From the Indian Ocean Maria Saburova, Igor Polikarpov and Faiza Al-Yamani Kuwait Institute for Scientiﬁc Research, PO Box 1638, Salmiyah-22017, Kuwait

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Marine Biodiversity Records, page 1 of 7. # Marine Biological Association of the United Kingdom, 2013 doi:10.1017/S1755267213000225; Vol. 6; e46; 2013 Published online First records of noctilucoid dinoﬂagellates Abedinium dasypus and Scaphodinium mirabile (Dinophyceae) from the Indian Ocean maria saburova, igor polikarpov and faiza al-yamani Kuwait Institute for Scientiﬁc Research, PO Box 1638, Salmiyah-22017, Kuwait

The occurrence of noctilucoid dinoflagellates Abedinium dasypus and Scaphodinium mirabile is reported for the first time from the Indian Ocean (Kuwait’s waters, north-western Arabian Gulf). The morphology of live cells is described on the basis of light microscopic examination and photographically documented for both species. The world distribution of these dinoflagellates is reviewed.

Keywords: Abedinium, Dinophyceae, Indian Ocean, Kuwait, Noctilucales, phytoplankton, Scaphodinium

Submitted 3 June 2012; accepted 17 February 2013

INTRODUCTION MATERIALS AND METHODS

The marine noctilucoid dinoflagellates Abedinium dasypus Sampling site (Cachon & Cachon-Enjumet) Loeblich & Loeblich III, 1966 and Scaphodinium mirabile Margalef, 1963 are rarely reported Kuwait’s marine area occupies the north-western edge of the worldwide and scarcely documented in the literature due to Mesopotamian shallow shelf of the northern part of the difficulties with their recognition from preserved samples. Arabian (Persian) Gulf, which is a marginal sea connected Despite their large size and characteristic shapes, these dino- to the Indian Ocean via the Strait of Hormuz. Kuwait’s flagellates with non-typical modified morphologies are often waters are shallow, rarely deeper than 30 m, and generally underestimated or absent from most of phytoplankton analy- well-mixed year-round, with mean salinity of 41.6. The sis (Larsen & Sournia, 1991;Go´mez & Furuya, 2004). mean annual seawater temperature is 23.88C and ranges Kuwait’s waters have been monitored for phytoplankton from 30.58C (up to 368C) in July and August to 148C (down community composition and density for a long time, and to 11.98C) in January–February (Al-Yamani et al., 2004). the phytoplankton diversity has been recently well documented based on Lugol’s preserved material (Al-Yamani et al., Sampling 2004; Al-Kandari et al., 2009). Among Noctilucales, Noctiluca scintillans (Macartney) Kofoid & Swezy, 1921 has A regular sampling programme was carried out from 2010 to been reported from Kuwait (Al-Kandari et al., 2009). A 2012 throughout Kuwait’s waters using speedboats. Systematic recent phytoplankton survey was conducted on the basis of monthly monitoring of the poorly-preserved phytoplankton unpreserved samples examination with a focus on the poorly- fraction was performed by sampling at seven sites, whereas preserved athecate dinoflagellates in Kuwait’s waters. Careful some additional localities were sampled occasionally. Water analysis of the freshly collected samples revealed two morpho- samples from the surface layer (0–1 m) were collected with a logically modified dinoflagellates belonging to the family 5 l Niskin bottle (General Oceanics, USA), stored in 1 l plastic Leptodiscaceae Taylor, 1987 (order Noctilucales Haeckel, bottles and brought directly to the laboratory in a cooler with ice. 1894)—Abedinium dasypus and Scaphodinium mirabile. The occurrence of these species has not been previously noted for Kuwait, or for the Arabian Gulf and the Indian Ocean as Sample processing a whole. In this paper, previous records of S. mirabile and Samples were either settled during 2–3 hours or gently concen- A. dasypus are summarized and new data on the distribution trated by centrifugation (200 revolutions per minute, 3 of these dinoflagellates within Kuwait’s waters are provided. minutes). Concentrated samples were scanned using an inverted Leica DMIL microscope (Leica, Wetzlar, Germany) at 50–200× magnification to estimate the phytoplankton composition. For detailed examination, cells were isolated by

Corresponding author: micropipetting and transferred to a glass slide in preparation M. Saburova for high-magniﬁcation photomicroscopy. Cells were examined Email: [email protected] and photographed using an upright Leica DMLM microscope

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(Leica, Wetzlar, Germany) equipped with Nomarski differen- description tial interference contrast optics and DFC 320 colour digital In non-folded view cells were extremely flattened, elongated, camera at 400–1000× magnifications. Cell dimensions were 239–251 mm long and 77–80 mm wide (N ¼ 2), strongly measured from images using Leica Application Suite v. 3.7 bilaterally symmetrical with slightly folded lateral margins (Leica Microsystems (Switzerland) Ltd) software. Two speci- (Figure 1A). Each cell end was terminated by distinct exten- mens of Scaphodinium mirabile and five specimens of sion. One extension (here considered as anterior) was Abedinium dasypus were measured. All observations presented narrow, approximately 34–35 mm long, slightly widened to here are based on light microscopy examination of live cells that the end and arranged with three small processes (one of were isolated from freshly collected samples. which was centrally located, while the other two were periph- eral) (Figure 1A, D). Reverse extension (here considered as posterior) was wider and shorter than the anterior one, approxi- RESULTS mately 30–32 mm long, bilobate (Figure 1A, C, E–G). There was the cytoplasm swelling below the median, where large During a three-year course of regular sampling in Kuwait’s elongate encapsulated nucleus was located (Figure 1A,E,F). waters, over which time approximately 180 samples were col- The cytoplasm was reticulated (Figure 1A, B, E) due to numer- lected, cells of Scaphodinium mirabile and Abedinium dasypus ous myofibrils forming a uniform network. One small pigmen- occurred extremely rarely, they were only found on several ted body (food particle?) was observed near the nucleus in both sampling occasions in 2010 and 2012, mostly in the offshore specimens examined (Figure 1A, B, E). Longitudinal flagellum area. Eight specimens of S. mirabile were found once was well visible, long (but shorter than the cell length) (Table 1) in the surface layer sampled on 30 November (Figure 1C), originated from the cytoplasm swelling, initially 2010 in near-shore waters with temperature of 22.88C and sal- curving along one side of the nucleus and then extended straight inity of 42.1. The occurrence of A. dasypus was recorded on along longitudinal cell axis within flagellar canal to the bilobate several occasions in winter and spring 2012 throughout the extension (Figure 1E–G). Transverse flagellum was observed offshore waters with temperatures ranging from 158Cto only in folded cells (Figure 1B). Chloroplasts and trichocysts 18.48C and salinity range from 42.1 to 43.2 (Table 1). were not seen. Live cells of these athecate dinoflagellates were extremely Live cells observed were more or less expanded, sliding delicate, and they disintegrated easily during manipulation, slowly with narrow extension pointing forward due to longi- but two specimens of Scaphodinium mirabile and five speci- tudinal flagellum oscillations. The lateral margins of the cells mens of Abedinium dasypus were successfully isolated and were strongly folded during the active movement. Being dis- their morphology was examined using high-magnification turbed, the cells folded rapidly into a ring on one of its light microscopy (LM) under bright field (BF) and differential sides, extension against extension. interference contrast (DIC) illumination. Genus Abedinium Loeblich & Loeblich III, 1966 Abedinium dasypus (Cachon & Cachon-Enjumet) Loeblich & Loeblich III, 1966 (Figures 2 & 3) systematics Class DINOPHYCEAE West & Fritch, 1927 synonym: Order NOCTILUCALES Haeckel, 1894 Leptophyllus dasypus Cachon & Cachon-Enjumet, 1964. Family LEPTODISCACEAE Taylor, 1987 Genus Scaphodinium Margalef, 1963 references: Scaphodinium mirabile Margalef, 1963 ´ (Figure 1) Cachon & Cachon-Enjumet, 1964;Gomez et al., 2010. description synonym: Cells were feather-shaped, extremely flattened, 163–251 mm Leptospathium navicula Cachon & Cachon-Enjumet, 1964. long and 76–94 mm wide (N ¼ 5), strongly bilaterally symmetrical (Figures 2A, D, H & 3A). Anterior part of the cell references: that points in the direction of the cell locomotion was termi- Margalef, 1963; Cachon & Cachon-Enjumet, 1964;Go´mez & nated by long (52–57 mm), narrow (5–6 mm wide), and Furuya, 2004. mobile tentacle with an orange-pigmented distal part

Table 1. Occurrence of Scaphodinium mirabile and Abedinium dasypus in Kuwait waters during 2010–2012 including geographical coordinates, dates, depth of the sampling site, water temperature of the surface layer, salinity, volume of sample and cell concentrations for each record of the species.

Sampling site Date Depth, m Water temperature, Salinity Examined Abundance, cells per 8C volume, litre examined volume

S. mirabile A. dasypus

29810′01′′N48810′05′′E 29 November 2010 21 22.8 42.1 1 8 2 29815′05′′N48823′57′′E 5 February 2012 15 16.3 43.2 5 2 2 29803′44′′N48830′20′′E 14 February 2012 29 15.2 42.2 2 2 4 28850′02′′N48846′57′′E 20 February 2012 16 15.0 42.1 1 2 1 28850′02′′N48846′57′′E 1 April 2012 20 18.4 41.5 1 2 2

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Fig. 1. Light micrographs of Scaphodinium mirabile recorded from Kuwait waters in November 2010: (A) cell in non-folded view showing general appearance; (B) folding cell; (C, E, F) detail of the posterior cell end in folded view during swimming (C), and in non-folded view (E, F); (D) detail of the anterior cell end; (G) detail of the bilobate extension. Arrows point to the pigmented body (Pb); longitudinal (Lf) and transverse (Tf) ﬂagella, ﬂagellar canal (Fc) and nucleus (N). A–G, LM, BF. Scale bars: A–C, 20 mm; D, 5 mm; E–G, 10 mm.

(Figures 2A, E, H, L & 3A–D). Opposite cell end (here con- swelling, radiating from the longitudinal cell axis to the cell sidered as posterior) was broadly rounded. Cell edge was bor- margins (Figure 2A, H, I). Chloroplasts were not seen. dered by a narrow undulated margin, 4–5 mm wide (Figures Freshly collected cells swam slowly, moving forward along 2A, F, H, J & 3J). There was almost centrally located fusiforme the longitudinal axis due to longitudinal flagellum oscillations cytoplasm swelling, 63–84 mm long and 47–56 mm wide, and feeling the space ahead with the tentacle. Cells were able containing the nucleus, food vacuoles and trichocysts to contract suddenly when the surrounding water was dis- (Figures 2A, E, D, H–K & 3A, B, G). Nucleus was large, turbed mainly due to contraction of the cell margins encapsulated, and elongate to roundish, 23 × 25–26 mm (Figure 3J–L). Being disturbed, cells rolled up into a ball (Figures 2H–J & 3G). Single large pigmented body (food par- immediately and folded tentacle inside (Figure 2B, C). The ticle) was often located near nucleus (Figures 2A,D,H–K& discharged trichocysts ejecting numerous long filaments 3G). Numerous elongate, clavate trichocysts were radiating were observed in the rolled cells just before lysis (Figure 2G). out from the centre of the cytoplasm swelling (Figures 2A, H, J & 3A, B, G–I). The bigger ones were up to 15–24 mm long, whereas smallest trichocysts were 7–9 mm long DISCUSSION (Figure 3H, I). Cytoplasm was transparent and densely granu- lated (Figures 2A, H–J & 3A, B, E, F, J). Cells were biflagellate. The noctilucoid dinoflagellates (order Noctilucales) constitute One of the flagella was included in the cytoplasm along its an important component of the marine heterotrophic plank- entire length, arising from the proximal part of the cytoplasm ton. Among them, Noctiluca scintillans is well investigated swelling, and lay throughout the cytoplasm along longitudinal due to its worldwide distribution and capacity to form red axis up to end of tentacle within tube-like flagellar canal tides (e.g. Elbra¨chter & Qi, 1998). In contrast to N. scintillans, (Figures 2H, L & 3A, B, E, F). The other flagellum (longitudi- a number of the noctilucoid genera are rarely encountered, but nal) was partially internal, originated from the distal part of on the basis of their descriptions they should be readily recog- the cytoplasm swelling and continued along longitudinal cell nizable (Sournia, 1986; Larsen & Sournia, 1991), including axis; its proximal part lay throughout tube-like flagellar Scaphodinium and Abedinium. canal, protruding with its distal part from the posterior cell Worldwide records for Scaphodinium mirabile are scarce. end (Figures 2H–J & 3C, D). On one occasion both flagella Over half of the documented records for this species are were seen protruding from the posterior cell end just before restricted to the Mediterranean Sea and adjacent waters of cell lysis (Figure 3L, M). Myofibrils were arranged to form the Marmara and Black Seas, and the eastern part of the two zones of oblique striation above and below the cytoplasm North Atlantic Ocean (Table 2). In the Mediterranean Sea,

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Fig. 2. Light micrographs of Abedinium dasypus recorded from the north-western offshore Kuwait waters on 20 February 2012: (A) cell in non-folded view showing general appearance; (B–D) the same cell in folded (B, C) and non-folded (D) view; (E, F) the same cell in lateral view at the different focal planes; (G) folded cell just before lysis showing numerous long filaments (indicated by arrows) from discharged trichocysts; (H, I–K) other cell in non-folded view showing general appearance (H), and detail of the posterior cell end (I–K), numerous trichocysts (black arrows) and undulated cell margin (white arrows) are visible; (L) detail of the anterior cell end showing the tentacle with pigmented distal end (indicated by arrow). Pigmented body (Pb), distal flagellar canal (Dfc), longitudinal flagellum (Lf), nucleus (N), and tentacle (Tn) are indicated by arrows. A–D, G, LM, BF; E, F, H–L, LM, DIC. Scale bars: A–H, 20 mm; I–L, 10 mm.

the occurrence of S. mirabile is variable among sub-basins. of the basin (Table 2), it has been recorded as commonly While the species has been reported mostly from the coastal occurred throughout the open Mediterranean waters (Go´mez, waters of the Ligurian and Balearic Seas in the western part 2010). Recently, the occurrence of S. mirabile in the Paciﬁc

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Fig. 3. Light micrographs of Abedinium dasypus recorded from the southern offshore Kuwait waters on 14 February 2012: (A, B) the same cell in non-folded view showing the different position of the tentacle; (C, D) detail of the anterior cell end showing the tentacle, the proximal flagellar canal and intracytoplasmic flagellum within flagellar canal (arrow); (E, F) detail of the distal flagellar canal; (G, H) detail of the fusiforme cytoplasm swelling showing numerous trichocysts (indicated by arrows); (I) detail of the trichocyst; (J) detail of the marginal area in non-folded cell showing the undulated cell margin (white arrow); (K, L) the same cell in folded view showing contracted cell margins (white arrows) and both flagella (black arrows) protruding from the posterior cell end; (M) detail of the posterior end in folded cell showing both flagella (black arrows) protruding from the distal flagellar canal. Pigmented body (Pb), distal flagellar canal (Dfc), proximal flagellar canal (Pfc), longitudinal flagellum (Lf), nucleus (N), and tentacle (Tn) are indicated by arrows. A–I, LM, BF; J–M, LM, DIC. Scale bars: A, B, 20 mm; C–H, G–M, 10 mm; I, 5 mm.

Ocean has been documented, and its spatial distribution in has been originally described from the Villefranche Bay various Pacific localities has been mapped (Go´mez & (north-west Mediterranean Sea) as Leptophyllus dasypus Furuya, 2004, 2005;Go´mez et al., 2007). Moreover, a few (Cachon & Cachon-Enjumet, 1964). Due to the illegitimate specimens that morphologically differed from the type generic name which is preoccupied under the International species of Scaphodinium were found among Pacific popu- Code of Zoological Nomenclature, the genus was further lation (Go´mez & Furuya, 2005) that casts doubt on the mono- renamed as Abedinium (Loeblich & Loeblich III, 1966; specific status of this genus. Despite the limited number of the Fensome et al., 1993). After the initial record, Margalef worldwide records, S. mirabile can be considered as cosmopo- (1973) reported this species from the eastern part of the litan species, being found in three oceans and in both northern North Atlantic Ocean, and several specimens of A. dasypus and southern hemispheres (Table 2), with the highest occur- were found in French coastal waters of the north-west rence in the Mediterranean Sea that could perhaps be attribu- Mediterranean Sea (Marseille and Banyuls-sur-Mer) much ted to the historical tradition of taxonomic studies and later (Go´mez et al., 2010). hydrographical peculiarity of the Mediterranean waters (e.g. Despite the intensive sampling throughout Kuwait’s waters Go´mez, 2006). during three years combined with the thorough examination Known records of Abedinium dasypus are much rarer and of freshly collected unpreserved samples, the observations of more geographically restricted (Table 2). This dinoflagellate Scaphodinium mirabile and Abedinium dasypus were extremely

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Table 2. Worldwide distribution of Scaphodinium spp. and Abedinium dasypus, as found in this and previous studies.

Locality Source

Scaphodinium mirabile Black Sea North-west, Sevastopol Bay Gavrilova, 2012∗∗ West, Bulgarian coast Stoyanova, 1999 Sea of Marmara Buÿu¨kçekmece Bay Balkis, 2000, 2003 Mediterranean Sea North-west, Ligurian Sea Cachon & Cachon-Enjumet, 19641,∗,∗∗;Le´ger, 1971; Go´mez & Gorsky, 2003; Lasternas et al., 2008 North-west, Balearic Sea Go´mez et al., 2010 West, Balearic Sea Margalef, 1963∗; 1969a, b East, Levantine Sea Abboud-Abi Saab, 1989 Balearic–Tyrrhenian–Ionian–Levantine Seas Go´mez, 2010∗∗ Atlantic Ocean North-east, off north-west Africa, North African Margalef, 1973 upwelling system Pacific Ocean North-west Kuroshio Current Go´mez & Furuya, 2004∗∗, 2005 Philippine Sea Sagami Bay, off Oshima Island Go´mez & Furuya, 2005 Sulu Sea Celebes Sea Equatorial Western Pacific Warm Pool Upwelling Region South-east Marquesas Islands Go´mez et al., 2007 Peru´ –Chile Current Tropical and South Pacific Gyre Indian Ocean North-west Arabian Gulf, Kuwait’s waters This study∗∗ Scaphodinium spp. Pacific Ocean North-west, Kuroshio Current Go´mez & Furuya, 2005∗∗ South-east, Tropical and South Pacific Gyre Go´mez et al., 2007 Abedinium dasypus Mediterranean Sea North-west, Ligurian Sea Cachon & Cachon-Enjumet, 19642,∗,∗∗ North-west, Balearic Sea Go´mez et al., 2010∗∗ Atlantic Ocean North-east, off north-west Africa, North African Margalef, 1973 upwelling system Indian Ocean North-west Arabian Gulf, Kuwait’s waters This study∗∗

1, recorded as Leptospathium navicula; 2, recorded as Leptophyllus dasypus; ∗, record was illustrated by line drawings; ∗∗, record was illustrated by microphotographs.

rare and cells of these species occurred in very low concen- Our observations of cells morphology in Scaphodinium trations, sometimes with a density of less than 1 cell per litre mirabile and Abedinium dasypus were similar to those pre- (Table 1). Records of A. dasypus specimens were numerous in viously described and illustrated for these species (Margalef, comparison with those of S. mirabile, whereas the latter was 1963; Cachon & Cachon-Enjumet, 1964; Sournia, 1986; more abundant per sample (Table 1). While the identification Larsen & Sournia, 1991; Fensome et al., 1993;Go´mez & of these dinoflagellates is relatively easy due to their distinct Furuya, 2004;Go´mez et al., 2010). Although not previously morphology, these species could be easily overlooked during reported for Abedinium dasypus, we were able to document sample analysis because of their rarity and extreme delicacy. the specimen with two flagella protruding from the posterior Most of the Noctilucales have a predominantly tropical to cell end, which indicates that the intracytoplasmic character of warm-temperate distribution (Cachon & Cachon, 1967, 1969; one flagellum in A. dasypus could be considered as a variable Gomez & Furuya 2005, 2007). The northernmost records of feature. This study presents photographic records of both Scaphodinium mirabile from temperate waters of the Black Sea species from the Indian Ocean region for the first time. (Stoyanova, 1999;Gavrilova,2012) and in the vicinity of the The observations of Scaphodinium mirabile and Abedinium Kuroshio Current in the north-west Pacific Ocean (Gomez & dasypus from this study can be considered as new records for Furuya, 2004, 2005) coincided with warm seasons. Kuwait. To our knowledge, this is the first time that S. mirabile Our observation of Scaphodinium mirabile and Abedinium and A. dasypus have been observed in the Indian Ocean, and dasypus in subtropical Kuwait waters supported previous this indicates an extension of the spatial distribution of these studies that have considered these species as thermophilic. species from that previously known. Because of the extremely rare occurrence of S. mirabile and A. dasypus in Kuwait waters, there are not enough data to make a conclusion about the spatial distribution and seasonal ACKNOWLEDGEMENTS prevalence pattern of these dinoflagellates, however, records of these species coincided with period of moderate water temp- We acknowledge the valuable help of Mr Alan Lennox eratures (15–22.88C: Table 1) and were associated mainly (Kuwait Institute for Scientific Research, Kuwait) during the with the offshore area. extensive field sampling. The authors thank Mr Alok Nigam

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Saburova Go´mez F. and Furuya K. (2004) New records of Scaphodinium mirabile Kuwait Institute for Scientific Research (Dinophyceae), an unnoticed dinoflagellate in the Pacific Ocean. PO Box 1638, Salmiyah-22017, Kuwait Phycological Research 52, 13–16. email: [email protected]