Recent Foraminifera from the coast of Mumbai, India: distribution and ecology

: Foraminifera have been used in biostratigraphy and paleoenvironmental research. They are useful environmental indicators for monitoring the marine environment. Intertidal sediment samples were analysed for their diversity in relation to physicochemical parameters and sediment characteristics along the Mumbai coast of India. Thirty-five species were found, divided into five orders and 18 families. The orders Rotaliida and Miliolida were identified to be dominant. Foraminifera were observed to be inversely related to sand particle size in relation to sediment and physicochemical parameters of water. Canonical correlation analysis explained the relationship between species abundance and water physicochemical parameters.


INTRODUCTION
Mumbai, the state capital of Maharashtra, has a population of about 22 million people. It is also the largest and busiest port on India's west coast. Intertidal zone of Mumbai represents the peak of adaptability by most types of marine life to harsh environmental circumstances such as wave action, desiccation and other associated aspects generated by the tides of the sea (Kameswara & Srinath 2002). Among marine microorganisms, foraminifera are exceptionally varied and widely spread (Cushman et al. 1928). They are distinguished as protists by having an external test and streaming granular ectoplasm. Their tests are composed of calcium carbonate or agglutinated sediments, which are well preserved after death (Vidya & Patil 2014). They are considered good ecological indicators for detection and monitoring of coastal pollution (Pravasini & Patra 2012). According to Fabrizio et al. (2013), Ammonia tepida has a high resistance to environmental stress while Ammonia parkinsoniana is sensitive to pollution. These are the most widely used fossil species for biostratigraphy, sediment correlation and palaeoenvironmental research (Murray 2006) and their usage as bio-indicators in offshore oil drilling operations is well documented (Mariéva et al. 2010). Abninath & Biswas (1954), Devi & Rajashekhar (2009), and Subhadra & Patil (2012) conducted intertidal studies of foraminifera from the Mumbai coast on diversity studies in the intertidal region. Coastal water is vulnerable to contamination since 38% of the world's population lives within 100 kilometres of the coast (Pravasini & Patra 2012). Coastal pollution is caused by point and non-point wastewater sources from cities, which include sewage water, waste from industry and harbours, beach tourism and fishing crafts activities. Pollution has a negative impact on organisations at all levels, from the organism to the community and the environment (Francisco et al. 2011).
The current study was undertaken to document the Foraminifera at several sites along the Mumbai coast. The objective was to determine the relationship between foram abundance and various physicochemical factors, as well as anthropological activities. This information will aid in the creation of a database of foraminifera along Mumbai's coastline and contribute to understanding the effects of natural and anthropogenic events on Foraminifera.

Study Area
Mumbai is located at 19.0760° N & 72.8777° E, with an overall coast length of 149 km. Four coastal locations with distinct ecology were chosen for sampling. These sites range from north to south along the Mumbai shoreline ( Figure 1). Gorai beach (M1) is located in Mumbai's northwestern outskirts. It is regarded as one of Mumbai's cleanest beaches. Juhu beach (M2) has a five-kilometre coastline. Dadar beach (M3) is situated on the south-west side of Mahim Island. Girgaon beach (M4) is located on Mumbai Island's south-west coast. M2, M3, and M4 are well-known tourist attractions. Mumbai's water quality is deteriorating as a result of pollutants from wastewater treatment facilities, sewage discharges, and discharges from point and non-point sources in the creek and along the shore (Ritesh et al. 2015).
Using a scientific spatula, the upper one cm layer of sand sediment was collected in duplicates between the intertidal zone during low tide. Forams were stained using Rose Bengal solution and stored in 70% isopropyl alcohol (Walton et al. 1952). The materials were washed through a 63 µm sieve and oven-dried at 60°C for analysis. A stereo microscope was used to examine one gram of sand from each station. The total number of specimens (live + dead) was used to calculate abundance. Foram tests were hand-picked and put on micro-paleontological slides using a foram sorting brush. 'JEOL JSM -5800VS' scanning electron microscope (SEM) was used to image selected specimens. The Loeblich & Tappan (1988) classification system and the e-site "World Foraminifera Database" (Hayward et al. 2022) were used for taxonomic analysis.
Temperature, pH, salinity, dissolved oxygen (DO), phosphates and nitrates were chosen as water physicochemical parameters. A digital thermometer was used to record the temperature of the water at sample sites. pH, salinity and DO were measured with a "Thermo Scientific Eutech PCD-650 multi-parameter metre." Nutrients nitrate and phosphate were estimated using standard methods given in the APHA manual (Lenore et al. 1999). Another batch of sand sediment was collected for measurement of organic carbon by titration with ammonium ferrous sulphate using the Walkley-Black technique with suitable modification (Syed et al. 2011).
To determine the texture of sand sediment, samples were sieved through multiple mesh sizes. The soil textural triangle approach (Derek et al. 2015) was used to determine their type. Past 3 v4.03 software was used to calculate diversity indices including the Shannon index, Simpson index, Evenness, Margalef index, canonical correlation, and Q-mode cluster.

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to 0.67 (M4). The Margalef index of species richness ranged from 2.09 (M4) to 5.04 (M1), and is directly related to taxonomic numbers 12 (M4) and 32 (M1). Table 3 presents the diversity indices. The water parameters including pH, temperature, salinity, dissolved oxygen, phosphate, and nitrate were considered for study of various seasons including, premonsoon, monsoon, post-monsoon, and winter, which are represented in Table 4.
The pH ranged from 6.54 at M2 during post-monsoon to 7.89 at M4 during monsoon. Water temperatures in the intertidal zone ranged from 25°C reflecting monsoon at M4 to 29°C representing pre-monsoon at M1. Salinity at all sites varied with the seasons, ranging from 17 during the monsoon at M1 to 41 during the premonsoon at M2.
Dissolved oxygen, phosphate and nitrate showed variations in its concentrations. DO levels were highest during the pre-monsoon (7.4 mg/l) and lowest during the winter (3.1 mg/l) at M1. Similarly, in monsoon, M4 station had the lowest phosphate and nitrate levels, viz., 0.14 mg/l and 0.1 mg/l and M3 in winter revealed the greatest phosphate and nitrate ranges 0.56mg/l to 1.5mg/l, respectively.
The sediment type study revealed that silt type occurred at the M1 and M2, loamy sand at the M3 and sandy loam at the M4. The organic carbon percentage of sediment varied between stations, ranging from 0.28% to 0.37% (Table 4).

Pearson Correlation & Canonical Correlation Analysis (CCA)
For the water parameters and diversity indices, a Pearson correlation matrix was calculated ( Table 5). The pH and dissolved oxygen correlated positively with species evenness but negatively with the other indices. Temperature correlated positively with the number of taxa, the H index and the Margalef index. Salinity only correlated positively with species dominance. Phosphate and nitrate had a significant negative correlation with species evenness.
CCA defined a relationship between species, stations and environmental parameters ( Figure 2). For this analysis, species having a total population more than 1% was chosen, which included population of 18 species. Phosphate and dissolved oxygen defined axis one, whereas nitrate, pH, salinity, and temperature defined axis two. According to CCA analysis nitrate, pH and salinity correlated positively, but temperature correlated negatively with all other physicochemical parameters. All of the water parameters were found to have a significant correlation with 12 species.
Ammonia beccarii, E. repandus, A. dentata, and S. raphana were abundant at three sample stations displayed in the top-right quadrant of the graph. A. beccarii and A. dentata are mainly found in waters with high nitrate levels. N. scaphum was well associated with ambient temperature and phosphate concentration. B. striatula, C. lobatulus and Q. tropicalis held the average positions for all parameters. E. hispidulum and T. tricarinata were significantly correlating with DO, pH, and salinity.

Species-ecological Relationship
This research attempted to investigate the relation of foraminifera to intertidal benthic ecology at different stations. Data from physicochemical parameters were correlated with dominant species using specific indices.
At M1 TFN ranged from 533 to 450 individuals per gram, it was represented by 34 species. N. scaphum (28.33%), A. dentata (12.3%), E. hispidulum (8%) and A. beccarii (7.64%) were dominant species representing the area. According to Kumar & Manivannan (2001) N. scaphum has shown positive correlation to an increase in temperature and DO, our data support this statement. During the winter, the Simpson's index 0.14 is correlating with nitrate value. There is cumulative impact of nitrate and temperature with bleaching response on foraminifera (Martina et al. 2017), allowing only tolerant species to thrive. Thirty-one species have been identified at M2, with a maximum foraminifera test count of 590 in pre-monsoon. Here major taxa were again N. scaphum (21%), A. dentata (10.82%), and A. beccarii (10.59%). Phosphate has long been recognized as a calcite formation inhibitor, adsorbing onto the calcite surface and inhibiting active crystal growth sites (Aldridge et al. 2011), which might account for lower test numbers than M1. After A. beccarii, the dominant species was B. striatula (8.12%). Lagena, Fissurina, Bolivina, Bulimina, and Uvigerina species are found in finer sediments and exist in the shelf to slope area, according to Rajiv et al. (1986); however their prevalence in the study area J TT may be due to wave action. M3 receives water runoff from the Mithi River and had low salinity during the monsoon due to monsoon water, in addition to large amount of sewage and industrial garbage from the Mithi (Jayasiri et al. 2014). At the M3, 33 distinct taxa were present. A. beccarii (24.18%), A. dentata (15.2%), and E. hispidulum (12.21%) dominated the station. M4 had taxa count 20 with a maximum of 198 individuals. The dominant species representing the area were A. beccarii (32.67%), T. tricarinata (15.02%), and E. hispidulum (11.55%).
The distribution of benthic Foraminifera is influenced by organic carbon (OC) and sediment type (Elakkiya & Manivannan 2013). Benthic foram have been shown to be closely associated with variations in percent gravel, organic carbon flux, temperature and salinity (Alexandra

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defined by coarser sediments. As M4 had sandy loam type of sediment suggesting good wave action due to its association with open sea. The moderate value of OC at this station is associated with sediment type, since in coarse-grained sand, interstitial water may travel easily through pore spaces, resulting in less organic particle settling (Hiroshi 1994).
A. beccarii and A. dentata correlated negatively with DO values from all stations, making them adaptable to anoxic conditions (Fatin et al. 2012;Sundara et al. 2016). B. striatula which thrived well in low oxygen stations (Abhijit & Nigam 2014) and was positively associated to salinity since it is an opportunistic species that can thrive in both high and low salinity conditions (Patricia et al. 2019). The dominance of Ammonia sp. and Elphidium sp. in study area indicated that they are resistant to decreased salinity, pH or a combination of the two factors (Laurie et al. 2018).
N. scaphum adapted to environments characterized by high organic matter (OM) quality and it indicates affinity for OM-rich sediments (Pierre et al. 2016), so its distribution is well associated with M1 and M2 as compared to M4 which had more coarse type of sediment. A. dentata and E. hispidulum was abundant at M1, M2 and M3 as silt sand is preferred by the species over coarse sandy sediment (Elakkiya & Manivannan 2013), with affinity for larger amount of organic carbon values (Maria et al. 2012). However, based on our understanding of above work on foraminifera, we may conclude that the cosmopolitan species A. beccarii, A. dentata, B. striatula, N. scaphum, and E. hispidulum thrive well in Mumbai waters.

Hierarchical Cluster Analysis
Foraminifera species were tested to a Bray-Curtis cluster analysis in relationship to stations (Figure 3). It divided stations into three groups: Cluster A (M1 + M2), Cluster B (Cluster A + M3), and Cluster C (Cluster B + M4).
Cluster B comprised of three stations (Cluster A + M3) with 31 species in common. In this cluster M3 is having more similarity with M2 than M1. The cluster had silt and loamy sand sediment which showed a little correlation with one another. The main species represented by the cluster were N. scaphum (8.2-28.3%), A. beccarii (7.6-24.1%), A. dentata (10.8-15.2%), E. hispidulum

Test Deformity
Environmental stress induced by large fluctuations in environmental factors such as salinity, DO, temperature, pH, sedimentation, pollution and hydrodynamics has been connected to a significant percentage of abnormal tests in foraminiferal assemblages (Rehab et al. 2011). Mumbai is India's economic hub, and increased urbanization and industrialization have resulted in an increase in marine discharges to coastal areas (Jayasiri et al. 2014). According to Maharashtra Pollution Control Board (MPCB) data on Maharashtra's water quality condition, water at stations Juhu (M2), Dadar (M3), and Girgaon (M4) had a bad water quality index (MPCB 2013(MPCB -14, 2016. In the present study Quinqueloculina sp. Quinqueloculina sp. (M3) showed reduced chambers, Triloculina sp. (M3) had twisted chambers, Siphogenerina raphana (M2, M3) represented by enlarged chambers and uneven costae lines, and the undetermined taxa had unusually extended chambers. These abnormalities imply that environmental conditions and industrialization have had a negative impact on foraminiferal diversity. All of these abnormalities were associated predominantly with M3 station. According to studies conducted by Shamrao & Kadam (2003), Jayasiri et al. (2014), and Ritesh et al. (2015), Dadar beach is extremely contaminated owing to effluents carried in by the Mithi River, with low-energy hydrodynamics generated by the lagoon region. According to MPCB publications (MPCB 2013(MPCB -14, 2016, the water quality index for M3 is also rated as bad to very-bad. According to Suresh & Sonia (2012) morphological abnormalities are induced by pollution, strongly in shallow waters than deep seas. According to Jayaraju et al. (2008), heavy metal contamination has a greater negative impact on

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foraminiferal test morphology than agricultural and aquacultural wastes. From these damaged shells it may be concluded that they act as a sensitive taxon to environmental and anthropogenic conditions.

CONCLUSION
The present study revealed diversity and distribution of Foraminifera along Mumbai coast with presence of 35 species belonging to four orders, 18 families, and 21 genera. The orders Rotaliida and Miliolida dominated the taxa. A. beccarii, N. scaphum, A. dentata, and E. hispidulum were the most opportunistic species present at all stations. Due to similarities in sediment and species distribution, CCA and Bray-Curtis similarity analysis revealed that M1-M2 and M3-M4 were more associated with each other. N. scaphum served as sensitive taxa by showing affinity for oxygen and finer sediment type. A. beccarii and E. hispidulum acted

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as stress tolerant taxa flourishing well in fine as well as coarse sediment type. The presence of B. striatula indicated the hypoxic condition of water and sediment during winter season. The study found that finer to medium grain sand was associated with more species than coarse sand. Organic carbon concentrations correlated directly with fine sediment type and stations with low-energy hydrodynamic circumstances (M1, M3), allowing more organic carbon to trap between sand particles. The presence of deformed tests suggested that Mumbai's coastal water had physicochemical parameter fluctuations and received contaminated water from industrial areas. It symbolized the potential use of foraminifera in understanding the effects of urbanization and industrialization on coastal water. This creates a great need to construct foraminifera study models to comprehend long-term consequences of changing environmental and anthropogenic activities along urban coasts, since we cannot halt industrialization, but such research will assist to limit the impact of pollution on the marine environment.

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