J Biosci Vol. 43, No. 1, March 2018, pp. 59–74 Ó Indian Academy of Sciences DOI: 10.1007/s12038-018-9730-0

Thalassiosira mala (Bacillariophyta), a potentially harmful, marine from Chilka Lake and other coastal localities of Odisha, India: Nomenclature, frustule morphology and global biogeography

1 2 3 AKSHINTHALA KSKPRASAD *, JAMES ANIENOW and ERIC LOCHNER 1Department of Biological Science, Florida State University, Tallahassee, FL 32306–4370, USA 2Department of Biology, Valdosta State University, Valdosta, GA 31698–1500, USA

3Department of Physics, Florida State University, Tallahassee, FL 32306–4351, USA

*Corresponding author (Email, [email protected]) MS received 7 August 2017; accepted 14 December 2017; published online 18 January 2018

Our examination of net collected from coastal localities in Odisha on the east coast of India, including Chilka Lake, Chandrabhaga Beach and Puri, in December 2015, revealed the overwhelming dominance of mala, a gelatinous colony-forming, potentially harmful, marine planktonic diatom. The large numbers of cells allowed us to observe details of the cingulum not previously reported. The epicingulum is composed of four open bands including an areolated valvocopula, an areolated copula and two non-areolated pleurae. The immature hypocingulum includes at least two bands. Openings of alternate bands are arranged in a dextral pattern. Based on previous reports from the west coast and our current findings, Thalassiosira mala appears to be a common, widely distributed primary producer in Indian coastal waters. The presence of morphologically similar species, especially those\20 lm in diameter, underscores the importance of reliable species-level using appropriate techniques for meaningful ecological and biogeographic considera- tions and for monitoring potentially harmful algae in India’s economically important coastal waters. Published reports suggest that Thalassiosira mala is widely distributed in temperate and tropical waters, present in 26 of 232 ecoregions and 18 of 62 provinces recognized in a recent classification of coastal marine ecoregions.

Keywords. Bay of Bengal; biogeography; Chilka Lake; diatom; fine structure; taxonomy; Thalassiosira mala

1. Introduction us a better understanding of the true relationships among the genera and species of . Therefore, we are currently Diatoms are single-celled, photosynthetic microalgae char- examining archived samples of marine diatoms in the col- acterized by the presence of a two-part siliceous covering lection of Professor Desikachary from the coastal waters of known as the frustule. In marine systems they are a major the Bay of Bengal, together with additional materials col- component of phytoplankton, and may contribute as much as lected recently by the senior author, and using a combination 20% of the global primary productivity (Field et al. 1998; of light and electron microscopy to determine the hidden Uitz et al. 2010; Malviya et al. 2016). In light of the diversity of the diatom flora of the region. Our preliminary importance of diatoms to marine ecosystems, 30 years ago investigations indicate that the diatom flora will include Professor T. V. Desikachary and his research group pub- many more species than currently reported. lished the six-volume Atlas of Indian Ocean Diatoms (De- Of particular interest to us are members of the genera sikachary 1986–89). This monumental work includes light Thalassiosira Cleve emend. Hasle and Coscinodiscus micrographs of nearly all of the diatom species known from Ehrenberg emend. Hasle and Sims, two of the dominant and the region at the time. However, many changes have most frequently encountered planktonic diatom genera in occurred in our understanding of diatom taxonomy since the Indian coastal waters. Before the advent of electron micro- publication of the Atlas. In particular, the widespread use of scopy, the differences between these two genera were not electron microscopy has provided new information on the clear. Both genera were included in the family Coscinodis- fine structure of the diatom frustule, including details not caceae Ku¨tzing and species were assigned to one genus or visible in light microscopy. This new information has given the other on the basis of characters now known to be of little http://www.ias.ac.in/jbiosci 59 60 A K S K Prasad et al. value in the delineation phylogenetic relationships. Thalas- morphology for the Indian materials, including the details of siosira and Coscinodiscus are now placed in separate fam- the cingulum not previously reported, and to compare frus- ilies, with Thalassiosira serving as the generitype of tule morphology with other small species of Thalassiosira Lebour emend. Hasle and Coscinodiscus also present in Indian coastal waters, some known to form serving as the generitype of Coscinodiscaceae. The two similar formless gelatinous colonies; and (4) to present an families are distinguished by details of the structure of the overview of the global distribution of T. mala following the areolae, including the position of the vela (internal in Tha- recent biogeographic classification of the coastal Marine lassiosiraceae, external in Coscinodiscaceae) and foramina Ecoregions of the World (MEOW) proposed by Spaulding (external in Thalassiosiraceae, internal in Coscinodiscaceae), et al. (2007). the nature of the marginal ring of processes (fultoportulae in Thalassiosiraceae, rimoportulae in Coscinodiscaceae), and the complete absence of fultoportulae in Coscinodiscaceae, 2. Materials and methods features that can only be resolved with certainty through the use of scanning electron microscopy (Hasle 1973b; Ross and 2.1 Materials and collection sites Sims 1973). Hasle (1968, 1972a, 1973a) first described structure of fultoportulae, the diagnostic valve processes Net phytoplankton (25 lm mesh) samples were collected in within the genus Thalassiosira, and emended the generic December 2015 from three coastal locations in Odisha description. The arrangement of areolae, fultoportulae, and (formerly, Orissa) on the east coast of India (Bay of Bengal): rimoportulae are widely considered to be important in the (1) Dolphin’s Cove (ca. 19.845° N, 85.479° E), near delineation of species of Thalassiosira (Fryxell 1975; Rivera Satapada Village, at the new mouth of Chilka Lake. 1981; Mahood et al. 1986; Makarova 1988; Hasle and This sampling site is located approximately 55 km Syvertsen 1996). Live cells in most species of Thalassiosira from Puri, Odisha, on the eastern side of Chilka Lake. form chains with sibling cells linked by threads of chitin Chilka Lake (also known as Chilika Lake) is the largest (McLachlan et al. 1965). However, about a dozen species of brackish water lake in Asia. It is connected to the Bay Thalassiosira form colonies of cells embedded in a common of Bengal by a long (35 km), narrow channel in the mucilage; the formation of mucilaginous colonies may be state of Odisha, India. Chilka Lake covers an area of associated with harmful effects (Hasle and Fryxell 1995; approximately 900–1100 km2 (Raman et al. 1990). Fryxell and Hasle 2003). During the monsoon season considerable quantities of The genus Thalassiosira is well represented in Indian freshwater are discharged into the lagoon through a waters, with *60 species reported from the region, includ- number of rivulets and rivers, including the Daya, ing the east (Bay of Bengal) and west coasts (Arabian Sea) Bhargabi and Nuna rivers, which drain into the and Indian Ocean waters (Venkataraman 1939; Subrah- northeast end; as a result, the area of the lake increases manyan 1946; Misra 1956; Simonsen 1974; Hasle 1976; by several hundred square kilometers during the Desikachary 1986–89; Samanta and Bhadury 2015), of monsoon season. The salinity varies from trace levels which at least five were described from Indian waters as new to 36% (Panigrahi et al. 2009). to science, T. coramandeliana Subrahmanyan, T. marginata (2) Chandrabhaga Beach (ca. 19.865o N, 86.113o E), Venkataraman, T. plicatoides (Simonsen) Akiba and located three km east of the Sun temple of Konark, in Yanagisawa (as Coscinodiscus plicatoides Simonsen), T. the Puri district in the state of Odisha, India. sundarbana Samanta and Bhadury and T. tropica Misra. In (3) Puri, Odisha (19.813° N, 85.832° E), located 30 km the present report we focus on Thalassiosira mala Takano, a southwest of the previous site. nanoplanktonic species forming massive gelatinous colo- nies, occasionally reaching bloom numbers. It was the dominant nanoplankter in net hauls collected from coastal areas of the state of Odisha (formerly known as Orissa), 2.2 Preparation of material for light and electron including Chilka Lake, Chandrabhaga Beach (near the city microscopy of Konark) and Puri, suggesting its widespread distribution in Bay of Bengal waters. Samples were preserved in Lugol’s iodine in the field. Ali- The purpose of the present paper is four-fold: (1) to quots of each sample were cleaned of organic matter using a record, for the first time, the presence and overwhelming combination of hydrogen peroxide and hot concentrated dominance of the potentially harmful marine planktonic sulfuric acid followed by 10 rinses with de-ionized water. diatom Thalassiosira mala in Chilka Lake and other coastal Small aliquots of a suspension of cleaned material were localities in the State of Odisha; (2) to clarify the correct date mounted in Naphrax for light microscopy (Prasad et al. of the validating publication for the name Thalassiosira 1990), dried onto circular coverslips mounted on aluminum mala by H. Takano; (3) to provide details of frustule stubs with double-sided carbon tape and sputter-coated with Marine diatom Thalassiosira mala from Odisha, India 61 gold/palladium for scanning electron microscopy, or directly TYPE LOCALITY: Futomi coast, Chiba Prefecture, dried onto formvar-coated grids for transmission electron Sagami Bay and Tokyo Bay, Japan microscopy. Naphrax-mounted slides were examined using a (Pacific Ocean) Leica-DMLB microscope equipped with differential inter- SIGNIFICANT REFERENCES: Takano 1965;p.1; ference contrast (DIC) and phase contrast (PC) optics. Takano 1976; p. 58, figs 1–18; Hasle 1976; figs 42 and Photomicrographs of cleaned materials were taken using 43; Hallegraeff 1984; p. 497, fig. 2; Makarova 1988; T-max 100 black-and-white film and yellow-green filters p. 78, pl. 51, figs 4–5; Takano 1990; pp 210–211; Cheng then digitally captured using Photoshop software. Material et al. 1993; p. 24, pl. 7, figs 52, 53; Licea 1994; Hasle and prepared for SEM was examined using a high-resolution Fryxell 1995; Herna´ndez-Becerril and Tapia Pen´a 1995; field emission FEI Nova 400 Nano SEM with through-the- p. 548, figs 23–25; Hasle and Syvertsen 1996; p. 54, lens differential pumping for low vacuum imaging capabil- table 7, pl. 13 d-f; Ake´-Castillo et al. 1999; p. 493, ities, operating at accelerating voltages of 5–10 kV, located figs 17–19; Sar et al. 2002; p. 382, figs 7–10; Fryxell and at Florida State University. Material for TEM was examined Hasle 2003; Park et al. 2009; Padmakumar 2010; figs 25a using a FEI CM120 TEM operating at 120 kV, also at the and b; Naya 2012; p. 148, figs 6, 34–35; Li et al. 2013; Florida State University. p.97, figs 75–77; Park et al. 2016; p. 41, fig. 22

2.3 Terminology of siliceous structures of diatom 3.1 Valve morphology (figures 1–5) frustules Small cells embedded in a vast expanse of gelatinous We used the standardized terminology for siliceous struc- material; no chains of sibling cells linked through central tures recommended by Anonymous (1975), von Stosch chitinous fibers were observed (figure 1a). Four or five dis- (1975) and Ross et al. (1979) in our descriptions of the coid plastids were easily seen in these small cells (figure 1e). diatoms discussed in this paper. The term marginal pore Frustules short barrel-shaped (drum-shaped), with rounded used by Takano (1965) is what is now known as a marginal ends in girdle view (figure 2a). Valve diameter varies strutted process or fultoportula; mucus pore is now an ec- between 3.6 and 9.8 lm, but the pervalvar axis of fully centric strutted process or fultoportula; surrounding holes or developed frustules is fairly consistent (5.8 to 6.9 lm). struts (Takano 1976) are now satellite pores and the isolated Areolae are hexagonal towards the center, becoming rect- apiculus is the labiate process or rimoportula. Takano angular towards the valve margin, arranged in radial rows, or (1976, 1990) later adopted the standardized terminology for in short fasciculated bundles with the rows running parallel valve processes, introduced by Hasle (1972a, p. 57) and to the central row, or in linear or curved tangential rows. Ross et al. (1979). Cingulum features are described using the There are 4 areolae in 1 lm near the center, 5 in 1 lm at the terminology introduced by von Stosch (1975) and Fryxell valve margin; this differs from the 2.5–3.0 areolae in 1 lm et al. (1981). in the type material (Takano 1965). The valve structure consists of loculi with foramina on the exterior (figure 3c–f), and vela (cribra) on the interior (figure 4c and d). There are 3. Results 9–12 cribral pores in each cribrum, without any definite pattern of arrangement (figure 4f and g). A marginal ring of The following description is based on our observations of fultoportulae is present with 12–22 fultoportulae per valve. field material collected from Chilka Lake and other Odisha These are closely spaced, 0.5 to 1.4 lm, or 2–4 areolae coastal material using TEM and field emission SEM as well apart, 6–11 fultoportulae in 10 lm; Takano (1965) reports as DIC (LM). 4–10 marginal fultoportulae in 10 lm. The fultoportulae Thalassiosira mala Takano 1983; p.31 (figs 1–5) open to the exterior through a rimmed pore within a hyaline Takano 1983. Bulletin of the Tokai Regional Fisheries space (figures 2c and 3f). Internally, the fultoportulae are Research Laboratory 109: p. 31; Takano 1965. Bulletin of operculate, each surrounded by four satellite pores (figure 4d the Tokai Regional Fisheries Research Laboratory 42, and e). A single fultoportula with three or four satellite pores p. 1 and 2, Fig. 1, a-m; Pl. I, figs 1–8 is located on the valve face, usually 3–4 areolae from the SYNONYM: Thalassiosira decipiens f. levanderi (Van center (figure 4a, b, f and g). There is no central fultoportula. Goor) Takano 1956;p.64(=T.levanderi Van Goor sensu A single rimoportula (labiate process) lies within the ring of Takano); sensu Hasle and marginal fultoportulae between two adjacent fultoportulae, Heimdal opening to the exterior through a rimmed pore without HOLOTYPE (designated by Takano 1983; p. 31): Plate 1, external tube (figures 4b, d and e). The labiate structure is fig. 3 of Takano 1965 (loc. cit.) usually radially directed, rarely obliquely, oriented. 62 A K S K Prasad et al.

Figure 1. Thalassiosira mala from Chilka Lake, Odisha, India. LM. (a) Mass of Lugol’s fixed cells in common mucilage. (b) Low- magnification phase contrast image of acid-cleaned cells. (c–d) Acid-cleaned material. DIC. Marginal processes (arrow heads) can just be discerned in some of the valves. (e) Lugol’s-fixed material showing 4–5 plastids per cell (Scale bar = 50 lmina,25lminb and 10 lmin c–e).

3.2 Cingulum morphology (figure 2) Thalassiosira: an ornate valvocopula, a copula and several pleurae (Fryxell et al. 1981, 1984; Prasad et al. 1993, 2011). The epicingulum is composed of four open bands (fig- ure 2a–c), including one areolated valvocopula, one areo- lated copula and two non-areolated pleurae (figure 2c); the 3.3 Comments on nomenclature and validation immature hypocingulum includes at least two bands (fig- ure 2a). The valvocopula is clearly areolate in the advalvar Takano (1965; p. 1, fig. 1, pl. 1, figs 1–8) provided English region, with 4–6 somewhat irregular rows of pores, 10–12 and Latin descriptions of Thalassiosira mala, along with line pores in 1 lm; the abvalvar area is free of areolation (fig- drawings and scanning and transmission electron micro- ure 2b–c). In a detached cingulum, a suggestion of an graphs of populations from Japanese coastal waters. The antiligula was noticed. The single copula is also perforated, English version of Takano’s description is reproduced here but by only a single row of pores, 11–12 in 1 lm; the two for reference. In LM: ‘Cells very small, 4–10 l in diameter, pleurae are hyaline (figure 2b–c). The openings of the disc-shaped or box-like, connected with mucilage thread alternate bands are arranged in a dextral pattern sensu each other in formless masses. Valves flat with rounded Fryxell et al. (1981); in other words, the openings of the margins and a spinule-like marking near the margin.’ In EM: bands on one side of the cell are offset so that alternate ‘Valves with a row of marginal pores (bases of apiculi (?), openings spiral to the right in an abvalvar direction. This 4–10 in 10 l. The marginal pore consists of a central main observed dextral pattern appears to be consistent in the pore and four surrounding holes. A mucous pore, from populations examined under scanning electron microscope. which probably a thread connecting cells each other The above structure of cingulum in T. mala follows the basic extrudes, consists of a central main pore and three (rarely pattern of the cingulum in the investigated marine species of four) surrounding holes, located in the subcentral area of Marine diatom Thalassiosira mala from Odisha, India 63 a name could be considered validly published (see Lan- jouw et al. 1956; Principle II and Article 35). Takano may have been unaware of this change in the Code, since he neglected to designate a nomenclatural type for Thalas- siosira mala (Takano 1965; p. 1) and for several other species he described during the 1960s and 1970s. As a result, although the detailed descriptions and figures pro- vided by Takano (1965) are sufficient for the positive identification of populations T. mala, the name of the species was not validly published. At some point Takano became aware of the change in the Code, and validated T. mala by referencing his previous description and illustra- tions and by designating a single specimen in a scanning electron micrograph (Takano 1965; plate 1, fig. 3) as the holotype (Takano 1983; p. 31). This met the requirements of the Code and at that point the name was validly pub- lished. Because the date of publication for a name or epi- thet corresponds to the date of publication of the last requirement (McNeill et al. 2012; Article 31.1), the correct date of publication of Thalassiosira mala Takano is 1983; not 1965. This issue was indicated by the late Dr. Reimer on the note card for Thalassiosira mala in the database of the Academy of Natural Sciences, Philadelphia (see the Diatom New Taxon File at ANSP, http://symbiont.ansp.org/ dntf/) and is further clarified in the Index Nominem Algarum (INA, http://ucjeps.berkeley.edu/INA.html). How- ever, all subsequent reports (listed in the significant refer- ences and elsewhere) refer to the original, incorrect, date of Figure 2. Thalassiosira mala from Chilka Lake, Odisha, India. publication date (see also Takano 1990). Acid-cleaned. SEM. Girdle view. Structure of the valvocopula and cingulum are clearly visible in all images. Valvocopula (Vc) is areolate with 4 rows of pores on the advalvar side, hyaline on the 4. Discussion abvalvar side. The copula (Co) has a single row of pores. Pleurae (Pl1, Pl2) appear completely hyaline. All bands are open with the opening arranged in dextral pattern. There is a poorly developed 4.1 Presence of Thalassiosira mala in Indian waters antiligula on the valvocopula in (b) (Scale bars = 1 lm). Previous investigations in Chilka Lake focused on phyto- plankton abundance in relation to water quality, especially valves about 1/5–1/2 of the radius apart from the center. A salinity. The initial studies of the algal flora Chilka Lake marginal pore–like marking (base of an isolated apiculus?) were conducted by Biswas (1932), followed by Roy (1954), situated on almost same radial line with the subcentral Patnaik (1978), Raman et al. (1990), Adhikary and Sahu mucous pore. Areolae hexagonal, arranged in radial, bundled (1992), Rath and Adhikary (2005), and Mohanty and line, or for rather many valves, in linear rows at the central Adhikary (2013). All of the studies documented the algal part and thereafter radial to the margin with rounded tan- flora and seasonal variation in salinity gradients the lagoon. gential rows concave against the margin of numerous Recent openings of Chilka Lake to the Bay of Bengal waters irregular systems. Areolae ca. 2.5–3 in 1 l in the center, 5 in facilitated extensive mixing of the freshwater in the lagoon 1 l near the margin. Marginal striae ca. 6 in 1 l.’ The above with seawater, resulting in a wide range of hydrologic con- description focuses on valve morphology; details of the ditions (Nayak and Behera 2004; Panigrahi et al. 2009; cingulum were not provided in any of Takano publications Mohanty et al. 2009). For example, Raman et al. (1990) on T. mala (Takano 1965; 1976 and 1990). identified 97 species of microalgae in Lake Chilka on the During the 8th International Botanical Congress, the basis of light microscopy. From their analyses of the distri- International Code of Botanical Nomenclature (Paris Code) butions of the various species, they recognized five different was amended to include a specific requirement for the ecological zones in Chilka Lake, each with a characteristic designation a nomenclatural type for each new taxon of the assemblage of phytoplankton species. Included in the spe- rank of family or lower beginning January 1, 1958; before cies lists was an undetermined species of the fultoportulate 64 A K S K Prasad et al.

Figure 3. Thalassiosira mala from Chilka Lake, India. Acid-cleaned. SEM. Valve exterior. (a) Low-magnification image showing a mass of valves. (b) Higher magnification of the same mass. (c–e) Images of single valves showing the arrangement of marginal processes (white arrow heads) and variations in the arrangement of areolae. Valve face fultoportula (white arrow) appears as circular opening just under halfway from the center of the valve to the valve margin. The opening of the rimoportula is obscure. (f) Detail of the valve margin showing the rim of silica bordering the external openings of the fultoportulae and the surrounding hyaline areas. (Scale bars = 50 lmina,5lmin b,2lminc–e and 1 lminf). freshwater diatom genus Stephanodiscus Ehrenberg (listed unfortunately, they did not provide any illustrations or as ‘Stephanodiscus sp.’). This species was present in the descriptions of the species. They did not include any rep- oligohalobe and mesohalobe sections of the lagoon, where it resentatives of the genus Thalassiosira in their species list. was sometimes the dominant member of the phytoplankton; More recent studies have included numerous brackish water Marine diatom Thalassiosira mala from Odisha, India 65

Figure 4. Thalassiosira mala from Chilka Lake, India. Acid-cleaned. SEM. Valve interior. (a) Two valves at low magnification. (b, d and f) Details of the right-hand valve in (a). (d) Areolae with domed cribra, position of the rimoportula, the four satellite pores and pore covers surrounding the marginal fultoportulae. (f) The valve face fultoportula with four satellite pores and pore covers. (c) Note the abnormal spacing of the two adjacent marginal fultoportulae in right-hand valve and the normal spacing of the fultoportulae in the left-hand valve. (e) Details of the left-hand valve in Fig. 4a, showing marginal fultoportulae and rimoportula. (g) Three satellite pores and pore covers surrounding the valve face fultoportula (Scale bars = 3 lmina,2lminb,1lminc, 500 nm in d–g). and marine diatoms in Chilka Lake, including fultoportulate T. eccentrica (Ehrenberg) Cleve emend. Fryxell and Hasle centric diatoms of the genera (Ku¨tzing) Bre´bis- and T. subtilis (Ostenfeld) Gran emend. Hasle, among others, son, Skeletonema Greville, Stephanodiscus, and Thalas- but not Thalassiosira mala (Adhikary and Sahu 1992; siosira. Representatives of Thalassiosira mentioned include Mohanty and Adhikary 2013). 66 A K S K Prasad et al.

Figure 5. Thalassiosira mala from Chilka Lake, Odisha, India. Acid-cleaned. TEM. (a-c) Complete valves illustrating variation in the arrangement of areolae. Note the rows of areolae in sectors, decrease in size and the change in the overall shape of the areolae from the center of the valve to the valve margin. (d) Detail of a valve with a labiate process at the 9 o’clock position and a valve-face fultoportula with three satellite pores. (e and f) Details of the cribral structure. Note the fultoportula with four satellite pores in (f). (Scale bars = 1 lm in a–c, 500 nm in d–f). Marine diatom Thalassiosira mala from Odisha, India 67 The present study, then, provides the first record of Tha- investigators. In LM, the formless gelatinous colonies of T. lassiosira mala in the region. Because the structure of T. mala can be easily confused with similar disrupted colonies mala is too fine to be resolved even in DIC-LM, we relied on of the haptophyte Phaeocystis Lagerheim (Takano 1956; SEM and TEM observations to determine key features of the Hasle 1976; Fryxell and Hasle 2003). Therefore, it is pos- valve, in particular, the density and arrangement of areolae sible that the lack of reports of T. mala from Chilka Lake and and the arrangement of fultoportulae and rimoportulae. The other localities on the east coast of India may have resulted recognition of T. mala in Chilka Lake and the coastal waters from the methodologies used. However, it is also possible of the Bay of Bengal demonstrates once again the inherent that T. mala was introduced to the region only recently, and difficulty of identifying small species of Thalassiosira by the dominance we noted in our samples was a response of light microscopy alone; electron microscopy is absolutely the species to favorable local conditions. An examination of necessary for the accurate identification of very small and archived samples from the region may shed some light on weakly silicified diatoms, even those known to be harmful to which of these options is the more likely. organisms higher in the food chain and, possibly, to humans More than 15 species of Thalassiosira are known, or at as well. These small diatoms represent an important potential least suspected, to form gelatinous colonies (Fryxell and source of organic carbon for higher trophic levels because of Hasle 2003). These include T. curviseriata Takano, T. deli- their potential for rapid growth (Fryxell 1975). The absence catula Ostenfeld emend. Hasle, T. diporocyclus Hasle, T. of reports of T. mala from this and other coastal waters of fragilis Fryxell, T. fryxelliae Sunesen and Sar, T. gravida India until recently may largely reflect on the limitations of Cleve, T. mala, T. mediterranea (Schroder) Hasle, T. minima conducting investigations using light microscopy alone for Gaarder emend. Hasle, T. minuscula Krasske emend. Hasle, identification. Small centric diatoms are often overlooked or T. minicosmica Lee and Park in Park and Lee, T. oceanica ignored because of the challenge their small size can pose to Hasle, T. partheneia Schrader, T. proschkinae Makarova, T.

Table 1. Distributional records of Thalassiosira mala, with biogeographic categories as defined in the marine ecoregions of the world (MEOW, Spaulding et al 2007). Numbers before the names of the ecoregions refer to the numbers on regions indicated in figure 6.

Realms Provinces Ecoregions Temperate Northern Atlantic Northern European Seas 1—North Sea6 Cold Temperate NW Atlantic 2—Virginian6 Warm Temperate NW Atlantic 3—Carolinian6,23 4—Gulf of Mexico4,5,6,18 Temperate Northern Pacific Cold Temperate NW Pacific 5—Sea of Okhost9,14 6—Sea of Japan5,22 7—Yellow Sea16,22 Warm Temperate NW Pacific 8—Central Kuroshio Current2,3 9—East China Sea22 Cold Temperate NE Pacific 10—Oregon, Washington, Vancouver Coast and Shelf6 Warm Temperate NE Pacific 11—Southern California Bight6 12—Cortezian12 Tropical Atlantic Tropical NW Atlantic 13—Southern Gulf of Mexico10,20 14—Floridian6 North Brazil Shelf 15—Guianan6 Western Indo-Pacific Somali/Arabian 16—Central Somali Coast6 Western Indian 17—Bight of Sofala6 West and South Indian Shelf 18—Western Indian6,17 Bay of Bengal 19—Eastern India1 South China Sea 20—Southern China11,21 Central Indo-Pacific Sahul Shelf 21—Gulf of Carpentaria7,8 Tropical Eastern Pacific Tropical East Pacific 22—Chiappas-Nicaragua13 Temperate South America Warm Temperate SW Atlantic 23—Southeastern Brazil18 24—Rio Grande6,19 25—Uruguay-Buenos Aires Shelf15 Temperate Australasia East Central Australian Shelf 26—Manning-Hawksberry7,8

Sources: 1present study, 2Takano (1956), 3Takano (1965), 4Conger et al. (1972), 5Takano (1976), 6Hasle (1976), 7Hallagraeff (1984), 8Hallegraeff and Jeffrey (1984), 9Makarova (1988), 10Licea (1994), 11Cheng et al. (1993), 12Herna´ndez-Becerril and Tapia Pen´a(1995), 13Ake´-Castillo et al. (1999), 14Orlova et al. (2002), 15Sar et al. (2002), 16Park et al. (2009), 17Padmakumar (2010), 18Prasad et al. (2010), 19Fernandes and Frassa˜o- Santos (2011), 20Licea et al.(2011), 21Li et al. (2013), 22Park et al. (2016), 23Nienow, unpublished observations. 68 A K S K Prasad et al. subtilis, T. sp. cf subtilis sensu Fryxell et al. 1984; T. tubifera development of the fultoportulae as primitive characters. Fryxell, and T. weissflogii (Grunow) Fryxell et Hasle (also Takano (1965) reported that the central tube of the valve face known as Conticribra weissflogii (Grunow) K. Stachura- process was typically surrounded by three satellite pores for Suchoples and D.M. Williams) (Fryxell et al. 1984; Hasle specimens from Japanese waters; however, he observed a and Fryxell 1995; Fryxell and Hasle 2003; Sunesen and Sar specimen from Gulf of Mexico in which the central tube was 2004; Park and Lee 2015). Additional species may produce surrounded by four satellite pores. In the present study of gelatinous colonies under certain conditions as suggested by Odisha material, valve-face fultoportulae with three or four Hustedt (1926)—Takano noted that the characteristic satellite pores were seen. All fultoportulae were operculate. gelatinous colonies of T. mala were scarcely recognizable in Cingulum morphology in T. mala is described here for the laboratory-grown cultures (Takano 1965) and Hasle (1983) first time. The general form of the cingulum – a valvocopula suggested that certain conditions in upwelling areas appear with several rows of pores, a copula with a single row of to favor the formation of gelatinous colonies. pores and several unstructured pleurae—is similar to that of As an aid for identification, Hasle and Fryxell (Fryxell many of the species of Thalassiosira investigated in SEM et al. 1984; Hasle and Fryxell 1995; Fryxell and Hasle 2003) (Fryxell et al. 1984), including other gelatinous-colony- separated the gelatinous-colony-forming species of Thalas- forming species, such as T. subtilis, T. diporocyclus, T. siosira into three morphological groups based on cell size minuscula, T. tubifera, and T. partheneia (Hasle 1972a, b; and shape and process patterns: 1) larger species with dome- Schrader 1972; Fryxell 1975; Hasle 1983; Fryxell et al. shaped valves, radial rows of areolae arranged in sectors, one 1984). In two other species, T. weissflogii and T. fragilis, all central fultoportula, at least one marginal ring of fultopor- of the bands are areolate (Fryxell et al. 1981; 1984). Hyaline tulae and an additional ring of fultoportulae on the valve pleurae are considered to be an advanced characteristic in face, as in T. diporocyclus, T. fragilis, T. subtilis and T. Thalassiosira (Fryxell et al. 1984). Thus, the valve shapes, tubifera; 2) species with flattened valves and strongly process patterns, band structures of the group of gelatinous developed external extensions of the fultoportulae, as in T. colony-forming species including T. mala exhibit a number curviseriata, T. delicatula, T. gravida, and T. weissflogii; and of characteristics that may be construed as primitive based 3) smaller species with rounded valves and poorly developed on our current understanding of the concepts within the external extensions of the marginal fultoportulae, as in T. genus (Fryxell et al. 1984). The dextral pattern of alternate mala, T. mediterranea, T. minuscula, T. partheneia and T. band openings observed in T. mala is common in species of proschkinae. Thalassiosira (Fryxell et al. 1981; 1984; Hasle and Lange At least three gelatinous-colony-forming species, T. mala, 1989; Syvertsen and Hasle 1984; Prasad et al. 1993; 2011). T. partheneia and T. subtilis have thus far been reported from Fryxell et al. (1981) suggested that band orientation could be the Bay of Bengal and Arabian Sea waters (Simonsen 1974; a useful tool in the assessment of phylogenetic relationships. Raman and Prakash 1989a, b, Sahu et al. 2010; 2012; Padmakumar 2010; present study). 4.3 Comparison of Thalassiosira mala with similar species from the coastal waters of India 4.2 Structure of Thalassiosira mala Thalassiosira mala can be easily confused with another The process pattern in our material, a single eccentric valve nanoplanktonic diatom, T. pseudonana Hasle and Heimdal face fultoportula, one ring of marginal fultoportulae and a (Hasle and Heimdal 1970; p. 564, figs 27–38). Thalassiosira single marginal rimoportula, is similar to that reported in the pseudonana was originally described as Cyclotella nana literature for T. mala, especially as described in the proto- Hustedt based on material collected from a freshwater logue (Takano 1965) and in later reports (Takano 1976; locality. Since then it has also been isolated from a number 1990). Fultoportulae in T. mala do not have well-developed of coastal areas, and is currently considered to be euryhaline. external extensions, however, the exterior openings of the The two species share a number of similar features, fultoportulae do have a thickened siliceous rim. All species including small size, approximately 4 to 9 lm in diameter in known to form a gelatinous matrix have operculate fulto- both species, the presence of a ring of marginal fultoportulae portulae (Fryxell and Hasle 1979). This is also the case for and an eccentric valve face fultoportula. The two species many of the Thalassiosira species previously investigated clearly differ in a number of significant features, however. and for other fultoportulate diatom genera including De- Valves of T. pseudonana are very weakly silicified, with tonula Schu¨tt ex De Toni (Hasle 1973b), Lauderia Cleve radial ribs but with only poorly developed tangential walls (Syvertsen and Hasle 1982), Livingstonia Prasad (Prasad and defining separate areolae. Further, the marginal fultoportulae Nienow 2011), and Skeletonema (Hasle 1973b, Medlin et al. each have three satellite pores and the valve face process has 1991; Sarno et al. 2005). Fryxell et al. (1984) considered only two satellite pores (Hasle and Heimdal 1970; figs 35 operculate fultoportulae and the lack of external and 38). Finally, T. pseudonana does not form gelatinous Marine diatom Thalassiosira mala from Odisha, India 69 colonies, but is invariably found as solitary cells. In Tha- encountered and mentioned as a dominant diatom species in lassiosira mala, on the other hand, valves have well-devel- ecological investigations of phytoplankton from the Indian oped locular areolae, the marginal fultoportulae have four coastal waters of the Bay of Bengal, the Arabian Sea and the satellite pores, the valve face process typically has three, Laccadive (Lachadive) Sea (Raman and Prakash 1989a, b, rarely four, satellite pores, and the cells are embedded in a Sahu et al. 2010, 2012; Baliarsingh et al. 2013, 2015; and colonial gelatinous matrix. Hasle and Heimdal (1970; many others). In the absence of accurate descriptions of the p. 567) regarded the valve features, particularly of the frustule morphology of specimens of T. subtilis encountered absence of radial ribs or the presence of poorly developed in Indian localities, it is difficult to comment on the identity areolae as insufficient to justify the distinction between T. of the species, let alone compare its populations with the mala and T. pseudonana and briefly treated T. mala as a later population of T. mala from Chilka Lake and Odisha coastal synonym of T. pseudonana. Takano (1976) rejected their locations. Since T. subtilis was the first species of the genus comparison and argued that his species was clearly distin- to be reported as forming gelatinous colonies (Ostedfeld guishable on the basis of its ability to form gelatinous 1899), it is possible that other gelatinous-colony-forming colonies, the consistent occurrence of a single eccentric species, such as T. mala, may have been included in the valve face fultoportula and well-developed radial rows of reports. T. mala from Chilka Lake and other sites can easily areolae. Subsequently, Hasle (1976) and Hasle and Syvert- be differentiated from T. subtilis in having much smaller sen (1996) treated T. mala and T. pseudonana as separate cells (2–12 lm in diameter vs. 15–49 lminT. subtilis), only taxa, although they did consider T. pseudonana to be a one marginal ring of fultoportulae, and no intermediate valve highly variable species. It is worth noting that Raman and face fultoportulae; both species have a single eccentrically Prakash (1989a, b) considered T. pseudonana to be bloom- located subcentral fultoportula (Hasle 1972b, Fryxell and forming and locally dominant on the east coast India, near Hasle 2003). T. subtilis is considered to be oceanic (Osten- Visakhapatnam Harbor and in the Bay of Bengal, not far feld 1899; Hasle 1976) whereas T. mala, by and large, has from the present study sites of Odisha. Unfortunately, but only been recorded from coastal waters and regions of they did not include descriptions or illustrations of the field upwelling (Takano 1956, 1965, 1976, 1990). Paul et al. populations that could be used to verify the identity of the (2008) reported an unidentified ‘Thalassiosira sp’ as one of species. They and their colleagues did not record T. mala in the dominant species in the Bay of Bengal in 2002 and 2003; either Visakhapatnam Harbor (Raman and Prakash 1989a, b) but provided no descriptions or illustrations to comment on or Chilka Lake (Raman et al. 1990). its identity. Ostenfeld (1899; p. 59, cited in Hasle 1972b,p.111) Thalassiosira partheneia is characterized by small cells, 4 provided the first description of Thalassiosira subtilis under to 14 lm in diameter, with an areolar density of 38–50 in the name Podosira ? subtilis n. sp. It was classified as a truly 10 lm, a marginal ring of fultoportulae with long internal oceanic plankton from the temperate Atlantic Ocean, char- extensions, and a single marginal rimoportula (Schrader acterized as small, with a cell diameter of 16–32 lm, weakly 1972; Hasle 1983). T. mala from the Odisha localities silicified, with no distinct structures visible in LM; the cells resembles T. partheneia in having small cells embedded in were embedded in homogenous, formless gelatinous sub- gelatinous material and in areola density, but differs in the stance. Gran (1900; p. 117), with some reservation, trans- structure of the marginal fultoportulae. T. partheneia has not ferred the species to Thalassiosira. Illustrations of what was been recorded from the east coast of India, but has been considered to be T. subtilis in Hustedt, (1930, fig. 266) and reported in bloom concentrations from west coast (Pad- Cupp (1943, fig. 23) were generally used for identification makumar 2010). until Hasle (1972b) examined the valve structure, and Thalassiosira marginata is a brackish water species from described the areolar structure and arrangement and position the River Cooum, Madras (now Chennai), which is influ- of fultoportulae and rimoportulae. She also amplified the enced by waters from the nearby Bay of Bengal. description of the species based on electron microscopy and Venkataraman (1939; p. 297, 298, figs 12, 13) described typified the name using Ostenfeld’s original material. massive concentrations of T. marginata, which imparted a According to Hasle (1972b) valve diameter ranges from 15 brownish-yellow color to the waters. The species is char- to 32 lm, the areolar density is about 30 in 10 lm with the acterized in LM by extremely small cells, measuring 4 to areolae arranged in sectors, with rows parallel to median 6 lm in diameter, with 18–22 marginal punctae; no other row. There is a single rimoportula located at some distance features were visible in LM. The type material is not from the margin, one marginal ring of fultoportulae, available so details of fine structure of the valve, including 2.7–3.6 lm apart, scattered intermediate valve-face fulto- the structure of marginal processes and areolae, cannot be portulae, and a single eccentrically-located subcentral ful- determined, precluding any speculations on its generic toportula. No details of the satellite pores surrounding the placement, let alone its species interrelationships. central tubes of the fultoportulae were provided in the Venkataraman (1939) did not mention the presence of chains emended diagnosis (Hasle 1972b). T. subtilis was frequently of cells wherein sibling cells are joined by threads extruded 70 A K S K Prasad et al. through the central processes; such chains are characteristic ecoregions, 62 provinces and 12 realms. In this system, of many the species of Thalassiosira. Since its first Indian coastal regions known to harbor T. mala are included description, T. marginata has only rarely been reported by in the Eastern India ecoregion of the Bay of Bengal province other investigators monitoring Bay of Bengal waters (Raman (the present study), and the Western India ecoregion of the and Prakash 1989a, b). Takano (1956; p.63) also drew West and South Indian Shelf province (Hasle 1976; Pad- attention to small cells of T. marginata and compared them makumar 2010); both provinces are subdivisions of the with T. mala (as a form of T. decipiens cf. levanderi). Western Indo-Pacific realm. A comparison of published reports verified by electron microscopy with MEOW sug- gests that T. mala may have a narrower distribution than 4.4 Biogeography of Thalassiosira mala suggested by Fryxell and Hasle (2003). Reports of T. mala are restricted to about 15% of the world’s tropical/temperate The massive concentrations of T. mala seen in Chilka Lake coastal ecoregions (26 of the 192 non-polar ecoregions and in coastal localities from Odisha suggest it is actually recognized), 33% of the provinces (18 of 57), nested within widely distributed in the Bay of Bengal and is able to form 8 of 10 realms (see table 1 and figure 6). extensive blooms in the region. In contrast, the presence of A striking feature of the distribution map (figure 6) is the T. mala in the Arabian Sea on the west coast of India has absence of literature records of T. mala from the entire South been known for some time. Hasle (1976; p. 331, figs 42, 43) Pacific, including the western coast of South America (see provided the first record of the species in Indian Ocean Rivera 1981, 1983) and from much of the eastern coastline waters, including SW coast of India, and in east African of the Atlantic. This raises the question whether T. mala has waters. More recently, Padmakumar (2010; p. 68, fig. 25) a discontinuous distribution or whether it is consistently reported a bloom (6.74 9 106 cells/L) of T. mala off overlooked through the misapplication of the names of better Azheekode, near Kochi, on the southwest coast of India (10° known species, e.g. T. subtilis, for any species of Thalas- 28.43 N, 75°36.10 E) during the monsoon period of 2006. In siosira seen in gelatinous colonies. Diatom diversity must be this case the bloom of T. mala was followed by a bloom of assessed by competent taxonomic authorities; the misappli- yet another gelatinous-colony forming species, T. parthe- cation of names can lead to a false perception of diatom neia. Unfortunately, no descriptions of the bloom popula- diversity, biogeographical patterns, and the rarity of certain tions were provided, precluding comparison with forms (Mann and Droop 1996). We believe that Thalas- populations of T. mala from the Bay of Bengal. It is possible siosira mala is actually far more widely distributed than the that the species is underreported in Indian waters— most of current records show, and that a careful examination using the earlier phytoplankton investigations relied almost electron microscopy will lead to additional reports within the exclusively on light microscopy. Additional records latitudinal boundaries suggested by Fryxell and Hasle expanding its distribution in Indian waters are likely as the (2003). use of electron microscopy increases. Outside India, Thalassiosira mala is well-distributed in coastal waters around the world (table 1; figure 6). Hasle 4.5 Thalassiosira mala as a harmful alga (1976; figs 39, 42, 43) reported mass occurrences in such widespread localities as Trinidad, the southern Atlantic, west Thalassiosira mala has been linked to shell-fish mortality. coast of India (Arabian Sea), the Gulf of Mexico, and the The first recorded instance took place in Tokyo Bay in 1951. North Sea. Based on these reports, she initially characterized In this instance, extensive mucilaginous colonies of T. mala, T. mala as a biogeographically cosmopolitan species (Hasle initially identified as T. decipiens var. levandari, caused the 1976). Later, as new information became available, she and waters of Tokyo Bay to turn yellowish brown (Takano 1956, Fryxell (Hasle and Fryxell 1995; Fryxell and Hasle 2003) p. 65). At the same time a massive die-off of cultured shell- considered it to be restricted to tropical and temperate fish took place (Takano 1956). Takano (1956) attributed the waters, and established the northern boundary for T. mala at deaths to the presence of the gelatinous substances produced about 58°–59° N and the southern boundary at about 35° S by T. mala, possibly clogging the gills of the shellfish, (Hasle and Fryxell 1995; Fryxell and Hasle 2003). Park et al. perhaps working in conjunction with poor water quality (2016), working with 44 species of Thalassiosira from conditions. The reported loss, according to Takano’s report Korean coastal waters, were able to distinguish four bio- (1956) amounted to ¥58 million (approximately US geographic groups; T. mala was placed in a group of 15 $161,000, based on the currency exchange rate in effect at species considered to be characteristic of temperate to the time, approximately US $1,500,000 in today’s dollars). tropical waters. Hasle and Syvertsen (1996, p. 54) regarded T. mala as Recently Spaulding et al. (2007) proposed a biogeo- probably the first marine planktonic diatom linked to the graphic classification system for coastal marine ecoregions death of shellfish. Even though T. mala blooms have been of the world (MEOW), recognizing a total of 232 reported from wide geographical localities, no toxin has ever Marine diatom Thalassiosira mala from Odisha, India 71

Figure 6. Global Distribution of Thalassiosira mala. Numbers correspond to the numbers associated with the ecoregions listed in table 1 (map developed using SurferÒ 13, Golden Software LLC). been reported from the species. In fact, although several and Karisiddaiah 2014), and the frequent occurrences of planktonic and benthic species of the raphid diatom genera, harmful algal blooms (HABs) and nuisance plankton blooms Amphora Ehrenberg and Pseudo-nitzschia Hustedt, in par- with adverse impacts on fishery and human health, accurate ticular, have been shown to produce the neurotoxin domoic identification of microalgae by trained taxonomists is acid, which has been proved to be harmful to humans, important not only for aquatic health management decisions mammals, birds, anchovies and other marine biota (Hasle but also for meaningful conservation programs and biogeo- and Fryxell 1995), no centric diatoms are known to produce graphic considerations. Since many of the known harmful domoic acid or any other toxins harmful to higher trophic algal bloom species, including diatoms, are cosmopolitan levels. However, according to Fryxell and Hasle (2003), any within their latitudinal ranges (Taylor 1987), familiarity with diatom species frequently reported in bloom numbers should recent taxonomic guides and identification manuals from be regarded as potentially harmful. Indeed, some centric diverse areas of the globe, in addition to regional guides diatoms, including several species of Coscinodiscus and based on indigenous populations, is required. Palmerina hardmaniana (Greville) Hasle (as Hemidiscus hardmanianus (Greville) Mann), have been associated with the heavy mortality of fish and invertebrates on the east coast Acknowledgements of India (Subramanian and Purushothaman 1985; Mathew et al. 1988; Padmakumar et al. 2007). We are not aware of AKSKP is grateful to A. K. Madhusudhan, Mridhula Babu, any reports of harmful effects associated with the over- Jayalakshmi Kamesh, A. Ramesh, Saroja Rupanagudi, and whelming dominance of Thalassiosira mala we noted in Vijaya Ramesh for their assistance with logistics and field December 2015 on the productivity of Chilka Lake in the collections. The authors thank Dr. Duncan Sousa, Coordi- higher trophic levels. nator of the Biological Science Imaging Resource at Florida The highly productive, yet unique and fragile ecosystem State University, for his technical assistance with transmis- of Chilka Lake, with its estuarine characteristics, contains sion electron microscopy. rich fishery resources, which sustain the livelihoods of increasingly dependent coastal communities (Mohanty et al. References 2009). 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