Sources of organic matter in Chilika lagoon, India inferred from stable C and N isotopic compositions of particulates and sediments

Journal of Marine Systems 194 (2019) 81–90

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Sources of organic matter in Chilika lagoon, India inferred from stable C and N isotopic compositions of particulates and sediments

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Mohd Amira, Debajyoti Paula, , Rabindro Nath Samalb a b

Department of Earth Sciences, Indian Institute of Technology Kanpur, Kanpur 208016, India Wetland Research and Training Centre, Chilika Development Authority, Odisha 752030, India

A R T I C LE I N FO

A B S T R A C T

Keywords: Chilika lagoon Particulate organic matter Sediment organic matter Stable carbon and nitrogen isotopes Anthropogenic input Phytoplankton

Stable isotopic compositions (δ13C and δ15N) and C/N ratios of suspended particulate organic matter (POM) and surface sediment organic matter (SOM) in the Asia's largest lagoon (Chilika, India) were analyzed to identify spatial and seasonal variabilities in sources of organic matter. The variability of POM composition (δ13C: −23.5‰ to −27.9‰, δ15N: 2.1‰ to 7.5‰, C/N: 9.5 ± 0.9) collected during monsoon, a period of highest river discharge, suggests dominant input of terrestrial organic matter, whereas wintertime POM (δ13C: −22.3‰ to −27.7‰, δ15N: −0.2‰ to 4.8‰, C/N: 9.1 ± 1.0) exhibits a mixed source of agricultural runoff, and lagoon phytoplankton and cyanobacteria. The composition of POM collected during summer/dry season (δ13C: −21.2‰ to −26.2‰, δ15N: 2.0‰ to 6.0‰, C/N: 8.9 ± 1.1) indicates enhanced lagoon phytoplankton and bacterial productivity. Spatial variability of POM isotopic composition clearly shows more contribution of terrestrial sources in the northern sector- influenced by perennial Mahanadi River distributaries- compared to the central and southern sectors. The isotopic compositions (δ13C: −20.9‰ to −22.9‰, δ15N: 1.9‰ to 6.6‰) and C/N ratios (10.1 ± 1.3) of SOM indicate major contribution from terrestrial and macrophyte sources and minor contribution from phytoplankton and/or cyanobacteria. The northern sector is also heavily influenced by urban/ industrial wastewater input, whereas the outer channel with higher salinity remains dominated by marine organic matter. Western part of the central sector is significantly influenced by untreated domestic sewage discharged from nearby townships and villages, which endangers the lagoon ecosystem.

1. Introduction Coastal lagoons, situated at the interface between land and sea, represent transitional environments and are generally shallow water bodies having limited exchange with sea (e.g., Berto et al., 2013; Remeikaitė-Nikienė et al., 2016, 2017). These lagoons act as both source and sink for organic matter (OM) and are among the most productive ecosystems (Nixon, 1988). A complex mixture of organic compounds derived from various sources are found in coastal lagoons; land-based and marine-derived OM represent allochthonous sources, whereas local production of phytoplankton, macroalgae, and benthic macrophyte represent autochthonous sources (Berto et al., 2013; Lesutienė et al., 2014; Remeikaitė-Nikienė et al., 2017). Seasonal variability in regional/local hydrological conditions modulated by local climate strongly controls the input of OM into the coastal lagoons (Vizzini and Mazzola, 2003; Carlier et al., 2007; Guerra et al., 2013). However, compared to estuarine and coastal marine environments, the coastal lagoons represent a complex environment that supports high

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biological productivity and rich biodiversity (Vizzini and Mazzola, 2003; Berto et al., 2013). In the last few decades, nutrient-rich anthropogenic inputs into the coastal ecosystems have resulted in eutrophication (e.g., Smith, 2003 and references therein). The major sources of nutrients include untreated domestic sewage, municipal, industrial and agricultural wastes, and fertilizers and aquaculture activities (Nixon, 1995; Costanzo et al., 2003; Vizzini and Mazzola, 2006; Sahu et al., 2014). The constantly increasing urban pollution has become a major threat to the environmental quality of the coastal ecosystems (Gao et al., 2012) that in turn severely affects primary biological productivity (Smith, 2003) leading to loss of fisheries (Nixon, 1995) as well as loss of biodiversity (Sahu et al., 2014). Carbon and nitrogen elemental (C/N) and isotopic (δ13C, δ15N) ratios are extensively used as robust tools to trace the source of OM and evaluate the effect of anthropogenic disturbance in coastal aquatic environments (Ramaswamy et al., 2008; Barros et al., 2010; Berto et al., 2013; Mazumder et al., 2015; Remeikaitė-Nikienė et al., 2016, 2017;

Corresponding author. E-mail address: [email protected] (D. Paul).

https://doi.org/10.1016/j.jmarsys.2019.03.001 Received 15 October 2018; Received in revised form 1 March 2019; Accepted 3 March 2019 Available online 05 March 2019 0924-7963/ © 2019 Elsevier B.V. All rights reserved.

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chemical parameters, Chilika is divided into four sectors (Gupta et al., 2008; Muduli et al., 2013): (i) northern sector, (ii) central sector, (iii) southern sector, and (iv) outer channel. Whereas the northern sector (salinity: 5.5 ± 1.3) receives a huge amount of freshwater discharge from the Mahanadi distributaries, the outer channel sector (salinity: 20.7 ± 1.8) marks the influx of sea water from the Bay of Bengal through the inlet channels (Fig. 1; see also Srichandan et al., 2015). The central (salinity: 12.5 ± 1.2) and southern (salinity: 13.1 ± 0.4) sectors are dominantly brackish because of mixing of freshwater from the northern sector and marine water from the outer channel. Sea water intrusion through the Palur Canal in the south (Fig. 1) leads to increasing salinity in the southern sector compared to the central sector. Chilika was declared as the first Indian Ramsar site (in 1981) signifying a wetland of international importance, due to its rich biodiversity. Local climate currently is tropical monsoonal with an average annual rainfall of ~1238 mm (Sahu et al., 2014). About 75% rainfall comes from the southwest summer monsoon (June–September) and the remainder comes from the northeast winter monsoon during November–December (Gupta et al., 2008). Due to mixing of fresh and marine water, a salinity gradient has developed from south to north supporting biodiversity (Ghosh et al., 2006). The lagoon is well-known for its fishes, the rare and endangered Irrawaddy dolphins, and intercontinental migratory birds during winter as Chilika lagoon lies along the Central Asian Flyway, which extends from the Arctic breeding grounds in the northern Russia to the wintering grounds in south Asia. The lagoon provides livelihoods to a large number of local population (> 200000) through fisheries thereby also contributing to the socioeconomic fabric of the locality (Ghosh et al., 2006). The distributaries of the Mahanadi River bring in freshwater into the lagoon that not only reduces the salinity of the lagoon, but also brings huge amount of silt and nutrients. This nutrient enrichment leads to eutrophication in the northern most part of the lagoon and results in growth of freshwater weeds mainly Hydrilla and Chara. Other important macrophyte vegetations include Phragmites karka, Potamogeton, Gracilaria, Ruppia, Najas etc. of which Potamogeton sp. is the most dominant one that is also found in the central sector (Ghosh et al., 2006; Sahu et al., 2014). The eastern side of the saline southern sector is characterized with dominant presence of seagrass, mainly Halophila sp. (Ghosh et al., 2006). In addition to a large amount of domestic waste from surrounding townships/villages, about 550 million L/day untreated domestic wastewater from the nearby city Bhubaneswar (capital of Odisha) flows into the lagoon (Ghosh et al., 2006).

Liénart et al., 2017; Zhou et al., 2018). In general, isotopic composition of terrestrial OM (average δ13C and δ15N: −27‰ and 2‰, respectively) is distinct from the marine OM that has an average δ13C and δ15N of −20.5‰ and 6‰, respectively (Gearing, 1988; Lamb et al., 2006; Gao et al., 2012). Note that δ15N can also be an excellent indicator of anthropogenic pollution because agricultural fertilizers (0.2‰), untreated sewage (1.2‰), and municipal wastewater (10–20‰) sources have distinct δ15N values (McClelland et al., 1997; Costanzo et al., 2003; Barros et al., 2010; Mazumder et al., 2015). Like most of the coastal systems elsewhere, Chilika lagoon in Indiathe largest brackish water lagoon in Asia- has also been increasingly impacted by anthropogenic activities that include mainly land reclamation for agriculture and human settlement, pollution from domestic, agriculture, aquaculture and industrial wastes, and increasing siltation due to deforestation and improper land use practices in the catchment area (Ghosh et al., 2006; Panigrahi et al., 2007, 2009; Sahu et al., 2014). Inflow of huge amount of anthropogenic nutrients into the lagoon has led to widespread eutrophication and weed infestation (Sahu et al., 2014; Ganguly et al., 2015). Additionally, increasing heavy metal pollution mainly originating from urban sources and transported by the Mahanadi River (Zachmann et al., 2009) into Chilika, non-degradable plastic litters from domestic and industrial wastes (Sahu et al., 2013), and petroleum hydrocarbons from boating activities used both for fishing and tourism (Mohanty et al., 2017) have endangered the lagoon biota. Existing studies on Chilika lagoon have focused on the water quality (Panigrahi et al., 2007, 2009; Barik et al., 2017), metal contamination (Zachmann et al., 2009; Panda et al., 2010), phytoplankton and zooplankton diversity (Naik et al., 2008; Srichandan et al., 2015 and references therein), nutrient dynamics (Ganguly et al., 2015), influence of suspended particulate matter on nutrient biogeochemistry (Patra et al., 2016), spatial and temporal variations of dissolved inorganic and organic carbon (Gupta et al., 2008; Muduli et al., 2013), and nitrogen uptake rates in the lagoon (Mukherjee et al., 2018). However, none of these studies has attempted to provide a detailed account of the spatiotemporal variability of the lagoon OM in regard to seasonal climate variability, except for a study by Patra et al. (2017) who reported δ13C, δ15N, and C/N ratios of particulate organic matter (POM) of a post monsoon season. The present study proposes to investigate the spatial and seasonal variability of OM sources of suspended particles and surface sediments in Chilika lagoon using δ13C, δ15N, and C/N ratios. The results document large spatial and seasonal variability in the dominant source of organics, which are mainly controlled by terrestrial inputs and biological primary productivity in the lagoon. This study also reveals significant anthropogenic inputs (urban wastewater, domestic sewage, agricultural runoff) to the lagoon.

2.2. Sample collection Samples were collected from 30 sampling stations (Fig. 1) maintained by the Chilika Development Authority, for which water quality data of several years are available. Suspended particulate matter (SPM) was collected in three different seasons: monsoon (September 2016), winter (January 2017), and summer (May 2017). About 1 L of water sample from 0.3 m depth from all the stations was collected in precleaned plastic bottles and immediately brought to the on-site laboratory of Wetland Research and Training Centre, Chilika Development Authority, where water was passed through a 250 μm sieve to limit the contribution of large zooplankton and detrital material to the water sample. Then about 0.5 L of water was filtered through a pre-combusted (450 °C for 4 h to remove trace OM) Whatman GF/F glass fiber filter (0.7 μm pore size, 47 mm diameter, and 0.42 mm thickness) under moderate vacuum to collect SPM. The filter papers containing SPM were then oven dried at 40 °C for 24 h, wrapped in pre-combusted (450 °C for 4 h) aluminium foil, and subsequently stored in a desiccator till further isotopic analysis. Lagoon sediments were collected during monsoon sampling in 2016. Sediment cores were obtained using a gravity corer and the top 0–3 cm representing the surface sediments was stored in polybags with the help of a plastic spoon. Based on average sedimentation rate of ~5–6 mm/year reported by Zachmann

2. Materials and methods 2.1. Study area Chilika lagoon (19°28′–19°54′ N and 85°05′–85°38′ E), situated along the east coast of India and in the state of Odisha, is the second largest lagoon in World (Fig. 1). The pear-shaped Chilika lagoon, covering an area of about 1165 km2, is on average about 64 km long, 5–18 km wide, and 2 m deep (Sahu et al., 2014). This shallow brackish water lagoon is influenced by two major hydrologic subsystems: (1) the freshwater system, which includes the perennial distributaries of the Mahanadi River namely Daya, Bhargavi, Makara, Malaguni, and Luna, as well as the ephemeral monsoon-fed rivers/rivulets including Kansari, Kusumi, Tarimi, Kalajhara, Salia etc. draining a catchment of ~4146 km2, and (2) the saline water system, which includes inflows from the Bay of Bengal sea through the Palur Canal in south and through the inlet within the 32 km long narrow outer channel region (Muduli et al., 2013). Therefore, Chilika lagoon represents a mixture of marine, brackish and freshwater ecosystems. Based on the physico82

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Fig. 1. Map of Chilika lagoon showing sampling locations and rivers/rivulets draining into the lagoon. Also shown are active inlet (new mouth) and Palur Canal; the two ways of saline water inputs into the lagoon. The four sectors: northern (salinity: 5.5 ± 1.3), central (12.5 ± 1.2), southern (13.1 ± 0.4), and outer channel (20.7 ± 1.8) are also marked with different colours. NB indicates Nalaban Island, a bird sanctuary.

Pee Dee Belemnite (VPDB) and atmospheric N2 (AIR) isotope reference scales, respectively (Paul et al., 2007). Additionally, repeated analyses of oxalic acid (IAEA-C8; δ13C: −18.31‰) for carbon and ammonium sulphate (IAEA-N-2; δ15N: 20.3‰) for nitrogen, performed along with the unknowns, gave an analytical precision of ± 0.12‰ (1σ, n = 11) for δ13C and ± 0.1‰ (n = 10) for δ15N. Several unknown samples (n = 20 for δ13C and n = 15 for δ15N) were analyzed twice and the values were within 0.2‰ for both the δ13C and δ15N measurements. The TOC and TN contents were calculated using the linear relationship between the peak areas of CO2 and N2 versus the C and N content of a standard (B2188 from Elemental Micro-Analysis, UK; C: 5.39% and N: 0.35%) analyzed for four different weight fractions (Jensen, 1991). Values of repeated measurements of B2188 and few unknown samples were within 0.01% for both C and N. The C/N atomic ratios of the samples were determined by multiplying TOC/TN weight ratios by 1.166185.

et al. (2009), the top 3 cm represents average of 5–6 years. The surface sediment samples were dried in an oven at 40 °C for 2–3 days and about 50 g of the dried sediment was ground to a fine powder using a vibrating agate cup mill (PULVERISETTE 9). Rivers/rivulets discharging freshwater into the lagoon were also sampled for SPM during the monsoon to identify the composition of the riverine sources. Live plant samples from the lagoon were also collected from the sampling stations (see Table S1). All plant samples were washed with 0.6 N HCl, ultrasonicated, rinsed with Milli Q (ultra-pure) water, oven dried at 40 °C for 3 days, and ground using a coffee grinder to prepare fine powders for isotopic analysis.

2.3. Elemental and stable isotope analyses The total organic carbon (TOC) and total nitrogen (TN) contents, and the δ13C and δ15N compositions of OM in SPM and surface sediments as well as in individual plant samples collected from Chilika lagoon were measured using the continuous-flow stable isotope ratio mass spectrometer (CF-IRMS) at the Indian Institute of Technology Kanpur. Prior to isotopic analyses of suspended particulate organic matter (POM), filters containing SPM were acidified by rinsing with 0.6 N HCl to remove inorganic carbonate, washed with Milli Q water and then dried at 40 °C for 24 h. Similarly, the powdered sediment samples were decarbonated using 0.6 N HCl at 70–80 °C prior to analyses of sedimentary organic matter (SOM). Subsequently, the dried decarbonated samples were crushed to fine powder. About 2–5 mg of carbonate-free samples for δ13C and about 15 to 30 mg for δ15N analyses were weighed into tin capsules and combusted at 1020 °C in an Elemental Analyzer (Flash EA 2000) that was coupled with an IRMS (Delta V Plus, Thermo-Scientific). A set of carbon isotope reference standards (LSVEC, NBS-19 and CH-3) and nitrogen isotope reference standards (IAEA-N-2, IAEA-NO-3 and USGS-35) from the International Atomic Energy Agency (IAEA) were analyzed along with each set of unknown samples, to convert the raw δ13C and δ15N in to the Vienna

2.4. Spatial and statistical analyses For better representation and visualization of δ13C and δ15N variabilities of POM and SOM in Chilika, spatial distribution maps were prepared using isotope data from the 30 sampling stations. These maps were prepared in the ArcGIS 10.4.1 environment (WGS84) using the Inverse Distance Weighting (IDW) interpolation method (Yao et al., 2013). The IDW interpolation method estimates cell values by averaging the values of sample data points in the neighbourhood of each processing cell. The analysis of variance (ANOVA) test was performed to compare the spatio-seasonal variability of isotopic compositions using SigmaPlot 12.0 software.

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submerged plants (macrophytes) varies from −13.0‰ to −18.8‰ with an average of −15.3‰ (see Fig. 2). The δ15N values in submerged macrophytes vary from 1.7‰ to 9.4‰ with an average of 5.4‰. The C/ N ratio of plant samples varies from 17.5 to 30.5 with an average of 23.9 (Table S1). A freshwater plant Eichornia, found to thrive in the local rivers, is typically brought into the lagoon during monsoon and found floating in the lagoon during our sampling. The δ13C of Eichornia (−27.1‰) and Phragmites karka (emerged weed; −27.9‰) is similar to that of the terrestrial OM (average: −27.0‰, Table S1). However, δ15N values of Eichornia and Phragmites karka are 17.4‰ and 7.1‰, respectively. The substantially higher δ15N of Eichornia (compared with the terrestrial OM average of 6.1‰, Table S1) clearly highlights a growth in a 15N-enriched environment. The δ13C and δ15N in POM collected from rivers and rivulets (i.e., terrestrial OM) draining into the lagoon vary from −25.7‰ to −28.9‰ (average: −27.0‰) and 3.8‰ to 8.9‰ (average: 6.1‰), respectively (Table S1). The C/N ratio of terrestrial OM samples varies between 10.0 and 12.8 with an average of 11.0. Fig. 2. Binary plot of δ13C (VPDB) versus δ15N (AIR) of suspended particulate and surface sediment organic matters. Isotopic values of plant samples collected from the lagoon during sampling and rivers averages are also plotted. Marine (Ramaswamy et al., 2008; Gearing, 1988), fertilizer (Vitòria et al., 2004), and untreated sewage (Barros et al., 2010) average values are plotted for comparison. Submerged plants (macrophytes) show 13C-enriched values compared to emergent plants.

3.2. δ13C, δ15N, and C/N ratios of POM and SOM The δ13CPOM and δ15NPOM values in the lagoon exhibit large seasonal variabilities (Fig. 2; Table S2). The δ13CPOM in monsoon, winter, and summer samples ranges from −23.5‰ to −27.9‰ (average: −25.7‰), −22.3‰ to −27.7‰ (average: −25.1‰), and −21.2‰ to −26.2‰ (average: −23.0‰), respectively. The δ15NPOM varies from 2.1‰ to 7.5‰ (average: 4.9‰), −0.2‰ to 4.8‰ (average: 2.1‰), and 2.0‰ to 6.0‰ (average: 3.9‰) during monsoon, winter and summer, respectively. Interestingly, the δ15N values of our summer POM are similar to that reported for the POM collected in summer 2015 (3.99 ± 1.68‰; n = 16) by Mukherjee et al. (2018). The C/N ratio during monsoon fluctuates between 7.4 and 11.3 (average: 9.5), and

3. Results 3.1. δ13C, δ15N and C/N ratios of plants and river POM The δ13C, δ15N, and C/N ratios of plant samples collected from Chilika lagoon and Bhargavi River are given in Table S1. The δ13C of

Fig. 3. Spatial and seasonal variations in δ13C (VPDB, ‰) of suspended particulate and surface sediment organic matter collected during monsoon, winter and summer seasons. 84

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Fig. 4. Spatial and seasonal variations in δ15N (AIR, ‰) of suspended particulate and surface sediment organic matter collected during monsoon, winter and summer seasons.

Nikienė et al., 2017 and references therein). The δ13C of seagrasses and lagoonal/estuarine macroalgae varies from −9‰ to −12‰ and −11.0‰ to −21.6‰, respectively (Hemminga and Mateo, 1996; Carlier et al., 2009; Cresson et al., 2012), while δ15N ranges from 4‰ to 9‰ and −0.1‰ to 11.6‰, respectively (Carlier et al., 2007, 2009). However, seagrasses and macroalgae have higher C/N ratios (Carlier et al., 2007). The δ13C and δ15N of lagoonal/estuarine phytoplanktons range from −18‰ to −30‰ and −2.2‰ to 8.6‰, respectively (Vizzini and Mazzola, 2003; Carlier et al., 2007, 2009; Guerra et al., 2013). The δ13C of aquatic plants is mainly controlled by the isotopic composition of dissolved inorganic carbon (DIC), whether derived from dissolved atmospheric CO2 (δ13Catm ~−8‰) or bicarbonate (δ13CHCO3− ~0‰). Whereas freshwater phytoplanktons prefer to utilize dissolved atmospheric CO2 (δ13C ~−8‰), marine phytoplanktons mostly uptake HCO3−, which is the dominant ion in the marine environment (Lamb et al., 2006; Guerra et al., 2013). Consequently, δ13C values of phytoplanktons vary from a 13C-depleted signature in freshwater to a 13C-enriched value in marine ecosystems. Similar to δ13C, the δ15N of macrophytes and phytoplanktons depends on the sources of dissolved inorganic nitrogen (DIN). Chilika is a river dominated lagoon and therefore its OM is significantly influenced by riverine/terrestrial inputs (Nazneen and Raju, 2017) mainly controlled by the local hydrology and seasonal climate. Indeed, during monsoonal precipitation, huge amount of freshwater laden with terrestrial OM and nutrients is discharged into the lagoon through numerous rivers (Fig. 1; see Sahu et al., 2014; Robin et al., 2016). However during summer/dry periods, freshwater discharge into the lagoon is largely reduced and limited via perennial distributaries of the Mahanadi River. Large amount of nutrient influx has resulted in an extensive growth of macrophytes especially in the northern and central sectors of the lagoon (Ghosh et al., 2006; Sahu et al., 2014). The average δ13CPOM of −27.0 ± 1.2‰ collected from the rivers draining

during winter varies from 7.3 to 11.7 (average: 9.1; Table S2). The summer samples are characterized with a C/N ratio ranging between 7.3 and 10.7 (average: 8.9). The δ13CSOM values (−20.9‰ to −22.9‰, average: −21.8‰) in the lagoon surface sediments are comparatively more positive than the POM and show less variability in isotopic signature throughout the lagoon (Figs. 2 and 3d; Table S2). Whereas the δ15NSOM varies from 1.9‰ to 6.6‰ (average: 4.3‰) and exhibits the most positive values close to the mouth connecting the lagoon with the Bay of Bengal (Fig. 4d). The C/N ratio in surface SOM ranges from 7.8 to 12.0 with an average of 10.1 (Table S2). 4. Discussion 4.1. Sources of OM in Chilika Coastal lagoons receive their OM from both allochthonous and autochthonous sources. Allochthonous sources include terrestrial (including anthropogenic) OM mainly delivered by rivers during monsoon and marine input through tidal influx. Autochthonous sources of OM are mainly phytoplanktons and macrophytes that grow in the lagoon. Terrestrial OM primarily comes from C3 and C4 plants that have distinct carbon fixation pathways and therefore are characterized with distinct δ13C values; C3: −22‰ to −33‰ with an average of −27‰, and C4: −9‰ to −16‰ with an average of −13‰ (Pancost and Boot, 2004). In general, terrestrial OM has lower δ13C (−25‰ to −33‰, average ~−27‰) and δ15N (−10‰ to 10‰, average ~3‰), and higher C/N ratios (> 12) compared to the marine OM derived mainly from marine phytoplanktons that have higher δ13C (−18‰ to −22‰, average −20.5‰) and δ15N (4‰ to 10‰, average 6‰), and lower C/N ratios (5–7) (Gearing, 1988; Lamb et al., 2006; Ramaswamy et al., 2008; Gao et al., 2012; Pradhan et al., 2014; Liénart et al., 2017; Remeikaitė85

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S1), (ii) marine (average δ13C: −20.5‰; Ramaswamy et al., 2008), and (iii) estuarine/lagoon phytoplankton (δ13C: −18‰ to −30‰; Vizzini and Mazzola, 2003; Guerra et al., 2013). In general, the δ13CPOM of the northern and southern sectors of Chilika are −24.9 ± 1.5‰ (n = 18) and −25.7 ± 1.7‰ (n = 23), respectively, whereas relatively high δ13CPOM characterizes the central sector (−24.2 ± 1.9‰, n = 35) and outer channel (−23.4 ± 1.0‰, n = 9) (Fig. 3). Note that these values are average of the three seasons. The δ13CPOM in the northern sector indicates more contribution of terrestrial OM, whereas that in the southern sector shows mixed sources of terrestrial and phytoplankton origin. On the other hand, slightly 13C-enriched signatures in the central sector (Fig. 3) indicate additional contribution from phytoplankton and cyanobacteria (Lesutienė et al., 2014; Robin et al., 2016); cyanobacteria is a specific type that performs photosynthesis. Significantly high δ13CPOM (p < 0.05) in the outer channel compared to the northern and southern sectors, clearly shows dominant contribution of marine OM sourced from the Bay of Bengal. The δ15NPOM in Chilika samples varies between −0.2‰ and 7.5‰, which is similar to the variabilities observed in other coastal ecosystems such as the Zuari Estuary, west coast of India (δ15NPOM: 0.7–7.3‰; Bardhan et al., 2015) and the Lapalme lagoon, northwestern Mediterranean, France (δ15NPOM: −1.8‰ to 8.4‰; Carlier et al., 2007). The spatial distribution pattern of δ15NPOM shows high values in the northern sector (4.9 ± 1.4‰) and outer channel (4.4 ± 1.3‰), and lower values in the central (3.1 ± 1.7‰) and southern (3.1 ± 1.8‰) sectors (Fig. 4). Significantly high δ15NPOM (p < 0.001) in the northern sector compared to the central and southern sectors, is attributed to terrestrial OM (ca. 6.1 ± 1.7‰; Table S1) input as well as wastewater discharged (ca. 10–20‰; McClelland et al., 1997) from the capital city Bhubaneswar by Mahanadi distributaries. Whereas, higher δ15NPOM in the outer channel compared to the central and southern sectors, is attributed to marine OM (p < 0.05; ca. 6‰; Gearing, 1988). Lower δ15NPOM of the central and southern sectors suggest decreasing influence of wastewater input from the Mahanadi distributaries. Further, C/ N ratio of POM of the lagoon varying between 7.3 and 11.7 indicates dominance of terrestrial input along with minor contribution from phytoplankton/bacterial productivity.

into Chilika is similar to that of terrestrial OM values found in literature (−27‰; Gao et al., 2012). However, the average δ15NPOM of the rivers (6.1 ± 1.7‰) is higher than that of terrestrial OM (average δ15N of ~3‰) dominated by C3 plants (see Remeikaitė-Nikienė et al., 2017 and references therein). One of the major distributaries of the Mahanadi in the northeast, the Bhargavi River, carries the highest discharge of agricultural, industrial, and urban wastes into the lagoon, and has the highest δ15NPOM of 8.9‰ (Table S1). Similar δ15N values (> 8‰) were also reported for the eutrophied rivers with high nutrient and municipal wastewater loads that enter the Baltic Sea (Lesutienė et al., 2014; Remeikaitė-Nikienė et al., 2017 and references therein). Generally terrestrial waters influenced by anthropogenic activity and municipal wastewater (δ15N of 10‰ to 20‰) are enriched in 15N (McClelland et al., 1997; Gao et al., 2012). The C/N ratio (11.0 ± 1.1) of POM collected from the rivers (Table S1) is lower compared to the C/N ratios of > 12 reported for terrestrial OM (Lamb et al., 2006); terrestrial plants are mainly composed of lignin and cellulose, which are nitrogen poor. This may be due to either high input of terrestrial soil (Kendall et al., 2001), supported by high turbidity observed during our sampling, or due to an increased contribution of anthropogenic nitrogen. Submerged macrophytes of Chilika have average δ13C and δ15N values of −15.3 ± 2.3‰ and 5.4 ± 2.1‰, respectively (Table S1). These values are within the range of that reported for macrophytes in coastal environments globally (−9.0‰ to −21.6‰ for δ13C and −0.1‰ to 11.6‰ for δ15N; Liénart et al., 2017 and references therein). Seagrass collected from the central sector of Chilika exhibits relatively less positive δ13C (−14.8‰) and more positive δ15N (4.7‰) compared to that collected from the southern sector (δ13C: −13.1‰ and δ15N: 1.7‰). The 13C-enrichment towards the southern sector may be explained by comparatively higher salinity (osmotic stress) that reduces the partial pressure of CO2 in the intercellular leaf space, thereby resulting in an increase in δ13C relative to those plants that grow in a less saline environment (Machás et al., 2003 and references therein). On the other hand, 15N-depleted values of seagrass in the southern sector are attributed to comparatively less influence of wastewater input from the Mahanadi distributaries. 4.2. Spatial variability in POM

4.3. Seasonal variability in POM Chilika lagoon shows significant spatial variability in δ13C, δ15N, and C/N ratio of POM. The δ13CPOM (−21.2‰ to −27.9‰, average of −24.7‰) of the lagoon falls within the range of variabilities reported for other transitional ecosystems such as the Zuari Estuary, west coast of India (δ13CPOM: −19.5‰ to −30.1‰; Bardhan et al., 2015), the Pearl River Estuary, China (δ13CPOM: −22.5‰ to −28.3‰; Ye et al., 2017 and references therein). However, compared to Chilika, most of the Mediterranean lagoons are characterized with relatively 13C-enriched POM, for example the Lake Sabaudia (−20.0 ± 2.1‰; average salinity: ~33; Vizzini and Mazzola, 2003) and Pialassa Baiona lagoon (−22.1 ± 1.3‰; average salinity: ~33; Guerra et al., 2013) of western Mediterranean, Italy, and the Lapalme lagoon (−22.1 ± 1.3‰; average salinity: ~28; Carlier et al., 2007) and the Salses-Leucate lagoon (−19.7 ± 0.8‰; average salinity: ~32; Carlier et al., 2009) of northwestern Mediterranean, France. The 13C-enriched signature of these Mediterranean lagoons has been attributed to reduced contribution from terrestrial organic carbon and increased marine input to the total POM pool of lagoons (Guerra et al., 2013). The δ13CPOM in Chilika suggests significant contribution of terrestrial OM brought into the lagoon by freshwater discharge during southwest summer monsoon as well as during northeast winter monsoon. Further, the salinity of Mediterranean lagoons is higher than Chilika lagoon due to larger marine water influx in the Mediterranean lagoons than the freshwater influenced semi-enclosed Chilika lagoon (average salinity: ~13). Spatially, the δ13CPOM exhibits characteristic values for all the four sectors of Chilika (Fig. 3) depending upon dominant contribution from a particular source mainly (i) terrestrial (average δ13C: −27‰; Table

Seasonal variations in POM compositions of shallow coastal lagoons are mainly governed by variations in the freshwater input and windinduced resuspension processes (Berto et al., 2013; Patra et al., 2016; Liénart et al., 2017). Tropical lagoon such as Chilika exhibits large seasonality in its POM compositions due to large variability in freshwater discharge; huge amount of freshwater discharge in monsoon and significantly low in summer. In general, monsoon season is characterized with highest freshwater (carrying terrestrial OM) input into Chilika lagoon (Figs. 3a and 4a). During summer, when freshwater discharge is significantly low and limited to the northern sector only via perennial distributaries of the Mahanadi River, phytoplanktons are the main contributor to POM (Figs. 3c and 4c). The winter season POM comprises contribution from both terrestrial and phytoplanktons (Figs. 3b and 4b). Details of POM seasonality and controlling factors are discussed below. 4.3.1. Monsoon season Previous studies reported that large amount of freshwater discharge into Chilika during southwest summer monsoon increases the average lagoon water level by > 0.5 m (e.g., Robin et al., 2016). During monsoon, fairly uniform distributions of δ13C (−25.7‰ ± 1.1‰), δ15N (4.9 ± 1.2‰), and C/N ratio (9.5 ± 0.9) of POM (p > 0.05) was observed within the lagoon, which as discussed earlier, are strongly influenced by terrestrial input (Figs. 3a and 4a). Typically, huge discharge of SPM during monsoon (average: 99.32 mg/L; Patra et al., 2016) into the lagoon creates high turbidity, which limits availability of 86

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depleted DIC and DIN substrates by phytoplankton. Due to low irradiance and availability of day light for shorter duration during winter, phytoplankton prefers NH4+, which is isotopically depleted (Glibert et al., 2016). Ganguly et al. (2015) reported that NH4+ was a major source of DIN supply to phytoplankton in Chilika followed by urea during winter. Similar variability in winter δ15NPOM has been reported from the Zuari Estuary, west coast of India, and attributed to uptake of isotopically lighter DIN (NH4+) by phytoplankton (Bardhan et al., 2015). Robin et al. (2016) reported significant bacterial productivity in the shallow northern and central sectors. The relatively 13C-enriched (δ13CPOM = −24.4 ± 1.4‰) signature in the shallow central sector can be due to N2-fixation by cyanobacteria, which results in high δ13C and low δ15N of POM (Lesutienė et al., 2014), a prominent feature also observed in our distribution patterns (Figs. 3b and 4b). However, although the northern sector is characterized with highest bacterial activity (Robin et al., 2016), the resultant isotopic effect is not observed in this sector. Generally, isotopic composition of POM in north seems to be influenced by terrestrial inputs. Comparatively higher isotopic values in macrophytes (δ13C: −15.3 ± 2.3‰, δ15N: 5.4 ± 2.1‰; Table S1) than the POM suggest negligible or minor contribution of macrophytes to the POM (p < 0.001 for both C and N). The Nalaban Island (near station–12, central sector) is a bird sanctuary, a feeding and resting place for thousands of migratory birds during winter. Bird guano supplies more nutrients to the lagoon in this area (Panigrahi et al., 2009), and is characterized with relatively high δ13C (−21.2 ± 2.8‰) and δ15N (10.5 ± 2.2‰) (Bird et al., 2008). Spatial distribution patterns show strong effect of guano on lagoon POM near the Nalaban Island (Figs. 3b and 4b) resulting in enriched isotopic compositions. The lowest C/N ratio of 7.3 from station–12 during winter also suggests guano influence (Bird et al., 2008). Furthermore, relatively high δ13CPOM and low δ15NPOM towards the western shoreline of the central sector (Figs. 3b and 4b) may have resulted due to sewage inputs from the surrounding townships and villages, while the outer channel remained dominated by marine influx.

light that in turn lowers primary productivity (Robin et al., 2016). Under limited light condition, phytoplankton mostly uptake NH4+ (depleted in δ15N) resulting in δ15N < 1‰ (Bardhan et al., 2015). The δ15N values much higher than 1‰ in our samples suggest a minimum contribution of lagoon phytoplankton to POM. In the recent times, very high discharge of untreated domestic sewage and fertilizers through agricultural runoffs from nearby townships/villages into Chilika has been reported (Ghosh et al., 2006; Sahu et al., 2014). However, during monsoon, our data suggest negligible contribution of untreated sewage (δ13C: −22‰, δ15N: 1.2‰; Barros et al., 2010) to the POM of lagoon as a result of dilution by monsoon precipitation. Nazneen and Raju (2017), using the organic carbon concentration in sediments, have reported significant amount of untreated sewage discharged from the Balugaon township into the lagoon near station–1 in the central sector. This is reflected in the lowest δ15NPOM value (2.1‰) observed for the sampling station–1 compared to the average δ15NPOM (4.9 ± 1.2‰) of the lagoon (Table S2). Further, agricultural practices in India are dependent on artificial fertilizers, mainly urea, which could significantly affect nearby estuarine ecosystems. Artificial fertilizers are characterized with δ13C of −28.5 ± 5.0‰ and δ15N of 0.2 ± 1.3‰ (Vitòria et al., 2004). The δ13C of artificial fertilizers is similar to those of Chilika POM, but the more positive δ15N values of the lagoon POM suggest negligible or less effect of the fertilizers to the POM pool during monsoon. Low δ13C (−25.7‰ ± 1.1‰), and C/N ratio (9.5 ± 0.9) of POM suggest negligible contribution of macrophytes (δ13C: −15.3 ± 2.3‰, C/N: 24.3 ± 4.3) to the POM pool of the lagoon (p < 0.001). A strong contribution of urban/industrial wastewater discharge (10–20‰; McClelland et al., 1997) is highlighted in the northern sector brought in by Mahanadi distributaries, resulting in the highest δ15NPOM values (5.7 ± 1.5‰) in the north. 4.3.2. Winter season Generally, the lagoon experiences low freshwater discharge during the winter relative to the monsoon season. Interestingly, the δ13C distribution pattern of wintertime POM is slightly 13C-enriched compared to that of the monsoon pattern (Fig. 3b), suggesting decreasing influence of terrestrial inputs. Compared to monsoon, a noticeable 13C-enrichment observed in the central sector (p < 0.05; Fig. 3b) may be attributed to increased contribution from cyanobacterial activity (Lesutienė et al., 2014; Robin et al., 2016), while 13C-enrichment in the outer channel indicates more marine inputs. The δ15NPOM becomes less positive from north to south (Fig. 4b), which is due to decreasing contribution of urban/industrial wastewater (having high δ15N) mainly discharged in the northern sector. Interestingly, the wintertime POM exhibits most 15N-depleted values (δ15NPOM: 2.1 ± 1.5‰, p < 0.05) among all the seasons indicating dominant contribution from fertilizer and phytoplankton sources. Chilika catchment is mainly used for rice cultivation by the native population, which is harvested during winter. Heavy use of artificial fertilizers (δ13C: −28.5 ± 5.0‰ and δ15N: 0.2 ± 1.3‰; Vitòria et al., 2004) have been reported in these paddy fields. Rice plants typically have δ13C of about −28.1‰ and δ15N of ~1.2‰ (Jennerjahn et al., 2004). If agricultural runoff containing plant remains and fertilizers from these harvested paddy fields are transported to Chilika during winter precipitation, a likely possibility, it is expected to significantly lower the δ15NPOM compared to monsoon, which is observed in our data (Fig. 4b). The southern sector represents the deepest part of the lagoon and is less affected by in situ growth of macrophytes compared to the northern and central sectors. It is also characterized with most depleted isotopic composition (δ13CPOM: −27.1 ± 0.6‰ and δ15NPOM: 1.1 ± 0.8‰; Figs. 3b and 4b) compared to other sectors. The lagoon in winter is characterized with less turbidity and wind speed, stable water column conditions, and longer water residence time, all of which are conducive for phytoplankton growth (e.g., Lu and Gan, 2015). Part of this 15N-depletion may also be due to preferential uptake of isotopically

4.3.3. Summer season Compared to the monsoon and winter seasons, freshwater discharge during summertime is significantly reduced and limited to the northern sector only via perennial distributaries of the Mahanadi River. Summer season is characterized with most positive δ13CPOM (−23.0 ± 1.4‰, p < 0.001; Fig. 3c) in the lagoon. The distribution pattern shows slightly higher average δ13CPOM values in the central sector (−22.4‰) compared to the northern (−23.9‰) and southern (−23.4‰) sectors. The lowest δ13CPOM (p > 0.05; Fig. 3c) observed in the northern sector suggests influence of terrestrial OM, while significantly higher δ15NPOM (5.2 ± 0.9‰, p < 0.05; Fig. 4c) indicates more influence of 15N-enriched wastewater discharged via the perennial Mahanadi distributaries in the northern sector compared to the central and southern sectors. Ganguly et al. (2015) reported that significantly low freshwater discharge into Chilika during summer results in the lowest DIN concentrations and a shift towards limited nitrogen availability. Further, Robin et al. (2016) reported a decreasing trend of DIN concentrations from north to south in Chilika. However, in the case of nitrogen limitation during dry periods, the N demand of phytoplankton is supported by nutrient (i.e., NH4+; 15N-depleted) release from sediments and/or biological fixation of N2 (Vybernaite-Lubiene et al., 2017). The NH4+ concentration among the other DIN species in the lagoon was found to be highest during summer, which was attributed to resuspension and remineralization of particulate OM caused by wind-induced resuspension of bottom sediments (Patra et al., 2016; Robin et al., 2016) resulting in about 2.5 times increase in phytoplankton biomass in summer relative to winter (Patra et al., 2016). Therefore, more positive δ13CPOM (−22.4 ± 1.0‰) and less positive δ15NPOM (3.4 ± 0.9‰) values in the central sector can be due to increased phytoplankton as well as cyanobacterial activity. Further, due to resuspension of bottom 87

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sector and minimum contribution in the central and southern sectors, which are more influenced by lagoon phytoplankton and bacterial productivity. The outer channel remains dominated by marine input. Our results show that during monsoon, when river discharge is highest, POM primarily comprises of allochthonous inputs (terrigenous including urban wastewater), but wintertime POM reflects a mixed source of agricultural runoff containing plant remains and fertilizers, and lagoon phytoplankton and cyanobacteria. During summer/dry season when freshwater discharge into the lagoon is minimal and limited via perennial distributaries of the Mahanadi River to the northern sector only, enhanced lagoon phytoplankton and bacterial productivity (autochthonous sources) mainly contribute to the POM. The δ13C values and C/N ratios of SOM imply major contribution from terrestrial and macrophyte sources and minor contribution from phytoplankton and/ or cyanobacteria. In general, the northern sector is heavily influenced by urban/industrial wastewater input, while the western part of the central sector is significantly influenced by untreated domestic sewage discharged from the nearby townships and villages. The isotopic signatures are clearly able to detect anthropogenic contributions to Chilika that can potentially endanger the lagoon ecosystem.

sediments in the shallow central sector, contribution from SOM to the POM cannot be neglected. Less positive δ13CPOM (−23.4 ± 0.9‰) and δ15NPOM (3.2 ± 0.7‰) values in the southern sector, which also has the lowest DIN concentration (Robin et al., 2016), suggest a dominance of NH4+ and/or N2-fixing phytoplankton than in the central sector. The lowest C/N ratio (8.9 ± 1.1) observed in this season also indicates increased contribution from phytoplankton/bacterial origin POM in the lagoon; high primary productivity and high phytoplankton biomass during low fresh water discharge was observed by Robin et al. (2016). In contrast, the outer channel with higher salinity shows the most positive δ13CPOM (−21.9 ± 0.6‰) and δ15NPOM (5.5 ± 0.02‰) values, and low C/N ratios (7.8 ± 0.6) suggesting dominance of marine inputs. However, during summertime when flow in rivers is almost negligible, sewage contribution from nearby townships and villages contribute to the N-isotope composition of western part of the central sector (Fig. 4c). 4.4. Spatial variability in SOM Unlike SPM of the lagoon, surface sediment also receives substantial amount of OM in the form of accumulated macrophyte litters. In contrast to the δ13CPOM, spatial distribution pattern of δ13CSOM (−21.8 ± 0.6‰) shows no major variability in the lagoon (Fig. 3d; p > 0.05), and is generally ~4‰ higher than that of the monsoon and winter seasons POM (p < 0.001). The observed less isotopic variability is likely due to resuspension and mixing of bottom sediments by windinduced water current before final redistribution in the lagoon (Dubois et al., 2012; Patra et al., 2016). Similar δ13CSOM values were also reported for the several coastal lagoons, for example the Lapalme lagoon (−21.0 ± 0.7‰; Carlier et al., 2007) and the Venice lagoon (−21.6‰; Berto et al., 2013) of Mediterranean region. However, δ13CSOM of coastal lagoons can also range from −10‰ to −20‰ because of dominant abundance of macrophytes (see Carlier et al., 2007 and references therein). Though Chilika receives its major OM from land based sources, more 13C-enriched values (~3‰ difference; p < 0.001) of SOM than POM clearly suggest substantial contribution of macrophyte (−15.3 ± 2.3‰) to the SOM pool. The C/N ratio of SOM (10.1 ± 1.3; Table S2) is suggesting major contribution from terrestrial (C/N ratio: 11.0 ± 1.1) and macrophyte (C/N ratio: 24.3 ± 4.3) sources along with some contribution from phytoplankton and/or cyanobacteria (C/N ratio: 5–7). The δ15NSOM varies from 1.9‰ to 6.6‰ (average: 4.3‰), similar to that reported for other coastal lagoons such as the Lapalme lagoon (4.3 ± 0.5‰; Carlier et al., 2007) and the Venice lagoon (~4‰; Berto et al., 2013). The δ15NSOM distribution pattern shows relatively more positive values in the northern (4.4 ± 0.7‰) and southern sectors (4.7 ± 0.3‰) and less positive (3.5 ± 1.1‰) in the central sector (Fig. 4d). Marked depletion in 15N of SOM towards the western periphery of the central sector (p < 0.001) strongly indicates influence of domestic sewage input from the nearby townships and villages (Fig. 4d). In general, δ15NSOM of Chilika reflects dominant input from terrestrial and macrophyte sources, but the most positive δ15NSOM (6.4 ± 0.2‰, p < 0.05) of outer channel suggests dominance of marine inputs.

Acknowledgements We thank Bita Mohanty and other supporting staffs of Chilika Development Authority for help during sample collection. Thanks are due to Abhishek Kumar for help in preparing the spatial distribution maps. Constructive comments of Prof. A. Piola (Editor-in-Chief) and three anonymous reviewers significantly improved the quality of the manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.jmarsys.2019.03.001. References Bardhan, P., Karapurkar, S.G., Shenoy, D.M., Kurian, S., Sarkar, A., Maya, M.V., Naik, H., Varik, S., Naqvi, S.W.A., 2015. Carbon and nitrogen isotopic composition of suspended particulate organic matter in Zuari Estuary, west coast of India. J. Mar. Syst. 141, 90–97. https://doi.org/10.1016/J.JMARSYS.2014.07.009. Barik, S.K., Muduli, P.R., Mohanty, B., Behera, A.T., Mallick, S., Das, A., Samal, R.N., Rastogi, G., Pattnaik, A.K., 2017. Spatio-temporal variability and the impact of Phailin on water quality of Chilika lagoon. Cont. Shelf Res. 136, 39–56. https://doi. org/10.1016/J.CSR.2017.01.019. Barros, G.V., Martinelli, L.A., Oliveira Novais, T.M., Ometto, J.P.H.B., Zuppi, G.M., 2010. Stable isotopes of bulk organic matter to trace carbon and nitrogen dynamics in an estuarine ecosystem in Babitonga Bay (Santa Catarina, Brazil). Sci. Total Environ. 408, 2226–2232. https://doi.org/10.1016/J.SCITOTENV.2010.01.060. Berto, D., Rampazzo, F., Noventa, S., Cacciatore, F., Gabellini, M., Aubry, F.B., Girolimetto, A., Brusà, R.B., 2013. Stable carbon and nitrogen isotope ratios as tools to evaluate the nature of particulate organic matter in the Venice lagoon. Estuar. Coast. Shelf Sci. 135, 66–76. https://doi.org/10.1016/J.ECSS.2013.06.021. Bird, M.I., Tait, E., Wurster, C.M., Furness, R.W., 2008. Stable carbon and nitrogen isotope analysis of avian uric acid. Rapid Commun. Mass Spectrom. 22, 3393–3400. https://doi.org/10.1002/rcm.3739. Carlier, A., Riera, P., Amouroux, J.-M., Bodiou, J.-Y., Escoubeyrou, K., Desmalades, M., Caparros, J., Grémare, A., 2007. A seasonal survey of the food web in the Lapalme Lagoon (northwestern Mediterranean) assessed by carbon and nitrogen stable isotope analysis. Estuar. Coast. Shelf Sci. 73, 299–315. https://doi.org/10.1016/J.ECSS. 2007.01.012. Carlier, A., Riera, P., Amouroux, J., Bodiou, J., Desmalades, M., Grémare, A., 2009. Spatial heterogeneity in the food web of a heavily modified Mediterranean coastal lagoon: stable isotope evidence. Aquat. Biol. 5, 167–179. https://doi.org/10.3354/ ab00147. Costanzo, S.D., O'Donohue, M.J., Dennison, W.C., 2003. Assessing the seasonal influence of sewage and agricultural nutrient inputs in a subtropical river estuary. Estuaries 26, 857–865. https://doi.org/10.1007/BF02803344. Cresson, P., Ruitton, S., Fontaine, M.-F., Harmelin-Vivien, M., 2012. Spatio-temporal variation of suspended and sedimentary organic matter quality in the bay of Marseilles (NW Mediterranean) assessed by biochemical and isotopic analyses. Mar. Pollut. Bull. 64, 1112–1121. https://doi.org/10.1016/J.MARPOLBUL.2012.04.003. Dubois, S., Savoye, N., Grémare, A., Plus, M., Charlier, K., Beltoise, A., Blanchet, H., 2012. Origin and composition of sediment organic matter in a coastal semi-enclosed

5. Conclusions This study was aimed to trace sources of OM in Chilika lagoon, India- Asia's largest brackish water lagoon- by analyzing both the spatial and seasonal variability of stable C and N isotopic compositions and C/N ratios of SPM and surface sediments. The lagoon is currently experiencing anthropogenic disturbances as well as huge amount of urban/industrial wastewater discharge from the capital city Bhubaneswar and untreated sewage from surrounding townships and villages. Spatial variability in the δ13C and δ15N compositions of POM suggests maximum contribution of terrestrial sources in the northern 88

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