First recorded bloom of Akashiwo sanguinea (Dinophyceae) from the Cochin backwaters, a tropical estuarine system along the South Eastern Arabian Sea

Akashiwo sanguinea (Hirasaka) G. Hansen and Moestrup is a well-known red tide-forming dinoflagellate that occurs in coastal marine ecosystems with varying salinity owing to its euryhaline nature. The tolerance to salinity fluctuations makes the species capable of thriving in different environmental conditions (Matsubara et al. 2007; Phlips et al. 2011; 2012; Park et al. 2013; Badylak et al. 2014a,b). Akashiwo sanguinea is a cosmopolitan species and has been observed in the form of blooms in many coastal and estuarine areas around the world, including the North Eastern Pacific and South Pacific (Fukuyo et al. 1990; Cai et al. 2006; Park et al. 2013; Kiefer & Lasker 1975; Robinson & Brown 1983; Horner et al. 1997; Gómez-Aguirre 1998; Cloern et al. 2005; Rines et al. 2010; Du et al. 2011; White et al. 2014; Hallegraeff 1991; Kahru et al. 2004). A. sanguinea has also been reported from the North Atlantic, the Mediterranean, the South-West Atlantic and from the Gulf of Mexico (Bochstahler & Coats 1993; Badylak & Phlips 2004; Phlips et al. 2011; 2012; O’Boyle & McDermott 2014; Gómez & Boicenco 2004; Feyzioğlu & Öğüt 2006; Domingos & Menezes 1998; Melo et al. 2007; Koening et al. 2014; Harper & Guillen 1989; Robichaux et al. 1998; Badylak et al. 2014a,b).

A. sanguinea is relatively large and lives as single cells. In the cross-section, the cell is ovoid and strongly dorso-ventrally compressed. The cingulum is approximately central and slightly descending. The epicone is bluntly rounded and the hypocone is bilobed with incised sulcus. The cell contains a large number of elongated yellow or brown chloroplasts, which radiate from the cell center. Like most dinoflagellates, it has two flagella, one wrapped around the equator of the cell in a groove and the other extending beyond the cell to facilitate its movement in water (Hargraves 2011). Reproduction takes place primarily by the asexual process via binary fission (Lalli & Parsons 1993), however, the sexual process through formation of isogametes also occurs occasionally (Silva & Faust 1995).

The taxon was first reported as Gymnodinium sanguine on the coast of Japan as a red tide-forming organism (Hirasaka 1922) and later, based on its morphological, ultrastructural, and phylogenetic relationship with a large assemblage of gymnoid-type dinoflagellates, it was renamed as Akashiwo sanguinea (Hirasaka) G. Hansen and Moestrup (Daugbjerg et al. 2000). Even though Akashiwo sanguinea is not associated with toxic production, blooms of these species were reported to coincide with depletion of dissolved oxygen and mortality of fish and shellfish in various parts of the world (Hirasaka 1922; Hallegraeff 1993; Robichaux et al. 1998; Wu et al. 2000). The inclusion of A. sanguinea as a harmful algal bloom (HAB) is based on various observations of adverse effects of these blooms on invertebrates, fish and bird communities through the formation of hypoxic conditions due to high respiratory oxygen demand of phytoplankton and accompanying bacterial communities (Diaz 2001; Diaz & Rosenberg 2008; Murray et al. 2015).

As most of the reports on Akashiwo sanguinea blooms come from temperate climate zones, this paper reports the first record of the A. sanguinea bloom along the tropical estuarine waters of Cochin (South Eastern Arabian Sea), thus delineating the dynamics of its population with temporal variability based on the main environmental parameters.

The study was carried out along the Cochin estuary (09°57’51”N; 76°16’56”E; Fig. 1), which is located on the southwest coast of India and is connected with the Arabian Sea through two inlets at Cochin and Azhikode. It is the second largest estuarine system in India, fed by six river discharges, more than 60% of which occur during the summer monsoon (June–September), 10–25% during the winter monsoon (November–December) and the remainder during the rest of the year.

Figure 1

Monthly sampling of dinoflagellates was conducted in the study area for a period of 12 months, from November 2018 to October 2019. Hydrobiological characteristics of the study area were also determined during the study period. Surface water temperature (SWT) was measured using a precision mercury thermometer with an accuracy of ± 0.01°C. Salinity was measured using a hand-held refractometer (RHS-10 ATC). Measurements of pH were taken using a portable pH meter (pHep®, Europe, accuracy ± 0.01), calibrated with standard buffers prior to field sampling. The Secchi disc was used to measure the euphotic column depth. Dissolved oxygen was estimated using modified Winkler’s method (Winkler 1888). Nutrients such as nitrate and phosphate were estimated using standard procedures (Grasshoff et al. 1983). Chlorophyll a was measured spectrophotometrically using a Hitachi U-2900 UV/VIS spectrophotometer following the acetone extraction method (Parsons et al. 1984). Phytoplankton samples were collected by filtering ~50 l of surface water through a 20 μm mesh bolting silk and preserved in 3% neutralized formaldehyde solution. Qualitative and quantitative analysis of phytoplankton samples were carried out using a Sedgewick-Rafter Counting Cell under a Leica DM2500 microscope following standard identification keys (Tomas 1997).

Blooms of Akashiwo sanguinea were previously observed mainly in temperate waters, including the California coast, the New Jersey coast in the U.S.A., Esquimalt in Canada, the Black Sea, Venice, Liverpool Bay and the Ariake Sea in Japan (Martin 1928; Voltolina 1975; Voltolina et al. 1986; Voltolina 1993; Horner et al. 1997; Gómez & Boicenco 2004; Matsubara et al. 2007; Rines et al. 2010). However, due to their eurythermal nature, their occurrence has also been reported from subtropical and tropical ecosystems of Brazil and Hong Kong Bay (Matsubara et al. 2007; Domingos & Menezes 1998; Lu & Hodgekiss 2004). The present report on A. sanguinea blooms from the Cochin estuary indicates the expansion of the species to tropical ecosystems, where it plays a major role in the microalgal community structure.

The Cochin estuary is exposed to significant fluctuations in salinity due to the large inflow of freshwater from discharging rivers and terrestrial input during monsoon seasons.

A. sanguinea was observed to survive in salinity ranging from 22 to 24 PSU and its abundance peaked (2.85 × 10⁵ cells l⁻¹) in June when salinity was 22 PSU (Fig. 6). The euryhaline character of A. sanguinea was established by Matsubara et al. (2007), who observed the growth of the species in salinity between 10 and 40 PSU. Another study on phytoplankton populations in the Indian River lagoon in Florida also showed the persistence of A. sanguinea over a wide range of salinity from 10 to 30 PSU (Phlips et al. 2012), thereby indicating its ability to thrive in a wide range of salinity. In the later phase of the monsoon season (July– August), the A. sanguinea cell density declined (9 × 10² cell l⁻¹) as the salinity dropped to the fresh water level (3 PSU). The inhibition of A. sanguinea growth in response to the rapid decline in salinity was previously reported by Shikata et al. (2008). The sudden drop in salinity could have resulted in the decline of A. sanguinea abundance during this period.

A. sanguinea shows a preference for water temperature between 10°C and 30°C, with the optimal growth at 25°C (Matsubara et al. 2007). In the present study, however, the blooms of A. sanguinea were observed in a temperature range of 26 to 30°C (Fig. 7), suggesting that the species in the Cochin estuary shows the maximum growth in the upper range of temperature, i.e. above 25°C, and its eurythermal nature likely contributes to its success in the ecosystem.

Changes in the nutrient availability affect the dynamics of A. sanguinea blooms and are positively correlated with total phosphorus and total nitrogen concentrations (Badylak et al. 2014a). The maximum cell density of A. sanguinea (2.85 × 10⁵ cells l⁻¹) in the Cochin estuary was observed during the period of elevated nitrate and phosphate concentration (26 μmol l⁻¹ and 3.8 μmol l⁻¹, respectively) in June (Fig. 3). Similar observations on the relationship between the increase in nutrient levels and the increase in A. sanguinea were observed in the British Columbia coastal waters (Robinson & Brown 1983), as well as in the tropical estuarine waters of northeastern Brazil (Koening et al. 2014).

In addition to these physicochemical factors, the success of Akashiwo sanguinea in a wide range of estuaries throughout the world is also associated with the extracellular mucus production. It has been observed that A. sanguinea produces large amounts of mucilage, with up to 50% of the photosynthate excreted through the pores in the cell surface (Smayda 2002; Badylak et al. 2014b). According to Smayda (2002), the mucus excretion by these dinoflagellates changes the physical and chemical structure of the water column, as well as reduces the turbulence of the water column, favoring the bloom formation. The excretion of mucus by algae has certain advantages, as it increases the nutrient availability, helps to compete with other phytoplankton species and reduces grazing losses (Reynolds 2006). In some cases, however, a large amount of mucilage is also said to have a negative effect on other planktic, pelagic and benthic organisms, compared to other mucus-producing algal species (Shumway 1990; Buskey & Hyatt 1995; Liu & Buskey 2000; Botes et al. 2002). Blooms of A. sanguinea were also associated with fish mortality in certain parts of the world (Lassus 1988; Hallegraeff 1993; Robichaux et al. 1998; Wu et al. 2000). The discoloration of surface water as a result of the accumulation of carotenoids (Cantonati et al. 2003) has attracted the attention of scientists and tourists due to the bloom-forming potential of the species.

A. sanguinea is a well-known bloom forming dinoflagellate that occurs all over the world and has been associated with upwelling systems as well as with climate change and the related water column stratification (Kudela et al. 2010). The study reports the occurrence of A. sanguinea along the Cochin estuary and determines its dynamics with seasonal changes based on parameters such as salinity, temperature and nutrient concentrations. The recurring blooms and continuous presence of A. sanguinea can be attributed to its euryhaline and eurythermal characteristics, which can be further linked to changes in physicochemical characteristics as well as microalgal community structure. Since the bloom of A. sanguinea is closely related to the increase in nutrient concentrations, particularly nitrate and phosphate, the impact of anthropogenic eutrophication on the expansion of the species to tropical estuarine waters cannot be neglected.