Marine Pollution Bulletin 85 (2014) 306–311

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Impact of multispecies diatom bloom on plankton community structure in Sundarban mangrove wetland, India Sejuti Naha Biswas a, Dibyendu Rakshit a, Santosh Kumar Sarkar a,⇑, Ranjit Kumar Sarangi b, Kamala Kanta Satpathy c a b c

Department of Marine Science, University of Calcutta, Calcutta, India Marine Biology Division, Marine, Geo and Planetary Sciences Group, Space Applications Centre (ISRO), Ahmedabad, India Environment and Safety Division, Indira Gandhi Centre for Atomic Research, Kalpakkam 603102, Tamil Nadu, India

a r t i c l e

i n f o

Article history: Available online 24 June 2014 Keywords: Diatom bloom Water quality Tintinnids Species diversity Sundarban wetland

a b s t r a c t A multispecies bloom caused by the centric diatoms, viz. Coscinodiscus radiatus, Chaetoceros lorenzianus and the pennate diatom Thalassiothrix frauenfeldii was investigated in the context of its impact on phytoplankton and microzooplankton (the loricate ciliate tintinnids) in the coastal regions of Sagar Island, the western part of Sundarban mangrove wetland, India. Both number (15–18 species) and cell densities (12.3  103 cells l1 to 11.4  105 cells l1) of phytoplankton species increased during peak bloom phase, exhibiting moderately high species diversity (H0 = 2.86), richness (R0 = 6.38) and evenness (E0 = 0.80). The diatom bloom, which existed for a week, had a negative impact on the tintinnid community in terms of drastic changes in species diversity index (1.09–0.004) and population density (582.5  103 to 50  103 ind m3). The bloom is suggested to have been driven by the aquaculture activities and river effluents resulting high nutrient concentrations in this region. An attempt has been made to correlate the satellite remote sensing-derived information to the bloom conditions. MODIS-Aqua derived chlorophyll maps have been interpreted. Ó 2014 Elsevier Ltd. All rights reserved.

Diatom blooms have been of major global interest during the last two decades. Phytoplankton has 3400–4100 microalgae species, of which 300 species can produce blooms (Smayda, 1997; Naz et al., 2012). Accordingly, different species might be involved in algal blooms in different regions (Hu et al., 2011). The health of estuaries and coastal oceans and their resilience towards extreme phytoplankton blooms varies considerably in different parts of the world (Clarke et al., 2006; Garnier et al., 2010; Seitzinger et al., 2010). Coastal upwelling and land runoff are the most important factors for the phytoplankton blooms (Mathew et al., 1988), and consequently, nutrient levels are highest near the continents (Sarangi et al., 2005a). Most estuaries in India are moderately to highly eutrophic, and it has been observed that fresh water discharge during the spring freshets enhances the nutrient load from the drainage basin and intensifies the phytoplankton bloom (Admiraal et al., 1990; Van Bennekom and Salomons, 1981). Although most diatom blooms are non-toxic, some more dangerous blooms include toxic species of phytoplankton that kill ⇑ Corresponding author. Present address: 35, B.C. Road, Department of Marine Science, University of Calcutta, Calcutta, India. Tel.: +91 98 3124 2492; fax: +91 33 2461 4849. E-mail address: [email protected] (S.K. Sarkar). http://dx.doi.org/10.1016/j.marpolbul.2014.04.015 0025-326X/Ó 2014 Elsevier Ltd. All rights reserved.

fish, invertebrates, and often pose an immediate health problem to humans. Non-toxic blooms can also have detrimental effects on the local marine ecosystem and cause a permanent reduction in the area’s species diversity. Incidence of algal blooms and discolorations of water in the Indian seas have been reported by Devassy and Nair (1987). Studies on algal blooms using the remote sensing satellite data along the west coast of India have been worked out by Sarangi et al. (2005a), and the type of bloom caused by the Trichodesmium sp. has been confirmed with satellite near-infrared channels reflectance and in situ observations (2005b). Indian Sundarban, the continuous tract of mangrove forest, is a part of the estuarine system of the River Ganges on the northeast coast of the Bay of Bengal. It covers a total area of 9630 km2, the total land area is 4143 km2 (including exposed sandbars of 42 km2) and the remaining water area of 1874 km2 encompasses rivers, small streams and canals. The area is covered with thick mangroves and is subdivided into a forest sub-ecosystem and a 1781 km2 aquatic sub-ecosystem in which phytoplankton has a huge importance. The area has a subtropical monsoon climate with an annual rainfall of approximately 1600–1800 mm as well as several cyclonic storms. This mangrove ecosystem of the Indian subcontinent is well known not only for the aerial extent but also

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for its species diversity, including numerous species of phytoplankton, zooplankton, micro-organisms, benthic invertebrates, mollusks, amphibians and mammals (Gopal and Chauhan, 2006). Among the vast array of diatoms and dinoflagellates identified in this region, Coscinodiscus radiatus was one of the most common species, and it predominated almost throughout the year. In January, 2013, this species created a severe bloom at a confined region of Sagar Island, the western part of Sundarban, along with two other diatoms: viz. Thalassiothrix. frauenfeldii, which is common in both temperate and tropical regions (Sahu et al., 2012), and Chaetoceros lorenzianus, the chain-forming marine diatom (Grunow, 1863). Complete discoloration (deep greenish color) of the water was noted for this multi-species diatom bloom where C. radiatus, a supportive species for paleoecological study (Liu et al., 2013), was predominant, accounting 5 times higher concentration than the other two species. Based on the occurrence of the bloom, a distinct sampling site (Light House) was identified at the southern tip of Sagar Island, as shown in Fig. 1 (average depth 8.0–9.8 m). Collection was conducted covering three different time phases of the bloom: (i) before the occurrence of bloom event (14th December, 2012–3rd January, 2013); (ii) during the bloom (4t–10th January, 2013); and (iii) after the bloom (25th January, 2013). It is worthwhile to mention that the bloom phase also coincided with the Gangasagar Annual Festival (GAF), held during 14–20th January, 2013 when 6 lakh people converged at this point to take their holy bath, which directly affected the water quality characteristics (Hazra et al., 2012). Phytoplankton net (20 lm mesh size) was trawled on the surface water for approximately 20 min, and collected samples were immediately preserved in 4% buffered formalin solution. An aliquot sample of 1 ml was taken in a Sedgwick-Rafter counting cell for quantitative and qualitative analyses (Kellar et al., 1980) and examined under a binocular microscope. Phytoplankton identification was performed following standard taxonomic monographs, such as Desikachary (1987) for diatoms, Subramanian (1968) for

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dinoflagellates and Fristch (1935) for green and blue-green algae (cyanobacteria). For tintinnids, 1000 ml of surface water samples were collected by pre-cleaned plastic bottles and immediately preserved with Lugol’s solution (2% final concentration) and stored refrigerated and in darkness except during transport and settling (Dolan et al., 2002). The particles were concentrated to a volume of 25 ml by settling (Godhantaraman, 2002), after which they were taken drop by drop with a micropipette onto a glass slide for qualitative and quantitative analyses under a phase contrast microscope at 40 magnification. Tintinnids were identified according to Kofoid and Campbell (1929, 1939). Lorica volume (LV, lm3) was converted to body carbon weight (Verity and Langdon, 1984), and production rate (P, lgCl1day1) was estimated (Muller and Geller, 1993) following standard equations. Simultaneously, water samples were also collected in precleaned bottles for analyses of dissolved oxygen (DO), biological oxygen demand (BOD), inorganic nutrients (nitrate, silicate and phosphate), temperature, pH, salinity, turbidity and chlorophyll pigments (a, b and c). They were immediately preserved at 4°C and taken to the laboratory for further analyses. For dissolved oxygen, water samples were taken in BOD bottles (125 ml) and were fixed in situ using Winkler’s reagents. The concentrations of nutrients and chlorophyll were analyzed following the standard methods as proposed by Strickland and Parsons (1972). Statistical analyses were performed using MINITAB 14 and STATISTICA 6 software. While performing any statistical test all the raw data were transformed to log(n + 1) to avoid any anomaly (Clarke and Warwick, 1994). Different diversity indices such as the diversity index (Shannon and Weaver, 1949), richness index (Margalef, 1958) and evenness index (Pielou, 1969) of plankton were calculated using community analysis software. Hydrological parameters showed considerable heterogeneity in three distinct phases of the diatom bloom: pre-bloom, bloom and post-bloom, as shown in Table 1. Surface water temperature was

Fig. 1. Map highlighting the location of Sagar Island in Indian Sundarban showing the study site.

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Table 1 Changes in water quality parameters during pre-, post- and bloom condition from the three sampling sites of Sundarban coastal regions. Period

Temp (°C)

Salinity (p.s.u)

pH

Turbidity (N.T.U)

D.O (mg l1)

B.O.D (mg l1)

Nitrate (lmol l1)

Silicate (lmol l1)

Phosphate (lmol l1)

Chla (mg m3)

Prebloom Bloom Postbloom

24 22 19.5

14.2 19.1 21.0

7.3 8.1 7.9

7 2 9

4.61 5.33 4.42

1.36 1.04 1.43

25.68 13.62 27.52

68.68 34.13 71.98

0.94 0.16 0.48

0.47 4.74 2.70

Fig. 2. MODIS AQUA derived satellite picture showing the concentration of chlorophyll during bloom period.

Fig. 3. (a) Favella ehrenbergii, the solitary tintinnid species found during algal bloom and (b) the bloom forming diatom species Coscinodiscus radiatus (taken at 10 magnification, NIKON Eclipse, E200).

comparatively lower with the value of 22 °C. However, low temperature was reported to be associated with the occurrence of at least one of the bloom-causing species (C. lorenzianus) from Departure Bay, British Columbia (Margolis, 1993). The minimum (4.42 mg l1) and maximum (5.33 mg l1) values of dissolved oxygen (DO) were observed during post-bloom and bloom phases, respectively. A relatively high DO concentration was noticed during bloom phase, which was attributed to photosynthetic release of O2 by the dense diatom mass; this explanation has also been endorsed by previous researchers (Satpathy et al., 2007). As expected, very low DO concentrations were observed during post-bloom phase, indicating the whole phytoplankton mass was in a decaying stage and the bacteria responsible for the decay process were consuming most of the DO in water.

Turbidity value was extremely low (2 N.T.U) during peak bloom phase due to the presence of huge a diatom mass in the surface layer. In contrast, the turbidity increased moderately (9 N.T.U) during post-bloom phase, when the entire diatom usually sedimented at the bottom as dead mass. The nutrient concentrations showed most pronounced changes due to the occurrence of the bloom. The concentration of nitrate, phosphate and silicate ranged from 13.62–27.52 lmol l1, 0.16–0.94 lmol l1 and 34.13–71.98 lmol l1, respectively, from pre-bloom to post-bloom phase. Nitrate and silicate showed maximum and minimum values during post-bloom and bloom phases, respectively. However, the phosphate concentration was found to be highest during pre-bloom phase. Apart from physical and chemical processes, phosphate concentrations in coastal waters mainly depend upon phytoplankton

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S.N. Biswas et al. / Marine Pollution Bulletin 85 (2014) 306–311 Table 2 Numerical density and diversity indices of phytoplankton species (Cells l1) during pre-, post- and bloom condition of Sundarban coastal region. Phytoplankton species

Coscinodiscus radiatus C. concinus C. lineatus C. hyalinus C. eccentricus Nitzschia sigma Chaetoceros lorenzianus Biddulphia sinensis B. mobiliensis Bacteriastrum hyalinum B. varians Ditylum brightwellii Ceratium trichoceros Ceratium furca Pleurosigma formosum Rhizosolenia settigera Eucampia zordiachus Fragilaria oceanica Thallasiothrix longissima T. nitzschioides T. frauenfeldii Navicula sp. Asterionella japonica Cyclotella striata Bacillaria sp. Anabaena sp. Diploneis sp. Lauderia sp. Total Phytoplankton Diversity index (H0 ) Richness index (d) Evenness index (J0 )

Abundance (cells l1) Prebloom

Bloom

Postbloom

689.5 ± 32.30 93.67 ± 132.46 0 1064.5 ± 91.21 675.615 ± 15.01 666.28 ± 0.53 1300.33 ± 46.66 380.06 ± 66.08 160.38 ± 226.81 0 339.115 ± 79.58 0 0 83.6 ± 118.22 333.33 ± 0 332.81 ± 0.72 0 0 339.27 ± 8.40 0 2384 ± 543.05 1046 ± 65.05 0 659.94 ± 9.50 393.615 ± 85.25 1019.15 ± 27.08 673.53 ± 9.71 0 12634.71 ± 1842.84 2.7 7.21 0.85

618,000 ± 4242.64 49,931 ± 2926.0 68,130 ± 1598.06 0 0 4448.27 ± 162.55 167,661 ± 479.41 3993 ± 9.89 2043.5 ± 61.51 2334.11 ± 1.10 0 1394.28 ± 86.19 0 617.16 ± 70.00 1041.5 ± 58.68 343.77 ± 14.76 7840.50 ± 245.84 2769.54 ± 145.49 3339.78 ± 9.11 1770.0 ± 146.21 205781.5 ± 1723.21 0 0 0 0 0 0 3616.94 ± 70.31 1,145,056 ± 1493.32 2.86 6.38 0.8

19932.3 ± 375.70 5385.36 ± 73.58 7322.5 ± 456.08 361.5 ± 36.06 442.22 ± 78.87 0 19,738 ± 1784.73 3506.39 ± 244.74 0 5674.5 ± 11.16 2083.5 ± 118.08 1269.5 ± 381.13 372.8 ± 55.92 0 1947 ± 74.95 1372.8 ± 55.94 4346 ± 489.31 0 0 360.3 ± 38.26 13173.0 ± 698.14 1875.11 ± 294.78 344.8 ± 16.33 0 0 0 0 7841.33 ± 247.01 97349.37 ± 5530.86 2.82 6.63 0.84

± Standard deviation.

Table 3 Numerical abundance and the diversity indices of tintinnids (ind m3) during pre-, post- and bloom condition from the three sampling sites of Sundarban coastal region. Species

Tintinnopsis beroidea Tintinnidium primitivum Tintinnopsis tubulosa Favella ehrenbergii Diversity index (H0 ) Richness index (d) Evenness index (J0 )

Abundance (ind m3) Prebloom

Bloom

Postbloom

84,086 ± 2242.9 340305.75 ± 9860.53 192972.5 ± 37202.02 0 1.09 1.09 0.79

0 0 0 52439.5 ± 3449.97 0.004 1.94 0.003

0 0 0 0 0 0 0

uptake and replenishment by microbial decomposition of organic matter (Satpathy et al., 2007). In addition, agricultural runoff and freshwater discharge during post-monsoon phase also help to increase the phosphate concentration in the water. However, diatoms account for more than half of the total suspended biogenic silica and are a substantial part of the primary production of the ocean (Nelson et al., 1995; Treguer et al., 1995). Hence, it is evident that an overall reduction in nutrients occurred during the bloom phase, which supported a rise in phytoplankton productivity in the area in relation to the pre- and post-bloom phases (Sasmal et al., 2005). Chlorophyll a (chl a) also exhibited wide range of variations (0.40–4.70 mg m3) and showed an exponential increase (4.70 mg m3) coinciding with the highest cell density (11.4  105 cells l1). In general, the concentration of chlorophyll remained high during bloom compared to pre- and post-bloom phase, and the peak value of the pigment was 4–5 times higher than the non-bloom phase. Similar observations of unusually high pigment concentration have been reported by Satpathy et al. (2007) and Mishra et al. (2006) during diatom bloom phases from the eastern

coastal part of India. Satellite remote sensing derived chlorophyll images have been retrieved from the MODIS-Aqua sensor data which also endorsed enriched concentration of chlorophyll (5.0–6.0 mg m3) in this coastal region (Fig. 2). Both qualitative and quantitative characteristics of the phytoplankton community were highly affected by the occurrence of the bloom. Out of 30 diatom species identified from this site, 18 were observed during the bloom phase with the overwhelming dominance of C. radiatus (6.15  105 cells l1) (Fig. 3b) followed by T. frauenfeldii (2.07  105 cells l1) and C. lorenzianus (1.68  105 cells l1), which together comprised 86% of the total community, forming a severe diatom bloom. It persisted for a week phase and could be categorized as a periodic event (Takahashi et al., 1977). The other species were observed in negligible concentrations (10–15%) (Table 2). All three species were common at the mouth of the Hugli river estuary, and the total phytoplankton population density increased abruptly from 12.3  103 (pre-bloom) to 11.4  105 cells l1 during the peak bloom phase. Again, in the post-bloom phase, the

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population density decreased to 9.6  104 cells l1, but was still much higher than the pre-bloom condition and the diversity was also lower (16 species recorded) during this time. The result of ANOVA also revealed significant variations (F = 3.86, p < 0.05) between different phases of the bloom in the context of phytoplankton abundance. For the microzooplankton community, exclusively tintinnid ciliates were considered for the present investigation as they possess the following characteristics: (i) they are ideal for studies of species distributions, diversity and changes in the structure or composition of microzooplankton communities because changes in population composition is easily detected because species identification is based upon morphological characteristics of preservable loricae (Dolan and Gallegos, 2001); and (ii) they often represent an important link between the microbial fraction and the larger grazers (Pierce and Turner, 1994). Strikingly, during the bloom phase, the tintinnid community was represented exclusively by the solitary species Favella ehrenbergii (Fig. 3a), with a density as high as 50,000 ind m3 (Table 3). This species possesses the largest lorica oral diameter (L.O.D = 151.1 ± 16.3 lm) among the identified tintinnids from Sundarban. This was also recorded during a sudden outburst of the phytoplankton community, dominated by a large centric diatom Hemidiscus hardmannianus (Bacillariophyceae), at Gangasagar, southern part of Sagar Island, during November, 2010, as documented by Naha Biswas et al. (2013). A similar phenomenon of low tintinnid abundance in the context of a diatom bloom was also reported by Barría de Cao et al. (2005) from Bahía Blanca estuary, Argentina during an algal bloom. The observed poor density of tintinnids is mainly related to lack of adequate food (Barría de Cao et al., 1997) related to the cell size of phytoplankton prey (Lynn and Montganes, 1991), and this coincided with previous findings from the coastal regions of Sundarban (Naha Biswas et al., 2013). It is noteworthy that few species of tintinnids (only those that have large peristome and lorica oral diameter) are able to graze on phytoplankton during the bloom (Barría de Cao et al., 1997). In our study, the cell size of the dominating bloom-forming species (C. radiatus) was sufficiently large (as mentioned before), indicating that they are not suitable food for any tintinnids in general (Barría de Cao et al., 1997). Again, this bloom was constructed by chain-forming and projection-bearing diatoms of the genus Thalassiothrix and Chaetoceros. Thread extrusion enlarged phytoplankton cell size, making it difficult to be ingested by some tintinnids (Verity and Villareal, 1986). A sharp decrease in microorganism population during the bloom of Coscinodiscus species has also been previously reported from Brazilian waters (Fernandes et al., 2001; Naz et al., 2012) and from Port Blair, Andaman Island (Elangovan et al., 2012), which could be due to the inability of microzooplankton to graze on large-cell phytoplankton of harbor sample (Dawson, ). A trophic coupling may exist between the other seasonal associations and a more diverse phytoplankton, which includes short peaks of phytoflagellates, principally during late spring and summer (Gayoso, 1999). However, the association of a Chaetoceros bloom with high concentrations of three tintinnid species (Helicostomella subulata, Tintinnopsis parvula and Mesodinium rubrum) was reported from Departure Bay, British Columbia (Margolis, 1993). Interestingly, during the post-bloom phase, which coincided with Gangasagar Annual Festival (as mentioned before), the species composition of the phytoplankton community was similar to that of the bloom, but with lower density. Tintinnids were completely absent during this time. The huge load of inorganic nutrients due to GAF induced the persistence of the large-sized diatoms during post bloom phase, which in turn retarded the growth of the tintinnids. The species richness increased from 1.09 (pre-bloom) to 1.94 (bloom) as the dominant solitary species (F. ehrenbergii) contributed

to the total abundance during bloom phase. A sharp reduction in species diversity (1.09–0.004) and species evenness (0.79–0.003) was observed as the number of species reduced drastically during the bloom phase. An abrupt increase in tintinnid biomass (0.19–18.08 lgCl1) and production rate (0.74–6.29 lgCl1day1) was recorded due to exclusive presence of the gigantic tintinnids species F. ehrenbergii (length = 531.9 lm and L.O.D = 151.1 lm). An unusual multispecies bloom, dominated by two centric and one pinnate diatoms, was observed on a regional scale of Sagar Island in the western part of Sundarban. The prolific abundance of bloom-causing cells in shallow waters was combined with low microzooplankton biomass, low dissolved oxygen and high biochemical-oxygen-demand values. Documentation of this sporadic high abundance, together with significant species richness of the diatoms, demands more intensive and comprehensive studies in the Sundarban coastal environment, which is facing severe environmental degradation. In addition, better understanding of the effects of algal blooms on seafood quality, the complex biological, chemical and physical interactions and subsequent effects on trophodynamics is needed to develop the strategy for effective coastal zone management. Acknowledgements The work was financially supported jointly by the Council of Scientific and Industrial Research (CSIR), New Delhi, India [Sanction No. 23(0014)/09/EMR-II] and University Grants Commission (U.G.C.), New Delhi, India [Sanction No. F No. 40 (388)/2011(SR)]. S.N. Biswas and D. Rakshit express their thanks to CSIR and U.G.C, respectively for extending them fellowship. R.K. Sarangi, the other coauthor, gratefully acknowledges the Director, SAC (ISRO), Ahmadabad and Group Director Dr. Ajai for encouragement and collaborative initiatives with Department of Marine Science, University of Calcutta. The satellite data used in this study were acquired as part of NASA TMI Satellite and MODIS AQUA Satellite. Thanks are also due to the anonymous reviewers whose comments and suggestions helped to improve this manuscript. References Admiraal, W., Breugem, P., Jacobs, D.M.L.H.A., Steveninck, E.D., 1990. Fixation of dissolved silicate and sedimentation of biogenic silicate in the lower river Rhine during diatom blooms. Biogeochemistry 9 (2), 175–185. Barría de Cao, M.S., Beight, M., Piccolo, C., 2005. Temporal variability of diversity and biomass of tintinnids (Ciliophora) in Southeastern Atlantic temperate estuary. J. Plank. Res. 27 (11), 1103–1111. Barría de Cao, M.S., Pettigrosso, R.E., Popovich, C., 1997. Planktonic ciliates during a diatom bloom in Bahia Blanca estuary, Argentina II. Tintinnids. Obelia 23, 21– 31. Clarke, K.R., Warwick, R.M., 1994. Change in Marine Communities. Plymouth Marine Laboratory, p. 144. Clarke, A.L., Weckström, K., Conley, D.J., Anderson, N.J., Adser, F., Andre´n, E., et al., 2006. Long-term trends in eutrophication and nutrients in the coastal zone. Limnol. Oceanogr. 51 (1, part 2), 385–397. Desikachary, T.V., 1987. Atlas of Diatoms III & IV. Madras Science Foundation, Madras, p. 239. Devassy, V.P., Nair, S.R., 1987. Discoloration of water and its effect on fisheries along the Goa coast. Mahasagar Bull. 20, 121–128. Dolan, J.R., Gallegos, C., 2001. Planktonic diversity of tintinnids (Planktonic ciliates). J. Plankton Res. 23, 1009–1027. Dolan, J.R., Claustre, H., Carlotti, F., Plounevez, S., Moutin, T., 2002. Microzooplankton diversity: relationship of tintinnid ciliate with resources, competitors and predators from the Atlantic Coast of Morocco to the Eastern Mediterranean. Deep Sea Res. Part I 49, 1217–1232. Elangovan, S.S., Arun Kumar, M., Karthik, R., Siva Sankar, R., Jayabarathi, R., Padmavati, G., 2012. Abundance, species composition of microzooplankton from the coastal waters of Port Blair, South Andaman Island. Aquat. Biosyst. 8, 20. Fernandes, L.F., Zehnder-Alves, L., Bassfeld, J.C., 2001. The recently established diatom Coscinodiscus wailesii (Coscinodiscales, Bacillariophyta) in Brazilian waters. I: Remarks on morphology and distribution. Phycol. Res. 49, 89–96. Fristch, E., 1935. The Structure and Reproduction of Algae, vol. II. Cambridge Univ. Press, London, p. 263.

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Impact of multispecies diatom bloom on plankton community structure in Sundarban mangrove wetland, India.

A multispecies bloom caused by the centric diatoms, viz. Coscinodiscus radiatus, Chaetoceros lorenzianus and the pennate diatom Thalassiothrix frauenf...
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