Field obServationS on rare or overlooKed

dinoFlagellateS From the argentine Sea

obServaCioneS de CamPo Sobre dinoFlageladoS raroS o

deSConoCidoS en el mar argentino

1,2

Elena Fabro * & Gastón O. Almandoz

Summary

Background and aims: Planktonic dinoﬂagellates have a great ecological signiﬁcance

in marine environments. While some dinoﬂagellate species commonly reach bloom

concentrations and are thus conspicuous components of marine phytoplankton, others

occur in very low abundances which make them diﬃcult to detect in ﬁeld studies.

Here we analyzed dinoﬂagellate composition and abundance in ﬁve oceanographic

expeditions carried out in continental shelf and slope waters of the Argentine Sea.

M&M: Plankton abundance was estimated by the Utermöhl method, using inverted

microscopy, whereas further optical and scanning electron microscopy was applied for

the identiﬁcation of dinoﬂagellate species.

1

. División Ficología, Facultad

de Ciencias Naturales y Museo,

Universidad Nacional de La Plata.

Paseo del Bosque s/n (B1900FWA),

La Plata, Argentina.

2

.

Consejo Nacional de

Investigaciones Científicas

Técnicas (CONICET). Godoy Cruz

290 (C1425FQB), Buenos Aires,

Argentina.

y

2

Results: We focused on the occurrence of seven dinoﬂagellates that have been

previously poorly documented or overlooked in marine environments worldwide:

Dinophysis microstrigiliformis; Gyrodinium sp.; Karlodinium elegans; Oxytoxum

laticeps; Peridiniella danica; Peridiniella globosa and Prorocentrum nux. The latest

and K. elegans are observed for the ﬁrst time in ﬁeld conditions after their original

descriptions based on cell cultures. While most species were detected in low or

moderate abundances, P. nux, which is the smallest Prorocentrum species, reached

*fabroelena@yahoo.com.ar

Citar este artículo

FABRO, E. & G. O. ALMANDOZ.

021. Field observations on rare

2

-1

2,000 cells L in slope waters. Very small Gyrodinium cells (11.5 µm long; 8.7 µm

8

or overlooked dinoflagellates from

the Argentine Sea. Bol. Soc. Argent.

Bot. 56: 123-140.

wide) with a distribution restricted to slope waters during spring, were not possible to

be accurately assigned to a species.

Conclusions: This study contributes to the understanding of dinoﬂagellate diversity in

the Argentine Sea and the worldwide distribution of little known species.

DOI: https://doi.

org/10.31055/1851.2372.v56.

n2.31421

Key WordS

Biogeography, dinoﬂagellates, diversity, Karlodinium elegans, Prorocentrum nux, South

Atlantic Ocean.

reSumen

Introducción y objetivos: Los dinoﬂagelados planctónicos son de gran relevancia en

los ecosistemas marinos. Mientras que algunas especies suelen forman ﬂoraciones

y ser componentes conspicuos del ﬁtoplancton, otras se encuentran en abundancias

muy bajas, lo cual hace difícil su detección. Aquí analizamos la composición y

abundancia de dinoﬂagelados en cinco expediciones oceanográﬁcas realizadas en

aguas de la plataforma continental y del talud del Mar Argentino.

M&M: La abundancia se estimó con microscopio invertido (método Utermöhl) y se utilizó

microscopía óptica y electrónica de barrido para la identiﬁcación especíﬁca.

Resultados: Nos enfocamos en la ocurrencia de siete dinoﬂagelados que previamente

han sido poco documentados en ambientes marinos de todo el mundo: Dinophysis

microstrigiliformis; Gyrodinium sp.; Karlodinium elegans; Oxytoxum laticeps;

Peridiniella danica; Peridiniella globosa y Prorocentrum nux. Esta última especie y K.

elegans se observan por primera vez en el campo desde su descripción basada en

cultivos celulares. Si bien la mayoría de las especies se detectaron en abundancias

bajas o moderadas, P. nux, el Prorocentrum más pequeño, alcanzó 82.000 células

-1

L en aguas del talud. Células pequeñas de Gyrodinium sp. (11,5 µm de largo y 8,7

µm de ancho), con un una distribución restringida a las aguas del talud durante la

primavera, no pudieron ser asignadas con precisión a nivel especíﬁco.

Conclusiones:Esteestudiocontribuyealconocimientodeladiversidaddedinoﬂagelados

en el Mar Argentino y la distribución mundial de especies poco conocidas.

Recibido: 15 Dic 2020

Aceptado: 17 May 2021

Publicado impreso: 30 Jun 2021

Editora: Sylvia Bonilla

PalabraS Clave

ISSN versión impresa 0373-580X

ISSN versión on-line 1851-2372

Biogeografía, dinoﬂagelados, diversidad, Karlodinium elegans, Océano Atlántico Sur,

Prorocentrum nux.

123

Bol. Soc. Argent. Bot. 56 (2) 2021

introduCtion

2016) suggest that dinoﬂagellate diversity in the

Argentine Sea is higher than previously known.

While some dinoﬂagellate species commonly

Planktonic microalgae comprise an essential

biotic component of the world oceans. Among reach bloom concentrations and are thus

microalgae, dinoﬂagellates are of great ecological conspicuous components of marine phytoplankton,

significance as they contribute to primary others occur in very low abundances which make

production and are determinant in trophic webs, them diﬃcult to detect in ﬁeld studies (Steidinger &

representing a strong inﬂuence in biogeochemical Tangen, 1997). Within this low-abundance species,

cycles and biotic interactions (Graham & Wilcox, small thecate and unarmored dinoﬂagellates are

2

000). Moreover, dinoflagellates include the less studied in ﬁeld conditions, as most of the

largest number of toxigenic species among marine research is directed to bigger armoured species

phytoplankton, which can produce harmful blooms with easily preserved morphological features (De

with negative impacts to human health and marine Salas et al., 2008). In order to increase knowledge

life and generate economic losses to ﬁsheries, on dinoﬂagellate diversity in the Argentine Sea,

aquaculture and exploitation of natural mussel’s we focused on the occurrence of small and rare

beds (Lassus et al., 2016).

dinoﬂagellates previously overlooked or poorly

Dinoflagellates are ubiquitous in marine documented, by the analysis of plankton samples

environments; comprising heterotrophic, obtained in five oceanographic expeditions in

autotrophic and mixotrophic species and also different seasons. Based on detailed light and

ecto- and endoparasitic species and symbionts electron microscopy observations, we found cells

(Hackett et al., 2004). According to the presence or of seven dinoﬂagellates that are poorly documented

absence of cellulose inside the amphiesmal vesicles or found for the ﬁrst time in the Southeast Atlantic

they are divided in two big groups: thecate and Ocean and have also been rarely mentioned from

unarmored dinoﬂagellates. Within the thecate group marine environments worldwide. For each taxa we

taxonomical classiﬁcation is based on the number, provide a detailed morphological characterization

position and shape of the thecal plates, while in the and describe their distribution patterns, compared

unarmored group cellular shape, ultra-structural with previous observations.

characters of the ﬂagellar apparatus and shape of

the apical groove are usually used to diﬀerentiate

genera (Daugbjerg et al., 2000). With the advent of materialS and methodS

molecular technics in the last decades, phylogeny

and morphological traits for classification of Field Sampling

some unarmored dinoﬂagellates were reconsidered

Daugbjerg et al., 2000).

The continental shelf and slope waters of

the Argentine Sea were sampled during five

(

An important contribution to knowledge about oceanographic expeditions (Fig. 1). Expedition 1

the diversity and distribution of dinoﬂagellates, not (E1) was conducted in austral autumn on board

only in the SouthAtlantic Ocean but also worldwide, the R/V Puerto Deseado from March 30th to April

comes from the copious work done by E. Balech 14th, 2012. A total of 47 stations were sampled

(e.g. Balech, 1976, 1988, 1995, 2002). More recent between ≈38 and 56 ºS. The second expedition

studies have continued this line of research in the (E2) was carried out in late austral summer on

Argentine Sea, mainly covering coastal areas or the R/V Bernardo Houssay from March 11th to

toxigenic species (e.g. Akselman 1985, 1986, 1987; March 22nd, 2013, with 24 sampling stations

Akselman & Negri, 2012; Akselman et al., 2015; located between ≈39 and 43 ºS. This cruise was

Fabro et al., 2015; Antacli et al., 2018; Tillmann divided in two legs K1 and K2, which comprise 8

et al., 2019; Sunesen et al., 2020a). However, the and 16 sampling stations, respectively. The third

recent description of new dinoﬂagellate species expedition (E3) was conducted in austral spring

(Tillmann & Akselman, 2016; Boutrup et al., 2017; aboard the R/V Puerto Deseado, from October

Tillmann, 2018; Tillmann et al. 2018; Sunesen et 26th to November 9th, 2013, with 47 sampling

al., 2020b) and the ﬁnding of new records (e.g. stations located between ≈40 and 47 ºS. The fourth

Fabro et al., 2016, 2017, 2019; Tillmann et al., expedition (E4) was conducted on board the

124

E. Fabro & G. O. Almandoz - Rare marine dinoﬂagellates

Fig. 1. Letters and numbers on maps indicate various sampling sites. Expeditions across the Argentine Sea.

E1: autumn; E2: late summer; E3: spring; E4 and E5: summer.

Canadian R/V Coriolis II in austral summer from sedimentation chamber prior to cell counting

3

0th January to 15th February 2014, in a transect under an inverted microscope (Leica DMIL LED).

consisting of 5 sampling stations from internal The organisms were counted in two stages; at

shelf waters of San Jorge Gulf to slope waters least 400 cells of the dominant taxa were counted

in front of the gulf. The last expedition (E5) was in random ﬁelds or in transects of the chamber to

carried out in austral summer from January 6th to estimate general plankton composition, whereas

January 12th, 2016, with seven sampling stations the whole chamber bottom was scanned to count

located between ≈38 and 55°S. The conductivity sparse species.

(

salinity)/temperature/depth (CTD) data were

Further morphological examination of

available throughout all expeditions, except from selected samples was conducted with a phase

leg K2 of expedition E2, during which no CTD contrast/diﬀerential interference contrast optical

measurements were performed. During this leg, microscope (LM) Leica DM2500 equipped with

only surface water temperature was measured with a DFC420C camera, and with scanning electron

a multiparameter probe TOA-DKK Model WQC.

microscopy (SEM): Jeol JSM-6360 LV SEM

During all expeditions, Niskin bottle samples (JEOL, Tokyo, Japan), Carl Zeiss NTS SUPRA

were taken from surface water (~4 m depth). 40 (Zeiss, Oberkochen, Germany) and FEI Quanta

Aliquots of 250 mL were fixed with acidic FEG 200 (FEI, Eindhoven, the Netherlands). Bottle

Lugol’s iodine solution for quantitative analyses. and net sample aliquots were ﬁltered through 0.2

Plankton net samples were additionally collected µm polyamide ﬁlters and 3 µm polycarbonate

for qualitative morphological analysis by vertical ﬁlters for SEM analyses. The material on the

net tows through the upper 20 m of the water ﬁlters was dehydrated by serial ethanol treatment

column with a 20 µm-mesh Nitex net and ﬁxed and ﬁnal critical point dehydration (BAL-TEC

with acidic Lugol’s iodine solution.

CPD-30, Balzers, Liechtenstein). Specimens

were sputter-coated with Au with a sputter ﬁne

coat Jeol JFC 1.100 (Jeol, Tokyo, Japan) for

Plankton analysis

Nano- (≈5-20 μm) and microplankton (20-200 samples observed with Jeol JSM-6360 LV SEM

μm) abundance was estimated using the Utermöhl or with gold-palladium (Cressington Scientiﬁc

(

1958) inverted microscope method. Subsamples Instruments, Watford, UK and Emscope SC500;

50 mL) from the mixed water obtained by Niskin Ashford, UK) for samples observed with Carl

bottles were left to settle for 24 h in a composite Zeiss NTS SUPRA 40 and FEI Quanta FEG 200.

125

Bol. Soc. Argent. Bot. 56 (2) 2021

reSultS and diSCuSSion

But the species has been found in the Southern

Atlantic in some occasions. Haraguchi & Odebrecht

Dinophysis microstrigiliformis Abé, Publ. Seto (2010) found one cell in internal shelf waters from

Mar. Biol. Lab. 15. 1967, Fig. 2.

Southern Brazil (≈34 °S, 51 °W) during winter. In

the Argentine Sea, records of the species correspond

to one cell found in external shelf waters in front of

Balech 1988, p. 230, lám. 8. Figs. 12-13.

Cells with elongated shape, longer than wide. Buenos Aires Province (37 °S) and a few more thecae

The left sulcal list (LSL) is long, extending until the at 41 °S (Balech et al., 1984; Balech, 1988). In our

posterior end of the cell. The three ribs from the LSL study, D. microstrigiliformis was only detected in

are thin, R3 is shorter than R2 and the distance between net tow samples and it was conﬁned to the southern

R2 and R3 is larger than between R1 and R2 (Fig. 2A). Argentine Sea (≈55 °S) during autumn (Table 1),

The anterior cingular list (ACL) is smooth and conic which supports its distribution in polar and sub-polar

(

Fig. 2B). Dinophysis species are mixotrophic with waters.

cryptophycean-like plastids (Schnepf & Elbräichter,

988). Dimensions: length average 36.4 µm ± 3.5,

width average 21.3 µm ± 2.5 (n = 8).

1

Observations. This species was described

based on one cell from Japan (Abé, 1967). The

author stated that it may be an aberrant form of

Distribution and habitat. D. microstrigiliformis D. lapidistrigiliformis, with smaller and more

is a very rare species, which has been mentioned elongated theca, and longer LSL. Balech (1988)

only a few times worldwide and always in very found also one cell from the northern Argentinean

low abundances. According to Ivin et al. (2014) is Sea (37 °S) and remarked that D. microstrigiliformis

probably a neritic and boreal species recorded near the is very similar to D. sacculus, but with a longer LSL

coast of northern Japan and in Avacha Bay, Russia. and a regular and convex dorsal edge. Dinophysis

Fig. 2. LM images of Dinophysis microstrigiliformis. A-B: lateral views; note that the LSL is large (ends

almost at the hypothecal antapex), R3 is shorter than R2 and the distance between R2 and R3 is larger than

between R1 and R2. Abbreviations= LSL: left sulcal list. ACL: anterior cingular list. R: sulcal list rib. Scale

bars: 10 µm.

126

E. Fabro & G. O. Almandoz - Rare marine dinoﬂagellates

Table 1. Summary of the occurrence, abundance, and physical conditions in which the reported

dinoﬂagellate taxa were found. n/d: not detected. M : median. Relative contribution: abundance

e

percentage of the analyzed taxa with respect to the total abundance of phytoplankton.

Expedition and

station

Relative

Taxon

Abundance Temperature Salinity Total Phytoplankton

contribution

-1

(cells L )

(cells L

)

(°C)

(psu)

(%)

Dinophysis

microstrigiliformis

113,500; 1,946,500;

969,400

E1: C20, I9, I22

E3: 5, 42

n/d

8.5

32.8; 33.3

-

Gyrodinium sp.

4,900; 6,500

,600;

8.0; 8.3

8.0; 9.4

33.7; 33.8 2,750,900; 3,253,300

0.2; 0.1

1

Karlodinium elegans E3: 5, 43

E1: I46, C16, I11,

33.7

2,750,900; 3,427,590

0.05; 0.4

4,600

I13, I14, I15

E2: 3K2

4

0-440

5.4-17.2

32.6-34.2

48,880-4,139,105

0.001-0.4

Oxytoxum laticeps

E3: 15, 43

E4: T1, T2, T3

E5: 7

(

M =100)

(M =8.5)

(M =33.7)

(M =541,990)

(M =0.03)

e

E1: C16,C21,I12,

I13, I14, I15, I48,

I49

E2: 18K1, 21K2

E3: 1, 2, 3, 5, 6,

2

0-9,000

7.9-16.3

33.2-33.8

74,760-24,050,740 0.00007-0.54

Peridiniella spp.

7, 8, 10-16, 20,

27, 30, 31, 37, 38,

41-44, 47, 48

(M =220)

(M =13.8)

(M =33.4)

(M =1,442,938)

(M =0.02)

e

E4: T2, T3

E5: 2, 4

Prorocentrum nux E2: 10K2

82

16.2

-

342,900

27

microstrigiliformis is considered as a currently conical (Fig. 3C). The apical groove is elliptical

accepted taxonomic entity (Guiry & Guiry, 2019). and bisected into two equal parts by a central line

However, the morphological similarity with D. (Fig. 3C). Cells are ornamented with longitudinal

lapidistrigiliformis and D. sacculus might justify striations, with the same number of striae in the epi-

a taxonomic revision. In this sense, Reguera and and hypocone, about 12 in ventral view. The sulcus

González-Gil (2001) suggested that small and is straight, narrow, well deﬁned, and extends into

dimorphic cells of D. sacculus mentioned by the epicone. On the hypocone, the sulcus is well

Bardouil et al. (1991) probably corresponds to deﬁned and deep, broadening toward the antapex.

D. microstrigiliformis. Likewise, Haraguchi & The cingulum is not superposed and only slightly

Odebrecht (2010) stated that D. lapidistrigiliformis displaced, about 1/10 of the total cell length. The

may be a stage in the life cycle of D. fortii.

genus Gyrodinium contains only heterotrophic

species (Daugbjerg et al. 2000). Dimensions: length

average 11.5 µm ± 2.0, width average 8.7 µm ± 1.9

Gyrodinium sp. Kofoid & Swezy, 1921. Fig. 3.

(n = 20).

Ovoid to spindle cell shape, slightly

dorsoventrally compressed. The epi- and hypocone

Distribution and habitat. In the Argentine Sea,

are similar in size (Fig. 3A-C). The apex is rounded the genus Gyrodinium is mainly represented by

whereas the antapex can be rounded (Fig. 3B) or G. fusus, a big species (≈80 µm long) frequently

127

Bol. Soc. Argent. Bot. 56 (2) 2021

Fig. 3. SEM images of Gyrodinium sp. A: lateral view; note the faint stria in the hyposome among pairs of

prominent striae (arrowheads). B-C: ventral views. Scale bars: 5 µm.

recorded in shelf waters from 36 to 39 °S, including described as Gyrodinium, only G. helveticum, G.

estuarine areas (Akselman, 1985; Barría de Cao & rubrum, G. spirale, G. fusiforme, G. moestrupii

Piccolo, 2008). By contrast, the small Gyrodinium and G. jinhaense (Takano & Horiguchi, 2004; Yoo

sp. cells found in this study were mainly observed et al., 2012; Jang et al., 2019), were assigned to

in high salinity slope waters (St. 5 and 42 from E3, Gyrodinium sensu Daugbjerg et al. (2000). The cells

Table 1). In those samples, Gyrodinium sp.-like analyzed in this study showed an elliptical apical

3

cells densities were 6.5 x10 and 4.9 x10 cells groove and longitudinal striations, which agrees

-1

L , respectively (Table 1). At both stations, total with the above mentioned Gyrodinium deﬁnition,

6

-1

plankton abundance was around 3 x10 cells L but which has also been supported by phylogenetic

species composition varied considerably: at station analysis (Takano & Horiguchi, 2004). Gyrodinium

5

diatoms were the dominant group, while at station sp. cells found in this study resemble, in general

4

2 a bloom of the dinoﬂagellate Prorocentrum shape and size (17 µm length, 12 µm wide), the

cordatum was observed.

species G. carteretensis described by Campbell

1973). However, no striation is mentioned in

(

Observations. The genus Gyrodinium was the original description of G. carteretensis and

described by Kofoid & Swezy (1921) to comprise the cingular displacement is bigger than in our

unarmored dinoﬂagellates with a descent cingulum specimens (1/3 vs. 1/10 of the total cell length).

displaced by more than one-ﬁfth of the total body Moreover, in the original description is established

length, in contrast to Gymnodinium which was that cells present chloroplast, so this species does

deﬁned by a cingulum displacement less than one- not agreed with the Gyrodinium definition by

ﬁfth of the cell length. More recently, Daugbjerg Daugbjerg et al. (2000). The recently described

et al. (2000) proposed the apical groove system Gyrodinium jinhaense (Jang et al., 2019) is similar

as a more useful character to distinguish these in size to the cells found in our study, especially

genera, as cingular displacement varies even within considering G. jinhaense cells starved for 2 days

clonal species (e.g., Takano & Horiguchi, 2004). (13-26 µm long, and 7-12 µm wide). However, G.

Consequently, the authors redeﬁned Gyrodinium to jinhaense contour is more slender, the cingulum is

contain exclusively heterotrophic species with an displaced about one quarter of the cell length and the

elliptical apical groove and longitudinal striations posterior sulcal area is widened toward the antapex,

in the amphiesma surface, while Gymnodinium forming a slightly S-shaped line. Moreover, the

species have a horseshoe-shaped apical groove and cell surface in G. jinhaense is ornamented with

no striations. From the about 100 species originally 16 longitudinal striations in ventral view; while

128

E. Fabro & G. O. Almandoz - Rare marine dinoﬂagellates

in Gyrodinium sp. there are no more than 12. In

Distribution and habitat. Karlodinium elegans

one of our pictures (lateral view) one faint stria is was recently described based on two clonal cultures

present in the hyposome among pairs of prominent (PTB601 and PTB602) obtained from samples

striae (Fig. 3A, arrowheads), thus resembling the collected during a dinoﬂagellate bloom in Pingtan

species G. heterostriatum (sensu Gómez et al., coastal area, Fujian, SE China. Our SEM analyses

2

020). However, cells in this study are considerably revealed the presence of K. elegans in bottle samples

smaller than cells from G. heterostriatum; despite at stations 5 and 43 from E3, which correspond to

this species has a very wide size range (30-70 µm relatively cold (8-9.4 °C) slope waters at ≈40 and

long; 25-60 µm wide). Moreover Gyrodinium sp. 45 °S. In these samples, Karlodinium-like cells

3

-1

cells have a lower number of striae in the hypocone densities were 1.6 x10 and 14.6 x10 cells L

in ventral view (12 or less vs. about 25) and ﬁnally respectively (Table 1); total plankton abundances

6

-1

in G. heterostriatum the episome is smaller than were 2.7 x10 and 3.4 x10 cells L . Both samples

the hyposome while in our species both are almost were dominated by diatoms, mainly Hemiaulus sp.

equal in size. Considering the above mentioned and also Thalassiossira sp. at station 5.

morphological and size diﬀerences compared to

Little is known about the occurrence of

other similar Gyrodinium species, the cells observed Karlodinium species, or the family Kareniaceae

in our study could not be assigned to species level. in general (De Salas et al., 2008 and references

Additional molecular and morphological analyses therein). Even though Kareniaceae representatives

are needed for a reliable identiﬁcation.

and other unarmored dinoﬂagellates may be a

dominant component of the dinoﬂagellate ﬂora in

Karlodinium elegans Cen, Lu & Huang. J. Antarctic (Gast et al., 2006, 2007; Mascioni et al.,

Oceanol. Limnol. 39: 245. 2021. Fig. 4.

2019) and Arctic waters (Luo et al., 2011), they

are widely unrecognized in ﬁeld surveys due to the

Ovoid cells with pointy apex, the epicone is potential for misidentiﬁcation when applying only

conical and displays rows of parallel furrows routine morphological analysis. For this reason, it

that are twisted to the left side in relation to is important to perform more deep morphological

the cell longitudinal axis. Each epicone furrow or molecular studies of this group, especially

carries rows of rounded structures ending in considering that several species in the lineage are

small pores (micro-processes sensu Paulmier et known to be ichthyotoxic (Bergholtz et al., 2005).

al., 1995; knobs sensu Cen et al., 2021) (Fig.

4

A, B). The hypocone is rounded and its surface

Observations. The family Kareniaceae comprises

is ornamented with quadrilateral pits formed by three genera, i.e. Karlodinium, Karenia and

longitudinal and horizontal stripes (Fig. 4C). Takayama, which share plastids with fucoxanthin

The cingulum is displaced; its anterior side is and its derivatives as the major accessory pigments

delineated from the epicone by a list; below the (De Salas et al., 2003; Benico et al., 2019). The

cingulum the surface displays two parallel rows genus Takayama possess a sigmoid apical groove

of knobs (Fig. 4C, arrows). The sulcus invades (De Salas et al., 2003), while in Karlodinium

slightly the epicone as a ﬁnger-like protrusion and Karenia the groove is straight; although

(

Fig. 4A, arrowhead). The apical groove begins Karlodinium diﬀers from Karenia by the presence

ventrally, above the sulcus, is directed obliquely of a ventral pore at the left side of the apical groove

to the apex and extends to the middle region of (Daugbjerg et al., 2000). The general appearance

the dorsal epicone (Fig. 4B, double arrowhead). and main morphological features (e.g. long slit-like

The ventral pore is a thin and long slit located “ventral pore”, longitudinal striations curving to the

far from the apical groove at the left side of left side on the epicone, the apical groove extending

the sulcal region (Fig. 4D, triangle; Fig. 4E). to the middle region of the dorsal epicone, and a

This is an autotrophic species with several very special and unusual surface ornamentation

yellowish-brown chloroplasts distributed in the on the hypocone) of Karlodinium cells analyzed

cell periphery (Cen et al., 2021). Dimensions: in this work were identical to that reported in

length average 14.9 µm ± 2.7, width average 11.1 the original description of K. elegans. Regarding

µm ± 2.0 (n = 24).

cells size, our specimens were a little smaller than

129

Bol. Soc. Argent. Bot. 56 (2) 2021

Fig. 4. SEM images of Karlodinium elegans. A: ventral view, note how the sulcus invades the epicone as

a ﬁnger-like protrusion (arrowhead). B: dorsal view, note the apical groove ending in the dorsal region of

the epicone (double arrowhead). C: antapical view, note the list in the anterior side of the cingulum, the

ornamentation of longitudinal and horizontal stripes forming quadrilateral pits in the hypocone and the two

rows of knobs in the upper hypocone and in the epicone striation (arrows). D: latero-ventral view, note that

the ventral pore is a thin and long slit (triangle). E: detail of D showing the ventral slit. Scale bars: 5 µm.

130

E. Fabro & G. O. Almandoz - Rare marine dinoﬂagellates

those described by Cen et al. (2021), i.e. 19-27

µm long, 15-23 µm wide. Morphologically two

species of Karlodinium are similar to K elegans:

K. corrugatum and K. gentenii. All of them show

parallel micro-processes rows below the cingulum.

Particularly, K. corrugatum diﬀers from K. elegans

by presenting parallel and not twisted furrows in the

epicone and K. gentenii has a ventral pore next the

apical grove instead of a long slit (De Salas et al.

2

008; Nézan et al., 2014). According to Nézan et al.

(2014) a mixed ﬁxation with Lugol’s solution and

glutaraldehyde allows to see ﬁne details of the cell

surface by removing the membranous material or

mucilage that covers the cell. Likewise, Cen et al.

(2021) established that the double ﬁxation revealed

a much clearer cell surface. Although cells analyzed

in our study were ﬁxed only with Lugol’s solution,

the main morphological features mentioned above

could be observed. Unfortunately, the lack of

samples preserved with other ﬁxatives such as

glutaraldehyde or osmium tetroxide did not allow

performing a more detail examination of other key

morphological features as the position and shape of

the cell organelles.

Fig. 5. LM (A-B) and SEM (C-D) images of

Oxytoxum laticeps. C: dorsal view. Note the

longitudinal ridges on the plates. D: ventral view.

Oxytoxum laticeps Schiller 1937, Fig. 5.

Burns & Mitchell 1982, pp. 72-73, ﬁgs. 5-11; Note the small sulcal wing covering the ﬂagellar

Gómez et al. 2008, p. 28, ﬁg. 35.

pores. Scale bars: 10 µm.

The epitheca represents 20-26 % of the total

cell length, shows a domed shape, without apical

spine, and it is smooth with occasional small pores

Distribution and habitat. The species of the

arranged in random orientation (Fig. 5A-D). The family Oxytoxaceae usually occur in low densities

hypotheca is cone-shaped, it is larger and wider than in the open ocean, and the smaller ones are rarely

the epitheca, with convex sides which taper down to retained in net samples (Gómez, 2018). However, O.

the antapex, ending in a pointy extension (Fig. 5A- laticeps is commonly found in New Zealand coastal

D). The cingulum is wide, deep, slightly displaced waters (Burns & Mitchell, 1982), and densities up

5

-1

and presents well developed lists (Fig. 5C). The to 2.6 x10 cells L have been observed in Crozet

sulcal plate extends slightly into the hypotheca and Basin (Indian Ocean) (Kopczyńska & Fiala, 2003).

a small sulcal wing covers the ﬂagellar pores. (Fig. O. laticeps was described from the Mediterranean

5

D). There is also a small ribbed list on the ventral Sea and it was listed in the north, central equatorial,

and dorsal antapical end of the hypotheca (Fig. tropical and southeast Paciﬁc (Hasle 1960; Venrick,

C, D). The hypothecal surface is covered with 1982; Iriarte & Fryxell, 1995; Gómez et al., 2008),

5

microtubular rods (sensu Burns & Mitchell, 1982) in Canary Islands (northeast Atlantic) (Ojeda, 1996)

arranged in rows from the antapex to the cingulum. and in the Caribbean Sea (Pérez-Castresana et al.,

The apical end of the tube is projected beyond 2014). Our ﬁnding represents the ﬁrst record of O.

the thecal plane and ends in a pore (Fig. 5C, D). laticeps for the southwest Atlantic Ocean, although

It is an autotrophic species (Gómez et al., 2016). Balech (1988) found one cell of the similar species

Dimensions: length average 16.7 µm ± 1.4, width O. mediterraneum at northeast Argentine Sea.

average 12.4 µm ± 1.8 (n = 20).

O. laticeps was found in bottle samples during

131

Bol. Soc. Argent. Bot. 56 (2) 2021

all expeditions but in low abundances and in a the identity of O. laticeps remains unclear, but both

few stations (Table 1). Maximum cell densities O mediterraneum and O. laticeps are considered as

-1

around 400 cells L ) were detected during both accepted names. Cell length measurements from

(

summer expeditions in slope waters at the southern our specimens were in the range mentioned by

sampling area (≈46-55 °S), where total planktonic Burns & Mitchell (1982) (15-25 µm) and by Dodge

6

-1

abundances of ≈1.3 x10 cells L were primarily & Saunders (1985) (15-20 µm), but were smaller

represented by blooms of the diatom genus Pseudo- than those mentioned in Gómez et al. (2008) (30

nitzschia (St 7 from E5) and small (<5 µm) µm). The surface morphological characteristics of

unidentiﬁed phytoﬂagellates (St. T2 from E4).

the hypotheca agreed with that mentioned by Burns

and Mitchell (1982) for cells with persistent outer

Observations. Oxytoxum and Corythodinium are wall, characterized by a system of microtubular

the only two genera within the family Oxytoxaceae, rods arranged in slanting rows from the antapex to

which form their own clade within the dinokaryotic the girdle with a microtubule that ends in a small

dinoﬂagellates according to molecular data (Gómez pore. Another morphologically similar species is

et al., 2016). Both genera are morphologically Oxytoxum stropholatum (Dodge & Saunders, 1995)

similar but can be distinguish by the position of the which was placed into Corythodinium by Gomez

cingulum, always anterior in Oxytoxum and median (2018). Our specimens share with C. stropholatum

or anterior in Corythodinium, and by the larger the presence of a sulcal wing covering the ﬂagellar

and broader epitheca in Corythodinium (Taylor, pores, but diﬀered in general cell size (24-25

1

976). Although some species possess intermediate µm long; 14-17 µm wide according to Dodge &

characteristics between both genera; molecular data Saunders, 1995) and in the shape of the epitheca,

support the generic separation (Gómez et al., 2016). which is flattened and only slightly narrower

Within the genus Oxytoxum, Dodge and Saunders than the hypotheca in C. stropholatum, while

(1985) designated O. laticeps as the type species of the cells analyzed in this study present a domed

Section Excavatum (II), which comprises species shaped epitheca which is sharply narrower than the

with a reduced and domed epitheca and sulcus hypotheca.

deeply excavated and partly covered by a large

list composed of extensions of Sd and 6’’ plates Peridiniella danica (Paulsen) Okolodkov &

and by a list which is an extension of 1’’”. The Dodge. Eur. J. Phycol 30. 1995. Fig. 6A-C

closest species to O. laticeps is O. mediterraneum,

Glenodinium danicum Paulsen (Basionym)

which was also described by Schiller (1937). Okolodkov & Dodge 1995, pp. 301-302, 304, ﬁgs.

The presence of rows of hexagonal pores on the 1-11.

hypotheca of O. mediterraneum, diﬀerentiate it

from O. laticeps. Additionally, a spine process in

Plate formula is: Po, X, 4′, 3a, 7′′, 6c, 4s, 6′″,

the antapex is found only in O. laticeps and the 2″″. Cells are almost rounded. The thecal surface

epitheca of O. mediterraneum is more ﬂattened is slightly or deeply rough. Cingulum is deeply

(Schiller, 1937). Burns & Mitchell (1982) analyzed excavated, displaced one girdle width, and presents

New Zealand ﬁeld material and found that these lists at both sides. Sulcus is concave with two lists,

features that diﬀerentiate both species were found the left one more prominent than the right one (Fig.

in the same specimen due to a multilayered 6A). The apical pore plates are surrounded by a

structure of the theca, and consequently considered collar that extends ventrally to the sulcus, covering

O. mediterraneum as a synonym of O. laticeps. partially plate 1’ (Figs. 6A-C). The apical pore

More recently, Gómez (2018) reviewed the complex consists of a central structure surrounded

synonymy of the dinoﬂagellate genera Oxytoxum by a horseshoe-shaped plate (Po) and another small

and Corythodinium and placed O. laticeps in a plate (x) located in the ventral left region of the

group composed by O. sphaeroideum and allied apical pore complex (Fig. 6B). Both epitheca and

species that present a small size, rounded cell shape hypotheca show pores in the plates which can be

and absence of spines. The author remarked that arranged in straight rows that run through the edges

there were lots of species misidentiﬁcations within of the plate or forming concentric rows (Fig. 6A,

Oxytoxum and Corythodinium in the past, and that arrowhead). Intercalary plate 2a can be six-sided

132

E. Fabro & G. O. Almandoz - Rare marine dinoﬂagellates

Fig. 6. SEM images of Peridiniella danica (A-C) and Peridiniella globosa (D-F). A: Ventral view, note the

collar surrounding the apical pore plates and the arrangement of the pores on the theca surface (arrowhead).

B-C: antapical views, note the diﬀerent shape of plate 2a, hexagonal in B and pentagonal in C-D: Ventral

view, note the collar surrounding the apical pore plates and the arrangement of the pores on the theca

surface (arrowhead). E: Dorso-apical view, note the small plate 2a with a depression on the center. F: Apical

view, note the small 2a plate. Scale bars: 10 µm.

(

hexagonal) (Fig. 6B) or ﬁve-sided (pentagonal) sides. Both epitheca and hypotheca show pores in

(Fig. 6C). Autotrophic species. Dimensions: length the plates which can be arranged in straight rows

average 23.9 µm ± 5.3 (n = 6), width average 22.0 that run through the edges of the plate or forming

µm ± 6.1 (n = 5).

concentric rows (Fig. 6D, arrowhead). Intercalary

plate 2a is pentagonal, very small and it is depressed

Peridiniella globosa (Dangeard) Okolodkov. Acta with respect to the cell surface or shows a depression

Bot. Mex. 74. 2006. Fig. 6D-F. on the center (Fig. 6E, F). Autotrophic species.

Peridinium globosum Dangeard (Basionym). Dimensions: length average 31.3 µm ± 5.7 (n = 5),

Dangeard 1927 (as Peridinium globosum), p. 355, width average 32.2 µm ± 6.1 (n = 6).

ﬁg. 20.

Distribution and habitat. P. danica seems to be

Plate formula is: Po, X, 4′, 3a, 7′′, 6c, 4s, 6′″, 2″″. a cosmopolitan species, although it has been found

Cells are rounded (Fig. 6D). The thecal surface is mainly in cold waters, being widely distributed

smooth or slightly rough. The collar surrounding in the northeast Atlantic Ocean (Okolodkov &

the apical pore plates is not so evident in cells with Dodge, 1995 and references therein). Moreover,

a smooth theca. Cingulum is deeply excavated, Peridiniella sp. recently mentioned for the western

displaced one girdle width and presents lists at both Antarctic Peninsula by Mascioni et al. (2019)

133

Bol. Soc. Argent. Bot. 56 (2) 2021

corresponds to P. danica (Mascioni M., pers. com.). shapes of plate 2a (hexagonal or pentagonal) and

By contrast, P. globosa is listed in the Mexican two diﬀerent arrangements of the pores (straight

Paciﬁc (Okolodkov & Gárate-Lizárraga, 2006) and rows that run through the edges of the plate or

in the Black Sea (Barinova et al., 2011). In the forming concentric rows). By contrast, P. globosa

southwest Atlantic, the only Peridiniella species showed a very small plate 2a and bigger size than

recorded, as far we know, is P. sphaeroidea found P. danica. Plate 1′ of our specimens is narrower

by Balech (1988) from 36°S to 39°S in temperate than that illustrated by Dangeard (1927; as

waters (15-18 °C). In our study, Peridiniella Peridinium globosum).

spp. cells were observed during all expeditions,

covering a wide area of the Argentine Sea (≈ 39- Prorocentrum nux Puigserver & Zingone.

5

4 °S). Their abundance was usually low (e.g. Phycologia 41. 2002. Fig. 7

-1

from 20 to 1,960 cells L ) in most expeditions, but

peaks of ≈7 x10 cells L were recorded during

3

-1

Globose cell shape (Fig. 7A) and very convex

spring at three stations (St. 37, 38 and 42) from valve shape (Fig. 7B, C). The periflagellar

southern slope waters. Maximum Peridiniella area is located on the right valve and is not

spp. abundances were detected in cold waters (8 depressed (Fig. 7D, E). The ﬂagellar pore is

°

C) (Table 1), which agrees with the background bi-lobed and surrounded by seven plates (Fig.

data mentioned above for P. danica. 7E). The surface of the valves is completely

The cell contour and size of Peridiniella smooth, but shows small and large pores, usually

species are very similar to species of the toxigenic with trichocysts emerging from them (Fig. 7E,

genus Alexandrium (Okolodkov & Gárate- F). The intercalary bands are well deﬁned and

Lizárraga, 2006), and therefore, both taxa can be overgrowth is evident in lateral view (Fig. 7D,

misidentiﬁed during routine cell counting with G, arrowheads). On the right valve, one small

optical microscopy. In this study, Peridiniella and three large pores are located in the apical

spp. and Alexandrium spp. co-occurred in 19 zone, close to the periﬂagellar area (Fig.7-F),

samples from E3, in which Alexandrium sp. cell while both valves show a large pore and three

abundances ranged between 20 and 28,000 cells small pores at the antapical extreme (Fig. 7G, H,

-

1

L . This highlights the importance of thecal plate arrows). Additionally, the left valve presents one

observations during monitoring of harmful algae.

small and two large pores grouped near the suture

halfway between the apical and antapical ends

Observations. There are only four described (Fig. 7I, arrow). This is an autotrophic species

species of Peridiniella: P. danica, P. catenata, with two ochre-yellow chloroplasts (Puigserver &

P. sphaeroidea and P. globosa. All these species Zingone, 2002). Dimensions: length average 7.9

have a similar almost rounded cell shape and µm ± 0.9 (n = 20), width average 7.3 µm ± 1.1 (n

present the median and deep sulcus with lists = 20), depth average 7.8 µm ± 1.5 (n =15).

in both margins, but they can be diﬀerentiated

by the following characteristics: P. danica is

Distribution and habitat. P. nux was described

slightly dorsoventrally compressed, P. catenata is based on a culture (Pronap I) from the Tyrrhenian

characterized by the presence of antapical spines Sea in the Gulf of Naples (Puigserver & Zingone,

(

Dodge, 1987), P. sphaeroidea shows a strong 2002). Another strain previously isolated from

polygonal ornamentation over the surface of the Plymouth waters (UK) in 1957 was also identiﬁed

thecal plates (Balech, 1979; Dodge, 1987), and P. as P. nux by Puigserver & Zingone (2002). By

globosa possess a very small second intercalary contrast, as far as we know, P. nux was never

plate (2a) and a more globose cell contour than detected elsewhere since its original description,

the other species (Dangeard, 1927; as Peridinium probably due to the extremely small size and very

globosum). Observed cells of P. danica were thin theca. In our study, very small and globose

similar in size to materials from the Norwegian cells of a thecate dinoﬂagellate were observed

Sea presented by Okolodkov & Dodge (1995) in the San Matías Gulf (station 10K2 from E2,

(

21-25 µm long, 20-22 µm wide). In accordance Table 1), and its abundance was estimated as

-1

with these authors, we observed two diﬀerent 82,000 cells L . Further SEM analyses of bottle

134

E. Fabro & G. O. Almandoz - Rare marine dinoﬂagellates

Fig. 7. LM (A-C) and SEM (D-I) images of Prorocentrum nux. A: Cell in lateral view. B: Empty valve in lateral

view. C: Empty right valve in apical view. D: Whole cell, apical view. Note the overgrowth from the intercalary

bands (arrowheads). E: Detail from 2, note the large pores and the small pore from the periﬂagellar area and

the trichocysts emerging from them. F: Empty right valve. G: Whole cell, lateral view. Note the overgrowth

from the intercalary bands (arrowheads) and the antapical group of pores (arrows). H: Whole broken cell,

note the antapical group of pores (arrows). I: empty left valve, note the pores near the suture in the middle

of the cell (arrow). Scale bars A-C, D, F-I: 5 µm; E: 1 µm.

sample concentrates revealed that those cells

Observations. P. nux has unique morphological

corresponded to P. nux, a species that has never characteristics that differentiate it from other

been quantiﬁed in ﬁeld samples before. Total Prorocentrum species, such as the globose shape

5

plankton abundance at station 10K2 was 3 x10

in apical and antapical view, the overgrowth

-

1

cells L and was dominated by small (<15 µm) of the intercalary bands and the particular

dinoflagellates, of which Prorocentrum nux distribution of small and large pores (Puigserver

and Azadinium-like cells were the dominant & Zingone, 2002). Cells analyzed in our study

taxa. Until now, there are no reports of harmful were similar in size to those provided in the

events related to P. nux, although is important to original description (6.3-9.0 µm long, 5.3-10.0

consider that small Prorocentrum species, such µm wide), which placed P. nux as the smallest

as P. cordatum, can produce dense blooms and from all Prorocentrum species and even one of

generate anoxia and harmful eﬀects on marine life the smallest thecate dinoflagellates known until

(

Heil et al., 2005).

now.

135

Bol. Soc. Argent. Bot. 56 (2) 2021

ConCluSionS

bibliograPhy

The detailed examination with optical and

electron microscopy of field plankton samples

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gradient across the Argentine Sea lead to the

finding of seven dinoflagellate that are little

known from marine waters worldwide. Most

of them were rare or scarce; which, together

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justifies the poor information about their

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