Estuaries and Coasts (2017) 40:447456
DOI 10.1007/s12237-016-0147-4
Carbon Uptake Rates in the Cochin Estuary and Adjoining
Coastal Arabian Sea
P. S. Bhavya 1 & Sanjeev Kumar 1 & G. V. M. Gupta 2 & V. Sudheesh 2,3
Received: 18 November 2015 / Revised: 28 July 2016 / Accepted: 3 August 2016 / Published online: 22 August 2016
# Coastal and Estuarine Research Federation 2016
Abstract Carbon uptake rates in a tropical eutrophic estuary
(Cochin estuary) and the adjacent coastal Arabian Sea were
measured for the first time using 13C-NaHCO3 labeling tech-
nique. The rates in the estuarine water (pre-monsoon 3.0
20.4; monsoon 2.5512.4; post-monsoon 3.116.3 mol C
l1 h1) were significantly higher than the coastal locations
(pre-monsoon 0.020.1; monsoon 0.133.1; post-monsoon
0.0070.032 mol C l1 h1). The measured primary produc-
tivity in the estuary was relatively higher at mesohaline loca-
tions influenced with lateral inputs and TN:TP close to the
Redfield ratio (16:1). It suggests that in nutrient replete trop-
ical systems, TN:TP plays a major role in controlling the pri-
mary productivity rates. The primary productivity data from
the coastal Arabian Sea suggests the effect of estuarine dis-
charge on the carbon uptake rate at nearshore regions and
ability of anthropogenic inputs to modulate the coastal
biogeochemistry.
Keywords Estuary . Carbon . Nitrogen . Coastal .
Eutrophication
Communicated by Alberto Vieira Borges
* P. S. Bhavya
bhavya@prl.res.in
* Sanjeev Kumar
sanjeev@prl.res.in
1
Physical Research Laboratory, Ahmedabad, Navrangpura, India
2
Centre for Marine Living Resources and Ecology, Ministry of Earth
Sciences, Kendriya Bhavan, Cochin, Kakkanad, India
3
School of Marine Sciences, Cochin University of Science and
Technology, Fine Arts Avenue, Cochin, India
Introduction
Estuarine and coastal systems are highly susceptible to anthro-
pogenic modulations. One of the direct aftermaths of anthro-
pogenic activities is the excess nutrient loads to the nearby
aquatic systems such as estuaries. Along with the nutrients,
loading of terrestrial organic matter (TOM) would also cause
alterations in the biogeochemical balance of the estuaries and
subsequently the coastal waters adjacent to it. These nutrients
enter the estuarine and coastal system in the form of organic
and inorganic nitrogen (N) and phosphorus (P) through rivers
and atmosphere, jeopardizing the ecosystem (Galloway et al.
2004). Consequently, these ecosystems sustain high primary
productivity and elevated heterotrophy, which has been
discussed in many previous works (e.g., Mulholland et al.
2003; Gupta et al. 2009; Sarma et al. 2009; Bhavya et al.
2016a, b). However, the potential primary productivity in
aquatic systems is greatly controlled by numerous factors.
Apart from physicochemical parameters such as light in-
tensity, temperature, and salinity, potential primary productiv-
ity substantially depends upon the availability of nutrients
(Mulholland and Bernhardt 2005; Thomas et al. 2012).
Recent studies reported that the imbalances in the relative
availability of N and P due to variations in the nutrient loading
can also be a major factor in controlling the potential primary
productivity (Arrigo 2005; Bhavya et al. 2016a, b). Ambient
N:P ratios also have the potential to tune the autotrophs di-
versity and harmful algal bloom developments (Hodgkiss and
Ho 1997).
Primary production along the continental margins is tightly
linked to estuarine effluences and biogeochemical processes
such as oceanatmosphere CO2 exchange, upwelling, and
ground water discharge (Bhavya et al. 2016a, b; Gupta et al.
2016). Therefore, primary production in the coastal waters
adjacent to estuarine systems is subjected to consequences of
448
anthropogenic loading. However, it remains a challenge to
quantify the influence of terrestrial chemical loading on vari-
ous coastal ecosystems, especially tropical systems (Eyre and
Balls 1999; Cloern 2001; Gupta et al. 2016). The influence of
other nutrient sources and sinks such as the atmosphere and
adjacent ocean (Smith 1984; Eyre and France 1997; Smith and
Hollibaugh 1997) also leads to complexity in the coastal
ocean biogeochemistry.
Another major concern about the estuarine-coastal
coupled systems is the changes in ecosystem metabolism
in response to eutrophication (Hoch and Kirchman 1995;
Frankignoulle et al. 1998; Gattuso et al. 1998; Bricker
et al. 1999; Middelburg and Nieuwenhuize 2000a, b;
Mulholland et al. 2003; Borges and Abril 2011; Cloern
et al. 2014). Intensive autotrophic as well as heterotrophic
activities have been observed in such ecosystems, which
ultimately promote microbial respiration leading to in-
crease in CO2,aq levels (Fasham 2003; Gupta et al. 2008,
2009; Borges et al. 2006). However, CO2 production and
O2 consumption in estuaries have also been observed due
to autotrophic nitrification (Ebeling et al. 2006). Studies
through culture experiments have pointed out that in-
crease in CO2 levels would not affect the total oceanic
primary productivity (e.g, Burkhardt et al. 2001).
However, influence of high pCO2 on primary productivity
in CO2 supersaturated estuaries has not been investigated
in detail. Present study attempted to measure primary pro-
ductivity in a CO2 supersaturated estuary, the Cochin es-
tuary, using 13C-NaHCO3 labeling technique. The study
was also extended to the adjacent coastal Arabian Sea to
understand the influences of estuarine inputs.
It is highly important to understand the flow of N and C in
these ecosystems to access the level of biogeochemical alter-
ations induced by human influences. Further, extended studies
are required at regional and global scales to construct mitiga-
tion strategies to avoid deterioration of these valuable re-
sources. Extensive studies have been carried out in coastal
and estuarine regions around the world including India
(Middelburg and Nieuwenhuize 2000a, b; Mulholland et al.
2003; Cloern et al. 2014; Gupta et al. 2008; Sarma et al. 2009,
2010, 2011, 2012, 2014; Rao and Sarma 2013). However,
limited studies exist vis--vis N and C assimilation rates in
Indian estuarine and coastal systems. One such important re-
gion is the Cochin estuary, located in southwest coast of India.
The Cochin estuary is a biogeochemical hot spot due to high
inputs of nutrients (Martin et al. 2008) which sustain elevated
rates of primary productivity and also supersaturated with
CO2 due to high rates of respiration and mineralization
(Thottathil et al. 2008; Gupta et al. 2009). Apart from in situ
sources, these studies have also emphasized the importance of
rivers and ground water as sources of CO2. Cochin estuary is a
monsoonal estuary where seasonally driven rainfall and asso-
ciated runoff (Qasim 2003) plays a dramatic role in the overall
Estuaries and Coasts (2017) 40:447456
functioning of the trophic food web and cycling of various
elements (Jyothibabu et al. 2006; Madhu et al. 2007). The
amount of inorganic nutrients discharge in the form of untreat-
ed industrial (0.104 10 6 m 3 d 1 ) and domestic
(0.26 103 m3 d1) effluents in to the estuary has remarkably
increased over the last three decades (KSPCB 1986; Martin
et al. 2008). Such nutrient inputs have led to extremely pol-
luted condition (Miranda et al. 2008) in the Cochin estuary by
altering the nutrient ratios (Martin et al. 2008) and elevated
levels of TOM (Thottathil et al. 2008; Gupta et al. 2009;
Bhavya et al. 2016a, b).
Even though several works focused on physicochemical
(Sankaranarayanan and Qasim 1969; Srinivas et al. 2003)
and biological characteristics (Menon et al. 2000; Qasim
2003; Gupta et al. 2009; Bhavya et al. 2016a) have been
carried out in the Cochin estuary, no studies have been report-
ed with direct measurements of C uptake rates so far. Recent
studies have reported that the coastal waters of Cochin estuary
suffer from eutrophication due to the anthropogenic nutrient
loading (Bhavya et al. 2016a; Gupta et al. 2016). Taking all
these factors together, the Cochin estuary and adjacent coastal
waters were subjected for a detailed primary productivity mea-
surement using 13C-NaHCO3 labeling technique. The main
objectives of the present study were to (1) estimate 13C based
primary productivity in tropical estuarine-coastal coupled sys-
tem, (2) understand the influence of TN:TP ratio on primary
productivity, and (3) examine the influence of estuarine efflu-
ences on the coastal primary productivity.
Material and Methods
The carbon uptake rates were measured using 13C-NaHCO3
technique across salinity gradient in the Cochin estuary, dur-
ing three different seasons of 2012 (pre-monsoon, 26th April
1st May; monsoon, 16th20th September; post-monsoon,
30th December2nd January; Fig. 1). The details of the estu-
arine stations sampled are summarized in Table 1. Seasonal
coastal surveys were conducted onboard FORV Sagar
Sampada prior to each estuarine sampling (12th20th April,
1st9th September, and 8th14th December 2012) along the
two coastal transects in the southeastern Arabian Sea (Fig. 1b)
viz. off Cochin (~10 N) and off Mangalore (12.8 N). The
stations (water column depths 13, 30, 50, and 100 m) and
depths of in situ incubations conducted along the coastal tran-
sects are provided in Table 2. During monsoon, the sampling
depths were limited to 20 m due to practical difficulty in
mooring under the hostile sea. The corresponding water col-
umn depth stations obtained at off Mangalore transect were
further away from the coast due to gentler slope of the conti-
nental shelf. For the convenience of discussion, the coastal
stations were classified into nearshore, inner shelf, mid-shelf,
and outer shelf, respectively.
Estuaries and Coasts (2017) 40:447456 449

Fig. 1 Sampling locations within Cochin estuary (numbers 15). Station 6 is in freshwater Vembanad Lake (6aupper star and 6b lower star). TB is
Thannermukkam dam between Cochin estuary and Vembanad Lake. The dots in (b) indicate the stations in coastal Arabian Sea

Environmental Parameters
Data for temperature and salinity during the study periods
were collected using Sea-Bird CTD profiler (model 911 plus
for coastal and model SBE 25 for the Cochin estuary).
Inorganic nutrients viz. NH4+, NO3 dissolved inorganic
phosphorous (DIP), and Si were analyzed spectrophotometri-
cally using standard methods (Grasshoff et al. 1999). Total
phosphorus (TP) and total nitrogen (TN) were measured using
persulfate oxidation method (Grasshoff et al. 1999). The ana-
lytical precisions for NH4+, NO3, DIP, Si, TN, and TP were
0.07, 0.05, 0.02, 0.03, 0.11, and 0.06 M, respective-
ly. The pH and TAlk (Frankignoulle and Borges 2001) were
measured using a potentiometric titrator (907 Titrando;
Metrohm, Switzerland) calibrated on the NBS scale as de-
scribed by Frankignoulle and Borges (2001). The pH values

Table 1 The hydrobiological parameters in the Cochin estuary during the sampling

Sampling period Stn. T (C) Salinity Chl a Si NO3 NH4+ PO43 TP TN TN/TP pH DIC %CO2 C uptake rates

Pre- monsoon 2012 1 29.51 1.58 1.77 47.6 26.6 75.2 3.64 3.70 117.77 31.9 6.418 822 44.6 3.00
2 29.85 15.6 17.2 42.2 1.25 5.22 2.95 3.15 20.44 6.50 7.255 1155 6.09 9.98
3 30.12 13.0 8.06 41.1 4.97 13.7 2.68 2.80 23.11 8.24 7.325 915 5.50 6.22
4 30.57 6.27 6.44 48.5 8.65 2.11 0.51 0.78 14.22 18.1 6.920 583 15.5 4.76
5 29.09 5.31 2.53 70.9 5.20 4.36 0.30 0.38 10.67 27.9 6.402 357 39.1 5.67
6.a 29.39 0.26 12.3 112 25.4 5.02 0.54 0.80 37.33 46.4 6.030 1004 71.2 20.4
Monsoon 2012 1 27.21 0.12 3.31 58.0 16.8 25.2 1.11 1.86 46.0 24.8 6.278 1191 59.98 2.55
2 28.90 1.60 2.76 144 0.73 0.39 3.13 3.83 8.83 2.30 7.275 855 10.08 7.73
3 28.51 5.36 3.05 110 12.9 5.51 2.11 2.86 24.7 8.64 7.192 623 9.45 2.57
4 29.90 0.02 5.05 102 8.37 4.22 2.50 2.83 21.5 7.58 6.629 647 41.32 8.77
5 29.71 0.07 6.74 40.3 4.71 4.36 0.33 0.81 14.8 18.2 5.906 1301 78.10 12.4
6.a 29.74 0.04 1.67 80.7 11.3 0.10 0.26 0.33 18.2 55.1 5.782 1632 82.87 8.71
6.b 29.73 0.04 7.76 83.3 5.01 2.84 0.61 1.28 22.2 17.3 6.112 1216 69.36 12.3
Post-monsoon 2012 1 28.46 12.9 21.7 47.4 4.20 2.11 0.73 1.36 20.3 14.9 7.547 915 5.85 16.3
2 28.89 20.5 26.8 42.4 0.09 1.59 1.27 2.58 25.3 9.80 7.635 1154 4.07 8.03
3 28.96 32.1 5.53 37.2 1.05 2.99 0.49 0.78 21.5 27.5 8.058 1567 0.91 3.10
4 29.61 18.5 22.4 29.7 1.13 2.13 1.29 1.93 27.3 14.1 7.527 959 2.26 9.77
5 30.03 11.1 5.30 36.6 1.74 3.21 1.79 2.44 17.3 7.08 7.364 511 14.02 4.04
6.a 29.80 1.92 13.6 76.4 2.05 2.18 0.44 0.59 20.0 34.0 6.466 403 40.97 3.81
6.b 29.61 1.89 11.2 79.6 2.44 2.29 0.34 0.60 27.1 45.4 6.414 473 44.00 4.34

The units of Si, NO3 , NH4+ , PO4+ , TP, TN, and DIC are in M; Chl a is in gl1 , and C uptake rates are in mol C l1 h1
 450

Table 2 The hydrobiological parameters in the coastal Arabian Sea during the year 2012

Sample Geographical Station Distance from the Sampling Chl a NO3 NH4+ PO43 Chl a NO3 NH4+ PO43 Chl a NO3 NH4+ PO43
code coordinates depth (m) coast (km) depth (m) (g l1) (M) (M) (M) (g l1) (M) (M) (M) (g l1) (M) (M) (M)

Cochin (CH) Pre-monsoon, 2012 Monsoon, 2012 Post-monsoon, 2012

CH10 09.58 N, 76.08 E 13 10.69 0 2.60 0.89 1.94 0.24 9.50 1.84 4.00 0.43 1.91 0.57 1.46 0.17
CH20 09.58 N, 75.59 E 30 25.13 0 0.11 0.05 0.22 0.50 5.61 0.41 0.27 0.10 0.19 0.14 0.08 0.38
CH210 10 0.22 0.09 0.24 0.18 2.21 11.2 0.53 1.13 0.25 0.25 BDL 0.31
CH220 25 0.45 0.09 0.22 0.55 0.72 13.3 0.03 1.18 0.43 0.31 0.26 0.67
CH30 09.97 N,75.84 E 50 44.29 0 0.24 0.13 1.73 0.22 1.39 0.35 2.81 0.36 0.15 0.33 BDL 0.11
CH310 10 0.21 0.07 1.51 0.23 3.15 2.81 1.08 0.46 0.14 0.36 BDL 0.11
CH320 20 0.31 0.20 1.47 0.23 4.33 19.7 0.73 0.95 0.18 0.42 BDL 0.13
CH340 40 2.05 5.77 1.67 0.47 0.13 22.6 1.21 1.71 0.21 1.17 BDL 0.15
CH40 09.58 N,75.39 E 100 65.99 0 0.11 0.06 0.41 0.11 0.40 0.15 0.35 0.27 0.13 0.23 0.48 0.13
CH410 10 0.10 0.06 0.87 0.17 0.38 0.25 0.54 0.27 0.13 0.09 0.73 0.20
CH420 20 0.13 0.15 0.76 0.08 0.73 11.2 0.41 0.91 0.15 0.19 0.45 0.22
CH440 40 NS NS NS NS NS NS NS NS 0.16 0.21 0.62 0.18
CH450 50 0.28 3.98 1.28 0.53 NS NS NS NS NS NS NS NS
CH475 75 0.16 13.7 0.68 1.23 NS NS NS NS NS NS NS NS
Mangalore (MR) Pre-monsoon, 2012 Monsoon, 2012 Post-monsoon, 2012
MR10 12.50 N, 74.50 E 13 12 0 2.31 0.24 0.92 0.40 4.79 0.09 2.97 0.40 7.10 1.71 0.89 0.63
MR20 12.84 N, 74.67 E 30 16.3 0 NS NS NS NS 1.26 0.29 2.01 0.21 0.37 0.59 0.37 0.18
MR210 10 NS NS NS NS 20.3 12.6 0.06 0.21 0.32 0.43 0.28 0.20
MR220 20 NS NS NS NS 2.49 0.49 4.37 0.24 0.68 1.91 0.94 0.53
MR20 12.50 N, 74.29 E 50 36.59 0 0.08 0.04 1.69 0.05 0.62 0.27 0.62 0.05 0.27 0.17 0.09 0.11
MR210 10 0.11 0.08 0.57 0.06 11.2 16.2 0.75 0.06 0.26 0.01 BDL 0.11
MR220 20 0.14 0.03 0.26 0.05 0.82 20.4 0.83 0.05 0.43 0.08 BDL 0.13
MR240 40 0.14 0.05 4.89 0.09 NS NS NS NS NS 2.82 0.08 0.47
MR30 12.85 N, 74.16 E 100 72.39 0 0.15 0.11 1.53 0.03 0.67 0.97 0.64 0.03 0.14 0.06 0.05 0.11
MR310 10 0.11 0.11 1.19 0.05 0.40 3.48 1.20 0.05 0.17 0.04 0.14 0.15
MR320 20 0.11 0.07 0.75 0.09 0.35 20.1 1.05 0.09 0.18 0.01 0.09 0.22
MR340 40 0.06 0.14 1.06 0.12 NS NS NS NS 0.24 0.63 NS 0.42
MR360 60 NS 3.30 0.56 0.49 NS NS NS NS 0.18 NS NS NS

NS not sampled, BDL Below detection limit

Estuaries and Coasts (2017) 40:447456
Estuaries and Coasts (2017) 40:447456
on NBS scale were first converted to the pH in situ and then to
total scale. Analytical precision of pH for freshwater samples
was 0.008 and for the rest 0.005. The accuracy of TAlk was
within 1 %. The dissolved inorganic carbon (DIC) concen-
trations and pCO2 were computed using measured tempera-
ture, salinity, TAlk, pH, and nutrients (P and Si) using the
carbonic acid dissociation constants for the whole range of
salinity derived by Millero et al. (2006) using the CO2SYS
program (Lewis et al. 1998). Precision of pCO2 was 9
13 atm. However, based on the recent studies of Abril et al.
(2015), the error in pCO2 for low pH and TAlk samples, es-
pecially during pre-monsoon and monsoon, would be much
higher. Chlorophyll a (Chl a) concentrations were measured
fluorometrically following 90 % acetone extraction
(Grasshoff et al. 1999).
Carbon Uptake Rates
For carbon uptake experiments, water samples (coastal 1 l and
estuary 0.5 l) were collected in duplicate in polycarbonate
Nalgene bottles, spiked with 98+ atom% enriched 13C-
NaHCO3 prepared in deionized water (MilliQ). Less than
100 l and <1 ml of 0.2 mmol/ml tracer solutions were added
for estuarine and coastal samples respectively, which was
equivalent to <10 % of ambient DIC concentrations.
Immediately after addition of 13C-tracer, samples were incu-
bated in situ for 4 h (approximately symmetrical to the local
noon). Post-incubation samples were filtered onto Whatman
GF/F filters (pre-combusted at 450 C) and oven dried at
50 C overnight. Prior to the isotopic analysis, samples were
acidified overnight using concentrated HCl to remove inor-
ganic carbon content and further dried at 50 C. The mass
spectrometric analyses of samples were performed using a con-
tinuous flow isotope ratio mass spectrometer (Delta V Plus) con-
nected to an elemental analyzer (Flash EA 2000) where 13C
atom% and particulate organic carbon (POC) content were mea-
sured. IAEA-CH3-cellulose (13C = 24.724 ) was used as a
standard for both isotopic composition and POC concentrations.
The POC concentration in the samples was obtained from a liner
fit equation (R2 > 0.99), where x axis is area (area under the curve
in the chromatogram) and y axis is POC concentration of the
standard. The uptake rates were calculated using following equa-
tion (Slawyk et al. 1977):


Uptake rate molC l1 h1
.h h . ii
P*Ip T * I0 S a Ir S t S a S t I0
Where, P is the POC content in the sample, Ip is the
increase in 13C atom% in POC during incubation, Sa and St
are ambient and added tracer concentrations, respectively, Ir
and I0 are 13C atom% of added tracer and natural 13C atom%,
and T is the incubation time.
451
Results and Discussion
Primary Productivity in the Cochin Estuary
In general, the Cochin estuary showed high rates of carbon
fixation with significant seasonal variations (pre-monsoon
3.020.4; monsoon 2.5512.4; post-monsoon 3.10
16.3 mol C l1 h1; Fig. 2). The rates observed during the
present study are comparable with previous studies using di-
rect and indirect methods in this and other estuaries around the
world (e.g., Gupta et al. 2009; Cloern et al. 2014). Like the
Cochin estuary, majority of the estuaries subjected to anthro-
pogenic activities tend to exhibit high primary productivity,
heterotrophy, and high CO2,aq concentrations (Cloern et al.
2014). The observed C uptake rates in the Cochin estuary
are significantly higher (Fig. 2) compared to nearby coastal
Arabian Sea (Gandhi et al. 2011). The higher C uptake rates in
the estuary might be due to the enriched nutrient concentra-
tions (Martin et al. 2008; Thottathil et al. 2008; Glibert and
Alexander 2011) which are necessary for sustained primary
productivity.
Since the Cochin estuary is a tropical estuary, the temper-
ature control on primary productivity is negligible due to nar-
row spread of the annual surface temperature (2830 C). The
salinity in the Cochin estuary was highly dynamic due to
interplay of freshwaters and tidal intrusion of sea waters
(Table 1). Accordingly, wet periods (pre-monsoon and
monsoon) recorded very low salinity values while post-
monsoon being a dry season registered saline conditions.
The Si distribution in the estuary showed an inverse relation-
ship with salinity (Fig. 3a) indicating its main loading through
rivers. NO3 also exhibited a declining pattern with increase in
salinity (Fig. 3c). However, PO43 and NH4+ did not show
such consistent pattern like Si, but the highest concentrations
observed in the estuary were mostly associated with
mesohaline regions (Fig. 3b, d). The Chl a and C uptake rate
distributions showed that mesohaline regions are active bio-
logical sites in terms of high plankton biomass and primary
productivity (Fig. 3e, f) as these regions receive high lateral
inputs (Thottathil et al. 2008; Gupta et al. 2009).
Even though microbes in the estuary are adapted to fluctu-
ating salinity range, there are direct and indirect influences of
freshwater inputs, such as nutrient stoichiometry imbalance,
increased pCO2 levels, fluctuating pH, etc. (Gupta et al. 2009).
Results from the present study did not show any significant
relationship of C uptake rates with pH and pCO2 (figure not
shown). Significant positive correlation was observed be-
tween C uptake rates and Chl a concentrations during pre-
monsoon (R2 = 0.85; p = 0.02), which weakened during mon-
soon (R2 = 0.66; p = 0.09) and post-monsoon (R2 = 0.50;
p = 0.18; Fig. 4). Chl a normalized primary productivity did
not show any correlation with DIC concentrations (figure not
shown).
452 Estuaries and Coasts (2017) 40:447456

Fig. 2 Carbon uptake rates in the Cochin estuary during three seasons
Fig. 4 The variation in C uptake rates with Chl a concentrations during
(pre-monsoon, monsoon, and post-monsoon)
the pre-monsoon, monsoon, and post-monsoon seasons in the Cochin
estuary

Fig. 3 Relationship of various

estuarine parameters with salinity
during three seasons
Estuaries and Coasts (2017) 40:447456
It has been observed that the relative abundance of N and P
is the major factor which controls the N uptake mechanism in
this estuary, rather than the individual nutrient concentrations
(Bhavya et al. 2016a). The N assimilation rates in the culture
experiments on Prorocentrum donghaiense showed maxi-
mum values near Redfield ratio and lower values otherwise
(Glibert and Alexander 2011). In general, autotrophs prefer a
balanced N:P (16:1), where in the Cochin estuary (including
Vembanad Lake), TN:TP varied between 2.30 and 55.07
(21 15). In agreement with the previous observations, Chl
a and C uptake rates during the present study also peaked up
close to the Redfield ratio (Fig. 5).
Primary Productivity in the Coastal Waters
Unlike the estuary, the influence of TN:TP on primary pro-
ductivity was not significantly evident in oceanic waters
(Figure not shown). The exchange between the estuary and
ocean was clearly reflected in many of the hydrological pa-
rameters (Tables 1 and 2). The nutrient concentrations in the
nearshore stations were significantly higher than the stations
farther from the coast. During the pre-monsoon and monsoon,
the NO3 and NH4+ concentrations at the nearshore station off
Cochin were more than two-fold higher compared to that off
Mangalore (Table 2) due to influence from the Cochin estua-
rine export fluxes. However, during post-monsoon, the same
nearshore region off Mangalore exhibited 3-fold higher NO3
concentration than at off Cochin though NH4+ continued to be
high at off Cochin (Table 2).
The carbon fixation rates off Cochin during pre-monsoon
and monsoon (0.0041.08 and 0.0094.91 mol C l1 h1,
respectively) were significantly higher than that off
Mangalore (0.0040.38 and 0.0111.61 mol C l1 h1, respec-
tively), while it was opposite during post-monsoon (off Cochin
0.0070.11, off Mangalore 0.013.4 mol C l1 h1). In
Fig. 5 Variation of Chl a and C uptake rates with the TN: TP ratio in the
estuarine region
453
general, these rates are comparable with the previously reported
values from the Arabian Sea (Gandhi et al. 2011). The season-
ality of winds and hence currents enables dynamic nature to the
mixed layer in the Arabian Sea (Burkill et al. 1993). Various
studies have reported the influence of physical processes such
as upwelling and winter cooling in the Arabian Sea on enhance-
ment of its primary productivity (Madhupratap et al. 1996). The
present study reports the depth-wise variations in primary pro-
ductivity over different seasons in the coastal Arabian Sea
(Fig. 6). During monsoon, primary production is known to be
the strongest contributor to the standing C stock in the coastal
Arabian Sea (Barber et al. 2001). Significantly, high primary
productivity was observed in the Cochin transect during the
monsoon compared to the pre- and post-monsoon (Fig. 6).
The distribution of C uptake rates (Fig. 6) showed season-
ality in primary productivity and influence of upwelling. The
upwelling in the Indian Ocean generally initiates during early
March near the equator and progresses towards the north,
where it strengthens during MayJuly. Our parallel study also
reported that the Cochin shelf followed the similar trend in its
intra-annual variability wherein nutrient replete upwelled wa-
ters entered the outer shelf during JanuaryMarch, peaked and
occupied entire shelf during summer monsoon (June
September) and withdrawn abruptly by October (Gupta et al.
2016). The signals of nutrient enrichment due to upwelling
were reflected in the bottom waters of the farthest station
(100 m) in our pre-monsoon observation (Table 2) albeit the
corresponding C uptake rates were very low (Fig. 6a) due to
light limitation at depth. Exceptionally high surface uptake
rates in the nearshore and inner shelf stations of Cochin tran-
sect during monsoon (Fig. 6b) are influenced by the extended
export fluxes from the Cochin estuary (up to ~25 km into the
sea, Gupta et al. 2016). Depleted 13C signatures of dissolved
inorganic carbon up to inner shelf during monsoon also show
the extended impact of anthropogenic discharge from Cochin
estuary to such distance (unpublished data). Despite nutrient
enrichment due to upwelling, the elevated C uptake rates dur-
ing monsoon were restricted to upper 10 m only, possibly due
to light limitation by cloud cover and light-shading effect by
high plankton biomass at surface. This is in agreement with
the prevalence of autotrophy within this shallow euphotic col-
umn and heterotrophy beyond this depth (Gupta et al. 2016).
Overall, uptake rates did not show any correlation with Chl a
albeit; they both exhibited significant subsurface maxima
(10 m) at mid-shelf station of Mangalore during monsoon
(Table 2, Fig. 6e). The post-monsoon C uptake rates were
comparable to that of pre-monsoon except nearshore station
of the Mangalore transect.
Mechanism of Carbon Uptake
A sufficient supply of CO2,aq is crucial for activation of the
main carbon-fixing enzyme in photosynthesis: ribulose-1,5-
454
Fig. 6 The depth profile of coastal carbon uptake rates at off Cochin (a, b, and c) and off Mangalore (d, e,and f) during pre-monsoon, monsoon, and
post-monsoon, respectively
bisphosphate-carboxylase/oxygenase (Rubisco). But, oceanic
DIC is comprised of <1 % of CO2,aq, about 90 % of HCO3
and about 10 % of CO32 (Zeebe and Wolf-Gladrow 2001),
and hence, the CO2,aq concentrations (1025 M) in the ocean
cannot meet the requirement of Rubisco for its half saturation
carboxylation constant (i.e., the CO2,aq concentration at which
Rubisco catalyzes chemical reactions at 50 % of its maximum
rate) which is typically at 2070 M (Neven et al. 2011). It is
CO2,aq concentration mechanism which helps autotrophs to
initiate photosynthesis by extracellular catalytic conversion
of HCO3 to CO2,aq in the presence of carbonic anhydrase
(Badger et al. 1998; Kaplan et al. 1998; Sultemeyer 1998).
However, it may be difficult to estimate the contribution of
CO2,aq and HCO3 individually to the total organic matter
production and the extent to which C uptake is affected by
changes in CO 2 , a q levels (Burkhardt et al. 2001).
Simultaneous uptake of CO2 and HCO3 in seawater by ma-
rine eukaryotic microalgae has been reported (Riebesell et al.
1993; Colman and Rotatore 1995; Rotatore et al. 1995; Korb
et al. 1997; Tortell et al. 1997; Elzenga et al. 2000; Zeebe and
Wolf-Gladrow 2001; Hopkinson et al. 2005; Neven et al.
2011).
During the present study, CO2,aq concentrations in the es-
tuary varied from 14 to 1352 M with an average of
317 391 M, ~182 % of the total DIC pool in the estuary
(Table 1). This can enhance CO2,aq uptake by suppressing the
HCO3 uptake (Kaplan et al. 1998; Sultemeyer 1998;
Burkhardt et al. 2001; Zeebe and Wolf-Gladrow 2001;
Estuaries and Coasts (2017) 40:447456
Neven et al. 2011), leading to a considerable change in the
C uptake pathway from that of oceanic one. The 13C tracer
introduced to the sample may be separated out in to three DIC
species (CO2, HCO3, and CO32) according to the pH of the
medium. The fraction of 13CO2 would be preferentially taken
over H13 CO3 for the purpose of photosynthesis. However,
the CO2 pool drawn for photosynthesis would be continuously
restored by conversion of HCO3 pool to CO2 according to
instantaneous pH of the sample. Since the restoring of CO2
fraction is possible from tracer pool of HCO3 as well as
existing natural substrate pool, the fraction of H13 CO3 con-
tributed is unknown.
Conclusions
Carbon uptake rates in the Cochin estuary, a tropical eutrophic
estuary and adjacent coastal waters were significantly higher
than that of open ocean waters. Primary production in the
Cochin estuary was found to be optimum when the TN:TP
ratio was closer to the Redfield ratio. The elevated C uptake
rates at the nearshore stations of the coastal Arabian Sea are
predominantly due to nutrient inputs through estuarine dis-
charge, which extends to large distance into the coastal sea
during high discharge periods. These findings directly point
towards the capability of anthropogenic inputs to modulate the
coastal biogeochemistry.
Estuaries and Coasts (2017) 40:447456
Acknowledgments We thank Director, CMLRE and Prof. R. Ramesh,
PRL for their support to this study. Thanks are also due to the crew and
fishing hands of the FORV Sagar Sampada. The authors PSB and VS
thank PRL and CMLRE, respectively, for financial support. Technical
discussions and field support extended by Dr. K. K. Balachandran, NIO
have greatly helped this study. This study was funded by the Ministry of
Earth Sciences and ISRO-GBP, Department of Space, Govt. of India.
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