZP, including the relationship between biological variables and environmental factors in the eastern equatorial Indian Ocean during the spring intermonsoon. We found that the MZP community in this ocean showed a high species diversity, with a total of 340 species. Among these, the heterotrophic dinoflagellates (HDS) (205 species) and ciliates (CTS) (126 species) were found to occupy the most significant advantageous position. In addition, CTS (45.3%) and HDS (39.7%) accounted for a larger proportion of the population abundance, while HDS (47.1%) and copepod nauplii (CNP) (46.4%) made a larger contribution to the carbon biomass. There are significant differences in the ability of different groups of MZP to assimilate organic carbon. In this sea area, MZP are affected by periodic currents, and temperature is the main factor affecting the distribution of the community. The MZP community is dominated by eurytopic species and CNP. CTS are more sensitive to environmental changes than HDS, among which Ascampbelliella armilla may be a better habitat indicator species. In low-latitude and oligotrophic ocean areas, phytoplankton with smaller cell diameters were found to occupy a higher proportion, while there was no significant correlation between the total concentration of integrated chlorophyll a and the biological variables of MZP. Therefore, we propose that the relationship between size-fractionated phytoplankton and MZP deserves further study. In addition, the estimation of the carbon biomass of MZP requires the establishment of more detailed experimental methods to reflect the real situation of organisms. This study provides more comprehensive data for understanding the diversity and community structure of MZP in the eastern equatorial Indian Ocean, which is also of good value for studying the adaptation mechanism and ecological functions of MZP in low-latitude and oligotrophic ocean ecosystems.
... There were distinct differences in DN uptake among different phytoplankton, in JB, we found that S. costatum preferred to absorb NH 4 -N and NO 3 -N, while P. pellucidum preferred to absorb DON Domestic . Most diatoms are photoautotrophic, while most dinoflagellates are heterotrophic or mixotrophs (Gaines, 1987;Lee et al., 2016) and can use organic matter for phytoplankton growth, metabolism, and reproduction (Sun and Guo, 2011), indicating that dinoflagellates have a higher competitive advantage in DON-rich environments, especially dinoflagellates that can directly phagocytose DON (Jeong et al., 2005). The uptake efficiency of DON Domestic depends on its composition, because usually small molecule DON Domestic can be directly absorbed by phytoplankton, while large molecules can be absorbed after degradation (Bronk and Ward, 2005). ...
... The seasonal differences of DDSi/ DDIN ratios were attributed to the difference of phytoplankton dominant species in different seasons. Studies have shown that diatoms prefer environments with low light and nutrient rich, while most dinoflagellates are heterotrophic or mixed trophic species, enabling them to adapt to waters with high light and low nutrient levels (Sun and Guo, 2011). As mentioned above, nutrients in autumn and winter were more abundant than those in late spring and summer in the Bohai Sea. ...
The Bohai Sea is a habitat for economically important fish in China, but its ecological environment has changed significantly, and it is necessary to further clarify the dynamics and the internal resupply channels of nutrients in the Bohai Sea. Based on four field observations in the Bohai Sea from May to December 2019, the nutrient dynamics were addressed. The concentration of dissolved inorganic nutrients was depleted throughout the water column in spring and in the euphotic zone in summer and accumulated in the bottom water in summer and in the water column in autumn and winter. Relative phosphorus limitation was present in Laizhou Bay and its surrounding area in all seasons, while relative silicon limitation was evident in spring and relative nitrogen limitation was significant in summer in most other study aeras. The results of end-member mixing model illustrated significant seasonal differences in the nutrient uptake ratios, which may be related to various factors such as different phytoplankton composition and phosphorus turnover rates. Turbulent entrainment was an important nutrient pathway for primary production in the euphotic zone of Central Bohai Sea during the stratification season, with an estimated average nutrient flux of 6.04 ± 9.63, 0.22 ± 0.19 and 6.97 ± 6.61 mmol·m-2·d-1 for DIN, DIP and DSi, respectively.
... Dinoflagellates have the ability of utilizing dissolved organic matters which compensates for the shortage of inorganic nutrients ( Smayda, 1997). In addition, many dinoflagellates (e.g., Gymnodinium, Gyrodinium) can live on mixotrophy modes which may also facilitate their dominance in the nutrient-limited environment ( Sun and Guo, 2011). The positive correlation between water temperature and pH can be explained by the influence of temperature on CO 2 solubility. ...
Pyrosequencing of the 18S rRNA gene has been widely adopted to study the eukaryotic diversity in various types of environments, and has an advantage over traditional morphology methods in exploring unknown microbial communities. To comprehensively assess the diversity and community composition of marine protists in the coastal waters of China, we applied both morphological observations and high-throughput sequencing of the V2 and V3 regions of 18S rDNA simultaneously to analyze samples collected from the surface layer of the Yellow and East China Seas. Dinoflagellates, diatoms and ciliates were the three dominant protistan groups as revealed by the two methods. Diatoms were the first dominant protistan group in the microscopic observations, with Skeletonema mainly distributed in the nearshore eutrophic waters and Chaetoceros in higher temperature and higher pH waters. The mixotrophic dinoflagellates, Gymnodinium and Gyrodinium, were more competitive in the oligotrophic waters. The pyrosequencing method revealed an extensive diversity of dinoflagellates. Chaetoceros was the only dominant diatom group in the pyrosequencing dataset. Gyrodinium represented the most abundant reads and dominated the offshore oligotrophic protistan community as they were in the microscopic observations. The dominance of parasitic dinoflagellates in the pyrosequencing dataset, which were overlooked in the morphological observations, indicates more attention should be paid to explore the potential role of this group. Both methods provide coherent clustering of samples. Nutrient levels, salinity and pH were the main factors influencing the distribution of protists. This study demonstrates that different primer pairs used in the pyrosequencing will indicate different protistan community structures. A suitable marker may reveal more comprehensive composition of protists and provide valuable information on environmental drivers.
... This result may relate to the heterotrophy feature of dinoflagellates. Most phototrophic dinoflagellates have been considered to be mixotrophic, which could utilize nutrients from particulate food or directly feed on co-occurring diatoms in nutrient-limited conditions (Jeong et al., 2004;Lagus et al., 2004;Sun and Guo, 2011). For example, Yoo et al. (2009) observed that P. donghaiense and P. triestinum could feed on S. costatum. ...
With the rapid development of economy and increase of population in the drainage areas, the nutrient loading has increased dramatically in the Changjiang estuary and adjacent coastal waters. To properly assess the impact of nutrient enrichment on phytoplankton community, seasonal microcosm experiments were conducted during August 2010–July 2011 in the coastal waters of Zhejiang Province. The results of the present study indicated that the chl a concentration, cell abundance, diversity indices, species composition and community succession of the phytoplankton varied significantly with different N/P ratios and seasons. Higher growth was observed in the 64:1 (spring), 32:1 (summer), 16:1 (autumn) and 128:1, 256:1 (winter) treatments, respectively. The values of Shannon-Wiener index (H′) and Pielou evenness index (J) were lower in the 8:1 and 16:1 treatments in autumn test, while H′ value was higher in the 128:1 and 8:1 treatments in winter test. A definite community succession order from diatoms to dinoflagellates was observed in the autumn and winter tests, while the diatoms dominated the community throughout the culture in the spring and summer tests.
... This result could be explained by the overriding effect of DIN limitation (1.35 μmol L −1 ) in this treatment. Moreover, most phototrophic dinoflagellates have been considered to be mixotrophic, which could utilize nutrients from particulate food or directly feed by co-occurring diatoms in nutrient-limited conditions (Jeong et al., 2004;Lagus et al., 2004;Sun and Guo, 2011). For example, Yoo et al. (2009) observed that P. donghaiense and P. triestinum could feed on S. costatum. ...
In the present study, a microcosm experiment was conducted for 12 days during the spring near Dongtou Island in the East China Sea with the aim of investigating the effects of different nitrogen-phosphorus (N/P) ratios (1N:1P, 4N:1P, 16N:1P, 64N:1P, and 256N:1P) on phytoplankton community growth and succession. The results indicated that the cell abundance, chlorophyll a (chl a) concentration, specific growth rate, diversity indices, and species composition of the phytoplankton community varied significantly with the N/P ratios. A higher growth rate (evaluated based on cell abundance and chl a) of the phytoplankton community was observed during the early phase of test (days 1 to 4) with high N/P ratio treatments and with low N/P ratio treatments during the late phase of test (after day 6). The H′ was most the sensitive among the diversity indices we used in the present study, and it decreased significantly in the low N/P ratio treatments on day 4 but increased in the low N/P ratio treatments on day 8 and day 12. On the other hand, a definite community succession order from diatoms (Skeletonema costatum) to dinoflagellates (Protoperidinium bipes and Prorocentrum donghaiense) was observed in all treatments. However, the proportion and occurrence time of the dominant species varied with different N/P treatments.
Based on survey data from the Bohai Sea of China in autumn (October) and winter (December) 2019, the structural characteristics of phytoplankton communities and their relationship with environmental factors were analysed. A total of 114 species of phytoplankton belonging to 84 genera and 3 phyla were identified. Warm-water species occurred frequently but cold-water species decreased in the Bohai Sea. This was associated with global warming and rising water temperatures. By comparing with historical data, Paralia sulcata gradually flourished and became the dominant species in autumn and winter, whereas the dominance of Skeletonema costatum decreased. The marine environment of the Bohai Sea has improved significantly in recent years, and phytoplankton biodiversity has increased. In autumn, both total phytoplankton and dinoflagellates were negatively correlated with salinity, and Pseudo-nitzschia delicatissima was positively correlated with nitrite and ammonia nitrogen. In winter, Nitzschia spp. showed a positive correlation with nitrate and a negative correlation with salinity.
The problem of aquatic invasive species caused by discharge of ballast water and sediments from ships’ ballast tanks has become extremely prominent. Seventeen sediment samples taken from ballast tanks of different ships docked in two Chinese shipyards were examined to identify the variety of resting dinoflagellate cysts. Twenty-two dinoflagellate cyst taxa were identified in these samples, including 11 photosynthetic and eleven heterotrophic species. These species represent 10 genera with the dominating assemblages of Alexandrium minutum, Scrippsiella acuminata, Lingulodinium polyedra, Protoperidinium sp. and Protoperidinium conicum. The total abundance of the dinoflagellate cysts ranged from 36 to 448 cysts g⁻¹ dry weight, which demonstrated a wide range of diversity for different ships. It was observed that the number of taxa and concentrations of cysts in ballast tank sediments were slightly greater for ships performing short voyage than ships performing longer voyage. The compositions of dinoflagellate cysts in sediments from ships sailing diverse routes were more variable than those sailing same routes. Sediment moisture content proved to be well correlated to the total cyst abundance (r = 0.7422, P < 0.01). Furthermore, nine toxic and harmful species were observed from all sediment samples, which indicated a wide range of distribution and potential risk of harmful algal blooms if being discharged to Chinese waters. As a result, full attention should be drawn to the studies on dinoflagellate cysts in the ballast tank sediments from ships arriving at China, this is of great significance for preventing introduction of toxic and harmful dinoflagellate cysts and protecting native marine biodiversity.
Red tide has always been an environmental issue with global concern. A Noctiluca scintillans red tide and a Mesodinium red tide occurred successively in Yantai nearshore, China, where is usually oligotrophic, in October 2019. Currents, phytoplankton community composition and nutrients were analyzed to access the driving factors of the red tides. The maximum N. scintillans and Mesodiniium abundance reached 124.92 ± 236.84 × 10³ cells/L and 1157.52 ± 1294.16 × 10³ cells/L respectively. The fast growth of N. scintillans was due to increasing abundance of phytoplankton. The currents were crucial to the assembly and dispersal of red tides. The red tides significantly redistributed the nutrients in the red tide patches and regulated the dominant species in phytoplankton community. Our study illuminates the influence of physical-biochemical coupling processes on red tides, and suggests that ocean dynamics such as currents and tidal factors deserve more attention when considering the ecosystem health problems of coastal zones.
To secure orderly and efficient production of fisheries products is one of the visions of the Agriculture, Fisheries and Conservation Department. The production of fisheries products relies on good water quality. The Aquaculture Environment Section is the team responsible for conducting regular water quality monitoring and also phytoplankton monitoring in fish culture zones.
Phytoplankton is the primary producers in aquatic food web. However, when there is a massive growth of toxic phytoplankton causing harmful algal bloom (HAB), some negative impacts may be created. Identification of toxic species is very important so that early warning can be issued to the mariculturists. It is also my major task in my career life in the Department.
The red-tide dinoflagellate Gonyaulax polygramma (GenBank accession number = AJ833631), previously known as an exclusively autotrophic dinoflagellate, has been found to be a mixotrophic species. We investigated feeding mechanisms, types of prey species, and the effects of prey concentration on the growth and ingestion rates of C. polygramma when feeding on an unidentified cryptophyte species (equivalent spherical diameter, ESD = 5.6 μm). We also calculated grazing coefficients by combining field data on abundances of G. polygramma and co-occurring cryptophytes with laboratory data on ingestion rates obtained in the present study. Among the phytoplankton prey offered, G. polygramma ingested small phytoplankton species with ESD ≤ 17 μm, but did not feed on large phytoplankton species with ESD > 22 μm. G. polygramma fed on prey cells by engulfing them through the apical horn, a previously unknown mechanism, as well as through the sulcus. The feeding mechanism of G. polygramma on phytoplankton mainly depended on the prey species. Specific growth rates of G. polygramma on a cryptophyte increased with increasing mean prey concentration, with saturation occurring at a mean prey concentration of approximately 600 ng C ml -1. The maximum specific (mixotrophic) growth rate of G. polygramma on a cryptophyte was 0.278 d-1, under a 14:10 h light:dark cycle of 50 μE m-2 s-1, while its (phototrophic) growth rate under the same light conditions without added prey was 0.186 d-1. Its maximum ingestion and clearance rates were 0.18 ng C grazer-1 d -1 (10.6 cells grazer-1 d-1) and 0.18 μl grazer-1 h-1, respectively. The grazing coefficients of G. polygramma on cryptophytes were up to 0.479 h-1. The results of the present study suggest that G. polygramma can have a considerable grazing impact on cryptophyte populations.
We documented the abundance of the heterotrophic dinoflagellate Oxyphysis oxytoxoides Kofoid along the Korean coast, cultured it (food source: the marine ciliate Myrionecta rubra Jankowski [= Mesodinium rubrum Lohmann]), sequenced its nuclear-encoded large-subunit (LSU) rDNA, and resolved its phylogenetic relationship within the Dinophysiales. Abundance was low, usually < 9.7 x 10(3) cells l(-1), in samples from 2005 and 2006. It co-occurred with the mixotrophic dinoflagellate Dinophysis acuminata, possibly indicating a common pool of prey. Growth on M. rubra reached a density of 38 x 10(5) cells l(-1). Observations on live cells from our established cultures revealed that O. oxytoxoides uses a peduncle to suck up the cell contents of M. rubra, the number of food vacuoles increasing as feeding proceeds. No regional variability was found in partial LSU rDNA sequences (domains D1-D2) of our strains, despite different sampling sites and dates. Phylogenetic analysis, based on LSU rDNA, showed that while Amphisolenia forms an early divergent basal group in the Dinophysiales, the other dinophysoids form 2 separate groups: (1) Oxyphysis and Phalacroma, and (2) Histioneis, Ornithocercus, Citharistes and Dinophysis. The presence of a peduncle in several genera, and the widespread distribution of pedunculate dinophysoids, indicate that these species may be fundamentally heterotrophic with a common feeding mechanism. Our results shed light on the feeding ecology and phylogenetic position of O. oxytoxoides.
Planktonic mixotrophic and heterotrophic dinoflagellates are ubiquitous protists and often abundant in marine environments. Recently many phototrophic dinoflagellate species have been revealed to be mixotrophic organisms and also it is suggested that most dinoflagellates may be mixotrophic or heterotrophic protists. The mixotrophic and heterotrophic dinoflagellates are able to feed on diverse prey items including bacteria, picoeukaryotes, nanoflagellates, diatoms, other dinoflagellates, heterotrophic protists, and metazoans due to their diverse feeding mechanisms. In turn they are ingested by many kinds of predators. Thus, the roles of the dinoflagellates in marine planktonic food webs are very diverse. The present paper reviewed the kind of prey which mixotrophic and heterotrophic dinoflagellates are able to feed on, feeding mechanisms, growth and ingestion rates of dinoflagellates, grazing impact by dinoflagellate predators on natural prey populations, predators on dinoflagellates, and red tides dominated by dinoflagellates. Based on this information, we suggested a new marine planktonic food web focusing on mixotrophic and heterotrophic dinoflagellates and provided an insight on the roles of dinoflagellates in the food web.
The food uptake mechanism and prey specificity of the most recently described member of the ichthyotoxic photosynthetic dinoflagellate genus Karlodinium (K. armiger) was studied. K. armiger extracts the contents of prey through an inconspicuous feeding tube (peduncle), but may also ingest whole prey cells. This species is omnivorous, ingesting prey from all major groups of marine protists. K armiger displays a searching pre-capture behavior with attraction to prey cells and formation of feeding aggregates. In batch cultures, growth rates in the light without food were low (0.01 to 0.10 d(-1)), but when the culture medium was enriched with soil extract, initial growth rate increased (0.19 d(-1)); it further increased (0.60 d(-1)) when fed the cryptophyte Rhodomonas marina in the light (170 mu mol photons m(2) s(-1)). R. marina was also ingested in the dark, but did not support positive growth rates and survival. Thus, K armiger is an omnivorous obligate phototrophic mixotroph which seems to obtain a growth-essential substance or growth factor through phagotrophy.
Laboratory experiments were performed to determine the growth and grazing capabilities of 2 heterotrophic dinoflagellates with different feeding modes (pallium feeder: Oblea rotunda; engulfment feeder Oxyrrhis marina) when fed the raphidophyte Fibrocapsa japonica, Both dinoflagellates readily ingested prey and exhibited positive growth when feeding on monocultures of F japonica. Maximum growth rates at food saturation were 0.54 and 0.72 d(-1) for O. rotunda and O, marina, respectively. Both dinoflagellates are thus able to grow faster than their prey, for which a maximum growth rate of 0.45 d(-1) has been previously reported. In the case of O. rotunda, it was found that a rather high food concentration of 300 F japonica cells ml(-1) (corresponding to 142 mug C l(-1)) was needed to sustain half-saturated growth. This is consistent with the quantification of behavioural aspects of the feeding process, In about 55% of cases, a failure to attach the tow filament after prey encounter was recorded, and in about 83% of cases, F. japonica was able to escape from the attached tow filament, indicating that motility of F. japonica is a quite effective defence mechanism against pallium-feeding dinoflagellates. In addition, qualitative observations suggest that trichocysts of F japonica may act mechanically as a grazer deterrent.
We investigated the feeding by 18 red-tide dinoflagellate species on the cyanobacterium Synechococcus sp. We also calculated grazing coefficients by combining the field data on abundances of the dinoflagellates Prorocentrum donghaiense and P. micans and co-occurring Synechococcus spp. with laboratory data on ingestion rates obtained in the present study. All 17 cultured red-tide dinoflagellates tested (Akashiwo sanguinea, Alexandrium catenella, A. minutum, A. tamarense, Cochlodinium polykrikoides, Gonyaulax polygramma, G. spinifera, Gymnodinium catenatum, G, impudicum, Heterocapsa rotundata, H. triquetra, Karenia brevis, Lingulodinium polyedrum, Prorocentrum donghaiense, P. minimum, P. micans, and Scrippsiella trochoidea) were able to ingest Synechococcus. Also, Synechococcus cells were observed inside the protoplasms of P, triestinum cells collected from the coastal waters off Shiwha, western Korea, during red tides dominated by the dinoflagellate in July 2005. When prey concentrations were 1.1 to 2.3 x 10(6) cells ml(-1), the ingestion rates of these cultured red-tide dinoflagellates on Synechococcus sp. (1.0 to 64.2 cells dinoflagellate(-1) h(-1)) generally increased with increasing size of the dinoflagellate predators (equivalent spherical diameters = 5.2 to 38.2 mu m). The ingestion rates of P. donghaiense and P. micans on Synechococcus sp. increased with increasing mean prey concentration, with saturation occurring at a mean prey concentration of approximately 1.1 to 1.4 x 10(6) cells ml(-1). The maximum ingestion and clearance rates of P. micans on Synechococcus sp. (38.2 cells dinoflagellate(-1) h(-1) and 4.3 mu l dinoflagellate(-1) h(-1)) were much higher than those of P. donghaiense on the same prey species (7.7 cells dinoflagellate(-1) h(-1) and 2.6 mu l dinoflagellate(-1) h(-1)). The ingestion rates of red-tide dinoflagellates on Synechococcus sp. were comparable to those of the heterotrophic nanoflagellates and ciliates on Synechococcus spp., so far reported in the literature. The calculated grazing coefficients attributable to small Prorocentrum spp. (R donghaiense + P. minimum) and P. micans on co-occurring Synechococcus spp. were up to 3.6 and 0.15 h(-1), respectively. The results of the present study suggest that red-tide dinoflagellates potentially have a considerable grazing impact on populations of Synechococcus.
The heterotrophic dinoflagellate Protopemdin-ium cf. divergens, known as prey for adult copepods, itself feeds on copepod eggs and early naupliar stages. One to several P. cf. divergens can attack an egg or nauplius larger than themselves. The time for an egg to be digested was proportional to the number of P. cf. divergens attacking it. Ingestion rates of P, cf. djvergens on Acartia tonsa eggs and on 100 pm diameter unidentified eggs with a smooth surface increased linearly with increasing mean prey concentration. Estimated daily consumption of eggs by P. cf. dlvergens suggests that it may sometimes have a considerable predation impact on the populations of copepod eggs. This predation may change the general concept of energy and cycling of carbon in the plank-tonic community because the genus Protoperidinium and copepods are often amongst the most abundant micro-and macrozooplankton.
The quantiative importance and trophic role of heterotrophic dinoflagellates was studied at a permanent station in the Kattegat, Denmark. Heterotrophic dinoflagellates were most abundant during periods characterized by large phytoplankton forms (e.g. diatoms and dinoflagellates). During these periods the heterotrophic dinoflagellate biomass corresponded to between 13 and 77 % of the phytoplankton biomass. Large forms (> 20-mu-m) dominated the heterotrophic dinoflagellate biomass, but smaller forms were important during periods dominated by nanoplankton. Observations on the feeding mechanisms of the most abundant heterotrophic dinoflagellates revealed species which engulf prey directly as well as species which feed with a peduncle and a pallium - mechanisms which all allow the ingestion of large prey. The succession of heterotrophic dinoflagellates is also discussed in relation to the distribution of potential competitors and predators.
Heterotrophic members of the marine plankton dinoflagellate genus Dinophysis are specialized predators, whose food includes the prostomatid ciliate Tiarina fusus. This ciliate differs from most planktonic ciliates in its ability to ingest prey of its own size including autotrophic Dinophysis spp. However, when trying to catch a heterotrophic Dinophy- sis sp., the ciliate is trapped instead by the dinoflagellate and emptied via a feeding tube (peduncle), which originates from the flagellar pore of the dinoflagellate. The specific predation on a ciliate by a heterotrophic dinoflagellate represents a new trophic link in the marine planktonic food web. The existence of colourl.ess thecate dinoflagellates in the marine pelagial has been recognized among taxo- nomists for more than a century (Gaines & Elbrachter 1987). In spite of this, few ecological studies dealing with the marine planktonic food webs have included them in the protozoan plankton even though they may make up a substantial part of the biomass of this group (Smetacek 1981). Knowledge about their trophic role in the marine pelagial has simply been too poor. Recent studies have revealed that a number of colourless thecate species belonging to the genera Protoperidinium, Oblea and Zygabikodinium are able to feed on large diatoms and dinoflagellates by a pseudopodium, a 'feeding veil' or a 'pallium', which encloses the prey (Gaines & Taylor 1984, Jacobson & Anderson 1986). The species studied so far all belong to the order Peridinales. The purpose of this work has been to study the trophic role and feeding mechanism of colourless species belonging to the order Dinophysiales. Materials and Methods. Samples of surface water were collected from a permanent station in the southern part of Kattegat (56' 15.42E, 12' 00.12N), Denmark, during 1989. The plankton was concentrated (net mesh size 20 pm) and incubated in 65 m1 tissue culture flasks
The thecate heterotrophic dinoflagellate Protoperidinium cf. divergens and the thecate mixotrophic dinoflagellate Fragilidium cf. mexicanum feed on each other. In general, F. cf. mexicanum is the predominant predator in this reciprocal predation. At initial concentration ratios less than or equal to 0.4 (F. cf, mexicanum: P. cf. divergens), both species fed on each other, but did not seriously affect the other's population. At ratios greater than or equal to 0.8, P. cf. divergens was drastically reduced to very low concentrations, and active predation by F. cf. mexicanum on P. cf, divergens was observed. This reciprocal predation may affect our view of energy and cycling of carbon in the planktonic community.
2 Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen, 12, 27570 Bremerhaven, Germany
In order to experimentally investigate feeding by mixotrophic dinoflagellates, we developed protocols for the use of live protistan prey as markers of ingestion. CMFDA (5-chloromethyl-fluorescein diacetate), a vital green fluorescent stain, was used to label cultures of photosynthetic nanoflagellates, a diatom, and an oligotrichous ciliate. Cryptophytes were not readily stained with CMFDA, but phycoerythrin-containing members of this phylum have a distinct yellow-orange fluorescence and thus can be used unstained to demonstrate ingestion. With these complementary techniques, we qualitatively demonstrated feeding by the dinoflagellates Ceratium furca, Gymnodinium sanguineum, Gyrodinium estuariale, Prorocentrum minimum (= mariae-lebouriae) and Peridinium brevipes in natural assemblages from Chesapeake Bay, USA. We also used CMFDA-stained Isochrysis galbana (Prymnesiophyta) and unstained Cryptomonas sp. (Cryptophyta) in laboratory and field studies, respectively, to examine prevalence of feeding by G. estuariale as a function of prey density. However, determination of in situ grazing rates for mixotrophic dinoflagellates proved difficult, as only a small percentage of cells contained labeled food vacuoles following short incubations (less than or equal to 4 h) with stained prey added at tracer concentrations. The use oi CMFDA-stained cells and phycoerythrin-containing prey as markers of ingestion should also be applicable to species-specific feeding studies with other phagotrophic protists and micro-metazoa. The protocols presented here have advantages over the use of fluorescent microspheres or fluorescently labeled heat-killed algae (FLA) for investigating grazing or predation because many micrograzers do not readily ingest, or discriminate against, inert particles.
Protoperidinium pellucidum is a pallium feeding heterotrophic dinoflagellate that captures phytoplankton cells individually and digests them externally. In laboratory cultures, P, pellucidum feeds on a variety of diatom species and a limited number of dinoflagellate species, and grows more rapidly on diatoms than dinoflagellates. When offered food in mixed assemblages, it feeds selectively on diatoms over dinoflagellates, and selects between diatom species. Selectivity between different diatom species does not appear to be related to size, and size alone does not explain the low selectivity for dinoflagellates. Computerized motion analysis studies of swimming behavior reveal that P, pellucidum appears to use chemoreception as the major sensory mode to detect and locate food. When P. pellucidum passes near a food cell it circles around the cell several times before attaching to the food particle, apparently using chemoreception to judge the location of the cell. Detailed behavioral observations reveal that P, pellucidum sometimes loses contact with motile dinoflagellate cells before the capture occurs; such losses were not observed with diatoms. In addition, motile dinoflagellate prey often escape after initial capture, their swimming behavior causing the capture filament to break before the cell can be engulfed by the pallium of P, pellucidum; loss of a diatom after attachment was extremely rare. Feeding selectivity may be explained in part by the nature of the chemosensory signals given off by different prey types, and therefore the distance at which P. pellucidum can detect food, and in part by the lower capture success of P. pellucidum with motile prey.
A Crypthecodinium cohnii-like dinoflagellate was found to prey on the unicellular red alga Porphyridium sp. The cytoplasm of the prey is ingested by myzocytosis within 10–30 s, and the contents of up to 20 Porphyridium cells can be taken up by one dinoflagellate. The feeding tube is retracted after each uptake process. Cytochalasin D disturbs the suction and the retraction of the feeding tube. Feeding behaviour depends on the light–dark regime: the dinoflagellates prey preferentially in the dark period and finish the trophic phase at the beginning of the light period. They then assemble and encyst, and digestion takes place in the light period. Cell division is restricted to the encysted stage. At the end of the light period excystment takes place, combined with defecation. Isogamy as well as anisogamy and nuclear cyclosis were observed. The trophonts have very thin thecal plates and a microtubular basket with two kinds of elongate vesicles. The microtubules of the tubular basket are also found in young cysts, formed after the end of the feeding period. The fine structure of the digestion vacuoles and of the faecal bodies is described.
Protoperidinium vorax sp. nov. is a small heterotrophic dinoflagellate with a plate formula of Po, X, 4′, 3a, 7′′, 3C, 5S, 5′′′, 0p, 2′′′′. P. vorax has an ortho-hexa thecal plate arrangement. Its peculiar features are the presence of only three cingular plates and the marked extension of the second intercalary plate (2a), which abuts the second precingular plate (2′′). TEM sections revealed the presence of a large sac pusule, several convoluted vesicular structures and electron-dense accumulation bodies scattered in the cell periphery. These accumulation bodies probably represent the Periodic Acid-Schiff (PAS) bodies, which fluoresce yellow–green under blue light excitation. P. vorax is a pallium feeder and was observed feeding on diatoms of different sizes. When fed with the chain-forming diatom Skeletonema pseudocostatum under non-limiting food concentrations, doubling rates up to 1.28 divisions d−1 were recorded. Ingestion rates of 35.95 cells dinoflagellate−1 h−1 and clearance rates of 18.34 µl dinoflagellate−1 h−1 were reached, the highest ever recorded for a small-sized dinoflagellate. These data support the hypothesis that small heterotrophic species might contribute to diatom bloom decay.
Gymnodinium acidotum, a blue-green dinoflagellate which contains cryptophycean chloroplasts and other organelles, was observed. The dinoflagellate excysts as a mononucleated colorless cell that is positively phototactic. Colorless cells in unialgal culture remain colorless and can only be maintained less than one week whereas pigmented cells cultured unialgally grow for 10 days but then decline rapidly. Colorless cells cultured with Chroomonas spp. regain chloroplasts and have been maintained in mixed cultures for nine months. -from Authors
The general ultrastructure of A. poecilochroum is typical of dinoflagellates. The proximal part of the longitudinal flagellum possesses a previously undescribed structure consisting of three dense rods running alongside, and attached to, the axoneme. Hexagonal vesicles containing crystalline rods are found regularly in the cell.
Dinophysis acuminata C1aparède et Lachmann and Dinophysis norvegica Ehrenberg (two toxic species responsible for diarrhoeic shellfish poisoning) from West Boothbay Harbor were both found to contain food vacuoles. Cells with food vacuoles constituted up to 6 and 36% of the D. norvegica and D. acuminata populations respectively. Food vacuoles were detected whenever these species were present except for a period in August/September when they were missing from the D. norvegica population. Cells containing food vacuoles were filledwith transparent globules, matching the appearance of two related, heterotrophic species which feed upon ciliates, Dinophysis rotundata Claparède et Lachmann and Oxyphysis oxytoxoides Kofoid. Cells were often megacytic and displayed a more intense orange-red plastidic pigmentation than did cells lacking food vacuoles, although no food vacuoles themselves were red. Feeding behaviour in D. acuminata and D. norvegica was not seen.
The ultrastructure of food vacuoles was examined in all four species. Food vacuoles in D. acuminata contained membranous vesicles, lipid-like globules, cylindrical ejectile-like organelles, abundant paracrystalline vesicles and, in three cells, abundant concave starch-like grains. The food vacuoles of D. norvegica match those of some D. acuminata cells. In D. rotundata food vacuoles contained plastids (of the simple type with internal pyrenoid) and rare prasinophyte scales. Some O. oxytoxoides food vacuoles resembled certain D. acuminata food vacuoles. Others contained well-preserved trichocysts, virus particles and (in one instance) prasinophyte scales. Details of D. acuminata food vacuoles, including the high density of starch-like grains, the characteristic extrusomes, the paracrystalline vesicles and the close resemblance of some of these food vacuoles to those of O. oxytoxoides, suggest that D. acuminata preys upon ciliates.
The ultrastructure of food vacuoles was examined in all four species. Food vacuoles in D. acuminata contained membranous vesicles, lipid-like globules, cylindrical ejectile-like organelles, abundant paracrystalline vesicles and, in three cells, abundant concave starch-like grains. The food vacuoles of D. norvegica match those of some D. acuminata cells. In D. rotundata food vacuoles contained plastids (of the simple type with internal pyrenoid) and rare prasinophyte scales. Some O. oxytoxoides food vacuoles resembled certain D. acuminata food vacuoles. Others contained well-preserved trichocysts, virus particles and (in one instance) prasinophyte scales. Details of D. acuminata food vacuoles, including the high density of starch-like grains, the characteristic extrusomes, the paracrystalline vesicles and the close resemblance of some of these food vacuoles to those of O. oxytoxoides, suggest that D. acuminata preys upon ciliates.
Chloroplasts of the diatom, Streptotheca thamesis, are considerably deformed when they pass the feeding tube of the parasitic dinoflagellate, Paulsenella sp. Nevertheless, chloroplasts resume their normal shape and structure inside the food vacuole. Even the chloroplast ER is partially preserved. The feeding tube channel of Paulsenella chaetoceratis is narrow (about 0.2 μm in diameter) and may be very long (generally 100 μm). The feeding tube invades a seta of Chaetoceros decipiens through the apical or a lateral aperture and elongates until reaching the cell body of the host. The host chloroplasts are ruptured when they pass the feeding tube. However, large stacks of thylakoids remain intact. Stability of diatom chloroplasts and thylakoid stacks may be important in plankton research, e.g. using chlorophyll determinations as a measure for biomass production.
The dinoflagellate Gymnodinium 'gracilentum' feeds on the cryptophyte Rhodomonas salina and retains the chloroplasts of the prey as functional kleptochloroplasts. Using kleptochloro- plasts, G. 'gracilentum' becomes a mixotroph, acquiring a proportion of its organic carbon demand through photosynthesis, but the kleptochloroplasts and their photosynthetic activity are lost within a few days. Photosynthesis seems, primarily, to be an important means of nutrition for G. 'gracilentum' during food depletion, thereby enhancing the survival of the species during food limitation and starva- tion. However, light has a positive effect on growth kinetics of G. 'gracilentum' in food replete cultures: growth and ingestion rates are higher at a high light intensity than at a low light intensity. This effect may be due to other factors than photosynthetic activity of kleptochloroplasts, since a control experi- ment with a supposed strictly heterotrophic dinoflagellate, Gymnodinium sp., also showed a depen- dence of growth kinetics on light intensity.
Summary The pusule system ofGymnodinium spec. consists of tubes formed by the invaginated plasmalemma which is ornamented with delicate ribs on its luminal surface and tightly surrounded by a special, perforated cisterna. The degeneration of the pusule, the fine structure of the theca with some peculiar structures (trichocyst-like vacuoles, collared pits, the developing cyst wall), the stigma and its connection with the flagellar base, and the Golgi apparatus with different types of vesicles are described.
A bloom-forming dinoflagellate was isolated from coastal waters in western Korea during a red tide event in March 2008 and clonal cultures were established. The dinoflagellate was identified as Gymnodinium aureolum based on morphological and genetic analyses (GenBank accession no. FN392226). We report here for the first time that the red-tide dinoflagellate G. aureolum, which has previously been thought to be exclusively autotrophic, is a mixotrophic species. G. aureolum fed on algal prey using a peduncle. Among the algal prey provided, G. aureolum ingested heterotrophic bacteria, the cyanobacterium Synechococcus sp., and small algal species that had equivalent spherical diameters (ESDs) of <= 11.5 mu m. However, it did not feed on larger algal species (ESD >= 12 mu m) or the small diatom Skeletonema costa turn. The specific growth rates for G. aureolum on the cryptophyte Teleaulax sp. increased continuously with increasing mean prey concentration before saturating at prey concentrations of ca. 190 ng C ml(-1) (11 050 cells ml(-1)). The maximum specific growth rate (mixotrophic growth) of G. aureolum on Teleaulax sp. was 0.169 d(-1), at 20 degrees C under a 14:10 h light:dark cycle of 20 mu E m(-2) S(-1), while its growth rate (phototrophic growth) under the same light conditions without added prey was 0.120 d(-1). The maximum ingestion and clearance rates of G. aureolum on Teleaulax sp. were 0.058 ng C grazer(-1) d(-1) (3.4 cells grazer(-1) d(-1)) and 0.003 mu l grazer(-1) h(-1), respectively. The calculated in situ grazing coefficient for G. aureolum on co-occurring cryptophytes ranged up to 0.498 d(-1). Bioassay results indicated that this strain of G. aureolum is not toxic. Results of the present study suggest that G. aureolum has a potentially considerable grazing impact on algal populations.
The thecate heterotrophic dinoflagellate Diplopsalis lenticula Bergh was shown to feed on a wide range of phytoplankton of different size and taxonomic groups. Growth and ingestion rates of D. lenticula feeding on the diatom Ditylum brightwellii (West) Grunow were measured as a function of food concentration. Growth rate increased with food concentration until it reached saturation at c. 300 D. brightwellii cells ml-1. Maximum specific growth rate was 0.25 d-1 at a food concentration of 500 cells ml-1. A prey concentration as low as 30 cells ml-1 supported growth. Ingestion and clearance rates were estimated by two different methods based on estimates of prey loss rate and on counts of digested food particles. Ingestion rate increased with increasing food concentration up to a maximum rate of 1 or 0.2 prey dinoflagellate-1 h-1, depending on which of the two methods of estimation was used. Clearance rate decreased with increasing prey concentration. Maximum clearance rates at low food concentration were 2.7 and 1.2 μl dinoflagellate-1 h-1, corresponding to volume-specific clearance rates of 1.5 x 105 and 6.4 x 104 h-1, respectively.
The marine thecate dinoflagellate Fragilidium subglobosum (von Stosch) Loeblich (= Helgolandinium subglobosum von Stosch), previously believed to be an obligate phototroph, is shown to be mixotrophic, apparently feeding exclusively on Ceratium spp. Food uptake involves neither a pallium nor a peduncle but depends on direct engulfment. The amphiesma of F. subglobosum possesses bodies which might be involved in the initial digestion of the prey's theca and perhaps also in the capture of the prey. Ceratium cells are ingested within 5-15 min, depending on their size. The prey theca is gradually dissolved during engulfment, but the theca of F. subglobosum remains intact until engulfment is completed, although the feeding cell is able to increase its volume approximately threefold during the process. This is possible because the individual thecal plates detach from one another making the theca more flexible.
Peridiniopsis berolinensis (Lemmermann) Bourrelly (Peridiniales, Dinophyceae) is attracted to injured or dying protists (including other dinoflagellates and cells of its own kind) and small metazoans. Punctured nematodes were used for experimental induction of feeding. Peridiniopsis berolinensis uses a filament to establish connection with potential food items and ingests their fluid contents through a feeding tube protruded from the mid-ventral region of the cell. Food items small enough to pass through the tube can be ingested whole. The feeding tube is supported by c. 20 rows of microtubules, and is lined by a single membrane, continuous with the plasma membrane and with the membrane of the forming food vacuole. The tube and the longitudinal flagellum pass through a sulcal cavity lined by amphiesmal plates that shows an unusual fibrous connection between the edge of a plate and the middle of another. Suction seems to be involved in food uptake, and it is proposed that the driving force is mechanical generation of lower pressure inside the food vacuole. This idea is supported by morphological changes in the episoma of pre-feeding cells. The membrane of the feeding tube was not seen to establish an intimate association with the plasma membrane of prey organisms and, therefore, use of the term myzocytosis in connection with the feeding mechanism of P. berolinensis is discouraged.
Feeding of a naked photosynthetic dinoflagellate, Gyrodinium instriatum, on loricated ciliates was investigated. Gyrodinium instriatum preyed on Favella azorica and Eutintinnus tubulosus by engulfment through the posterior end of the sulcus. In the case of E.tubulosus, G.instriatum preyed on this small ciliate keeping the original gymnodinioid cell shape. On the other hand, G.instriatum preyed on Favella taraikaensis by absorbing the cell contents of this large ciliate, which resulted in a balloon-like inflation of its body size. It seemed that G.instriatum can change its feeding style according to the size of prey. Thus, the present study shows, by using direct observations on the feeding of G.instriatum on loricated ciliates, a reversal of energy flow processes in the food chain in which photosynthetic organisms eat primary consumers. The growth of G.instriatum after feeding on E.taraikaensis and E.tubulosus is also described briefly.
Summary Motile dinospores ofPaulsenella attach to a host diatom frustule, form a feeding tube, drive it between epi- and hypocingulum, pierce the host plasmalemma and suck up host cytoplasm gradually. This mode of endocytosis (“myzocytosis”) implies that the host plasmalemma is not ingested and that the host cytoplasm within the food vacuole is bounded only by the vacuolar membrane. The feeding tube is formed by the emergence of a preformed “microtubular basket” consisting of plates of microtubules. At its entrance into the cell body the feeding tube channel is surrounded by an electron-dense ring. Similar “sphincters” enclose the two exits through which the two flagella emerge. These sphincters are composed of microfibrils which reveal a cross striation when the fixative does not contain calcium ions. The flagellar bases as well as the internal part of the feeding tube are surrounded by a common cavity which is in open connection also with the ampullae of the pusule. The light and electron microscopical observations do not support the assumption that food uptake is driven by a flow of the membrane of the feeding tube channel caused by an interaction with the microtubular basket (as postulated for food uptake inSuctoria) but rather by an hydrostatic gradient which might be caused by rhythmical ion pumping and be based on the existence of the common cavity and the sphincters. Myzocytosis is inhibited by cytochalasin B.—The fine structure of dinospores and trophonts, especially with respect to the cell covering, the amphiesma, and the en- and excystment, is described.
Algae were either heat-killed and labelled with 5-(4,6-dichlorotriazin-2-yl amino fluorescein) (DTAF) or stained with hydroethidine (HYD). Both DTAF and HYD-stained algae were readily visible within the digestive vacuoles of most microzooplankton collected in estuarine and coastal waters of Massachusetts, but DTAF was ineffective at staining several chromophytic algae and the heat-kill process reduced cell volume by ≥50% in several of the algae which were effectively stained. HYD effectively stained all algae tested except chlorophytes. -from Author
Individuals of the common coastal marine dinoflageilate genus Protoperidinium have been found to perform extracellular digestion of chain-forming diatoms by means of a pseudopodial ‘feeding veil’. This
mechanism of feeding explains the absence of food particles in these non-photosynthetic, thecate organisms, and seems to be
an adaptation for opportunistic feeding
Several papers give brief accounts of unarmored Dinophyceae found along the eastern coast of the United States. Calkins (1902) described from Woods Hole three European species, with one as a new variety. Herdman (1924a) listed five European, sand-living species from Woods Hole. Lackey (1936) listed thirteen species, all European, in his account of Woods Hole protozoa. Martin (1929) described thirteen species, four of which were new, from Barnegat Bay. It would be expected that further study would show many more extensions of range from the east to the west side of the Atlantic. One wonders, though, whether new species would be few, as suggested by these figures, or on the contrary would be many, since studies hitherto have not been very detailed. Further, the Barnegat Bay list suggests that the shallow, estuarine type of habitat has as many species as coastal waters, since Martin's number is matched only by that of Lackey. The following study covers twenty-six species, of which twelve are completely
Although Oblea can feed and grow on a wide range of phytoplankton species, the highest observed growth rates (c1 doubling d-1) were supported by the large diatom Ditylum brightwellii. Functional and numerical responses curves, obtained with the green alga Dunaliella tertiolecta and D. brightwellii as foods, were typical in form of those obtained previously for other planktonic protozoans. Ditylum, however, consistently supported higher rates of growth and grazing than Dunaliella. Gross growth efficiencies for Oblea were relatively high. A chemosensory response to phytotoplankton exudates was observed during motion analysis of swimming behaviour. -from Authors
Phytoplankton populations near Igloolik, northern Foxe Basin, began to increase in late April, and reached their climax in mid-August. The rapid late-August decline of the phytoplankton populations coincided with diminishing light. Diatoms were the main biomass producers in Igloolik and the principal food for the marine fauna. The succession of spring Pennatae and summer Centriceae apparently was caused by light and ice conditions. Taxonomic composition of the Igloolik phytoplankton was influenced by the fast ice and by the shallowness and hydrographic uniformity of the adjacent areas. Descriptions are given of two new species of dinoflagellates, Gyrodinium arcticum and Gymnodinium intercalaris, and the new coccolithine flagellate Pontospkaera ditrematolitha.
A small, freshwater dinoflagellate with an incomplete cingulum, identified as Esoptrodinium gemma Javornický (=Bernardinium bernardinense sensu auctt. non sensu Chodat), was maintained in mixed culture and examined using light and serial section TEM. Vegetative flagellate cells, large cells with two longitudinal flagella (planozygotes), and cysts were examined. The cells displayed a red eyespot near the base of the longitudinal flagellum, made of two or three layers of pigment globules not bounded by a membrane. Yellow-green, band-shaped chloroplasts, bounded by three membranes and containing lamella with three thylakoids, were present in both flagellate cells and cysts. Most cells had food vacuoles, containing phagotrophically ingested chlamydomonads or chlorelloid green algae; ingestion occurred through the ventral area, involving a thin pseudopod apparently driven by the peduncle. The pusule was tubular, with numerous diverticula in its distal portion, and opened into the longitudinal flagellar canal. Three roots were associated with each pair of flagellar bases, both in vegetative cells and in a planozygote. The longitudinal microtubular root bifurcated around the longitudinal basal body. The planozygote contained a single peduncle and associated structures, and a single transverse flagellar canal with the two converging transverse flagella. Using two ciliates as outgroup species, phylogenetic analyses based on maximum parsimony, neighbor-joining and posterior probability (Bayesian analysis) supported a clade comprising Esoptrodinium, Tovellia, and Jadwigia.