Distribution, sources and biogeochemistry of organic matter in a
mangrove dominated estuarine system (Indian Sundarbans) during
the pre-monsoon
R. Ray a, *, T. Rixen a, A. Baum a, A. Malik b, G. Gleixner b, T.K. Jana c
a Department of Biogeochemistry, Leibniz Center for Tropical Marine Ecology, Fahrenheitstr. 6, 28359 Bremen, Germany
b Department of Biogeochemical Processes, Max Planck Institute for Biogeochemistry, Hans, Knoell Str. 10, 07745 Jena, Germany
c Department of Marine Science, University of Calcutta, 35 B. C.Road, Kolkata 700019, India
a r t i c l e i n f o
Article history:
Received 12 February 2015
Received in revised form
29 September 2015
Accepted 16 October 2015
Available online xxx
Keywords:
Organic and inorganic carbon Stable isotopes (C, N) Sundarbans
a b s t r a c t
The sources and distribution of dissolved organic carbon (DOC), particulate organic carbon (POC) and dissolved inorganic carbon (DIC) in the Indian Sundarbans mangrove and Hooghly estuarine system were examined during the pre-monsoon (summer) 2014. DOC is the dominant form of organic matter (OM) in the studied estuarine waters and represents a mixture of mangrove and riverine sources. Microbial degradation of land derived OM results in a high pCO2 in the Hooghly estuarine waters while enrichment in d13C-DIC ascribes to CO2 uptake by phytoplankton in the Sundarbans water. Higher d15N in the particulate organic nitrogen (PON) of the mangrove and marine zone could be associated with enhanced phytoplankton production sustained by nitrate from mangrove derived OM decomposition and/or nitrate imported from the Bay of Bengal. Low organic carbon contents and elemental ratios (TN/TOC) indicate an intense mineralization and transformation of OM in the sediments, resulting insignificantly different OM compositions compared to those of the three major sources: land derived OM, mangrove leaf litter (Avicennia marina) and in situ phytoplankton production.
© 2015 Elsevier Ltd. All rights reserved.
1. Introduction
The majority of the worlds estuaries are net sources of CO2 due
to the processing of land derived dissolved and particulate organic
carbon (DOC and POC) as well as dissolved inorganic carbon (DIC)
during their transport to the global ocean (Harrison et al., 2005).
Highly productive mangrove swamps are a prominent feature of
many tropical and subtropical estuaries (Twilley et al., 1992). The
mangrove dominated estuaries are mostly heterotrophic due to
intense decomposition of organic matter (OM) (Mukhopadhyay
et al., 2006; Bouillon et al., 2003; Biswas et al., 2004), suggesting
active processing and high turnover rates of organic matter
(Nedwell et al., 1994) before their transport to coastal water
(Dittmar and Lara, 2001). Recent studies have shown that
mangrove pore-water seepage enrich mangrove tidal creeks in
dissolved organic and inorganic elements (Gleeson et al., 2013;
Maher et al., 2013; Stieglitz et al., 2013). After tropical peatlands
(storage of 88.6 Pg C, Page et al., 2011), mangroves are the most
productive ecosystems (storage of 15 Pg C in the live biomass and
soil) and sequester at a faster rate (174 g C m 2 yr 1, Donato et al.,
2011) than any other coastal habitats e.g. sea grasses
(138 g C m 2 yr 1, Fourqurean et al., 2012) highlighting their
importance as most proficient carbon fixers on earth (Donato et al.,
2011). Mangroves export organic carbon to estuaries and the ocean
(Dittmar et al., 2006; Jennerjahn and Ittekkot, 2002), of which DOC
can account for more than 80% of the exported organic carbon,
depending on the seasonal pattern of tidal amplitude, inundation
frequency, faunal activity etc. (Twilley, 1985; Machiwa and
Hallberg, 2002). This high DOC export supports the “outwelling
hypothesis” proposed by Odum and Heald (1975), which highlights
the litterfall contribution towards the total export and consequent
trophic level subsidy in adjacent coastal waters. The DOC, being a
potential source of energy to aquatic organisms, may be either
consumed during export ((Bernhardt and McDowell, 2008; Taylor
and Townsend, 2010), or photochemically degraded in the water
column (especially in warm tropical regions; Zika, 1981). Mangroves
annually export 28 Tg C of POC derived from plant debris,
* Corresponding author. Current affiliation: IUEM-LEMAR, UBO, rue Dumont
dUrville, 29280, Plouzane, France.
E-mail addresses: raghab.ray@gmail.com, raghab.ray@univ-brest.fr (R. Ray).
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science
journal homepage: www.elsevier.com/locate/ecss
http://dx.doi.org/10.1016/j.ecss.2015.10.017
0272-7714/© 2015 Elsevier Ltd. All rights reserved.
Estuarine, Coastal and Shelf Science xxx (2015) 1e10
Please cite this article in press as: Ray, R., et al., Distribution, sources and biogeochemistry of organic matter in a mangrove dominated estuarine
system (Indian Sundarbans) during the pre-monsoon, Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.10.017
1. Introduction
The majority of the worlds estuaries are net sources of CO2 due
to the processing of land derived dissolved and particulate organic
carbon (DOC and POC) as well as dissolved inorganic carbon (DIC)
during their transport to the global ocean (Harrison et al., 2005).
Highly productive mangrove swamps are a prominent feature of
many tropical and subtropical estuaries (Twilley et al., 1992). The
mangrove dominated estuaries are mostly heterotrophic due to
intense decomposition of organic matter (OM) (Mukhopadhyay
et al., 2006; Bouillon et al., 2003; Biswas et al., 2004), suggesting
active processing and high turnover rates of organic matter
(Nedwell et al., 1994) before their transport to coastal water
(Dittmar and Lara, 2001). Recent studies have shown that
mangrove pore-water seepage enrich mangrove tidal creeks in
dissolved organic and inorganic elements (Gleeson et al., 2013;
Maher et al., 2013; Stieglitz et al., 2013). After tropical peatlands
(storage of 88.6 Pg C, Page et al., 2011), mangroves are the most
productive ecosystems (storage of 15 Pg C in the live biomass and
soil) and sequester at a faster rate (174 g C m 2 yr 1, Donato et al.,
2011) than any other coastal habitats e.g. sea grasses
(138 g C m 2 yr 1, Fourqurean et al., 2012) highlighting their
importance as most proficient carbon fixers on earth (Donato et al.,
2011). Mangroves export organic carbon to estuaries and the ocean
(Dittmar et al., 2006; Jennerjahn and Ittekkot, 2002), of which DOC
can account for more than 80% of the exported organic carbon,
depending on the seasonal pattern of tidal amplitude, inundation
frequency, faunal activity etc. (Twilley, 1985; Machiwa and
Hallberg, 2002). This high DOC export supports the “outwelling
hypothesis” proposed by Odum and Heald (1975), which highlights
the litterfall contribution towards the total export and consequent
trophic level subsidy in adjacent coastal waters. The DOC, being a
potential source of energy to aquatic organisms, may be either
consumed during export ((Bernhardt and McDowell, 2008; Taylor
and Townsend, 2010), or photochemically degraded in the water
column (especially in warm tropical regions; Zika, 1981). Mangroves
annually export 28 Tg C of POC derived from plant debris,
* Corresponding author. Current affiliation: IUEM-LEMAR, UBO, rue Dumont
dUrville, 29280, Plouzane, France.
E-mail addresses: raghab.ray@gmail.com, raghab.ray@univ-brest.fr (R. Ray).
phytoplankton, and microphytobenthos to the sea (Alongi, 2014)
which is similar in quantity to the annual export of DOC (26.4 Tg C,
Dittmar et al., 2006). Supply of mangrove derived organic carbon
(mangrove detritus or microphytobenthos) or allochthonous
(phytoplankton or non-mangrove) to waters surrounding mangroves
could enhance net heterotrophic activity and their mineralization
could affect DIC composition (Gattuso et al., 1998; Kon e
and Borges, 2008). Although several investigations have been carried
out to understand possible sources and biogeochemical cycling
of OM in estuaries (Canuel, 2001;Wang et al., 2004; Hu et al., 2006;
Zhang et al., 2007; Bauchez et al., 2014; Bardhan et al., 2014;
Krishna et al., 2015 and references therein), there are few studies
that delineate the origin and distribution of organic carbon in
mangroves, in general (Kuramato and Minagawa, 2001; Bouillon
et al., 2003) and in the Sundarbans and Hooghly estuarine systems,
in particular.
The mangroves of the Indo-Pacific region are known for their
high aboveground primary production (Twilley et al., 1992). The
Indian Sundarbans, located at the land-ocean boundary (highly
irregular coast consisting of a network of interconnected tidal
creeks) of the Bay of Bengal, is the world's largest mangrove delta
constituting approximately 3% of total area of mangroves worldwide,
and is UNESCO world heritage site. Ray et al. (2011, 2013) and
Ganguly et al. (2008) demonstrated that the Sundarbans biosphere
(4264 km2) is potentially sensitive to increasing atmospheric CO2,
sequestering 2.79 Tg C (teragram ¼ 1012 g) annually. Sources of OM
in the waters and sediments surrounding mangroves can be
differentiated by using two geochemical proxies; the atomic [TN/
TOC] ratio of total nitrogen to total organic carbon (Tesi et al., 2007)
and with stable carbon and nitrogen isotopes (e.g. Cifuentes et al.,
1996; Bouillon et al., 2003; Kennedy et al., 2004; Liu et al., 2006;
Zhang et al., 2007). The aims of this study were (1) to determine the
quantity, quality and spatial variation of organic and inorganic
carbon in mangrove estuarine waters and sediment (2) to identify
the sources of OM using proxies of TN and TOC contents, their ratios,
stable carbon and nitrogen isotopes (d13C-DOC, d13C-DIC, d13CPOC
and d15N-PON), and possible OM end members (riverine POC,
phytoplankton and Avicennia plant leaves), collected from the study
area.
2. Material and methods
2.1. Study area
The Sundarbans (21 32
0
e21 42
0
N and 88 05
0
e89 E, Fig. 1)
cover an area of 10,200 km2, of which 4200 km2 of reserved forest is
located in India and remainder in Bangladesh. The Indian Sundarbans
ecosystem is situated at the land ocean boundary of the
Ganges-Brahmaputra delta and the Bay of Bengal. This largest
natural mangrove is crisscrossed by the estuarine phases of several
distributaries of the River Ganges: Hooghly, Mooriganga, Saptamukhi,
Thakuran, Matla, Bidya, Gosaba and Haribhanga forming a
sprawling archipelago of 102 islands out of which 54 are reclaimed
for human settlement while the rest are in natural state. Lothian
Island, is situated at the buffer zone of the Sundarbans Biosphere
Reserve and covers an area of 38 km2. This island is completely
intertidal and occupied by thick dominant mangrove species, Avicennia
alba, Avicennia marina and Avicennia officinalis.
The Ganges drains much of the southern slopes of the Himalayas
and delivers large sediment loads (324 106 t annually) to the
Bengal fan (Galy et al., 2007). The sediment of recent origin is the
result of extensive fluviomarine deposits of the river Ganges and
Bay of Bengal while silt loam is the dominant textural class (sand
9.23%, silt 79.6%, clay 11.2%, Ray et al., 2011). Semidiurnal tides with
meso-microtidal amplitude (i.e., 2.5e7 m) and extremely gentle
shelves (1.2-4.08) with muddy substrate favour water current and
tidal action quite appropriate for extensive mangrove occurrence.
Climate in the region is characterized by the southwest monsoon
(June to September), north east monsoon or post-monsoon
(October to January) and pre-monsoon (February to May);
70e80% of the annual rainfall occurs during the monsoon resulting
in high river discharges (3000 ± 1000 m3 s 1) that gradually diminishes
to minimum (1000 ± 80 m3 s 1) during the pre-monsoon
(Mukhopadhyay et al., 2006).
Sampling was undertaken in three connected systems in the
Hooghly and Saptamukhi estuary: 1) along the salinity gradient of
the Hooghly estuary with riverine terrestrial material input, 2) the
mangrove dominated Saptamukhi estuary 3) the adjacent coastal
water, the Bay of Bengal to study the contribution of mangrove
terrestrial and marine derived (phytoplankton) organic matter. The
Lothian Island and associated Saptamukhi estuary (station 1: Point
I, II and III, 21 41.63
0
N and 88 18.18
0
E, Fig. 1) was taken as being
representative of the Sundarbans mangrove ecosystem. During
high tide the island is inundated upto 3 m. Biswas et al. (2010)
observed higher phytoplankton abundance during high tide
compared with low tide and no change of the composition of
abundant species during low tide at the study site. However,
further investigations that consider seasonal and tidal cycle are
required for the comprehensive investigation of the organic carbon
dynamics in the study area. Water samples were collected from
three stations along the estuary and island within one hour of each
other. A tidal creek (Hatani Duani) connects the Saptamukhi estuary
and the Hooghly estuary near Chemaguri and the area is
covered by extensive mangrove forests and mudflats.
The Hooghly estuary (station 2a,b,c) is the main artery of the
Sundarbans mangrove ecosystem and influenced by the freshwater
discharge from the Farrakka dam, which is located 285 km upstream
from the mouth of the river. Mean current velocities range
from 108 to 117 cm s 1 between high and low tide, respectively
(Mukhopadhyay et al., 2006). The Hooghly estuary is selected as a
study site based on a consideration of factors (e.g. mangrove
coverage, anthropogenic input and conservative mixing). Three
sampling points were selected in the mixing zone of the Hooghly
estuary: Diamond Harbour (Stn.2a, 22 8.780N and 88 090E) at the
upper stretch of the river (riverine zone); Lot 8 (Stn.2b 21 48.480N
and 88 3.490E), 30 km downstream from Diamond Harbour (mixing
zone) and Chemaguri (Stn.2c, 21 39034.400N and 88 02038.100E)
at the confluence of the Mooriganga river and the Bay of Bengal
with fringing mangroves (marine zone).
2.2. Sampling and analytical part
The pre-monsoon season was selected for sampling as it represents
a uniform salinity profile with relatively minimum terrestrial
inputs due to low discharge of the Ganges. The Hooghly
estuary, Lothian Island and associated Saptamukhi estuary were
sampled in May, 2014. A Niskin bottle (2 L) was used to sample
surface waters. Temperature, salinity, dissolved oxygen and pH
were measured immediately after collection using a multiparameter
water quality meter (WTW Multi 3500i, with a precision of
±0.1 (salinity, withWTWprobes), ±0.1 C (temp), ±0.1 (DO), ±0.001
(pH, calibrated on the NBS scale). Total alkalinity (TA) was
measured by Gran electro titration with a reproducibility of ±
2 mMkg 1 and an accuracy of ± 3 mMkg 1. Tidal water samples for
DIC and d13DIC analyses were collected using 100 ml polyethylene
bottles and preserved with saturated HgCl2 solution. Samples of
25 ml were taken for the d13DIC measurements and overfilled in a
screw-capped glass vial without any bubble formation and kept in
an icebox. The spectrophotometric method was used for the analyses
of nitrate, nitrite, and ammonia in the water (Grasshoff, 1983;
APHA, 1995). Samples for total suspended matter (TSM) were
stored in a cool box before filtration of a known volume of tidal
water on preweighed and precombusted (overnight at 450 C)
47mmWhatman GF/F filters, and subsequently dried. TSM samples
were also used for the POC and PON elemental and isotope (d13C,
d15N) determinations. For DOC and DON analyses samples where
filtered through syringe filters (cellulose-acetate membrane) and
acidified with 0.2 M H3PO4 until the pH level reduced to 2. Dissolved
organic nitrogen (DON) was calculated by subtracting dissolved
inorganic nitrogen DIN (nitrate þ nitrite þ ammonia) from
TDN and was expressed in mM.
Fresh leaves of A. marina were collected from Lothian Island (stn.
1) and Chemaguri (stn.2c). Washed samples were dried at 40 C in
an electric oven and then powdered in a Retsch Centrifugal
Grinding Mill. Surface sediments from the same locations were
sampled by a hand used PVC cores (inner diameter 7.5 cm). Samples
were then dried and powdered by a Fritsch Pulverisette. All samples
were transported to the laboratory on ice for further processing.
2.3. Analyses of elemental C, N and isotopes of suspended matter,
plant and sediment
Total carbon and nitrogen in the suspended matter, sediment
and leaf samples were analysed using Eurovector EA3000. LECO
1013 Standards were introduced every five samples in order to
control the precision of the samples. The relative standard
deviation for the C and N percentage measurement was ±0.04 and
±0.01 respectively. A Thermo Finningan Delta plus mass spectrometer
coupled with a flash EA 1112 and ConFloII interface was
used for analysing d13C and d15N of the sediment, TSM and plant
samples. All data are expressed in conventional delta (d) notation,
where the isotopic ratio of d15N/d14N is expressed relative to Air and
d13C/d12C relative to the international PDB standard as defined by:
d‰ ¼ [(Ratiosample/Ratiostandard) 1] 1000
The CO2 reference gas used is research grade and has been
calibrated to PDB using NBS22 (National Bureau of Standards) and
USGS24 (United States Geological Survey, carbon isotopes in
graphite). The N2 reference gas used is research grade and has been
calibrated to Air using IAEA-N1 and IAEA-N2 (both are coarse
grained salt of ammonium sulphate). OAS (IVA) and Pepton (Merck)
was used as working standard and reproducibility based on
duplicate analyses of a sample was ±0.13‰ for d13C and ±0.2‰ for
d15N.
2.4. DOC, DON and d13DOC measurement
DOC and TDN concentrations were determined using a Shimadzu
TOC-VCSH Analyser and NDIR detector (non-dispersive infra
red detector) calibrated against potassium hydrogen phthalate
(KHP) and potassium nitrate. The error of measurements was less
than 2%.DOC stable isotope analysis was carried out using a HPLC
system coupled to a Deltaþ XP IRMS through an LC IsoLink interface
(Thermo Fisher Scientific, Germany) (Malik et al., 2012; Scheibe
et al., 2012). Linearity of the system was ascertained using varying
concentrations (5e40 mgC L 1) of citric acid
(d13C: 18.58‰VPDB; Fluka, Germany) and pulses of CO2 reference
gas (d13C: 38.16‰ VPDB) were used for calibration of the LC-IRMS
system during every chromatographic run that lasted for 20 min.
The d13DOC values were reported as per mil relative to the PDB
standard with an overall uncertainty of ±0.10‰.
2.5. DIC and d13DIC measurement
The pCO2 and DIC were computed from pH and TA measurements
with the thermodynamic constants described by
Frankignoulle et al. (1998). The accuracy of computed DIC and pCO2
values are estimated at ±4 mmol kg 1 and ±4 ppm, respectively. For
the analysis of the d13DIC, a headspace was created which is filled
with helium and 300 mL of H3PO4 was added to convert all inorganic
carbon species to CO2. After overnight equilibration, part of
the headspace was injected into the helium stream of an elemental
analyser-isotope ratio mass spectrometer (EA-IRMS, MAT 253
coupled with gas bench II, Thermo scientific) for d13C
measurements.
3. Results
Physicochemical parameters as well as concentrations and isotopic
signatures of dissolved and particulate carbon and nitrogen of
the mangrove estuarine waters are presented in Table 1. During the
pre-monsoon, salinity varied from 1.75 to 30.9 along the Hooghly
estuary, whereas salinity in the Saptamukhi estuarine mangrove
water (Sundarbans) was generally high (26e31). The mean temperature
during the study was recorded as 31.2 ± 0.4 C. The pH in
the Hooghly estuary was lowest in the riverine zone (7.76 at stn.2a)
and increased progressively towards in the marine end of the estuary
(8.01 at stn.2c). The average pH of mangrove water was
8.03 ± 0.05. Dissolved oxygen and O2 saturation (%) along the
Hooghly salinity gradient ranged from 5.92 to 6.7 mg L 1 and
80e101% respectively and was greatest at the marine end of the
transition (stn.2c). Oxygen concentration and saturation was high
in the Saptamukhi estuarine mangrove waters (6.44e6.87 mg L 1;
103e109%) with no discernable pattern of variation. Total suspended
matter (TSM) concentration in the Hooghly and Saptamukhi
estuarine waters ranged from 60.69 to 119.35 mg L 1 and
112.2e182.7 mg L 1, respectively. POC and PON concentrations
showed a clear increasing trend along the salinity gradient of
estuarine mangrove waters ranged from 11.04 to 37.0 mM and
1.08e3.9 mM, respectively and were greatest in the Saptamukhi
estuarine waters (Table 1, Fig. 2a). The d13POC varied
between 24.4 and 23.6‰ over the salinity gradient of the
Hooghly estuary, and increased significantly in the Saptamukhi
estuary ( 22.3 to 23.0‰) (Fig. 2b). The PON concentration in the
Hooghly estuary (1.08e2.44 mM) was lower than that of the Saptamukhi
estuary (2.9e3.9 mM). In the Saptamukhi estuarine
mangrove water d15PON values increased considerably compared
to Hooghly upstream, with values ranging between 7.92‰ and
10.6‰ (Table 1). Elemental ratios (POC/PON) of suspended matter
were relatively high in both of the estuaries (mean ratio, Hooghly:
12.75 and Saptamukhi: 9.70) reflecting the contribution of riverine
and mangrove derived material in addition to phytoplankton in the
POC pool during the pre-monsoon.
The DOC concentrations of the Hooghly and Saptamukhi estuarine
waters varied over a narrow range from 245.5 to 324 mM and
260.3e328.3 mM respectively, being greatest at the marine end. In
the Hooghly estuary, DOC concentrations increased with increasing
salinities (Fig. 2c). The d13DOC increased from 25.3 to 24.3‰
along the salinity gradient of the Hooghly toward the marine end,
and values were lower ( 24.4 to 24.9‰) compared to d13POC
(Fig. 2d) in the Saptamukhi estuary. For both DON and DIN the
highest values were measured in the Hooghly estuary
(70.4 ± 34.3 mM; 20.0 ± 3.5 mM) and the lowest in the Saptamukhi
estuary (32.6 ± 10.2 mM; 15.5 ± 0.5 mM). The total alkalinity (TA)
varied over a narrow range: from 2.97 to 2.79 mmol kg 1 along the
salinity gradient of the Hooghly estuary and between 2.70 and
2.76 mmol kg 1 in the Saptamukhi estuary. The overall trend of TA
mirrored the changes in DIC, which ranged between 2.4 and
2.88 mmol kg 1 in the Hooghly estuary and 2.26 and
2.17 mmol kg 1 in the Saptamukhi estuary (Fig. 3a). The average
pCO2 values in the Hooghly estuary accounted for 785 ± 212 matm,
while the pCO2 values in the Saptamukhi estuary was
633 ± 111 matm. The pCO2 values showed a significant negative
correlation with O2 saturation (%) (R2 ¼ 0.65, p ¼ 0.003, Fig. 3b).
The d13DIC varied between 4.87‰and 1.91‰ in the Hooghly
Table 1
Spatial distribution of physicochemical, particulate and dissolved organic matter parameters in the Hooghly and Saptamukhi estuaries (mean ± standard deviation).
Water parameters Stn 1 (point I) Stn. 1 (point II) Stn. 1 (point III) Stn.2a Stn.2b Stn.2c
Saptamukhi estuary (Sundarbans) Hooghly estuary
Salinity (psu) 26 30 31 1.75 18.1 30.9
Tw ( C) 31.5 31.2 31.5 30.5 31.4 30.9
pH 8.021 7.981 8.096 7.763 7.873 8.014
DO (mg L 1) 6.67 6.87 6.44 5.92 ± 0.10 6.47 ± 0.24 6.7 ± 0.16
O2 saturation (%) 104 109 103 80 ±2 92 ± 2 101 ± 2
TSM (mg L 1) 182.74 157.34 112.2 60.69 ± 0.18 119.35 ± 11 79.46 ± 29
POC (mM) 37 27 32 11.04 ± 2.5 28.9 ± 1.66 25.8 ± 5.9
PON (mM) 3.91 3.15 2.90 1.08 ± 0.3 2.44 ± 0.05 1.76 ± 0.23
d13POC (‰) 23.0 22.5 22.3 24.1 ± 0.01 23.6 ± 0.13 24.4 ± 0.2
d15 PON (‰) 9.9 10.3 10.1 7.92 ± 0.6 9.5 ± 0.3 10.6 ± 1.2
DOC (mM) 328.2 260.3 294.3 245.5 ± 26 249 ± 25.5 324 ± 27
d13DOC 24.9 24.7 24.4 25.1 ± 0.07 24.7 ± 0.07 24.3 ± 0.1
DIN (mM) 15.15 16.04 15.6 25.25 ± 2.5 21.76 ± 1.0 17.9 ± 2.0
DON(mM) 35 41.3 21.4 60.89 ± 6.5 41.81 ± 1.2 108.46 ± 26.6
TA (mmol kg 1) 2.76 2.72 2.70 2.97 ± 0.04 2.86 ± 0.02 2.79 ± 0.01
pCO2(matm) 506 715 680 1013 ± 60 749 ± 45 592 ± 81
DIC (mmol kg 1) 2.17 2.26 2.20 2.88 ± 0.06 2.60 ± 0.01 2.40 ± 0.03
d13DIC (‰) 3.73 1.91 2.65 4.87 ± 0.2 3.62 ± 0.1 3.24 ± 0.2
4 R. Ray et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e10
Please cite this article in press as: Ray, R., et al., Distribution, sources and biogeochemistry of organic matter in a mangrove dominated estuarine
system (Indian Sundarbans) during the pre-monsoon, Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.10.017
Fig. 2. Relative distribution of POC, DOC and their isotopes with salinity.
Fig. 3. Relative distribution and correlation of DIC, isotopes and associated water parameters.
R. Ray et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e10 5
Please cite this article in press as: Ray, R., et al., Distribution, sources and biogeochemistry of organic matter in a mangrove dominated estuarine
system (Indian Sundarbans) during the pre-monsoon, Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.10.017
and Saptamukhi estuaries, with increasing gradually with salinity
(Fig. 3c). A significant inverse correlation was found between DIC
concentrations and d13DIC (R2 ¼ 0.61, p ¼ 0.004, Fig. 3d).
The mean TOC and TN values of mangrove leaves were
44.45% ± 0.25% and 1.62% ± 0.11%, respectively (Table 2) with mean
atomic [TN/TOC]ratio of 0.031 ± 0.001. The corresponding d13C
values ranged from 28.08 to 26.3‰, with a mean of
27.2 ± 1.25‰. The leaves were enriched in 15N, showing a mean
d15N value of 4.9 ± 0.93‰. The sediments showed enrichment in
d13C ( 24.5 ± 0.21‰) in contrast to the mangrove leaves
( 27.2 ± 1.2‰). The [TN/TOC] atomic ratios in the sediment varied
between 0.036 and 0.051 with d15N ranging from 3.7 to 4.64‰. The
[TN/TOC]ratios in the particulate organic matter (as phytoplankton)
were observed to be 0.094 with d13C and d15N values of 22.3‰and
10.1‰, respectively.
4. Discussions
The Hooghly estuarine water is characterized by a pronounced
salinity gradient in contrast to the Saptamukhi estuary which
showed only small salinity variations, reflecting a very limited
freshwater supply to the Saptamukhi estuary during pre-monsoon.
Temperature variations in both the estuarine surface waters were
small. Distinct differences in biogeochemical variability were
evident between these two estuaries. The Hooghly estuary had
lower pH, dissolved oxygen concentrations and oxygen saturations,
POC, PON, DOC, d13DIC, d13POC and d15PON, compared to the Saptamukhi
estuary, however higher values of pCO2, DIC, TA, DON and
DIN were recorded indicating input of local organic matter and its
microbial metabolism.
4.1. Organic carbon and nitrogen in plants, sediments and
suspended matter
TOC in the sediment of Lothian Island and Chemaguri mangrove
was lower in comparison with that of the south west coast of India
(mean 2.10%, Gireeshkumar et al., 2013). The significantly lower
[TN/TOC] ratios of these mangrove sediment compared to the value
reported for the mangrove dominated Macouria mud bank in
French Guiana (0.07e0.11, Gontharet et al., 2014) indicates that
intense mineralization takes place in the intertidal mangrove
sediment (which is similar to the other Indo Pacific mangroves;
Donato et al., 2011). Carbon isotopes (d13C) were relatively enriched
in the surface sediments than the mangrove leaves but more
depleted than the phytoplankton in the POC pool. The lower [TN/
TOC]ratios and depleted nitrogen isotopes (d15N) recorded in the
sediments compared to the phytoplankton and leaves indicate
intense microbial degradation of mangrove derived organic matter
to CO2, CH4 and inorganic nitrogen under oxic and anoxic conditions
(Ray et al., 2013). Ehleringer et al. (2000) suggested that the
d13C enrichment in the soil organic matter compared to plant leaves
could be the result of decomposition of organic matter both by
microbial and fungal activity. However, N2 fixation by benthic
diazotrophs (Sharaki et al., 2014; Ray et al., 2014; Voss et al., 2011)
could account for the lower ranges of nitrogen isotopes (d15N)
observed in the sediments relative to mangrove leaves. The range of
d13C observed in Avicennia sp. ( 28.08 to 26.31‰) is close to the
d13C range of mangrove C3 plants ( 29.0 to 25.4‰; Kuramato and
Minagawa, 2001; Hayase et al., 1999). The senescent leaves are the
major component of mangrove litter and main source of organic
matter in mangrove soils. Gontharet et al. (2014) showed the
change of atomic [TN/TOC] ratio from 0.05 to 0.03 and d13C
from 27.6‰ to 27.0‰ in Avicennia germinans for senescent
leaves.
The particulate organic matter (POM) concentrations in the
Hooghly and Saptamukhi estuaries were consistent with results
reported for other estuaries (Zuary estuary, Bardhan et al., 2014;
Changjiang estuary, Tan et al., 1991; Yangtzhe and Yellow river estuaries,
Cauwet and Mackenzie, 1993; and nine tidal estuaries
across European coast, Middelburg and Herman, 2007). During the
pre-monsoon, high phytoplankton productivity due to increased
transparency of the water column (Biswas et al., 2004) along with
the observed mean d13C of POC and d15N of PON in the range of
phytoplankton derived organic matter indicates that POM is predominantly
of in situ origin in the Saptamukhi estuary. However
mean elemental TN/OC ratio found in POM in the riverine zone of
the Hooghly estuary (0.082 ± 0.04) was close to that of the
terrestrial OM (>0.085; Hedges et al., 1997; Lamb et al., 2006).
Furthermore mean d13C of POC ( 24.1 ± 0.01‰) and d15N of PON
(7.92 ± 0.6‰) in the riverine zone were close to the mean d13C and
d15N ratios of C3 ( 25.9 ± 1.2 and 5.1 ± 2.1‰, respectively) land
plants (Krishna et al., 2015). All these results strongly suggest that
POC and PON observed in the riverine zone of the Hooghly estuary
could face microbial degradation during their transport from the
land to the estuary.
In this study, d15N of the PON increased with increasing salinity
showing higher ranges (9.9e11.7‰) in the marine and mangrove
dominated zone (Table 1). So far there is no report on higher
d15PON values measured in POM collected from the Bay of Bengal.
Kumar et al. (2004) reported highest d15PON values of 7.6‰ both
during pre and post monsoon along the south west coast of the Bay
of Bengal and highlighted the occurrence of denitrification that
causes the remaining nitrate in the heavier 15N. We also found a
significant negative correlation between DIN and d15PON
(DIN¼ 0.21 d15PON þ 13.66, R2 ¼ 0.55, n ¼ 10 figure not shown)
which was similar to the trend observed in the Montery Bay by Rau
et al. (1998). This trend was attributed to the preferential uptake of
14N during photosynthesis of organic matter in the cause of which
d15N values in the POC increased with decreasing nitrate concentrations.
In our case the highest d15PON (11.73‰) was measured at
the marine reference site (stn. 2c) showing a DIN concentration of
17.9 ± 2.0 mM which was as high as those found in the ocean most
productive upwelling systems (Rixen et al., 2006). Since such high
nitrate concentrations exclude an enrichment of 15N caused by the
preferential uptake of the lighter 14N during plankton bloom our
results support the finding of Kumar et al. (2004). In the Hooghly
estuary the decreasing d15PON values with decreasing salinity indicates
a mixing of nitrogen that originates from mangroves
Table 2
Mean elemental (total organic carbon TOC%, total nitrogen TN%, with standard deviation) and stable isotopic (d13C‰, d15N‰) composition of sediments, Avicennia leaf and
phytoplankton at Lothian Island (stn.1) and Chemaguri (stn.2c).
Mangroves TOC TN d13C d15N TN: TOC
Surface sediment Lothian Island 0.66 ± 0.21 0.04 ± 0.001 24.65 3.7 0.051
Chemaguri 0.70 ± 0.01 0.03 ± 0.001 24.35 4.64 0.036
Avicennia leaf Lothian Island 45.9 ± 0.33 1.7 ± 0.05 26.31 5.56 0.031
Chemaguri 43.0 ± 0.20 1.54 ± 0.04 28.08 4.24 0.030
Phytoplankton Lothian Island (pt.III Coastal water) 0.20 ± 0.02 0.02 ± 0.001 22.30 10.1 0.094
6 R. Ray et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e10
Please cite this article in press as: Ray, R., et al., Distribution, sources and biogeochemistry of organic matter in a mangrove dominated estuarine
system (Indian Sundarbans) during the pre-monsoon, Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.10.017
through benthic N2 fixation and marine nitrogen input through
denitrification in the oxygen depleted subsurface waters of the
northern Bay of Bengal.
4.2. Sources of DOM
The mean DOC concentrations of 294 ± 34 mM in the Saptamukhi
estuary and 273 ± 44 mM in the Hooghly estuary were close
to that reported for Brazilian mangrove waters (360 mM, Dittmar
and Lara, 2001), but were relatively lower in comparison to the
Florida mangrovewaters (500e2000 mM, Davis et al., 2001; Romigh
et al., 2006). Since contrary to Florida, the Brazilian and the Sundarbans
are flushed by large rivers (Amazon and Hooghly) it is
assumed that the low DOC contents result from low residence
times of water in the mangroves rather than from differences in the
DOC formation and decomposition rates. However, Mukherjee and
Ray (2012) reported an annual mean DOC concentration of 450 mM
along the HooghlyeMatla estuarine system, which is higher than
our mean value (273 ± 44 mM, station 2a,b,c) and indicates seasonal
effects. Nevertheless, the mean DOC concentration in our studywas
10 times higher than POC (around 30 mM) that is also consistent
with observations by other authors (Bouillon et al., 2003;
Kristenson and Suraswadi, 2002). The difference between the
Saptamukhi and the Hooghly estuary with respect to the d13DOC
was insignificant with a mean of 24.7‰which is consistent to the
values reported by other authors (Wafar et al., 1997; Dittmar et al.,
2001). In Fig. 4, the scattered plot between d13C versus atomic [TN/
TOC] ratio confirms the similarity of DOM composition with that
from riverine transport. However, standard deviation of DOM indicates
that considerable fraction of DOM could also be derived
from the mangrove sediment in addition by the processes of litter
leaching in the upper layer during tidal flushing and tidal pumping
from deeper layers. Dutta et al. (2015) reported that the average
pore water specific discharge was 90 times higher in the Sundarbans
than the value reported for silty clay sediment in Southern
Chesapeake Bay due to bioturbation by burrowing crab species and
further concluded that DOM could be transported by advective
fluxes from the sediment column (pore water) into the estuarine
water. Due to mixing of different sources and probably varying
degrees of decomposition a significant correlation between C and N
in the dissolved form could not be found (R2 ¼ 0.18, figure not
shown). However, DON having average concentration of 51.2 mM
contributed 73% to the total dissolved nitrogen (DON and DIN) and
70% to the total nitrogen (PON þ DON þ DIN) showing that it was
the major form of nitrogen in both estuaries. This implies furthermore
that leaf litter leaching could be the most important loss term
for nitrogen in mangroves. Except for the most offshore site in the
Hooghly estuary, DIN correlated positively with DON suggesting
that DIN concentrations were influenced by the decomposition of
DON that was leached from leaf litter. The negative correlation
between DIN and PON in turn indicates the uptake of DIN by
phytoplankton, which, as discussed before, composes to a large
extent of POM.
4.3. Sources of DIC
Considerable spatial variations of DIC and ancillary parameters
were found to occur with salinity changes. Highest DIC concentration
(2.88 ± 0.06 mmol kg 1)was observed in the riverine part of
Hooghly estuary with bicarbonate as the dominant species. The
d13C of DIC was relatively depleted in heavier 13C compared to the
ocean waters and further depleted (around 4.2‰) with
decreasing salinity along the Hooghly estuary. This relative depletion
of d13C-DIC along the Hooghly upstream coincided with the
significantly higher DIC and pCO2 concentrations and lower O2
saturation and pH. This indicates respiration of DOM supporting
the heterotrophy and implying that river outgassing is part of the
ecosystem respiration (Sarma et al., 2012, Biswas et al., 2004).
However, enrichment of d13C-DIC pool in both marine and
mangrove water corresponds to the increasing influence of ocean
waters into the system and enhanced uptake of DIC during
phytoplankton production in the saline mangrove water system
(Middelburg and Nieuwenhuize, 1998). In our study, relatively
higher d13C-DIC in the Saptamukhi estuary was associated with
higher concentrations of POC attributing to the planktonic uptake
of CO2 during photosynthesis. Therefore, during premonsoon, DIC
chemistry along the Hooghly upstream was governed by the
metabolic conversion of DOM to DIC causing heterotrophy and
increasing surface pCO2 while the Sundarbanswas primarily driven
by the phytoplankton productivity.
4.4. Three end-member model
Assuming that diagenetic reactions do not significantly alter the
OM, [TN/TOC] ratios and d13C values, following three end-member
mixing equations were used based on these values and mass balance
(Gontharet et al., 2014):
[TN/TOC]POC/sediment ¼ fMangrove [TN/TOC]Mangrove þ fPhytoplankton
[TN/TOC]Phytoplankton þ fPOC(Riveine)
[TN/TOC]POC(Riverine) (1)
d13CPOC/sediment ¼ fMangrove d13CMangrove þ fPhytoplankton
d13CPhytoplankton þ fPOC(Riverine)
d13CPOC(Riverine) (2)
1 ¼ fMangrove þ fPhytoplankton þ fPOC(Riverine) (3)
with mangrove end-member ([TN/TOC]Mangrove ¼ 0.037;
d13CMangrove ¼ 28.4‰), phytoplankton end-member ([TN/
TOC]Phytoplankton ¼ 0.11; d13CPhytoplankton ¼ 22.3‰) and
riverine particulate organic carbon (POC) end-member ([TN/
TOC]POC(Riverine) ¼ 0.098; d13CPOC(Riverine) ¼ 24.1‰); [TN/
TOC]POC/sediment and d13CPOC/sediment are the measured atomic
elemental ratio and the stable carbon isotopic composition of a
given POC/sediment sample, respectively; fMangrove, fPhytoplankton and
fPOC(Riverine) represent the relative fraction of each of these OM sources.
The POC collected from Diamond Harbour (stn.2a) were used as
riverine end member value, while POC collected from the
Fig. 4. Mixing plot between mean d13C and TN/TOC (±SD) of mangrove Leaf, Sediments,
dissolved organic matter (DOM), Riverine POC and Phytoplankton (Phyto).
R. Ray et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e10 7
Please cite this article in press as: Ray, R., et al., Distribution, sources and biogeochemistry of organic matter in a mangrove dominated estuarine
system (Indian Sundarbans) during the pre-monsoon, Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.10.017
Saptamukhi (point II and III) were considered as phytoplankton.
Hence to maintain maximum differences in d13C between the end
members, minimum value of d13C ( 28.4‰) for mangrove leaf (Avicennia
marina) was considered in the model.
The relationships between the [TN/TOC] ratios, the d13C values
of the three potential OM sources (A. marina leaves, riverine POC
and phytoplankton) and the typical ranges of these markers are
given in Fig. 5. The magnitude of [TN/TOC] ratios and d13C for these
three OM sources are found in the decreasing order:
Phytoplankton > Riverine > Leaf (Table 2, Fig. 5) and they are
considered as three different end-member components of the POC
and sedimentary OM. The calculated relative percentages of OM
contribution varied between 0 and 65.3% for mangrove leaves,
between 0 and 91.7% for riverine and between 0 and 89.9% for
phytoplankton. Sediments exhibited the predominance of OM
originating from mangrove leaves (~100%). The relative contributions
of these three OM sources were significantly different to each
site.
The contribution of riverine POC was 0e7.27% at stn.1, in
contrast to the stn.2b and 2c where it varied between 83.0e91.7%
and 0e87.5%, respectively. The increase in the contribution of
phytoplankton from mixing zone (2.44e17%, stn.2b) to the Sundarbans
mangroves (67.0e90%, stn.1) was linked to enhanced
phytoplankton production associated with the improvement of
transparency of the water column. There was an increase in the
contribution of mangrove derived material at stn.1 (2.85e33.0%)
and stn.2c relative to stn.2b (0e5.89%) due to the occurrences of
mangroves in the study area. The observed compositions of POC fell
within the domain defined by the three end member or very close
to the domain such that the differences were within the uncertainty
range. The sediments composition was found outside of the
angular domain defined by the three end members. The model
showed negative values except mangrove leaf end member. Such
conditions could arise due to the modification of leaf organic
matter by biogeochemical processes occurring in the mangrove
sediment. The mean atomic [TN/TOC]ratio (0.041 ± 0.011) in the
sediment was similar in magnitude with that of leaves (0.037) but
varied in isotopes (d13C ¼ 24.36 ± 1.01) which increased by 14.6%
compared to the leaves (d13C ¼ 27.19‰). Gontharet et al. (2014)
suggested that extensive remineralization of labile organic matter
and its conversion to more refractory organic matter could result in
higher d13C values ( 23.4‰ to 24.9‰) in the French Guiana mud
bank colonized by A. germinans. Organic carbon content
(0.64e0.79%) in the Sundarbans mangrove sediment was significantly
lower than that of Indo-Pacific mangroves (1.7e18%, Donato
et al., 2011) indicating its rapid turnover and resulting in an export
of CO2 (8.36 mg C m 2 s 1, Ray et al., 2013) from sediment to the
atmosphere, which is similar to that found in other mangroves
(Leopold et al., 2015; Lovelock et al., 2014; Chen et al., 2012, 2014).
5. Conclusion
This is the first time study where isotopic compositions of
organic/inorganic C and N were used to discriminate material
sources and to understand their origin and mixing in the riverine
and mangrove (the Sundarbans) dominated estuarine system along
the Bay of Bengal. During premonsoon, average DOC concentration
was about ten times greater than the mean POC concentrations and
considerable fraction of DOC was derived from mangrove sediment
and riverine transport. DON was the predominant form of nitrogen
and the elemental ratio, d13C of POC and d15N of PON in the riverine
zone were close to those of mangrove leaf litter. POC in the Sundarbans
was dominated by phytoplankton which growth was sustained
by nitrate that originated from the decomposition of
mangrove derived DON and nitrate imported from the Bay of
Bengal. Decomposition of mangrove derived organic matter
controlled the variation of DIC along the riverine and mixing zone
of the Hooghly estuary while phytoplankton production dominated
the DIC chemistry in the Sundarbans. In order to understand
possible sources of organic matter and its preservation in the
sediments a three end-member model was used. The obtained
results demonstrated that POCwas sourced from riverine transport,
phytoplankton and mangrove leaf litter and that the relative contributions
of these three sources to the total POM were 0e91.7%,
0e89.9%, 0e65.3% respectively along the estuaries. On the other
hand, extensive remineralization and transformation of organic
matter in the mangrove sediment resulted in significant deviation
from the composition of three end-member sources which further
coincided with low organic carbon percentages in the world's
largest mangrove delta.
Acknowledgements
Our first author (RR) is indebted to Leibniz-DAAD for providing
the postdoctoral fellowship funding (Sanction no. A/13/93589).
Thanks are also due to our boatman, helpers and field partners
especially Mr. Polas Gon for their continuous assistance during the
field trip. The authors are particularly thankful to Ulrike Machulik,
Institute of Geology/Biogeochemistry, University of Hamburg, for
analyzing the DOC and DON part of the water samples. The authors
are cordially grateful to our ZMT colleagues, in particular Dorothee
Dasbach for helping during IRMS analysis. We are highly indebted
to Dr. Sally Little, School of Animal Rural & Environmental Sciences,
Nottingham Trent University, UK, for improving the English language
and checking the manuscript. Finally authors are thankful to
the Associate Editor, Dr. Tim Jennerjahn and two anonymous reviewers
for their thoughtful and constructive comments.
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mangrove dominated estuarine system (Indian Sundarbans) during
the pre-monsoon
R. Ray a, *, T. Rixen a, A. Baum a, A. Malik b, G. Gleixner b, T.K. Jana c
a Department of Biogeochemistry, Leibniz Center for Tropical Marine Ecology, Fahrenheitstr. 6, 28359 Bremen, Germany
b Department of Biogeochemical Processes, Max Planck Institute for Biogeochemistry, Hans, Knoell Str. 10, 07745 Jena, Germany
c Department of Marine Science, University of Calcutta, 35 B. C.Road, Kolkata 700019, India
a r t i c l e i n f o
Article history:
Received 12 February 2015
Received in revised form
29 September 2015
Accepted 16 October 2015
Available online xxx
Keywords:
Organic and inorganic carbon Stable isotopes (C, N) Sundarbans
a b s t r a c t
The sources and distribution of dissolved organic carbon (DOC), particulate organic carbon (POC) and dissolved inorganic carbon (DIC) in the Indian Sundarbans mangrove and Hooghly estuarine system were examined during the pre-monsoon (summer) 2014. DOC is the dominant form of organic matter (OM) in the studied estuarine waters and represents a mixture of mangrove and riverine sources. Microbial degradation of land derived OM results in a high pCO2 in the Hooghly estuarine waters while enrichment in d13C-DIC ascribes to CO2 uptake by phytoplankton in the Sundarbans water. Higher d15N in the particulate organic nitrogen (PON) of the mangrove and marine zone could be associated with enhanced phytoplankton production sustained by nitrate from mangrove derived OM decomposition and/or nitrate imported from the Bay of Bengal. Low organic carbon contents and elemental ratios (TN/TOC) indicate an intense mineralization and transformation of OM in the sediments, resulting insignificantly different OM compositions compared to those of the three major sources: land derived OM, mangrove leaf litter (Avicennia marina) and in situ phytoplankton production.
© 2015 Elsevier Ltd. All rights reserved.
1. Introduction
The majority of the worlds estuaries are net sources of CO2 due
to the processing of land derived dissolved and particulate organic
carbon (DOC and POC) as well as dissolved inorganic carbon (DIC)
during their transport to the global ocean (Harrison et al., 2005).
Highly productive mangrove swamps are a prominent feature of
many tropical and subtropical estuaries (Twilley et al., 1992). The
mangrove dominated estuaries are mostly heterotrophic due to
intense decomposition of organic matter (OM) (Mukhopadhyay
et al., 2006; Bouillon et al., 2003; Biswas et al., 2004), suggesting
active processing and high turnover rates of organic matter
(Nedwell et al., 1994) before their transport to coastal water
(Dittmar and Lara, 2001). Recent studies have shown that
mangrove pore-water seepage enrich mangrove tidal creeks in
dissolved organic and inorganic elements (Gleeson et al., 2013;
Maher et al., 2013; Stieglitz et al., 2013). After tropical peatlands
(storage of 88.6 Pg C, Page et al., 2011), mangroves are the most
productive ecosystems (storage of 15 Pg C in the live biomass and
soil) and sequester at a faster rate (174 g C m 2 yr 1, Donato et al.,
2011) than any other coastal habitats e.g. sea grasses
(138 g C m 2 yr 1, Fourqurean et al., 2012) highlighting their
importance as most proficient carbon fixers on earth (Donato et al.,
2011). Mangroves export organic carbon to estuaries and the ocean
(Dittmar et al., 2006; Jennerjahn and Ittekkot, 2002), of which DOC
can account for more than 80% of the exported organic carbon,
depending on the seasonal pattern of tidal amplitude, inundation
frequency, faunal activity etc. (Twilley, 1985; Machiwa and
Hallberg, 2002). This high DOC export supports the “outwelling
hypothesis” proposed by Odum and Heald (1975), which highlights
the litterfall contribution towards the total export and consequent
trophic level subsidy in adjacent coastal waters. The DOC, being a
potential source of energy to aquatic organisms, may be either
consumed during export ((Bernhardt and McDowell, 2008; Taylor
and Townsend, 2010), or photochemically degraded in the water
column (especially in warm tropical regions; Zika, 1981). Mangroves
annually export 28 Tg C of POC derived from plant debris,
* Corresponding author. Current affiliation: IUEM-LEMAR, UBO, rue Dumont
dUrville, 29280, Plouzane, France.
E-mail addresses: raghab.ray@gmail.com, raghab.ray@univ-brest.fr (R. Ray).
Contents lists available at ScienceDirect
Estuarine, Coastal and Shelf Science
journal homepage: www.elsevier.com/locate/ecss
http://dx.doi.org/10.1016/j.ecss.2015.10.017
0272-7714/© 2015 Elsevier Ltd. All rights reserved.
Estuarine, Coastal and Shelf Science xxx (2015) 1e10
Please cite this article in press as: Ray, R., et al., Distribution, sources and biogeochemistry of organic matter in a mangrove dominated estuarine
system (Indian Sundarbans) during the pre-monsoon, Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.10.017
1. Introduction
The majority of the worlds estuaries are net sources of CO2 due
to the processing of land derived dissolved and particulate organic
carbon (DOC and POC) as well as dissolved inorganic carbon (DIC)
during their transport to the global ocean (Harrison et al., 2005).
Highly productive mangrove swamps are a prominent feature of
many tropical and subtropical estuaries (Twilley et al., 1992). The
mangrove dominated estuaries are mostly heterotrophic due to
intense decomposition of organic matter (OM) (Mukhopadhyay
et al., 2006; Bouillon et al., 2003; Biswas et al., 2004), suggesting
active processing and high turnover rates of organic matter
(Nedwell et al., 1994) before their transport to coastal water
(Dittmar and Lara, 2001). Recent studies have shown that
mangrove pore-water seepage enrich mangrove tidal creeks in
dissolved organic and inorganic elements (Gleeson et al., 2013;
Maher et al., 2013; Stieglitz et al., 2013). After tropical peatlands
(storage of 88.6 Pg C, Page et al., 2011), mangroves are the most
productive ecosystems (storage of 15 Pg C in the live biomass and
soil) and sequester at a faster rate (174 g C m 2 yr 1, Donato et al.,
2011) than any other coastal habitats e.g. sea grasses
(138 g C m 2 yr 1, Fourqurean et al., 2012) highlighting their
importance as most proficient carbon fixers on earth (Donato et al.,
2011). Mangroves export organic carbon to estuaries and the ocean
(Dittmar et al., 2006; Jennerjahn and Ittekkot, 2002), of which DOC
can account for more than 80% of the exported organic carbon,
depending on the seasonal pattern of tidal amplitude, inundation
frequency, faunal activity etc. (Twilley, 1985; Machiwa and
Hallberg, 2002). This high DOC export supports the “outwelling
hypothesis” proposed by Odum and Heald (1975), which highlights
the litterfall contribution towards the total export and consequent
trophic level subsidy in adjacent coastal waters. The DOC, being a
potential source of energy to aquatic organisms, may be either
consumed during export ((Bernhardt and McDowell, 2008; Taylor
and Townsend, 2010), or photochemically degraded in the water
column (especially in warm tropical regions; Zika, 1981). Mangroves
annually export 28 Tg C of POC derived from plant debris,
* Corresponding author. Current affiliation: IUEM-LEMAR, UBO, rue Dumont
dUrville, 29280, Plouzane, France.
E-mail addresses: raghab.ray@gmail.com, raghab.ray@univ-brest.fr (R. Ray).
phytoplankton, and microphytobenthos to the sea (Alongi, 2014)
which is similar in quantity to the annual export of DOC (26.4 Tg C,
Dittmar et al., 2006). Supply of mangrove derived organic carbon
(mangrove detritus or microphytobenthos) or allochthonous
(phytoplankton or non-mangrove) to waters surrounding mangroves
could enhance net heterotrophic activity and their mineralization
could affect DIC composition (Gattuso et al., 1998; Kon e
and Borges, 2008). Although several investigations have been carried
out to understand possible sources and biogeochemical cycling
of OM in estuaries (Canuel, 2001;Wang et al., 2004; Hu et al., 2006;
Zhang et al., 2007; Bauchez et al., 2014; Bardhan et al., 2014;
Krishna et al., 2015 and references therein), there are few studies
that delineate the origin and distribution of organic carbon in
mangroves, in general (Kuramato and Minagawa, 2001; Bouillon
et al., 2003) and in the Sundarbans and Hooghly estuarine systems,
in particular.
The mangroves of the Indo-Pacific region are known for their
high aboveground primary production (Twilley et al., 1992). The
Indian Sundarbans, located at the land-ocean boundary (highly
irregular coast consisting of a network of interconnected tidal
creeks) of the Bay of Bengal, is the world's largest mangrove delta
constituting approximately 3% of total area of mangroves worldwide,
and is UNESCO world heritage site. Ray et al. (2011, 2013) and
Ganguly et al. (2008) demonstrated that the Sundarbans biosphere
(4264 km2) is potentially sensitive to increasing atmospheric CO2,
sequestering 2.79 Tg C (teragram ¼ 1012 g) annually. Sources of OM
in the waters and sediments surrounding mangroves can be
differentiated by using two geochemical proxies; the atomic [TN/
TOC] ratio of total nitrogen to total organic carbon (Tesi et al., 2007)
and with stable carbon and nitrogen isotopes (e.g. Cifuentes et al.,
1996; Bouillon et al., 2003; Kennedy et al., 2004; Liu et al., 2006;
Zhang et al., 2007). The aims of this study were (1) to determine the
quantity, quality and spatial variation of organic and inorganic
carbon in mangrove estuarine waters and sediment (2) to identify
the sources of OM using proxies of TN and TOC contents, their ratios,
stable carbon and nitrogen isotopes (d13C-DOC, d13C-DIC, d13CPOC
and d15N-PON), and possible OM end members (riverine POC,
phytoplankton and Avicennia plant leaves), collected from the study
area.
2. Material and methods
2.1. Study area
The Sundarbans (21 32
0
e21 42
0
N and 88 05
0
e89 E, Fig. 1)
cover an area of 10,200 km2, of which 4200 km2 of reserved forest is
located in India and remainder in Bangladesh. The Indian Sundarbans
ecosystem is situated at the land ocean boundary of the
Ganges-Brahmaputra delta and the Bay of Bengal. This largest
natural mangrove is crisscrossed by the estuarine phases of several
distributaries of the River Ganges: Hooghly, Mooriganga, Saptamukhi,
Thakuran, Matla, Bidya, Gosaba and Haribhanga forming a
sprawling archipelago of 102 islands out of which 54 are reclaimed
for human settlement while the rest are in natural state. Lothian
Island, is situated at the buffer zone of the Sundarbans Biosphere
Reserve and covers an area of 38 km2. This island is completely
intertidal and occupied by thick dominant mangrove species, Avicennia
alba, Avicennia marina and Avicennia officinalis.
The Ganges drains much of the southern slopes of the Himalayas
and delivers large sediment loads (324 106 t annually) to the
Bengal fan (Galy et al., 2007). The sediment of recent origin is the
result of extensive fluviomarine deposits of the river Ganges and
Bay of Bengal while silt loam is the dominant textural class (sand
9.23%, silt 79.6%, clay 11.2%, Ray et al., 2011). Semidiurnal tides with
meso-microtidal amplitude (i.e., 2.5e7 m) and extremely gentle
shelves (1.2-4.08) with muddy substrate favour water current and
tidal action quite appropriate for extensive mangrove occurrence.
Climate in the region is characterized by the southwest monsoon
(June to September), north east monsoon or post-monsoon
(October to January) and pre-monsoon (February to May);
70e80% of the annual rainfall occurs during the monsoon resulting
in high river discharges (3000 ± 1000 m3 s 1) that gradually diminishes
to minimum (1000 ± 80 m3 s 1) during the pre-monsoon
(Mukhopadhyay et al., 2006).
Sampling was undertaken in three connected systems in the
Hooghly and Saptamukhi estuary: 1) along the salinity gradient of
the Hooghly estuary with riverine terrestrial material input, 2) the
mangrove dominated Saptamukhi estuary 3) the adjacent coastal
water, the Bay of Bengal to study the contribution of mangrove
terrestrial and marine derived (phytoplankton) organic matter. The
Lothian Island and associated Saptamukhi estuary (station 1: Point
I, II and III, 21 41.63
0
N and 88 18.18
0
E, Fig. 1) was taken as being
representative of the Sundarbans mangrove ecosystem. During
high tide the island is inundated upto 3 m. Biswas et al. (2010)
observed higher phytoplankton abundance during high tide
compared with low tide and no change of the composition of
abundant species during low tide at the study site. However,
further investigations that consider seasonal and tidal cycle are
required for the comprehensive investigation of the organic carbon
dynamics in the study area. Water samples were collected from
three stations along the estuary and island within one hour of each
other. A tidal creek (Hatani Duani) connects the Saptamukhi estuary
and the Hooghly estuary near Chemaguri and the area is
covered by extensive mangrove forests and mudflats.
The Hooghly estuary (station 2a,b,c) is the main artery of the
Sundarbans mangrove ecosystem and influenced by the freshwater
discharge from the Farrakka dam, which is located 285 km upstream
from the mouth of the river. Mean current velocities range
from 108 to 117 cm s 1 between high and low tide, respectively
(Mukhopadhyay et al., 2006). The Hooghly estuary is selected as a
study site based on a consideration of factors (e.g. mangrove
coverage, anthropogenic input and conservative mixing). Three
sampling points were selected in the mixing zone of the Hooghly
estuary: Diamond Harbour (Stn.2a, 22 8.780N and 88 090E) at the
upper stretch of the river (riverine zone); Lot 8 (Stn.2b 21 48.480N
and 88 3.490E), 30 km downstream from Diamond Harbour (mixing
zone) and Chemaguri (Stn.2c, 21 39034.400N and 88 02038.100E)
at the confluence of the Mooriganga river and the Bay of Bengal
with fringing mangroves (marine zone).
2.2. Sampling and analytical part
The pre-monsoon season was selected for sampling as it represents
a uniform salinity profile with relatively minimum terrestrial
inputs due to low discharge of the Ganges. The Hooghly
estuary, Lothian Island and associated Saptamukhi estuary were
sampled in May, 2014. A Niskin bottle (2 L) was used to sample
surface waters. Temperature, salinity, dissolved oxygen and pH
were measured immediately after collection using a multiparameter
water quality meter (WTW Multi 3500i, with a precision of
±0.1 (salinity, withWTWprobes), ±0.1 C (temp), ±0.1 (DO), ±0.001
(pH, calibrated on the NBS scale). Total alkalinity (TA) was
measured by Gran electro titration with a reproducibility of ±
2 mMkg 1 and an accuracy of ± 3 mMkg 1. Tidal water samples for
DIC and d13DIC analyses were collected using 100 ml polyethylene
bottles and preserved with saturated HgCl2 solution. Samples of
25 ml were taken for the d13DIC measurements and overfilled in a
screw-capped glass vial without any bubble formation and kept in
an icebox. The spectrophotometric method was used for the analyses
of nitrate, nitrite, and ammonia in the water (Grasshoff, 1983;
APHA, 1995). Samples for total suspended matter (TSM) were
stored in a cool box before filtration of a known volume of tidal
water on preweighed and precombusted (overnight at 450 C)
47mmWhatman GF/F filters, and subsequently dried. TSM samples
were also used for the POC and PON elemental and isotope (d13C,
d15N) determinations. For DOC and DON analyses samples where
filtered through syringe filters (cellulose-acetate membrane) and
acidified with 0.2 M H3PO4 until the pH level reduced to 2. Dissolved
organic nitrogen (DON) was calculated by subtracting dissolved
inorganic nitrogen DIN (nitrate þ nitrite þ ammonia) from
TDN and was expressed in mM.
Fresh leaves of A. marina were collected from Lothian Island (stn.
1) and Chemaguri (stn.2c). Washed samples were dried at 40 C in
an electric oven and then powdered in a Retsch Centrifugal
Grinding Mill. Surface sediments from the same locations were
sampled by a hand used PVC cores (inner diameter 7.5 cm). Samples
were then dried and powdered by a Fritsch Pulverisette. All samples
were transported to the laboratory on ice for further processing.
2.3. Analyses of elemental C, N and isotopes of suspended matter,
plant and sediment
Total carbon and nitrogen in the suspended matter, sediment
and leaf samples were analysed using Eurovector EA3000. LECO
1013 Standards were introduced every five samples in order to
control the precision of the samples. The relative standard
deviation for the C and N percentage measurement was ±0.04 and
±0.01 respectively. A Thermo Finningan Delta plus mass spectrometer
coupled with a flash EA 1112 and ConFloII interface was
used for analysing d13C and d15N of the sediment, TSM and plant
samples. All data are expressed in conventional delta (d) notation,
where the isotopic ratio of d15N/d14N is expressed relative to Air and
d13C/d12C relative to the international PDB standard as defined by:
d‰ ¼ [(Ratiosample/Ratiostandard) 1] 1000
The CO2 reference gas used is research grade and has been
calibrated to PDB using NBS22 (National Bureau of Standards) and
USGS24 (United States Geological Survey, carbon isotopes in
graphite). The N2 reference gas used is research grade and has been
calibrated to Air using IAEA-N1 and IAEA-N2 (both are coarse
grained salt of ammonium sulphate). OAS (IVA) and Pepton (Merck)
was used as working standard and reproducibility based on
duplicate analyses of a sample was ±0.13‰ for d13C and ±0.2‰ for
d15N.
2.4. DOC, DON and d13DOC measurement
DOC and TDN concentrations were determined using a Shimadzu
TOC-VCSH Analyser and NDIR detector (non-dispersive infra
red detector) calibrated against potassium hydrogen phthalate
(KHP) and potassium nitrate. The error of measurements was less
than 2%.DOC stable isotope analysis was carried out using a HPLC
system coupled to a Deltaþ XP IRMS through an LC IsoLink interface
(Thermo Fisher Scientific, Germany) (Malik et al., 2012; Scheibe
et al., 2012). Linearity of the system was ascertained using varying
concentrations (5e40 mgC L 1) of citric acid
(d13C: 18.58‰VPDB; Fluka, Germany) and pulses of CO2 reference
gas (d13C: 38.16‰ VPDB) were used for calibration of the LC-IRMS
system during every chromatographic run that lasted for 20 min.
The d13DOC values were reported as per mil relative to the PDB
standard with an overall uncertainty of ±0.10‰.
2.5. DIC and d13DIC measurement
The pCO2 and DIC were computed from pH and TA measurements
with the thermodynamic constants described by
Frankignoulle et al. (1998). The accuracy of computed DIC and pCO2
values are estimated at ±4 mmol kg 1 and ±4 ppm, respectively. For
the analysis of the d13DIC, a headspace was created which is filled
with helium and 300 mL of H3PO4 was added to convert all inorganic
carbon species to CO2. After overnight equilibration, part of
the headspace was injected into the helium stream of an elemental
analyser-isotope ratio mass spectrometer (EA-IRMS, MAT 253
coupled with gas bench II, Thermo scientific) for d13C
measurements.
3. Results
Physicochemical parameters as well as concentrations and isotopic
signatures of dissolved and particulate carbon and nitrogen of
the mangrove estuarine waters are presented in Table 1. During the
pre-monsoon, salinity varied from 1.75 to 30.9 along the Hooghly
estuary, whereas salinity in the Saptamukhi estuarine mangrove
water (Sundarbans) was generally high (26e31). The mean temperature
during the study was recorded as 31.2 ± 0.4 C. The pH in
the Hooghly estuary was lowest in the riverine zone (7.76 at stn.2a)
and increased progressively towards in the marine end of the estuary
(8.01 at stn.2c). The average pH of mangrove water was
8.03 ± 0.05. Dissolved oxygen and O2 saturation (%) along the
Hooghly salinity gradient ranged from 5.92 to 6.7 mg L 1 and
80e101% respectively and was greatest at the marine end of the
transition (stn.2c). Oxygen concentration and saturation was high
in the Saptamukhi estuarine mangrove waters (6.44e6.87 mg L 1;
103e109%) with no discernable pattern of variation. Total suspended
matter (TSM) concentration in the Hooghly and Saptamukhi
estuarine waters ranged from 60.69 to 119.35 mg L 1 and
112.2e182.7 mg L 1, respectively. POC and PON concentrations
showed a clear increasing trend along the salinity gradient of
estuarine mangrove waters ranged from 11.04 to 37.0 mM and
1.08e3.9 mM, respectively and were greatest in the Saptamukhi
estuarine waters (Table 1, Fig. 2a). The d13POC varied
between 24.4 and 23.6‰ over the salinity gradient of the
Hooghly estuary, and increased significantly in the Saptamukhi
estuary ( 22.3 to 23.0‰) (Fig. 2b). The PON concentration in the
Hooghly estuary (1.08e2.44 mM) was lower than that of the Saptamukhi
estuary (2.9e3.9 mM). In the Saptamukhi estuarine
mangrove water d15PON values increased considerably compared
to Hooghly upstream, with values ranging between 7.92‰ and
10.6‰ (Table 1). Elemental ratios (POC/PON) of suspended matter
were relatively high in both of the estuaries (mean ratio, Hooghly:
12.75 and Saptamukhi: 9.70) reflecting the contribution of riverine
and mangrove derived material in addition to phytoplankton in the
POC pool during the pre-monsoon.
The DOC concentrations of the Hooghly and Saptamukhi estuarine
waters varied over a narrow range from 245.5 to 324 mM and
260.3e328.3 mM respectively, being greatest at the marine end. In
the Hooghly estuary, DOC concentrations increased with increasing
salinities (Fig. 2c). The d13DOC increased from 25.3 to 24.3‰
along the salinity gradient of the Hooghly toward the marine end,
and values were lower ( 24.4 to 24.9‰) compared to d13POC
(Fig. 2d) in the Saptamukhi estuary. For both DON and DIN the
highest values were measured in the Hooghly estuary
(70.4 ± 34.3 mM; 20.0 ± 3.5 mM) and the lowest in the Saptamukhi
estuary (32.6 ± 10.2 mM; 15.5 ± 0.5 mM). The total alkalinity (TA)
varied over a narrow range: from 2.97 to 2.79 mmol kg 1 along the
salinity gradient of the Hooghly estuary and between 2.70 and
2.76 mmol kg 1 in the Saptamukhi estuary. The overall trend of TA
mirrored the changes in DIC, which ranged between 2.4 and
2.88 mmol kg 1 in the Hooghly estuary and 2.26 and
2.17 mmol kg 1 in the Saptamukhi estuary (Fig. 3a). The average
pCO2 values in the Hooghly estuary accounted for 785 ± 212 matm,
while the pCO2 values in the Saptamukhi estuary was
633 ± 111 matm. The pCO2 values showed a significant negative
correlation with O2 saturation (%) (R2 ¼ 0.65, p ¼ 0.003, Fig. 3b).
The d13DIC varied between 4.87‰and 1.91‰ in the Hooghly
Table 1
Spatial distribution of physicochemical, particulate and dissolved organic matter parameters in the Hooghly and Saptamukhi estuaries (mean ± standard deviation).
Water parameters Stn 1 (point I) Stn. 1 (point II) Stn. 1 (point III) Stn.2a Stn.2b Stn.2c
Saptamukhi estuary (Sundarbans) Hooghly estuary
Salinity (psu) 26 30 31 1.75 18.1 30.9
Tw ( C) 31.5 31.2 31.5 30.5 31.4 30.9
pH 8.021 7.981 8.096 7.763 7.873 8.014
DO (mg L 1) 6.67 6.87 6.44 5.92 ± 0.10 6.47 ± 0.24 6.7 ± 0.16
O2 saturation (%) 104 109 103 80 ±2 92 ± 2 101 ± 2
TSM (mg L 1) 182.74 157.34 112.2 60.69 ± 0.18 119.35 ± 11 79.46 ± 29
POC (mM) 37 27 32 11.04 ± 2.5 28.9 ± 1.66 25.8 ± 5.9
PON (mM) 3.91 3.15 2.90 1.08 ± 0.3 2.44 ± 0.05 1.76 ± 0.23
d13POC (‰) 23.0 22.5 22.3 24.1 ± 0.01 23.6 ± 0.13 24.4 ± 0.2
d15 PON (‰) 9.9 10.3 10.1 7.92 ± 0.6 9.5 ± 0.3 10.6 ± 1.2
DOC (mM) 328.2 260.3 294.3 245.5 ± 26 249 ± 25.5 324 ± 27
d13DOC 24.9 24.7 24.4 25.1 ± 0.07 24.7 ± 0.07 24.3 ± 0.1
DIN (mM) 15.15 16.04 15.6 25.25 ± 2.5 21.76 ± 1.0 17.9 ± 2.0
DON(mM) 35 41.3 21.4 60.89 ± 6.5 41.81 ± 1.2 108.46 ± 26.6
TA (mmol kg 1) 2.76 2.72 2.70 2.97 ± 0.04 2.86 ± 0.02 2.79 ± 0.01
pCO2(matm) 506 715 680 1013 ± 60 749 ± 45 592 ± 81
DIC (mmol kg 1) 2.17 2.26 2.20 2.88 ± 0.06 2.60 ± 0.01 2.40 ± 0.03
d13DIC (‰) 3.73 1.91 2.65 4.87 ± 0.2 3.62 ± 0.1 3.24 ± 0.2
4 R. Ray et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e10
Please cite this article in press as: Ray, R., et al., Distribution, sources and biogeochemistry of organic matter in a mangrove dominated estuarine
system (Indian Sundarbans) during the pre-monsoon, Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.10.017
Fig. 2. Relative distribution of POC, DOC and their isotopes with salinity.
Fig. 3. Relative distribution and correlation of DIC, isotopes and associated water parameters.
R. Ray et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e10 5
Please cite this article in press as: Ray, R., et al., Distribution, sources and biogeochemistry of organic matter in a mangrove dominated estuarine
system (Indian Sundarbans) during the pre-monsoon, Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.10.017
and Saptamukhi estuaries, with increasing gradually with salinity
(Fig. 3c). A significant inverse correlation was found between DIC
concentrations and d13DIC (R2 ¼ 0.61, p ¼ 0.004, Fig. 3d).
The mean TOC and TN values of mangrove leaves were
44.45% ± 0.25% and 1.62% ± 0.11%, respectively (Table 2) with mean
atomic [TN/TOC]ratio of 0.031 ± 0.001. The corresponding d13C
values ranged from 28.08 to 26.3‰, with a mean of
27.2 ± 1.25‰. The leaves were enriched in 15N, showing a mean
d15N value of 4.9 ± 0.93‰. The sediments showed enrichment in
d13C ( 24.5 ± 0.21‰) in contrast to the mangrove leaves
( 27.2 ± 1.2‰). The [TN/TOC] atomic ratios in the sediment varied
between 0.036 and 0.051 with d15N ranging from 3.7 to 4.64‰. The
[TN/TOC]ratios in the particulate organic matter (as phytoplankton)
were observed to be 0.094 with d13C and d15N values of 22.3‰and
10.1‰, respectively.
4. Discussions
The Hooghly estuarine water is characterized by a pronounced
salinity gradient in contrast to the Saptamukhi estuary which
showed only small salinity variations, reflecting a very limited
freshwater supply to the Saptamukhi estuary during pre-monsoon.
Temperature variations in both the estuarine surface waters were
small. Distinct differences in biogeochemical variability were
evident between these two estuaries. The Hooghly estuary had
lower pH, dissolved oxygen concentrations and oxygen saturations,
POC, PON, DOC, d13DIC, d13POC and d15PON, compared to the Saptamukhi
estuary, however higher values of pCO2, DIC, TA, DON and
DIN were recorded indicating input of local organic matter and its
microbial metabolism.
4.1. Organic carbon and nitrogen in plants, sediments and
suspended matter
TOC in the sediment of Lothian Island and Chemaguri mangrove
was lower in comparison with that of the south west coast of India
(mean 2.10%, Gireeshkumar et al., 2013). The significantly lower
[TN/TOC] ratios of these mangrove sediment compared to the value
reported for the mangrove dominated Macouria mud bank in
French Guiana (0.07e0.11, Gontharet et al., 2014) indicates that
intense mineralization takes place in the intertidal mangrove
sediment (which is similar to the other Indo Pacific mangroves;
Donato et al., 2011). Carbon isotopes (d13C) were relatively enriched
in the surface sediments than the mangrove leaves but more
depleted than the phytoplankton in the POC pool. The lower [TN/
TOC]ratios and depleted nitrogen isotopes (d15N) recorded in the
sediments compared to the phytoplankton and leaves indicate
intense microbial degradation of mangrove derived organic matter
to CO2, CH4 and inorganic nitrogen under oxic and anoxic conditions
(Ray et al., 2013). Ehleringer et al. (2000) suggested that the
d13C enrichment in the soil organic matter compared to plant leaves
could be the result of decomposition of organic matter both by
microbial and fungal activity. However, N2 fixation by benthic
diazotrophs (Sharaki et al., 2014; Ray et al., 2014; Voss et al., 2011)
could account for the lower ranges of nitrogen isotopes (d15N)
observed in the sediments relative to mangrove leaves. The range of
d13C observed in Avicennia sp. ( 28.08 to 26.31‰) is close to the
d13C range of mangrove C3 plants ( 29.0 to 25.4‰; Kuramato and
Minagawa, 2001; Hayase et al., 1999). The senescent leaves are the
major component of mangrove litter and main source of organic
matter in mangrove soils. Gontharet et al. (2014) showed the
change of atomic [TN/TOC] ratio from 0.05 to 0.03 and d13C
from 27.6‰ to 27.0‰ in Avicennia germinans for senescent
leaves.
The particulate organic matter (POM) concentrations in the
Hooghly and Saptamukhi estuaries were consistent with results
reported for other estuaries (Zuary estuary, Bardhan et al., 2014;
Changjiang estuary, Tan et al., 1991; Yangtzhe and Yellow river estuaries,
Cauwet and Mackenzie, 1993; and nine tidal estuaries
across European coast, Middelburg and Herman, 2007). During the
pre-monsoon, high phytoplankton productivity due to increased
transparency of the water column (Biswas et al., 2004) along with
the observed mean d13C of POC and d15N of PON in the range of
phytoplankton derived organic matter indicates that POM is predominantly
of in situ origin in the Saptamukhi estuary. However
mean elemental TN/OC ratio found in POM in the riverine zone of
the Hooghly estuary (0.082 ± 0.04) was close to that of the
terrestrial OM (>0.085; Hedges et al., 1997; Lamb et al., 2006).
Furthermore mean d13C of POC ( 24.1 ± 0.01‰) and d15N of PON
(7.92 ± 0.6‰) in the riverine zone were close to the mean d13C and
d15N ratios of C3 ( 25.9 ± 1.2 and 5.1 ± 2.1‰, respectively) land
plants (Krishna et al., 2015). All these results strongly suggest that
POC and PON observed in the riverine zone of the Hooghly estuary
could face microbial degradation during their transport from the
land to the estuary.
In this study, d15N of the PON increased with increasing salinity
showing higher ranges (9.9e11.7‰) in the marine and mangrove
dominated zone (Table 1). So far there is no report on higher
d15PON values measured in POM collected from the Bay of Bengal.
Kumar et al. (2004) reported highest d15PON values of 7.6‰ both
during pre and post monsoon along the south west coast of the Bay
of Bengal and highlighted the occurrence of denitrification that
causes the remaining nitrate in the heavier 15N. We also found a
significant negative correlation between DIN and d15PON
(DIN¼ 0.21 d15PON þ 13.66, R2 ¼ 0.55, n ¼ 10 figure not shown)
which was similar to the trend observed in the Montery Bay by Rau
et al. (1998). This trend was attributed to the preferential uptake of
14N during photosynthesis of organic matter in the cause of which
d15N values in the POC increased with decreasing nitrate concentrations.
In our case the highest d15PON (11.73‰) was measured at
the marine reference site (stn. 2c) showing a DIN concentration of
17.9 ± 2.0 mM which was as high as those found in the ocean most
productive upwelling systems (Rixen et al., 2006). Since such high
nitrate concentrations exclude an enrichment of 15N caused by the
preferential uptake of the lighter 14N during plankton bloom our
results support the finding of Kumar et al. (2004). In the Hooghly
estuary the decreasing d15PON values with decreasing salinity indicates
a mixing of nitrogen that originates from mangroves
Table 2
Mean elemental (total organic carbon TOC%, total nitrogen TN%, with standard deviation) and stable isotopic (d13C‰, d15N‰) composition of sediments, Avicennia leaf and
phytoplankton at Lothian Island (stn.1) and Chemaguri (stn.2c).
Mangroves TOC TN d13C d15N TN: TOC
Surface sediment Lothian Island 0.66 ± 0.21 0.04 ± 0.001 24.65 3.7 0.051
Chemaguri 0.70 ± 0.01 0.03 ± 0.001 24.35 4.64 0.036
Avicennia leaf Lothian Island 45.9 ± 0.33 1.7 ± 0.05 26.31 5.56 0.031
Chemaguri 43.0 ± 0.20 1.54 ± 0.04 28.08 4.24 0.030
Phytoplankton Lothian Island (pt.III Coastal water) 0.20 ± 0.02 0.02 ± 0.001 22.30 10.1 0.094
6 R. Ray et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e10
Please cite this article in press as: Ray, R., et al., Distribution, sources and biogeochemistry of organic matter in a mangrove dominated estuarine
system (Indian Sundarbans) during the pre-monsoon, Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.10.017
through benthic N2 fixation and marine nitrogen input through
denitrification in the oxygen depleted subsurface waters of the
northern Bay of Bengal.
4.2. Sources of DOM
The mean DOC concentrations of 294 ± 34 mM in the Saptamukhi
estuary and 273 ± 44 mM in the Hooghly estuary were close
to that reported for Brazilian mangrove waters (360 mM, Dittmar
and Lara, 2001), but were relatively lower in comparison to the
Florida mangrovewaters (500e2000 mM, Davis et al., 2001; Romigh
et al., 2006). Since contrary to Florida, the Brazilian and the Sundarbans
are flushed by large rivers (Amazon and Hooghly) it is
assumed that the low DOC contents result from low residence
times of water in the mangroves rather than from differences in the
DOC formation and decomposition rates. However, Mukherjee and
Ray (2012) reported an annual mean DOC concentration of 450 mM
along the HooghlyeMatla estuarine system, which is higher than
our mean value (273 ± 44 mM, station 2a,b,c) and indicates seasonal
effects. Nevertheless, the mean DOC concentration in our studywas
10 times higher than POC (around 30 mM) that is also consistent
with observations by other authors (Bouillon et al., 2003;
Kristenson and Suraswadi, 2002). The difference between the
Saptamukhi and the Hooghly estuary with respect to the d13DOC
was insignificant with a mean of 24.7‰which is consistent to the
values reported by other authors (Wafar et al., 1997; Dittmar et al.,
2001). In Fig. 4, the scattered plot between d13C versus atomic [TN/
TOC] ratio confirms the similarity of DOM composition with that
from riverine transport. However, standard deviation of DOM indicates
that considerable fraction of DOM could also be derived
from the mangrove sediment in addition by the processes of litter
leaching in the upper layer during tidal flushing and tidal pumping
from deeper layers. Dutta et al. (2015) reported that the average
pore water specific discharge was 90 times higher in the Sundarbans
than the value reported for silty clay sediment in Southern
Chesapeake Bay due to bioturbation by burrowing crab species and
further concluded that DOM could be transported by advective
fluxes from the sediment column (pore water) into the estuarine
water. Due to mixing of different sources and probably varying
degrees of decomposition a significant correlation between C and N
in the dissolved form could not be found (R2 ¼ 0.18, figure not
shown). However, DON having average concentration of 51.2 mM
contributed 73% to the total dissolved nitrogen (DON and DIN) and
70% to the total nitrogen (PON þ DON þ DIN) showing that it was
the major form of nitrogen in both estuaries. This implies furthermore
that leaf litter leaching could be the most important loss term
for nitrogen in mangroves. Except for the most offshore site in the
Hooghly estuary, DIN correlated positively with DON suggesting
that DIN concentrations were influenced by the decomposition of
DON that was leached from leaf litter. The negative correlation
between DIN and PON in turn indicates the uptake of DIN by
phytoplankton, which, as discussed before, composes to a large
extent of POM.
4.3. Sources of DIC
Considerable spatial variations of DIC and ancillary parameters
were found to occur with salinity changes. Highest DIC concentration
(2.88 ± 0.06 mmol kg 1)was observed in the riverine part of
Hooghly estuary with bicarbonate as the dominant species. The
d13C of DIC was relatively depleted in heavier 13C compared to the
ocean waters and further depleted (around 4.2‰) with
decreasing salinity along the Hooghly estuary. This relative depletion
of d13C-DIC along the Hooghly upstream coincided with the
significantly higher DIC and pCO2 concentrations and lower O2
saturation and pH. This indicates respiration of DOM supporting
the heterotrophy and implying that river outgassing is part of the
ecosystem respiration (Sarma et al., 2012, Biswas et al., 2004).
However, enrichment of d13C-DIC pool in both marine and
mangrove water corresponds to the increasing influence of ocean
waters into the system and enhanced uptake of DIC during
phytoplankton production in the saline mangrove water system
(Middelburg and Nieuwenhuize, 1998). In our study, relatively
higher d13C-DIC in the Saptamukhi estuary was associated with
higher concentrations of POC attributing to the planktonic uptake
of CO2 during photosynthesis. Therefore, during premonsoon, DIC
chemistry along the Hooghly upstream was governed by the
metabolic conversion of DOM to DIC causing heterotrophy and
increasing surface pCO2 while the Sundarbanswas primarily driven
by the phytoplankton productivity.
4.4. Three end-member model
Assuming that diagenetic reactions do not significantly alter the
OM, [TN/TOC] ratios and d13C values, following three end-member
mixing equations were used based on these values and mass balance
(Gontharet et al., 2014):
[TN/TOC]POC/sediment ¼ fMangrove [TN/TOC]Mangrove þ fPhytoplankton
[TN/TOC]Phytoplankton þ fPOC(Riveine)
[TN/TOC]POC(Riverine) (1)
d13CPOC/sediment ¼ fMangrove d13CMangrove þ fPhytoplankton
d13CPhytoplankton þ fPOC(Riverine)
d13CPOC(Riverine) (2)
1 ¼ fMangrove þ fPhytoplankton þ fPOC(Riverine) (3)
with mangrove end-member ([TN/TOC]Mangrove ¼ 0.037;
d13CMangrove ¼ 28.4‰), phytoplankton end-member ([TN/
TOC]Phytoplankton ¼ 0.11; d13CPhytoplankton ¼ 22.3‰) and
riverine particulate organic carbon (POC) end-member ([TN/
TOC]POC(Riverine) ¼ 0.098; d13CPOC(Riverine) ¼ 24.1‰); [TN/
TOC]POC/sediment and d13CPOC/sediment are the measured atomic
elemental ratio and the stable carbon isotopic composition of a
given POC/sediment sample, respectively; fMangrove, fPhytoplankton and
fPOC(Riverine) represent the relative fraction of each of these OM sources.
The POC collected from Diamond Harbour (stn.2a) were used as
riverine end member value, while POC collected from the
Fig. 4. Mixing plot between mean d13C and TN/TOC (±SD) of mangrove Leaf, Sediments,
dissolved organic matter (DOM), Riverine POC and Phytoplankton (Phyto).
R. Ray et al. / Estuarine, Coastal and Shelf Science xxx (2015) 1e10 7
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system (Indian Sundarbans) during the pre-monsoon, Estuarine, Coastal and Shelf Science (2015), http://dx.doi.org/10.1016/j.ecss.2015.10.017
Saptamukhi (point II and III) were considered as phytoplankton.
Hence to maintain maximum differences in d13C between the end
members, minimum value of d13C ( 28.4‰) for mangrove leaf (Avicennia
marina) was considered in the model.
The relationships between the [TN/TOC] ratios, the d13C values
of the three potential OM sources (A. marina leaves, riverine POC
and phytoplankton) and the typical ranges of these markers are
given in Fig. 5. The magnitude of [TN/TOC] ratios and d13C for these
three OM sources are found in the decreasing order:
Phytoplankton > Riverine > Leaf (Table 2, Fig. 5) and they are
considered as three different end-member components of the POC
and sedimentary OM. The calculated relative percentages of OM
contribution varied between 0 and 65.3% for mangrove leaves,
between 0 and 91.7% for riverine and between 0 and 89.9% for
phytoplankton. Sediments exhibited the predominance of OM
originating from mangrove leaves (~100%). The relative contributions
of these three OM sources were significantly different to each
site.
The contribution of riverine POC was 0e7.27% at stn.1, in
contrast to the stn.2b and 2c where it varied between 83.0e91.7%
and 0e87.5%, respectively. The increase in the contribution of
phytoplankton from mixing zone (2.44e17%, stn.2b) to the Sundarbans
mangroves (67.0e90%, stn.1) was linked to enhanced
phytoplankton production associated with the improvement of
transparency of the water column. There was an increase in the
contribution of mangrove derived material at stn.1 (2.85e33.0%)
and stn.2c relative to stn.2b (0e5.89%) due to the occurrences of
mangroves in the study area. The observed compositions of POC fell
within the domain defined by the three end member or very close
to the domain such that the differences were within the uncertainty
range. The sediments composition was found outside of the
angular domain defined by the three end members. The model
showed negative values except mangrove leaf end member. Such
conditions could arise due to the modification of leaf organic
matter by biogeochemical processes occurring in the mangrove
sediment. The mean atomic [TN/TOC]ratio (0.041 ± 0.011) in the
sediment was similar in magnitude with that of leaves (0.037) but
varied in isotopes (d13C ¼ 24.36 ± 1.01) which increased by 14.6%
compared to the leaves (d13C ¼ 27.19‰). Gontharet et al. (2014)
suggested that extensive remineralization of labile organic matter
and its conversion to more refractory organic matter could result in
higher d13C values ( 23.4‰ to 24.9‰) in the French Guiana mud
bank colonized by A. germinans. Organic carbon content
(0.64e0.79%) in the Sundarbans mangrove sediment was significantly
lower than that of Indo-Pacific mangroves (1.7e18%, Donato
et al., 2011) indicating its rapid turnover and resulting in an export
of CO2 (8.36 mg C m 2 s 1, Ray et al., 2013) from sediment to the
atmosphere, which is similar to that found in other mangroves
(Leopold et al., 2015; Lovelock et al., 2014; Chen et al., 2012, 2014).
5. Conclusion
This is the first time study where isotopic compositions of
organic/inorganic C and N were used to discriminate material
sources and to understand their origin and mixing in the riverine
and mangrove (the Sundarbans) dominated estuarine system along
the Bay of Bengal. During premonsoon, average DOC concentration
was about ten times greater than the mean POC concentrations and
considerable fraction of DOC was derived from mangrove sediment
and riverine transport. DON was the predominant form of nitrogen
and the elemental ratio, d13C of POC and d15N of PON in the riverine
zone were close to those of mangrove leaf litter. POC in the Sundarbans
was dominated by phytoplankton which growth was sustained
by nitrate that originated from the decomposition of
mangrove derived DON and nitrate imported from the Bay of
Bengal. Decomposition of mangrove derived organic matter
controlled the variation of DIC along the riverine and mixing zone
of the Hooghly estuary while phytoplankton production dominated
the DIC chemistry in the Sundarbans. In order to understand
possible sources of organic matter and its preservation in the
sediments a three end-member model was used. The obtained
results demonstrated that POCwas sourced from riverine transport,
phytoplankton and mangrove leaf litter and that the relative contributions
of these three sources to the total POM were 0e91.7%,
0e89.9%, 0e65.3% respectively along the estuaries. On the other
hand, extensive remineralization and transformation of organic
matter in the mangrove sediment resulted in significant deviation
from the composition of three end-member sources which further
coincided with low organic carbon percentages in the world's
largest mangrove delta.
Acknowledgements
Our first author (RR) is indebted to Leibniz-DAAD for providing
the postdoctoral fellowship funding (Sanction no. A/13/93589).
Thanks are also due to our boatman, helpers and field partners
especially Mr. Polas Gon for their continuous assistance during the
field trip. The authors are particularly thankful to Ulrike Machulik,
Institute of Geology/Biogeochemistry, University of Hamburg, for
analyzing the DOC and DON part of the water samples. The authors
are cordially grateful to our ZMT colleagues, in particular Dorothee
Dasbach for helping during IRMS analysis. We are highly indebted
to Dr. Sally Little, School of Animal Rural & Environmental Sciences,
Nottingham Trent University, UK, for improving the English language
and checking the manuscript. Finally authors are thankful to
the Associate Editor, Dr. Tim Jennerjahn and two anonymous reviewers
for their thoughtful and constructive comments.
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