Nitrous oxide (N2O) is an important greenhouse gas, which is 298 times greater with regard to global warming potential (Forster et al., 2007) than carbon dioxide (CO2), and has a lifetime of 114 year in the atmosphere (IPCC, 2007). Since pre-industrial time atmospheric N2O has increased ~18% in the atmosphere (IPCC, 2007). Oceans are the second major natural source of N2O to the atmosphere after soils (Bange et al., 1996; Seitzinger et al., 2000). The N2O is produced as a by-product in the first step of nitrification and as an obligate intermediate during denitrification. Both nitrification and denitrification occur in water columns, sediments or interior sediment particles (Nevison et al., 2003; Codispoti et al., 2005; Bange, 2008), depending highly on dissolved oxygen concentration (Goreau et al., 1980; De Bie et al., 2002). To the global emission of atmospheric N2O, aquatic sources contribute ~30% of which 60% come from estuaries and coastal regions (Bange et al., 1996; Seitzinger et al., 2000). Bange (2006) estimated N2O emission to the atmosphere from European estuaries based on data collected in nine estuaries as 0.33–0.67×1012 g N annually, which represents up to 26% of global N2O emission. They further concluded that coastal N2O is mainly formed in the estuarine system. Recently Barnes and Upstill-Goddard (2011) revised these estimates to 6.8±13.2×109 g N2O y−1 and noticed that higher estimates by Bange (2006) come from use of a larger area for estuaries. Conversely, Bange et al. (1996) estimated N2O emissions from the world estuaries to be 3.68–5.71×1012 g N2O y−1, and these estimates may have to be revised due to recent modifications in the area of European estuaries. Overall, the estimates from the estuaries suffer from large uncertainties due to large variability and lack of consistent data. It is especially true for Southeast Asian estuaries where the biogeochemical cycling of material is different due to high atmospheric temperature, seasonality of monsoons, and discharge pattern, high fertilizer use, etc. These regions were also highly under-sampled with reference to time and space.
India houses ~220 major and minor estuaries, which are influenced by monsoonal rainfall, and therefore called as monsoonal estuaries. These estuaries have characteristic runoff periods, mostly from June to September when the Indian subcontinent receives rainfall, when they exhibit non-steady state behaviour (Vijith et al., 2009). Seasonal runoff into these monsoonal estuaries far exceeds their total volume and when discharges are at peak level, the entire estuary turns into a river (Sarma et al., 2009, 2010, 2011). Discharges of variable magnitudes occur for a period of 4–6 months, and other periods, the upstream river almost dries up giving place to dominance of seawater in the estuary. Hence, the biogeochemical processes in monsoonal estuaries during discharge period could be completely different from that of a dry period. Recently, Sarma et al. (2012) estimated emissions of CO2 from the Indian estuaries as ~2×1012 gC to the atmosphere annually, which is about 10 times less compared to European estuaries. Such low CO2 fluxes from the Indian estuaries result from high flushing rates and less dense human settlements along the banks of estuaries. In India, N2O emissions were estimated for the Adayar estuary, in the south east of India, and found to emit ~23.2 µmol N2O m−2 d−1 to the atmosphere (Rajkumar et al., 2008). With the exception of this report, no information is available from other Indian estuaries. Indian Mangroves, which are part of the estuarine system, are found to be a strong source of trace gases to the atmosphere (Chauhan et al., 2008; Krithika et al., 2008; Fernandes et al., 2012). The annual emission of N2O from the mangroves located along the east coast of India was estimated to be 5.8×103 gN2O. The objective of this study is to estimate the contribution of N2O emissions from the Indian monsoonal estuaries to the atmosphere.
In order to examine the variations in N2O concentrations and related atmospheric fluxes from the Indian estuaries, sampling was conducted in 28 major estuaries along the Indian coast during peak discharge (wet) period (28 July–18th August 2011), and dry period (2–15 January 2012) (Fig. 1). From each estuary, samples were collected at 5–10 locations from river mouth to upper reaches of the estuary. Temperature and salinity were measured using a CTD system (Sea Bird Electronics, SBE 19 plus, USA). Nutrients were measured using a spectrophotometric method following Grashoff et al. (1992). Dissolved oxygen (DO) was measured using Winkler's titration method of Carritt and Carpenter (1966) with a potentiometric end-point detection technique. The analytical precision, expressed as standard deviation, was 0.07% for DO and ±0.2 µM for ammonium, nitrite and nitrate. Dissolved N2O in the water was determined by a multiphase head space equilibration technique (McAuliffe, 1971) coupled with Gas Chromatographic analysis. Briefly, predetermined volume (25 ml) of sample was equilibrated with an equal volume of helium in a gas tight syringe by vigorously shaking the syringe at room temperature for 5 minutes using a wrist action shaker. After equilibrium, the head space was dried over drierite and then injected through a 5-ml sampling loop into a gas chromatograph (Agilent- 6820, USA) and separated over a chromosorb column (80/100 mesh) at 35°C, and N2O peak was detected with a 63Ni Electron Capture Detector (ECD). Wind speed data were obtained from the Indian Meteorological Department (IMD) from the stations close to the respective estuaries. The air-to-sea fluxes of N2O were estimated using the following equation:
Hourly measured wind speed was averaged to obtain seasonal mean and was used for piston velocity calculations. The piston velocity at the Schmidt number of 660 (Sc 660) was computed following Wanninkhof (1992):
Several investigators found that flux estimates based on the Wanninkhof (1992) coefficients may provide under-estimates due to the tidal enhancement of turbulence (Zappa et al., 2003; Borges et al., 2004); hence caution is warranted. Nitrification rates were measured using the Schell (1978) method. Briefly, 250 ml of surface sample was incubated in dark for 24 hours by adding 2 µmol of N15 labelled ammonium chloride solution (99 atom% excess). After incubation, the nitrate in the water was extracted with aniline and β-napthol, and the resultant Azo-dye was filtered on pre-combusted Whatman GF/F filter. The filter was then dried, packed in the tin cups and combusted in elemental analyser (Flash EA 1112 Series, Thermo Electron, Germany) for content, and the atomic ratio of N14/N15 was measured using isotopic ratio mass spectrometer (IRMS; Delta V Plus, Thermo Electron, Germany).
Nitrification rates were measured following uptake rates of substrate (nitrate) enriched with 15N (Dugdale and Goering, 1967). Specific nitrate uptake rates (µmolN l−1 d−1) were calculated as:
River discharge data was obtained from dam authorities of respective rivers (Sarma et al., 2012).
The Indian estuaries display a range of hydrological conditions driven by variable freshwater flows and flushing rates during the wet period and variable tidal amplitudes during the dry period. The mean river discharge from the Indian estuaries varied from ~28 to 3505 m3 s−1 (Table 1). The magnitude of discharge determines the amount of organic matter and nutrients entering the estuary and also the stability of water column that governs the interaction with the microbial processes (Sarma et al., 2011, 2012).
The water discharged by the monsoonal estuaries is significantly modified during storage in dam reservoirs. Several dams had been constructed across most rivers sampled in this study. The water is stored in the dam reservoirs for over 6 months during the dry period for irrigation and domestic usage. This storage leads to the formation of stagnant conditions that favour microbial degradation of organic matter and the release of nutrients. Formation of N2O is possible due to nitrification in the dam reservoir, and discharge of reservoir water into the estuary during the wet period may enhance its concentrations in the estuary. In addition to this, rivers also carry excess fertilizers used in the agricultural farms to the estuary during the wet period. India is ranked second globally in terms of consumption of nitrogen and phosphate as fertilizer (The Fertilizer Association of India, New Delhi) and consumes about 0.025 Tg per year (1 Tg=1012 g). On the other hand, seawater dominates during the dry period due to the closing of dam gates and increased seawater intrusion through tides, resulting in a significant decrease in nutrient levels (Sarma et al., 2010). The relationship between river discharge and DIN indicates that higher DIN concentrations were found in the rivers opened to the east coast compared to the west coast except Narmada, Tapti, Sabarmati and Cochin back waters, which are highly polluted due to local industrial activities (Fig. 2). This relationship is consistent with the fertilizer usage in India, which is higher (~65%) in the regions located along the east coast compared to the west coast (35%) and central India (Ministry of Agriculture, Government of India; http://eands.dacnet.nic.in/latest_2006.html).
The N2O showed wide variations in the Indian estuaries (Table 1). The concentrations of N2O (mean±standard deviation) varied between ~3.5 and 14.6 (6.7±3.5) nM in the estuaries located along the east coast of India while between 6.8 and 47.6 (18.8±11.9) nM in the west coast of India during the wet period. During the dry period, the N2O concentrations ranged between 4.9 and 22.1 (11.4±5) nM in the estuaries located along the east coast of India, except at the Ponnayar estuary where exceptionally high N2O of 414 nM was recorded, and between 9.3 and 47.1 (21.0±13) nM in the west coast of India. The mean concentrations of N2O were slightly higher during the dry period (15.5±10 nM) than the wet period (12.0±10 nM) in the Indian estuaries. Super-saturation of N2O was noticed in the Indian estuaries with relatively lower values associated with estuaries located on the east coast (108±53%) than on the west coast of India (290±158%) during the wet period. On the other hand, comparatively higher saturation was observed in the estuaries located along the east coast of India (161±76%) during dry than the wet period and no significant seasonal variations being noticed in estuaries located along the west coast of India (292±150%).
The N2O saturation showed weak inverse correlation with salinity (r2=0.36; p<0.05) with large scatter, especially at the lower salinity region in the Indian estuaries (Fig. 3a). In order to examine the scatter in the relationship, we have plotted these relationships for selected estuaries from both the east and west coasts of India in Fig. 4. The strong correlation was observed when salinity and N2O data were plotted for individual estuaries. The slope of the relation was changed among estuaries and ranged between 2.8 and 16.1, whereas it ranged from 3.8 to 15.1 and 47.2 to 188.3 with DO saturation and ammonium, respectively, suggesting that the scatter in the relationship was the result of variations in the slopes. The variable slopes of the relationship suggest that the concentration of N2O in the freshwater received by the Indian estuaries is different. Though the relation between salinity and N2O was shown only for a few estuaries in Fig. 4, a similar relationship was found for other estuaries also. Nevertheless, the salinity to N2O relationship suggests that the estuaries which receive high freshwater inputs from upstream act as a stronger source of N2O than others (Figs. 3a and 4). An increase in N2O saturation with a decrease in salinity was reported in several estuaries (Berounsky and Nixson, 1993; Bange, 2006; Silvennoinen et al., 2008; Zhang et al., 2010). Similarly, N2O saturation showed an inverse relation with dissolved oxygen saturation (r2=0.30; p<0.05; Fig. 3b), whereas it showed a positive relation with ammonium (r2=0.42; p<0.001; Fig. 3c) and with DIN (r2=0.47; p<0.001; Fig. 3d), suggesting that nitrification is the possible mechanism for the production of N2O in the Indian estuaries. Berounsky and Nixson (1993) observed an increase in nitrification rates with an increase in DIN in Narragansetti Bay, USA. Bange et al. (1996) and Barnes and Upstill-Goddard (2011) suggested that N2O in the European estuaries was contributed to by nitrification. Relatively higher N2O saturation in the west coast estuaries was associated with higher DIN concentrations (36±26 µM) than east coast estuaries (15.8±22 µM; Fig. 2). In addition to this, dissolved oxygen saturation was also lower in the west coast estuaries (83±8%) than east coast estuaries (94±6%) (Table 1). The east–west gradients in the nutrients load could possibly be due to either over-consumption of fertilizers or intense remineralization of organic matter in the estuary. The state-wise fertilizer consumption in India suggests that ~65% of the fertilizers are consumed in states located along the east coast of Indian and ~28% in states located along the west coast and the remaining (~7%) in the central India (Indian Agricultural department, http://indiastat.com/agriculture/2/stats.aspx). On the other hand, lower mean values of pH were found in the west coast estuaries (6.82±0.52) than the east coast estuaries (7.65±0.57), suggesting that further higher nutrients in the former are caused by higher rates of organic matter decomposition and it is consistent with DO saturation. Recently Sarma et al. (2012) found higher pCO2 levels in the Indian estuaries, which were attributed to organic matter decomposition. Nevertheless, the annual mean N2O saturation in the Indian estuaries (204±137%) was significantly less than the European (465%; Bange, 2006 and 271% Barnes and Upstill-Goddard, 2011) and the American estuaries (165–618%; Table S1; supplementary information).
The hourly mean wind speed (u10) ranged between 0.31 and 2.66 m s−1 during the study period. The seasonal mean wind speed data, prepared from the hourly mean data, were used to compute fluxes. The N2O efflux from the Indian estuaries ranged between −1.1 and 12.1 µmol m−2 d−1 during the wet period and between −0.01 and 14.1 µmol m−2 d−1 during the dry period (Table 1). Higher fluxes were noticed in the Baitharini, Godavari, Ponnayar, Cochin Black waters, Tapti, Nethravathi, Khali and Mondovi estuaries (0.2–14.2 µmol N2O m−2 d−1), while lower fluxes were found in other estuaries (−1.12–5.36 µmol N2O m−2 d−1; Table 1). Such high fluxes in the former estuaries were driven not only by high N2O levels but also by winds. The mean flux from the Indian estuaries amounts to 1.07 and 1.65 µmol m−2 d−1 during the wet and dry periods, respectively, with an annual mean of 1.34 µmol m−2 d−1.
The annual mean emissions from the Indian estuaries were significantly less than the European estuaries (~2.7 µmol m−2 d−1), and they contribute to 0.6% to the world estuaries. Such significant difference might have been caused by variations in DIN loading and nitrification rates. The DIN concentrations in the European and American estuaries were in the range of 5–500 µM (Table S2, supplementary information) with nitrification rates of 0.2–336 µmol N l−1 d−1. Higher ammonium concentrations were found in the Shelde estuary, and higher nitrification rates in the Girode estuary (Table S3, supplementary information). On the other hand, ammonium concentrations in the Indian estuaries were 0.6–16.6 µM during the wet period, whereas they were 0.6–13.5 µM during the dry period and these concentrations are significantly less than the world estuaries (Table 1, S3). Sarma et al. (2009, 2010) showed that monsoonal estuaries received significant amount of nutrients during the peak discharge period. However, nutrients are not utilized in the estuary due to high flushing rates and high suspended load (Sarma et al., 2009; Acharyya et al., 2012). As a result, nutrients are flushed to the coastal regions where they support primary production. Hence, low nitrification rates were found during the dry period in the Indian estuaries (0.007 and 0.87 µmol N l−1 d−1) compared to world estuaries (0.2–336 µmol N l−1 d−1; Table S3).
India houses a total of 14 major, 44 medium and 162 minor estuaries, and the total surface area of Indian estuaries comes to 27 000 km2 calculated from the mouth of the estuary to the region where tidal oscillations are almost negligible (Qasim, 2003). The weight averaged net annual emission of N2O from the Indian estuaries amounts to 0.71×10−3 and 0.46×10−3 Tg N2O during dry and wet periods, respectively (each of 6 months), and the annual emission amounts to 0.0006 Tg N2O y−1 covering an area of 0.027×106 km2, which is about half of the revised emission estimate from European estuaries (0.012 Tg N2O y−1; Barnes and Upstil-Goddard, 2011) covering an almost similar area (0.03×106 km2). The fluxes from the Indian estuaries were much smaller (0.01%) compared to world estuaries (4.7 Tg N2O y−1). Mangroves are a strong source of trace gases to the atmosphere (Chauhan et al., 2008; Krithika et al., 2008; Fernandes et al., 2012). Mangroves are located close to several Indian estuaries. Chauhan et al. (2008) estimated N2O fluxes from the mangrove located along the east coast of India to be 5.8×103 gN2O y−1. Assuming a similar emission from the west coast, the N2O emission from the mangrove amounts to an insignificant fraction compared to the fluxes from Indian estuaries.
The errors arise from various sources such as scaling errors arise from the consideration of studied 28 estuaries representing Indian estuaries as a whole, uncertainties from transfer velocity, bias in mean dissolved N2O values due to low spatial and temporal data resolution. Estimating fluxes to the area representing all estuaries in India may be prone to significant error. We have calculated the flux budget for individual estuaries, where samples were collected, and the mean saturation was used to apply to other Indian estuaries where data were not available. Since other Indian estuaries were mainly minor estuaries and unpolluted, being situated away from the human settlements, their mean N2O was computed from the data measured in non-polluted estuaries, given in Table 1. However, the calculated areas of Indian estuaries can have an error of up to 15% (Qasim, 2003). The transfer velocity versus wind speed relations carry low errors at the lower wind speeds (up to 20%), which are normally encountered in our study region (<2 m s−1). Based on our 28 Indian estuaries study, the uncertainty in Indian estuarine N2O saturations can be 25% (1σ of the estuarine mean) including the uncertainty in N2O analysis. Using these individual errors, the maximum uncertainty in our N2O emission estimate for Indian estuaries was up to ±62%.
The present study reveals that Indian estuaries are a source for atmospheric N2O. A wide range of N2O saturation levels were observed in the Indian estuaries varying from 70 to 631% and from 75 to 567% during the wet and dry periods, respectively. Exceptionally high saturation (5902%) was observed only in the Ponnayar estuary during the wet period. The annual mean N2O saturation in the Indian estuaries (204±137%) was significantly less than European (271–465%) and American estuaries (165–618%). The mean flux of N2O from the Indian estuaries amounts to 1.07 and 1.65 µmol N2O m−2 d−1 during the wet and dry periods, respectively, with annual mean of 1.34 µmol N2O m−2 d−1, which is significantly less than European estuaries (~2.7 µmol N2O m−2 d−1). Such low saturation and fluxes of N2O in the Indian estuaries were related to mean low concentrations of DIN and nitrification rates compared to world estuaries. Despite the high amount of artificial fertilizers, in terms of nitrogen and phosphorus, used in India which are expected to end up in the estuaries, however, they are little modified within the estuary, due to high flushing rates during the wet period. Sarma et al. (2012) calculated the mean flushing time for the Indian estuaries to be <10 d, whereas it is >40 d for the estuaries from Europe and USA. Hence, microbes are not able to oxidize ammonium efficiently resulting in low nitrification rates in the Indian estuaries. In addition to this, Indian estuaries due to less human settlements along the banks of Indian estuaries receive less domestic and industrial pollution. As a result, Indian estuaries contribute less N2O to the atmosphere than elsewhere in the world.
We would like to thank Director, National Institute of Oceanography and Scientist-in-charge, Regional Centre for constant encouragement and support. We appreciate the Council of Scientific and Industrial Research (CSIR) for financial support through Supra Institutional Project (SIP 1308). We appreciate Drs. R. Rengarajan and P. Parameswaran for their help during sampling along the west coast of India. We would also like to thank two anonymous reviewers for their constructive comments and suggestions to improve the clarity of the manuscript. This is NIO contribution number: 5333.
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