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Tidal and spatial variability of nitrous oxide (N2O) in Sado estuary (Portugal)
Estuarine, Coastal and Shelf Science 167 (2015) 466e474
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Tidal and spatial variability of nitrous oxide (N2O) in Sado estuary (Portugal) lia Gonçalves*, Maria Jose Brogueira, Marta Nogueira Ce IPMA, Instituto Portugu^ es do Mar e da Atmosfera, Avenida de Brasília, 6, 1449-006 Lisboa, Portugal
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 April 2014 Received in revised form 6 August 2015 Accepted 29 October 2015 Available online 3 November 2015
The estimate of the nitrous oxide (N2O) fluxes is fundamental to assess its impact on global warming. The tidal and spatial variability of N2O and the air-sea fluxes in the Sado estuary in July/August 2007 are examined. Measurements of N2O and other relevant environmental parameters (temperature, salinity, dissolved oxygen and dissolved inorganic nitrogen e nitrate plus nitrite and ammonium) were recorded during two diurnal tidal cycles performed in the Bay and Marateca region and along the estuary during ebb, at spring tide. N2O presented tidal and spatial variability and varied spatially from 5.0 nmol L1 in Marateca region to 12.5 nmol L1 in Sado river input. Although the Sado river may constitute a considerable N2O source to the estuary, the respective chemical signal discharge was rapidly lost in the main body of the estuary due to the low river flow during the sampling period. N2O varied with tide similarly between 5.2 nmol L1 (Marateca) and 10.0 nmol L1 (Sado Bay), with the maximum value reached two hours after flooding period. The influence of N2O enriched upwelled seawater (~10.0 nmol L1) was well visible in the estuary mouth and apparently represented an important contribution of N2O in the main body of Sado estuary. Despite the high water column oxygen saturation in most of Sado estuary, nitrification did not seem a relevant process for N2O production, probably as the concentration of the substrate, NHþ 4 , was not adequate for this process to occur. Most of the estuary functioned as a N2O source, and only Marateca zone has acted as N2O sink. The N2O emission from Sado estuary was estimated to be 3.7 Mg NeN2O yr1 (FC96) (4.4 Mg NeN2O yr1, FRC01). These results have implications for future sampling and scaling strategies for estimating greenhouse gases (GHGs) fluxes in tidal ecosystems. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Nitrous oxide Spatial variability Tidal cycles Upwelling Air-sea fluxes Sado estuary
1. Introduction Nitrous oxide (N2O) is an important long-lived greenhouse gas (GHGs) in terms of radiative forcing (0.181 W m2 in 2012) (NOAA, 2013) and represents the major anthropogenic contributor to stratospheric ozone destruction (Ravishankara et al., 2009). The N2O atmospheric lifetime is relatively long (120 years) compared with other GHGs but its global warming potential is 310 times greater than that of carbon dioxide, in a time horizon of 100 years, and accounts for about 6.2% to the overall global radiative forcing (Forster et al., 2007). The global mean level of N2O increased from about 270 ppb prior to industrial times up to 324.2 ± 0.1 ppb in 2011, which is 1.0 ppb above the previous year and 120% of the preindustrial level. The annual increase from 2010 to 2011 is greater
* Corresponding author. E-mail address: [email protected] (C. Gonçalves). http://dx.doi.org/10.1016/j.ecss.2015.10.028 0272-7714/© 2015 Elsevier Ltd. All rights reserved.
than the mean increase rate over the past 10 years (0.78 ppb yr1) (WMO, 2013). The ocean is a large contributor to atmospheric N2O budget accounting for 4.5 Tg NeN2O yr1, which represents approximately 23% of the current estimated global N2O emissions (19.8 Tg NeN2O yr1) (Syakila and Kroeze, 2011). However, N2O emissions from the oceans are not uniformly distributed as processes contributing to its production in the ocean are complex and oxygen dependent (Suntharalingam and Sarmiento, 2000). In aerobic environments, N2O is primarily formed through nitrification (NHþ 4 / NO2 / NO3 ) as a by-product (Bange, 2008), and in suboxic conditions N2O can also be formed as an intermediate in the denitrification process during nitrite reduction (NO 3 / NO2 / NO / N2O / N2) (Ward, 2008). These microbially-mediated nitrogen transformations are strongly sensitive to the ongoing environmental changes, although the exact metabolism used for N2O production and its respective contribution to the global N2O inventory in the ocean remains unclear (Bange et al., 2010; Codispoti, 2010). Estuaries, coastal
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regions and upwelling areas are important sites of N2O emissions. Upwelling provides an effective pathway for ventilating N2O produced primarily in subsurface waters to the atmosphere (e.g. Charpentier et al., 2010; Cornejo et al., 2006; Foster et al., 2009; Naqvi et al., 2000). The contribution of Portuguese coastal upwelling system to N2O emission was evaluated to range from 0.040 to 0.102 Gg NeN2O yr1 (Gonçalves et al., 2012), which corresponds to 0.02e0.05% of the global emissions from coastal upwelling areas (0.4 Tg NeN2O yr1, Anderson et al., 2010). Further, a N2O flux of 15 mmol m2 d1 was estimated from Setúbal Bay during an upwelling event (Gonçalves et al., 2012), which is considered a high emission, according to the criterion proposed by Paulmier et al. (2008) (>8.1 mmol m2 d1). Estuaries are characterized by high variability of hydrodynamics and biogeochemistry, related to topographic features, environmental factors and tidal fluctuations, being very sensitive to human activities. As a consequence of their high productivity and additional anthropogenic nitrogen inputs over recent decades, rates of microbial N2O production have increased contributing to the enhancement of N2O emission from these ecosystems (De Wilde and De Bie, 2000; Garnier et al., 2006; Kroeze et al., 2010; LaMontagne et al., 2003; Marty et al., 2001). Considerable efforts have been made in recent decades to quantify the N2O fluxes in different coastal ecosystems, especially in estuaries. Barnes and Upstill-Goddard (2011) identified European estuaries (Iberian estuaries not included) as important N2O sources, representing a contribution of 6.8 ± 13.2 Gg NeN2O yr1 to global emissions. In recent years, studies on the N2O dynamics and emissions have been carried out in some Portuguese estuaries (e.g. Cabrita and Brotas, 2000; Cartaxana and Lloyd, 1999; Gonçalves et al., 2010; Middelburg in Barnes and Upstill-Goddard, 2011; Teixeira et al., 2010, 2013). However, due to a great diversity of hydrological and geomorphological conditions and anthropogenic pressures on these systems, further investigation is required. In this paper we analyze the first results of tidal and spatial variability of N2O concentrations in the Sado estuary, we assess the importance of the respective sources and estimate N2O fluxes and contribution of this system to the global emissions. 2. Materials and methods 2.1. Area description The Sado estuary is the second largest estuary in Portugal, with an area of approximately 180 km2 (Ferreira et al., 2003). It is located on the western Portuguese coast, Setúbal Peninsula, and discharges into the Atlantic Ocean. Most of the estuary is classified as a natural reserve, although it encloses Setúbal city border and important industrial and harbor-associated activities mainly on the northern margin, which represent a considerable anthropogenic pressure (Lillebø et al., 2011). The main nitrogen sources to the estuary are the load from the Sado river which aggregates the main agricultural, domestic and industrial sources from the river basin (approximately 2500 ton yr1) and the effluents from domestic (191 ton yr1) and industrial (1262 ton yr1) origin (Ferreira et al., 2003). The intertidal area includes large areas of salt marshes and intertidal flats and corresponds to approximately 30% of the total estuary area (OSPAR, 2002). The estuary comprises a wide bay, partially separated by intertidal sandbanks into the Northern and the Southern Channels and is linked to the ocean by a narrow and deep channel (maximum depth of 50 m) (Neves, 1986). The Sado estuary margins are also subjected to intensive agriculture, playing an important role in local and national economy. The hydrodynamics of the Sado estuary is forced by tides, which are semidiurnal and range from about 1.6 m at spring tides to 0.6 m at neap tides,
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and by the Sado River discharge. The river presents an annual mean flow of 40 m3 s1 (Ferreira et al., 2003) displaying, however, a striking seasonal variability with very low freshwater discharges occurring in summer. Thus, during spring/summer, when the river flow is low, the hydrography of the Sado estuary is dominated by tide, and the coastal Atlantic waters inundate the estuary. The Sado coastal zone is largely influenced by the coastal upwelling which develops seasonally (MarcheSeptember) along the Iberian coast. The system also referred as a lagoon-type estuary (Cabeçadas et al., 1999b) has a water volume of 500 106 m3 and mean water residence time of 21 days (Ferreira et al., 2003). Marateca zone, which comprises an area of 25.6 km2 (Ferreira et al., 2003), is a shallow specific area of the estuary, mostly occupied by extensive intertidal flats and salt marshes, being greatly exposed to light and wind which favors the evaporation. Salt-pans exploitation is carried out over this area and the respective runoff influences the salinity of the estuarine waters. 2.2. Sampling The sampling programme was carried out during ebb tide (spring tide) at 12 stations located along the Sado estuary, from the Alc acer Channel to the estuary mouth, between 31 July and 02 August 2007, on board the research vessel Tellina (Fig. 1). The Sado ~o). Additionally, samRiver input was also sampled (St.1, S. Roma pling was undertaken along the tidal cycle (spring tide) at two fixed estuarine sites with very distinct morphology and hydrodynamics, one in the Marateca channel and another one at the lower estuary (Sado Bay) (Fig. 1). Sampling was performed when upwelling conditions prevailed in the coastal area adjacent to Sado estuary (Fig. 2). Surface water (0.2 m depth) samples were collected in triplicate for analysis of chemical parameters (nitrate plus nitrite, ammonium, oxygen and nitrous oxide) using 2 L Niskin bottles (General Oceanics). The river flow was reduced (Q ¼ 0.5 m3 s1; Table 1) when sampling was carried out, so the estuary hydrodynamics was dominated by the tide. 2.3. Analytical procedures Temperature was determined in situ with a Seabird SBE19/CTD probe. Practical salinity measurements were carried out using a
Fig. 1. Map of Sado estuary showing the location of sampling sites along the estuary (numbered dots). Station B e Bay tidal cycle; station M e Marateca tidal cycle.
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Upwelling Index (m-3 s-1 km-1)
700 600 500 400 300 200 100 0 -100 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 Days (July 2007) Fig. 2. Upwelling index (July 2007).
temperature-controlled conductive salinometer (Guideline), calibrated with respect to a certified IAPSO Standard Seawater reference. Meteorological parameters were determined using a portable meteorological station (Campbell Scientific CR 510). Measured wind speeds were converted to wind speed at 10 m height (u10) using a logarithmic correction (Hartman and Hammond, 1985). To calculate the upwelling index (UI), Ekman transport (Q) is mez-Gesteira et al., 2006; derived from the wind stress (t) fields (Go Santos et al., 2012), registered at a permanent meteorological station located at Sines (37.57 N) (OGIMET, 2013). The zonal (tx) and meridional (ty) components of wind stress were calculated on the basis of daily geostrophic wind components (Wx, Wy) at 10 m above the sea surface, as follows:
1=2 1=2 tx ¼ ra Cd Wx2 þ Wy2 Wx ; and; ty ¼ ra Cd Wx2 þ Wy2 Wy and then, Qx ¼ y/rw f and Qy ¼ x/rw f, where rw is the density of seawater (1025 kg m3), Cd is the empirical dimensionless drag coefficient (1.3 103) according to Hidy (1972), ra is the density of air (1.22 kg m3 at 15 C) and f is the Coriolis parameter defined as twice the vertical component of the Earth's angular velocity, U, at latitude q, given by f ¼ 2Usin(q), where U ¼ 7.292 105 s1. Finally, UI was calculated through the equation UI ¼ (sin((4p)/2)$Qx) þ (cos((4-p)/2)$Qy), where 4 is the angle between the mez-Gesteira et al., 2006). Thus, shoreline and the equator (Go positive (negative) UI values mean upwelling favorable (unfavorable) conditions. The Sado River flow, measured at the hydrometric station of Moinho da Gamitinha (37.941 N, 8.383 W) upstream of the Sado estuary, was obtained from SNIRH data base (SNIRH, 2013).
The Winkler method (Aminot and Chaussepied, 1983) was used to determine dissolved oxygen (referred herein as DO). Precision of the method was in the range of 0.08%e0.25%. DO saturation, expressed in %, was determined as the ratio of the oxygen concentration determined and the equilibrium values of DO calculated with Weiss (1970) equation. Water samples for determination of dissolved inorganic nitrogen (DIN) were filtered through acetate cellulose filters (pore size 0.45 mm) and frozen until analysis. Analyses were carried out using a TRAACS auto-analyzer following colorimetric techniques outlined by the manufacturer. Estimated precision was ±0.8% for nitrate plus nitrite (referred as NO 3 þ NO2 ) and ±2.0% for ammonium (referred as NHþ 4 ), at mid-scale concentrations. Accuracy of nutrient measurements was maintained by using daily CSK Standards (WAKO, Japan). For the determination of nitrous oxide (N2O) three replicates of bubble free sub-samples were poured into 20 mL glass vials, overflowed more than 100 mL of water, immediately poisoned with 40 mL of saturated aqueous mercury chloride (HgCl2) to stop biological activity, and the sample vial sealed with gastight cap. The vials were stored upside down, in the dark, at 4 C in the refrigerator until analysis, performed within 10 days. Samples containing air bubbles were discarded. Headspace N2O concentration was determined using a gas chromatograph (GC-3800, Varian) equipped with an electron capture detector (63Ni-ECD). In this procedure 5 mL of highly purified helium (purity ¼ 99.9999%) was injected into the sampling vial, using an airtight syringe, and 5 mL water sample was displaced. Equilibrium was reached in a headspace CombiPAL autosampler being the vials vigorously shaken for 4 h. Gas chromatographic separation was carried out using a stainless steel column packed with 80/100 (mesh) Porapak. To remove water vapor and carbon dioxide, absorbent columns, packed respectively with Mg(ClO4)2 and Carbosorb, were located in the carrier gas line between the sample loop and the separation column. Calibration of ECD response was done using standard N2O gas mixtures in synthetic air (Air Liquide) and the precision of the method was 3% (30 replicate measurements using samples containing 10 nmol L1 of N2O). In situ concentration of N2O was calculated from the concentrations measured in the headspace according to the solubility equation of Weiss and Price (1980). The N2O equilibrium concentrations were calculated assuming an atmospheric N2O mixing ratio of 319 ± 0.12 ppb (Forster et al., 2007). N2O saturation, expressed in percentage (%) was determined as the ratio of the measured dissolved N2O concentration and the equilibrium concentration. The N2O air-sea flux, FN2 O (mmol m2 d1), was estimated as FN2 O ¼ kN2 O $DN2O, where DN2O (nmol L1), the apparent N2O productioneconsumption, is the difference between the measured concentration and the equilibrium concentration with the atmosphere in the estuarine water; kN2 O (cm h1) is the N2O transfer velocity, which is expressed as a function of the wind speed and the Schmidt number (Sc). Since no direct measurements of kN2 O were made in situ, we used both the k-wind parameterization proposed by Carini et al. (1996) and Raymond and Cole (2001) in order to minimize any substantial errors in the estimated air-sea fluxes, due to the use of a single k relationship. The gas transfer velocities and
Table 1 Hydrological characteristics of Sado estuary and meteorological conditions observed in July/August 2007. Q e Sado River flow; u10 e wind speed at 10 m heigh. Sampling date 31 July 01 August 02 August a b
Estuary (spatial) Sado Bay (tidal cycle) Marateca (tidal cycle)
Tidal amplitude (m)
Qa (m3 s1)
u10b (m s1)
0.5e3.5 0.5e3.6 0.6e3.6
0.5
3.1e8.8 3.2e9.0 3.6e9.7
Q e Sado River mean flow 10 days before sampling date (SNIRH, 2013). u10 e Average wind speed at 10 m height, measured 10 days before sampling date.
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air-sea fluxes were estimated using in situ wind speeds. The coefficients kN2 O were corrected at in situ temperature by using the relationship kN2 O /k600 ¼ (ScN2 O /600)0.5, where ScN2 O is the Schmidt number for N2O calculated according to the equation of Wanninkhof (1992). Positive N2O fluxes indicate emission of N2O to the atmosphere and negative values represent uptake from the atmosphere. 2.4. Data analysis Box-and-whisker plots are used to give a first insight on the variability of water quality parameters. The central horizontal line of the box is the median of the data, which is the point where 50% of the data is above it and 50% below it. The bottom and the top of the box represent the 25th and 75th percentiles (quartiles), and the ends of the whiskers are the 5th and 95th percentiles. The notch in the box is the 95% confidence interval of the median. These plots were developed with Grapher (version 9.6) software. Isopleth maps were generated with Surfer (version 8.0) software. 3. Results 3.1. Tidal variability A first comparison of data obtained along tidal cycles at the Sado Bay and Marateca (Fig. 3) shows that most of parameters, temperature, salinity, DO and N2O, exhibit significant differences between the Sado Bay and Marateca, as data boxes of these parameters do not overlap. In the Bay, lower median values of temperature and salinity and higher values of DO and N2O were measured. Median values of temperature increased from 18 C in the Bay to 24 C in Marateca. Also, salinity median value increased from 36 in the Bay to 36.4 in Marateca, where the range of values was wider and the maximum exceeded 36.8. DO median value was higher in the Bay (~230 mmol L1) than in Marateca (~195 mmol L1), and also a wider range of levels was measured. DO values were close to saturation in the Bay and down to 80% in Marateca, which reflects higher oxygen utilization and lower water renewal in this last zone. þ The NO 3 þ NO2 and NH4 exhibited a greater similarity in Mar ateca and Bay areas. NO3 þ NO 2 median concentration in the Bay was 1.7 mmol L1 and in Marateca 1.4 mmol L1. However, a higher range of values was observed in the Bay revealing a major tidal influence. Median NHþ 4 concentration value was also slightly higher in the Bay (2.2 mmol L1) than in Marateca (1.6 mmol L1), although a higher maximum (3.1 mmol L1) was reached at this last site. In relation to N2O, median value is about twice that observed in Marateca, suggesting the existence of additional sources/production of this biogas in the Bay. In this area, surface water was N2O supersaturated, reaching a maximum value of 124%. In Marateca N2O concentrations were, in general, below the equilibrium concentration and a minimum saturation value of 80% was detected. þ The variability of temperature, salinity, DO, NO 3 þ NO2 , NH4 and N2O with the tide is shown in Fig. 4. In the Bay, tidal influence was more perceptible on temperature, NO 3 þ NO2 and N2O, while in Marateca the tidal influence is more visible on salinity, NHþ 4 and DO. In both areas the highest values of temperature and salinity were measured at low tide (LT), with maximum values occurring in Marateca, probably as a consequence of greater evaporation over this shallow area where salt-pans are still working. The estuarine water was well oxygenated along both tidal cycles, although higher values were detected in the Bay (Fig. 4a). The maximum value (240 mmol L1; 98.5% saturation) was reached at high tide (HT)/slack tide, reflecting, in particular, a more intense circulation and seawater exchange. In Marateca (Fig. 4b) DO concentrations increase until mid-ebb, when a value of 213 mmol L1
þ Fig. 3. Box plots of temperature, salinity, DO, NO 3 þ NO2 , NH4 and N2O along tidal cycles in Sado Bay and Marateca.
(102% saturation) is attained. In the Bay (Fig. 4a), NO 3 þ NO2 and N2O increased, in general, during the flood (values ranging between 0.2e2.1 mmol L1 and 7.6e10.0 nmol L1, respectively) attaining the highest values 2e3 h after the high tide. This pattern may reflect the complex estuarine circulation as given the strong curvature of the entrance channel of
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(Fig. 4a). In Marateca, NHþ 4 values ranged between 1.3 and 2.3 mmol L1 (Fig. 4b). 3.2. Spatial variability The spatial distribution of environmental parameters (temper þ ature, salinity, DO, NO 3 þ NO2 , NH4 and N2O) along Sado estuary, during ebb tide, is shown in Figs. 5 and 6. There was (Fig. 5a) a welldefined band of colder water (19 Ce21 C) visible in the lower estuary, indicating a major influence of seawater, likely from upwelling origin. Maximum temperature values (24 Ce28 C) were reached in Marateca and Alc acer Channel entrance. The estuarine salinity pattern reveals that in the lower part of the Bay values no higher than 36.0 were recorded, despite the greater seawater influence (Fig. 5b). A minimum of 0.5 was measured in the upper estuary (Sado River). However, due to the low Sado River discharge during sampling period the influence of fresh water on the main water body of the estuary was almost imperceptible. The highest salinity value (36.1) was measured in
þ Fig. 4. Variability of temperature, salinity, DO, NO 3 þ NO2 , NH4 and N2O in (a) Bay tidal cycle and (b) Marateca tidal cycle. Tidal amplitude is represented by dotted lines. HT e High Tide; LT e Low Tide. (Error bars ¼ ±1 SD).
the estuary the interaction between the tidal circulation patterns and the estuarine morphology leads to an important residual secondary flow (Martins et al., 2002) close to our sampling point. The increase in NO 3 þ NO2 and N2O along the tidal cycle suggests the influence of more NO 3 þ NO2 and N2O enriched seawater, likely recently upwelled, given the intense upwelling episode occurring during this sampling period as mentioned earlier. Furthermore, maximum levels of NO 3 þ NO2 and N2O detected along tidal cycle agree with those found by Gonçalves et al. (2012) in a previous study carried out in Setúbal Bay, near to the Sado estuary mouth 1 N2O), during (approximately 5e8 mmol L1 NO 3 and 10.0 nmol L upwelling favorable conditions. In Marateca (Fig. 4b), NO 3 þ NO2 show a similar tidal variability, despite the lower levels registered (0.8e2.0 mmol L1). Levels of N2O range only from 5.2 nmol L1 to 6.5 nmol L1 (80%e100% saturation), pointing out to a possible N2O sink in this area (e.g. Kieskamp et al., 1991). The NHþ 4 values in the Bay increased slightly from 1.5 to 2.8 mmol L1 in the first part of flooding declining to a value approximately constant (2.3 mmol L1) until high tide/mid ebb
Fig. 5. Spatial distribution of (a) temperature, (b) salinity and (c) DO, in July 2007.
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(a) NO3- + NO2(μmol L-1) 1.2 3.4 1.4
0.2 11.4
(b) NH4+ (μmol L-1) 0.9 0.8 0.9
1.0
1.9
1.3 1.8
(c) N2O (nmol L-1) 5.0
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for 35%. Concerning NO 3 þ NO2 (Fig. 6a) a considerable spatial variability was found in the estuary. The highest value ~o, indicating the nutrient input (11.4 mmol L1) was found at S. Roma from the Sado River to the estuary. However, due to the very low Sado River flow in this summer period, levels decreased rapidly towards mid-estuary where concentrations varied from 0.2 to 2.0 mmol L1. Downstream, concentrations increased again, reaching 3.0 mmol L1 in the estuary mouth, which constitute an additional signal of upraised nutrient-rich water, as already observed in the Bay along the tidal cycle. In Marateca zone NO3 þ NO 2 concentration did not surpass1.2 mmol L1. Regarding NHþ 4 spatial distribution (Fig. 6b), a small variability was detected during sam1 pling period. At mid Bay, NHþ 4 values varied between 0.9 mmol L 1 and 2.0 mmol L while the minimum value was registered in Marateca (0.8 mmol L1). These low levels compare with those found by Cabeçadas and Brogueira (1991) in Marateca (approxiþ mately 0.5e0.6 mmol L1 NO 3 and NH4 ) and by Cabeçadas et al. þ (1999a) in Sado Bay (approximately 1e2 mmol L1 NO 3 and NH4 ) in summer. The distribution pattern of N2O (Fig. 6c, d) reveals that the Sado River is a source of this biogas to the estuary, as a maximum value ~o (12.5 nmol L1; 162% saturation), similarly to was found at S. Roma þ NO . But also in this case, the very low Sado River flow in NO 3 2 summer leads to a decrease towards mid-estuary where N2O levels varied from 6.0 to 7.0 nmol L1. Concentrations increased again towards the estuary mouth where a concentration of 10.0 nmol L1 was attained. Once again, N2O levels compare with data obtained by Gonçalves et al. (2012) in the coastal zone adjacent to the Sado estuary and constitute a signal of upraised N2O enriched water. N2O saturation values reached the maximum value (143%) at the estuary mouth, being saturation levels above equilibrium over most of the estuary, except in Marateca. This indicates that the estuary acts predominantly as a potential source of N2O to the atmosphere.
3.3. N2O air-sea fluxes during tidal cycles
11.5 6.3
7.1 12.5
(d) N2O (% saturation) 91 143 101
120 162
þ Fig. 6. Spatial distribution of (a) NO 3 þ NO2 , (b) NH4 and (c, d) N2O, in July 2007.
Marateca, as a consequence of the great evaporation over the area. The surface water was well oxygenated, DO levels ranging between 210 mmol L1 in Marateca and 240 mmol L1 in lower/central estuary (Fig. 5c). þ DIN was dominated by NO 3 þ NO2 , while NH4 accounted only
N2O air-sea fluxes, based on gas transfer velocity parameterization of Carini et al. (1996) (FC96) and Raymond and Cole (2001) (FRC01) along tidal cycles in the Sado Bay and Marateca are shown in Fig. 7. During the sampling period persistent and strong winds were recorded with intensity ranging between a minimum of 3.2 m s1 and a maximum of 9.7 m s1. Distinct N2O flux patterns could be observed along the Sado and Marateca tidal cycles. In the Sado Bay (Fig. 7a) N2O air-sea fluxes were always towards the atmosphere, increasing progressively from a minimum value of 0.7 mmol m2 d1 (FC96) (0.9 mmol m2 d1, FRC01) at mid-flood tide to a maximum value of 7.0 mmol m2 d1 (FC96) (17.0 mmol m2 d1, FRC01) during the first hours of ebb tide. The highest emissions match approximately the highest N2O saturations, revealing the influence of N2O enriched upwelled seawater on N2O fluxes. The mean N2O air-sea flux along the tidal cycle was positive (3.0 mmol m2 d1, FC96 and 6.1 mmol m2 d1, FRC01) corresponding to N2O concentration mean value of 8.8 nmol L1 (112% saturation) and high wind speed (mean value 6.9 m s1). By contrast, in Marateca (Fig. 7b) N2O air-sea fluxes along the tidal cycle were mostly negative and a minimum value of 6.2 mmol m2 d1 (FC96) (11.4 mmol m2 d1, FRC01) was attained at high tide, corresponding to the lowest N2O saturation level (approximately 80%). 3.4. N2O air-sea fluxes along Sado estuary N2O air-sea fluxes estimated along Sado estuary (Fig. 8) were mostly positive, except for the Marateca zone. In general, values increased progressively from the central part of the Bay (St. 9)
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estuary to the global N2O emissions was estimated. Considering an ~o, mid estuary zone and area of 151.4 km2, which includes S. Roma Sado Bay functioning as N2O source and assuming a mean N2O flux of 3.0 mmol m2 d1 (FC96) (3.8 mmol m2 d1, FRC01) an emission of 4.3 Mg NeN2O yr1 (FC96) (5.5 Mg NeN2O yr1; FRC01) is extrapolated. Further, considering an area of 25.6 km2 for Marateca zone and a N2O flux of 2.2 mmol m2 d1 (FC96) (4.3 mmol m2 d1; FRC01) an uptake of N2O from the atmosphere of 0.6 Mg NeN2O yr1 (FC96) (1.1 Mg NeN2O yr1; FRC01) is estimated. Hence, a N2O air-sea net/emission from Sado estuary is estimated as 3.7 mmol m2 d1 (FC96) (4.4 Mg NeN2O yr1; FRC01). 4. Discussion
Fig. 7. Air-sea N2O fluxes (bar charts) along tidal cycles in (a) Bay and (b) Marateca. Wind speed is represented by solid line and tidal amplitude by dotted line. HT e High Tide; LT e Low Tide. (Error bars ¼ ±1 SD).
towards the estuary mouth (St. 20) where a maximum value of 10.4 mmol m2 d1 (FC96) (17.0 mmol m2 d1, FRC01) was attained. The estimated Sado estuary mean N2O air-sea flux was positive (3.0 mmol m2 d1, FC96 and 3.8 mmol m2 d1, FRC01) and similar to the one found in the Bay tidal cycle (3.0 mmol m2 d1, FC96 and 6.1 mmol m2 d1, FRC01). Concerning Marateca zone a negative N2O flux of 2.2 mmol m2 d1 (FC96) (4.3 mmol m2 d1; FRC01) was estimated. Although N2O air-sea fluxes have been obtained during a single sampling and being aware of the seasonal variability that, in general, characterizes estuarine systems, the contribution of Sado
Fig. 8. Air-sea N2O fluxes (bar charts) along Sado estuary. Wind speed is representing by solid line.
The present study reveals that dissolved N2O shows considerable spatial and tidal variability in the Sado estuary, in summer. In this period the Sado river is an important source of N2O as maximum concentration was found in the riverine input zone (St.1, S. Rom~ ao). Nevertheless, the N2O chemical signal from the Sado River discharge was lost further in the main body of the Sado estuary, as water flow was reduced in the studied period. In fact, the impact of nutrient input in the Sado estuary is classified as moderate, as a result of the high dilution potential and the moderate flushing potential of the estuary, according to Ferreira et al. (2003). Furthermore, with the increase of percentage of treated wastewater in the estuarine area it is expected, in the future, there to be a significant reduction of nutrient pressure in the estuary and consequently a decrease of N2O levels in Sado estuary. In the turbidity maximum zones (TMZ) of estuaries higher N2O concentrations are usually observed (Barnes and Owens, 1998; Abril et al., 2000). However, during the study period no samples for N2O analysis were collected along the TMZ of the Sado estuary cer do Sal) (e.g. Cabeçadas (approximately between St. 8 and Alca et al., 1994) and no conclusions about the existence of such N2O estuarine source can be derived. In oxygen saturated waters as the Sado estuary is, nitrification may be an important contributor to N2O production (e.g. Bianchi et al., 1999). Nevertheless, in the Sado estuary N2O production through pelagic nitrification could not be deduced from the relevant parameters connected with this process, since no significant correlations have been found between N2O and NHþ 4 , NO3 þ NO2 . The half saturation constant (Ks) for nitrification process was estimated to be 1.9e4.2 mmol L1 of NH3 for Nitrosomonas oligotropha and N. ureae, and even much higher (30e61 mmol L1 of NH3) for N. europaea (Koops and € ser, 2001). Despite no information on the nitriPommerening-Ro fying bacterial community of Sado estuary being available, the concentration of the substrate NHþ 4 does not seem adequate for nitrification process to occur in the water column during the study period. In contrast to other estuaries including the Portuguese Tagus estuary (Gonçalves et al., 2010), N2O levels in the main body of the Sado estuary increased towards the estuary mouth in the summer period, which can be attributed to the influence of upwelled water containing higher N2O concentrations. As a matter of fact, levels of N2O in the lower estuary compare with those found in coastal waters adjacent to the Sado estuary during the upwelling event (Gonçalves et al., 2012). Apparently, the income of upwelled seawater in Sado estuary constitutes the most important N2O source to the estuary during summer. Despite the high N2O variability observed during tidal cycles and along the estuary, N2O saturation levels were above equilibrium, except in Marateca. The highest values of N2O saturation attained in the Sado estuary (92%e162%) are similar to those reported from less eutrophic European estuaries (Table 2). For example, maximum N2O saturation values of 118% and 143% were reported from Tay and
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473
Table 2 N2O emissions from several European estuaries (adapted from Barnes and Upstill-Goddard, 2011). Estuary
Area (km2) Nitrous oxide (N2O)
Sampling
Reference
Seasonal study Single survey Seasonal study Seasonal study Single survey Seasonal study Single survey Single survey Seasonal study Single survey
De wilde and de Bie (2000) J. Middelburg in Barnes and Upstill-Goddard (2011) J. Middelburg in Barnes and Upstill-Goddard (2011) Barnes and Upstill-Goddard (2011) Barnes and Upstill-Goddard (2011) Dong et al. (2004) De wilde and de Bie (2000) J. Middelburg in Barnes and Upstill-Goddard (2011) Gonçalves et al. (2010) This study
Saturation (%) Air-sea flux (mmol m2 d1) Emission (Mg NeN2O yr1) Scheldt, Belgium Ems, Germany Gironde, France Humber, UK Tay, UK Stour, UK Loire, France Douro, Portugal Tagus, Portugal Sado, Portugal a b c d
269 162 442 303.6 121.3 24.4 41 2.4 320 180
710 181e1794 120e463 100e4250 100e118 143 84e271 280e650 101e147 91e162
66.6a 76.7a 25.5a 76.6a 2.5a 20.6a 14.3a 74.7a 0.1 to 10.4a 2.2b to 3.8c
1.8 102 1.3 102 1.2 102 2.5 102 2.5 5.2 6.1 1.9 12.8e16.0d 3.7e4.4
Estimated using Clark et al. (1995) relationship. Carini et al. (1996) relationship. Raymond and Cole (2001) relationship. Unpublished data.
Stour estuaries, respectively. Also, Gonçalves et al. (2010) found in the Tagus estuary maximum N2O saturation values of 147%. The contrasting behavior of N2O air-sea fluxes between Sado bay and Marateca is likely related to the specific morphological features of Marateca, namely shallow water column and extensive intertidal areas. Otherwise, the simultaneous low concentrations of N2O and NO 3 þ NO2 suggest that N2O may be used in the denitrification process in sediments. The phenomenon of N2O influxes has been described for several marine systems, as in intertidal (Middelburg et al., 1995; Miller et al., 1986), brackish subtidal (Jensen et al., 1984) and marine sediments (Van Raaphorst et al., 1992) as well as in experiments on denitrification in subtidal sediments (Limfjorden-Denmark) (Jensen et al., 1984). The utilization of N2O as a terminal electron acceptor for organic carbon degradation in the absence of nitrate is a possible explanation for the flux of N2O to the sediment during summer, as during this period oxygen penetration in the sediment is limited and NO 3 pore-water concentrations are usually low (Kieskamp et al., 1991; Koike and Hattori, 1975). The pelagic N2O emission (3.7 Mg NeN2O yr1, FC96; 4.4 Mg NeN2O yr1, FRC01) from the Sado estuary compares with those from other European estuaries such as the Tay (2.5 Mg NeN2O yr1), Stour (5.2 Mg NeN2O yr1) and Loire (6.1 Mg NeN2O yr1; Table 2) but is higher than value reported from Douro (1.9 Mg NeN2O yr1; Barnes and Upstill-Goddard, 2011; Table 2) and much lower than values from Tagus (Gonçalves et al., 2010; Table 2). In a global perspective the estimated N2O emission from Sado estuary represents a reduced fraction (<0.1%) of global emissions from European estuaries (6.8 Gg NeN2O yr1, Barnes and UpstillGoddard, 2011). Nevertheless, higher N2O emissions in estuaries may occur during winter and spring (Sun et al., 2013, 2014) as reported from the nearby Tagus estuary (Gonçalves et al., 2010). Thus, the N2O emission from the Sado estuary on an annual basis, needs further confirmation. Acknowledgments The authors thank the crew of the R/V Telina for their assistance during sample collection. Acknowledgments are also due to collegues of IPMA Oceanography Laboratory for their assistance in sampling, technical and analytical procedures. The research was supported by the PoPesca MARE project (Contract N. 22-05-01FDR-00015) and by the FCT-Portuguese Foundation of Science and Technology (POCI 2010 and FSE) through grant SFRH/BD/28569/ 2006.
References Abril, G., Riou, S.A., Etcheber, H., Frankignoulle, M., de Wit, R., Middelburg, J.J., 2000. Transient, tidal time-scale, nitrogen transformations in an estuarine turbidity maximum-fluid mud system (the Gironde, South-west France). Estuar. Coast. Shelf Sci. 50, 703e715. Aminot, A., Chaussepied, M., 1983. Manuel des analyses chimiques en milieu marin. ans (CNEXO), Brest, France, p. 395. Centre National pour l'Exploitation des Oce Anderson, B., Bartlett, K., Frolking, S., Hayhoe, K., Jenkins, J., Salas, W., 2010. Methane and Nitrous Oxide Emissions from Natural Sources. U.S. Environmental Protection Agency technical report, Washington, D.C., U.S.A, p. 194. Bange, H.W., 2008. Gaseous nitrogen compounds (NO, N2O, N2, NH3) in the ocean. In: Capone, D.G., Bronk, D.A., Mulholland, M.R., Carpenter, E.J. (Eds.), Nitrogen in the Marine Environment, second ed. Elsevier, Amsterdam, pp. 51e94. €scher, C., 2010. Marine pathways to nitrous oxide. Bange, H.W., Freing, A., Kock, A., Lo In: Smith, K.A. (Ed.), Nitrous Oxide and Climate Change. Earthscan, London, UK, pp. 36e62. Barnes, J., Owens, N.J.P., 1998. Denitrification and nitrous oxide concentrations in the Humber estuary, UK, and adjacent coastal zones. Mar. Pollut. Bull. 37 (3e7), 247e260. Barnes, J., Upstill-Goddard, R.C., 2011. N2O seasonal distributions and air-sea exchange in UK estuaries: Implications for the tropospheric N2O source from European coastal waters. J. Geophys. Res. Biogeosci. 116, G01006. http:// dx.doi.org/10.1029/2009JG001156. Bianchi, M., Feliatra, F., Lefevre, D., 1999. Regulation of nitrification in the land^ne River plume (NW Mediterranean). Aquat. ocean contact area of the Rho Microb. Ecol. 18, 301e312. http://dx.doi.org/10.3354/ame018301. Cabeçadas, G., Brogueira, M.J., 1991. The Sado estuary, Portugal: Eutrophication conditions in areas of aquacultural activities. Environ. Pollut. 1, 810e820. ^ncia do azoto na proCabeçadas, G., Brogueira, M.J., Ferronha, H., 1994. A importa rio do Sado. In: 4ª Confere ^ncia Nacional Sobre dutividade prim aria do Estua Qualidade Do Ambiente, vol. I, pp. 181e190. Cabeçadas, G., Nogueira, M., Brogueira, M.J., 1999a. Nutrient dynamics and productivity in three European estuaries. Mar. Pollut. Bull. 38, 1092e1096. Cabeçadas, L., Brogueira, M.J., Cabeçadas, G., 1999b. Phytoplankton spring bloom in the Tagus coastal waters: hydrological and chemical conditions. Aquat. Ecol. 33, 243e250. Cabrita, M.T., Brotas, V., 2000. Seasonal variation in denitrification and dissolved nitrogen fluxes in intertidal sediments of the Tagus Estuary, Portugal. Mar. Ecol. Prog. Ser. 202, 51e65. Carini, S., Weston, N., Hopkinson, C., Tucker, J., Giblin, A., Vallino, J., 1996. Gas exchange rates in the Parker River estuary, Massachusetts. Biol. Bull. 191, 333e334. Cartaxana, P., Lloyd, D., 1999. N2, N2O and O2 profiles in a Tagus estuary salt marsh. Estuar. Coast. Shelf Sci. 48, 751e756. http://dx.doi.org/10.1006/ecss.1998.0475. Charpentier, J., Farías, L., Pizarro, O., 2010. Nitrous oxide fluxes in the central and eastern South Pacific. Glob. Biogeochem. Cycles 24, GB3011,. http://dx.doi.org/ 10.1029/2008GB003388. Clark, J.F., Schlosser, P., Simpson, H.J., Stute, M., Wanninkhof, R., Ho, D.T., 1995. Relationship between gas transfer velocities and wind speeds in the tidal Hudson River determined by the dual tracer technique. In: Jhane, B., Monahan, E. (Eds.), Air-water Gas Transfer. AEON Verlag and Studio, Hanau, Germany, pp. 785e800. Codispoti, L.A., 2010. Interesting times for marine N2O. Science 327, 1339e1340. http://dx.doi.org/10.1126/science.1184945. Cornejo, M., Farías, L., Paulmier, A., 2006. Temporal variability in N2O water content and its airesea exchange in an upwelling area off central Chile (36 S). Mar. Chem. 101, 85e94. http://dx.doi.org/10.1016/j.marchem.2006.01.004. De Wilde, H.P.J., De Bie, M.J.M., 2000. Nitrous oxide in the Schelde estuary:
474
C. Gonçalves et al. / Estuarine, Coastal and Shelf Science 167 (2015) 466e474
production by nitrification and emission to the atmosphere. Mar. Chem. 69, 203e216. http://dx.doi.org/10.1016/S0304-4203(99)00106-1. Dong, L.F., Nedwell, D.B., Colbeck, I., Finch, J., 2004. Nitrous oxide emission from some English and Welsh rivers and estuaries. Water Air Soil Pollut. 4, 127e134. http://dx.doi.org/10.1007/s11267-004-3022-4. Ferreira, J.G., Simas, T., Nobre, A., Silva, M.C., Shifferegger, K., Lencart-Silva, J., 2003. Identification of sensitive areas and vulnerable zones in transitional and coastal Portuguese systems. In: INAG-Instituto da Agua and IMAR-Instituto do Mar (Ed.), Application of the United States National Estuarine Eutrofication Assessement to the Minho, Lima, Douro, Ria de Aveiro, Mondego, Tagus, Sado, Mira, Ria Formosa and Guadiana systems, pp. 95e107. Forster, P., Ramaswamy, V., Artaxo, P., Berntsen, T., Betts, R., Fahey, D.W., Haywood, J., Lean, J., Lowe, D.C., Myhre, G., Nganga, J., Prinn, R., Raga, G., Schulz, M., Van Dorland, R., 2007. Changes in atmospheric constituents and in radiative forcing. In: Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L. (Eds.), Climate Change 2007: the Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge Univ. Press, Cambridge, UK and New York, NY, pp. 129e234. Forster, G., Upstill-Goddard, R.C., Gist, N., Robinson, C., Uher, G., Malcolm, E., Woodward, S., 2009. Nitrous oxide and methane in the Atlantic Ocean between 50 N and 52 S: latitudinal distribution and sea-to-air flux. Deep Sea Res. II 56, 964e976. http://dx.doi.org/10.1016/j.dsr2.2008.12.002. bron, A., Tallec, G., Billen, G., Sebilo, M., Martinez, A., 2006. Nitrogen Garnier, J., Ce behaviour and nitrous oxide emission in the tidal Seine River estuary (France) as influenced by human activities in the upstream watershed. Biogeochemistry 77, 305e326. mez-Gesteira, M., Moreira, C., Alvarez, I., De Castro, M., 2006. Ekman transport Go along the Galician coast (northwest Spain) calculated from forecasted winds. J. Geophys. Res. Biogeosci. 111, C10005. http://dx.doi.org/10.1029/2005JC003331. ~es, M.F., 2010. Seasonal and tidal influence on Gonçalves, C., Brogueira, M.J., Camo the variability of nitrous oxide in the Tagus estuary, Portugal. Sci. Mar. 74 (S1), 57e66. http://dx.doi.org/10.3989/scimar.2010.74s1057. ~es, M.F., 2012. Nitrous oxide content and fluxes Gonçalves, C., Brogueira, M.J., Camo in Setúbal Bay, Portugal, during upwelling events. Cienc. Mar. 38 (1B), 177e190. Hartman, B., Hammond, D., 1985. Gas exchange in San Francisco Bay. Hydrobiology 129, 59e68. Hidy, G.M., 1972. A view of recent airesea interaction research. Bull. Am. Meteorol. Soc. 53, 1083e1102. Jensen, H.B., Jørgensen, K.S., Sørensen, J., 1984. Diurnal variation of nitrogen cycling in coastal, marine sediments. II nitrous oxide emission. Mar. Biol. 83, 177e183. Kieskamp, W.M., Lohse, L., Epping, E., Helder, W., 1991. Seasonal variation in denitrification rates and nitrous oxide fluxes in intertidal sediments of the western Wadden Sea. Mar. Ecol. Prog. Ser. 72, 145e151. Koike, I., Hattori, A., 1975. Energy yield of denitrification: an estimate from growth yield in continuous cultures of Pseudomonas denitrificans under nitrate-, nitriteand oxide-limited conditions. J. General Microbiol. 88, 11e19. http://dx.doi.org/ 10.1099/00221287-88-1-11. €ser, A., 2001. Distribution and ecophysiology of the Koops, H.P., Pommerening-Ro nitrifying bacteria emphasizing cultured species. FEMS Microbiol. Ecol. 37, 1e19. Kroeze, C., Dumont, E., Seitzinger, S., 2010. Future trends in emissions of N2O from rivers and estuaries. J. Integr. Environ. Sci. 7 (S1), 71e78. http://dx.doi.org/ 10.1080/1943815X.2010.496789. LaMontagne, M.G., Duran, R., Valiela, I., 2003. Nitrous oxide sources and sinks in coastal aquifers and coupled estuarine receiving waters. Sci. Total Environ. 309, 139e149. Lillebø, A.I., Coelho, J.P., Pato, P., V alega, M., Margalho, R., Reis, M., Raposo, J., Pereira, E., Duarte, A.C., Pardal, M.A., 2011. Assessment of mercury in water, sediments and biota of a southern European estuary (Sado estuary, Portugal). Water Air Soil Pollut. 214 (1e4), 667e680. http://dx.doi.org/10.1007/s11270010-0457-2. Martins, F., Leit~ ao, P., Neves, R., 2002. Simulating vertical water mixing in homogeneous estuaries: the SADO Estuary case. Hydrobiologia 475/476, 221e227. Marty, D., Bonin, P., Michotey, V., Bianchi, M., 2001. Bacterial biogas production in coastal systems affected by freshwater inputs. Cont. Shelf Res. 21, 2105e2115. Middelburg, J.J., Klaver, G., Nieuwenhuize, J., Markusse, R.M., Vlug, T., Van der
Nat, F.J.W.A., 1995. Nitrous oxide emissions from estuarine intertidal sediments. Hydrobiologia 311 (1e3), 43e55. http://dx.doi.org/10.1007/BF00008570. Miller, L.G., Oremland, R.S., Paulsen, S., 1986. Measurement of nitrous oxide reductase activity in aquatic sediments. Appl. Environ. Microbiol. 51, 18e24. Naqvi, S.W.A., Jayakumar, D.A., Narvekar, P.V., Naik, H., Sarma, V.V.S.S., D'Souza, W., Joseph, S., George, M.D., 2000. Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf. Nature 408, 346e349. Neves, R.J.J., 1986. Hidrodynamical modelling as a toll in waste disposal selection. A casa study on sado estuary. In: Kullenberg (Ed.), The Role of the Oceans as a Waste Disposal Option, pp. 563e576. NOAA (National Oceanic & Atmospheric Administration/Earth System Research Laboratory (www.esrl.noaa.gov/gmd/aggi/aggi.html) (accessed 09.10.13.). OGIMET (Weather Information Service) (www.ogimet.com) (accessed 06.03.13.). OSPAR, 2002. Comprehensive procedure, Portugal, Mondego, Tagus and Sado Estuaries, Maretec and IST. In: OSPAR Convention for the Protection of the Marine Environment of the North-East Atlantic. OSPAR Commission, London. Paulmier, A., Ruiz-Pino, D., Garcon, V., 2008. The oxygen minimum zone (OMZ) off Chile as intense source of CO2 and N2O. Cont. Shelf Res. 28, 2746e2756. http:// dx.doi.org/10.1061/j.csr.2008.09.012. Ravishankara, A.R., Daniel, J.S., Portmann, R.W., 2009. Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326, 123e125. http://dx.doi.org/10.1126/science.1176985. Raymond, P.A., Cole, J.J., 2001. Gas exchange in rivers and estuaries: choosing a gas transfer velocity. Estuaries 24, 312e317. mez-Gesteira, M., Alvarez, Santos, F., DeCastro, M., Go I., 2012. Differences in coastal and oceanic SST warming rates along the Canary upwelling ecosystem from 1982 to 2010. Cont. Shelf Res. 47, 1e6. ~o de Recursos Hídricos do Instituto da Agua, SNIRH (Sistema Nacional de Informaça I.P.) (http://snirh.pt) (accessed 17.10.13.). Sun, Z., Wang, L., Tian, H., Jiang, H., Mou, X., Sun, W., 2013. Fluxes of nitrous oxide and methane in different coastal Suaeda salsa marshes of the Yellow River estuary, China. Chemosphere 90, 856e865. http://dx.doi.org/10.1016/j.chemosphere. 2012.10.004. Sun, Z., Wang, L., Mou, X., Jiang, H., Sun, W., 2014. Spatial and temporal variations of nitrous oxide flux between coastal marsh and the atmosphere in the Yellow River estuary of China. Environ. Sci. Pollut. Res. Int. 21 (1), 419e433. http:// dx.doi.org/10.1007/s11356-013-1885-5. Suntharalingam, P., Sarmiento, J.L., 2000. Factors governing the oceanic nitrous oxide distribution: Simulations with an ocean general circulation model. Glob. Biogeochem. Cycles 14 (1), 429e454. http://dx.doi.org/10.1029/1999GB900032. Syakila, A., Kroeze, C., 2011. The global nitrous oxide budget revisited. Greenh. Gas Meas. Manag. 1 (1), 17e26. http://dx.doi.org/10.3763/ghgmm. 2010.0007. Teixeira, C., Magalh~ aes, C., Boaventura, R.A.R., Bordalo, A.A., 2010. Potential rates and environmental controls of denitrification and nitrous oxide production in a temperate urbanized estuary. Mar. Environ. Res. 70 (5), 336e342. http:// dx.doi.org/10.1016/j.marenvres.2010.07.001. ~es, C., Joye, S.B., Bordalo, A.A., 2013. The role of salinity in Teixeira, C., Magalha shaping dissolved inorganic nitrogen and N2O dynamics in estuarine sedimentwater interface. Mar. Pollut. Bull. 66, 225e229. http://dx.doi.org/10.1016/ j.marpolbul.2012.11.004. Van Raaphorst, W., Kloosterhuis, H.T., Berghuis, E.M., Gieles, A.J.M., Malschaert, J.F.P., Van Noort, G.J., 1992. Nitrogen cycling in two types of sediments of the southern North Sea (Frisian front, broad fourteens): field data and mesocosm results. Neth. J. Sea Res. 28, 293e316. Wanninkhof, R., 1992. Relationship between wind speed and gas exchange over the ocean. J. Geophys. Res. 97, 7373e7382. http://dx.doi.org/10.1029/92JC00188. Ward, B.B., 2008. Nitrification in marine systems. In: Capone, D.G., Bronk, D.A., Mulholland, M.R., Carpenter, E.J. (Eds.), Nitrogen in the Marine Environment. Elsevier, Amsterdam, pp. 199e262. Weiss, R.F., 1970. The solubility of nitrogen, oxygen, and argon in water and seawater. Deep Sea Res. Oceanogr. Abstr. 17 (4), 721e735. http://dx.doi.org/ 10.1016/0011-7471(70)90037-9. Weiss, R.F., Price, B.A., 1980. Nitrous oxide solubility in water and seawater. Mar. Chem. 8, 347e359. http://dx.doi.org/10.1016/0304-4203(80)90024-9. WMO (World Meteorological Organization - Global Atmosphere Watch) (http:// www.wmo.int/gaw) (accessed 05.09.13.).
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Tidal and spatial variability of nitrous oxide (N2O) in Sado estuary (Portugal) lia Gonçalves*, Maria Jose Brogueira, Marta Nogueira Ce IPMA, Instituto Portugu^ es do Mar e da Atmosfera, Avenida de Brasília, 6, 1449-006 Lisboa, Portugal
a r t i c l e i n f o
a b s t r a c t
Article history: Received 2 April 2014 Received in revised form 6 August 2015 Accepted 29 October 2015 Available online 3 November 2015
The estimate of the nitrous oxide (N2O) fluxes is fundamental to assess its impact on global warming. The tidal and spatial variability of N2O and the air-sea fluxes in the Sado estuary in July/August 2007 are examined. Measurements of N2O and other relevant environmental parameters (temperature, salinity, dissolved oxygen and dissolved inorganic nitrogen e nitrate plus nitrite and ammonium) were recorded during two diurnal tidal cycles performed in the Bay and Marateca region and along the estuary during ebb, at spring tide. N2O presented tidal and spatial variability and varied spatially from 5.0 nmol L1 in Marateca region to 12.5 nmol L1 in Sado river input. Although the Sado river may constitute a considerable N2O source to the estuary, the respective chemical signal discharge was rapidly lost in the main body of the estuary due to the low river flow during the sampling period. N2O varied with tide similarly between 5.2 nmol L1 (Marateca) and 10.0 nmol L1 (Sado Bay), with the maximum value reached two hours after flooding period. The influence of N2O enriched upwelled seawater (~10.0 nmol L1) was well visible in the estuary mouth and apparently represented an important contribution of N2O in the main body of Sado estuary. Despite the high water column oxygen saturation in most of Sado estuary, nitrification did not seem a relevant process for N2O production, probably as the concentration of the substrate, NHþ 4 , was not adequate for this process to occur. Most of the estuary functioned as a N2O source, and only Marateca zone has acted as N2O sink. The N2O emission from Sado estuary was estimated to be 3.7 Mg NeN2O yr1 (FC96) (4.4 Mg NeN2O yr1, FRC01). These results have implications for future sampling and scaling strategies for estimating greenhouse gases (GHGs) fluxes in tidal ecosystems. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Nitrous oxide Spatial variability Tidal cycles Upwelling Air-sea fluxes Sado estuary
1. Introduction Nitrous oxide (N2O) is an important long-lived greenhouse gas (GHGs) in terms of radiative forcing (0.181 W m2 in 2012) (NOAA, 2013) and represents the major anthropogenic contributor to stratospheric ozone destruction (Ravishankara et al., 2009). The N2O atmospheric lifetime is relatively long (120 years) compared with other GHGs but its global warming potential is 310 times greater than that of carbon dioxide, in a time horizon of 100 years, and accounts for about 6.2% to the overall global radiative forcing (Forster et al., 2007). The global mean level of N2O increased from about 270 ppb prior to industrial times up to 324.2 ± 0.1 ppb in 2011, which is 1.0 ppb above the previous year and 120% of the preindustrial level. The annual increase from 2010 to 2011 is greater
* Corresponding author. E-mail address: [email protected] (C. Gonçalves). http://dx.doi.org/10.1016/j.ecss.2015.10.028 0272-7714/© 2015 Elsevier Ltd. All rights reserved.
than the mean increase rate over the past 10 years (0.78 ppb yr1) (WMO, 2013). The ocean is a large contributor to atmospheric N2O budget accounting for 4.5 Tg NeN2O yr1, which represents approximately 23% of the current estimated global N2O emissions (19.8 Tg NeN2O yr1) (Syakila and Kroeze, 2011). However, N2O emissions from the oceans are not uniformly distributed as processes contributing to its production in the ocean are complex and oxygen dependent (Suntharalingam and Sarmiento, 2000). In aerobic environments, N2O is primarily formed through nitrification (NHþ 4 / NO2 / NO3 ) as a by-product (Bange, 2008), and in suboxic conditions N2O can also be formed as an intermediate in the denitrification process during nitrite reduction (NO 3 / NO2 / NO / N2O / N2) (Ward, 2008). These microbially-mediated nitrogen transformations are strongly sensitive to the ongoing environmental changes, although the exact metabolism used for N2O production and its respective contribution to the global N2O inventory in the ocean remains unclear (Bange et al., 2010; Codispoti, 2010). Estuaries, coastal
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regions and upwelling areas are important sites of N2O emissions. Upwelling provides an effective pathway for ventilating N2O produced primarily in subsurface waters to the atmosphere (e.g. Charpentier et al., 2010; Cornejo et al., 2006; Foster et al., 2009; Naqvi et al., 2000). The contribution of Portuguese coastal upwelling system to N2O emission was evaluated to range from 0.040 to 0.102 Gg NeN2O yr1 (Gonçalves et al., 2012), which corresponds to 0.02e0.05% of the global emissions from coastal upwelling areas (0.4 Tg NeN2O yr1, Anderson et al., 2010). Further, a N2O flux of 15 mmol m2 d1 was estimated from Setúbal Bay during an upwelling event (Gonçalves et al., 2012), which is considered a high emission, according to the criterion proposed by Paulmier et al. (2008) (>8.1 mmol m2 d1). Estuaries are characterized by high variability of hydrodynamics and biogeochemistry, related to topographic features, environmental factors and tidal fluctuations, being very sensitive to human activities. As a consequence of their high productivity and additional anthropogenic nitrogen inputs over recent decades, rates of microbial N2O production have increased contributing to the enhancement of N2O emission from these ecosystems (De Wilde and De Bie, 2000; Garnier et al., 2006; Kroeze et al., 2010; LaMontagne et al., 2003; Marty et al., 2001). Considerable efforts have been made in recent decades to quantify the N2O fluxes in different coastal ecosystems, especially in estuaries. Barnes and Upstill-Goddard (2011) identified European estuaries (Iberian estuaries not included) as important N2O sources, representing a contribution of 6.8 ± 13.2 Gg NeN2O yr1 to global emissions. In recent years, studies on the N2O dynamics and emissions have been carried out in some Portuguese estuaries (e.g. Cabrita and Brotas, 2000; Cartaxana and Lloyd, 1999; Gonçalves et al., 2010; Middelburg in Barnes and Upstill-Goddard, 2011; Teixeira et al., 2010, 2013). However, due to a great diversity of hydrological and geomorphological conditions and anthropogenic pressures on these systems, further investigation is required. In this paper we analyze the first results of tidal and spatial variability of N2O concentrations in the Sado estuary, we assess the importance of the respective sources and estimate N2O fluxes and contribution of this system to the global emissions. 2. Materials and methods 2.1. Area description The Sado estuary is the second largest estuary in Portugal, with an area of approximately 180 km2 (Ferreira et al., 2003). It is located on the western Portuguese coast, Setúbal Peninsula, and discharges into the Atlantic Ocean. Most of the estuary is classified as a natural reserve, although it encloses Setúbal city border and important industrial and harbor-associated activities mainly on the northern margin, which represent a considerable anthropogenic pressure (Lillebø et al., 2011). The main nitrogen sources to the estuary are the load from the Sado river which aggregates the main agricultural, domestic and industrial sources from the river basin (approximately 2500 ton yr1) and the effluents from domestic (191 ton yr1) and industrial (1262 ton yr1) origin (Ferreira et al., 2003). The intertidal area includes large areas of salt marshes and intertidal flats and corresponds to approximately 30% of the total estuary area (OSPAR, 2002). The estuary comprises a wide bay, partially separated by intertidal sandbanks into the Northern and the Southern Channels and is linked to the ocean by a narrow and deep channel (maximum depth of 50 m) (Neves, 1986). The Sado estuary margins are also subjected to intensive agriculture, playing an important role in local and national economy. The hydrodynamics of the Sado estuary is forced by tides, which are semidiurnal and range from about 1.6 m at spring tides to 0.6 m at neap tides,
467
and by the Sado River discharge. The river presents an annual mean flow of 40 m3 s1 (Ferreira et al., 2003) displaying, however, a striking seasonal variability with very low freshwater discharges occurring in summer. Thus, during spring/summer, when the river flow is low, the hydrography of the Sado estuary is dominated by tide, and the coastal Atlantic waters inundate the estuary. The Sado coastal zone is largely influenced by the coastal upwelling which develops seasonally (MarcheSeptember) along the Iberian coast. The system also referred as a lagoon-type estuary (Cabeçadas et al., 1999b) has a water volume of 500 106 m3 and mean water residence time of 21 days (Ferreira et al., 2003). Marateca zone, which comprises an area of 25.6 km2 (Ferreira et al., 2003), is a shallow specific area of the estuary, mostly occupied by extensive intertidal flats and salt marshes, being greatly exposed to light and wind which favors the evaporation. Salt-pans exploitation is carried out over this area and the respective runoff influences the salinity of the estuarine waters. 2.2. Sampling The sampling programme was carried out during ebb tide (spring tide) at 12 stations located along the Sado estuary, from the Alc acer Channel to the estuary mouth, between 31 July and 02 August 2007, on board the research vessel Tellina (Fig. 1). The Sado ~o). Additionally, samRiver input was also sampled (St.1, S. Roma pling was undertaken along the tidal cycle (spring tide) at two fixed estuarine sites with very distinct morphology and hydrodynamics, one in the Marateca channel and another one at the lower estuary (Sado Bay) (Fig. 1). Sampling was performed when upwelling conditions prevailed in the coastal area adjacent to Sado estuary (Fig. 2). Surface water (0.2 m depth) samples were collected in triplicate for analysis of chemical parameters (nitrate plus nitrite, ammonium, oxygen and nitrous oxide) using 2 L Niskin bottles (General Oceanics). The river flow was reduced (Q ¼ 0.5 m3 s1; Table 1) when sampling was carried out, so the estuary hydrodynamics was dominated by the tide. 2.3. Analytical procedures Temperature was determined in situ with a Seabird SBE19/CTD probe. Practical salinity measurements were carried out using a
Fig. 1. Map of Sado estuary showing the location of sampling sites along the estuary (numbered dots). Station B e Bay tidal cycle; station M e Marateca tidal cycle.
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Upwelling Index (m-3 s-1 km-1)
700 600 500 400 300 200 100 0 -100 1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 Days (July 2007) Fig. 2. Upwelling index (July 2007).
temperature-controlled conductive salinometer (Guideline), calibrated with respect to a certified IAPSO Standard Seawater reference. Meteorological parameters were determined using a portable meteorological station (Campbell Scientific CR 510). Measured wind speeds were converted to wind speed at 10 m height (u10) using a logarithmic correction (Hartman and Hammond, 1985). To calculate the upwelling index (UI), Ekman transport (Q) is mez-Gesteira et al., 2006; derived from the wind stress (t) fields (Go Santos et al., 2012), registered at a permanent meteorological station located at Sines (37.57 N) (OGIMET, 2013). The zonal (tx) and meridional (ty) components of wind stress were calculated on the basis of daily geostrophic wind components (Wx, Wy) at 10 m above the sea surface, as follows:
1=2 1=2 tx ¼ ra Cd Wx2 þ Wy2 Wx ; and; ty ¼ ra Cd Wx2 þ Wy2 Wy and then, Qx ¼ y/rw f and Qy ¼ x/rw f, where rw is the density of seawater (1025 kg m3), Cd is the empirical dimensionless drag coefficient (1.3 103) according to Hidy (1972), ra is the density of air (1.22 kg m3 at 15 C) and f is the Coriolis parameter defined as twice the vertical component of the Earth's angular velocity, U, at latitude q, given by f ¼ 2Usin(q), where U ¼ 7.292 105 s1. Finally, UI was calculated through the equation UI ¼ (sin((4p)/2)$Qx) þ (cos((4-p)/2)$Qy), where 4 is the angle between the mez-Gesteira et al., 2006). Thus, shoreline and the equator (Go positive (negative) UI values mean upwelling favorable (unfavorable) conditions. The Sado River flow, measured at the hydrometric station of Moinho da Gamitinha (37.941 N, 8.383 W) upstream of the Sado estuary, was obtained from SNIRH data base (SNIRH, 2013).
The Winkler method (Aminot and Chaussepied, 1983) was used to determine dissolved oxygen (referred herein as DO). Precision of the method was in the range of 0.08%e0.25%. DO saturation, expressed in %, was determined as the ratio of the oxygen concentration determined and the equilibrium values of DO calculated with Weiss (1970) equation. Water samples for determination of dissolved inorganic nitrogen (DIN) were filtered through acetate cellulose filters (pore size 0.45 mm) and frozen until analysis. Analyses were carried out using a TRAACS auto-analyzer following colorimetric techniques outlined by the manufacturer. Estimated precision was ±0.8% for nitrate plus nitrite (referred as NO 3 þ NO2 ) and ±2.0% for ammonium (referred as NHþ 4 ), at mid-scale concentrations. Accuracy of nutrient measurements was maintained by using daily CSK Standards (WAKO, Japan). For the determination of nitrous oxide (N2O) three replicates of bubble free sub-samples were poured into 20 mL glass vials, overflowed more than 100 mL of water, immediately poisoned with 40 mL of saturated aqueous mercury chloride (HgCl2) to stop biological activity, and the sample vial sealed with gastight cap. The vials were stored upside down, in the dark, at 4 C in the refrigerator until analysis, performed within 10 days. Samples containing air bubbles were discarded. Headspace N2O concentration was determined using a gas chromatograph (GC-3800, Varian) equipped with an electron capture detector (63Ni-ECD). In this procedure 5 mL of highly purified helium (purity ¼ 99.9999%) was injected into the sampling vial, using an airtight syringe, and 5 mL water sample was displaced. Equilibrium was reached in a headspace CombiPAL autosampler being the vials vigorously shaken for 4 h. Gas chromatographic separation was carried out using a stainless steel column packed with 80/100 (mesh) Porapak. To remove water vapor and carbon dioxide, absorbent columns, packed respectively with Mg(ClO4)2 and Carbosorb, were located in the carrier gas line between the sample loop and the separation column. Calibration of ECD response was done using standard N2O gas mixtures in synthetic air (Air Liquide) and the precision of the method was 3% (30 replicate measurements using samples containing 10 nmol L1 of N2O). In situ concentration of N2O was calculated from the concentrations measured in the headspace according to the solubility equation of Weiss and Price (1980). The N2O equilibrium concentrations were calculated assuming an atmospheric N2O mixing ratio of 319 ± 0.12 ppb (Forster et al., 2007). N2O saturation, expressed in percentage (%) was determined as the ratio of the measured dissolved N2O concentration and the equilibrium concentration. The N2O air-sea flux, FN2 O (mmol m2 d1), was estimated as FN2 O ¼ kN2 O $DN2O, where DN2O (nmol L1), the apparent N2O productioneconsumption, is the difference between the measured concentration and the equilibrium concentration with the atmosphere in the estuarine water; kN2 O (cm h1) is the N2O transfer velocity, which is expressed as a function of the wind speed and the Schmidt number (Sc). Since no direct measurements of kN2 O were made in situ, we used both the k-wind parameterization proposed by Carini et al. (1996) and Raymond and Cole (2001) in order to minimize any substantial errors in the estimated air-sea fluxes, due to the use of a single k relationship. The gas transfer velocities and
Table 1 Hydrological characteristics of Sado estuary and meteorological conditions observed in July/August 2007. Q e Sado River flow; u10 e wind speed at 10 m heigh. Sampling date 31 July 01 August 02 August a b
Estuary (spatial) Sado Bay (tidal cycle) Marateca (tidal cycle)
Tidal amplitude (m)
Qa (m3 s1)
u10b (m s1)
0.5e3.5 0.5e3.6 0.6e3.6
0.5
3.1e8.8 3.2e9.0 3.6e9.7
Q e Sado River mean flow 10 days before sampling date (SNIRH, 2013). u10 e Average wind speed at 10 m height, measured 10 days before sampling date.
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air-sea fluxes were estimated using in situ wind speeds. The coefficients kN2 O were corrected at in situ temperature by using the relationship kN2 O /k600 ¼ (ScN2 O /600)0.5, where ScN2 O is the Schmidt number for N2O calculated according to the equation of Wanninkhof (1992). Positive N2O fluxes indicate emission of N2O to the atmosphere and negative values represent uptake from the atmosphere. 2.4. Data analysis Box-and-whisker plots are used to give a first insight on the variability of water quality parameters. The central horizontal line of the box is the median of the data, which is the point where 50% of the data is above it and 50% below it. The bottom and the top of the box represent the 25th and 75th percentiles (quartiles), and the ends of the whiskers are the 5th and 95th percentiles. The notch in the box is the 95% confidence interval of the median. These plots were developed with Grapher (version 9.6) software. Isopleth maps were generated with Surfer (version 8.0) software. 3. Results 3.1. Tidal variability A first comparison of data obtained along tidal cycles at the Sado Bay and Marateca (Fig. 3) shows that most of parameters, temperature, salinity, DO and N2O, exhibit significant differences between the Sado Bay and Marateca, as data boxes of these parameters do not overlap. In the Bay, lower median values of temperature and salinity and higher values of DO and N2O were measured. Median values of temperature increased from 18 C in the Bay to 24 C in Marateca. Also, salinity median value increased from 36 in the Bay to 36.4 in Marateca, where the range of values was wider and the maximum exceeded 36.8. DO median value was higher in the Bay (~230 mmol L1) than in Marateca (~195 mmol L1), and also a wider range of levels was measured. DO values were close to saturation in the Bay and down to 80% in Marateca, which reflects higher oxygen utilization and lower water renewal in this last zone. þ The NO 3 þ NO2 and NH4 exhibited a greater similarity in Mar ateca and Bay areas. NO3 þ NO 2 median concentration in the Bay was 1.7 mmol L1 and in Marateca 1.4 mmol L1. However, a higher range of values was observed in the Bay revealing a major tidal influence. Median NHþ 4 concentration value was also slightly higher in the Bay (2.2 mmol L1) than in Marateca (1.6 mmol L1), although a higher maximum (3.1 mmol L1) was reached at this last site. In relation to N2O, median value is about twice that observed in Marateca, suggesting the existence of additional sources/production of this biogas in the Bay. In this area, surface water was N2O supersaturated, reaching a maximum value of 124%. In Marateca N2O concentrations were, in general, below the equilibrium concentration and a minimum saturation value of 80% was detected. þ The variability of temperature, salinity, DO, NO 3 þ NO2 , NH4 and N2O with the tide is shown in Fig. 4. In the Bay, tidal influence was more perceptible on temperature, NO 3 þ NO2 and N2O, while in Marateca the tidal influence is more visible on salinity, NHþ 4 and DO. In both areas the highest values of temperature and salinity were measured at low tide (LT), with maximum values occurring in Marateca, probably as a consequence of greater evaporation over this shallow area where salt-pans are still working. The estuarine water was well oxygenated along both tidal cycles, although higher values were detected in the Bay (Fig. 4a). The maximum value (240 mmol L1; 98.5% saturation) was reached at high tide (HT)/slack tide, reflecting, in particular, a more intense circulation and seawater exchange. In Marateca (Fig. 4b) DO concentrations increase until mid-ebb, when a value of 213 mmol L1
þ Fig. 3. Box plots of temperature, salinity, DO, NO 3 þ NO2 , NH4 and N2O along tidal cycles in Sado Bay and Marateca.
(102% saturation) is attained. In the Bay (Fig. 4a), NO 3 þ NO2 and N2O increased, in general, during the flood (values ranging between 0.2e2.1 mmol L1 and 7.6e10.0 nmol L1, respectively) attaining the highest values 2e3 h after the high tide. This pattern may reflect the complex estuarine circulation as given the strong curvature of the entrance channel of
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(Fig. 4a). In Marateca, NHþ 4 values ranged between 1.3 and 2.3 mmol L1 (Fig. 4b). 3.2. Spatial variability The spatial distribution of environmental parameters (temper þ ature, salinity, DO, NO 3 þ NO2 , NH4 and N2O) along Sado estuary, during ebb tide, is shown in Figs. 5 and 6. There was (Fig. 5a) a welldefined band of colder water (19 Ce21 C) visible in the lower estuary, indicating a major influence of seawater, likely from upwelling origin. Maximum temperature values (24 Ce28 C) were reached in Marateca and Alc acer Channel entrance. The estuarine salinity pattern reveals that in the lower part of the Bay values no higher than 36.0 were recorded, despite the greater seawater influence (Fig. 5b). A minimum of 0.5 was measured in the upper estuary (Sado River). However, due to the low Sado River discharge during sampling period the influence of fresh water on the main water body of the estuary was almost imperceptible. The highest salinity value (36.1) was measured in
þ Fig. 4. Variability of temperature, salinity, DO, NO 3 þ NO2 , NH4 and N2O in (a) Bay tidal cycle and (b) Marateca tidal cycle. Tidal amplitude is represented by dotted lines. HT e High Tide; LT e Low Tide. (Error bars ¼ ±1 SD).
the estuary the interaction between the tidal circulation patterns and the estuarine morphology leads to an important residual secondary flow (Martins et al., 2002) close to our sampling point. The increase in NO 3 þ NO2 and N2O along the tidal cycle suggests the influence of more NO 3 þ NO2 and N2O enriched seawater, likely recently upwelled, given the intense upwelling episode occurring during this sampling period as mentioned earlier. Furthermore, maximum levels of NO 3 þ NO2 and N2O detected along tidal cycle agree with those found by Gonçalves et al. (2012) in a previous study carried out in Setúbal Bay, near to the Sado estuary mouth 1 N2O), during (approximately 5e8 mmol L1 NO 3 and 10.0 nmol L upwelling favorable conditions. In Marateca (Fig. 4b), NO 3 þ NO2 show a similar tidal variability, despite the lower levels registered (0.8e2.0 mmol L1). Levels of N2O range only from 5.2 nmol L1 to 6.5 nmol L1 (80%e100% saturation), pointing out to a possible N2O sink in this area (e.g. Kieskamp et al., 1991). The NHþ 4 values in the Bay increased slightly from 1.5 to 2.8 mmol L1 in the first part of flooding declining to a value approximately constant (2.3 mmol L1) until high tide/mid ebb
Fig. 5. Spatial distribution of (a) temperature, (b) salinity and (c) DO, in July 2007.
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(a) NO3- + NO2(μmol L-1) 1.2 3.4 1.4
0.2 11.4
(b) NH4+ (μmol L-1) 0.9 0.8 0.9
1.0
1.9
1.3 1.8
(c) N2O (nmol L-1) 5.0
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for 35%. Concerning NO 3 þ NO2 (Fig. 6a) a considerable spatial variability was found in the estuary. The highest value ~o, indicating the nutrient input (11.4 mmol L1) was found at S. Roma from the Sado River to the estuary. However, due to the very low Sado River flow in this summer period, levels decreased rapidly towards mid-estuary where concentrations varied from 0.2 to 2.0 mmol L1. Downstream, concentrations increased again, reaching 3.0 mmol L1 in the estuary mouth, which constitute an additional signal of upraised nutrient-rich water, as already observed in the Bay along the tidal cycle. In Marateca zone NO3 þ NO 2 concentration did not surpass1.2 mmol L1. Regarding NHþ 4 spatial distribution (Fig. 6b), a small variability was detected during sam1 pling period. At mid Bay, NHþ 4 values varied between 0.9 mmol L 1 and 2.0 mmol L while the minimum value was registered in Marateca (0.8 mmol L1). These low levels compare with those found by Cabeçadas and Brogueira (1991) in Marateca (approxiþ mately 0.5e0.6 mmol L1 NO 3 and NH4 ) and by Cabeçadas et al. þ (1999a) in Sado Bay (approximately 1e2 mmol L1 NO 3 and NH4 ) in summer. The distribution pattern of N2O (Fig. 6c, d) reveals that the Sado River is a source of this biogas to the estuary, as a maximum value ~o (12.5 nmol L1; 162% saturation), similarly to was found at S. Roma þ NO . But also in this case, the very low Sado River flow in NO 3 2 summer leads to a decrease towards mid-estuary where N2O levels varied from 6.0 to 7.0 nmol L1. Concentrations increased again towards the estuary mouth where a concentration of 10.0 nmol L1 was attained. Once again, N2O levels compare with data obtained by Gonçalves et al. (2012) in the coastal zone adjacent to the Sado estuary and constitute a signal of upraised N2O enriched water. N2O saturation values reached the maximum value (143%) at the estuary mouth, being saturation levels above equilibrium over most of the estuary, except in Marateca. This indicates that the estuary acts predominantly as a potential source of N2O to the atmosphere.
3.3. N2O air-sea fluxes during tidal cycles
11.5 6.3
7.1 12.5
(d) N2O (% saturation) 91 143 101
120 162
þ Fig. 6. Spatial distribution of (a) NO 3 þ NO2 , (b) NH4 and (c, d) N2O, in July 2007.
Marateca, as a consequence of the great evaporation over the area. The surface water was well oxygenated, DO levels ranging between 210 mmol L1 in Marateca and 240 mmol L1 in lower/central estuary (Fig. 5c). þ DIN was dominated by NO 3 þ NO2 , while NH4 accounted only
N2O air-sea fluxes, based on gas transfer velocity parameterization of Carini et al. (1996) (FC96) and Raymond and Cole (2001) (FRC01) along tidal cycles in the Sado Bay and Marateca are shown in Fig. 7. During the sampling period persistent and strong winds were recorded with intensity ranging between a minimum of 3.2 m s1 and a maximum of 9.7 m s1. Distinct N2O flux patterns could be observed along the Sado and Marateca tidal cycles. In the Sado Bay (Fig. 7a) N2O air-sea fluxes were always towards the atmosphere, increasing progressively from a minimum value of 0.7 mmol m2 d1 (FC96) (0.9 mmol m2 d1, FRC01) at mid-flood tide to a maximum value of 7.0 mmol m2 d1 (FC96) (17.0 mmol m2 d1, FRC01) during the first hours of ebb tide. The highest emissions match approximately the highest N2O saturations, revealing the influence of N2O enriched upwelled seawater on N2O fluxes. The mean N2O air-sea flux along the tidal cycle was positive (3.0 mmol m2 d1, FC96 and 6.1 mmol m2 d1, FRC01) corresponding to N2O concentration mean value of 8.8 nmol L1 (112% saturation) and high wind speed (mean value 6.9 m s1). By contrast, in Marateca (Fig. 7b) N2O air-sea fluxes along the tidal cycle were mostly negative and a minimum value of 6.2 mmol m2 d1 (FC96) (11.4 mmol m2 d1, FRC01) was attained at high tide, corresponding to the lowest N2O saturation level (approximately 80%). 3.4. N2O air-sea fluxes along Sado estuary N2O air-sea fluxes estimated along Sado estuary (Fig. 8) were mostly positive, except for the Marateca zone. In general, values increased progressively from the central part of the Bay (St. 9)
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estuary to the global N2O emissions was estimated. Considering an ~o, mid estuary zone and area of 151.4 km2, which includes S. Roma Sado Bay functioning as N2O source and assuming a mean N2O flux of 3.0 mmol m2 d1 (FC96) (3.8 mmol m2 d1, FRC01) an emission of 4.3 Mg NeN2O yr1 (FC96) (5.5 Mg NeN2O yr1; FRC01) is extrapolated. Further, considering an area of 25.6 km2 for Marateca zone and a N2O flux of 2.2 mmol m2 d1 (FC96) (4.3 mmol m2 d1; FRC01) an uptake of N2O from the atmosphere of 0.6 Mg NeN2O yr1 (FC96) (1.1 Mg NeN2O yr1; FRC01) is estimated. Hence, a N2O air-sea net/emission from Sado estuary is estimated as 3.7 mmol m2 d1 (FC96) (4.4 Mg NeN2O yr1; FRC01). 4. Discussion
Fig. 7. Air-sea N2O fluxes (bar charts) along tidal cycles in (a) Bay and (b) Marateca. Wind speed is represented by solid line and tidal amplitude by dotted line. HT e High Tide; LT e Low Tide. (Error bars ¼ ±1 SD).
towards the estuary mouth (St. 20) where a maximum value of 10.4 mmol m2 d1 (FC96) (17.0 mmol m2 d1, FRC01) was attained. The estimated Sado estuary mean N2O air-sea flux was positive (3.0 mmol m2 d1, FC96 and 3.8 mmol m2 d1, FRC01) and similar to the one found in the Bay tidal cycle (3.0 mmol m2 d1, FC96 and 6.1 mmol m2 d1, FRC01). Concerning Marateca zone a negative N2O flux of 2.2 mmol m2 d1 (FC96) (4.3 mmol m2 d1; FRC01) was estimated. Although N2O air-sea fluxes have been obtained during a single sampling and being aware of the seasonal variability that, in general, characterizes estuarine systems, the contribution of Sado
Fig. 8. Air-sea N2O fluxes (bar charts) along Sado estuary. Wind speed is representing by solid line.
The present study reveals that dissolved N2O shows considerable spatial and tidal variability in the Sado estuary, in summer. In this period the Sado river is an important source of N2O as maximum concentration was found in the riverine input zone (St.1, S. Rom~ ao). Nevertheless, the N2O chemical signal from the Sado River discharge was lost further in the main body of the Sado estuary, as water flow was reduced in the studied period. In fact, the impact of nutrient input in the Sado estuary is classified as moderate, as a result of the high dilution potential and the moderate flushing potential of the estuary, according to Ferreira et al. (2003). Furthermore, with the increase of percentage of treated wastewater in the estuarine area it is expected, in the future, there to be a significant reduction of nutrient pressure in the estuary and consequently a decrease of N2O levels in Sado estuary. In the turbidity maximum zones (TMZ) of estuaries higher N2O concentrations are usually observed (Barnes and Owens, 1998; Abril et al., 2000). However, during the study period no samples for N2O analysis were collected along the TMZ of the Sado estuary cer do Sal) (e.g. Cabeçadas (approximately between St. 8 and Alca et al., 1994) and no conclusions about the existence of such N2O estuarine source can be derived. In oxygen saturated waters as the Sado estuary is, nitrification may be an important contributor to N2O production (e.g. Bianchi et al., 1999). Nevertheless, in the Sado estuary N2O production through pelagic nitrification could not be deduced from the relevant parameters connected with this process, since no significant correlations have been found between N2O and NHþ 4 , NO3 þ NO2 . The half saturation constant (Ks) for nitrification process was estimated to be 1.9e4.2 mmol L1 of NH3 for Nitrosomonas oligotropha and N. ureae, and even much higher (30e61 mmol L1 of NH3) for N. europaea (Koops and € ser, 2001). Despite no information on the nitriPommerening-Ro fying bacterial community of Sado estuary being available, the concentration of the substrate NHþ 4 does not seem adequate for nitrification process to occur in the water column during the study period. In contrast to other estuaries including the Portuguese Tagus estuary (Gonçalves et al., 2010), N2O levels in the main body of the Sado estuary increased towards the estuary mouth in the summer period, which can be attributed to the influence of upwelled water containing higher N2O concentrations. As a matter of fact, levels of N2O in the lower estuary compare with those found in coastal waters adjacent to the Sado estuary during the upwelling event (Gonçalves et al., 2012). Apparently, the income of upwelled seawater in Sado estuary constitutes the most important N2O source to the estuary during summer. Despite the high N2O variability observed during tidal cycles and along the estuary, N2O saturation levels were above equilibrium, except in Marateca. The highest values of N2O saturation attained in the Sado estuary (92%e162%) are similar to those reported from less eutrophic European estuaries (Table 2). For example, maximum N2O saturation values of 118% and 143% were reported from Tay and
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Table 2 N2O emissions from several European estuaries (adapted from Barnes and Upstill-Goddard, 2011). Estuary
Area (km2) Nitrous oxide (N2O)
Sampling
Reference
Seasonal study Single survey Seasonal study Seasonal study Single survey Seasonal study Single survey Single survey Seasonal study Single survey
De wilde and de Bie (2000) J. Middelburg in Barnes and Upstill-Goddard (2011) J. Middelburg in Barnes and Upstill-Goddard (2011) Barnes and Upstill-Goddard (2011) Barnes and Upstill-Goddard (2011) Dong et al. (2004) De wilde and de Bie (2000) J. Middelburg in Barnes and Upstill-Goddard (2011) Gonçalves et al. (2010) This study
Saturation (%) Air-sea flux (mmol m2 d1) Emission (Mg NeN2O yr1) Scheldt, Belgium Ems, Germany Gironde, France Humber, UK Tay, UK Stour, UK Loire, France Douro, Portugal Tagus, Portugal Sado, Portugal a b c d
269 162 442 303.6 121.3 24.4 41 2.4 320 180
710 181e1794 120e463 100e4250 100e118 143 84e271 280e650 101e147 91e162
66.6a 76.7a 25.5a 76.6a 2.5a 20.6a 14.3a 74.7a 0.1 to 10.4a 2.2b to 3.8c
1.8 102 1.3 102 1.2 102 2.5 102 2.5 5.2 6.1 1.9 12.8e16.0d 3.7e4.4
Estimated using Clark et al. (1995) relationship. Carini et al. (1996) relationship. Raymond and Cole (2001) relationship. Unpublished data.
Stour estuaries, respectively. Also, Gonçalves et al. (2010) found in the Tagus estuary maximum N2O saturation values of 147%. The contrasting behavior of N2O air-sea fluxes between Sado bay and Marateca is likely related to the specific morphological features of Marateca, namely shallow water column and extensive intertidal areas. Otherwise, the simultaneous low concentrations of N2O and NO 3 þ NO2 suggest that N2O may be used in the denitrification process in sediments. The phenomenon of N2O influxes has been described for several marine systems, as in intertidal (Middelburg et al., 1995; Miller et al., 1986), brackish subtidal (Jensen et al., 1984) and marine sediments (Van Raaphorst et al., 1992) as well as in experiments on denitrification in subtidal sediments (Limfjorden-Denmark) (Jensen et al., 1984). The utilization of N2O as a terminal electron acceptor for organic carbon degradation in the absence of nitrate is a possible explanation for the flux of N2O to the sediment during summer, as during this period oxygen penetration in the sediment is limited and NO 3 pore-water concentrations are usually low (Kieskamp et al., 1991; Koike and Hattori, 1975). The pelagic N2O emission (3.7 Mg NeN2O yr1, FC96; 4.4 Mg NeN2O yr1, FRC01) from the Sado estuary compares with those from other European estuaries such as the Tay (2.5 Mg NeN2O yr1), Stour (5.2 Mg NeN2O yr1) and Loire (6.1 Mg NeN2O yr1; Table 2) but is higher than value reported from Douro (1.9 Mg NeN2O yr1; Barnes and Upstill-Goddard, 2011; Table 2) and much lower than values from Tagus (Gonçalves et al., 2010; Table 2). In a global perspective the estimated N2O emission from Sado estuary represents a reduced fraction (<0.1%) of global emissions from European estuaries (6.8 Gg NeN2O yr1, Barnes and UpstillGoddard, 2011). Nevertheless, higher N2O emissions in estuaries may occur during winter and spring (Sun et al., 2013, 2014) as reported from the nearby Tagus estuary (Gonçalves et al., 2010). Thus, the N2O emission from the Sado estuary on an annual basis, needs further confirmation. Acknowledgments The authors thank the crew of the R/V Telina for their assistance during sample collection. Acknowledgments are also due to collegues of IPMA Oceanography Laboratory for their assistance in sampling, technical and analytical procedures. The research was supported by the PoPesca MARE project (Contract N. 22-05-01FDR-00015) and by the FCT-Portuguese Foundation of Science and Technology (POCI 2010 and FSE) through grant SFRH/BD/28569/ 2006.
References Abril, G., Riou, S.A., Etcheber, H., Frankignoulle, M., de Wit, R., Middelburg, J.J., 2000. Transient, tidal time-scale, nitrogen transformations in an estuarine turbidity maximum-fluid mud system (the Gironde, South-west France). Estuar. Coast. Shelf Sci. 50, 703e715. Aminot, A., Chaussepied, M., 1983. Manuel des analyses chimiques en milieu marin. ans (CNEXO), Brest, France, p. 395. Centre National pour l'Exploitation des Oce Anderson, B., Bartlett, K., Frolking, S., Hayhoe, K., Jenkins, J., Salas, W., 2010. Methane and Nitrous Oxide Emissions from Natural Sources. U.S. Environmental Protection Agency technical report, Washington, D.C., U.S.A, p. 194. Bange, H.W., 2008. Gaseous nitrogen compounds (NO, N2O, N2, NH3) in the ocean. In: Capone, D.G., Bronk, D.A., Mulholland, M.R., Carpenter, E.J. (Eds.), Nitrogen in the Marine Environment, second ed. Elsevier, Amsterdam, pp. 51e94. €scher, C., 2010. Marine pathways to nitrous oxide. Bange, H.W., Freing, A., Kock, A., Lo In: Smith, K.A. (Ed.), Nitrous Oxide and Climate Change. Earthscan, London, UK, pp. 36e62. Barnes, J., Owens, N.J.P., 1998. Denitrification and nitrous oxide concentrations in the Humber estuary, UK, and adjacent coastal zones. Mar. Pollut. Bull. 37 (3e7), 247e260. Barnes, J., Upstill-Goddard, R.C., 2011. N2O seasonal distributions and air-sea exchange in UK estuaries: Implications for the tropospheric N2O source from European coastal waters. J. Geophys. Res. Biogeosci. 116, G01006. http:// dx.doi.org/10.1029/2009JG001156. Bianchi, M., Feliatra, F., Lefevre, D., 1999. Regulation of nitrification in the land^ne River plume (NW Mediterranean). Aquat. ocean contact area of the Rho Microb. Ecol. 18, 301e312. http://dx.doi.org/10.3354/ame018301. Cabeçadas, G., Brogueira, M.J., 1991. The Sado estuary, Portugal: Eutrophication conditions in areas of aquacultural activities. Environ. Pollut. 1, 810e820. ^ncia do azoto na proCabeçadas, G., Brogueira, M.J., Ferronha, H., 1994. A importa rio do Sado. In: 4ª Confere ^ncia Nacional Sobre dutividade prim aria do Estua Qualidade Do Ambiente, vol. I, pp. 181e190. Cabeçadas, G., Nogueira, M., Brogueira, M.J., 1999a. Nutrient dynamics and productivity in three European estuaries. Mar. Pollut. Bull. 38, 1092e1096. Cabeçadas, L., Brogueira, M.J., Cabeçadas, G., 1999b. Phytoplankton spring bloom in the Tagus coastal waters: hydrological and chemical conditions. Aquat. Ecol. 33, 243e250. Cabrita, M.T., Brotas, V., 2000. Seasonal variation in denitrification and dissolved nitrogen fluxes in intertidal sediments of the Tagus Estuary, Portugal. Mar. Ecol. Prog. Ser. 202, 51e65. Carini, S., Weston, N., Hopkinson, C., Tucker, J., Giblin, A., Vallino, J., 1996. Gas exchange rates in the Parker River estuary, Massachusetts. Biol. Bull. 191, 333e334. Cartaxana, P., Lloyd, D., 1999. N2, N2O and O2 profiles in a Tagus estuary salt marsh. Estuar. Coast. Shelf Sci. 48, 751e756. http://dx.doi.org/10.1006/ecss.1998.0475. Charpentier, J., Farías, L., Pizarro, O., 2010. Nitrous oxide fluxes in the central and eastern South Pacific. Glob. Biogeochem. Cycles 24, GB3011,. http://dx.doi.org/ 10.1029/2008GB003388. Clark, J.F., Schlosser, P., Simpson, H.J., Stute, M., Wanninkhof, R., Ho, D.T., 1995. Relationship between gas transfer velocities and wind speeds in the tidal Hudson River determined by the dual tracer technique. In: Jhane, B., Monahan, E. (Eds.), Air-water Gas Transfer. AEON Verlag and Studio, Hanau, Germany, pp. 785e800. Codispoti, L.A., 2010. Interesting times for marine N2O. Science 327, 1339e1340. http://dx.doi.org/10.1126/science.1184945. Cornejo, M., Farías, L., Paulmier, A., 2006. Temporal variability in N2O water content and its airesea exchange in an upwelling area off central Chile (36 S). Mar. Chem. 101, 85e94. http://dx.doi.org/10.1016/j.marchem.2006.01.004. De Wilde, H.P.J., De Bie, M.J.M., 2000. Nitrous oxide in the Schelde estuary:
474
C. Gonçalves et al. / Estuarine, Coastal and Shelf Science 167 (2015) 466e474
production by nitrification and emission to the atmosphere. Mar. Chem. 69, 203e216. http://dx.doi.org/10.1016/S0304-4203(99)00106-1. Dong, L.F., Nedwell, D.B., Colbeck, I., Finch, J., 2004. Nitrous oxide emission from some English and Welsh rivers and estuaries. Water Air Soil Pollut. 4, 127e134. http://dx.doi.org/10.1007/s11267-004-3022-4. Ferreira, J.G., Simas, T., Nobre, A., Silva, M.C., Shifferegger, K., Lencart-Silva, J., 2003. Identification of sensitive areas and vulnerable zones in transitional and coastal Portuguese systems. In: INAG-Instituto da Agua and IMAR-Instituto do Mar (Ed.), Application of the United States National Estuarine Eutrofication Assessement to the Minho, Lima, Douro, Ria de Aveiro, Mondego, Tagus, Sado, Mira, Ria Formosa and Guadiana systems, pp. 95e107. Forster, P., Ramaswamy, V., Artaxo, P., Berntsen, T., Betts, R., Fahey, D.W., Haywood, J., Lean, J., Lowe, D.C., Myhre, G., Nganga, J., Prinn, R., Raga, G., Schulz, M., Van Dorland, R., 2007. Changes in atmospheric constituents and in radiative forcing. In: Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L. (Eds.), Climate Change 2007: the Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge Univ. Press, Cambridge, UK and New York, NY, pp. 129e234. Forster, G., Upstill-Goddard, R.C., Gist, N., Robinson, C., Uher, G., Malcolm, E., Woodward, S., 2009. Nitrous oxide and methane in the Atlantic Ocean between 50 N and 52 S: latitudinal distribution and sea-to-air flux. Deep Sea Res. II 56, 964e976. http://dx.doi.org/10.1016/j.dsr2.2008.12.002. bron, A., Tallec, G., Billen, G., Sebilo, M., Martinez, A., 2006. Nitrogen Garnier, J., Ce behaviour and nitrous oxide emission in the tidal Seine River estuary (France) as influenced by human activities in the upstream watershed. Biogeochemistry 77, 305e326. mez-Gesteira, M., Moreira, C., Alvarez, I., De Castro, M., 2006. Ekman transport Go along the Galician coast (northwest Spain) calculated from forecasted winds. J. Geophys. Res. Biogeosci. 111, C10005. http://dx.doi.org/10.1029/2005JC003331. ~es, M.F., 2010. Seasonal and tidal influence on Gonçalves, C., Brogueira, M.J., Camo the variability of nitrous oxide in the Tagus estuary, Portugal. Sci. Mar. 74 (S1), 57e66. http://dx.doi.org/10.3989/scimar.2010.74s1057. ~es, M.F., 2012. Nitrous oxide content and fluxes Gonçalves, C., Brogueira, M.J., Camo in Setúbal Bay, Portugal, during upwelling events. Cienc. Mar. 38 (1B), 177e190. Hartman, B., Hammond, D., 1985. Gas exchange in San Francisco Bay. Hydrobiology 129, 59e68. Hidy, G.M., 1972. A view of recent airesea interaction research. Bull. Am. Meteorol. Soc. 53, 1083e1102. Jensen, H.B., Jørgensen, K.S., Sørensen, J., 1984. Diurnal variation of nitrogen cycling in coastal, marine sediments. II nitrous oxide emission. Mar. Biol. 83, 177e183. Kieskamp, W.M., Lohse, L., Epping, E., Helder, W., 1991. Seasonal variation in denitrification rates and nitrous oxide fluxes in intertidal sediments of the western Wadden Sea. Mar. Ecol. Prog. Ser. 72, 145e151. Koike, I., Hattori, A., 1975. Energy yield of denitrification: an estimate from growth yield in continuous cultures of Pseudomonas denitrificans under nitrate-, nitriteand oxide-limited conditions. J. General Microbiol. 88, 11e19. http://dx.doi.org/ 10.1099/00221287-88-1-11. €ser, A., 2001. Distribution and ecophysiology of the Koops, H.P., Pommerening-Ro nitrifying bacteria emphasizing cultured species. FEMS Microbiol. Ecol. 37, 1e19. Kroeze, C., Dumont, E., Seitzinger, S., 2010. Future trends in emissions of N2O from rivers and estuaries. J. Integr. Environ. Sci. 7 (S1), 71e78. http://dx.doi.org/ 10.1080/1943815X.2010.496789. LaMontagne, M.G., Duran, R., Valiela, I., 2003. Nitrous oxide sources and sinks in coastal aquifers and coupled estuarine receiving waters. Sci. Total Environ. 309, 139e149. Lillebø, A.I., Coelho, J.P., Pato, P., V alega, M., Margalho, R., Reis, M., Raposo, J., Pereira, E., Duarte, A.C., Pardal, M.A., 2011. Assessment of mercury in water, sediments and biota of a southern European estuary (Sado estuary, Portugal). Water Air Soil Pollut. 214 (1e4), 667e680. http://dx.doi.org/10.1007/s11270010-0457-2. Martins, F., Leit~ ao, P., Neves, R., 2002. Simulating vertical water mixing in homogeneous estuaries: the SADO Estuary case. Hydrobiologia 475/476, 221e227. Marty, D., Bonin, P., Michotey, V., Bianchi, M., 2001. Bacterial biogas production in coastal systems affected by freshwater inputs. Cont. Shelf Res. 21, 2105e2115. Middelburg, J.J., Klaver, G., Nieuwenhuize, J., Markusse, R.M., Vlug, T., Van der
Nat, F.J.W.A., 1995. Nitrous oxide emissions from estuarine intertidal sediments. Hydrobiologia 311 (1e3), 43e55. http://dx.doi.org/10.1007/BF00008570. Miller, L.G., Oremland, R.S., Paulsen, S., 1986. Measurement of nitrous oxide reductase activity in aquatic sediments. Appl. Environ. Microbiol. 51, 18e24. Naqvi, S.W.A., Jayakumar, D.A., Narvekar, P.V., Naik, H., Sarma, V.V.S.S., D'Souza, W., Joseph, S., George, M.D., 2000. Increased marine production of N2O due to intensifying anoxia on the Indian continental shelf. Nature 408, 346e349. Neves, R.J.J., 1986. Hidrodynamical modelling as a toll in waste disposal selection. A casa study on sado estuary. In: Kullenberg (Ed.), The Role of the Oceans as a Waste Disposal Option, pp. 563e576. NOAA (National Oceanic & Atmospheric Administration/Earth System Research Laboratory (www.esrl.noaa.gov/gmd/aggi/aggi.html) (accessed 09.10.13.). OGIMET (Weather Information Service) (www.ogimet.com) (accessed 06.03.13.). OSPAR, 2002. Comprehensive procedure, Portugal, Mondego, Tagus and Sado Estuaries, Maretec and IST. In: OSPAR Convention for the Protection of the Marine Environment of the North-East Atlantic. OSPAR Commission, London. Paulmier, A., Ruiz-Pino, D., Garcon, V., 2008. The oxygen minimum zone (OMZ) off Chile as intense source of CO2 and N2O. Cont. Shelf Res. 28, 2746e2756. http:// dx.doi.org/10.1061/j.csr.2008.09.012. Ravishankara, A.R., Daniel, J.S., Portmann, R.W., 2009. Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326, 123e125. http://dx.doi.org/10.1126/science.1176985. Raymond, P.A., Cole, J.J., 2001. Gas exchange in rivers and estuaries: choosing a gas transfer velocity. Estuaries 24, 312e317. mez-Gesteira, M., Alvarez, Santos, F., DeCastro, M., Go I., 2012. Differences in coastal and oceanic SST warming rates along the Canary upwelling ecosystem from 1982 to 2010. Cont. Shelf Res. 47, 1e6. ~o de Recursos Hídricos do Instituto da Agua, SNIRH (Sistema Nacional de Informaça I.P.) (http://snirh.pt) (accessed 17.10.13.). Sun, Z., Wang, L., Tian, H., Jiang, H., Mou, X., Sun, W., 2013. Fluxes of nitrous oxide and methane in different coastal Suaeda salsa marshes of the Yellow River estuary, China. Chemosphere 90, 856e865. http://dx.doi.org/10.1016/j.chemosphere. 2012.10.004. Sun, Z., Wang, L., Mou, X., Jiang, H., Sun, W., 2014. Spatial and temporal variations of nitrous oxide flux between coastal marsh and the atmosphere in the Yellow River estuary of China. Environ. Sci. Pollut. Res. Int. 21 (1), 419e433. http:// dx.doi.org/10.1007/s11356-013-1885-5. Suntharalingam, P., Sarmiento, J.L., 2000. Factors governing the oceanic nitrous oxide distribution: Simulations with an ocean general circulation model. Glob. Biogeochem. Cycles 14 (1), 429e454. http://dx.doi.org/10.1029/1999GB900032. Syakila, A., Kroeze, C., 2011. The global nitrous oxide budget revisited. Greenh. Gas Meas. Manag. 1 (1), 17e26. http://dx.doi.org/10.3763/ghgmm. 2010.0007. Teixeira, C., Magalh~ aes, C., Boaventura, R.A.R., Bordalo, A.A., 2010. Potential rates and environmental controls of denitrification and nitrous oxide production in a temperate urbanized estuary. Mar. Environ. Res. 70 (5), 336e342. http:// dx.doi.org/10.1016/j.marenvres.2010.07.001. ~es, C., Joye, S.B., Bordalo, A.A., 2013. The role of salinity in Teixeira, C., Magalha shaping dissolved inorganic nitrogen and N2O dynamics in estuarine sedimentwater interface. Mar. Pollut. Bull. 66, 225e229. http://dx.doi.org/10.1016/ j.marpolbul.2012.11.004. Van Raaphorst, W., Kloosterhuis, H.T., Berghuis, E.M., Gieles, A.J.M., Malschaert, J.F.P., Van Noort, G.J., 1992. Nitrogen cycling in two types of sediments of the southern North Sea (Frisian front, broad fourteens): field data and mesocosm results. Neth. J. Sea Res. 28, 293e316. Wanninkhof, R., 1992. Relationship between wind speed and gas exchange over the ocean. J. Geophys. Res. 97, 7373e7382. http://dx.doi.org/10.1029/92JC00188. Ward, B.B., 2008. Nitrification in marine systems. In: Capone, D.G., Bronk, D.A., Mulholland, M.R., Carpenter, E.J. (Eds.), Nitrogen in the Marine Environment. Elsevier, Amsterdam, pp. 199e262. Weiss, R.F., 1970. The solubility of nitrogen, oxygen, and argon in water and seawater. Deep Sea Res. Oceanogr. Abstr. 17 (4), 721e735. http://dx.doi.org/ 10.1016/0011-7471(70)90037-9. Weiss, R.F., Price, B.A., 1980. Nitrous oxide solubility in water and seawater. Mar. Chem. 8, 347e359. http://dx.doi.org/10.1016/0304-4203(80)90024-9. WMO (World Meteorological Organization - Global Atmosphere Watch) (http:// www.wmo.int/gaw) (accessed 05.09.13.).