Distribution and abundance of dinoflagellates from the coastal waters of Karachi, Pakistan, northern part of the Arabian Sea

Distribuição e abundância de dinoflagelados nas águas costeiras de Karachi, Paquistão, parte norte do Mar da Arábia

F. N. Khokhar N. Ahmed A. Ali K. Gabol A. R. Khooharo M. Faheem A. Hussain Z. N. Burhan P. J. A. Siddiqui About the authors

Abstract

The present study reports on seasonal and spatial variations in diversity, distribution and abundance of dinoflegellates and indicates the presence of HAB species in Pakistan waters. A total of 179 taxa, recorded in this study from offshore and near-shore waters, belong to 41 genera in 26 families and 10 orders. The high species count (149 species) was recorded from Manora Island offshore station (MI-1) and 105 spp, 109 spp and 115 spp were encountered from the Mubarak village offshore station (MV-1), Manora near shore station (MI-2) and Mubarak Village near-shore station (MV-2) respectively. Tripos furca was the dominant and frequently occurring species (> 1 x103 to > 25 x103 cells L-1 from coastal and >1x 105 cells L-l from near-shore stations) in addition to less abundant Alexandrium catenella, Alexandrium sp., Alexandrium minutum, and Prorocentrum micans (>103 to 25x 103cells/L). Another 44 species occurred in relatively low numbers (<103 cell L-l). Seventy species were found throughout the study period at all four stations. High number of species in three genera (Tripos (38), Protoperidinium (34) and Prorocentrum (20) was recorded. Potently toxic (16 genera 43 species) and HAB related (19 genera and 30 species) dinoflagellate taxa were also recorded. The percent contribution of dinoflagellates in total phytoplankton population generally remained below 20% except for a few instances. Manora Island stations had comparatively higher Shannon index and equitability and slightly lower dominance index. The PCA plot showed strong positive correlation among chlorophyll-a concentration, dissolved oxygen, total number of phytoplankton and dinoflagellates.

Keywords:
Harmful algal blooms; Phytoplankton; Karachi coast; Pakistan; Manora

Resumo

O presente estudo relata variações sazonais e espaciais na diversidade, na distribuição e na abundância de dinoflegelados e indica a presença de espécies de HAB nas águas do Paquistão. Um total de 179 táxons, registrados nesse estudo de águas offshore e próximas à costa, pertence a 41 gêneros em 26 famílias e 10 ordens. A alta contagem de espécies (149 espécies) foi registrada na estação offshore da Ilha de Manora (MI-1) e 105 spp., 109 spp. e 115 spp. foram encontrados na estação offshore da vila de Mubarak (MV-1), Manora perto da estação costeira (MI- 2) e estação próxima à costa da Vila de Mubarak (MV-2), respectivamente. Tripos furca foi a espécie dominante e de ocorrência frequente (> 1 x103 a > 25 x103 células L-1 da costa e > 1x 105 células Ll de estações próximas à costa), além de Alexandrium catenella menos abundante, Alexandrium sp., Alexandrium minutum e Prorocentrum micans (> 103 a 25x 103 células/L). Outras 44 espécies ocorreram em números relativamente baixos (< 103 células L-1). Setenta espécies foram encontradas durante o período de estudo em todas as quatro estações. Foi registrado um alto número de espécies em três gêneros (Tripos (38), Protoperidinium (34) e Prorocentrum (20). Potencialmente tóxicos (16 gêneros e 43 espécies) e HAB relacionados (19 gêneros e 30 espécies), táxons de dinoflagelados também foram registrados. A contribuição percentual de dinoflagelados na população fitoplanctônica total geralmente permaneceu abaixo de 20%, exceto em alguns casos. As estações da Ilha de Manora tinham índice de Shannon comparativamente mais alto e equitabilidade e índice de dominância ligeiramente mais baixos. O gráfico de PCA mostrou forte correlação positiva entre concentração de clorofila-a e oxigênio dissolvido, número total de fitoplânctons e dinoflagelados.

Palavras-chave:
Harmful algal blooms; fitoplâncton; costa de Karachi; Paquistão; Manora

1. Introduction

The phytoplankton is a diverse group, including prokaryotic and eukaryotic organisms (Vadrucci et al., 2008VADRUCCI, M.R., SABETTA, L., FIOCCA, A., MAZZIOTTI, C., SILVESTRI, C., CABRINI, M., GUARDIANI, B., KONJKA, E., EVANGELOPOULOS, A., KOUTSOUBAS, D. and BASSET, A., 2008. Statistical evaluation of differences in phytoplankton richness and abundance as constrained by environmental drivers in transitional waters of the Mediterranean basin. Aquatic Conservation, vol. 18, no. S1, pp. 88-104. http://dx.doi.org/10.1002/aqc.951.
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), which play a significant role in the primary production, maintenance the ocean’s health and as indicators of climate change (Reid et al., 1998REID, P.C., EDWARDS, M., HUNT, H.G. and WARNER, A.J., 1998. Phytoplankton change in the North Atlantic. Nature, vol. 391-546.; Cermeño et al., 2008CERMEÑO, P., DUTKIEWICZ, S., HARRIS, R.P., FOLLOWS, M., SCHOFIELD, O. and FALKOWSKI, P.G., 2008. The role of nutricline depth in regulating the ocean carbon cycle. Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 51, pp. 20344-20349. http://dx.doi.org/10.1073/pnas.0811302106. PMid:19075222.
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). They are adapted to variable environmental conditions (e.g. light, temperature, salinity, nutrients, water circulation pattern), which control their distribution, diversity and migration (Levandowsky and Kaneta, 1987LEVANDOWSKY, M. and KANETA, P.J., 1987. Behaviour in dinoflagellates. In: F.J.R. TAYLOR, ed. The biology of dinoflagellates. Oxford: Blackwell, pp. 360-397., Behrenfeld et al., 2006BEHRENFELD, M.J., O’MALLEY, R.T., SIEGEL, D.A., MCCLAIN, C.R., SARMIENTO, J.L., FELDMAN, G.C., MILLIGAN, A.J., FALKOWSKI, P.G., LETELIER, R.M. and BOSS, E.S., 2006. Climate-driven trends in contemporary ocean productivity. Nature, vol. 444, no. 7120, pp. 752-755. http://dx.doi.org/10.1038/nature05317. PMid:17151666.
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). Dinoflagellates form a major component of phytoplankton; occur in a variety of habitat having different shapes and modes of nutrition (Kimor, 1981KIMOR, B., 1981. The role of phagotrophic dinoflagellates in marine ecosystems. Kieler Meeresforsch. Sonderh, vol. 5, pp. 164-173.; Tomas, 1997TOMAS, C.R., 1997. Identifying marine diatoms and dinoflagellates. Marine Geology, vol. 3, no. 136, pp. 320-321.). A total of 2377 species in 259 genera are known from the world’s oceans (Gómez, 2012GÓMEZ, F., 2012. A checklist and classification of living dinoflagellates (Dinoflagellata, Alveolata). Cicimar Oceanides, vol. 27, no. 1, pp. 65-140. http://dx.doi.org/10.37543/oceanides.v27i1.111.
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) including 200 toxic and harmful algal blooms (HAB) forming species (Smayda, 1997SMAYDA, T.J., 1997. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnology and Oceanography, vol. 42, no. 5 part. 2, pp. 1137-1153. http://dx.doi.org/10.4319/lo.1997.42.5_part_2.1137.
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; Gómez 2005GÓMEZ, F., 2005. A list of free-living dinoflagellate species in the world’s oceans. Acta Botanica Croatica, vol. 64, no. 1, pp. 129-212.). Toxins from dinoflagellates have a deleterious impact on other organisms that pose a threat to human and environmental health (Shumway, 1990SHUMWAY, S.E., 1990. A review of the effects of algal blooms on shellfish and aquaculture. Journal of the World Aquaculture Society, vol. 21, no. 2, pp. 65-104. http://dx.doi.org/10.1111/j.1749-7345.1990.tb00529.x.
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; Smayda, 1990SMAYDA, T., 1990. Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic. In: E. GRANÉLI, B. SUNDSTRÖM, L. EDLER and D.M. ANDERSON, eds. Toxic marine phytoplankton. New York: Elsevier, pp. 29-40.; Hallegraeff, 1993HALLEGRAEFF, G.M., 1993. A review of harmful algal blooms and their apparent global increase. Phycologia, vol. 32, no. 2, pp. 79-99. http://dx.doi.org/10.2216/i0031-8884-32-2-79.1.
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; Landsberg, 2002LANDSBERG, J.H., 2002. The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science, vol. 10, no. 2, pp. 113-390. http://dx.doi.org/10.1080/20026491051695.
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; Imai et al., 2006IMAI, I., YAMAGUCHI, M. and HORI, Y., 2006. Eutrophication and occurrences of harmful algal blooms in the Seto Inland Sea, Japan. Plankton & Benthos Research, vol. 1, no. 2, pp. 71-84. http://dx.doi.org/10.3800/pbr.1.71.
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; Steidinger et al., 2008STEIDINGER, K.A., LANDSBERG, J.H., FLEWELLING, L.J. and KIRKPATRICK, B.A. 2008. Toxic dinoflagellates. In: S. SMITH, L. FLEMING, H. SOLO-GABRIELE and W.H. GERWIC, eds. Oceans and Human Health; Risks and Remedies from the Seas. Burlington, MA: Academic Press, pp. 239-256.; Richlen et al., 2010RICHLEN, M.L., MORTON, S.L., JAMALI, E.A., RAJAN, A. and ANDERSON, D.M., 2010. The catastrophic 2008–2009 red tide in the Arabian Gulf region, with observations on the identification and phylogeny of the fish-killing dinoflagellate Cochlodinium polykrikoides. Harmful Algae, vol. 9, no. 2, pp. 163-172. http://dx.doi.org/10.1016/j.hal.2009.08.013.
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). Water discoloration (red, green, brown) indicating dinoflegellate blooms (Smayda, 1990SMAYDA, T., 1990. Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic. In: E. GRANÉLI, B. SUNDSTRÖM, L. EDLER and D.M. ANDERSON, eds. Toxic marine phytoplankton. New York: Elsevier, pp. 29-40.; Hallegraeff, 1993HALLEGRAEFF, G.M., 1993. A review of harmful algal blooms and their apparent global increase. Phycologia, vol. 32, no. 2, pp. 79-99. http://dx.doi.org/10.2216/i0031-8884-32-2-79.1.
http://dx.doi.org/10.2216/i0031-8884-32-...
; Landsberg, 2002LANDSBERG, J.H., 2002. The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science, vol. 10, no. 2, pp. 113-390. http://dx.doi.org/10.1080/20026491051695.
http://dx.doi.org/10.1080/20026491051695...
; Rensel and Whyte, 2003RENSEL, J.E. and WHYTE, J.N.C., 2003. Finfish mariculture and harmful algal blooms. Manual on harmful marine microalgae. Monographs on Oceanographic Methodology, vol. 11, pp. 693-722.) have been reported from Australia (Hallegraeff, 1992HALLEGRAEFF, G.M., 1992. Harmful algal blooms in the Australian region. Marine Pollution Bulletin, vol. 25, no. 5-8, pp. 186-190. http://dx.doi.org/10.1016/0025-326X(92)90223-S.
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), Japan, Hong Kong and China (Huang and Qi, 1997HUANG, C. and QI, Y., 1997. The abundance cycle and influence factors on red tide phenomena of Noctiluca scintillans (Dinophyceae) in Dapeng Bay, the South China Sea. Journal of Plankton Research, vol. 19, no. 3, pp. 303-318. http://dx.doi.org/10.1093/plankt/19.3.303.
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), and northern Arabian Sea (LeFevre and Grall, 1970; Venugopal et al., 1979VENUGOPAL, P., HARIDAS, P., MADHUPRATAP, M. and RAO, T.S.S., 1979. Incidence of red water along south Karala coast. Indian Jounal of Marine Science, vol. 8, pp. 94-97.; do Rosário Gomes et al., 2014DO ROSÁRIO GOMES, H., GOES, J.I., MATONDKAR, S.G.P., BUSKEY, E.J., BASU, S., PARAB, S. and THOPPIL, P., 2014. Massive outbreaks of Noctiluca scintillans blooms in the Arabian Sea due to spread of hypoxia. Nature Communications, vol. 5, no. 1, pp. 4862. http://dx.doi.org/10.1038/ncomms5862. PMid:25203785.
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).

A number of potential blooms forming species have been reported from coastal waters of Pakistan in the northern Arabian Sea (Saifullah and Chaghtai, 1990SAIFULLAH, S.M. and CHAGHTAI, F., 1990. Incidence of Noctiluca-scintillans (Macartney) Ehrenb., blooms along Pakistan shelf. Pakistan Journal of Botany, vol. 22, no. 2, pp. 94-99.; Baig et al., 2006BAIG, H.S., SAIFULLAH, S.M. and DAR, A., 2006. Occurrence and toxicity of Amphidinium carterae Hulburt in the North Arabian Sea. Harmful Algae, vol. 5, no. 2, pp. 133-140. http://dx.doi.org/10.1016/j.hal.2005.06.010.
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). In general, reports on phytoplankton from Pakistan are scarce and only a few studies are (Latif et al., 2013LATIF, S., AYUB, Z. and SIDDIQUI, G., 2013. Seasonal variability of phytoplankton in a coastal lagoon and adjacent open sea in Pakistan. Turkish Journal of Botany, vol. 37, no. 2, pp. 398-410.; Khokhar et al., 2018KHOKHAR, F.N., NAZ, T., BURHAN, Z.N., ABASSI, M.J. and SIDDIQUI, P.J.A., 2018. Occurrence of HAB / toxic Dinoflagellates species from the coast of Karachi, Pakistan (Northern Arabian Sea). Indian Journal of Geo-Marine Sciences, vol. 47, no. 1, pp. 73-88., 2020KHOKHAR, F.N., BURHAN, Z.N., NAZ, T., ABBASI, J., AHMAD, N., ALI, A., IQBAL, P. and SIDDIQUI, P.J.A., 2020. Phytoplankton community dynamics during Asian monsoon system preponderate in the coastal waters of northern region of Arabian Sea boarding Pakistan. Pakistan Journal of Botany, vol. 52, no. 2, pp. 703-709. http://dx.doi.org/10.30848/PJB2020-2(28).
http://dx.doi.org/10.30848/PJB2020-2(28)...
) and the remaining contributions are restricted to taxonomy and coastal waters (Munir et al., 2011MUNIR, S., SIDDIQUI, P.J.A. and MORTON, S.L, 2011. The occurrence of the ciguatera fish poisoning producing dinoflagellate genus Gambierdiscus in Pakistan waters. Algae - Korean Phycological Society, vol. 26, no. 4, pp. 317-325. http://dx.doi.org/10.4490/algae.2011.26.4.317.
http://dx.doi.org/10.4490/algae.2011.26....
, 2013MUNIR, S.T., BURHAN, Z. U. N., SIDDIQUI, P. J. A. and MORTON, S. L., 2013. Seasonal abundance, biovolume and growth rate of the heterotrophic dinoflagellate (Noctiluca scintillans) from coastal waters of Pakistan. Pakistan Journal of Botany, vol. 45, no. 3, pp. 1109-1113., 2015MUNIR, S., SIDDIQUI, P.J.A., NAZ, T., BURHAN, Z.U.N. and MORTON, S.L., 2015. Growth rates of dinoflagellates along the Karachi coast assessed by the size fractionation method. Oceanological and Hydrobiological Studies, vol. 44, no. 3, pp. 326-334. http://dx.doi.org/10.1515/ohs-2015-0031.
http://dx.doi.org/10.1515/ohs-2015-0031...
; Mansoor and Saifullah, 1995MANSOOR, S. and SAIFULLAH, S.M., 1995. A new species and a new variety of Amphisolenia Stein from the North Arabian Sea bordering Pakistan. Pakistan Journal of Marine Sciences, vol. 4, no. 1, pp. 5-8.). The few reports on dinoflagellates were available on growth rate and seasonal abundance (Munir et al., 2016MUNIR, S., NAZ, T., BURHAN, Z., SIDDIQUI, P.J.A. and MORTON, S.L., 2016. Species composition and abundance of dinoflagellates from the coastal waters of Pakistan. Journal of Coastal Life Medicine, vol. 4, no. 6, pp. 448-457. http://dx.doi.org/10.12980/jclm.4.2016J6-58.
http://dx.doi.org/10.12980/jclm.4.2016J6...
; Khokhar et al., 2018KHOKHAR, F.N., NAZ, T., BURHAN, Z.N., ABASSI, M.J. and SIDDIQUI, P.J.A., 2018. Occurrence of HAB / toxic Dinoflagellates species from the coast of Karachi, Pakistan (Northern Arabian Sea). Indian Journal of Geo-Marine Sciences, vol. 47, no. 1, pp. 73-88.).

The present study reports on seasonal and spatial variations in diversity, distribution and abundance of dinoflegellates occurring in the coastal and near-shore off Karachi. The presence of HAB species in coastal and near-shore waters, where most of the artisanal fishery operations are located, is alarming for fisheries industry as well as human and environmental health.

2. Materials and Methods

2.1. Study area

The study was conducted at 2 stations (Manora Island (MI) and Mubarak Village (MV) along the Karachi coast during April 2008 to March 2010 (Figure 1). Samples were collected from 4 sites e.g. 2 at Manora Island (MI-1: Manora Island offshore (24°45'4.75”N, 66°59' 9.29”E); MI-2: Manora Island nearshore (24°35'5.91”N, 66°46' 6.34”E) and 2 at Mubarak Village (MV-1: Mubarak Village offshore (24°52'6.18”N, 66°37'21.86”E); MV-2: Mubarak Village nearshore (24°45'39.12”N, 66°26'13.38”E).

Figure 1
Map of the Karachi coast showing location in the coastal and near-shore waters off of Manora Island (MI-1; 10m contour line and MI-2; 50m contour line) and Mubarak Village (MV-1; 10 m contour line and MV-2; 50 m contour line).

2.2. Sample collection and analysis

A total of 144 replicates from offshore waters and 108 from near-shore waters were collected using 1.7L Niskin water sampler from 1m below the surface. Samples were fixed in 1% Lugol’s solution in amber bottles and stored at 4°C for further analysis. A Known volume of sample (50 ml) was concentrated (Utermohl, 1958UTERMÖHL, H., 1958. Zur Vervollkommnung der quantitative Phytoplankton-Methodik. International Association of Theoretical and Applied Limnology = Communications, vol. 9, pp. 1-38.) and cell counts were recorded using an inverted microscope (Olympus, IX-51, Japan). Dinoflagellate species were identified following (Taylor, 1987TAYLOR, F.J.R., 1987. The biology of dinoflagellates. Oxford: Blackwell Scientific Publications. 785 p. Botanical Monographs, Vol. 21. ; Tomas, 1997TOMAS, C.R., 1997. Identifying marine diatoms and dinoflagellates. Marine Geology, vol. 3, no. 136, pp. 320-321.). Species nomenclature was used following Gómez (2012GÓMEZ, F., 2012. A checklist and classification of living dinoflagellates (Dinoflagellata, Alveolata). Cicimar Oceanides, vol. 27, no. 1, pp. 65-140. http://dx.doi.org/10.37543/oceanides.v27i1.111.
http://dx.doi.org/10.37543/oceanides.v27...
, 2013GÓMEZ, F., 2013. Reinstatement of the dinoflagellate genus Tripos to replace Neoceratium, marine species of Ceratium (Dinophyceae, Alveolata). Cicimar Oceánides, vol. 28, no. 1, pp. 1-22. http://dx.doi.org/10.37543/oceanides.v28i1.119.
http://dx.doi.org/10.37543/oceanides.v28...
), Guiry and Guiry (2016)GUIRY, M.D. and GUIRY, G.M., 2016 [viewed 2016]. AlgaeBase [online]. Galway: World-Wide Electronic Publication, National University of Ireland Available from: http://www.algaebase.org
http://www.algaebase.org...
and online websites (http://marinespecies.org, http://ucjeps.berkeley.edu/ina/img). Water parameters, such as, water and air temperature were recorded using mercury thermometer, pH (Hanna HI 9023), transparency (Secchi disc), dissolved oxygen (Wrinkler’s method HANNA-C100), salinity (refrectometer) and total chlorophyll (Chl a) following Strickland and Parsons (1972)STRICKLAND, J.D. and PARSONS, T.R., 1972. A practical handbook of seawater analysis. 2nd ed. Ottawa, Canada: Fisheries Research Board of Canada. Fisheries Research Board of Canada Bulletin, n. 167. The diversity indices (Shannon wiener, equitability, dominance) and principal component analysis (PCA) were also assessed using PAST version 2.17 software.

3. Results

Occurrence and distribution of dinoflagellate species in the coastal and near-shore waters of Pakistan is shown in Table 1. A total 179 taxa and 154 species belonging to 41 genera were recorded. Offshore waters had 105 (MV-1) to 149 (MI-1) species in 27 (MV-1) and 36 (MI-1) genera, respectively. On the other hand, near-shore waters had representation of 109 species at MI-2 to 115 species at MV-2 representing 30 (MI-2) and 29 (MV-2) genera, respectively. Variable numbers of species were recorded in 41 genera of dinoflagellates (Table 2). Three genera (Tripos (38 species), Protoperidinium (34 species) and Prorocentrum (20 species)) had high species counts. In addition, 5-9 spp. were recorded in 4 genera; 3-4 species in six genera; 2 spp. in 10 genera and only one species in 18 genera. About 39% of the total species (70 species) were distributed at all stations (Table 2). Diversity indices (Table 1) showed that Manora Island stations (MI-1 and MI-2) had slightly higher Shannon index and equitability, and slightly lower dominance thereby depicting high dinoflagellate diversity compared to Mubarak Village stations (MV-1 and MV-2). Variability in occurrence and abundance of dinoflegellate species was recorded at different stations (Table 2, Figure 3). Only one species, Tripos furca, was dominantly abundant at all stations (> 1 x103 cells L-1 at MV-1 and MI-2, > 25 x103 cells L-1 at MV-2 and >100x 103 cells L-l from MI-1).Twenty species were commonly present at all stations (between 1x103 and 25x103 cells L-1). Some of the species were termed as frequent (51 spp.; present at three stations; <1x103 cells L-1), and the rest (107 spp.; <1x103 cells L-1) were classified as occasional (present at two stations) and rare (present at only station). The highest total cell density of dinoflagellates was generally observed during NE monsoon i.e., October (149x103cellsL-l at MI-1) and November (25x103 cells L-l at MV-1) (Figure 2).

Table 1
Diversity indices of dinoflagellates distributed at four stations in the coastal (MI-1, MV-1) and near-shore (MI-2, MV-2) waters of Pakistan.
Table 2
List of dinoflagellates taxa identified from coastal (MI-1 and MV-1) and near-shore (MV-2 and MI-2) waters (April 2008 - March 2010) showing distribution and abundance (cells L-l) for recorded species (+ = <103 cellsL-1 (Rare: present only at one station; occasional: present at two stations; Frequent: present at three to four stations); ++ = 103-25x103 Cells L-1 (Common); +++ = 25x103 – 75x103 (Abundant); ++++ = >75x103 (Dominant).
Figure 3
Monthly distribution of Phytoplankton and dinoflagellate species in offshore (MI-1 and MV-1) and nearshore (MI-2 and MV-2) waters along the Sindh coast of Pakistan. Abbreviations are as: MI: Manora Island; MV: Mubarak Village.
Figure 2
Phytoplankton cell abundance (cellx103L-l) and dinoflagellates percentage (%) recorded from offshore and nearshore waters along the Sindh coast of Pakistan. A-B: Manora Island and Mubarak Village offshore waters; C-D: Manora Island and Mubarak Village nearshore waters.

A total of 73 HAB related species in 27 genera (including 43 potentially toxic species) were recorded from the coastal and near-shore waters (Table 2). Forty two potentially toxic species were noted in following genera: Alexandrium (8 spp.), Dinophysis (8 spp.), Prorocentrum (7 spp.), Gonyaulax (4 spp.), Gymnodinium, Karenia, Phalacroma (2 spp. each), and reaming ten genera (Amphidinium, Azadinium, Diplopsalopsis, Gambierdiscus, Gyrodinium, Heterocapsa, Lingulodinium, Ostreopsis, Protoceratium, Protoperidinium) had one species only. In addition, 30 non-toxic HAB related species were also included, viz., Prorocentrum (6 spp.), Pyrocystis (4 spp.), Tripos (4 spp.), Scrippsiella (3 spp.), Gymnodinium, Peridinium, Pyrophacus (2 spp. each), Akashiwo, Cochlodinium, Gyrodinium, Heterocapsa, Lepidodinium, Noctiluca scintillans, Oblea (1 spp. each).

Dinoflagellates had low contribution in total phytoplankton population (<10% at all instances) in offshore and near-shore stations (Figure 2), except for the high values recorded in 2009 October (64% at MI-1, 51% at MV-2), and in 2008 during April (24%, MI-2), July (24%, MV-1) and November (27%, MV-1) and in 2010 during January (14%) and February (20%) (Figure 2). High numbers of species were recorded in April 2008 at MI-2 (73) and in May 2008 at MI-1 (90). Seasonal variations in the number of species at different station follow the pattern observed for total phytoplankton and dinoflagellate abundance, i.e., high diversity was observed in October and November with some exceptions. (Figure 2).

The PCA plot of hydro-biological variables (Figure 4) showed two significant components (PC-1 and PC-2) which represent 99.9% of the total variability in water quality. PC-1 accounted for 94.86% of the total variance, which was due to the positive loading of chlorophyll-a (0.811), dissolved oxygen (0.210), total number of phytoplankton (0.711), dinoflagellates (0.243) and negative loading of salinity (-0.441), pH (-0.441) and transparency (-0.428) and water temperature (-0.493) Figure 4. PC-2 contributed 5.13% of the total variability which was found to be positively loaded by water temperature (0.584), pH (0.64), dissolved oxygen (0.05), salinity (0.41), chlorophyll-a (0.114), total number of phytoplankton (0.42), and dinoflagellates (0.59) and negatively loaded by transparency (-0.30). The PCA plot showed that axis I was highly and positively correlated with DO, chlorophyll a, cell counts of phytoplankton and dinoflagellates, whereas axis II was strongly correlated with water temperature, pH, and salinity. The transparency of water appeared to be negatively correlated with axis I. The difference in the relative size of axis I and axis II was small with eigen values of 6.37 and 3.44, respectively (Figure 4).

Figure 4
Principal Component analysis (PCA) of hydro-biological variables, such as, phytoplankton (Phy) and dinoflagellates (Dino) abundance, chlorophyll a (Chl a), dissolved oxygen (DO), salinity (Sal), water temperature (W.tem), pH and transparency (trans) recorded for the coastal and near-shore waters (combined data).

4. Discussion

This study reports on the seasonal variability in population structure and composition of dinoflagellates in the offshore and nearshore waters of Karachi (Northern Arabian Sea). The dinoflagellates are one of the major components in marine ecosystem and play significant role in energy transfer between different trophic levels (Nagata et al., 1996NAGATA, T., TAKAI, K., KAWABATA, K.I., NAKANISHI, M. and URABE, J., 1996. The trophic transfer via a picoplankton-flagellate-copepod food chain during a picocyanobacterial bloom in Lake Biwa. Archiv für Hydrobiologie, vol. 137, no. 2, pp. 145-160. http://dx.doi.org/10.1127/archiv-hydrobiol/137/1996/145.
http://dx.doi.org/10.1127/archiv-hydrobi...
; Ganjian and Makhlogh, 1998; Nuuk, 1999NUUK, G., 1999. The significance of food web structure for the condition and tracer lipid content of juvenile snail fish (Pisces: liparis spp.) along 65–72 N off West Greenland. Journal of Plankton Research, vol. 21, no. 9, pp. 1593-1611. http://dx.doi.org/10.1093/plankt/21.9.1593.
http://dx.doi.org/10.1093/plankt/21.9.15...
; Ganjian and Makhlogh, 2003GANJIAN, A. and MAKHLOGH, A., 2003. Distribution pattern of the dominant groups of phytoplankton (Chrysophyta and pyrrophyta) in the southern Caspian Sea. Iranian Journal of Fisheries Science, vol. 12, no. 1, pp. 103-116.; Carter et al., 2005CARTER, C.M., ROSS, A.H., SCHIEL, D.R., HOWARD-WILLIAMS, C. and HAYDEN, B., 2005. In situ microcosm experiments on the influence of nitrate and light on phytoplankton community composition. Journal of Experimental Marine Biology and Ecology, vol. 326, no. 1, pp. 1-13. http://dx.doi.org/10.1016/j.jembe.2005.05.006.
http://dx.doi.org/10.1016/j.jembe.2005.0...
) and their blooms can cause eutrophication (Micheli, 1999MICHELI, F., 1999. Eutrophication, fisheries, and consumer-resource dynamics in marine pelagic ecosystems. Science, vol. 285, no. 5432, pp. 1396-1398. http://dx.doi.org/10.1126/science.285.5432.1396. PMid:10464097.
http://dx.doi.org/10.1126/science.285.54...
) and change water quality (Richardson and Schoeman, 2004RICHARDSON, A.J. and SCHOEMAN, D.S., 2004. Climate impact on plankton ecosystems in the Northeast Atlantic. Science, vol. 305, no. 5690, pp. 1609-1612. http://dx.doi.org/10.1126/science.1100958. PMid:15361622.
http://dx.doi.org/10.1126/science.110095...
; Leterme et al., 2006LETERME, S.C., SEURONT, L. and EDWARDS, M., 2006. Differential contribution of diatoms and dinoflagellates to phytoplankton biomass in the NE Atlantic Ocean and the North Sea. Marine Ecology Progress Series, vol. 312, pp. 57-65. http://dx.doi.org/10.3354/meps312057.
http://dx.doi.org/10.3354/meps312057...
). Dinoflagellate maintained low proportion (<20%) in the total phytoplankton population with a few exceptions, which is in conformity with other studies reported previously (Azov, 1986AZOV, Y., 1986. Seasonal patterns of phytoplankton productivity and abundance in nearshore oligotrophic waters of the Levant Basin (Mediterranean). Journal of Plankton Research, vol. 8, no. 1, pp. 41-53. http://dx.doi.org/10.1093/plankt/8.1.41.
http://dx.doi.org/10.1093/plankt/8.1.41...
; Zingone et al., 1995ZINGONE, A., CASOTTI, R., D’ALCALA, M.R., SCARDI, M. and MARINO, D., 1995. ‘St Martin’s Summer’: the case of an autumn phytoplankton bloom in the Gulf of Naples (Mediterranean Sea). Journal of Plankton Research, vol. 17, no. 3, pp. 575-593. http://dx.doi.org/10.1093/plankt/17.3.575.
http://dx.doi.org/10.1093/plankt/17.3.57...
) and has been attributed to surface temperature and wind conditions (Hinder et al., 2012HINDER, S.L., HAYS, G.C., EDWARDS, M., ROBERTS, E.C., WALNE, A.W. and GRAVENOR, M.B., 2012. Changes in marine dinoflagellate and diatom abundance under climate change. Nature Climate Change, vol. 2, no. 4, pp. 271-275. http://dx.doi.org/10.1038/nclimate1388.
http://dx.doi.org/10.1038/nclimate1388...
). It may be noted (Figure 2) that stations towards the west (MV-1 and MV-2) showed peaks of phytoplankton abundance slightly earlier compared to stations towards the east (MI-1 and MI-2). This may be due to the eastwards circulation of water, bringing up-sloped nutrient rich water that has been upwelled off the coast of Oman during the SW monsoon (Swallow, 1984SWALLOW, J.C., 1984. Some aspects of the physical oceanography of the Indian Ocean. Deep-Sea Research. Part A, Oceanographic Research Papers, vol. 31, no. 6-8, pp. 639-650. http://dx.doi.org/10.1016/0198-0149(84)90032-3.
http://dx.doi.org/10.1016/0198-0149(84)9...
; Elliott and Savidge, 1990ELLIOTT, A.J. and SAVIDGE, G., 1990. Some features of the upwelling off Oman. Journal of Marine Research, vol. 48, no. 2, pp. 319-333. http://dx.doi.org/10.1357/002224090784988764.
http://dx.doi.org/10.1357/00222409078498...
). The phytoplankton abundance during the NE monsoon along the Pakistan coast is also the effect of delayed transmission of nutrient rich upwelled water in this area. Higher dinoflagellate abundance in the coastal waters at MI-1 and MV-1 compared to the corresponding near-shore stations may be generally attributed to the coastal effect which may be noted much enhanced in the Manora Island stations where the coastal and near-shore waters appeared to have inputs of sewage and industrial wastes and agricultural runoff through Malir and Layari rivers (Nergis et al., 2012NERGIS, Y., SHARIF, M., CHOUDHRY, A. F., HUSSAIN, A., and BUTT, J. A., 2012. Impact of industrial and sewage effluents on Karachi coastal water and sediment quality.Middle-East Journal of Scientific Research, vol. 11, no.10, pp.1443-1454.; Chan et al., 2021CHAN, M. W. H., HASAN, K. A., BALTHAZAR-SILVA, D., MIRANI, Z. A., and ASGHAR, M., 2021. Evaluation of heavy metal pollutants in salt and seawater under the influence of the Lyari River and potential health risk assessment.Marine Pollution Bulletin, vol. 166, pp. 112215. https://doi.org/10.1016/j.marpolbul.2021.112215.
https://doi.org/10.1016/j.marpolbul.2021...
). The regional effect of temperature and wind conditions and upwelled nutrient-rich water is also evident on a seasonal scale. For the same reason discussed above, the diversity of dinoflagellates is higher at Manora Island stations compared to other two stations off of Mubarak Village. Again the diversity and the species richness were higher in the coastal waters as oppose to the corresponding near-shore stations.

Information recorded on dinoflagellate species (74 species) by Shameel and Tanaka (1992)SHAMEEL, M. and TANAKA, J. 1992. A preliminary check-list of marine algae from the coast and inshore waters of Pakistan. In: T. NAKAIKE, S. MALIK, eds. Cryptogamic Flora of Pakistan. Tokyo: National cience Museum, vol. 1, pp. 1-64. and others reported in the later on (Mansoor and Saifullah, 1995MANSOOR, S. and SAIFULLAH, S.M., 1995. A new species and a new variety of Amphisolenia Stein from the North Arabian Sea bordering Pakistan. Pakistan Journal of Marine Sciences, vol. 4, no. 1, pp. 5-8.; Saeed et al.,1995SAEED, H., KHAN, N. and RIZVI, S.N., 1995. Distributions of Chlorophyll a and phytoplanktom along the Karachi coast. In: M.-F. Thompson and N.M. Tirmizi. The Arabian Sea: Living Marine Resources and the Environment. Lahore, Pakistan: Vanguard Books (PVT) Ltd., pp. 509-517.; Baig et al., 2006BAIG, H.S., SAIFULLAH, S.M. and DAR, A., 2006. Occurrence and toxicity of Amphidinium carterae Hulburt in the North Arabian Sea. Harmful Algae, vol. 5, no. 2, pp. 133-140. http://dx.doi.org/10.1016/j.hal.2005.06.010.
http://dx.doi.org/10.1016/j.hal.2005.06....
; Latif et al., 2013LATIF, S., AYUB, Z. and SIDDIQUI, G., 2013. Seasonal variability of phytoplankton in a coastal lagoon and adjacent open sea in Pakistan. Turkish Journal of Botany, vol. 37, no. 2, pp. 398-410.; Munir et al., 2011MUNIR, S., SIDDIQUI, P.J.A. and MORTON, S.L, 2011. The occurrence of the ciguatera fish poisoning producing dinoflagellate genus Gambierdiscus in Pakistan waters. Algae - Korean Phycological Society, vol. 26, no. 4, pp. 317-325. http://dx.doi.org/10.4490/algae.2011.26.4.317.
http://dx.doi.org/10.4490/algae.2011.26....
, 2012MUNIR, S., NAZ, T., BURHAN, Z.N., SIDDIQUI, P.J.A. and MORTON, S.L., 2012. First report of the athecate, chain forming dinoflagellate Cochlodinium fulvescens (Gymnodiniales) from Pakistan. Pakistan Journal of Botany, vol. 44, pp. 2129-2134.,, 2013; 2016; Gul and Nawaz, 2014GUL, S. and NAWAZ, M.F., 2014. The Dinoflagellate genera Protoperidinium and Podolampas from Pakistan’s shelf and deep Sea Vicinity (North Arabian Sea). Turkish Journal of Fisheries and Aquatic Sciences, vol. 14, no. 1, pp. 91-100. http://dx.doi.org/10.4194/1303-2712-v14_1_11.
http://dx.doi.org/10.4194/1303-2712-v14_...
; Khokhar et al., 2018KHOKHAR, F.N., NAZ, T., BURHAN, Z.N., ABASSI, M.J. and SIDDIQUI, P.J.A., 2018. Occurrence of HAB / toxic Dinoflagellates species from the coast of Karachi, Pakistan (Northern Arabian Sea). Indian Journal of Geo-Marine Sciences, vol. 47, no. 1, pp. 73-88.) indicated a total of 235 taxa (204 species) in 40 genera from Pakistan. This is now improved by adding 51 new records to a total of 286 species (255 species). The current study reports 179 taxa, 154 species in 41 genera of dinoflagellates as oppose to worldwide distribution of 2377 species (259 genera) (Gómez, 2012GÓMEZ, F., 2012. A checklist and classification of living dinoflagellates (Dinoflagellata, Alveolata). Cicimar Oceanides, vol. 27, no. 1, pp. 65-140. http://dx.doi.org/10.37543/oceanides.v27i1.111.
http://dx.doi.org/10.37543/oceanides.v27...
). Similar dinoflagellate species have been reported from other regional waters, for example, India (179 spp; Padmakumar et al., 2012PADMAKUMAR, K.B., MENON, N.R. and SANJEEVAN, V.N., 2012. Is occurrence of harmful algal blooms in the exclusive economic zone of India on the rise? International Journal of Oceanography, vol. 2012, pp. 1-7. http://dx.doi.org/10.1155/2012/263946.
http://dx.doi.org/10.1155/2012/263946...
), Arabian Gulf and Sea of Oman (194 spp) (Polikarpov et al., 2016POLIKARPOV, I., SABUROVA, M. and AL-YAMANI, F., 2016. Diversity and distribution of winter phytoplankton in the Arabian Gulf and the Sea of Oman. Continental Shelf Research, vol. 119, pp. 85-99. http://dx.doi.org/10.1016/j.csr.2016.03.009.
http://dx.doi.org/10.1016/j.csr.2016.03....
), Kuwait waters in the Persian Gulf (105 spp) (Al-Kandari et al., 2009AL-KANDARI, M., AL-YAMANI, F. and AL-RIFAIE, K., 2009. Marine phytoplankton atlas of Kuwait’s waters. Safat, Kuwait: Kuwait Institute for Scientific Research.).

Only six genera (Tripos, Protoperidinium, Prorocentrum, Alexandrium, Diniphysis and Gonyaulax) that represent high species numbers (seven or more) are recorded in this study. Similar data has been obtained from the Arabian Gulf and Sea of Oman (Polikarpov et al., 2016POLIKARPOV, I., SABUROVA, M. and AL-YAMANI, F., 2016. Diversity and distribution of winter phytoplankton in the Arabian Gulf and the Sea of Oman. Continental Shelf Research, vol. 119, pp. 85-99. http://dx.doi.org/10.1016/j.csr.2016.03.009.
http://dx.doi.org/10.1016/j.csr.2016.03....
) where all these genera had higher diversity except for Alexandrium. Tripos (38 spp.) had highest number of species including five new records, whereas 53 species were reported previously (Shameel and Tanaka, 1992SHAMEEL, M. and TANAKA, J. 1992. A preliminary check-list of marine algae from the coast and inshore waters of Pakistan. In: T. NAKAIKE, S. MALIK, eds. Cryptogamic Flora of Pakistan. Tokyo: National cience Museum, vol. 1, pp. 1-64.; Munir et al., 2016MUNIR, S., NAZ, T., BURHAN, Z., SIDDIQUI, P.J.A. and MORTON, S.L., 2016. Species composition and abundance of dinoflagellates from the coastal waters of Pakistan. Journal of Coastal Life Medicine, vol. 4, no. 6, pp. 448-457. http://dx.doi.org/10.12980/jclm.4.2016J6-58.
http://dx.doi.org/10.12980/jclm.4.2016J6...
; Latif et al., 2013LATIF, S., AYUB, Z. and SIDDIQUI, G., 2013. Seasonal variability of phytoplankton in a coastal lagoon and adjacent open sea in Pakistan. Turkish Journal of Botany, vol. 37, no. 2, pp. 398-410.) that give rise to a total of 58 species of Tripos from coastal and shelf area of Pakistan. Thirty four taxa and 32 spp of Protoperidinium, including 12 new records, together with previously reported 27 species (Munir et al., 2016MUNIR, S., NAZ, T., BURHAN, Z., SIDDIQUI, P.J.A. and MORTON, S.L., 2016. Species composition and abundance of dinoflagellates from the coastal waters of Pakistan. Journal of Coastal Life Medicine, vol. 4, no. 6, pp. 448-457. http://dx.doi.org/10.12980/jclm.4.2016J6-58.
http://dx.doi.org/10.12980/jclm.4.2016J6...
; Latif et al., 2013LATIF, S., AYUB, Z. and SIDDIQUI, G., 2013. Seasonal variability of phytoplankton in a coastal lagoon and adjacent open sea in Pakistan. Turkish Journal of Botany, vol. 37, no. 2, pp. 398-410.; Gul and Nawaz, 2014GUL, S. and NAWAZ, M.F., 2014. The Dinoflagellate genera Protoperidinium and Podolampas from Pakistan’s shelf and deep Sea Vicinity (North Arabian Sea). Turkish Journal of Fisheries and Aquatic Sciences, vol. 14, no. 1, pp. 91-100. http://dx.doi.org/10.4194/1303-2712-v14_1_11.
http://dx.doi.org/10.4194/1303-2712-v14_...
) make a total of 59 species in this genus. A total of 24 species of Prorocentrum are now known from Pakistan, including 20 taxa (18 species) and 5 new records (current study) and 15 previously recorded species (Shameel and Tanaka, 1992SHAMEEL, M. and TANAKA, J. 1992. A preliminary check-list of marine algae from the coast and inshore waters of Pakistan. In: T. NAKAIKE, S. MALIK, eds. Cryptogamic Flora of Pakistan. Tokyo: National cience Museum, vol. 1, pp. 1-64.; Munir et al., 2013MUNIR, S.T., BURHAN, Z. U. N., SIDDIQUI, P. J. A. and MORTON, S. L., 2013. Seasonal abundance, biovolume and growth rate of the heterotrophic dinoflagellate (Noctiluca scintillans) from coastal waters of Pakistan. Pakistan Journal of Botany, vol. 45, no. 3, pp. 1109-1113.). Four new records of Alexandrium (current study; 9 taxa, 8 species) improved previously reported 5 species (Munir et al., 2016MUNIR, S., NAZ, T., BURHAN, Z., SIDDIQUI, P.J.A. and MORTON, S.L., 2016. Species composition and abundance of dinoflagellates from the coastal waters of Pakistan. Journal of Coastal Life Medicine, vol. 4, no. 6, pp. 448-457. http://dx.doi.org/10.12980/jclm.4.2016J6-58.
http://dx.doi.org/10.12980/jclm.4.2016J6...
) to 9 species in this genus. Eight taxa and 7 species of genus Dinophysis (including one new record) and 7 species of genus Gonyaulax are reported here. This report together with previously recorded species makes a total of 16 species of Dinophysis and 8 species of Gonyaulax (Saeed et al., 1995SAEED, H., KHAN, N. and RIZVI, S.N., 1995. Distributions of Chlorophyll a and phytoplanktom along the Karachi coast. In: M.-F. Thompson and N.M. Tirmizi. The Arabian Sea: Living Marine Resources and the Environment. Lahore, Pakistan: Vanguard Books (PVT) Ltd., pp. 509-517.; Baig et al., 2006BAIG, H.S., SAIFULLAH, S.M. and DAR, A., 2006. Occurrence and toxicity of Amphidinium carterae Hulburt in the North Arabian Sea. Harmful Algae, vol. 5, no. 2, pp. 133-140. http://dx.doi.org/10.1016/j.hal.2005.06.010.
http://dx.doi.org/10.1016/j.hal.2005.06....
; Gul and Saifullah, 2010GUL, S. and SAIFULLAH, S. M., 2010. Taxonomic and ecological studies on three marine genera of Dinophysiales from Arabian Sea shelf of Pakistan. Pakistan Journal of Botany, vol. 42, no. 4, pp. 2647-2660., 2012GUL, S. and SAIFULLAH, S. M., 2012. Marine planktic dinoflagellates of the order Gonyaulacales taylor from coastal waters of Sindh, Pakistan. International Journal of Phycology and Phycochemistry, vol. 8, no. 2, pp. 163-170.; Yaqoob et al., 2013YAQOOB, N., MASHIATULLAH, A., CHUGHTAI, F., SEHR, N., JAVED, T. and GHAFFAR, A., 2013. Phytoplanktons and zooplanktons diversity in Karachi coastal seawater under high and low tide during winter monsoon. The Nucleus, vol. 50, no. 2, pp. 141-148.; Latif et al., 2013LATIF, S., AYUB, Z. and SIDDIQUI, G., 2013. Seasonal variability of phytoplankton in a coastal lagoon and adjacent open sea in Pakistan. Turkish Journal of Botany, vol. 37, no. 2, pp. 398-410.).

Presence of bloom forming harmful algal species (73 HAB species in 27 genera), including 43 potentially toxic species, recorded in considerable cell density from coastal and near-shore waters imposes a threat to fisheries industry and human health. For example, some of the Prorocentrum species (P. gracile, P. micans, P. sigmoides and P. triestinum) have the ability to bloom with red discoloration which is not toxic but can cause fish mortality (Faust and Gulledge, 2002FAUST, M.A. and GULLEDGE, R.A., 2002. Identifying harmful marine dinoflagellates. Contributions from the United States National Herbarium, vol. 42, pp. 1-144.; Cohen-Fernandez et al., 2006; D’Silva et al., 2012D’SILVA, M.S., ANIL, A.C., NAIK, R.K. and D’COSTA, P.M., 2012. Algal blooms: a perspective from the coasts of India. Natural Hazards, vol. 63, no. 2, pp. 1225-1253. http://dx.doi.org/10.1007/s11069-012-0190-9.
http://dx.doi.org/10.1007/s11069-012-019...
; Sahraoui et al., 2013SAHRAOUI, I., BOUCHOUICHA, D., HADJ MABROUK, H. and SAKKA HLAILI, A., 2013. Driving factors of the potentially toxic and harmful species of Prorocentrum Ehrenberg in a semi-enclosed Mediterranean lagoon (Tunisia, SW Mediterranean). Mediterranean Marine Science, vol. 14, no. 2, pp. 353-362. http://dx.doi.org/10.12681/mms.338.
http://dx.doi.org/10.12681/mms.338...
). On the other hand, species of genus Alexandrium reported here are toxic and have cosmopolitan distribution (Taylor et al., 2003TAYLOR, F.J.R., FUKUYO, Y., LARSEN, J. and HALLEGRAEFF, G.M., 2003. Taxonomy of harmful marine dinoflagellates. In: G.M. HALLEGRAEFF, D.M. ANDERSON and A.D. CEMBELLA, eds. Manual on Harmful Marine Microalgae. Paris: 11IOC-UNESCO, pp. 389-432.). This and other HAB species of dinoflagellates have previously been reported from Pakistan waters (Khokhar et al., 2018KHOKHAR, F.N., NAZ, T., BURHAN, Z.N., ABASSI, M.J. and SIDDIQUI, P.J.A., 2018. Occurrence of HAB / toxic Dinoflagellates species from the coast of Karachi, Pakistan (Northern Arabian Sea). Indian Journal of Geo-Marine Sciences, vol. 47, no. 1, pp. 73-88.; Munir et al., 2016MUNIR, S., NAZ, T., BURHAN, Z., SIDDIQUI, P.J.A. and MORTON, S.L., 2016. Species composition and abundance of dinoflagellates from the coastal waters of Pakistan. Journal of Coastal Life Medicine, vol. 4, no. 6, pp. 448-457. http://dx.doi.org/10.12980/jclm.4.2016J6-58.
http://dx.doi.org/10.12980/jclm.4.2016J6...
), Indian waters (Baliarsingh et al., 2015BALIARSINGH, S.K., SRICHANDAN, S., NAIK, S., SAHU, K.C., LOTLIKER, A.A. and KUMAR, T.S., 2015. Seasonal variation of phytoplankton community composition in coastal waters off Rushikulya Estuary, East Coast of India. Indian Journal of Geomarine Science, vol. 44, no. 4, pp. 1-19.; Shahi et al., 2015SHAHI, N., GODHE, A., MALLIK, S.K., HÄRNSTRÖM, K. and NAYAK, B.B., 2015. The relationship between variation of phytoplankton species composition and physico-chemical parameters in northern coastal waters of Mumbai, India. Indian. Journal of Geomarine. Science, vol. 44, no. 5, pp. 673-684.; Padmakumar et al., 2012PADMAKUMAR, K.B., MENON, N.R. and SANJEEVAN, V.N., 2012. Is occurrence of harmful algal blooms in the exclusive economic zone of India on the rise? International Journal of Oceanography, vol. 2012, pp. 1-7. http://dx.doi.org/10.1155/2012/263946.
http://dx.doi.org/10.1155/2012/263946...
), Thailand (Karunasagar et al., 1990KARUNASAGAR, I., KARUNASAGAR, I., OSHIMA, Y. and YASUMOTO, T., 1990. A toxin profile for shellfish involved in an outbreak of paralytic shellfish poisoning in India. Toxicon, vol. 28, no. 7, pp. 868-870. http://dx.doi.org/10.1016/S0041-0101(09)80010-X. PMid:2219145.
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), Sea of Oman (Al Hashmi et al., 2012; Polikarpov et al., 2016POLIKARPOV, I., SABUROVA, M. and AL-YAMANI, F., 2016. Diversity and distribution of winter phytoplankton in the Arabian Gulf and the Sea of Oman. Continental Shelf Research, vol. 119, pp. 85-99. http://dx.doi.org/10.1016/j.csr.2016.03.009.
http://dx.doi.org/10.1016/j.csr.2016.03....
), Kuwait waters (Al-Kandari et al., 2009AL-KANDARI, M., AL-YAMANI, F. and AL-RIFAIE, K., 2009. Marine phytoplankton atlas of Kuwait’s waters. Safat, Kuwait: Kuwait Institute for Scientific Research.), Mediterranean Sea (Honsell et al., 1992HONSELL, G., BONI, L., CABRINI, M. and POMPEI, M., 1992. Toxic or potentially toxic dinoflagellates from the Northern Adriatic Sea. In: R.A. VOLLENWEIDER, R.A. VOLLENWEIDER, R. VIVIANI, eds. Marine Coastal Eutrophication. Elsevier Science, pp. 107-114. http://dx.doi.org/10.1016/B978-0-444-89990-3.50015-8.
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; Giacobbe et al., 1996GIACOBBE, M.G., OLIVA, F.D. and MAIMONE, G., 1996. Environmental factors and seasonal occurrence of the dinoflagellate Alexandrium minutum, a PSP Potential Producer, in a Mediterranean Lagoon. Estuarine, Coastal and Shelf Science, vol. 42, no. 5, pp. 539-549. http://dx.doi.org/10.1006/ecss.1996.0035.
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; Vila et al., 2001VILA, M., GARCÉS, E., MASÓ, M. and CAMP, J., 2001. Is the distribution of the toxic dinoflagellate Alexandrium catenella expanding along the NW Mediterranean coast? Marine Ecology Progress Series, vol. 222, pp. 73-83. http://dx.doi.org/10.3354/meps222073.
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; Lilly et al., 2002LILLY, E.L., KULIS, D.M., GENTIEN, P. and ANDERSON, D.M., 2002. Paralytic shellfish poisoning toxins in France linked to a human-introduced strain of Alexandrium catenella from the western Pacific: Evidence from DNAand toxin analysis. Journal of Plankton Research, vol. 24, no. 5, pp. 443-452. http://dx.doi.org/10.1093/plankt/24.5.443.
http://dx.doi.org/10.1093/plankt/24.5.44...
; Turki and Balti, 2005TURKI, S. and BALTI, N., 2005. Detection of toxic Alexandrium catenella (Whedon & Kofoid) Balech in clam production zone of North Lake and Channel, Tunisia. Harmful Algae News, no. 28, pp. 1-2.) and Australia (Hallegraeff, 2010HALLEGRAEFF, G.M., 2010. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge1. Journal of Phycology, vol. 46, no. 2, pp. 220-235. http://dx.doi.org/10.1111/j.1529-8817.2010.00815.x.
http://dx.doi.org/10.1111/j.1529-8817.20...
, Murray et al., 2012MURRAY, S.A., WIESE, M., NEILAN, B.A., ORR, R.J., DE SALAS, M., BRETT, S. and HALLEGRAEFF, G., 2012. A reinvestigation of saxitoxin production and sxtA in the ‘non-toxic’Alexandrium tamarense Group V clade. Harmful Algae, vol. 18, pp. 96-104. http://dx.doi.org/10.1016/j.hal.2012.05.001.
http://dx.doi.org/10.1016/j.hal.2012.05....
; Ajani et al., 2013AJANI, P., BRETT, S., KROGH, M., SCANES, P., WEBSTER, G. and ARMAND, L., 2013. The risk of harmful algal blooms (HABs) in the oyster-growing estuaries of New South Wales, Australia. Environmental Monitoring and Assessment, vol. 185, no. 6, pp. 5295-5316. http://dx.doi.org/10.1007/s10661-012-2946-9. PMid:23111868.
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). In general dinoflagellate toxin causes paralytic shellfish poisoning and diarrhetic shellfish poisoning and other potential hepato and neuro toxins (Anderson et al., 2012ANDERSON, D.M., ALPERMANN, T.J., CEMBELLA, A.D., COLLOS, Y., MASSERET, E. and MONTRESOR, M., 2012. The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. Harmful Algae, vol. 14, pp. 10-35. http://dx.doi.org/10.1016/j.hal.2011.10.012. PMid:22308102.
http://dx.doi.org/10.1016/j.hal.2011.10....
; Llewellyn et al., 2006LLEWELLYN, L., NEGRI, A. and ROBERTSON, A., 2006. Paralytic shellfish toxins in tropical oceans. Toxin Reviews, vol. 25, no. 2, pp. 159-196. http://dx.doi.org/10.1080/15569540600599217.
http://dx.doi.org/10.1080/15569540600599...
; Wiese et al., 2010WIESE, M., D’AGOSTINO, P.M., MIHALI, T.K., MOFFITT, M.C. and NEILAN, B.A., 2010. Neurotoxic alkaloids: saxitoxin and its analogs. Marine Drugs, vol. 8, no. 7, pp. 2185-2211. http://dx.doi.org/10.3390/md8072185. PMid:20714432.
http://dx.doi.org/10.3390/md8072185...
). The frequency of HAB events showed an increasing trend over last several decades owing to the changing environmental conditions, such as, wind, temperature, etc. (Smayda, 1990SMAYDA, T., 1990. Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic. In: E. GRANÉLI, B. SUNDSTRÖM, L. EDLER and D.M. ANDERSON, eds. Toxic marine phytoplankton. New York: Elsevier, pp. 29-40.; Anderson et al., 2002ANDERSON, D.M., GLIBERT, P.M. and BURKHOLDER, J.M., 2002. Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries, vol. 25, no. 4, pp. 704-726. http://dx.doi.org/10.1007/BF02804901.
http://dx.doi.org/10.1007/BF02804901...
; Glibert et al., 2005GLIBERT, P.M., ANDERSON, D.M., GENTIEN, P., GRANÉLI, E. and SELLNER, K.G., 2005. The global, complex phenomena of harmful algal blooms. Oceanography, vol. 18, no. 2, pp. 137-147. http://dx.doi.org/10.5670/oceanog.2005.49.
http://dx.doi.org/10.5670/oceanog.2005.4...
; Hallegraeff, 1993HALLEGRAEFF, G.M., 1993. A review of harmful algal blooms and their apparent global increase. Phycologia, vol. 32, no. 2, pp. 79-99. http://dx.doi.org/10.2216/i0031-8884-32-2-79.1.
http://dx.doi.org/10.2216/i0031-8884-32-...
, 2003HALLEGRAEFF, G.M., 2003. Harmful algal blooms: A global overview. Manual on Harmful Marine Microalgae, vol. 33, pp. 1-22., 2010HALLEGRAEFF, G.M., 2010. Ocean climate change, phytoplankton community responses, and harmful algal blooms: a formidable predictive challenge1. Journal of Phycology, vol. 46, no. 2, pp. 220-235. http://dx.doi.org/10.1111/j.1529-8817.2010.00815.x.
http://dx.doi.org/10.1111/j.1529-8817.20...
), which consequently has increased upwelling of nutrient rich waters. In addition anthropogenic activities also increase nutrient input in the coastal waters, causing increased planktonic bloom formation (Parab et al., 2006PARAB, S.G., PRABHU MATONDKAR, S.G., GOMES, H.R. and GOES, J.I., 2006. Monsoon driven changes in phytoplankton populations in the eastern Arabian Sea as revealed by microscopy and HPLC pigment analysis. Continental Shelf Research, vol. 26, no. 20, pp. 2538-2558. http://dx.doi.org/10.1016/j.csr.2006.08.004.
http://dx.doi.org/10.1016/j.csr.2006.08....
; Gomes et al., 2009GOMES, H.R., MATONDKAR, S.G.P., PARAB, S.G., GOES, J.I., PEDNEKAR, S., AL-AZRI, A.R. and THOPPIL, P.G., 2009. Unusual blooms of green Noctiluca miliaris (Dinophyceae) in the Arabian Sea during the winter monsoon. Indian Ocean Biogeochemical Processes and Ecological Variability, vol. 185, 347-363.). Such blooms tend to deplete dissolved oxygen in the water column and as a result health and abundance of fish in these waters would be effected (Goes et al., 2005GOES, J.I., THOPPIL, P.G., GOMES, H.R. and FASULLO, J.T., 2005. Warming of the Eurasian landmass is making the Arabian Sea more productive. Science, vol. 308, no. 5721, pp. 545-547. http://dx.doi.org/10.1126/science.1106610. PMid:15845852.
http://dx.doi.org/10.1126/science.110661...
). This will also have an implication on the population structure of plankton in the regional waters and in turn will influence the marine food chain and shift the balance towards the HAB species (Ramsdell et al., 2005RAMSDELL, J.S., ANDERSON, D.M. and GLIBERT, P.M., 2005. Harmful algal research and response: a national environmental science strategy 2005-2015. Washington, DC: Ecological Society of America. 96p.). Occurrence and increasing cell densities of HAB related dinoflagellates species pose threat to the safety of fishery products as well as human and environmental health. Therefore, regular monitoring of the occurrence, distribution and abundance of HAB related species and their blooms is recommended for fishery management and food and health safety.

Acknowledgement

The first author is highly thankful to the Director, Center of Excellence in Marine Biology, University of Karachi for providing research facilities.

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Publication Dates

  • Publication in this collection
    09 July 2021
  • Date of issue
    2022

History

  • Received
    30 Oct 2020
  • Accepted
    10 Nov 2020
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