gomez artigas sand-dwelling dinoflagellates 2014

High diversity of dinoagellates in theintertidal sandy sediments of Wimereux(north-east English Channel, France)

fernando gomez1,2 and luis f. artigas1

1Laboratoire dOceanologie et Geosciences, CNRS UMR 8187, Universite du Littoral Cote dOpale, MRENULCO, 32 av. Foch, 62930Wimereux, France, 2Laboratory of Plankton Systems, Oceanographic Institute, University of Sao Paulo, Praca do Oceanograco 191,sala 100, Sao Paulo, SP 05508-120, Brazil

Benthic dinoagellates collected in springsummer 2010 and 2011 from intertidal sandy sediments of the shore of Wimereux(north-east English Channel, France) were examined by light microscopy, and some of them by scanning electron microscopy.High dinoagellate species richness, 70 species, was evidenced when compared to the plankton observed in the coastal watersof the north-east English Channel. The greatest difculty in performing accurate species identication mainly concerned theheterotrophic species of Amphidinium sensu lato, the laterally attened species of Amphidiniopsis, as well as some hetero-trophic species of Thecadinium. Several undescribed species are here illustrated, mainly within these genera. The differences insize between species of Herdmania and Sabulodinium suggest the occurrence of at least a second species for these monotypicgenera. The species Amphidiniopsis hexagona, A. rotundata, A. uroensis and Sinophysis minima are reported for the rsttime in the Atlantic Ocean and on European coasts. Although these species were only previously known from the PacicOcean, they should not necessarily be considered as newcomers or invasive species due to the scarce coverage of the previousstudies on sand-dwelling dinoagellates.

Keywords: benthic microbial loop, biodiversity, Dinophyta, microphytobenthos, north-east Atlantic, psammophilic protist,sand-dwelling Dinophyceae, taxonomy

Submitted 25 June 2013; accepted 19 November 2013; rst published online 20 December 2013

I NTRODUCT ION

Benthic dinoagellates have been historically relatively littlestudied in comparison to their planktonic counterparts.Since the late 1970s, the epiphytic dinoagellates attached tomacroalgae have received more attention because they havebeen identied as responsible for ciguatera sh poisoning(Yasumoto et al., 1977). The sand-dwelling dinoagellates,living in the interstitial waters between the sand grains, havereceived less attention. The rst studies were carried out inthe sandy tidal ats of the British Isles (Herdman, 1922,1924; Saunders & Dodge, 1984), France (Balech, 1956;Dragesco, 1965; Dodge & Lewis, 1986; Paulmier, 1992) andDenmark (Larsen, 1985). The studies have largely increasedin the last fteen years with the description of numerousnew species from the beaches of the North Sea, Japan,Russian Pacic, Australia, Canadian Pacic and Kuwait (seereferences in Al-Yamani & Saburova, 2010). In recent years,the description of new benthic species has accounted foralmost one half of the total new dinoagellates species(Gomez, 2012). The publications of sand-dwelling dinoagel-lates are usually restricted to the description of a single or afew species, and the review of the closer relatives. This

implies a disperse literature, with few compilations of thediversity for a given area (Al-Yamani & Saburova, 2010).

This study compiles the observations of sand-dwellingdinoagellates carried out over two years on the shore ofWimereux, north-eastern English Channel, France. Thisarea, located in the southern side of the Straits of Dover(Pas de Calais) is characterized by strong winds and currents(Brylinski et al., 1991; Sentchev et al., 2007; Korotenko &Sentchev, 2011). Planktonic dinoagellates, usually betteradapted to calmer waters (Margalef, 1978), are not favouredin this highly turbulent environment, with few recordedspecies (Gomez & Souissi, 2007, 2008; Grattepanche et al.,2011; Gomez & Artigas, 2013). In the north-eastern EnglishChannel, the semidiurnal macrotidal regime (.8 m height)results in important emersion periods affecting wide sandybeaches. During ebb tide, the exposed substratum becomesgreen or golden brown in colour in irregular areas of the inter-tidal sand-ats. This is due to a supercial accumulation ofenormous numbers of protists. These organisms dwell in thesediments during tidal inundation and move up onto thesurface sands during tidal exposure. These vertical-migrationrhythms have been described worldwide for sand-dwellingprotists such as dinoagellates (Herdman, 1924; Horiguchi& Pienaar, 1988), euglenoids (Palmer & Round, 1965;Kingston & Gough, 2009) and diatoms (Janssen et al., 1999;Consalvey et al., 2004; Mitbavkar & Anil, 2004). These dis-colorations reach high primary production and respirationrates on the beach of Wimereux (Spilmont et al., 2005;Hubas et al., 2007). Two previous studies provided the rst

Corresponding author:F. GomezEmail: [email protected]

443

Journal of the Marine Biological Association of the United Kingdom, 2014, 94(3), 443457. # Marine Biological Association of the United Kingdom, 2013doi:10.1017/S0025315413001744

molecular data of the dinoagellate genera Amphidiniopsisand Sinophysis (Gomez et al., 2011, 2012). However, the com-position of the species has not yet been examined.

This study presents a rst inventory of the benthic dinoa-gellates in the region, with micrographs of several species thathave not yet been described. Several species are illustrated forthe rst time in the area, since their original descriptions in thePacic Ocean. This constitutes the rst observations of severalspecies in the Atlantic Ocean and European seas.

MATER IALS AND METHODS

This study was undertaken in the soft sandy sediments of theshore of Wimereux, France (5084612N 183642E) fromMarch to October in 2010 and 2011. There were two samplingsites, the border of a large pool (50 m diameter,1 m depth),and several smaller pools and moist sands with a faint brownishdiscoloration, in front of the LOG laboratory (MREN ULCOand Marine Station of Wimereux UL1). The upper centimetreof sand was collected with a spoon and deposited into a bottle.There, the sand was rinsed with seawater and stirred vigorously,and the suspension settled in a composite settling chamber. Thesettled material was examined with a Nikon inverted micro-scope (Nikon Eclipse TE2000-S) and photographed with aNikon Digital Sight DS-2M camera.

For scanning electron microscopy, aliquots of the agitatedsand samples were xed with glutaraldehyde (5%) and lteredonto a 0.8 mm pore size Nucleopore membrane lter, washedwith distilled water, xed with osmium, dehydrated with agraded series of ethanol and critical-point-dried with CO2.Filters were mounted on stubs, sputter-coated with gold andviewed using a Hitachi S4800 scanning electron microscope(SEM). Images were presented on a black background usingAdobe Photoshop CS3.

RESULTS

The sand discolorations on the beach of Wimereux were moreconspicuous during sunny periods. There were two main types:green patches tended to occur in the upper limit of the eulittoralzone associated with monospecic proliferations of Euglena sp.,and greenish-brown patches were observed in moist sands inthe middle of the eulittoral zone and on the bottom of tidalpools. These patches were due to diatoms and photosyntheticdinoagellates, mainly proliferations of Togula britannica, T.cf. compacta, Polykrikos lebouriae, Amphidinium herdmanii,or more sporadically Spiniferodinium. A total of 70 specieswere found (Table 1). See video at: http://www.youtube.com/watch?v=BEjD-1wvBTs. A brief description of each species isprovided below.

Amphidinium sensu latoConspicuous patches in the sandy sediments ofWimereux weredue to photosynthetic species that were formerly describedunder the genus Amphidinium. This unarmoured genus ofdorso-ventrally attened species was traditionally dened byits small episome size, not exceeding one third of the totalcell length. Currently Amphidinium sensu stricto is valid forspecies with minute irregular triangular or crescent-shapedepisome, deected to the left and overlaid in the anterior

Table 1. List of sand-dwelling dinoagellate species from the shore ofWimereux, France.

Taxa Figure

Adenoides eludens (Herdman) Balech 8AFAmphidiniopsis aculeata Hoppenrath, Koeman &

B.S. Leander3JL

Amphidiniopsis arenaria Hoppenrath 4AEAmphidiniopsis cristata Hoppenrath 3XAEAmphidiniopsis galericulata Hoppenrath 4FIAmphidiniopsis hexagona S. Yoshimatsu,

S. Toriumi & J.D. Dodge3MO

Amphidiniopsis aff. hexagona small form 3P, QAmphidiniopsis hirsuta (Balech) J.D. Dodge 3AFAmphidiniopsis rotundata Hoppenrath &

M.S. Selina3AFAI

Amphidiniopsis sp. 1 square 3T, UAmphidiniopsis sp. 2 3V, Wcf. Amphidiniopsis sp. 3 4JMcf. Amphidiniopsis sp. 4 4N, OAmphidiniopsis swedmarkii (Balech) J.D. Dodge 3GIAmphidiniopsis uroensis S. Toriumi, S. Yoshimatsu

& J.D. Dodge3R, S

Amphidinium bipes Herdman 1IKAmphidinium carterae Hulburt 1ACAmphidinium herdmanii Kof. & Swezy 1D, EAmphidinium incoloratum P.H. Campb. 1MAmphidinium mootonorum Sh. Murray &

D.J. Patterson1G, H

Amphidinium aff. operculatum Clap. & J. Lachm. 1FAmphidinium sp. 1 heterotrophic form 1LAmphidinium sp. 2 round form 1NAmphidinium scissum Kof. & Swezy 1AAACAmphidinium sensu lato sp. 1 with a granulate

surface1AD, AE

Amphidinium sensu lato sp. 2 heterotrophic form 1O, PAmphidinium sensu lato sp. 3 heterotrophic form 1QAmphidinium sensu lato sp. 4 heterotrophic form 1RAmphidinium sensu lato sp. 5 heterotrophic form 1SAmphidinium sensu lato sp. 6 heterotrophic form 1TAmphidinium sensu lato sp. 7 photosynthetic form 1AXAmphidinium sensu lato sp. 8 photosynthetic form 1AYAmphidinium sensu lato aff. A. mananninii

photosynthetic form1AZ

Ankistrodinium semilunatum (Herdman) Hoppenrath,Sh. Murray, Sparmann & B.S. Leander

1AFAK

Apicoporus glaber (Hoppenrath & Okolodkov)S.F. Sparmann, B.S. Leander & Hoppenrath

1W, X

cf. Apicoporus sp. 1Zgymnodinioid species 1 2Egymnodinioid species 2 2FGymnodinium venator Fl Jrg. & Sh. Murray 2AEHerdmania litoralis J.D. Dodge large form 4P, Q, T, UHerdmania litoralis J.D. Dodge small form 4PScf. Herdmania sp. lacking apical notch 4X, YKatodinium asymmetricum (Massart) Loebl. 8X, YKatodinium glandula (Herdman) A.R. Loebl. 8SWPlanodinium striatum R.D. Saunders & J.D. Dodge 6PYPolykrikos herdmaniae Hoppenrath & B.S. Leander 2GKPolykrikos lebouriae Herdman 2LOProrocentrum fukuyoi Sh. Murray & Y. Nagah. 8GRSabulodinium sp. small form 6N, OSabulodinium undulatum var. glabromarginatum 6AGSabulodinium undulatum var. undulatum 6HMSinophysis ebriola (Herdman) Balech 7AGSinophysis aff. grandis 7JMSinophysis grandis Hoppenrath 7NQ

Continued

444 fernando go mez and luis f. artigas

ventral part of the hyposome (as dened by Fl Jrgensen et al.,2004). Other Amphidinium species have been transferred intothe genus Gymnodinium (i.e. G. venator), new genera(Ankistrodinium, Apicoporus, Bispinodinium, Testudodinium,Togula) and other species also need to be placed into a separategenus (i.e. Amphidinium scissum).

Amphidinium sensu strictoThe photosynthetic species Amphidinium carterae, A. opercu-latum and A. herdmanii are characterized by a small episome,crescent-shaped and deected towards the left. The cells ofAmphidinium carterae are oval, more or less elongated, 1315 mm long and 913 mm wide (Figure 1AC). When com-pared to A. operculatum and A. herdmanii, the shape of thehyposome of A. carterae is more asymmetrical, with theepisome closer to the right side of the cell (Figure 1AC).The species A. carterae, A. massartii and A. thermaeum arehighly morphologically similar, overlapping completely insize range and in shape. According to Murray et al. (2012)these three species can be distinguished on the basis of theshape of the plastidwhich is reticulate and distributedthroughout the whole cell area in A. carterae, but generallymore sparse, with several lobes, in A. massartii and A. ther-maeumand the slightly lower position of agellar insertionin A. massartii and A. thermaeum compared to A. carterae.

The cells of A. operculatum and A. herdmanii are oval,oblong to egg-shaped from the ventral side, length about25 mm and width about 20 mm. The species A. herdmaniihas been illustrated in the literature with different mor-phologies (Schiller, 1933, gure 238af). We consider thatA. herdmanii corresponds to the rst illustration byHerdman (1922, gure 8a). The episome of A. herdmanii issymmetrical and protrudes over the hyposome. The hypo-some is slightly asymmetrical, with the left side longer thanthe right one, appearing indented at the antapex by thesulcus (Figure 1D, E). Consequently, A. herdmanii shows aslightly bi-lobulated antapex in comparison to A. opercula-tum. The specimens of Figure 1F show the cell shape of

A. operculatum. However, they are named Amphidinium aff.operculatum because the episome is wider than in the originaldescription of A. operculatum (Figure 1F). The cells of A. moo-tonorum differ from other species of Amphidinium sensustricto in the episome, which does not project beyond theoutline of the cell. The cingulum is V-shaped and encirclesthe episome (Figure 1G, H). The nucleus is usually posteriorlylocated in the species of Amphidinium sensu stricto. However,the nucleus of A. mootonorum is located in the middle of thecell (Figure 1G, H). This species can be easily confused withTestudodinium testudo.

There is less information on the heterotrophic species ofAmphidinium when compared to the photosynthetic ones,because they do not form large proliferations and because ofthe difculties of establishing cultures. Amphidinium bipes isone of the most distinctive heterotrophic species ofAmphidinium because the hyposome is divided into tworounded antapical lobes (Figure 1IK). The differentiationamong other heterotrophic species of Amphidinium is moredifcult. Figure 1L illustrates a specimen of similar size toA. bipes, with a similar episome that protrudes over the hypo-some. The main difference is the oblong rectangular shape ofthe hyposome (Figure 1L). We are unable to assign this speci-men to any known species.

Amphidinium incoloratum shows an oval hyposome,asymmetrical, relatively straight, with the right side convex(Figure 1M). The small episome slightly protrudes over thehyposome. The cell is about 32 mm long and 20 mm wide(Figure 1M). Figure 1N illustrates a specimen examined byscanning electron microscopy. It was not observed by lightmicroscopy, and we were unable to determinate the presenceof plastids. The episome is at, 6 mm wide, and it protrudesover the hyposome, as typical in Amphidinium sensu stricto(Figure 1N). The most distinctive character is a round cellbody (diameter of 20 mm). We are unable to assign this speci-men to any known species.

heterotrophic species of amphidinium sensu

latoSeveral heterotrophic species show a at episome that slightlyprotrudes over the hyposome. The shape of the hyposomevaries from ovate (Figure 1O, P), or rounder with the antapicalmargin slightly divided into two rounded lobes (Figure 1Q).Other heterotrophic specimens show an episome almostembedded in the hyposome (Figure 1RT). The shape ofthe hyposome ranges from oval (Figure 1R, S) to elongatewith a slightly pointed antapex (Figure 1T). We are unableto assign these specimens to known species.

genus testudodiniumThe genus Testudodinium has been recently proposed for aspecies with a small episome that does not project beyond theoutline of the cell. The cingulum is V-shaped and encircles theepisome. The sulcus is about one-third of the total cell lengthand is located at the centre of the hyposome. This morphologyis close to the species Amphidiniummootonorum which has thenucleus located in the middle of the cell (Figure 1G, H). Wefound a species that ts the characteristics of the genus(Figure 1U, V). The small episome is embedded in the hypo-some, protruding from the hyposome on the ventral side. Thehyposome is elongated with a slightly pointed margin. Thespecimen shows a brownish pigmentation (Figure 1U, V).

Table 1. Continued

Taxa Figure

Sinophysis minima M.S. Selina & Hoppenrath 7TVSinophysis sp. with dorsal lobule 7ISinophysis stenosoma Hoppenrath 7R, SSinophysis cf. verruculosa Chomerat & Nezan 7HSpiniferodinium galeiforme T. Horig. & Chihara 2PTTestudodinium sp. 1U, VThecadinium acanthium Hoppenrath 5LPThecadinium inclinatum Balech 5VYThecadinium kofoidii (Herdman) J. Larsen 5AEThecadinium neopetasatum R.D. Saunders &

J.D. Dodge5F, G

Thecadinium sp. 5HKThecadinium yashimaense S. Yoshimatsu, S. Toriumi

& J.D. Dodge5QU

Togula britannica (Herdman) Fl Jrg., Sh. Murray &Daugbjerg

1AL, AM

Togula cf. compacta (Herdman) Fl Jrg., Sh. Murray &Daugbjerg

1ANAR

Unidentied cf. Togula sp. 1 1AVUnidentied cf. Togula sp. 2 1AW

sand-dwelling dinoflagellates from wimereux 445

genus apicoporusThe heterotrophic species Apicoporus glaber (Amphidiniumgabrum) is characterized by a small, low, wide, beak-shaped,asymmetrical episome. The cells shows an oblong shape(Figure 1W, X). The specimen in Figure 1Z shows a lowepisome and a smooth cell surface, as in Apicoporus. Thecell shows a pointed antapical margin, as in Amphidiniumscissum (Figure 1Z).

amphidinium sensu lato: genus ofamphidinium scissumThe species of Amphidinium sensu stricto have a smooth cellsurface. The shape of the episome of A. scissum does not

match with the recent denition of Amphidinium sensustricto, and it also differs in the surface striation, with nelongitudinal striations that resemble the genus Gyrodinium(Figure 1AAAC).

amphidinium sensu lato: unidentified genuswith granulate surfaceFigure 1AD illustrates a specimen found in a sample examinedby scanning electron microscopy. The hyposome is slightlybifurcated. The most characteristic feature is a cell surfacecovered with homogeneous rounded granules (Figure 1AE).To the best of our knowledge, this type of surface ornamenta-tion is unknown for species of Amphidinium sensu lato.

Fig. 1. Micrographs of unarmoured sand-dwelling dinoagellates from the shore of Wimereux: (AC) Amphidinium carterae; (D, E) Amphidinium herdmanii;(F) Amphidinium aff. operculatum the arrow points to an orange spot; (G, H) Amphidinium mootonorum; (IK) Amphidinium bipes; (L) unidentiedheterotrophic Amphidinium; (M) Amphidinium incoloratum; (N) unidentied round Amphidinium; (OT) several unidentied heterotrophic species ofAmphidinium sensu lato (see Table 1); (U, V) Testudodinium sp.; (W, X) Apicoporus glaber; (Z) cf. Apicoporus sp.; (AAAC) Amphidinium scissum; (AD,AE) unidentied species with granulate surface; (AFAK) Ankistrodinium semilunatum; (AL, AM) Togula britannica; (AOAR) Togula cf. compacta; (AS)Togula inside a hyaline capsule; (AT, AU) ameboid cells of Togula; (AVAY) unidentied photosynthetic species of Amphidinium sensu lato (see Table 1);(AZ) photosynthetic species close to Amphidinium mananninii. Scale bar: 10 mm.


genus ankistrodiniumThe cells of Ankistrodinium semilunatum are oval to oblong-shaped in lateral view, strongly laterally compressed. The cin-gulum rises from its origin towards the dorsal side of the cell,then tilts downwards slightly. The cell size varies from 30 to50 mm long and from 20 to 30 mm wide. This heterotrophicspecies usually shows food particles (Figure 1AFAK).

genus togulaThe most conspicuous discolorations in the moist sands ofWimereux are due to species of the genus Togula. The cellsare highly pigmented with irregular greenish-yellow chloro-plast lobes radiating from the centre towards the periphery.The episome and hyposome are asymmetrical. The cingulumoriginates posteriorly to centrally, taking an anterior straightcourse, turning left from the apex and descending in asigmoid-straight fashion dorsally, descending in a straightcourse upon reaching the ventral side.

The genus currently accounts for three species: Togula brit-annica, T. compacta and T. jolla. Togula britannica(Figure 1AL, AM) can be identied by its larger size, and byits slimmer appearance when compared to the smallerspecies T. cf. compacta (Figure 1ANAR). The distinctionbetween T. compacta, T. jolla and Amphidinium ovum is dif-cult. The motile cells of Togula cf. compacta are broadly ellip-soidal in the dorso-ventral view, with the width of the episomea little less than the width of the hyposome, and golden-brownto dark-brown in colour. The apex and antapex are broadlyrounded, but the antapex can appear slightly pointed in thedorsal view (Figure 1ANAR). During cell division inthe genus Togula the two daughter cells initially separate atthe antapex, and the epicones are the last parts to split(Figure 1AL, AP). It was common to observe immotile cellssurrounded by a hyaline sheath. These immotile cells tendedto be broader than the motile cells (Figure 1AS). A shortperiod of metabolic movement occurred during the changefrom immotile to motile cell (Figure 1AT, AU).

unidentified photosynthetic species of

amphidinium sensu latoFigure 1AVAY represents several unidentied species thatsupercially resemble Togula. Much research is needed tofacilitate the distinction between these species under routinemicroscopical analysis. Figure 1AZ illustrates a small cell(20 mm long) with yellowish pigmentation resembling the het-erotrophic species Amphidinium mananninii. The cell body isbroadly ellipsoidal, the episome angular and the hyposomecordate with a rounded point at the antapex. The morphologyof the episome does not match with the current denition ofAmphidinium sensu stricto. The species A. mananninii isdescribed as colourless, while this specimen shows yellowish-brown pigmentation that suggests the occurrence of plastids(Figure 1AZ).

Family GymnodiniaceaeThe cells of the heterotrophic species Gymnodinium venator(Amphidinium pellucidum) are oval to oblong from theventral side. Coloured food particles and colourless lipid glo-bules were often present. The length is variable from 30 to35 mm and the width from 15 to 25 mm (Figure 2AE). Aclosely related species, Amphidinium exum, is described by

Herdman as rectangular in shape. The species Amphidiniumlatum shows a cone-shaped episome with a pointed apex.The shorter and attened episome is the main characteristicof G. venator when compared to Amphidinium latum.Figure 2F shows two specimens of different sizes which corre-spond to an unidentied species.

genus polykrikosA photosynthetic species of Polykrikos was also responsible fordiscolorations in the moist sands of the beach at Wimereux,and was more usually found in the bottom of tidal poolsduring low water. Polykrikos is a distinctive genus of pseudo-colonies consisting of eight zooids, sometimes four zooids.Currently, there are two benthic species within this genus:Polykrikos lebouriae and Polykrikos herdmaniae. The morpho-logical distinction is the presence of plastids in P. lebouriae.Both species contained red coloured food bodies of variablenumber and size that were positioned in different areas ofthe pseudo-colony. The transparency of the heterotrophicP. herdmaniae (Figure 2GK) facilitated observation of thetaeniocystnematocyst complexes that were less prominentin the photosynthetic P. lebouriae (Figure 2LO).

The photosynthetic P. lebouriae shows a high variability incell size, ranging from 40 to 90 mm long and from 20 to 50 mmwide (Figure 2LO). The pseudo-colonies were ovate in shapeand obliquely attened, with terminal zooids about half aswide as central zooids. The heterotrophic P. herdmaniae(Figure 2GK) did not form proliferations, and mainlyappeared in the proliferations of Togula and Polykrikoslebouriae.

genus spiniferodiniumThis genus was highly distinctive in its immotile stage becauseit formed a spine shell and was strongly attached to the sub-strate (Figure 2QT). In contrast, the motile form can beeasily confused with typical photosynthetic Gymnodinium-like cells (Figure 2P). Spiniferodinium appeared in sands per-manently covered by water during low tide, such as thebottom of tidal pools. The presence of Spiniferodinium wassporadic. However, its presence was always associated withlarge proliferations, where Spiniferodinium was the mainphotosynthetic species. The observations of live cells underthe microscope revealed that the switch from the swimmingform to the immotile cells is very fast. In the settlingchamber, the motile cells stopped swimming, settled on thebottom, and in less than 2 s the cell acquired a attenedround shape covered by a transparent, spiny helmet shell.The cell strongly attached itself to the surface of substratum.Without doubt, this is a mechanism to avoid re-suspensionin the water column.

It was quite easy to identify the genus Spiniferodiniumbased on the observations of the immotile spiny stages.However, it was difcult to differentiate between the twospecies described to date (the type Spiniferodinium galeiformeand S. palauense). According to the original description, S.palauense shows a thinner cell body, the cingulum is slightlydisplaced and the episome is smaller than the hyposome.The cingulum of S. galeiforme is not displaced and is locatedalmost in the middle of the cell (as reported by Horiguchiet al., 2011) (Figure 2RT). The specimens observed on thebeach of Wimereux have been assigned to S. galeiforme(Figure 2PT).


Family Amphidiniopsidaceae

genus amphidiniopsisAmphidiniopsis is the most speciose genus of armouredsand-dwelling dinoagellates, with 15 marine species, and allknown species are devoid of chloroplasts. The general appear-ance is the typical Amphidinium-like shape with a relativelysmall epitheca and a larger hypotheca. The cingulum isnearly horizontal, with the left ventral part running posteriorlyinto the sulcus (slightly ascending cingulum). The sulcusshows a characteristic curved left side and reaches the antapex.

The genus Amphidiniopsis is separated into two groups:dorso-ventrally (Figure 3) and laterally (Figure 4) compressedspecies, the latter containing the type species. The dorso-ventrally compressed species were more common in thesamples of Wimereux, and more easily recognized asmembers of Amphidiniopsis. The laterally compressedspecies were less abundant, the morphology of the sulcuswas less evident, and the identication as members of thegenus Amphidiniopsis was more difcult. Some laterally at-tened cells can be confused with heterotrophic species ofThecadinium (Figure 5).

Dorso-ventral attened species of AmphidiniopsisThe genus Amphidiniopsis on the shore of Wimereux waslargely dominated by three species: Amphidiniopsis hirsuta,

followed by A. aculeata and A. swedmarkii. These species arerounded in the posterior margin, the epitheca, slightly narrowerthan the hypotheca, is cap-like and pointed at the front part. Anapical hook or crest-like process is absent in these three species(Figure 3AL). The most common species, Amphidiniopsishirsuta, shows a row of irregular spines at its antapical cellmargin (Figure 3AF). Due to the difculties in observingthe spines, some specimens lacking the spines and having amore rounded hyposome may correspond to Amphidiniopsisswedmarkii sensu Yoshimatsu et al. (2000) or the recentlydescribed species A. konovalovae. Two prominent antapicalspines are the distinctive characteristic of Amphidiniopsis swed-markii (Figure 3GI). Amphidiniopsis aculeata is characterizedby prominent spines that are especially visible at the lateralcontour of the cell at mid focus (Figure 3JL).

The species Amphidiniopsis hexagona is characterized byits hexagonal shape and the absence of spines. We foundspecimens of two different sizes, both with a hexagonalshape. The theca was covered with small spines. The largerspecimen was 35 mm length (Figure 3MO), while thesmaller specimen (20mm in length) showed a moremarked hexagonal shape (Figure 3P, Q). The latter is namedAmphidiniopsis aff. hexagona small form.

Another group of dorsal-ventrally attened species wascharacterized by a prominent apical hook or crest-like process(Figure 3RW). We found specimens with this characteristic

Fig. 2. Micrographs of unarmoured sand-dwelling dinoagellates from the shore of Wimereux: (AD) Gymnodinium venator; (E) Gymndoinium venator (small)and an unidentied gymnodinioid species; (F) unidentied gymnodinioid species; (GK) Polykrikos herdmaniae; (LO) Polykrikos lebouriae; (PT)Spiniferodinium galeiforme. Scale bar: 10 mm.


of different sizes and shapes that ranged from oval (Figure 3R, S)to square (Figure 3T, U), and specimens with an intermediateshape and more irregular contour (Figure 3V, W). The speci-mens with an oval hypotheca are here assigned toAmphidiniopsis uroensis (Figure 3R, S). The accurate identi-cation of other specimens remains uncertain (Figure 3TW).

Amphidiniopsis cristata was one of the most distinctive taxaamong the dorso-ventrally attened species with an apicalhook. The cells are roughly square in shape and smallerthan the other dorso-ventrally compressed species ofAmphidiniopsis. The epitheca is slightly narrower than thehypotheca and shows a conspicuous apical crest-like process.There are several conspicuous but irregular antapical spines,of which the two most lateral are the largest (Figure 3XAE).

Amphidiniopsis rotundata was other dorso-ventrally at-tened species. It is difcult to recognize it as a member of

Amphidiniopsis due to the rounded shape and the lack ofother distinctive characteristics, lack of the apical hook andno antapical spines of any kind. Under routine light microscopyobservations of live specimens, the sulcus curving to the left sideand reaching the antapex was the main character that relatedthis species to the genus Amphidiniopsis (Figure 3AFAI).

Laterally attened species of AmphidiniopsisA common characteristic for the laterally compressedAmphidiniopsis species is a list-like ange that runs downinto the sulcus. This group of species includes the type ofAmphidiniopsis, A. kofoidii, and one of the problems in identi-cation is the lack of reliable records for the type species. Somerecords in the literature of A. kofoidii are currently consideredto be A. arenaria. Some lateral attened species ofAmphidiniopsis may be also misidentied with heterotrophic

Fig. 3. Micrographs of dorso-ventrally attened species of Amphidiniopsis from the shore of Wimereux: (AF) Amphidiniopsis hirsuta; (GI) A. swedmarkii;(JL) A. aculeata; (MO) A. hexagona; (P, Q) Amphidiniopsis aff. hexagona small form; (R, S) Amphidiniopsis uroensis; (TW) unidentied species ofAmphidiniopsis (see Table 1); (XAE) Amphidiniopsis cristata; (AFAI) Amphidiniopsis rotundata. Scale bar: 10 mm.


species of Thecadinium (i.e. Thecadinium acanthium andAmphidiniopsis dentata).

Amphidiniopsis arenaria is nearly rectangular (Figure 4AE),with a characteristic list-like ange that runs down into thesulcus (Figure 4C), and a conspicuous ventral spine(Figure 4E). Amphidiniopsis galericulata is smaller than otherlaterally attened species of Amphidiniopsis (about 25 mm inlength). The epitheca is slightly narrower than the hypothecaand shows a helmet-like appearance, with a conspicuousapical, hook-like spine pointing towards the dorsal side. Thereis a ventral antapical spine and a row of short irregular spine-likeprojections (Figure 4FI). We were unable to identify severalspecimens that show a Phalacroma-like shape (Figure 4JO).It is uncertain whether they belong to the genus Amphidiniopsis.

genus herdmaniaThe cells of the monotypic heterotrophic genus Herdmania areattened dorso-ventrally and rounded in ventral view, with a

distinct small, hook-like apical notch pointing to the leftlateral side of the cell. The incomplete cingulum starts at theleft ventral side, runs around the dorsal side just above thecells middle and ends at the right ventral side (Figure 4PW).The specimens of Herdmania showed different sizes andwere grouped into two populations that often coexisted(Figure 4PU). These two groups of specimens were of about25 mm (Figure 4R, S) and about 35 mm in diameter(Figure 4T, U), respectively. This suggests the occurrence of,at least, two separate species. We include here an unidentiedspecies that resembles Herdmania, but lacks the distinctiveapical notch (Figure 4X, Y).

Family Thecadiniacae: ThecadiniumThe cells of Thecadinium are attened laterally with an ovalshape, and the typical Amphidinium-like shape, a relativelysmall epitheca and a larger hypotheca. Most of the species

Fig. 4. Micrographs of Herdmania, laterally attened species of Amphidiniopsis and unidentied species from the shore of Wimereux. The arrows point theventral or antapical spine: (AE) Amphidiniopsis arenaria; (FI) Amphidiniopsis galericulata; (JO) several unidentied species close to Amphidiniopsis(see Table 1); (PW) Herdmania litoralis; (X, Y) cf. Herdmania sp. lacking the apical notch. Scale bar: 10 mm.


are heterotrophic, with the exception of a few photosyntheticspecies: Thecadinium yashimaense, T. arenarium and the typeT. kofoidii.

The cells of Thecadinium kofoidii are strongly laterally at-tened, roughly elliptical in side view and slightly pointed in theantapical margin, and show a reduced epitheca. The cell con-tains a number of yellowish chloroplasts that radiate from acentral pyrenoid (Figure 5AE).

The cells of Thecadinium neopetasatum are rather similar inshape to T. kofoidii. Thecadinium neopetasatum is heterotrophicand slightly larger (30 mm length) and rounder than T. kofoidii(Figure 5F, G). The specimen of Figure 5HK is a heterotrophicspecies of large size (45 mm), with a large episome and an asym-metrical hypotheca. In some way, the shape resembles thephotosynthetic species Pseudothecadinium campbellii. We are

unable to provide an accurate identication of this species(Figure 5HK).

The cells of Thecadinium acanthium are oval to almost rec-tangular (55 mm long and 35 mm wide). The very smallepitheca is cap-like, and there is a ventral antapical spineand a row of regular tooth-like projections (Figure 5LP). Itcould be confused with Amphidiniopsis dentata.

The cells of Thecadinidum yashimaensis are pigmentedgolden-brown. The shape is broadly ovoid and slightly later-ally compressed (Figure 5QU). In lateral view, the cellsrange from ovoid to squarish-ovoid. The cingulum is deeplyexcavated, descending and displaced approximately half ofthe cell length deep (Figure 5QU).

The cells of Thecadinium inclinatum are heterotrophic, fre-quently with large orange-red food bodies. The cell shape is

Fig. 5. Micrographs of Thecadinium from the shore of Wimereux: (AE) Thecadinium kofoidii; (F, G) Thecadinium neopetasatum; (IK) Thecadinium sp.; (LP)Thecadinium acanthium; (QU) Thecadinium yashimaense; (VY) Thecadinium inclinatum. Scale bar: 10 mm.


oval to slightly rectangular, with a laterally asymmetricalepitheca smaller than the hypotheca, about one fourth toone-third of the cell length. The cells are larger than otherspecies of Thecadinium, ranging from 55 to 80 mm long and40 to 60 mm deep (Figure 5VY).

Family incertae: Genus SabulodiniumThe cells of Sabulodinium undulatum are laterally attened,more or less oval with a truncated apex in lateral view, andelongatedelliptical in ventral view (Figure 6AO). Thelower dorsal margin of the cell is either slightly irregular(undulating) with rounded edges, or has more pronouncedundulations containing one spiny dorsal edge or two spinyedges one dorsal and one posterior. The cingulum isdeep and not displaced, and the sulcus is positioned on theright lateral side of the cells. This is a monotypic genus,although the morphological differences between the speci-mens suggests the occurrence of undescribed species. Thereare two main morphologies in the large specimens:Sabulodinium undulatum var. glabromarginatum for moreround specimens with smooth/straight dorsal hypothecaborder (Figure 6AG) and Sabulodinium undulatum var.undulatum, where the antapical contour could form onespiny dorsal edge or two spiny edgesone dorsal and one

posterior (Figure 6HM). A third morphology was foundSabulodinium sp. was a smaller species with three spinyedges (Figure 6N, O).

Family incertae: PlanodiniumThe cells of this heterotrophic genus are laterally compressedwith an oval shape. The cingulum is horizontal. The epithecais much reduced and narrower than the hypotheca. Thesurface of the hypotheca is ridged (Figure 6PY).

Family of Sinophysis: Genus SinophysisThese species show dinophysoid morphology, laterally at-tened, with a minute crown-like epitheca that resembles theplanktonic genus Dinophysis. The genus Sinophysis containsseven species; ve species have been described from temperatewaters, and two species from tropical coasts. The species oftemperate waters show a smooth thecal surface, with theexception of S. verruculosa. All the species described fromtemperate waters were found in our sampling area(Figure 7). The cells of Sinophysis ebriola (about 3545 mm)are roughly oval. The small episome is about 912 mm wide(dorso-ventrally), surrounded by a wide collar and slightlytilted back to the dorsal side (Figure 7AG). The species

Fig. 6. Micrographs of Sabulodinium and Planodinium from the shore of Wimereux: (AG) Sabulodinium undulatum var. glabromarginatum; (HM)Sabulodinium undulatum var. undulatum; (N, O) Sabulodinium sp. small form the arrows point to the spiny edges; (PY) Planodinium striatum. Scalebar: 10 mm.


S. verruculosa is distinguished from S. ebriola by the verrucoseornamentation of the theca. This diagnostic characteristic isnot easy to observe under light microscopy. We glimpsedsome kind of thecal ornamentation in the specimen ofFigure 7H. This specimen, with a more circular cell shapeand wider episome than S. ebriola, we identied as S. cf. ver-ruculosa (Figure 7H). Sinophysis sp. corresponded to a speci-men with an antapical lobule in the dorsal side (Figure 7I).

The cells of Sinophysis grandis are large (about 5060 mm),roughly rectangular, with roundish edges. The episome is thelargest found in Sinophysis, surrounded by a weakly developedsmooth girdle list, and less tilted to the dorsal side (Figure 7JQ).The specimens can be divided into two groups according totheir size. The larger specimens (5560 mm in length) arecloser to the original description of S. grandis, with morequadrangular cell shape and wider episome (Figure 7NQ).Other specimens identied as Sinophysis aff. grandis aresmaller (5055 mm in length) with a more oval cell shapeand narrower episome (Figure 7JM).

The cells of Sinophysis stenosoma are oblong ellipsoidal,epitheca cylindrical, crown-like, and 58 mm wide. The

small cylindrical, crown-like episome is notably small com-pared with the other Sinophysis species. It is surrounded bya well-developed smooth girdle list of the hypotheca andslightly tilted back to the dorsal side (Figure 7R, S). Thecells Sinophysis minima are very small (20 mm long),roughly rectangular to almost square, with more or lessround edges. The cylindrical epitheca is small, 57 mmdeep, constituting about one-third of the hypotheca depth,and is notably asymmetric (Figure 7TV). This species cango easily unnoticed due to its small size and transparency.

Family incertae: Genus AdenoidesThe cells of Adenoides eludens are asymmetrical, oval toround, slightly attened laterally (3035 mm). The minuteepitheca is cup-shaped, depressed and scarcely visible. Thecingulum is almost at the anterior end of the cell, completelyencircling the epitheca and meeting without displacement.The sulcal area is on the anterior third of the cell, neitherextending onto the epitheca nor reaching the antapex, and is

Fig. 7. Micrographs of Sinophysis from the shore of Wimereux: (AG) Sinophysis ebriola; (H) Sinophysis cf. verruculosa; (I) Sinophysis sp. with dorsal lobule;(JM) Sinophysis aff. grandis; (NQ) Sinophysis grandis; (R, S) Sinophysis stenosoma; (TV) Sinophysis minima. Scale bar: 10 mm.


slightly depressed (Figure 8AF). The cytoplasm containsbrown chloroplasts (Figure 8AD).

Prorocentraceae sensu stricto: GenusProrocentrumThe genus Prorocentrum contains numerous benthic species,mainly epiphytes in macroalgae. However, the diversity inthe sands of Wimereux was low, restricted to a commonspecies, Prorocentrum fukuyoi. The cells are oval to ovalelongate (40 mm long and 35 mm wide). The left valveshows a broad noticeable depression in the anterior region.The right valve is asymmetrical; its right upper corner is obli-quely truncate and has a long wedge-shaped indentationoblique to the right, with a small ange on the right side(Figure 8GR). This ange usually appears under light micro-scope as a spine 36 mm long (Figure 8R). The valve surface issmooth. Two pore sizes are present, one approximately of0.3 mm, and a second approximately of 0.1 mm. The smaller-sized pores are present around the periphery of the valve andscattered in the centre. The larger pores are scattered over thevalve, sometimes in short (of three pores) radial rows toward

the centre (Figure 8NQ). It was common to nd specimenswith deformations in the shape of the valve (Figure 8JM),and specimens under division inside a hyaline capsule(Figure 8I). This species is closely related to Prorocentrumemarginatum, which is rounder, with a wider apical regionand with a left valve less deeply indented than P. fukuyoi.Both species show a smooth valve surface with small andlarge pores but the pattern generally radiates more clearlyfrom the centre in P. emarginatum than in P. fukuyoi (asexplained in Murray et al., 2007).

Family incertae: Genus KatodiniumThe genus Katodinium contains small cells which characteristi-cally have a much longer and wider episome than hyposome.They were rst classied as unarmoured dinoagellates.However, the cell is covered by a delicate theca which containsthin plates. In the sands, they appear sporadically and in hugenumbers. The identication of these small and fast-moving cellsfrom live material is difcult.

The cells of Katodinium glandula are ovoid and attened,somewhat asymmetrical. The episome is helmet-shaped with

Fig. 8. Micrographs of Adenoides, Prorocentrum and Katodinium from the shore of Wimereux: (AF) Adenoides eludens; (GR) Prorocentrum fukuyoi; (SW)Katodinium glandula; (X, Y) Katodinium asymmetricum. Scale bar: 10 mm.


the apex produced into a sharp point, which is bent backwardsso as to lie closely along the surface. The cingulum is post-median, deeply impressed; its ends meeting without displace-ment. The hyposome is only half the height of the episome.The cells are colourless with some refractive granules or redbodies (Figure 8SW). The cells of Katodinium asymmetri-cum are smaller and with an irregular contour of the hypo-some (Figure 8X, Y).

D ISCUSS ION

The thecate sand-dwelling dinoagellates tend to show at-tened morphologies, usually rounded or oval shapes and lacklong spines or protuberances. In other groups such as eugle-noids, the metaboly movement favours migration betweenthe sand grains (Palmer & Round, 1965). Another importantaspect is the adhesion to the substrate in order to avoidre-suspension in the water column. This phenomenon isevident for Spiniferodinium, which is able to change its mor-phology in a few seconds and to adhere strongly to the sub-strate. When compared to observations of planktonic species,sand-dwelling dinoagellates such as Sinophysis orSabulodinium are able to strongly attach to the bottom ofthe settling chamber. In sand-dwelling diatoms the productionof extracellular polymeric substances has been described,which favour adhesion to the sand grains, and that also playsan important role in the cohesion of the sediments on sandybeaches (Underwood et al., 2004). The mechanism of adhesionto the sand particles remains under-investigated for most ofthe sand-dwelling dinoagellates.

When compared with the planktonic dinoagellates, theprimary production of the sand-dwelling photosyntheticdinoagellates is restricted to shorter periods (during thelow tide in daylight). The photosynthetic species (Togula brit-tanica, T. cf. compacta, Amphidinium herdmanii) form denseproliferations concentrated in the upper few millimetres ofthe moist sands (see video at: http://www.youtube.com/watch?v=BEjD-1wvBTs). High primary production rates canbe attributed to them, considering the high rates alreadyrecorded in the sands of Wimereux (Spilmont et al., 2005;Hubas et al., 2007). The sandy shore of Wimereux seems tobe a high favourable environment for microphytobenthicprimary production, and adaptation to the photosyntheticmetabolism. For example, all the planktonic species ofPolykrikos are well adapted to heterotrophy, with the develop-ment of specialized ejective organelles for prey capture. Theonly known species with plastids, Polykrkios lebouriae, isfound in the sands (Figure 2LO).

This study reports numerous species that have never beenreported in the area. The rst nding of a species is often con-fused with the arrival of an invasive species. In the lastdecades, marine invasive species have received increasingattention. In a recent review, Dewarumez et al. (2011) ident-ied 40 non-indigenous marine species in the easternEnglish Channel and the southern North Sea, among which30 were from Asia. They are mainly macroscopic species,and the few examples of invasive protists are doubtful(Gomez, 2008; Gomez & Souissi, 2010). While it is easier totrack the occurrence of newcomers amongst the macroscopicspecies, it is more difcult to do so for protist species, due tothe lack of previous inventory studies. It is even more difcultto evaluate the arrival of newcomers in the case of the

sand-dwelling dinoagellates. While marine biology studieson the coast of Wimereux began in 1874, until now, thesand-dwelling dinoagellates had not been examined. In thisstudy the species Amphidiniopsis hexagona, A. rotundata,A. uroensis and Sinophysis minima are reported for the rsttime in the Atlantic Ocean and the European seas. To datethese species were only known from the Pacic Ocean.However, in no way should these species be consideredexotic; they might just have been unnoticed until now dueto the scarce coverage of studies in the microbenthos. Forexample, Amphidiniopsis rotundata is difcult to recognizeas a member of Amphidiniopsis, and Sinophysis minima isvery small and transparent and easily goes unnoticed for non-trained observers. Amphidiniopsis hexagona or A. uroensis canbe confused with more common Amphidiniopsis species suchas A. hirsuta. Most of the literature on sand-dwelling dinoa-gellates is restricted to the original descriptions, with detailedillustrations of the species by scanning electron microscopy.The literature is dispersed, with few light microscopy picturesand often from xed material.

Other species were also rst described in the Pacic Ocean,although recently reported in the Atlantic Ocean. They arecandidates to be included in the list of non-indigenousspecies in Europe based only on the exotic etymology of thespecies epithets. For example, Prorocentrum fukuyoi wasdescribed in 2007 from Japanese and Australian coastalwaters (Murray et al., 2007), but it is also a common specieson the European Atlantic coasts (Laza-Martnez et al.,2011). In the pioneer studies on sand dwelling dinoagellates,Herdman (1924) reported this species as Exuviaella marina,and it was further illustrated by Dragesco (1965) andPaulmier (1992) from French coasts. Other species rstdescribed from the Pacic Ocean, such as Spiniferodiniumgaleiforme and Thecadinium yashimaense, are responsiblefor important proliferations. However, these proliferationsare sporadic and, consequently, they might easily have beenby the few previous studies in European coastal waters.Amphidinium mootonorum was described from the SouthPacic Ocean (Murray & Patterson, 2002); on Europeancoasts this species can be easily confused withTestudodinium testudo, which was described from theBritish Isles by Herdman (1924).

Although the number of species of sand-dwelling dinoa-gellates has largely increased in the last 15 years, this seemsto be only the tip of the iceberg of the still unknown diversity.For example, the genus Amphidiniopsis accounted for fourmarine species in 1999, while there are currently morethan 16 described species (Gomez, 2012). The usual mor-phology of the sand-dwelling dinoagellates results in ahigh percentage of monotypic genera, restricted to a singlespecies, such as Sabulodinium or Herdmania. However, theevidences reveal that these genera are not monotypic(Figures 4PW, 6N, O). The records of Sinophysis grandismay pool two different species (Figure 7JQ). The taxonomyof the unarmoured dinoagellates of Amphidinium sensu latohas been revised in recent years, with the erection of severalnew genera. This split is still incomplete (i.e. Amphidiniumscissum), and numerous heterotrophic species still need tobe described (Figure 1). In addition, it is necessary to applya standardized methodology for the ecological studies. Thepresent study constitutes a rst step in investigating thediversity, ecological role and adaption mechanisms ofthe sand-dwelling dinoagellates.


ACKNOWLEDGEMENTS

We appreciate the improvements of an anonymous referee.

F INANC IAL SUPPORT

F.G. was supported by a UL1 post-doctoral grant and a CNRSconvention of research. F.G. is currently supported by theBrazilian Conselho Nacional de Desenvolvimento Cientcoe Tecnologico (grant number BJT 370646/2013-14).

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Correspondence should be addressed to:F. GomezLaboratory of Plankton SystemsOceanographic Institute, University of Sao PauloPraca do Oceanograco 191, sala 100Sao Paulo, SP 05508-120, Brazilemail: [email protected]


High diversity of dinoflagellates in the intertidal sandy sediments of Wimereux (north-east English Channel, France)INTRODUCTIONMATERIALS AND METHODSRESULTS

&emphasis type=&emphasis type=HETEROTROPHIC SPECIES OF &emphasis type=GENUS &emphasis type=GENUS &emphasis type=&emphasis type=&emphasis type=GENUS &emphasis type=GENUS &emphasis type=UNIDENTIFIED PHOTOSYNTHETIC SPECIES OF &emphasis type=Outline placeholderFamily Gymnodiniaceae

GENUS &emphasis type=GENUS &emphasis type=Outline placeholderFamily Amphidiniopsidaceae

GENUS &emphasis type=Dorso-&?h 0,14;ventral flattened species of &emphasis type=Laterally flattened species of&emphasis type=GENUS &emphasis type=Family Thecadiniacae: &emphasis type=Family incertae: Genus &emphasis type=Family incertae: &emphasis type=Family of &emphasis type=Family incertae: Genus &emphasis type=Prorocentraceae &emphasis type=Family incertae: Genus &emphasis type=DISCUSSIONACKNOWLEDGEMENTSFINANCIAL SUPPORTREFERENCES

gomez artigas sand-dwelling dinoflagellates 2014

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