Seasonal variations influencing the abundance and diversity of plankton in the Swarnamukhi River Estuary, Nellore, India

: An integrated approach was used to study the seasonal influence on the abundance and diversity of phytoplankton and zooplankton in the Swarnamukhi River Estuary (SRE) and the adjacent coast covering five stations by collecting monthly samples from the years 2014 to 2017. A total of 54 phytoplankton species conforming to four families and 58 zooplankton species conforming to nine families were recorded. Phytoplankton abundance and richness were high during pre-monsoon (PRM - 56410 cells/L) followed by monsoon (MON – 42210 cells/L). A similar trend was observed in the case of zooplankton, where abundance was recorded high during PRM (124261 ind./m 3 ) followed by MON (111579 ind./m 3 ). Moreover, phytoplankton and zooplankton were dominated by the diatoms and copepods, respectively. Both phytoplankton and zooplankton exhibited significant temporal (F= 26.4, p <0.05) and spatial (F= 32.1, p <0.05) variations. The higher density and abundance were recorded in the inner stations compared to the open sea. The present study reveals that the SRE have a rich diversity which could be attributed to a higher nutrient influx in the inner stations. The anthropogenic discharge from the surrounding aqua farms, agricultural land, and human settlement area could cause concerns for the local flora and fauna if a proper mitigation plan is not evolved through long-term monitoring study in this coastal region.


INTRODUCTION
Estuaries act as transitional zones and support the coastal economy in the form of fishing, aquaculture, transport, and tourism activities. They are also known to be highly productive ecosystems that provide shelter and breeding grounds for various marine aquatic organisms (Nybakken & Bertness 2005). Unlike salt marshes and backwaters, estuaries are complex and highly dynamic and their structure and function are influenced by anthropogenic inputs (e.g., aquaculture, agriculture, and industrial discharges) from the land and get transferred to the sea (Shenai-Tirodkar et al. 2016). Such anthropogenic activities can alter the physicochemical properties of water and immensely influence the migration, richness, distribution, diversity, and feeding of the associated marine aquatic organisms (Unanam & Akpan 2006). Plankton are aggregates of organisms (plants and animals) passively floating, drifting, or somewhat motile occurring in aquatic ecosystems (Lalli & Parsons 1993). Phytoplankton is grazed upon by zooplankton and other higher aquatic organisms (nektons) (Calbet 2008). Nutrient enrichment through, riverine inputs, and discharge from anthropogenic activities can significantly alter the phytoplankton growth and in turn affect the zooplankton grazing pressure (Berdalet et al. 1996). Therefore, plankton assemblages are usually helpful in assessing the water quality as they quickly respond to the environmental changes, hence; act as ecological indicators of an ecosystem (Hays et al. 2005;Longhurst 2007).
In the Indian scenario, most of the estuarine ecosystems are under stress due to natural and anthropogenic inputs from the surrounding environment. With the increase in nearby aquaculture, agricultural, and anthropogenic activities, the effluent discharges find their way into the nearby coastal areas which provides an advantageous environment to the organisms for proliferation. Similar activities have been reported in the Swarnamukhi River Estuary (SRE) region, fewer studies have been carried out to assess the tidal variations (Reddi et al. 1993), hydrographic properties of water (Sreenivasulu et al. 2015), contamination studies on the presence of heavy metal in seawater, sediments, & organisms (Reddy et al. 2016;Sreenivasulu et al. 2018;Jha et al. 2019), and the benthic organisms (Pandey et al. 2021). However, an elaborate study for the plankton communities is not available for the SRE region. A long-term study (2014)(2015)(2016)(2017) was conducted to analyze the planktonic (phytoplankton and zooplankton) assemblages. This study can serve as baseline information for future ecological assessment related to the SRE and other similar tropical ecosystems.

Study area
The SRE region (14.072-14.077 °N and 80.126-80.154 °E), situated in the Vakadu Mandal of Nellore district, Andhra Pradesh. This estuarine runs about 1.5 km in length perpendicular to the Bay of Bengal with an average depth of 1.0 m and an area of 6.25 km 2 (Reddi et al. 1993). Nellore receives the majority of the rainfall during the north-east monsoon (October to December) than the south-east monsoon (Kannan et al. 2016). Altogether, five sampling stations were fixed; four stations covering SRE and a reference station in the open sea (OS) about a kilometer from the shore. The coordinates were fixed using GPS (Garmin) covering the study area and the surrounding coast. The selected sampling stations are shown in (Figure 1

Temperature and rainfall
The temperature and rainfall data for the sampling period were obtained from the Indian Meteorological Department, Ministry of Earth Sciences, Government of India. The obtained data (monthly) was plotted for better interpretation (refer to Figure 2).

Biological parameters
For phytoplankton sampling, 5.0 L of surface seawater samples (in triplicate) were collected in a polyethylene container and preserved with 4% formalin and Lugol's iodine. Phytoplankton analysis was carried out using Utermöhl (1931) sedimentation technique. The samples were allowed to settle in a measuring cylinder for a period of 48 hours and siphoned (using a 10 µ mesh) to obtain 50 mL concentrate (Hasle,1978). For phytoplankton enumeration, 1 mL of the concentrated sample was taken onto a Sedgewick rafter plankton counting chamber and the total number of organisms was examined under a compound microscope. Phytoplankton was identified using standard identification keys (Subrahmanyan  1946, 1959Santhanam et al. 1987;Tomas 1997). For chlorophyll-a (chl-a) analysis, 1,000 mL of the water sample was filtered through Whatman GF/F filter paper and chl-a, was extracted by following the modified acetone extraction method (Parson et al. 1984). The extracted chl-a samples were analyzed using a spectrofluorometer (make Hitachi model F-4600) and obtained results were expressed in mg/m 3 . The surface zooplankton samples were collected using a zooplankton net (150 μm mesh size, 0.5 m diameter, 1.8 m length) fitted with a digital flow meter (make Hydro-Bios). The surface hauls were made from the stern side of the boat running at a speed of 1 km/hr and the collected plankton was transferred to 500 mL polythene containers and preserved using 5% buffered formalin. In the laboratory, triplicate subsamples were taken onto a Sedgewick rafter plankton counting chamber and the total numbers of organisms were enumerated under the compound microscope (Nikon model SMZ 1500). The zooplankton was identified following the standard identification key of Kasturirangan (1963) and Santhanam & Srinivasan (1994). The zooplankton biomass was determined by the settled volume method, where the collected sample was allowed to settle and the obtained biomass was expressed as mL/m 3 .
Statistical analysis PRIMER v6.1 was used for univariate indices, e.g., species richness (S), abundance, Margalef's diversity (d), Shannon-Wiener diversity index (H′, log 2 ), Simpson's diversity (1-λ), and Pielou's evenness (J′) (Clarke & Gorley 2006). The sitewise variation between the environmental parameters were analyzed using one way analysis of variance (ANOVA) in Microsoft Excel 2007. To determine the phytoplankton diversity and dominance in different seasons and the stations, univariate diversity indices were applied. The abundance of phytoplankton and zooplankton was represented using a box plot using SPSS v10 software.

Temperature and rainfall
The rainfall data were analyzed for the years 2014-2017 and it indicates that maximum rainfall was recorded from September to December ( Figure 2). It ranged 6.2-221.1 mm (2014)
During the study period, the highest phytoplankton density was recorded in the SRM (56,410 cells/L) and it was lowest in the OS (2,440 cells/L). Phytoplankton density in the inner riverside stations, BC, SR2, and SR1 ranged 9,605-50,160 cells/L, 7,785-56,340 cells/L, and 10,500-55,850 cells/L, respectively. In SRM and OS, phytoplankton density ranged 10,033-56,410 cells/L and 2,440-37,100 cells/L, respectively. The mean phytoplankton density recorded in the inner stations BC, SR2, and SR1 were 19,785, 21,005, and 18,815 cells/L, respectively (Figure 4a). In the SRM and OS region, the mean phytoplankton density was 20000 and 17864 cells/L, respectively. The maximum density recorded in PRM, MON,and POM was 56,410,42,210,and 24,480 cells/L, respectively. The phytoplankton density in PRM ranged 13,647-23,217 cells/L, in MON it ranged 18,585-22,746 cells/L, and in POM it ranged 9,492-16,973 cells/L (Figure 4a). Among diatoms, Rhizosolenia sp. was the dominant species in all the stations, followed by Thalassiosira subtilis and Navicula sp. The Protoperidinium sp. dominated the dinoflagellates community followed by Ceratium sp. and Prorocentrum sp. during the study period. All the three species of green algae (Chlorella sp., Oocystis sp., and Pediastrum sp.) were present during MON, while only Chlorella sp. and Oocystis sp. were represented during PRM and none of the three species mentioned above were present during POM. Among the four blue-green algae recorded during the study, Trichodesmium sp. and Spirulina sp. were observed during PRM, Microcystis sp. and Oscillatoria sp. were observed during POM, and all the four species were present during the MON. The SRE received precipitation during the POM (north-east monsoon) which could enhance the land-driven run-off from the aqua farms, agricultural land, and domestic discharge which consequently could have attributed higher nutrient inputs helping phytoplankton to proliferate and bloom. Higher phytoplankton density in the inner stations could be attributed to higher nutrient input in those stations from the surrounding regions Univariate diversity indices have shown variations between the three different seasons (Table 1). Throughout the study, maximum phytoplankton species were recorded in the BC station in the monsoon (45 species). Marglef's species richness (d) was the highest in MON, followed by PRM whereas it was lowest in POM. This could be attributed to the high species diversity in MON compared to the other two seasons. were relatively higher in the PRM and POM compared to the MON season. The relatively low value in MON can be attributed to the high species diversity during this season. In general, the high species dominance in PRM and POM can be related to the low species richness in these seasons. The maximum phytoplankton abundance and chl-a biomass were recorded during the PRM followed by MON season. The highest phytoplankton abundance and biomass was recorded during 2014 and 2015.

Zooplankton density and diversity
A total of 58 different species of zooplankton conforming to nine different phyla, i.e., Sarcomastigophora, Ciliophora, Ctenophora, Cnidaria, Chordata, Chaetognatha, and Arthropoda were recorded. The increased diversity of zooplankton especially the copepods observed in the estuarine region was on par with previous reports from the east coast of India (Madhupratap et al. 1992;Thippeswamy & Malathi 2009). However, the number of copepod taxa     and site-specific variation. Copepods followed by invertebrate larval forms dominated the zooplankton community during all three seasons. A total of 37 species of copepods were recorded during the survey, with the major species being Acartia danae, A. spinicauda, A. clausii, Paracalanus parvus, Acrocalanus gibber, A. longicornis, Corycaeus danae, C. catus, Oithona rigida, and Euterpina acutifrons were recorded throughout the year irrespective of seasons. Copepods followed by larval forms dominate the entire zooplankton community irrespective of seasons ( Figure 6). The least contributing groups (less than 10%) include organisms belonging to phyla/group Sarcomastigophora, Ciliophora, Ctenophora, Cnidaria, Chordata, Chaetognatha, and Annelida. Copepods species such as Eucalanus sp., Subeucalanus sp., Onacaea sp., Centropages sp., and Copilia sp. were present only during POM season in higher numbers in all stations which correlates with the lowering salinity in all stations due to the north-east monsoon. Apart from the copepods, some other larval forms exhibited seasonality such as bivalve (PRM and MON) and gastropod veligers (MON and POM). Larval forms belonging to phylum Mollusca, e.g., Creisis sp. and the Ophiothrix larva were exclusively present only in monsoon. Copepod nauplius, crustacean nauplius, and polychaete larvae were present throughout the year in all the stations. Univariate diversity indices have shown variations between the three seasons (Table 2). Marglef's species richness (d) was the highest in MON, followed by PRM and POM. Among the five stations, a significant difference in the diversity indices was observed during the POM. BC region was more diverse and recorded maximum zooplankton species (19-23). This could be attributed to anthropogenic activities in the surrounding environment (Pandey et al. 2021).
The zooplankton community exhibited significant differences between the seasons (F= 191.1, p <0.001) as well as the stations (F= 224.5, p <0.001). The present investigation has shown the presence of discrete assemblages of zooplankton communities observed in the SRE and coastal region indicating a strong seasonal fluctuation with lower abundances in POM and higher during the PRM and MON season. A similar study conducted elsewhere suggested that phytoplankton abundance plays a very important role in regulating zooplankton population in estuaries (Jagadeesan et al. 2013;Nandy & Mandal 2020).
The coast is prone to heavy rainfall, the likely discharges from the nearby aquaculture activities in the inner stations (BC, SR2, and SR1) of the SRE region which was supported with previous studies (Sreenivasulu et al. 2018). The results of this study are in agreement with Jha et al. (2019) and Pandey et al. (2021) in the same region.

CONCLUSION
The present long-term study reveals the spatial and temporal variations of phytoplankton and zooplankton in the SRE and the adjoining coast. The study also J TT highlights that the SRE region receives very little rainfall during the MON period and most of the rainfall occurred only during the POM period, i.e., during the north-east monsoon (NEM) period. The SRE region is known to have a good cover of mangroves swamps and is usually impacted by anthropogenic activities, such as, aquaculture farms, agriculture activities, and discharge areas from nearby vicinity. The increased nutrient concentration significantly affected the plankton community in the SRE region. Our study indicates that the phytoplankton community exhibited significant variations between seasons. The zooplankton density also showed significant variation and revealed the anthropogenic impact in the study. The present study suggests that phytoplankton and zooplankton are important indicators of a healthy ecosystem which was evident in the present study. Moreover, the study also suggests that a long-term monitoring could help in understanding the ecosystem and planning the mitigation management strategy for the tropical coastal environment.

www.threatenedtaxa.org
The Journal of Threatened Taxa (JoTT) is dedicated to building evidence for conservation globally by publishing peer-reviewed articles online every month at a reasonably rapid rate at www.threatenedtaxa.org. All articles published in JoTT are registered under Creative Commons Attribution 4.0 International License unless otherwise mentioned. JoTT allows allows unrestricted use, reproduction, and distribution of articles in any medium by providing adequate credit to the author(s) and the source of publication.