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Spatio-temporal variation of CO2 emission from Chilika Lake, a tropical coastallagoon, on the east coast of India

Pradipta R. Muduli a,*, Vishnu Vardhan Kanuri a, R.S. Robin a, B. Charan Kumar b, Sivaji Patra a,A.V. Raman b, G. Nageswarara Rao c, B.R. Subramanian a

a ICMAM- Project Directorate, Ministry of Earth Sciences, NIOT Campus, Pallikaranai, Chennai 600 100, IndiabDepartment of Zoology, Marine Biological Laboratory, Andhra University, Visakhapatnam 530 013, IndiacDepartment of Inorganic and Analytical Chemistry, Andhra University, Visakhapatnam 530 013, India

a r t i c l e i n f o

Article history:Received 18 March 2012Accepted 21 August 2012Available online 13 September 2012

Keywords:airewater exchangesmineralizationorganic matterbiological productioncoastal waters region: IndiaOdishaChilika lagoon

a b s t r a c t

Biogeochemical Carbon cycling was studied in Asia’s largest brackish lagoon, Chilika on the east coast ofIndia. Systematic time-series observations were made at 35 hydrologically different stations over theentire lagoon. The first of these kinds of measurements reveal, inter and intra annual variability of partialpressure of CO2 (pCO2). A comparative analysis of pCO2, CO2 flux over four years (2005, 2009, 2010 and2011) showed that the northern part of the lagoon maintained the highest levels of pCO2, with maximumCO2 efflux to the atmosphere associated with peak monsoon period. The high pCO2 corresponded toa significant decrease in pH (w0.8) from the low to high flow periods. Higher bacterial abundance(1.55 � 0.28 � 109 cells L�1) and bacterial respiration (185.31 � 105.37 mg C L�1 d�1), suggested highlevels of organic carbon decomposition during the high flow period. In contrast, the southern sector wasleast affected by river discharge, with low pCO2 values and CO2 flux as in the dry period. The central partand outer channel of the lagoon had intermediate characteristics. During high flow, the airewater CO2

flux from the entire lagoon was estimated to be 31.2 mol C m�2 y�1, which was comparatively very highwith respect to the mean CO2 emission from the entire subtropical and tropical estuaries. Highest CO2

flux (65.98 mol C m�2 y�1) was observed in the northern sector, followed by the outer channel(17.61 mol C m�2 y�1), central sector (15.69 mol C m�2 y�1) and southern sector (14.44 mol C m�2 y�1).The northern part of Chilika lagoon being an important river-influenced region was responsible for thebiological transformation of organic carbon to inorganic carbon and emitting CO2 to the atmosphere.Such a sectoral approach would reveal zonal influences of CO2 within a water body along with conditionsleading to sink or a source.

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1. Introduction

The net source or sink of CO2 can act as an indicator of auto-trophic or heterotrophic nature of a water body; hence the sourcesand mechanisms of CO2 transport and transformation are amongthe most important current issues in marine and freshwaterbiogeochemistry (Smith and Hollibaugh, 1993; Kempe, 1995). Somerecent studies (Cai et al., 2006; Chen and Borges, 2009) have shownthat temperate coastal ecosystems behave as a significant sink foratmospheric CO2 (Frankignoulle et al., 2001; Chen et al., in press;Thomas et al., 2004; Borges et al., 2005), whereas tropical andsubtropical systems act as sources of CO2 (Cai et al., 2003; Ito et al.,

2005). However, the role of coastal bodies on global CO2 fluxesremains unclear due to lack of data (Borges et al., 2005; Cai et al.,2006; Chen and Borges, 2009; Laurelle et al., 2010). Among thepotential zones of CO2 efflux, lagoons are the greatest supplier ofinorganic carbon to the atmosphere (Hanson et al., 2003), eventhough smaller in size than other coastal bodies. There have beena few systematic studies on the flux of CO2 in lagoon systems(Borges et al., 2005; Koné et al., 2009). The degree of CO2 emissionis well comparablewith those of rivers (0.34 pg C y�1) and estuaries(0.32 Pg C y�1) (Cole et al., 1994). Lagoons are also known to havehigh pCO2 values in the upper regions, because of the heterotrophicrespiration of organic carbon (Frankignoulle et al., 1998; Cai et al.,1999). Thus, lagoons are the sites of terrigenous organic carbonmineralization (Jansson et al., 2000). These are potentially impor-tant conduits for carbon from terrestrial sources to the atmosphericsink of CO2 (Cai and Wang, 1998; Frankignoulle et al., 1998;

* Corresponding author.E-mail address: pr.muduli@gmail.com (P.R. Muduli).

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Raymond et al., 2000; Abril and Borges, 2004). Various factorsinfluence the CO2 flux of a coastal environment such as decompo-sition of labile organic matter, high turbidity and anthropogenicorganic matter can enhance the respiration rate and thus CO2production (Frankignoulle and Middelburg, 2002). CO2 flux alsovaries directly as a function of wind speed (Jiang et al., 2008; Hoet al., 2011), water current and depth (Borges et al., 2004).

There is a scarcity of airewater CO2 flux data in coastal envi-ronments of subtropical and tropical latitudes that receive about60% of the global freshwater discharge (Richey, 2004). The fewstudies of carbon cycling in some coastal ecosystems such aslagoons have focused solely on the ecosystem metabolism (Sidineiet al., 2001; Hung and Hung, 2003). In this context, the Indian riversand estuaries have been studied by many researchers (e.g. Sarmaet al., 2001, 2012; Mukhopadhyay et al., 2002; Gupta et al., 2008,2009). Chilika lake the largest brackish water lagoon in Asia(19�280e19�540 N: 85�060e85�350 E), was designated as a Ramsarsite in the Ramsar convention on wetlands in 1981. The only studyof Chilika lagoon in this directionwas that of Gupta et al. (2008) fortwo months, May (low flow) and August (high flow) of 2005, whichprovided a rough estimate of the budget. In order to providea holistic picture on CO2 dynamics the present study was carriedout for two years for an accurate estimation of the seasonal budget.

2. Materials and methods

2.1. Study area

Chilika lagoon is a shallow body of water (depth w1.5 m) witha linear axis of 64.3 km andmeanwidth of 20.1 km (Pattnaik, 1998).The lagoon spreads over an area of w704 km2 during summer,which swells up to w1020 km2 during the monsoon (Gupta et al.,2008). Ecologically, the shallow lagoon is a mixture of marine,brackish and freshwater ecosystems. Hydrographically the lagoonwas classified into four different sectors. Southern sector connectedwith the sea through Palur canal, Northern sector receiving themaximum discharge through rivers, Outer Channel connected with

the sea and Central sector, the mixing zone of Northern sector andOuter channel (Fig. 1).

2.2. Field sampling and analysis

Sub-surface water samples (w0.2 m) were collected using a 5 LNiskin water sampler from the lagoon on a monthly basis in theyear 2009 and 2010 to measure all the desired parameters. Someselected parameters were compared with data from 2005 to 2011,for which samples were collected once each during low flow (May)and once during high flow (August). On the basis of river dischargeand rainfall pattern thewhole year was divided as high flow (July toNovember) and Low flow (December to June). Thirty six GPS fixedlocations, stations 1e14 in the southern sector, stations 15e21, 23 inthe central sector, stations 22, 24e33 in the northern sector andstations 34e36 in the outer channel were chosen to collect surfacewater samples for a detailed analysis of biogeochemical variables(Fig. 1). Observations for River discharges were made at all rivers/rivulets at 10-day intervals. Experiments for nitrification wereconducted at 4 stations (one station in each sector) during May andAugust of 2009.

2.2.1. Physiochemical and biological parametersIn situ air and water temperatures were measured using

a thermometer (1e51 �C range, �0.1 �C; Brannan, UK) and currentspeed was recorded by deploying a self-recording current meter(Nortek, USA) for 15 min at each station. Monthly rainfall and windspeed data for Chilika lagoon were collected from self-recordingweather stations (R.M. Young, USA; Model 05106) installed at thewestern end (Chandraput) and eastern end (Satpada). To estimatethe discharge from the rivers that drain into the lagoon, currentmeter (Aquadopp) was deployed at every river outlet. The currentmeter was deployed in every 10 days interval for aminimum periodof 15 min. The discharge rate was calculated by multiplying thecurrent speed, width and average depth of the river.

Salinity was measured by the argentometric method (Knudsenscale), nutrients (dissolved inorganic nitrogen, dissolved inorganic

Fig. 1. Map of Chilka Lagoon with 36 stations and dotted lines indicating the imaginary boundaries of the four sectors [southern sector, central sector, northern sector and outercannel].

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phosphate and dissolved silicate) were measured using spectro-photometric method and DO was estimated by Winkler’s method(Grasshoff et al., 1999). Metrohm pH meter with ROSS combinationglass electrode calibrated on the National Bureau of Standards(NBS) as described by Frankignoulle et al. (2001) was used for pHmeasurement. The analytical precision of pH measurement was�0.008 for freshwater samples and �0.005 for the rest. Suspendedparticulate matter (SPM) was measured by filtering a knownvolume of water through 0.45 mm cellulose acetate membranefilters (Milipore), rinsed with copious Milli-Q water and by takingthe difference of initial and final weights of filter. Bacterial Abun-dance (BA) was estimated using the acridine orange direct countmethod (Hobbie et al., 1977). Bacterial respiration (BR), bacterialproduction (BP) and primary production (PP) were measuredfollowing methods as adopted by Thottathil et al. (2008). Nitrifi-cation rates were measured using N-Serve, a specific inhibitor ofammonium oxidation (Campbell and Aleem, 1965) following theprocedure adopted by Miranda et al. (2008).

2.2.2. DIC, pCO2 and CO2 fluxesSamples of 100 ml were preserved with 10 ml of saturated

mercuric chloride for dissolved inorganic carbon (DIC) and esti-mated using a Coulometer (UIC Inc., USA; Model CM 140-02). Theresults were obtained to an accuracy of 0.1%, compared withCertified Reference Material (Batch No. 67) obtained from ScrippsInstitution of Oceanography, USA. The pCO2 was computed usingmeasured salinity, temperature, nutrients (phosphate, silicate), pHand DIC using dissociation constants derived by Cai and Wang(1998) with a precision of 9e13 matm. Since during the studyperiod salinity ranged from 0.1 to 36 and water temperature was inthe range of 20e35 �C, Cai and Wang (1998) was preferred overMillero et al. (2006). However the later was suitable for highersalinity range (up to 50) and higher temperature (up to 50 �C)(Pelletier et al., 2007) and also noted by Gupta et al. (2008).Maximum frequency of salinity observed during the study periodwasw7, the pCO2 derived may be lowered by 4.5� 2% (Gupta et al.,

2008) than the pCO2 if calculated using constants by Millero et al.(2006). Although magnitude varies, both the constants showssystematic variation, and the basic conclusion will not be changedon the use of Millero et al. (2006) constants (Gupta et al., 2008). CO2SYS.XLS (version 14), developed by Pelletier et al. (2007), anupdated version of the original (Lewis andWallace, 1998), was usedfor computing pCO2. The CO2 fluxes across the airewater interfacewere calculated as:

F ¼ a$k$DpCO2;

Where, F is the airewater CO2 flux (mmol m�2 d�1), a is theCO2 solubility coefficient according to Weiss (1974), k is the gastransfer velocity of CO2 (m d�1) and DpCO2 is the difference inpCO2 between water and air. The average atmospheric pCO2 valuefor dry air (388.3 and 392.2 matm during 2009 and 2010 respec-tively) was obtained from a monitoring station in India (15.08�N;73.83�E) which is closest to Chilka region (WDCGG, 2012) andcorrected for water vapour using the algorithms proposed byWeiss and Price (1980). k was computed as a function of windspeed, water current and water column depth according to Borgeset al. (2004).

3. Results and discussion

3.1. Effect of discharge on pH and salinity

The pH was ranged from 6.672 to 9.981, with lower valuesduring high flow period. Since the effect of discharge into thelagoon varied with respect to different sectors, the pH also variedaccordingly (Table 1; Fig. 2). There was a significant increase in pH(from 7.381 to 9.982) during low flow, as the seawater intruded,and there was higher primary production (216 mg C l�1 d�1) thanduring the high flow period (123 mg C l�1 d�1). The low pH valuesduring the high flow period of 2009 in the northern sector wereassociated with high levels of nutrients and bacterial abundance,

Table 1Spatio-temporal variation of pH, Salinity, pCO2, CO2 flux, Bacterial respiration (BR) and Bacterial abundance (BA), represented as average � standard error with range, for theyear 2009 and 2010 (SS: Southern sector, CS: Central sector, NS: Northern sector, OC: Outer channel).

Low flow High flow

SS CS NS OC SS CS NS OC

2009pH 8.43 � 0.04 8.64 � 0.08 8.45 � 0.06 8.22 � 0.03 8.26 � 0.02 8.31 � 0.06 7.65 � 0.07 8.11 � 0.06

7.70e9.53 7.79e9.96 7.63e9.98 8.02e8.50 7.90e8.65 7.62e9.00 6.67e8.46 7.73e8.54Salinity 12.78 � 0.36 14.21 � 1.49 12.01 � 1.45 34.63 � 0.36 11.71 � 0.37 4.46 � 0.47 1.06 � 0.25 5.70 � 1.7

4.29e21.97 0.91e35.88 0.26e35.88 29.98e35.88 6.15e16.38 0.26e11.96 0.13e9.89 0.51e19.34pCO2 (matm) 598 � 51 497 � 70 600 � 59 480 � 25 730 � 30 650 � 72 2678 � 359 732 � 71

11e1980 5e1808 4e2942 275e638 270e1458 104e1977 377e11548 263e1200CO2 flux

(mmol C m�2 d�1)18.07 � 4.4 8.65 � 6.44 21.23 � 5.99 12.26 � 3.24 19.69 � 1.69 20.32 � 5.92 165.67 � 24.88 31.84 � 7.42(�39.93)e130.25 (�54.55)e161.49 (�46.42)e233.45 (�12.25)e40.28 (�6.64)e64.61 (�28.07)e155.57 (�0.57)e744.43 (�15.01)e93.41

BR (mg C L�1 d�1) 63.42 � 9.34 40.77 � 5.44 109.35 � 19.25 111.36 � 53.19 81.73 � 10.19 61.44 � 7.10 180.41 � 36.30 178.33 � 110.7916.32e121.24 27.23e72.28 56.18e231.32 32.16e212.46 29.15e144.83 35.23e86.83 84.75e389.61 39.82e397.4

BA (X 109 cells L�1) 0.79 � 0.06 1.25 � 0.04 1.40 � 0.06 0.81 � 0.24 0.95 � 0.08 1.56 � 0.08 1.67 � 0.07 0.87 � 0.350.42e1.11 1.15e1.5 1.05e1.62 0.41e1.22 0.43e1.43 1.23e1.86 1.18e1.99 0.32e1.52

2010pH 8.58 � 0.04 8.74 � 0.06 8.36 � 0.04 8.43 � 0.05 8.29 � 0.02 8.18 � 0.03 7.88 � 0.06 8.25 � 0.04

7.81e9.50 8.12e9.98 7.38e9.50 8.12e8.92 7.85e8.64 7.85e8.39 6.72e8.29 7.99e8.43Salinity 13.04 � 0.47 13.99 � 1.26 9.78 � 1.06 28.78 � 1.82 11.69 � 0.46 8.18 � 1.01 2.90 � 0.51 9.92 � 3.09

5.71e21.90 2.03e35.99 0.26e31.76 14.86e35.74 6.28e18.57 0.26e28.95 0.13e16.14 1.02e33.31pCO2 (matm) 787 � 85 509 � 58 922 � 120 702 � 79 1313 � 60 1453 � 115 3392 � 611 1073 � 104

25e4369 11e1974 67e6080 102e1490 514e3237 757e3490 555e22487 597e1871CO2 flux

(mmol C m�2 d�1)28.99 � 5.66 10.28 � 4.79 53.35 � 11.91 33.14 � 4.58 59.45 � 5.01 65.65 � 6.69 195.86 � 39.73 64.65 � 10.08(�58.48)e207.31 (�53.78)e119.26 (�40.5)e660.51 (�58.47)e660.52 11.34e216.24 17.13e166.16 13.97e1268.34 14.17e167.09

BR (mg C L�1 d�1) 49.78 � 7.24 33.45 � 4.81 92.24 � 20.12 122.34 � 32.44 108.26 � 7.36 84.38 � 19.23 190.21 � 29.84 126.33 � 78.3424.34e89.74 18.97e52.99 42.45e109.45 44.65e187.34 45.32e167.84 27.45e106.44 94.65e347.81 39.82e244.63

BA (�109 cells L�1) 0.82 � 0.06 1.12 � 0.05 1.08 � 0.05 0.76 � 0.30 0.84 � 0.06 1.26 � 0.08 1.43 � 0.07 0.52 � 0.260.29e1.17 0.89e1.54 0.87e1.43 0.46e1.37 0.47e1.83 1.07e1.93 1.09e2.89 0.12e1.44

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similar to the observation in Godavari estuary (Sarma et al., 2011).Lower pH (<7.5) and higher pCO2 (>1000 matm) were recorded inwaters with salinity less than 2 (Fig. 3). These patterns were inexcellent agreementwith those observed elsewherewith respect toparticle maxima of the Hudson, European and Mandovi estuariesby Raymond et al. (1997), Frankignoulle et al. (1998) and Sarmaet al. (2001) respectively.

The decrease in salinity (Range 0.13e9.89) observed in thenorthern sector during the high flow period could be attributedto severe dilution as a consequence of addition of massivefreshwater into this sector by rivers, streams, but higher valuesduring low flow period may result from the restricted entry offreshwater and the higher resident time of saline water in thelagoon (Panigrahi, 2006; Gupta et al., 2008). The high and stablesalinity observed in the southern sector (ANOVA, p > 0.05) duringlow and high flow period, could be attributed to the mixing withsaline water from the Rushikulya estuary, through the enclosedPalur canal. Even though, the salinity regime of Chilika lagoonremains lower, the pattern of distribution was similar to that inCochin Backwater (Sankaranarayan and Qasim,1969; Manikoth andSalih, 1974), Pulicat Lake (Kaliamurthy, 1973) and Ashtamudi Lake(Nair et al., 1984), where such a persistent decline was reported infreshwater influenced zones.

3.2. Bacterial respiration and nitrification

Bacterial respiration was very high in the northern sectorcompared to rest of the sectors in the lagoon during the studyperiod and was almost twice during the high flow period comparedwith that during the low flow period (Table 1). CO2 flux equivalentof depth integrated BR indicated that it contributed 83% of total CO2

flux from the lagoon during the study period. Bacterial carbondemand (BCD) was calculated only for 2009 as the Bacterialproduction was only estimated during May and August of this year.BCD during the high flow period wasw2 fold higher than low flow,irrespective of the sectors and the northern sector of the lagoonobserved to have highest BCD irrespective of the seasons. Duringhigh flow the BCD in the northern sector ranged between 299 and946 (mean 571) mg C m�2 d�1 followed by outer channel (288e966, mean 542 mg C m�2 d�1), central sector (208e305, mean264 mg C m�2 d�1) and southern sector (113e361, mean233 mg C m�2 d�1). The similar seasonal variation was alsoobserved in the equatorial Pacific Ocean (Kirchman, 2008). TheBCD in the lagoon was comparable to that in Ross Sea, Bermuda,Hawaii and subarctic North Pacific Ocean, while it is one-fourth ofthat in the Arabian Sea, North Atlantic and equatorial Pacific Ocean(Ducklow and Carlson, 1992; Kirchman, 2008).

Fig. 2. Temporal variation of pH and pCO2 in different sectors (SS-Southern sector, CS-central sector, NS-northern sector and OC- outer channel) with river discharge (averagedvalues of all rivers for each observation).

a b

Fig. 3. Distribution of pH (a) and pCO2 (b) along the salinity gradient in Chilika lagoon during low and high flow period of the year 2009 and 2010.

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High BR and associated high bacterial number along with highnitrate concentrations (15� 7with a peak of 27 mmol l�1) especiallyin the northern sector during the high flow period suggest that thevery low pH values are due to organic matter decomposition(Table 1). High nitrogen, low pH and low oxygen saturation arethe signature of nitrification (Frankignoulle et al., 1996). The resultsobtained for BR, include nitrification, and hence might be over-estimated due to the oxygen demand by nitrification (Taylor et al.,2003). For instance in the Scheldt estuary, 50% of O2 consumptionis due to nitrification (Vanderborght et al., 2002; Gazeau et al.,2005a), but it was found to be negligible (<0.4%) in case ofChilika lagoon as the nitrification was estimated to be84.24 � 62.97 nmol N L�1 h�1during the low flow period and fourfold less during the highflowperiod (24.38� 34.92 nmolN L�1 h�1).

3.3. Factors influencing pCO2 and CO2 supersaturation

A significant negative relation between pCO2 and temperature(n ¼ 250, r ¼ 0.15, p < 0.001) indicated the higher pCO2 in lowtemperature and vice versa. Apart from which DO%, pH, SPM, PPand BR also influenced pCO2 significantly. During the active period,the lagoon water in all the sectors was found to be undersaturatedwith respect to dissolved oxygen (3%e25%) during both 2009 and2010 evidently due to oxygen depletion caused by intensifiedheterotrophic activity. In contrast, supersaturation of DO from104% to 120% was observed throughout the lagoon during lowflow. The higher supersaturation in the southern sector may beattributable to lower SPM (3e45 mg l�1), higher photic depth(0.5e1.82 m), and lower BR associated with lower BA, whichpromote intense photosynthesis over respiration.

The lagoon received a heavy freshwater influx during themonsoon season when 80% of the annual rainfall occurs, and thelarge amount of organic matter transported into this lagoon mayhave a significant effect upon the metabolism. (e.g. Sarma et al.,2009, 2010). During high flow, BR in the northern sector was w2times higher than that during low flow (Table 1) and consistentwith findings in Godavari estuary by Sarma et al. (2009). In additionto this, high bacterial activity in the rivers during the storageperiod, before its discharge into the lagoon, further decreases pH.The oxygen undersaturation and sharp rise in pCO2 level towardsthe northern sector in the high flow period was mostly due to rapidmineralization of terrestrial organic matter (both dissolved andsuspended) and the buffering capacity of inorganic carbon thatshifts towards CO2 in low pH (saline) waters. The present studysuggested that the elevated CO2 supersaturation in the northernsector was caused by high BR (in excess of PP) as a result of bacterialdegradation of allochthonous organic matter (Gupta et al., 2009;Sarma et al., 2011). Similarly high pCO2 levels were observed inother Indian estuaries such as Cochin estuary (Gupta et al., 2009)and, Mandovi-Zuari estuarine systems (Sarma et al., 2001) associ-ated with dominant heterotrophic respiration exceeding autotro-phic production (Ram et al., 2003; Gupta et al., 2009; Sarma et al.,2009).

The wide variation of pH in the low saline range could beattributed to waters of different chemical characteristics from 19rivers draining into the lagoon (Gupta et al., 2008). The lower pHrange of <7.5 observed in the lower saline (<2) region during thehigh flow period (Fig. 3a) could be due to addition of lower pHwater from northeast rivers and higher BR observed in this region.Higher pH values of >8.5 in this region was observed only duringthe low flow period (Fig. 3a) could be attributed by higher primaryproduction (216 � 77, 82e296 mg C l�1 d�1) than during high flow(123 � 37, 62e182 mg C l�1 d�1). Very high pCO2 that was observed(only during high flow), in low saline condition (Fig. 3b) corre-sponds to the very low pH in the same salinity range (Fig. 3a).

3.4. Spatio-temporal variation of pCO2

The averaged pCO2 in the lagoon, during high flow was1683 matm which was within the range observed for the estuariesalong the east coast of India, but lower than that observed for thosealong the west coast (Sarma et al., 2012). During the low flowperiod, the pCO2 level was <1000 matm (623 matm) as in otherIndian estuaries such as Godavari (Bouillon et al., 2003; Sarma et al.,2011), Mandovi-Zuari (Sarma et al., 2001), Cochin estuary (Guptaet al., 2009), Mahanadi and Krishna rivers (Sarma et al., 2012).Such low pCO2 was attributed to higher primary production overbacterial respiration (PP/BR > 1). During this period pCO2 wasbelow equilibrium at some stations of southern sector, and similarobservations were made elsewhere (Borges and Frankignoulle,1999; Sarma et al., 2011).

A pronounced north-south gradient of pCO2, with relativelyhigher values (supersaturation) in the northern sector, wasobserved during high flow, whereas during low flow, the lagoonwas largely undersaturated (Frankignoulle et al., 1998; Sarma et al.,2001; Mukhopadhyay et al., 2002). The similar observations werealso made by Gupta et al. (2008) although the range of pCO2 waslower. During both seasons, the pCO2 values followed the patternof, northern sector > southern sector > central sector throughoutthe period of 2005e2011 except in the low flow period of 2011.Among all the sectors, the northern exhibited highest pCO2 (atstation 33) of 11, 548 during 2009 and 22,487 during 2010suggesting direct influence of river discharge (w80% dischargefrom Makara river), in addition to highest BR and lowest pH(Table 1). The CO2 supersaturation during the peak dischargeperiod was maximum in the northern sector which decreasingtowards the southern sector and reaching undersaturation levelduring low flow period as the lagoon recovered from monsoonaleffects (Fig. 4). The wide variation in pCO2 level (4e22,487 matm) inthe lagoon throughout the year makes it quite different from othersystems around the world with pCO2 was <10,000 matm (Table 2).High pCO2 levels found in the Scheldt estuary were attributed todischarge of pollutants (Borges and Frankignoulle, 2002). TheChilika lagoon cannot be classified as a polluted estuary based onthe average nutrient ratios of N: P 20� 7 and it does not receive anysignificant domestic or industrial effluents. In Chilika lagoon, thebacterial decomposition of land derived organic material, as well asthat produced in situ supported by high nutrients, leads to thesupersaturation of CO2 in the northern regions of the lagoon duringthe high flow period.

Excluding station.33, the pCO2 varied between 3.6 matm and1980 matm (mean 546 matm) in the low flow period and between104 matm and 4916 matm (mean 920 matm) during the high flowperiod of 2009. In 2010, the observed pCO2 during low flowwas much lower, 732.97 matm (11.4e5361 matm, excluding station33) than that of the high flow period (mean 1436 matm, 513.9e6594 matm). These seasonal pCO2 maxima differed significantlyfrom the low flow period values observed, in the mangrove creeksof the Godavari estuary (500e6500 matm, Borges et al., 2003;Bouillon et al., 2003) and showed an entirely opposite pattern tothe Mandovi-Zuari estuarine systems where the low flow pCO2exceeded the pCO2 during high flow (monsoon: 2250 matm, non-monsoon: 2600 matm; Sarma et al., 2001). The monthly meanpCO2 values of the lagoon showed strong positive relation withthe rate of discharge (n ¼ 24, r2 ¼ 0.54; p < 0.001; Fig. 5), sug-gesting that the magnitude of discharge had a significant impacton the CO2 fluxes. This observation supports the recent study(Sarma et al., 2012), which showed the CO2 emission in Indianestuaries strongly influenced by discharge (pCO2 vs. discharge:r2 ¼ 0.71; p < 0.001) and the relationship is applicable to allIndian estuaries.

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3.5. CO2 emission from the lagoon

A comparison of CO2 fluxes estimated using k parameterizationproposed by different authors (Table 3) showed large differences.Ho et al. (2006) obtained the lowest and Borges et al. (2004), washighest. The value resulted following Raymond and Cole (2001)was almost one-fourth the highest value. The flux estimatedwhen only wind was considered, was almost half of that estimatedwhen wind, current and depth were considered together (Borgeset al., 2004). Because of shallow depth, the turbulence by bottomshear of the lagoon can transfer to surface, hence depth and currentwere considered in this study. CO2 flux of Hudson River Estuaryestimated by k parameterizations used for ocean and was able to

predict gas exchange with high accuracy (Ho et al., 2011). Therelationship of gas exchange with various environmental variablesis site specific, and a relationship developed in a particular estuarymay not be applicable for others. Unless specified, we used Borgeset al. (2004) for interpreting the results, discussion and comparisonof the flux estimated for Chilika, by Gupta et al. (2008) using thesame parameterization.

The net CO2 efflux, observed during the present study, from theentire lagoon during high flowwas 4 times higher than that duringlow flow while, a difference of 44 times was observed by Guptaet al. (2008) considering the same k parameterization (Borgeset al., 2004). CO2 fluxes were lowest in the southern sectorduring low flow (�58.48 mmol C m�2 d�1) and highest

Table 2Latitude pCO2 range (ppm), airewater CO2 fluxes (CO2 flux in mol C m�2 y�1) in near-shore ecosystems and negative sign of CO2 flux indicates the sink of CO2 in the system.(Ref: Chen and Borges, 2009).

Site (Inner estuaries) N pCO2 range CO2 flux References

Betsiboka (Madagascar) �15.7 270e1530 3.3 Ralison et al., 2008Tendo lagoon (Ivory Coast) 4.3 90e3600 5.1 Koné et al., 2009Aby lagoon (Ivory Coast) 4.4 60e325 �3.9 Koné et al., 2009Tagba lagoon (Ivory Coast) 4.4 800e4250 18.4 Koné et al., 2009Ebrié lagoon (Ivory Coast) 4.5 1365e3575 31.1 Koné et al., 2009Potou lagoon (Ivory Coast) 4.6 1235e5120 40.9 Koné et al., 2009Randers Fjord (Denmark) 6.6 220e3440 2.2 Gazeau et al., 2005(b)Mekong (Vietnam) 10 280e4105 30.8 Borges, unpublishedMandovi-Zuari (India) 15.3 500e3500 14.2 Sarma et al., 2001Godavari estuary (India) 16.7 100e33,391 52.6 Sarma et al., 2011Godavari (India) 16.7 220e500 5.5 Bouillon et al., 2003Chilika (India) 19.1 70e6350 25 Gupta et al., 2008Chilika (India) 19.1 104e22,487 31.2 This studyHooghly (India) 22 80e1520 5.1 Mukhopadhyay et al., 2002Satilla River (United States) 31 360e8200 42.5 Cai and Wang, 1998Altamaha Sound (United States) 31.3 390e3380 32.4 Jiang et al., 2008aDoboy Sound (United States) 31.4 390e2400 13.9 Jiang et al., 2008aChangjiang,Yantze (China) 31.5 200e4600 24.9 Gao et al., 2005, Zhai et al., 2007Sapelo Sound (United States) 31.6 390e2400 13.5 Jiang et al., 2008aLoire (France) 37.2 630e2910 64.4 Abril et al., 2003York River (United States) 37.2 350e1900 6.2 Raymond et al., 2000Guadalquivir (Spain) 37.4 520e3606 31.1 De la Paz et al., 2007Sado (Portugal) 38.5 575e5700 31.3 Frankignoulle et al., 1998Aveiro lagoon (Portugal) 40.7 143e11335 12.4 Borges and Frankignoulle, unpublishedDouro (Portugal) 41.1 1330e2200 76 Frankignoulle et al., 1998Saja-Besaya (Spain) 43.4 264e9728 52.2 Ortega et al., 2005Gironde (France) 45.6 465e2860 30.8 Frankignoulle et al., 1998Tamar (United Kingdom) 50.4 380e2200 74.8 Frankignoulle et al., 1998Scheldt (Belgium, Netherlands) 51.4 125e9425 63 Frankignoulle et al., 1998Thames (United Kingdom) 51.5 505e5200 73.6 Frankignoulle et al., 1998Rhine (The Netherlands) 52 545e1990 39.7 Frankignoulle et al., 1998Ems (Germany) 53.4 560e3755 67.3 Frankignoulle et al., 1998Elbe (Germany) 53.9 580e1100 53 Frankignoulle et al., 1998Bothnian Bay (Finland) 63 150e550 3.1 Algesten et al., 2004

The present study (Chilika, Odisha, India) as been highlighted as bold which has been compared with other similar studies world wide.

CO2 flux (mol C m-2 y-1)

a b

Fig. 4. Spatial variation of CO2 emission during low flow (a) and high flow (b), considering average values of 2009 and 2010.

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(1268.34 mmol C m�2 d�1) in the northern lagoon during high flowof 2010. The values were lower than observed in the earlier study(Gupta et al., 2008). Strong seasonal gradients persisted in thenorthern lagoon, where high flow evasion rates were about 4e8times higher than low flow (Table 1) which was 58 times (higher)as recorded by Gupta et al. (2008). The CO2 flux during high flow forthe entire lagoon was about 4 and 3 times higher than low flowduring 2009 and 2010 respectively. Sarma et al. (2012) similarlyobserved 4e5 times higher values in wet than in dry period for theentire Indian estuaries. During the present study period, thecontribution of CO2 fluxes to the atmosphere from the lagoon,during low flow period was 20% as for other Indian estuaries(Sarma et al., 2012). The CO2 efflux from the lagoon during highflow period was 56 mmol C m�2 d�1, which was in the range of theeffluxestimated for entire coastal estuaries of India, but about thricethemean flux (27mmol Cm�2 d�1, Sarma et al., 2012) and a third ofthat in European estuaries (170 mmol C m�2 d�1, Frankignoulleet al., 1998). Although the magnitude varied, the lagoon was netsources of CO2 to the atmosphere, since they were oversaturated inCO2 throughout the year similar to other lagoons such as Ebrié,Potou, and Grand-Lahou lagoons (Koné et al., 2009). However Abylagoon, acts as a sink of CO2 throughout the yearwhile Tendo lagoonacts as a source of CO2 during high flowperiod and a net sink duringrest of the period (Koné et al., 2009). The annual mean value(20mol Cm�2 y�1) is consistent with those reported for macro tidalestuaries worldwide (18e37 mol C m�2 y�1) and higher (5e14 mol C m�2 y�1) than those reported so far at tropical andsubtropical latitudes (Frankignoulle et al., 1998; Abril and Borges,2004; Borges, 2005; Borges et al., 2005, 2006; Chen and Borges,2009). The estimated annual flux was higher than that reported

from other ecosystems of India (Sarma et al., 2001; Mukhopadhyayet al., 2002; Bouillon et al., 2003; Biswas et al., 2004) and elsewhere(Frankignoulle et al.,1998; Bouillon et al., 2007) whereas lower thansome Indian estuaries such as Ponnayaar and Tapti (Sarma et al.,2012) and estuaries in other countries (Table 2: Frankignoulleet al., 1998; Jiang et al., 2008; Koné et al., 2009; Cai and Wang,1998; Ortega et al., 2005; Abril et al., 2003).

The average CO2 flux in the entire lagoon during high flow of2009 and 2010 was 31.2 mol C m�2 y�1, which is comparable withother lagoons and inner shore ecosystems around the world(Table 2). Mean CO2 emission (16.83 mol C m�2 y�1) from thesubtropical and tropical estuaries (�30 to þ30� latitudinal belt)reported by Borges et al. (2005) was several times lower than thepresent observations. Tropical estuaries such as the Godavari wasincluded in their CO2 flux estimation (Bouillon et al., 2003) but theChilika lagoon was not considered for want of data. However, theCO2 flux found in the present studywas similar to the data reportedfor the Godavari estuary by Borges et al. (2005). Several major andminor estuaries open into the northern Indian Ocean and monsoon(high flow) associated processes would make these coastal bodiesvery significant sources of atmosphere CO2. The plot of CO2 fluxfrom the estuaries estimated all over the world (Table 2) showeda very significant positive correlation (n¼ 34, r¼ 0.527, p¼ 0.0011)with the latitude indicated that there is an increase in CO2 emissionfrom the estuaries at lower latitude towards higher latitudes. Inhigher latitudes, except Bothnian Bay, all European near shoreecosystems (>48.4�N; Table 2) showed the higher range of CO2 flux(Frankignoulle et al., 1998) compared to those at lower latitudes.For instance, CO2 fluxes from all Indian estuaries (lower latitude)were about a tenth of those in European estuaries. This observedpattern along the latitude may be attributed to population density,port activity, industry and domestic pollution, along the banks ofthe ecosystems (Sarma et al., 2012).

3.6. Conceptual outline

From our study of CO2 emission, a conceptual scheme of possiblefactors influencing the CO2 flux in Chilika lagoon has been pre-sented for high flow and low flow periods (Fig. 6). During high flowperiod, lagoon received high DOC (Gupta et al., 2008), nutrients andbacterial load (BA)which triggered bacterial respiration resulting inan increases in CO2 emission. In addition to this, high suspendedparticulate matter brought in to the lagoon substantially reducedwater column light penetration (Gupta et al., 2008) which subse-quently decreased the primary production, allowing the BR todominate over it. During the low flow period, the salinity levelincreased along with pH, and SPM concentrations reducedsubstantially. Consequently, lower BA and BR combined withhigher primary production (compared to the high flow) decreasedthe water to air CO2 efflux during the low flow period.

Table 3Comparision of annual CO2 fluxes (mol C m�2 y�1) during low flow (LF) and high flow (HF), computed according to different k value (Gas transfer velocity) parameterizations,represented as average � standard error with range.

2009 2010 Average

LF HF LF HF

Borges et al. (2004) 5.99 � 1.07 24.37 � 3.44 12.1 � 1.68 38.03 � 4.94 20.1219.92e85.21 10.25e271.72 21.35e241.09 4.14e462.95

Borges et al. (2004; wind only) 4.29 � 0.72 14.92 � 2.16 8.4 � 1.19 21.59 � 2.59 12.39.59e49.67 6.57e205 16.87e182.21 2.22e224.31

Jiang et al., 2008 2.82 � 0.47 10.99 � 1.58 6.89 � 0.97 17.01 � 2.11 9.436.49e33.1 4.23e129.96 17.42e130.69 0.67e201.1

Raymond and Cole (2001) 2.01 � 0.34 7.13 � 1.03 5.07 � 0.73 10.7 � 1.31 6.234.72e22.48 2.93e91.19 15.73e96.22 18e119.21

Ho et al. (2006) 1.47 � 0.24 2.88 � 0.48 3.59 � 0.64 3.65 � 0.48 2.894.28e19.7 1.59e54.67 14.65e92.78 0.24e62.45

Fig. 5. Relationship of pCO2 with river discharge in Chilika lagoon during 2009 and2010.

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4. Conclusion

From this study, Chilika lagoon can be considered as a netsource of CO2 because of the significant influence of contrastingfeatures in the northern sector, which is most affected by thefreshwater discharges from northeast rivers during high flow.The riverine freshwater discharges with lower pH and highbacterial abundance, trigger increased BR followed by themineralization of organic matter into CO2, and this is largelyresponsible for the CO2 supersaturation observed in the northernpart of the lagoon. During high flow, the estimated air water CO2flux was comparatively very high with respect to the mean CO2emission from the entire subtropical and tropical estuaries. Thisflux can be recalculated using the CO2 flux estimated by monthlyobservations, for the years 2009 and 2010. Taken together, thesefinding indicate that CO2 evasion in the northern part of thelagoon could be a characteristic feature for such coastal lagoonsand this region may be considered a hot spot in terms of regionalcarbon budgets. Sectoral budgeting indicated that the brackishwater conditions, with moderate to high phytoplankton ideallyfacilitate sinking of CO2. Hence by ensuring the best possible flowof neritic waters into different parts of the lagoon during lowflow, at least during that period more CO2 can be trapped into thesystem.

Acknowledgements

The authors are grateful to Dr. Shailesh Nayak, Secretary,Ministry of Earth Sciences, Government of India for the encour-agement. We are also grateful to the Indian Navy (INS Chilika) forlogistic support during the course of this investigation. We arethankful to research staff of Andhra University for generous help inthe field. We also wish to thank the three anonymous referees fortheir thoughtful and constructive comments on earlier form of thismanuscript. This study is a part of MoESeICMAM’s comprehensiveproject “Ecosystem Modelling for Chilika Lagoon”.

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Riv

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Atmosphere

Water

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SPMSPM

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