Eutrophication enhances phytoplankton abundance in the Maheshkhali channel, Bay of Bengal, Bangladesh

INTRODUCTION

Eutrophication defined as the increased rate of primary production and accumulation of organic matter,[1] usually results from the excessive addition of nutrients that results in an undesirable change in ecosystems, food webs, water quality, and aquatic chemistry.[2,3] Consistent with global features, eutrophication is also a common phenomenon in the coastal area of the Bay of Bengal (BoB) because the bay receives large volume of freshwater that injects loads of nutrients and suspended sediment[4,5] and makes the BoB as a zone prone for algal blooms including harmful ones. The potential toxicity of harmful algal blooms causes fish kills in the coastal area of the BoB by toxin production (i.e., paralytic shellfish poisoning)[6,7] and negative impact on human health.[8,9]

In general, phytoplankton blooms in various coastal waters of the BoB are found throughout the year. The west coast of the BoB, for instance, undergoes periods of strong upwelling during monsoon and delivers cold, nutrient-rich waters from bottom depth result in higher primary production.[10] In contrast, the east coast of the BoB experiences strongly stratified surface layer and restricts the transport of nutrient from deeper layer to the surface during southwest monsoon (June– September) due to enormous influx of freshwater through precipitation and riverine discharge result in lower productivity.[11] The majority of bloom cases are reported in the BoB during the pre-monsoon (February–May).[12] However, the entire BoB is considered to have lower biological productivity than its western counterpart, the Arabian Sea, due to various reasons such as narrow shelf, cloud cover during summer monsoon, turbidity resulting from sediment influx and freshwater-induced stratification.[13-15]

The coastal waters of Bangladesh including the Maheshkhali channel are also vulnerable to eutrophication because it receives huge nutrients from river discharge, shrimp culture, agricultural, and industrial effluents which induces the growth of many harmful algal species (i.e., Dinophysis caudata, Dinophysis mitra, Alexandrium catenella, Lingulodinium polyedrum, and Gymnodinium coeruleum).[16] Although massive fish kills are being seen in this channel during heavy blooms of D. caudata in different years since 1998,[16] there are very few studies focusing on eutrophication and harmful algal blooms in the coastal waters of the BoB, Bangladesh. Therefore, the purpose of this research is to analyze the temporal distribution of phytoplankton abundances and its relationship with environmental parameters in the Maheshkhali channel. We hypothesize that eutrophication enhances phytoplankton abundance in the Maheshkhali channel, BoB, Bangladesh.

MATERIALS AND METHODS

Study Area

The present study was carried out in the Maheshkhali channel, situated at the south-eastern coast of the BoB [Figure 1]. Three sampling sites were selected at the mouth of this channel. The channel includes Bakkhali River in the north that brings much of domestic, agricultural and industrial wastes, and opens into the BoB in the south. This channel, like Cox’s Bazar coast, has a semidiurnal tidal regime. Its hydrology is also heavily influenced by monsoon wind.[17] The Maheshkhali channel is very important as a large fishing ground and a center for recreation. Different traditional capture fisheries and commercial shrimp farms have developed around the estuary. This channel considered as highly productive because of excessive nutrients invaded from industrial wastes, agricultural lands, rural and urban sewages and from the adjacent shrimp/bivalve farms, which sometimes induces the growth of many harmful algal blooms.[18]

Figure 1: Map showing the sampling stations in the Maheshkhali channel, south-east coast of the Bay of Bengal, Bangladesh

RESULTS

Higher abundance of phytoplankton (33 × 105 ± 16 × 105 cells l−1) was recorded in October during early post-monsoon [Figure 2] followed by November (27 × 105 ± 1.3 × 105 cells l−1) and December (22 × 105 ± 0.66 × 105 cells l−1). The lowest phytoplankton abundance was detected in June during the early monsoon (6 × 105 ± 1 × 105 cells l−1). After that, phytoplankton abundance was progressively increased, and comparatively higher abundances were detected during August (20 × 105 ± 3.7 × 105 cells l−1) and September (21.61 × 105 ± 1.4 × 105 cells l−1). However, comparatively low abundance of phytoplankton was detected during pre-monsoon (February–May) (mean 10 × 105 ± 2 × 105 cells l−1). During the study period, about 98 species of phytoplankton belonging to Bacillariophyceae (67), Dinophyceae (23), Chlorophyceae (4), and Cyanophyceae (4) were recorded. The dominant species of Bacillariophyceae and Dinophyceae are shown in Table 1.

Figure 2: Temporal distribution of total phytoplankton abundances from January to December in the Maheshkhali channel, Bay of Bengal, Bangladesh

Table 1: List of some dominant species obtained in the Maheshkhali channel during the study period

Comparatively high temperature was recorded in August (31.67 ± 0.29°C), September (29.67 ± 0.29°C) and April (29.83 ± 0.29°C), whereas lower temperature was observed in October (21.17 ± 0.76°C) and November (20.83 ± 0.29°C) [Figure 3a]. The highest salinity was recorded in April (34) [Figure 3b]. After that, it was gradually decreased to 17.67 ± 1.5 in August, and the lowest salinity was in October (13.67 ± 1.5). The highest concentration of NO₃-N (15.7 ± 1.47 µM) was recorded during August, whereas the lowest concentration (4.3 ± 0.27 µM) was in June [Figure 4a]. After August, NO₃-N was gradually decreased to 9.67 ± 0.43 µM in December. On average, comparatively low concentration of NO₃-N was recorded in pre-monsoon (7.8 ± 1.46 µM). Two peaks of PO₄-P values were found in August (32 ± 4.2 µM) and November (34.43 ± 2.98 µM) [Figure 4b]. The lowest concentration of PO₄-P was recorded in June (6.11 ± 2.44 µM) during early monsoon. Total phytoplankton abundances in the Maheshkhali channel were found to be significantly positively related with NO₃-N (r = 0.533, P < 0.01) and PO₄-P (r = 0.719, P < 0.01). It showed significantly negative relation with temperature (r = −0.42, P < 0.05) and salinity (r = −0.613, P < 0.01) [Table 2]

Figure 3: (a) Temporal distribution of total phytoplankton abundances and temperature from January to December in the Maheshkhali channel. (b) Temporal distribution of total phytoplankton abundances and salinity from January to December in the Maheshkhali channel

Figure 4: (a) Temporal distribution of total phytoplankton abundances and nitrate-nitrogen from January to December in the Maheshkhali channel. (b) Temporal distribution of total phytoplankton abundances and phosphate-phosphorus from January to December in the Maheshkhali channel

Table 2: Pearson’s correlation coefficient between phytoplankton abundance and water quality parameters

DISCUSSION

Phytoplankton blooms in the Maheshkhali channel were found in October (33 × 105 ± 16 × 105 cells l−1)during early post-monsoon [Figure 2] due to higher concentration of NO₃-N and PO₄-P from the Bakkhali river discharge and precipitation. In this study, phytoplankton abundance has significantly positive relation with NO₃-N (r = 0.533, P < 0.001) and PO₄-P (r = 0.719, P < 0.001) [Table 2]. In fact, during post-monsoon, the conditions were favorable, such as bright sunlight and nutrient input from rainfall, which helped in the formation of algal bloom. Consistently, post-monsoon blooms were usually observed in some coastal areas of the BoB including coast of Mangalore, Goa, Tamil Nadu, and Gulf of Mannar, Orissa.[22-25] Ideally, after monsoon, cloud cover is reduced and sunlight irradiance enhanced, and therefore, phytoplankton appeared to benefit from both improved light conditions and nutrient inputs from estuarine mechanisms and river runoff.[15] However, the blooming process in the BoB is mainly influenced by seasonal upwelling and monsoonal forcing that causes high riverine discharge, resulting in nutrient-reached water that provides a competitive edge for blooms of phytoplankton species.[12]

In this study, phytoplankton not only significantly positively related with nutrients but also significantly negatively related with water temperature and salinity [Table 2], partially agreeing with the previous studies in the Maheshkhali channel by Jewel et al.,[26] who reported the highest cell density and species diversity of phytoplankton in post-monsoon (November), when phosphate and salinity were found to be highest. In the present study, phytoplankton peaks during the lowest level of salinity [Figure 3b] might be due to comparatively higher river discharge during early post-monsoon. Consistently, salinity is the lowest in the northern part of the BoB, where monsoon rains and flow from the Ganga-Brahmaputra-Meghna delta combine to give a great input of freshwater, especially between June and October.[27] Furthermore, phytoplankton in the east coast of the BoB during the northeast monsoon (November-February) is limited by nutrients but not by light.[15] Entrainment of nutrient-rich water by wind mixing is not efficient in the BoB.[28] Consistently, it could be said that phytoplankton blooms in early post-monsoon at the Maheshkhali channel support the phase-I eutrophication model[2] emphasizing that changing nutrient input acts as a signal and responses to that signal is increased phytoplankton abundance. It also follows pressure-state-response approach;[29-31] it relates pressures (i.e., increased nutrients) to primary effects such as increased phytoplankton blooms and secondary effects such as potentially increased harmful algal blooms. For instance, harmful algae (i.e., Pseudo-nitzschia spp.) created blooms in November that strongly related with PO₄-P concentration and codominant with other diatom species (i.e., Chaetoceros curvisetus, Asterionellopsis glacialis, and Coscinodiscus wailesii) in the Maheshkhali channel.[18]

Although the highest concentration of NO₃-N in the Maheshkhali channel from the Bakkhali river discharge and precipitation was recorded during the late monsoon, comparatively moderate abundance of phytoplankton (39% lower abundance than October) was observed in August when the highest temperature was observed [Figure 3a]. This might be related to non-efficient utilization of nutrients by phytoplankton under low irradiance due to monsoonal cloud cover.[32] Nutrient uptake is an energy-demanding process and is partly light-dependent.[33] However, there is less occurrence of blooms during monsoon in the west coast of the BoB.[12] The underlying mechanism is that huge river discharge in monsoon stimulate stratification in water column inhibiting coastal mixing and makes the scarcity of nutrients in surface water.[11] Furthermore, the increased river flux during summer and fall inter-monsoon months considerably reduced the depth of light penetration and restricts primary productivity in spite of availability of nutrient.[34] However, the BoB is traditionally considered to be a region of lesser biological productivity primarily from the lack of availability of nitrate in the upper layers arising from strong stratification and weaker winds, which inhibits vertical mixing.[11]

During monsoon, mixotrophic dinoflagellates such as Ceratium furca, C. tripos, C. fusus, Dinophysis caudata, and Prorocentrum micans were dominant in the Maheshkhali channel;[26] their unique characteristics of vertical migration and heterotrophy are reasonably well-understood.[35-37] Consistently, Patil[38] reported high concentration of dinoflagellates (i.e., Cochlodinium polykrikoides and Gymnodinium catenatum) during a monsoon break in coastal water off Goa and their concentration decreased with restart of freshwater discharge.

The lowest abundance was detected in June during early monsoon which may be due to the lowest concentration of NO₃-N and PO₄-P, possibly resulted from lower freshwater discharge and precipitation, agreeing with the previous record in Maheshkhali channel by Jewel et al.,[26] who reported the lowest phytoplankton abundances in June associated with lower nutrients. Comparatively lower abundance was detected during pre-monsoon (February–May) due to the lower nutrients and comparatively high water temperature [Figure 3a]. A similar pattern was reported by Paul et al.[39] in that higher temperature (>30°C), calm waters and lower nutrients are prevalent in the BoB during spring inter-monsoon (April–May) and also attributed that this condition is ideal for the growth of cyanobacteria. A similar pattern was reported by Rivera-Monroy et al.[40] in that depression in primary productivity occurred during dry months of February–May. In contrast, the majority of bloom cases in east coast of the BoB have been reported during pre-monsoon, mostly dominated by diatom (i.e., Asterionella japonica) and cyanobacteria (Trichodesmium erythraeum); warm waters and low nutrients during pre-monsoon are known to favor Trichodesmiun blooms.[41]

CONCLUSION

Consistent with our hypothesis, it is attributed that higher concentration of NO₃-N and PO₄-P from Bakkhali river discharge and precipitation enhanced phytoplankton abundance in October during early post-monsoon in the Maheshkhali channel. Along with nutrients, lower salinity resulted from freshwater discharge and lower temperature in surface water might have an impact on bloom formation. Inversely, lower abundances of phytoplankton were observed during early monsoon (June) and pre-monsoon due to comparatively lower concentration of NO₃-N and PO₄-P. During that period, comparatively higher water temperature and salinity were also observed. Furthermore, moderate abundance of phytoplankton was observed during late monsoon (August), although the highest concentration of NO₃-N and PO₄-P was recorded. The underlying mechanism was likely that huge river discharge might have caused higher turbidity that inhibited light penetration and restricted phytoplankton abundance. Therefore, it is observed that nutrient could enhance phytoplankton abundance along with suitable environmental parameters. However, further studies are needed to understand phytoplankton community response to the changing nutrients levels as well as environmental parameters in the Maheshkhali channel of the BoB.