Thalassiosira mala (Bacillariophyta), a potentially

Thalassiosira mala (Bacillariophyta), a potentially harmful,marine diatom from Chilka Lake and other coastal localities

of Odisha, India: Nomenclature, frustule morphology and globalbiogeography

AKSHINTHALA K S K PRASAD1*, JAMES A NIENOW2 and ERIC LOCHNER

3

1Department of Biological Science, Florida State University, Tallahassee, FL 32306–4370, USA2Department 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 phytoplankton collected from coastal localities in Odisha on the east coast of India, includingChilka Lake, Chandrabhaga Beach and Puri, in December 2015, revealed the overwhelming dominance of Thalassiosiramala, a gelatinous colony-forming, potentially harmful, marine planktonic diatom. The large numbers of cells allowed us toobserve details of the cingulum not previously reported. The epicingulum is composed of four open bands including anareolated valvocopula, an areolated copula and two non-areolated pleurae. The immature hypocingulum includes at leasttwo bands. Openings of alternate bands are arranged in a dextral pattern. Based on previous reports from the west coast andour current findings, Thalassiosira mala appears to be a common, widely distributed primary producer in Indian coastalwaters. The presence of morphologically similar species, especially those\20 lm in diameter, underscores the importanceof reliable species-level taxonomy using appropriate techniques for meaningful ecological and biogeographic considera-tions and for monitoring potentially harmful algae in India’s economically important coastal waters. Published reportssuggest that Thalassiosira mala is widely distributed in temperate and tropical waters, present in 26 of 232 ecoregions and18 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

Diatoms are single-celled, photosynthetic microalgae char-acterized by the presence of a two-part siliceous coveringknown as the frustule. In marine systems they are a majorcomponent of phytoplankton, and may contribute as much as20% of the global primary productivity (Field et al. 1998;Uitz et al. 2010; Malviya et al. 2016). In light of theimportance of diatoms to marine ecosystems, 30 years agoProfessor T. V. Desikachary and his research group pub-lished the six-volume Atlas of Indian Ocean Diatoms (De-sikachary 1986–89). This monumental work includes lightmicrographs of nearly all of the diatom species known fromthe region at the time. However, many changes haveoccurred in our understanding of diatom taxonomy since thepublication of the Atlas. In particular, the widespread use ofelectron microscopy has provided new information on thefine structure of the diatom frustule, including details notvisible in light microscopy. This new information has given

us a better understanding of the true relationships among thegenera and species of diatoms. Therefore, we are currentlyexamining archived samples of marine diatoms in the col-lection of Professor Desikachary from the coastal waters ofthe Bay of Bengal, together with additional materials col-lected recently by the senior author, and using a combinationof light and electron microscopy to determine the hiddendiversity of the diatom flora of the region. Our preliminaryinvestigations indicate that the diatom flora will includemany more species than currently reported.

Of particular interest to us are members of the generaThalassiosira Cleve emend. Hasle and CoscinodiscusEhrenberg emend. Hasle and Sims, two of the dominant andmost frequently encountered planktonic diatom genera inIndian coastal waters. Before the advent of electron micro-scopy, the differences between these two genera were notclear. Both genera were included in the family Coscinodis-caceae Kutzing and species were assigned to one genus orthe other on the basis of characters now known to be of little

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value in the delineation phylogenetic relationships. Thalas-siosira and Coscinodiscus are now placed in separate fam-ilies, with Thalassiosira serving as the generitype ofThalassiosiraceae Lebour emend. Hasle and Coscinodiscusserving as the generitype of Coscinodiscaceae. The twofamilies are distinguished by details of the structure of theareolae, including the position of the vela (internal in Tha-lassiosiraceae, external in Coscinodiscaceae) and foramina(external in Thalassiosiraceae, internal in Coscinodiscaceae),the nature of the marginal ring of processes (fultoportulae inThalassiosiraceae, rimoportulae in Coscinodiscaceae), andthe complete absence of fultoportulae in Coscinodiscaceae,features that can only be resolved with certainty through theuse of scanning electron microscopy (Hasle 1973b; Ross andSims 1973). Hasle (1968, 1972a, 1973a) first describedstructure of fultoportulae, the diagnostic valve processeswithin the genus Thalassiosira, and emended the genericdescription. The arrangement of areolae, fultoportulae, andrimoportulae are widely considered to be important in thedelineation of species of Thalassiosira (Fryxell 1975; Rivera1981; Mahood et al. 1986; Makarova 1988; Hasle andSyvertsen 1996). Live cells in most species of Thalassiosiraform chains with sibling cells linked by threads of chitin(McLachlan et al. 1965). However, about a dozen species ofThalassiosira form colonies of cells embedded in a commonmucilage; the formation of mucilaginous colonies may beassociated with harmful effects (Hasle and Fryxell 1995;Fryxell and Hasle 2003).

The genus Thalassiosira is well represented in Indianwaters, with *60 species reported from the region, includ-ing the east (Bay of Bengal) and west coasts (Arabian Sea)and Indian Ocean waters (Venkataraman 1939; Subrah-manyan 1946; Misra 1956; Simonsen 1974; Hasle 1976;Desikachary 1986–89; Samanta and Bhadury 2015), ofwhich at least five were described from Indian waters as newto science, T. coramandeliana Subrahmanyan, T. marginataVenkataraman, T. plicatoides (Simonsen) Akiba andYanagisawa (as Coscinodiscus plicatoides Simonsen), T.sundarbana Samanta and Bhadury and T. tropica Misra. Inthe present report we focus on Thalassiosira mala Takano, ananoplanktonic species forming massive gelatinous colo-nies, occasionally reaching bloom numbers. It was thedominant nanoplankter in net hauls collected from coastalareas of the state of Odisha (formerly known as Orissa),including Chilka Lake, Chandrabhaga Beach (near the cityof Konark) and Puri, suggesting its widespread distributionin Bay of Bengal waters.

The purpose of the present paper is four-fold: (1) torecord, for the first time, the presence and overwhelmingdominance of the potentially harmful marine planktonicdiatom Thalassiosira mala in Chilka Lake and other coastallocalities in the State of Odisha; (2) to clarify the correct dateof the validating publication for the name Thalassiosiramala by H. Takano; (3) to provide details of frustule

morphology for the Indian materials, including the details ofthe cingulum not previously reported, and to compare frus-tule morphology with other small species of Thalassiosiraalso present in Indian coastal waters, some known to formsimilar formless gelatinous colonies; and (4) to present anoverview of the global distribution of T. mala following therecent biogeographic classification of the coastal MarineEcoregions of the World (MEOW) proposed by Spauldinget al. (2007).

2. Materials and methods

2.1 Materials and collection sites

Net phytoplankton (25 lm mesh) samples were collected inDecember 2015 from three coastal locations in Odisha(formerly, Orissa) on the east coast of India (Bay of Bengal):

(1) Dolphin’s Cove (ca. 19.845� N, 85.479� E), nearSatapada Village, at the new mouth of Chilka Lake.This sampling site is located approximately 55 kmfrom Puri, Odisha, on the eastern side of Chilka Lake.Chilka Lake (also known as Chilika Lake) is the largestbrackish water lake in Asia. It is connected to the Bayof Bengal by a long (35 km), narrow channel in thestate of Odisha, India. Chilka Lake covers an area ofapproximately 900–1100 km2 (Raman et al. 1990).During the monsoon season considerable quantities offreshwater are discharged into the lagoon through anumber of rivulets and rivers, including the Daya,Bhargabi and Nuna rivers, which drain into thenortheast end; as a result, the area of the lake increasesby several hundred square kilometers during themonsoon season. The salinity varies from trace levelsto 36% (Panigrahi et al. 2009).

(2) Chandrabhaga Beach (ca. 19.865o N, 86.113o E),located three km east of the Sun temple of Konark, inthe Puri district in the state of Odisha, India.

(3) Puri, Odisha (19.813� N, 85.832� E), located 30 kmsouthwest of the previous site.

2.2 Preparation of material for light and electronmicroscopy

Samples were preserved in Lugol’s iodine in the field. Ali-quots of each sample were cleaned of organic matter using acombination of hydrogen peroxide and hot concentratedsulfuric acid followed by 10 rinses with de-ionized water.Small aliquots of a suspension of cleaned material weremounted in Naphrax for light microscopy (Prasad et al.1990), dried onto circular coverslips mounted on aluminumstubs with double-sided carbon tape and sputter-coated with

60 A K S K Prasad et al.

gold/palladium for scanning electron microscopy, or directlydried onto formvar-coated grids for transmission electronmicroscopy. Naphrax-mounted slides were examined using aLeica-DMLB microscope equipped with differential inter-ference contrast (DIC) and phase contrast (PC) optics.Photomicrographs of cleaned materials were taken usingT-max 100 black-and-white film and yellow-green filtersthen digitally captured using Photoshop software. Materialprepared for SEM was examined using a high-resolutionfield emission FEI Nova 400 Nano SEM with through-the-lens differential pumping for low vacuum imaging capabil-ities, operating at accelerating voltages of 5–10 kV, locatedat Florida State University. Material for TEM was examinedusing a FEI CM120 TEM operating at 120 kV, also at theFlorida State University.

2.3 Terminology of siliceous structures of diatomfrustules

We used the standardized terminology for siliceous struc-tures recommended by Anonymous (1975), von Stosch(1975) and Ross et al. (1979) in our descriptions of thediatoms discussed in this paper. The term marginal poreused by Takano (1965) is what is now known as a marginalstrutted process or fultoportula; mucus pore is now an ec-centric strutted process or fultoportula; surrounding holes orstruts (Takano 1976) are now satellite pores and the isolatedapiculus is the labiate process or rimoportula. Takano(1976, 1990) later adopted the standardized terminology forvalve processes, introduced by Hasle (1972a, p. 57) andRoss et al. (1979). Cingulum features are described using theterminology introduced by von Stosch (1975) and Fryxellet al. (1981).

3. Results

The following description is based on our observations offield material collected from Chilka Lake and other Odishacoastal material using TEM and field emission SEM as wellas DIC (LM).

Thalassiosira mala Takano 1983; p.31 (figs 1–5)Takano 1983. Bulletin of the Tokai Regional FisheriesResearch Laboratory 109: p. 31; Takano 1965. Bulletin ofthe Tokai Regional Fisheries Research Laboratory 42,p. 1 and 2, Fig. 1, a-m; Pl. I, figs 1–8SYNONYM: Thalassiosira decipiens f. levanderi (VanGoor) Takano 1956; p. 64 (= T. levanderi Van Goor sensuTakano); Thalassiosira pseudonana sensu Hasle andHeimdalHOLOTYPE (designated by Takano 1983; p. 31): Plate 1,fig. 3 of Takano 1965 (loc. cit.)

TYPE LOCALITY: Futomi coast, Chiba Prefecture,Sagami Bay and Tokyo Bay, Japan(Pacific Ocean)SIGNIFICANT REFERENCES: Takano 1965; p. 1;Takano 1976; p. 58, figs 1–18; Hasle 1976; figs 42 and43; Hallegraeff 1984; p. 497, fig. 2; Makarova 1988;p. 78, pl. 51, figs 4–5; Takano 1990; pp 210–211; Chenget al. 1993; p. 24, pl. 7, figs 52, 53; Licea 1994; Hasle andFryxell 1995; Hernandez-Becerril and Tapia Pena 1995;p. 548, figs 23–25; Hasle and Syvertsen 1996; p. 54,table 7, pl. 13 d-f; Ake-Castillo et al. 1999; p. 493,figs 17–19; Sar et al. 2002; p. 382, figs 7–10; Fryxell andHasle 2003; Park et al. 2009; Padmakumar 2010; figs 25aand b; Naya 2012; p. 148, figs 6, 34–35; Li et al. 2013;p.97, figs 75–77; Park et al. 2016; p. 41, fig. 22

3.1 Valve morphology (figures 1–5)

Small cells embedded in a vast expanse of gelatinousmaterial; no chains of sibling cells linked through centralchitinous fibers were observed (figure 1a). Four or five dis-coid plastids were easily seen in these small cells (figure 1e).Frustules short barrel-shaped (drum-shaped), with roundedends in girdle view (figure 2a). Valve diameter variesbetween 3.6 and 9.8 lm, but the pervalvar axis of fullydeveloped frustules is fairly consistent (5.8 to 6.9 lm).Areolae are hexagonal towards the center, becoming rect-angular towards the valve margin, arranged in radial rows, orin short fasciculated bundles with the rows running parallelto the central row, or in linear or curved tangential rows.There are 4 areolae in 1 lm near the center, 5 in 1 lm at thevalve margin; this differs from the 2.5–3.0 areolae in 1 lmin the type material (Takano 1965). The valve structureconsists of loculi with foramina on the exterior (figure 3c–f),and vela (cribra) on the interior (figure 4c and d). There are9–12 cribral pores in each cribrum, without any definitepattern of arrangement (figure 4f and g). A marginal ring offultoportulae is present with 12–22 fultoportulae per valve.These are closely spaced, 0.5 to 1.4 lm, or 2–4 areolaeapart, 6–11 fultoportulae in 10 lm; Takano (1965) reports4–10 marginal fultoportulae in 10 lm. The fultoportulaeopen to the exterior through a rimmed pore within a hyalinespace (figures 2c and 3f). Internally, the fultoportulae areoperculate, each surrounded by four satellite pores (figure 4dand e). A single fultoportula with three or four satellite poresis located on the valve face, usually 3–4 areolae from thecenter (figure 4a, b, f and g). There is no central fultoportula.A single rimoportula (labiate process) lies within the ring ofmarginal fultoportulae between two adjacent fultoportulae,opening to the exterior through a rimmed pore withoutexternal tube (figures 4b, d and e). The labiate structure isusually radially directed, rarely obliquely, oriented.

Marine diatom Thalassiosira mala from Odisha, India 61

3.2 Cingulum morphology (figure 2)

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); theimmature hypocingulum includes at least two bands (fig-ure 2a). The valvocopula is clearly areolate in the advalvarregion, with 4–6 somewhat irregular rows of pores, 10–12pores in 1 lm; the abvalvar area is free of areolation (fig-ure 2b–c). In a detached cingulum, a suggestion of anantiligula was noticed. The single copula is also perforated,but by only a single row of pores, 11–12 in 1 lm; the twopleurae are hyaline (figure 2b–c). The openings of thealternate bands are arranged in a dextral pattern sensuFryxell et al. (1981); in other words, the openings of thebands on one side of the cell are offset so that alternateopenings spiral to the right in an abvalvar direction. Thisobserved dextral pattern appears to be consistent in thepopulations examined under scanning electron microscope.The above structure of cingulum in T. mala follows the basicpattern of the cingulum in the investigated marine species of

Thalassiosira: an ornate valvocopula, a copula and severalpleurae (Fryxell et al. 1981, 1984; Prasad et al. 1993, 2011).

3.3 Comments on nomenclature and validation

Takano (1965; p. 1, fig. 1, pl. 1, figs 1–8) provided Englishand Latin descriptions of Thalassiosira mala, along with linedrawings and scanning and transmission electron micro-graphs of populations from Japanese coastal waters. TheEnglish version of Takano’s description is reproduced herefor reference. In LM: ‘Cells very small, 4–10 l in diameter,disc-shaped or box-like, connected with mucilage threadeach other in formless masses. Valves flat with roundedmargins and a spinule-like marking near the margin.’ In EM:‘Valves with a row of marginal pores (bases of apiculi (?),4–10 in 10 l. The marginal pore consists of a central mainpore and four surrounding holes. A mucous pore, fromwhich probably a thread connecting cells each otherextrudes, consists of a central main pore and three (rarelyfour) surrounding holes, located in the subcentral area of

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 bediscerned in some of the valves. (e) Lugol’s-fixed material showing 4–5 plastids per cell (Scale bar = 50 lm in a, 25 lm in b and 10 lm inc–e).


valves about 1/5–1/2 of the radius apart from the center. Amarginal pore–like marking (base of an isolated apiculus?)situated on almost same radial line with the subcentralmucous pore. Areolae hexagonal, arranged in radial, bundledline, or for rather many valves, in linear rows at the centralpart and thereafter radial to the margin with rounded tan-gential rows concave against the margin of numerousirregular systems. Areolae ca. 2.5–3 in 1 l in the center, 5 in1 l near the margin. Marginal striae ca. 6 in 1 l.’ The abovedescription focuses on valve morphology; details of thecingulum were not provided in any of Takano publicationson T. mala (Takano 1965; 1976 and 1990).

During the 8th International Botanical Congress, theInternational Code of Botanical Nomenclature (Paris Code)was amended to include a specific requirement for thedesignation a nomenclatural type for each new taxon of therank of family or lower beginning January 1, 1958; before

a name could be considered validly published (see Lan-jouw et al. 1956; Principle II and Article 35). Takano mayhave been unaware of this change in the Code, since heneglected to designate a nomenclatural type for Thalas-siosira mala (Takano 1965; p. 1) and for several otherspecies he described during the 1960s and 1970s. As aresult, although the detailed descriptions and figures pro-vided by Takano (1965) are sufficient for the positiveidentification of populations T. mala, the name of thespecies was not validly published. At some point Takanobecame 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 scanningelectron micrograph (Takano 1965; plate 1, fig. 3) as theholotype (Takano 1983; p. 31). This met the requirementsof 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 lastrequirement (McNeill et al. 2012; Article 31.1), the correctdate of publication of Thalassiosira mala Takano is 1983;not 1965. This issue was indicated by the late Dr. Reimeron the note card for Thalassiosira mala in the database ofthe Academy of Natural Sciences, Philadelphia (see theDiatom New Taxon File at ANSP, http://symbiont.ansp.org/dntf/) and is further clarified in the Index NominemAlgarum (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 ofpublication date (see also Takano 1990).

4. Discussion

4.1 Presence of Thalassiosira mala in Indian waters

Previous investigations in Chilka Lake focused on phyto-plankton abundance in relation to water quality, especiallysalinity. The initial studies of the algal flora Chilka Lakewere conducted by Biswas (1932), followed by Roy (1954),Patnaik (1978), Raman et al. (1990), Adhikary and Sahu(1992), Rath and Adhikary (2005), and Mohanty andAdhikary (2013). All of the studies documented the algalflora and seasonal variation in salinity gradients the lagoon.Recent openings of Chilka Lake to the Bay of Bengal watersfacilitated extensive mixing of the freshwater in the lagoonwith seawater, resulting in a wide range of hydrologic con-ditions (Nayak and Behera 2004; Panigrahi et al. 2009;Mohanty et al. 2009). For example, Raman et al. (1990)identified 97 species of microalgae in Lake Chilka on thebasis of light microscopy. From their analyses of the distri-butions of the various species, they recognized five differentecological zones in Chilka Lake, each with a characteristicassemblage of phytoplankton species. Included in the spe-cies lists was an undetermined species of the fultoportulate

Figure 2. Thalassiosira mala from Chilka Lake, Odisha, India.Acid-cleaned. SEM. Girdle view. Structure of the valvocopula andcingulum are clearly visible in all images. Valvocopula (Vc) isareolate with 4 rows of pores on the advalvar side, hyaline on theabvalvar side. The copula (Co) has a single row of pores. Pleurae(Pl1, Pl2) appear completely hyaline. All bands are open with theopening arranged in dextral pattern. There is a poorly developedantiligula on the valvocopula in (b) (Scale bars = 1 lm).


http://symbiont.ansp.org/dntf/

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http://ucjeps.berkeley.edu/INA.html

freshwater diatom genus Stephanodiscus Ehrenberg (listedas ‘Stephanodiscus sp.’). This species was present in theoligohalobe and mesohalobe sections of the lagoon, where itwas sometimes the dominant member of the phytoplankton;

unfortunately, they did not provide any illustrations ordescriptions of the species. They did not include any rep-resentatives of the genus Thalassiosira in their species list.More recent studies have included numerous brackish water

Figure 3. Thalassiosira mala from Chilka Lake, India. Acid-cleaned. SEM. Valve exterior. (a) Low-magnification image showing a massof valves. (b) Higher magnification of the same mass. (c–e) Images of single valves showing the arrangement of marginal processes (whitearrow heads) and variations in the arrangement of areolae. Valve face fultoportula (white arrow) appears as circular opening just underhalfway from the center of the valve to the valve margin. The opening of the rimoportula is obscure. (f) Detail of the valve margin showingthe rim of silica bordering the external openings of the fultoportulae and the surrounding hyaline areas. (Scale bars = 50 lm in a, 5 lm inb, 2 lm in c–e and 1 lm in f).


and marine diatoms in Chilka Lake, including fultoportulatecentric diatoms of the genera Cyclotella (Kutzing) Brebis-son, Skeletonema Greville, Stephanodiscus, and Thalas-siosira. Representatives of Thalassiosira mentioned include

T. eccentrica (Ehrenberg) Cleve emend. Fryxell and Hasleand T. subtilis (Ostenfeld) Gran emend. Hasle, among others,but not Thalassiosira mala (Adhikary and Sahu 1992;Mohanty and Adhikary 2013).

Figure 4. Thalassiosira mala from Chilka Lake, India. Acid-cleaned. SEM. Valve interior. (a) Two valves at low magnification. (b, d andf) Details of the right-hand valve in (a). (d) Areolae with domed cribra, position of the rimoportula, the four satellite pores and pore coverssurrounding the marginal fultoportulae. (f) The valve face fultoportula with four satellite pores and pore covers. (c) Note the abnormalspacing 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 coverssurrounding the valve face fultoportula (Scale bars = 3 lm in a, 2 lm in b, 1 lm in c, 500 nm in d–g).


Figure 5. Thalassiosira mala from Chilka Lake, Odisha, India. Acid-cleaned. TEM. (a-c) Complete valves illustrating variation in thearrangement of areolae. Note the rows of areolae in sectors, decrease in size and the change in the overall shape of the areolae from thecenter 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 fultoportulawith three satellite pores. (e and f) Details of the cribral structure. Note the fultoportula with four satellite pores in (f). (Scale bars = 1 lmin a–c, 500 nm in d–f).


The present study, then, provides the first record of Tha-lassiosira mala in the region. Because the structure of T.mala is too fine to be resolved even in DIC-LM, we relied onSEM and TEM observations to determine key features of thevalve, in particular, the density and arrangement of areolaeand the arrangement of fultoportulae and rimoportulae. Therecognition of T. mala in Chilka Lake and the coastal watersof the Bay of Bengal demonstrates once again the inherentdifficulty of identifying small species of Thalassiosira bylight microscopy alone; electron microscopy is absolutelynecessary for the accurate identification of very small andweakly silicified diatoms, even those known to be harmful toorganisms higher in the food chain and, possibly, to humansas well. These small diatoms represent an important potentialsource of organic carbon for higher trophic levels because oftheir potential for rapid growth (Fryxell 1975). The absenceof reports of T. mala from this and other coastal waters ofIndia until recently may largely reflect on the limitations ofconducting investigations using light microscopy alone foridentification. Small centric diatoms are often overlooked orignored because of the challenge their small size can pose to

investigators. In LM, the formless gelatinous colonies of T.mala can be easily confused with similar disrupted coloniesof the haptophyte Phaeocystis Lagerheim (Takano 1956;Hasle 1976; Fryxell and Hasle 2003). Therefore, it is pos-sible that the lack of reports of T. mala from Chilka Lake andother localities on the east coast of India may have resultedfrom the methodologies used. However, it is also possiblethat T. mala was introduced to the region only recently, andthe dominance we noted in our samples was a response ofthe species to favorable local conditions. An examination ofarchived samples from the region may shed some light onwhich of these options is the more likely.

More than 15 species of Thalassiosira are known, or atleast suspected, to form gelatinous colonies (Fryxell andHasle 2003). These include T. curviseriata Takano, T. deli-catula Ostenfeld emend. Hasle, T. diporocyclus Hasle, T.fragilis Fryxell, T. fryxelliae Sunesen and Sar, T. gravidaCleve, T. mala, T. mediterranea (Schroder) Hasle, T. minimaGaarder emend. Hasle, T. minuscula Krasske emend. Hasle,T. minicosmica Lee and Park in Park and Lee, T. oceanicaHasle, 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), 8Hallegraeffand Jeffrey (1984), 9Makarova (1988), 10Licea (1994), 11Cheng et al. (1993), 12Hernandez-Becerril and Tapia Pena (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 Frassao-Santos (2011), 20Licea et al. (2011), 21Li et al. (2013), 22Park et al. (2016), 23Nienow, unpublished observations.


subtilis, T. sp. cf subtilis sensu Fryxell et al. 1984; T. tubiferaFryxell, and T. weissflogii (Grunow) Fryxell et Hasle (alsoknown as Conticribra weissflogii (Grunow) K. Stachura-Suchoples and D.M. Williams) (Fryxell et al. 1984; Hasleand Fryxell 1995; Fryxell and Hasle 2003; Sunesen and Sar2004; Park and Lee 2015). Additional species may producegelatinous colonies under certain conditions as suggested byHustedt (1926)—Takano noted that the characteristicgelatinous colonies of T. mala were scarcely recognizable inlaboratory-grown cultures (Takano 1965) and Hasle (1983)suggested that certain conditions in upwelling areas appearto favor the formation of gelatinous colonies.

As an aid for identification, Hasle and Fryxell (Fryxellet al. 1984; Hasle and Fryxell 1995; Fryxell and Hasle 2003)separated the gelatinous-colony-forming species of Thalas-siosira into three morphological groups based on cell sizeand shape and process patterns: 1) larger species with dome-shaped valves, radial rows of areolae arranged in sectors, onecentral fultoportula, at least one marginal ring of fultopor-tulae and an additional ring of fultoportulae on the valveface, as in T. diporocyclus, T. fragilis, T. subtilis and T.tubifera; 2) species with flattened valves and stronglydeveloped external extensions of the fultoportulae, as in T.curviseriata, T. delicatula, T. gravida, and T. weissflogii; and3) smaller species with rounded valves and poorly developedexternal extensions of the marginal fultoportulae, as in T.mala, T. mediterranea, T. minuscula, T. partheneia and T.proschkinae.

At least three gelatinous-colony-forming species, T. mala,T. partheneia and T. subtilis have thus far been reported fromthe Bay of Bengal and Arabian Sea waters (Simonsen 1974;Raman and Prakash 1989a, b, Sahu et al. 2010; 2012;Padmakumar 2010; present study).

4.2 Structure of Thalassiosira mala

The process pattern in our material, a single eccentric valveface fultoportula, one ring of marginal fultoportulae and asingle marginal rimoportula, is similar to that reported in theliterature for T. mala, especially as described in the proto-logue (Takano 1965) and in later reports (Takano 1976;1990). Fultoportulae in T. mala do not have well-developedexternal extensions, however, the exterior openings of thefultoportulae do have a thickened siliceous rim. All speciesknown to form a gelatinous matrix have operculate fulto-portulae (Fryxell and Hasle 1979). This is also the case formany of the Thalassiosira species previously investigatedand for other fultoportulate diatom genera including De-tonula Schutt ex De Toni (Hasle 1973b), Lauderia Cleve(Syvertsen and Hasle 1982), Livingstonia Prasad (Prasad andNienow 2011), and Skeletonema (Hasle 1973b, Medlin et al.1991; Sarno et al. 2005). Fryxell et al. (1984) consideredoperculate fultoportulae and the lack of external

development of the fultoportulae as primitive characters.Takano (1965) reported that the central tube of the valve faceprocess was typically surrounded by three satellite pores forspecimens from Japanese waters; however, he observed aspecimen from Gulf of Mexico in which the central tube wassurrounded by four satellite pores. In the present study ofOdisha material, valve-face fultoportulae with three or foursatellite pores were seen. All fultoportulae were operculate.

Cingulum morphology in T. mala is described here for thefirst time. The general form of the cingulum – a valvocopulawith several rows of pores, a copula with a single row ofpores and several unstructured pleurae—is similar to that ofmany of the species of Thalassiosira investigated in SEM(Fryxell et al. 1984), including other gelatinous-colony-forming species, such as T. subtilis, T. diporocyclus, T.minuscula, T. tubifera, and T. partheneia (Hasle 1972a, b;Schrader 1972; Fryxell 1975; Hasle 1983; Fryxell et al.1984). In two other species, T. weissflogii and T. fragilis, allof the bands are areolate (Fryxell et al. 1981; 1984). Hyalinepleurae are considered to be an advanced characteristic inThalassiosira (Fryxell et al. 1984). Thus, the valve shapes,process patterns, band structures of the group of gelatinouscolony-forming species including T. mala exhibit a numberof characteristics that may be construed as primitive basedon our current understanding of the concepts within thegenus (Fryxell et al. 1984). The dextral pattern of alternateband openings observed in T. mala is common in species ofThalassiosira (Fryxell et al. 1981; 1984; Hasle and Lange1989; Syvertsen and Hasle 1984; Prasad et al. 1993; 2011).Fryxell et al. (1981) suggested that band orientation could bea useful tool in the assessment of phylogenetic relationships.

4.3 Comparison of Thalassiosira mala with similarspecies from the coastal waters of India

Thalassiosira mala can be easily confused with anothernanoplanktonic diatom, T. pseudonana Hasle and Heimdal(Hasle and Heimdal 1970; p. 564, figs 27–38). Thalassiosirapseudonana was originally described as Cyclotella nanaHustedt based on material collected from a freshwaterlocality. Since then it has also been isolated from a numberof coastal areas, and is currently considered to be euryhaline.The two species share a number of similar features,including small size, approximately 4 to 9 lm in diameter inboth species, the presence of a ring of marginal fultoportulaeand an eccentric valve face fultoportula. The two speciesclearly differ in a number of significant features, however.Valves of T. pseudonana are very weakly silicified, withradial ribs but with only poorly developed tangential wallsdefining separate areolae. Further, the marginal fultoportulaeeach have three satellite pores and the valve face process hasonly two satellite pores (Hasle and Heimdal 1970; figs 35and 38). Finally, T. pseudonana does not form gelatinous


colonies, but is invariably found as solitary cells. In Tha-lassiosira mala, on the other hand, valves have well-devel-oped locular areolae, the marginal fultoportulae have foursatellite pores, the valve face process typically has three,rarely four, satellite pores, and the cells are embedded in acolonial gelatinous matrix. Hasle and Heimdal (1970;p. 567) regarded the valve features, particularly of theabsence of radial ribs or the presence of poorly developedareolae as insufficient to justify the distinction between T.mala and T. pseudonana and briefly treated T. mala as a latersynonym of T. pseudonana. Takano (1976) rejected theircomparison and argued that his species was clearly distin-guishable on the basis of its ability to form gelatinouscolonies, the consistent occurrence of a single eccentricvalve face fultoportula and well-developed radial rows ofareolae. Subsequently, Hasle (1976) and Hasle and Syvert-sen (1996) treated T. mala and T. pseudonana as separatetaxa, although they did consider T. pseudonana to be ahighly variable species. It is worth noting that Raman andPrakash (1989a, b) considered T. pseudonana to be bloom-forming and locally dominant on the east coast India, nearVisakhapatnam Harbor and in the Bay of Bengal, not farfrom the present study sites of Odisha. Unfortunately, butthey did not include descriptions or illustrations of the fieldpopulations that could be used to verify the identity of thespecies. They and their colleagues did not record T. mala ineither Visakhapatnam Harbor (Raman and Prakash 1989a, b)or Chilka Lake (Raman et al. 1990).

Ostenfeld (1899; p. 59, cited in Hasle 1972b, p. 111)provided the first description of Thalassiosira subtilis underthe name Podosira ? subtilis n. sp. It was classified as a trulyoceanic plankton from the temperate Atlantic Ocean, char-acterized as small, with a cell diameter of 16–32 lm, weaklysilicified, with no distinct structures visible in LM; the cellswere embedded in homogenous, formless gelatinous sub-stance. Gran (1900; p. 117), with some reservation, trans-ferred the species to Thalassiosira. Illustrations of what wasconsidered to be T. subtilis in Hustedt, (1930, fig. 266) andCupp (1943, fig. 23) were generally used for identificationuntil Hasle (1972b) examined the valve structure, anddescribed the areolar structure and arrangement and positionof fultoportulae and rimoportulae. She also amplified thedescription of the species based on electron microscopy andtypified the name using Ostenfeld’s original material.According to Hasle (1972b) valve diameter ranges from 15to 32 lm, the areolar density is about 30 in 10 lm with theareolae arranged in sectors, with rows parallel to medianrow. There is a single rimoportula located at some distancefrom the margin, one marginal ring of fultoportulae,2.7–3.6 lm apart, scattered intermediate valve-face fulto-portulae, and a single eccentrically-located subcentral ful-toportula. No details of the satellite pores surrounding thecentral tubes of the fultoportulae were provided in theemended diagnosis (Hasle 1972b). T. subtilis was frequently

encountered and mentioned as a dominant diatom species inecological investigations of phytoplankton from the Indiancoastal waters of the Bay of Bengal, the Arabian Sea and theLaccadive (Lachadive) Sea (Raman and Prakash 1989a, b,Sahu et al. 2010, 2012; Baliarsingh et al. 2013, 2015; andmany others). In the absence of accurate descriptions of thefrustule morphology of specimens of T. subtilis encounteredin Indian localities, it is difficult to comment on the identityof the species, let alone compare its populations with thepopulation of T. mala from Chilka Lake and Odisha coastallocations. Since T. subtilis was the first species of the genusto be reported as forming gelatinous colonies (Ostedfeld1899), it is possible that other gelatinous-colony-formingspecies, such as T. mala, may have been included in thereports. T. mala from Chilka Lake and other sites can easilybe differentiated from T. subtilis in having much smallercells (2–12 lm in diameter vs. 15–49 lm in T. subtilis), onlyone marginal ring of fultoportulae, and no intermediate valveface fultoportulae; both species have a single eccentricallylocated subcentral fultoportula (Hasle 1972b, Fryxell andHasle 2003). T. subtilis is considered to be oceanic (Osten-feld 1899; Hasle 1976) whereas T. mala, by and large, hasonly been recorded from coastal waters and regions ofupwelling (Takano 1956, 1965, 1976, 1990). Paul et al.(2008) reported an unidentified ‘Thalassiosira sp’ as one ofthe dominant species in the Bay of Bengal in 2002 and 2003;but provided no descriptions or illustrations to comment onits identity.

Thalassiosira partheneia is characterized by small cells, 4to 14 lm in diameter, with an areolar density of 38–50 in10 lm, a marginal ring of fultoportulae with long internalextensions, and a single marginal rimoportula (Schrader1972; Hasle 1983). T. mala from the Odisha localitiesresembles T. partheneia in having small cells embedded ingelatinous material and in areola density, but differs in thestructure of the marginal fultoportulae. T. partheneia has notbeen recorded from the east coast of India, but has beenreported in bloom concentrations from west coast (Pad-makumar 2010).

Thalassiosira marginata is a brackish water species fromthe River Cooum, Madras (now Chennai), which is influ-enced by waters from the nearby Bay of Bengal.Venkataraman (1939; p. 297, 298, figs 12, 13) describedmassive concentrations of T. marginata, which imparted abrownish-yellow color to the waters. The species is char-acterized in LM by extremely small cells, measuring 4 to6 lm in diameter, with 18–22 marginal punctae; no otherfeatures were visible in LM. The type material is notavailable so details of fine structure of the valve, includingthe structure of marginal processes and areolae, cannot bedetermined, precluding any speculations on its genericplacement, let alone its species interrelationships.Venkataraman (1939) did not mention the presence of chainsof cells wherein sibling cells are joined by threads extruded


through the central processes; such chains are characteristicof many the species of Thalassiosira. Since its firstdescription, T. marginata has only rarely been reported byother investigators monitoring Bay of Bengal waters (Ramanand Prakash 1989a, b). Takano (1956; p.63) also drewattention to small cells of T. marginata and compared themwith T. mala (as a form of T. decipiens cf. levanderi).

4.4 Biogeography of Thalassiosira mala

The massive concentrations of T. mala seen in Chilka Lakeand in coastal localities from Odisha suggest it is actuallywidely distributed in the Bay of Bengal and is able to formextensive blooms in the region. In contrast, the presence ofT. mala in the Arabian Sea on the west coast of India hasbeen known for some time. Hasle (1976; p. 331, figs 42, 43)provided the first record of the species in Indian Oceanwaters, including SW coast of India, and in east Africanwaters. More recently, Padmakumar (2010; p. 68, fig. 25)reported a bloom (6.74 9 106 cells/L) of T. mala offAzheekode, near Kochi, on the southwest coast of India (10�28.43 N, 75�36.10 E) during the monsoon period of 2006. Inthis case the bloom of T. mala was followed by a bloom ofyet another gelatinous-colony forming species, T. parthe-neia. Unfortunately, no descriptions of the bloom popula-tions were provided, precluding comparison withpopulations of T. mala from the Bay of Bengal. It is possiblethat the species is underreported in Indian waters— most ofthe earlier phytoplankton investigations relied almostexclusively on light microscopy. Additional recordsexpanding its distribution in Indian waters are likely as theuse of electron microscopy increases.

Outside India, Thalassiosira mala is well-distributed incoastal waters around the world (table 1; figure 6). Hasle(1976; figs 39, 42, 43) reported mass occurrences in suchwidespread localities as Trinidad, the southern Atlantic, westcoast of India (Arabian Sea), the Gulf of Mexico, and theNorth Sea. Based on these reports, she initially characterizedT. mala as a biogeographically cosmopolitan species (Hasle1976). Later, as new information became available, she andFryxell (Hasle and Fryxell 1995; Fryxell and Hasle 2003)considered it to be restricted to tropical and temperatewaters, and established the northern boundary for T. mala atabout 58�–59� N and the southern boundary at about 35� S(Hasle and Fryxell 1995; Fryxell and Hasle 2003). Park et al.(2016), working with 44 species of Thalassiosira fromKorean coastal waters, were able to distinguish four bio-geographic groups; T. mala was placed in a group of 15species considered to be characteristic of temperate totropical waters.

Recently Spaulding et al. (2007) proposed a biogeo-graphic classification system for coastal marine ecoregionsof the world (MEOW), recognizing a total of 232

ecoregions, 62 provinces and 12 realms. In this system,Indian coastal regions known to harbor T. mala are includedin the Eastern India ecoregion of the Bay of Bengal province(the present study), and the Western India ecoregion of theWest and South Indian Shelf province (Hasle 1976; Pad-makumar 2010); both provinces are subdivisions of theWestern Indo-Pacific realm. A comparison of publishedreports verified by electron microscopy with MEOW sug-gests that T. mala may have a narrower distribution thansuggested by Fryxell and Hasle (2003). Reports of T. malaare restricted to about 15% of the world’s tropical/temperatecoastal ecoregions (26 of the 192 non-polar ecoregionsrecognized), 33% of the provinces (18 of 57), nested within8 of 10 realms (see table 1 and figure 6).

A striking feature of the distribution map (figure 6) is theabsence of literature records of T. mala from the entire SouthPacific, including the western coast of South America (seeRivera 1981, 1983) and from much of the eastern coastlineof the Atlantic. This raises the question whether T. mala hasa discontinuous distribution or whether it is consistentlyoverlooked through the misapplication of the names of betterknown species, e.g. T. subtilis, for any species of Thalas-siosira seen in gelatinous colonies. Diatom diversity must beassessed by competent taxonomic authorities; the misappli-cation of names can lead to a false perception of diatomdiversity, biogeographical patterns, and the rarity of certainforms (Mann and Droop 1996). We believe that Thalas-siosira mala is actually far more widely distributed than thecurrent records show, and that a careful examination usingelectron microscopy will lead to additional reports within thelatitudinal boundaries suggested by Fryxell and Hasle(2003).

4.5 Thalassiosira mala as a harmful alga

Thalassiosira mala has been linked to shell-fish mortality.The first recorded instance took place in Tokyo Bay in 1951.In this instance, extensive mucilaginous colonies of T. mala,initially identified as T. decipiens var. levandari, caused thewaters of Tokyo Bay to turn yellowish brown (Takano 1956,p. 65). At the same time a massive die-off of cultured shell-fish took place (Takano 1956). Takano (1956) attributed thedeaths to the presence of the gelatinous substances producedby T. mala, possibly clogging the gills of the shellfish,perhaps working in conjunction with poor water qualityconditions. The reported loss, according to Takano’s report(1956) amounted to ¥58 million (approximately US$161,000, based on the currency exchange rate in effect atthe time, approximately US $1,500,000 in today’s dollars).Hasle and Syvertsen (1996, p. 54) regarded T. mala asprobably the first marine planktonic diatom linked to thedeath of shellfish. Even though T. mala blooms have beenreported from wide geographical localities, no toxin has ever


been reported from the species. In fact, although severalplanktonic and benthic species of the raphid diatom genera,Amphora Ehrenberg and Pseudo-nitzschia Hustedt, in par-ticular, have been shown to produce the neurotoxin domoicacid, which has been proved to be harmful to humans,mammals, birds, anchovies and other marine biota (Hasleand Fryxell 1995), no centric diatoms are known to producedomoic acid or any other toxins harmful to higher trophiclevels. However, according to Fryxell and Hasle (2003), anydiatom species frequently reported in bloom numbers shouldbe regarded as potentially harmful. Indeed, some centricdiatoms, including several species of Coscinodiscus andPalmerina hardmaniana (Greville) Hasle (as Hemidiscushardmanianus (Greville) Mann), have been associated withthe heavy mortality of fish and invertebrates on the east coastof India (Subramanian and Purushothaman 1985; Mathewet al. 1988; Padmakumar et al. 2007). We are not aware ofany reports of harmful effects associated with the over-whelming dominance of Thalassiosira mala we noted inDecember 2015 on the productivity of Chilka Lake in thehigher trophic levels.

The highly productive, yet unique and fragile ecosystemof Chilka Lake, with its estuarine characteristics, containsrich fishery resources, which sustain the livelihoods ofincreasingly dependent coastal communities (Mohanty et al.2009). This and other such productive water bodies must becarefully monitored for known and potentially harmful algaethat may become established in the lake and subsequentlyimpact the health of the aquatic system. Given the economicimportance of the commercial fishery along the vast coast-line of India, estimated as over 7,500 km (Mukhopadhyay

and Karisiddaiah 2014), and the frequent occurrences ofharmful algal blooms (HABs) and nuisance plankton bloomswith adverse impacts on fishery and human health, accurateidentification of microalgae by trained taxonomists isimportant not only for aquatic health management decisionsbut also for meaningful conservation programs and biogeo-graphic considerations. Since many of the known harmfulalgal bloom species, including diatoms, are cosmopolitanwithin their latitudinal ranges (Taylor 1987), familiarity withrecent taxonomic guides and identification manuals fromdiverse areas of the globe, in addition to regional guidesbased on indigenous populations, is required.

Acknowledgements

AKSKP is grateful to A. K. Madhusudhan, Mridhula Babu,Jayalakshmi Kamesh, A. Ramesh, Saroja Rupanagudi, andVijaya Ramesh for their assistance with logistics and fieldcollections. The authors thank Dr. Duncan Sousa, Coordi-nator of the Biological Science Imaging Resource at FloridaState University, for his technical assistance with transmis-sion electron microscopy.

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Corresponding editor: ULLASA KODANDARAMAIAH


https://doi.org/10.1029/2009gb003680

https://doi.org/10.1029/2009gb003680

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