- Email: [email protected]
Temporal and spatial variability of methane in the north-eastern shelf of the Gulf of Cádiz (SW Iberian Peninsula)
Journal of Sea Research 64 (2010) 213–223
Contents lists available at ScienceDirect
Journal of Sea Research j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s e a r e s
Temporal and spatial variability of methane in the north-eastern shelf of the Gulf of Cádiz (SW Iberian Peninsula) Sara Ferrón ⁎, Teodora Ortega, Jesús M. Forja Departamento de Química Física, Facultad de Ciencias del Mar y Ambientales, Universidad de Cádiz, Campus Río San Pedro, s/n. 11510, Puerto Real, Cádiz, Spain
a r t i c l e
i n f o
Article history: Received 19 January 2009 Received in revised form 24 October 2009 Accepted 14 February 2010 Available online 21 February 2010 Keywords: Methane Air–Sea Fluxes Gulf of Cádiz Coastal Continental Shelf
a b s t r a c t Methane (CH4) concentrations were investigated in shelf waters of the north-eastern shelf of the Gulf of Cádiz (SW Iberian Peninsula) during four campaigns that took place in June 2006, November 2006, February 2007 and May 2007. CH4 saturations, ranging from 70 to 1820%, showed great spatial and temporal variabilities. In general, strong onshore–offshore CH4 gradients indicated an important coastal input, which was further supported by punctual data collected within the Guadalquivir and Guadalete estuaries, as well as in Rio San Pedro creek. Tidal exchange and enhanced freshwater inputs during rainy periods were found to be important factors controlling CH4 distribution in shelf waters. The sediment was potentially another considerable source of biogenic CH4 to bottom waters. CH4 concentrations were found to be significantly higher in June and November 2006 compared to February and May 2007. The annual air–sea flux was estimated to range from 4.7 to 8.4 µmol CH4 m−2 d− 1. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Methane (CH4) is an important atmospheric trace gas that contributes significantly to the greenhouse effect and also plays a key role in tropospheric and stratospheric chemistry (IPCC, 2007). In the troposphere CH4 is involved in photochemical reactions that regulate the concentration of ozone and hydroxyl radicals, whereas its oxidation in the stratosphere is an important source of stratospheric water vapour (Crutzen, 1991). Methane levels in the atmosphere have more than doubled since pre-industrial times, accounting for around one-fifth of the human contribution to greenhouse gas-driven global warming (IPCC, 2007). The oceans are natural sources of CH4 to the atmosphere, although oceanic emissions account for only a small portion (2%) of the global CH4 budget (Reeburgh, 2007). Estimates of the marine methane flux to the atmosphere differ and range from 0.4 to 0.8 Tg CH4 yr− 1, based on measurements in oceanic surface waters (Bates et al., 1996), and from 11 to 18 Tg CH4 yr− 1, including the contribution of shelf \and estuarine areas (Bange et al., 1994). Although continental shelves and estuaries occupy only a small portion of the world oceans, they account for as much as 75% of the total oceanic CH4 flux (Bange et al., 1994). Subsequent re-evaluations of the coastal CH4 emission found even higher contributions from these ecosystems (Upstill-Goddard et al., 2000; Middelburg et al., 2002), adding 0.6–9% to the total oceanic CH4 flux derived by Bange et al. (1994). Recently, Bange (2006) estimated that mean CH4 emissions ⁎ Corresponding author. Now at Department of Oceanography, University of Hawaii, 1000 Pope Road, Honolulu, HI 96822, USA. Tel.: +1 808 956 7072. E-mail address: [email protected] (S. Ferrón). 1385-1101/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2010.02.007
from European shelf and estuaries are 0.28 Tg CH4 yr− 1 and 0.73 Tg CH4 yr− 1, respectively, and concluded that they contributed significantly to overall CH4 oceanic emissions. However, mostly due to the scarcity of data, insufficient regional and seasonal coverage and the uncertainties related to applied air–sea exchange models, there are still large uncertainties associated with these estimations. Measured CH4 saturations and emissions from coastal and estuarine waters vary over a wide range of spatial and temporal scales (e.g. Upstill-Goddard et al., 2000; Middelburg et al., 2002; Bange, 2006). Therefore, more measurements are needed in order to better understand the role of these environments in the oceanic CH4 budget and better quantify their emissions to the atmosphere. In this paper, we investigate the spatial and temporal trends in the distribution of CH4 concentration in waters of the north-eastern shelf of the Gulf of Cádiz, as well as the associated air–sea fluxes. 2. Study site description 2.1. Gulf of Cádiz The study was performed in the north-eastern shelf of the Gulf of Cádiz (Fig. 1). The Gulf of Cádiz is a wide basin located between the south-western Iberian Peninsula and the north-western African continent, where the North Atlantic Ocean and the Mediterranean Sea meet through the Strait of Gibraltar. The Gulf of Cadiz is a tectonically active area of the European continental margin and it is characterized by the existence of numerous gas-related sea floor structures, such as mud volcanoes, diapirs, pockmarks and carbonate chimneys (Somoza et al., 2002; Pinheiro et al., 2003).
214
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
Fig. 1. Map of the north-eastern shelf of the Gulf of Cádiz showing the location of sampled stations. Crosses refer to the sampling stations where benthic flux measurements were performed. Isolines represent the bathymetry in meters. Also depicted is the location of the Seawatch oceanographic buoy from Spanish Puertos del Estados.
The surface circulation in the Gulf of Cádiz is influenced by the seasonal fluctuations of the North Atlantic subtropical gyre and is primarily anti-cyclonic in the central and southern part (Vargas et al., 2003), resulting in the transport of water from the north-eastern shelf of the Gulf of Cádiz to the Alborán basin in the Mediterranean Sea (García-Lafuente et al., 2006). However, some authors suggest episodic seasonal changes to cyclonic circulation during the winter (Folkard et al., 1997). On a smaller scale, a quasi-permanent upwelling zone is observed near Cape San Vincent, as well as an intermittent minor up-welling area east of Cape Santa María, which is generated by westerly winds. In the northern near-shore area, the surface circulation is controlled by two cells of cyclonic circulation located over the eastern and western continental shelves. These cells are separated by Cape Santa María and coupled to the open seasurface circulation (García-Lafuente et al., 2006). Although the continental shelf dynamics is strongly influenced by the wind regime, the cyclonic circulation over the eastern shelf seems to be linked to coastal processes and persists independently of it (García-Lafuente and Ruiz, 2007). Continental shelf waters off the Guadalquivir River and Cádiz embayment present the greatest range of seasonal temperature variation and the highest primary production within the Gulf of Cádiz (Navarro and Ruiz, 2006). These patterns are mainly linked to the tidally-forced exchange of heat and nutrients between land and sea (Ruiz et al., 2006). Nevertheless, phytoplankton distribution in this sector of the gulf is also tightly coupled to meteorological and hydrodynamic conditions. The predominance of westerly winds is associated to the generation of up-welling events and, therefore, to an increase in primary production, whereas easterlies favour oligotrophy (Navarro and Ruiz, 2006). Primary production can also be enhanced after precipitation episodes which result in the input of fresh and nutrient-rich waters from the rivers (Ruiz et al., 2006). Furthermore, the alternation of mixing and stratification periods in the region affects the position of the nutricline and thus also regulates the primary production (Navarro et al., 2006). These fluctuations directly
affect the partial pressure of CO2 in this region, which seems to behave as a net annual sink for atmospheric CO2 (Huertas et al., 2006). 2.2. Guadalquivir estuary The Guadalquivir River is the main fluvial source draining into the Gulf of Cádiz margin, with an annual water discharge of 160 m3 s− 1 (Van Geen et al., 1977). The river is 560 km long and its drainage basin covers an area of approximately 58,000 km2. The 108-km long Guadalquivir estuary is a completely mixed or vertically homogeneous estuary (De la Paz et al., 2007) characterized by an irregular river discharge, which is relatively low for most of the year and considerably higher during rainy season (February–March). The hydrodynamics in the estuary is mainly controlled by the tidal regime. The maximum turbidity zone is located at a salinity of 5 during the summer; although its position is highly variable and depends on the tidal regime and the river discharge (De la Paz et al., 2007). 2.3. The Bay of Cádiz The Bay of Cádiz is a shallow environment divided into two basins, the southern and shallower inner bay and the northern and deeper external bay. A 18-km long tidal channel (Sancti Petri) connects the inner bay with Atlantic waters. The bay is surrounded by an extensive salt marsh area and several towns and cities, with a total population of about 700,000 inhabitants. The external bay is connected to the Gulf of Cádiz through a 13.5-km long opening and has a surface area of 88 km2. Water renewal ranges from 13.2 to 37.2% during neap and spring tides, respectively, indicating that it takes between 1.5 and 4 days to completely replace the water volume of the external bay (Manzano Harriero et al., 2002). The former receives the waters from the 157-km long Guadalete River. This river receives the effluent of the wastewater treatment plant of Jerez de la Frontera (200,000 inhabitants) as well as the drainage from agricultural cultivations. Río
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
215
San Pedro creek, which used to be a tributary of Guadalete River until it was artificially blocked at 12 km from the mouth, also flows into the external bay. Its main signature is seawater except for occasional freshwater inputs from precipitation. The tidal regime is the main force driving water exchange between the creek and the Bay of Cádiz. The creek is affected by the inputs of organic carbon and nutrients coming from surrounding fish farms (Tovar et al., 2000).
concentration. The atmospheric CH4 concentration was assumed to correspond to the annual average global concentration at Terceira Inland station (Azores, Portugal), taken from the National Oceanic and Atmospheric Administration/Climate Monitoring and Diagnostics Laboratory/Carbon Cycle Greenhouse Gases Group (NOAA/CMDL/CCGG) air sampling network (available at http://www.cmdl.noaa.gov/). Fluxes across the air–water interface were calculated from:
3. Methods
F = kðCw −aCa Þ
3.1. Field sampling and analysis The data reported in this work were collected during 4 cruises that took place from 16 to 28 June 2006, from 19 to 29 November 2006 and from 31 January to 10 February 2007 on board R/V Mytilus; and from 14 to 26 May 2007 on board R/V Ucádiz. A total of 72 stations located between 36.39 and 36.93°N and between 6.83 and 6.25°W were sampled, ranging in depth from 8 to 95 m (Fig. 1). At each station, surface (∼3 m below the sea surface) and near-bottom (∼ 5 m above the seafloor) water samples were collected with Niskin bottles, which were mounted on a rosette-sampler coupled to a Seabird CTD equipped with a Seatech fluorometer and a Seabird 43. Additionally, water samples were collected at other depths in various stations. Some observations made in November 2006 along a short section of the Guadalquivir estuary are also included, as well as some measurements made at longitudinal transects along Río San Pedro tidal creek (September 2003) and Guadalete River (January 2004). Water samples for methane analysis were carefully drawn in airtight glass bottles, preserved with saturated mercuric chloride to inhibit microbial activity, sealed with Apiezon® grease to prevent gas exchange, and stored in the dark until analysis in the laboratory within a month of collection. Methane was determined using a gas chromatograph equipped with flame ionization detector (300 °C) using helium as carrier gas (30 mL min− 1). Gases were separated in a 4.5 m × 1/8-in. stainless steel column packed with 80/100 Porapack N and a 1.5-m × 1/8-in. Molecular Sieve 5A column. The detector was calibrated using three standard gas mixtures which were made and certified by Air Liquide (France), with certified CH4 concentrations of 0.489 ppmv, 1.07 ppmv and 2.53 ppmv. The precision of the method, including the equilibration step and expressed as the coefficient of variation based on replicate analysis (n = 25), was 4.8%. Dissolved CH4 concentrations in the water samples were calculated by applying the solubility equation given by Wiesenburg and Guinasso (1979). 3.2. CH4 benthic fluxes In addition, benthic fluxes of dissolved CH4 were measured in situ at nine sampling sites (see Fig. 1) in June 2006, November 2006 and February 2007 (Ferrón et al., 2009). Benthic fluxes were determined by benthic chamber incubations, using an opaque cylindrical stirred chamber that covers 0.50 m2 of sediment and which is described in detail by Ferrón et al. (2008). The incubations were performed during the day and they lasted approximately 8 h. Samples were collected by a multiple water sampler provided with 50 mL-syringes (KCDenmark), and they were carefully drawn right after chamber recovery in 25 mL air-tight glass bottles, preserved with saturated mercuric chloride and sealed with Apiezon® grease and stored in the dark until analysis in the laboratory. Fluxes across the sediment– water interface were calculated as the product of the chamber height and the slope of the linear regression of the time series concentration evolution. 3.3. Saturation ratio and flux calculations Saturation values, expressed in %, were calculated as the ratio of the concentration of dissolved gas to the expected equilibrium water
where k (cm h− 1) is the gas transfer velocity, Cw is the concentration of dissolved gas in the water (mol L− 1), α is the Bunsen solubility and Ca is the atmospheric gas concentration. A positive flux indicates a transfer of gas from the water to the atmosphere. Gas transfer velocities were calculated using the tri-linear wind speed parameterization proposed by Liss and Merlivat (1986) (hereinafter referred to as LM86) and also the quadratic wind speed relationship established by Wanninkhof (1992) (hereinafter referred to as W92). The k coefficients were adjusted by multiplying with (Sc/600)n for LM86 (n = 2/3 for wind speeds ≤ 3.6 m s− 1 and n = 1/2 for wind speeds N 3.6 m s− 1) and (Sc/660)n for W92 (n = 1/2), where Sc is the Schmidt number for CH4, which was calculated according to Jähne et al. (1987). Wind speed data, recorded at the Seawatch buoy station (Fig. 1; 36°28.6′N; 6°57.8′W), were provided by the Spanish Puertos del Estado network (available at http://www.puertos.es/es/oceanografia_y_ meteorologia/banco_de_datos/index.html), and normalized to 10 m height by using the relationship of Garratt (1977). Daily averaged wind speeds were used for the calculation of gas transfer velocities. 3.4. Statistical analysis Statistical analyses were performed using Statgraphics Plus 5.1 software. Differences were analysed by one-way ANOVA followed by the Bonferroni post-hoc test. When data did not fulfil ANOVA requirements, differences were determined by Kruskal–Wallis test. The threshold value for statistical significance was assumed to be p b 0.05. 4. Results 4.1. Surface waters Fig. 2 shows the distribution of temperature, salinity and dissolved CH4 concentration in surface waters for the four periods sampled. Temperature and salinity in surface waters presented a wide range of variation (Table 1). Surface water temperature varied significantly among the different surveys (p b 0.001), whereas salinity was significantly higher in June 2006 (p b 0.001) relative to the other surveys, when the influence of freshwater inputs was more evident. In June 2006, surface water temperature, ranging from 21.1 to 24.2 °C, was higher in the northern part, whereas salinity, which ranged between 35.9 and 36.4, showed less spatial variability. In November 2006, surface water temperature ranged from 18.4 to 19.9 °C and a marked salinity gradient was observed near the mouth of the Guadalquivir estuary, with salinities decreasing northwards and onshore (range: 35.0–36.4). In February 2007, surface temperature showed a strong offshore–onshore gradient, with values decreasing from 16.0 °C to 12.6 °C towards the coast. The fluvial discharge in this period was manifested by a rapid decrease of salinity down to 33 near the mouth of the Guadalquivir estuary; a smaller salinity decrease was also evident near the Bay of Cádiz. In May 2007, surface temperatures increased northwards and varied between 17.6 and 20.3 °C, whereas salinity ranged from 35.7 to 36.1, showing a slight decrease towards the north.
216
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
Fig. 2. Surface water distributions of temperature, salinity and dissolved methane concentration for the different surveys. A: June 2006; B: November 2006; C: February 2007; D: May 2007.
The distribution of CH4 in coastal waters showed strong temporal and spatial variabilities (Fig. 2). CH4 concentrations in surface waters varied significantly among the surveys (p b 0.001), ranging from 8.4 to Table 1 Range of temperature, salinity, dissolved CH4 concentration and CH4 saturation measured during the four surveys in surface waters (excluding Station BC). In brackets: mean ± standard deviation. In italics: values corresponding to Station BC, located within the Bay of Cadiz (see Fig. 1).
June 2006 Stn BC November 2006 Stn BC February 2007 Stn BC May 2007
T (°C)
Salinity
CH4 (nM)
% CH4
21.14–24.24 (22.41 ± 0.81) 22.32 18.02–19.92 (19.17 ± 0.45) 18.33 12.55–15.97 (14.65 ± 0.89) 12.01 17.59–20.28 (18.59 ± 0.62)
35.89–36.44 (36.33 ± 0.08) 36.67 33.76–36.45 (35.93 ± 0.51) 35.73 34.51–36.36 (36.05 ± 0.41) 34.05 35.71–36.15 (36.04 ± 0.10)
8.40–14.94 (11.06 ± 1.60) 38.74 4.73–10.97 (6.69 ± 1.23) 26.22 2.46–18.55 (5.29 ± 3.54) 51.11 1.64–8.73 (3.63 ± 1.26)
370–690 (495 ± 75) 1725 200–440 (280 ± 50) 1080 95–690 (200 ± 130) 1820 70–365 (150 ± 50)
14.9 nmol L− 1 in June 2006, from 4.7 to 11.0 nmol L− 1 in November 2006, from 2.5 to 18.5 nmol L− 1 in February 2007 and from 1.6 to 8.7 nmol L− 1 in May 2007, corresponding to saturations of 370–690%, 200–440%, 95–690% and 70–365%, respectively (Table 1). Station BC, which was located outside the sampling grid, within the external Bay of Cádiz and near the mouths of Guadalete River and San Pedro tidal creek (see Fig. 1), showed significantly higher CH4 concentrations relative to the other sampling stations, ranging from 26.2 to 51.1 nmol L− 1, which corresponded to saturations of up to 1823%. In general, a clear onshore–offshore gradient was observed in all the surveys, with the concentrations decreasing rapidly offshore, indicating a coastal source (Fig. 2). The highest variability in surface CH4 concentration was observed in February 2007, with concentrations markedly increasing towards the coast. 4.2. Bottom waters The distributions of temperature, salinity and dissolved CH4 concentration in near-bottom waters for the four periods sampled are plotted in Fig. 3. Water temperature decreased offshore towards
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
217
Fig. 3. Bottom water distributions of temperature, salinity and dissolved methane concentration for the different surveys. A: June 2006; B: November 2006; C: February 2007; D: May 2007.
the deeper stations and showed the smallest gradient in February 2007, when water mixing was more effective. Near-bottom salinity tended to increase offshore, due to the influence of freshwater inputs in the shallower stations, except in June 2006. Near-bottom CH4 distributions measured during the four surveys (Table 2) ranged from 5.7 to 18.8 nmol L− 1 in June 2006, from 5.5 to 12.1 nmol L− 1 in November 2006, from 2.8 to 10.2 nmol L− 1 in February 2007 and from 2.5 to 28.6 nmol L− 1 in May 2007, corresponding to saturations of 215–825%, 230–495%, 105–390% and 100–1080%, respectively (station BC not included). Station BC presented the highest CH4 concentrations, ranging from 14.0 to 39.0 nmol L− 1 and corresponding to saturations of 580 to 1730%. Whereas the ranges of CH4 concentration in bottom waters were rather similar to those measured in surface waters for June and November 2006, in February and May 2007 bottom water CH4 concentrations were significantly higher than those in surface waters (p b 0.001). CH4 concentrations in bottom waters were significantly higher in June and November 2006 relative to February 2007 (p b 0.001); CH4 concentrations in June 2006 were also significantly higher than those measured in May 2007 (p b 0.01). In general, bottom
CH4 concentrations increased towards the coast, especially in June 2006 when the strongest offshore–inshore gradient was observed. In May 2007 a plume of CH4-enriched bottom water was observed in the southern part, with concentrations of up to 28.6 nmol L− 1. Table 2 Range of temperature, salinity, dissolved CH4 concentration and CH4 saturation measured during the four surveys in bottom waters (excluding Station BC). In brackets: mean ± standard deviation. In italics: values corresponding to Station BC, located within the Bay of Cadiz (see Fig. 1).
June 2006 Stn BC November 2006 Stn BC February 2007 Stn BC May 2007
T (°C)
Salinity
CH4 (nM)
% CH4
14.16–23.42 (18.41 ± 2.42) 21.96 15.35–19.60 (18.12 ± 1.19) 18.38 12.79–15.29 (14.32 ± 0.54) 12.17 13.48–19.19 (16.46 ± 1.56)
36.04–36.55 (36.32 ± 0.14) 36.67 35.49–36.40 (36.19 ± 0.23) 35.83 35.67–36.37 (36.21 ± 0.14) 35.20 35.90–36.16 (36.08 ± 0.06)
5.68–18.79 (9.11 ± 3.18) 39.05 5.47–12.12 (8.01 ± 1.59) 14.01 2.83–10.21 (5.66 ± 1.61) 30.55 2.48–28.61 (7.06 ± 4.26)
215–825 (370 ± 140) 1730 230–495 (325 ± 70) 580 105–390 (215 ± 60) 1100 100–1080 (275 ± 160)
218
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
4.3. Vertical distribution Figs. 4 and 5 show, as examples, the water column temperature, salinity and CH4 distribution along two transects perpendicular to the coast, one starting from station BC (the solid line representing the threshold of the Bay of Cádiz) (Fig. 4) and the other near the mouth of the Guadalquivir River (Fig. 5). Water temperature showed a marked decrease with depth in all cases, except for February 2007 when it was vertically rather uniform due to more effective vertical mixing of the water column. The presence of freshwater inputs from land was evident mainly in November 2006 and February 2007. CH4 concentrations in the water column showed a marked increase towards the shallower coastal stations. In November 2006 and February 2007, local CH4 enrichment was observed locally in near-bottom layers (Figs. 4 and 5), whereas in May 2007, a CH4-enriched water layer was observed at medium depths along the vertical transect off the Guadalquivir estuary, with concentrations decreasing again towards deeper waters (Fig. 5). Fig. 6 shows a vertical transect parallel to the coast at the deepest stations. CH4 concentrations in these waters were significantly lower in February and May 2007 relative to both June and November 2006 (p b 0.05). In June 2006, there was a marked vertical gradient with concentrations increasing rapidly towards the surface, possibly due to a more stratified water column and less advective mixing. In the other three surveys, there was a general increase of dissolved CH4 concentration towards the bottom.
an annual average of 280 ± 150% (Station BC not included) (Table 1). These values are within the range reported by Bange (2006) for European shelf waters, which present an average CH4 saturation of 224 ± 142% (range: 100–567%). The annual average of CH4 surface saturation for the external Bay of Cádiz, based on the samples taken at station BC, was 1540 ± 330%, which is more in the range of the values reported for estuarine systems and river plumes (Bange, 2006). The distribution of CH4 observed in the water column is the balance between inputs (land drainage and tidal exchange), benthic supply, in situ biological production and consumption, and removal by physical processes of diffusion, advection and gas exchange. 5.1. Water column production Water column CH4 production has been observed previously and can be related to methanogenesis in anoxic microniches of sinking organic particles (Sansone et al., 2001) or production of CH4 by zooplankton grazing (De Angelis and Lee, 1994). There was no evidence for in situ CH4 production in the study site. For example, no consistent correlations were found between CH4 concentration and parameters such as turbidity and chlorophyll a. However, such associations can often be masked by CH4 oxidation or air–sea exchange and, therefore, it is not possible to assess the potential importance of in situ water column production as a source of CH4 with the available data. 5.2. Estuarine inputs
5. Discussion Shelf waters in the north-eastern shelf of the Gulf of Cádiz were in general supersaturated with CH4. Mean surface saturations in the study site ranged from 150% in May 2007 to 495% in June 2006, with
The general CH4 onshore–offshore gradients observed in this study indicated an important coastal source. Tidal exchange through the rivers that discharge into the Gulf of Cádiz and inside the Bay of Cádiz has a significant influence on the physicochemical characteristics of
Fig. 4. Water column distribution of temperature, salinity and dissolved methane concentration in a transect perpendicular to the coast off the Bay of Cádiz (T3) A: June 2006; B: November 2006; C: February 2007; D: May 2007. Solid line represents the threshold of the Bay of Cádiz.
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
219
Fig. 5. Water column distribution of temperature, salinity and dissolved methane concentration in a transect perpendicular to the coast off the Guadalquivir estuary (T6). A: June 2006; B: November 2006; C: February 2007; D: May 2007.
Fig. 6. Water column distribution of temperature, salinity and dissolved methane concentration along a transect parallel to the coast at the deepest stations. The position corresponding to transects T1 to T9 are indicated on the X-axis (see Fig. 1).
220
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
nearby waters (García-Lafuente et al., 2006). According to these authors, the presence of localised spots of warm water off the mouth of Guadalquivir River and the Bay of Cádiz is linked to the propagation of heat from land, which is the result of inland propagation of the tides along the Guadalquivir River and associated arms and marshes, as well as along the marshes around the Bay of Cádiz and minor rivers. This heat export does not depend on the net freshwater discharge, which is negligible during the dry season (spring/summer), but rather on the tidal dynamics and the heating of land relative to water. Furthermore, the same mechanism was used to explain the nutrient pumping from land into the sea (Reul et al., 2006), and could therefore be extensible to CH4, partly explaining the strong onshore–offshore CH4 gradients found in the study site, a pattern observed regardless of the freshwater input. Surface water CH4 concentrations along transects T3 and T6 (see Fig. 1), the former starting near the mouths of the Guadalete River and Río San Pedro creek and the latter near the mouth of Guadalquivir estuary, were found to correlate with salinity (Fig. 7), indicating an estuarine input for dissolved CH4. The relationships between CH4 and
salinity for T3 were strongly nonlinear, being better described by a second-order polynomial. These deviations from conservative behaviour imply a substantial removal during mixing between waters from the Bay of Cádiz and nearby shelf waters. Note that these correlations were not always negative, due to an increase of salinity inside the Bay of Cádiz during the dry season. On the other hand, CH4 distribution along T6 showed a more conservative behaviour. The large estuarine input is further supported by the data collected within the Guadalquivir estuary, the Guadalete River and Río San Pedro creek (Fig. 8). CH4 concentrations in the lower part of the Guadalquivir estuary and its plume, measured in November 2006, were linearly correlated with salinity, indicating a conservative behaviour in that part of the estuary (Fig. 8A) with concentrations reaching up to 50.3 nmol L− 1 at a salinity of 15.8, which corresponded to a saturation of 1740%. Unfortunately, no samples were taken at lower salinities. Ferrón et al. (2007) investigated CH4 seasonal and tidal variability in Río San Pedro creek and found CH4 concentrations that ranged from 13 to 88 nmol L− 1, corresponding to saturations ranging from 500 to
Fig. 7. Surface water CH4 concentration versus salinity along transects T3 and T6 (see Fig. 1).
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
221
southern North Sea (Upstill-Goddard et al., 2000). It should be noted that if the low-salinity CH4 end-member measured did not represent the maximum CH4 concentration (no samples were collected upstream of this station), the removal calculated would be a minimum estimate. Although our estimation is based on a single campaign and, therefore, cannot be extrapolated to the annual situation, it highlights the importance of CH4 removal during estuarine mixing, which can be through microbial oxidation or air– sea exchange. Whereas CH4 oxidation is known to be an important estuarine sink of CH4 at low salinities (b6) (De Angelis and Scranton, 1993), a large fraction of the CH4 carried out by rivers or advected from tidal marshes has been found to be physically ventilated to the atmosphere in many inner estuaries (Upstill-Goddard et al., 2000; Middelburg et al., 2002) or adjacent plumes at sea (Bange et al., 1994). Summarizing, the tidal exchange between waters from the bay and waters from the river, the creeks and the surrounding salt marshes, together with enhanced land drainage during rainy periods and direct wastewater outlets, are important factors controlling CH4 saturation in near-shore waters of the Gulf of Cádiz. 5.3. Air–sea fluxes
Fig. 8. Dissolved CH4 concentration versus salinity along: (A) a longitudinal transect in Guadalquivir estuary (November 2006) and (B) a longitudinal transect in Guadalete River (January 2004); (C) CH4 concentration versus distance to the mouth in Río San Pedro tidal creek (September 2003).
5000%. Major processes controlling CH4 variability in this system were related to tidal advection and mixing with seawater coming from the Bay of Cádiz, and the range of variation was related to the amplitude of the tides. On a seasonal time scale, CH4 variations were associated with the dependence of respiratory processes on temperature, as well as seasonal changes in the fish farm discharges. Fig. 8C shows dissolved CH4 distribution measured in the creek along a longitudinal transect in September 2003. Dissolved CH4 concentrations increased, almost linearly with salinity (r2 = 0.77), towards the location of the main fish farm (about 10 km upstream of the mouth) going from 30 to 58 nmol L− 1. High CH4 concentrations were found in the Guadalete River along a longitudinal transect that took place in January 2004, ranging from 25 to 1841 nmol L− 1 and corresponding to saturations of 920–58,800%. These values are within the range reported by other authors in rivers (for a review refer to Upstill-Goddard et al., 2000), which are generally characterized by large and variable CH4 supersaturations. The CH4 versus salinity distribution along the Guadalete River (Fig. 8B) showed a clear non-conservative behaviour, with the highest concentration located upstream at the lower salinity, which corresponds to the location of the effluent from the wastewater treatment plant. The degree to which this high CH4 concentration is removed along the river was estimated by the tangent of the CH4 versus salinity plot at the seawater end-member (the first four points) extrapolated to the low-salinity end-member, as proposed by Upstill-Goddard et al. (2000). The extrapolated CH4 concentration for the low-salinity endmember estimated in this way was 285.5 nmol L− 1, implying an estuarine removal of about 84%.This is consistent with the percent of CH4 removal reported for other estuaries that discharge into the
During the four surveys, surface waters of the north-eastern shelf of the Gulf of Cádiz were found to be oversaturated with CH4 relative to the atmosphere, indicating that this region represents a source of this gas to the atmosphere. Table 3 summarizes the range, mean and standard deviation of CH4 flux densities derived from LM86 and W92 parameterizations. Although there is considerable uncertainty associated with existing air–sea exchange models, estimates of gas transfer velocities obtained from LM86 and W92 often fall within the upper and lower ranges of other gas exchange parameterizations (Nightingale et al., 2000; Upstill-Goddard, 2006) and, therefore, fluxes calculated from LM86 and W92 can be considered as lower and upper estimates, respectively. CH4 air–sea fluxes in the study site showed high spatial and temporal variabilities. Average CH4 fluxes for each survey ranged from 0.8 µmol CH4 m−2 d− 1 in May 2007 to 11.3 µmol CH4 m−2 d− 1 in June 2006, when applying LM86 parameterization, and from 1.7 to 19.7 µmol CH4 m−2 d− 1 for W92. The temporal variability in air–sea CH4 fluxes was mainly dominated by the variability of surface CH4 saturation values. The mean CH4 fluxes for the four surveys were 4.7 ± 4.6 µmol m−2 d− 1 and 8.4 ± 7.8 µmol m−2 d− 1, for LM86 and W92 respectively. These values fall within the range reported for other coastal and shelf areas (e.g. Bange et al., 1994; Patra et al., 1998; Amouroux et al., 2002). 5.4. Sedimentary supply CH4 supply from the sediments can have a biogenic or a thermal origin. In deeper areas of the Gulf of Cadiz (N400 m depth) there is an extensive field of mud volcanoes and diapiric structures hosting methane-hydrates which have been intensely surveyed (e.g. Somoza Table 3 Range of daily averaged wind speed (normalized to 10 m height) and calculated CH4 air–sea fluxes (± SD) derived from LM86 and W92 parameterizations. In brackets: mean ± standard deviation.
June 2006 November 2006 February 2007 May 2007 Mean ± SD
U10 (m s− 1)
CH4 flux LM86 (µmol m− 2 d− 1)
CH4 flux W92 (µmol m− 2 d− 1)
3.08–6.17 (5.10 ± 1.16) 2.09–6.40 (3.94 ± 1.61) 1.61–8.33 (5.27 ± 2.20) 3.54–5.86 (4.49 ± 0.93) 4.70 ± 0.61
0.7–22.7 (11.3 ± 7.1) 0.2–19.3 (3.2 ± 4.0) − 0.2–42.5 (3.6 ± 7.6) − 0.6–4.4 (0.8 ± 1.0) 4.7 ± 4.6
4.4–35.4 (19.7 ± 9.3) 1.0–37.1 (6.2 ± 6.2) − 0.3–68.1 (6.2 ± 12.0) − 1.0–7.0 (1.7 ± 1.8) 8.4 ± 7.8
222
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
et al., 2002; Pinheiro et al., 2003). However, the geochemical and microbial activity in these sites and their potential methane emission to the hydrosphere remain poorly understood. Recent studies indicate that methane is anaerobically consumed in subsurface sediments of several mud volcanoes from the Gulf of Cádiz before reaching the hydrosphere, suggesting that the emission of methane from these sites may be insignificant at present (Niemann et al., 2006; Stadnitskaia et al., 2006). While seepage from mud volcanoes and diapiric structures is limited to specific and deeper regions, biogenic methane production in sediments may be more widespread. Ivanov et al. (2002) demonstrated that, in the north-western shelf of the Black Sea, a considerable portion of the biogenic CH4 produced in the sediments escaped to the atmosphere. Water column CH4 distributions (Figs. 4–6) showed that bottom sediments could often be significant sources of CH4 to shelf waters. Biogenic methane is produced in anoxic sediments in the last step of organic matter mineralization, normally after the sulphate pool has been exhausted, as sulphate reducing bacteria compete with methanogens for the same substrates (Martens and Berner, 1974). CH4 fluxes across the sediment–water interface are then controlled by CH4 transport to the sediment surface, which can be through molecular diffusion and/or bubble ebullition, and are mainly limited by CH4 anaerobic oxidation in the sulphate reducing zone (Valentine, 2002). Apart from dissolved CH4 diffusing from sediments, near-bottom enrichment could be a consequence of resuspension events that could liberate CH4 accumulated in porewaters and also provide favourable microniches for potential water column methanogenesis (UpstillGoddard et al., 2000). However, no correlations were observed between bottom CH4 concentration and turbidity, making this option rather improbable during the sampling periods. Dissolved CH4 fluxes across the sediment–water interface were measured in situ at nine near-shore locations in the near-shore north-eastern shelf of the Gulf of Cádiz during the first three cruises (June 2006, November 2006 and February 2007) (Ferrón et al., 2009). Benthic CH4 fluxes were highly variable, not showing any spatial or temporal trend, and ranged from 0.5 to 24.1 µmol CH4 m−2 d− 1, although on most occasions they were below 10 µmol CH4 m−2 d− 1 (average ± SD; 5 ± 6 µmol CH4 m−2 d− 1). These values, although measured only for the shallower stations (depth range: 8– 34 m), are of the same order of magnitude as estimated air–sea fluxes for the study site, indicating that sediments are potentially important sources of CH4 to these coastal waters. 5.5. Temporal variability Although this study did not have enough seasonal coverage to explain the seasonal patterns of dissolved CH4 variability, the results indicate strong temporal fluctuations in CH4 distribution and emission to the atmosphere, which highlights the importance of having long time series of dissolved CH4 measurements in coastal waters to fully understand the biogeochemistry of CH4 in these systems and to resolve its seasonality. In the north-eastern shelf of the Gulf of Cádiz, higher concentrations were observed during June and November 2006 compared to February and March 2007. A strong positive correlation was observed between surface water CH4 saturations and temperature for the warmer surveys (June 2006, November 2006 and May 2007) (Fig. 9). The seasonal variability of dissolved CH4 concentrations in coastal temperate systems is often attributed to the enhancement of methanogenesis with temperature, as well as the seasonality of organic matter availability (e.g. Bange et al., 1998; Ferrón et al., 2007). In February 2007, when water temperatures were lower, CH4 saturations did not follow the thermal relationship observed for the other 3 surveys (Fig. 9). This survey showed the greatest CH4 variability and, despite the fact that water column was considerably well mixed (see Figs. 4 and 6), there were strong horizontal onshore– offshore gradients, with CH4 concentrations rapidly increasing
Fig. 9. CH4 saturation versus surface water temperature for the surveys in June 2006, November 2006 and May 2007 (open circles) (r2 = 0.78), and February 2007 (triangles).
towards the coast. The increase of CH4 saturations coincided with a decrease in salinity as a consequence of significant estuarine freshwater inputs (Figs. 2, 4 and 5). Therefore, the temporal variability of CH4 saturation in the study site was influenced by both the observed temperature and the magnitude of freshwater inputs. The CH4 accumulation observed in February 2007 could also be partly explained by seasonal changes in the hydrography of the northeastern shelf of the gulf. In this sense, the cyclonic circulation over the eastern shelf seems to be driven by the pool of warm water observed off the Guadalquivir River mouth and Cádiz embayment, which presumably produces the necessary sea-level slope to drive the coastal counter current that closes the cell at the north (GarcíaLafuente et al., 2006). Sánchez et al. (2006) observed winter changes in the coastal counter current which were not correlated to local wind stress but were probably linked to seasonal fluctuations of the basinscale wind-driven circulation (Machín et al., 2006). Moreover, the buoyancy input at the mouth of the Guadalquivir River stops in the winter, which would imply that the alongshore sea-level slope that drives the coastal current and, hence, the coastal counter current itself would both disappear. This would imply a less effective transport of water towards the north, which together with the enhanced freshwater inputs would lead to the accumulation of CH4 in the shallower stations. 6. Conclusions The distribution of CH4 in the north-eastern shelf of the Gulf of Cádiz showed great spatial and temporal variabilities. Surface waters were in all cases supersaturated with respect to the atmosphere, indicating that the area studied behaves as an atmospheric source of CH4 during the whole year. The magnitude of CH4 saturation in shelf waters was directly influenced by the continental inputs and varied seasonally depending on water temperature and the magnitude of freshwater discharge. CH4 benthic fluxes, although subjected to high variability, seemed to be another considerable CH4 source to bottom waters. Overall, annual CH4 emission was estimated to range from 0.04 (LM86) to 0.08 (W92) Gg CH4 yr− 1 for the area studied (1586 km2). Acknowledgments The authors would like to thank the crew of the R/V Mytilus and R/ V Ucádiz for their valuable assistance during the cruises, M. Fernández Díez-Picazo for his advice on how to treat and analyse the samples and S. Smith for language correction. The authors also acknowledge Spanish Puertos del Estado for providing meteorological data. This work was supported by the Spanish CICYT (Spanish Program for Science and Technology) under contract CTM2005-01364/MAR. S.F.
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
was funded by a grant from the Spanish MECD. The manuscript benefited from the comments provided by two anonymous reviewers. References Bange, H.W., 2006. Nitrous oxide and methane in European coastal waters. Estuar. Coast. Shelf Sci. 70, 367–374. Bange, H.W., Bartel, U.H., Rapsomanikis, S., Andreae, M.O., 1994. Methane in the Baltic and North Seas and reassessment of the marine emissions of methane. Glob. Biochem. Cycles 8, 465–480. Bange, H.W., Dahlke, S., Ramesh, R., Meyer-Reil, L.-A., Rapsomanikis, S., Andreae, M.O., 1998. Seasonal study of methane and nitrous oxide in the coastal waters of the Southern Baltic Sea. Estuar. Coast. Shelf Sci. 47, 807–817. Bates, T.S., Kelly, K.C., Johnson, J.E., Gammon, R.H., 1996. A reevaluation of the open ocean source of methane to the atmosphere. J. Geophys. Res. 101, 6953–6961. Crutzen, P.J., 1991. Methane's sinks and sources. Nature 350, 380–381. De Angelis, M.A., Scranton, M.I., 1993. Fate of methane in the Hudson river and estuary. Glob. Biogeochem. Cycles 7, 509–523. De Angelis, M.A., Lee, C., 1994. Methane production during zooplankton grazing on marine phytoplankton. Limnol. Oceanogr. 39, 1298–1308. De la Paz, M., Gómez-Parra, A., Forja, J., 2007. Inorganic carbon dynamic and air–water CO2 exchange in the Guadalquivir Estuary (SW Iberian Peninsula). J. Mar. Syst. 265–277. Ferrón, S., Ortega, T., Gómez-Parra, A., Forja, J.M., 2007. Seasonal study of dissolved CH4, CO2 and N2O in a shallow tidal system of the Bay of Cádiz (SW Spain). J. Mar. Syst. 66, 244–257. Ferrón, S., Alonso-Pérez, F., Castro, C.G., Ortega, T., Pérez, F.F., Ríos, A.F., Gómez-Parra, A., Forja, J.M., 2008. Hydrodynamic characterization and performance of an autonomous benthic chamber for use in coastal systems. Limnol. Oceanogr. Methods 6, 558–571. Ferrón, S., Alonso-Pérez, F., Ortega, T., Forja, J.M., 2009. Benthic respiration in the northeastern shelf of the Gulf of Cádiz (SW Iberian Peninsula). Mar. Ecol. Prog. Ser. 392, 69–80. Folkard, A.M., Davies, P.A., Fiúza, A.F.G., Ambar, I., 1997. Remotely sensed sea surface thermal patterns in the Gulf of Cadiz and the Strait of Gibraltar: variability, correlations, and relationships with the surface wind field. J. Geophys. Res. 102, 5669–5683. García-Lafuente, J., Ruiz, J., 2007. The Gulf of Cádiz pelagic ecosystem: a review. Prog. Oceanogr. 74, 228–251. García-Lafuente, J., Delgado, J., Criado-Aldeanueva, F., Bruno, M., del Río, J., Miguel Vargas, J., 2006. Water mass circulation on the continental shelf of the Gulf of Cádiz. Deep-Sea Res. Part II 53, 1182–1197. Garratt, J.R., 1977. Review of the drag coefficients over oceans and continents. Mon. Weather Rev. 105, 915–929. Huertas, I.E., Navarro, G., Rodríguez-Gálvez, S., Lubián, L.M., 2006. Temporal patterns of carbon dioxide in relation to hydrological conditions and primary production in the northeastern shelf of the Gulf of Cádiz (SW Spain). Deep-Sea Res. Part II 53, 1344–1362. IPCC, 2007. Climate change 2007: the physical science basis. In: Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L. (Eds.), Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel of Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, USA. 996 pp. Ivanov, M.V., Pimenov, N.V., Rusanov, I.I., Lein, A.Yu., 2002. Microbial processes of the methane cycle at the north-western shelf of the Black Sea. Estuar. Coast. Shelf Sci. 54, 589–599. Jähne, B., Heinz, G., Dietrich, W., 1987. Measurements of the diffusion coefficients of sparingly soluble gases in the water. J. Geophys. Res. 92, 10767–10776. Liss, P.S., Merlivat, L., 1986. Air–sea exchange rates: introduction and synthesis. In: Buat-Ménard, P. (Ed.), The Role of Air–Sea Exchanges in Geochemical Cycling. Reidel, Dordrecht, The Netherlands, pp. 113–127. Machín, F., Pelegrí, J.L., Marrero-Díaz, A., Laiz, I., Ratsimandresy, A.W., 2006. Nearsurface circulation in the southern Gulf of Cádiz. Deep-Sea Res. Part II 53, 1161–1181. Manzano Harriero, J.C., Naranjo Márquez, J.M., Aguilar Perea, M., Sánchez-Lamadrid, A., Jiménez Peral, T., Ruiz Segura, J., Gutiérrez Mas, J.M., Muñoz Pérez, J.L., Saavedra Martín, M., Juárez Dávila, A., Pérez Pastor, A., Romero Romero, Z. 2002. Bahía de
223
Cádiz: Protección de los recursos naturales pesqueros y aplicaciones para instalaciones acuícolas. Dirección General de Pesca y Acuicultura. Consejería de Agricultura y Pesca. Junta de Andalucía. Sevilla, España: 198 pp. Martens, C.S., Berner, R.A., 1974. Methane production in the interstitial waters of sulfate depleted marine sediments. Science 185, 1167–1169. Middelburg, J.J., Nieuwenhuize, J., Iversen, N., Høgh, N., De Wilde, H., Helder, W., Seifert, R., Christof, O., 2002. Methane distribution in European tidal estuaries. Biogeochem 59, 95–119. Navarro, G., Ruiz, J., 2006. Spatial and temporal variability of phytoplankton in the Gulf of Cádiz through remote sensing images. Deep-Sea Res. Part II 53, 1241–1260. Navarro, G., Ruiz, J., Huertas, I.E., García, C.M., Criado-Aldeanueva, F., Echevarría, F., 2006. Basin-scale structures governing the position of the deep fluorescence maximum in the Gulf of Cádiz. Deep-Sea Res. Part II 53, 1261–1281. Niemann, H., Duarte, J., Hensen, C., Omoregie, E., Magalhães, V.H., Elvert, M., Pinheiro, L.M., Kopf, A., Boetius, A., 2006. Microbial methane turnover at mud volcanoes of the Gulf of Cadiz. Geochim. Cosmochim. Acta 70, 5336–5355. Nightingale, P.D., Malin, G., Law, C.S., Watson, A.J., Liss, P.S., Liddicoat, M.I., Boutin, J., Upstill-Goddard, R.C., 2000. In situ evaluation of air–sea gas exchange parameterizations using novel conservative and volatile tracers. Global Biogeochem. Cycles 14, 373–387. Patra, P.K., Lal, S., Venkataramani, S., Gauns, M., Sarma, V.V.S.S., 1998. Seasonal variability in distribution and fluxes of methane in the Arabian Sea. J. Geophy. Res. 103, 1167–1176. Pinheiro, L.M., Ivanov, M.K., Sautkin, A., Akhmanov, G., Magalhães, V.H., Volkonskaya, A., Monteiro, J.H., Somoza, L., Gardner, J., Hamouni, N., Cunha, M.R., 2003. Mud volcanism in the Gulf of Cadiz: results from the TTR-10 cruise. Mar. Geol. 195, 131–151. Reeburgh, W.S., 2007. Oceanic methane biogeochemistry. Chem. Rev. 107, 486–513. Reul, A., Muñoz, M., Criado-Aldeanueva, F., Rodríguez, V., 2006. Spatial distribution of phytoplankton b 13 μm in the Gulf of Cádiz in relation to water masses and circulation pattern under westerly and easterly wind regimes. Deep-Sea Res. Part II 53, 1294–1313. Ruiz, J., Garcia-Isarch, E., Huertas, E., Prieto, L., Juárez, A., Muñoz, J.L., Sánchez-Lamadrid, A., Rodríaguez-Gálves, S., Naranjo, J.M., Baldó, F., 2006. Meteorological and oceanographic factors influencing Engraulis encrasicolus early life stages and catches in the Gulf of Cádiz. Deep-Sea Res. Part II 53, 1363–1376. Sánchez, R.F., Mason, E., Relvas, P., da Silva, A.J., Peliz, A., 2006. On the inner-shelf circulation in the northern Gulf of Cádiz, southern Portuguese shelf. Deep-Sea Res. Part II 53, 1198–1218. Sansone, F.J., Popp, B.N., Gasc, A., Graham, A.W., Rust, T.M., 2001. Highly elevated methane in the Eastern tropical North Pacific and associated isotopically enriched fluxes to the atmosphere. Geophys. Res. Lett. 28, 4567–4570. Somoza, L., Gardner, J.M., Díaz-Del-Río, V., Vazquez, J.T., Pinheiro, L.M., HernandezMolina, F.J., 2002. Numerous methane gas-related sea floor structures identified in Gulf of Cádiz. EOS 83, 541–547. Stadnitskaia, A., Ivanov, M.K., Blinova, V., Kreulen, R., van Weering, T.C.E., 2006. Molecular and carbon isotopic variability of hydrocarbon gases from mud volcanoes in the Gulf of Cadiz, NE Atlantic. Mar. Petrol. Geol. 23, 281–296. Tovar, A., Moreno, C., Manuel-Vez, M.P., García-Vargas, M., 2000. Environmental implications of intensive marine aquaculture in earthen ponds. Mar. Pollut. Bull. 40, 981–988. Upstill-Goddard, R.C., Barnes, J., Frost, T., Punshon, S., Owens, N.J.P., 2000. Methane in the southern North Sea: low-salinity inputs, estuarine removal, and atmospheric flux. Global Biogeochem. Cycles 14, 1205–1217. Upstill-Goddard, R.C., 2006. Air–sea gas exchange in the coastal zone. Estuar. Coast. Shelf Sci. 70, 388–404. Valentine, D., 2002. Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review. Antonie Van Leeuwenhoek 81, 271–282. Van Geen, A., Adkins, J.F., Boyle, E.A., Nelson, C.H., Palanques, A., 1977. A 120 yr record of widespread contamination from mining of the Iberian pyrite belt. Geology 25, 291–294. Vargas, J.M., García-Lafuente, J., Delgado, J., Criado, F., 2003. Seasonal and wind-induced variability of Sea Surface Temperature patterns in the Gulf of Cádiz. J. Mar. Syst. 38, 205–219. Wanninkhof, R., 1992. Relationship between wind speed and gas exchange over the ocean. J. Geophys. Res. 97, 7373–7382. Wiesenburg, D.A., Guinasso, N.L., 1979. Equilibrium solubilities of methane, carbon monoxide, and hydrogen in water and seawater. J. Chem. Eng. Data. 24, 356–360.
Contents lists available at ScienceDirect
Journal of Sea Research j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s e a r e s
Temporal and spatial variability of methane in the north-eastern shelf of the Gulf of Cádiz (SW Iberian Peninsula) Sara Ferrón ⁎, Teodora Ortega, Jesús M. Forja Departamento de Química Física, Facultad de Ciencias del Mar y Ambientales, Universidad de Cádiz, Campus Río San Pedro, s/n. 11510, Puerto Real, Cádiz, Spain
a r t i c l e
i n f o
Article history: Received 19 January 2009 Received in revised form 24 October 2009 Accepted 14 February 2010 Available online 21 February 2010 Keywords: Methane Air–Sea Fluxes Gulf of Cádiz Coastal Continental Shelf
a b s t r a c t Methane (CH4) concentrations were investigated in shelf waters of the north-eastern shelf of the Gulf of Cádiz (SW Iberian Peninsula) during four campaigns that took place in June 2006, November 2006, February 2007 and May 2007. CH4 saturations, ranging from 70 to 1820%, showed great spatial and temporal variabilities. In general, strong onshore–offshore CH4 gradients indicated an important coastal input, which was further supported by punctual data collected within the Guadalquivir and Guadalete estuaries, as well as in Rio San Pedro creek. Tidal exchange and enhanced freshwater inputs during rainy periods were found to be important factors controlling CH4 distribution in shelf waters. The sediment was potentially another considerable source of biogenic CH4 to bottom waters. CH4 concentrations were found to be significantly higher in June and November 2006 compared to February and May 2007. The annual air–sea flux was estimated to range from 4.7 to 8.4 µmol CH4 m−2 d− 1. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Methane (CH4) is an important atmospheric trace gas that contributes significantly to the greenhouse effect and also plays a key role in tropospheric and stratospheric chemistry (IPCC, 2007). In the troposphere CH4 is involved in photochemical reactions that regulate the concentration of ozone and hydroxyl radicals, whereas its oxidation in the stratosphere is an important source of stratospheric water vapour (Crutzen, 1991). Methane levels in the atmosphere have more than doubled since pre-industrial times, accounting for around one-fifth of the human contribution to greenhouse gas-driven global warming (IPCC, 2007). The oceans are natural sources of CH4 to the atmosphere, although oceanic emissions account for only a small portion (2%) of the global CH4 budget (Reeburgh, 2007). Estimates of the marine methane flux to the atmosphere differ and range from 0.4 to 0.8 Tg CH4 yr− 1, based on measurements in oceanic surface waters (Bates et al., 1996), and from 11 to 18 Tg CH4 yr− 1, including the contribution of shelf \and estuarine areas (Bange et al., 1994). Although continental shelves and estuaries occupy only a small portion of the world oceans, they account for as much as 75% of the total oceanic CH4 flux (Bange et al., 1994). Subsequent re-evaluations of the coastal CH4 emission found even higher contributions from these ecosystems (Upstill-Goddard et al., 2000; Middelburg et al., 2002), adding 0.6–9% to the total oceanic CH4 flux derived by Bange et al. (1994). Recently, Bange (2006) estimated that mean CH4 emissions ⁎ Corresponding author. Now at Department of Oceanography, University of Hawaii, 1000 Pope Road, Honolulu, HI 96822, USA. Tel.: +1 808 956 7072. E-mail address: [email protected] (S. Ferrón). 1385-1101/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2010.02.007
from European shelf and estuaries are 0.28 Tg CH4 yr− 1 and 0.73 Tg CH4 yr− 1, respectively, and concluded that they contributed significantly to overall CH4 oceanic emissions. However, mostly due to the scarcity of data, insufficient regional and seasonal coverage and the uncertainties related to applied air–sea exchange models, there are still large uncertainties associated with these estimations. Measured CH4 saturations and emissions from coastal and estuarine waters vary over a wide range of spatial and temporal scales (e.g. Upstill-Goddard et al., 2000; Middelburg et al., 2002; Bange, 2006). Therefore, more measurements are needed in order to better understand the role of these environments in the oceanic CH4 budget and better quantify their emissions to the atmosphere. In this paper, we investigate the spatial and temporal trends in the distribution of CH4 concentration in waters of the north-eastern shelf of the Gulf of Cádiz, as well as the associated air–sea fluxes. 2. Study site description 2.1. Gulf of Cádiz The study was performed in the north-eastern shelf of the Gulf of Cádiz (Fig. 1). The Gulf of Cádiz is a wide basin located between the south-western Iberian Peninsula and the north-western African continent, where the North Atlantic Ocean and the Mediterranean Sea meet through the Strait of Gibraltar. The Gulf of Cadiz is a tectonically active area of the European continental margin and it is characterized by the existence of numerous gas-related sea floor structures, such as mud volcanoes, diapirs, pockmarks and carbonate chimneys (Somoza et al., 2002; Pinheiro et al., 2003).
214
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
Fig. 1. Map of the north-eastern shelf of the Gulf of Cádiz showing the location of sampled stations. Crosses refer to the sampling stations where benthic flux measurements were performed. Isolines represent the bathymetry in meters. Also depicted is the location of the Seawatch oceanographic buoy from Spanish Puertos del Estados.
The surface circulation in the Gulf of Cádiz is influenced by the seasonal fluctuations of the North Atlantic subtropical gyre and is primarily anti-cyclonic in the central and southern part (Vargas et al., 2003), resulting in the transport of water from the north-eastern shelf of the Gulf of Cádiz to the Alborán basin in the Mediterranean Sea (García-Lafuente et al., 2006). However, some authors suggest episodic seasonal changes to cyclonic circulation during the winter (Folkard et al., 1997). On a smaller scale, a quasi-permanent upwelling zone is observed near Cape San Vincent, as well as an intermittent minor up-welling area east of Cape Santa María, which is generated by westerly winds. In the northern near-shore area, the surface circulation is controlled by two cells of cyclonic circulation located over the eastern and western continental shelves. These cells are separated by Cape Santa María and coupled to the open seasurface circulation (García-Lafuente et al., 2006). Although the continental shelf dynamics is strongly influenced by the wind regime, the cyclonic circulation over the eastern shelf seems to be linked to coastal processes and persists independently of it (García-Lafuente and Ruiz, 2007). Continental shelf waters off the Guadalquivir River and Cádiz embayment present the greatest range of seasonal temperature variation and the highest primary production within the Gulf of Cádiz (Navarro and Ruiz, 2006). These patterns are mainly linked to the tidally-forced exchange of heat and nutrients between land and sea (Ruiz et al., 2006). Nevertheless, phytoplankton distribution in this sector of the gulf is also tightly coupled to meteorological and hydrodynamic conditions. The predominance of westerly winds is associated to the generation of up-welling events and, therefore, to an increase in primary production, whereas easterlies favour oligotrophy (Navarro and Ruiz, 2006). Primary production can also be enhanced after precipitation episodes which result in the input of fresh and nutrient-rich waters from the rivers (Ruiz et al., 2006). Furthermore, the alternation of mixing and stratification periods in the region affects the position of the nutricline and thus also regulates the primary production (Navarro et al., 2006). These fluctuations directly
affect the partial pressure of CO2 in this region, which seems to behave as a net annual sink for atmospheric CO2 (Huertas et al., 2006). 2.2. Guadalquivir estuary The Guadalquivir River is the main fluvial source draining into the Gulf of Cádiz margin, with an annual water discharge of 160 m3 s− 1 (Van Geen et al., 1977). The river is 560 km long and its drainage basin covers an area of approximately 58,000 km2. The 108-km long Guadalquivir estuary is a completely mixed or vertically homogeneous estuary (De la Paz et al., 2007) characterized by an irregular river discharge, which is relatively low for most of the year and considerably higher during rainy season (February–March). The hydrodynamics in the estuary is mainly controlled by the tidal regime. The maximum turbidity zone is located at a salinity of 5 during the summer; although its position is highly variable and depends on the tidal regime and the river discharge (De la Paz et al., 2007). 2.3. The Bay of Cádiz The Bay of Cádiz is a shallow environment divided into two basins, the southern and shallower inner bay and the northern and deeper external bay. A 18-km long tidal channel (Sancti Petri) connects the inner bay with Atlantic waters. The bay is surrounded by an extensive salt marsh area and several towns and cities, with a total population of about 700,000 inhabitants. The external bay is connected to the Gulf of Cádiz through a 13.5-km long opening and has a surface area of 88 km2. Water renewal ranges from 13.2 to 37.2% during neap and spring tides, respectively, indicating that it takes between 1.5 and 4 days to completely replace the water volume of the external bay (Manzano Harriero et al., 2002). The former receives the waters from the 157-km long Guadalete River. This river receives the effluent of the wastewater treatment plant of Jerez de la Frontera (200,000 inhabitants) as well as the drainage from agricultural cultivations. Río
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
215
San Pedro creek, which used to be a tributary of Guadalete River until it was artificially blocked at 12 km from the mouth, also flows into the external bay. Its main signature is seawater except for occasional freshwater inputs from precipitation. The tidal regime is the main force driving water exchange between the creek and the Bay of Cádiz. The creek is affected by the inputs of organic carbon and nutrients coming from surrounding fish farms (Tovar et al., 2000).
concentration. The atmospheric CH4 concentration was assumed to correspond to the annual average global concentration at Terceira Inland station (Azores, Portugal), taken from the National Oceanic and Atmospheric Administration/Climate Monitoring and Diagnostics Laboratory/Carbon Cycle Greenhouse Gases Group (NOAA/CMDL/CCGG) air sampling network (available at http://www.cmdl.noaa.gov/). Fluxes across the air–water interface were calculated from:
3. Methods
F = kðCw −aCa Þ
3.1. Field sampling and analysis The data reported in this work were collected during 4 cruises that took place from 16 to 28 June 2006, from 19 to 29 November 2006 and from 31 January to 10 February 2007 on board R/V Mytilus; and from 14 to 26 May 2007 on board R/V Ucádiz. A total of 72 stations located between 36.39 and 36.93°N and between 6.83 and 6.25°W were sampled, ranging in depth from 8 to 95 m (Fig. 1). At each station, surface (∼3 m below the sea surface) and near-bottom (∼ 5 m above the seafloor) water samples were collected with Niskin bottles, which were mounted on a rosette-sampler coupled to a Seabird CTD equipped with a Seatech fluorometer and a Seabird 43. Additionally, water samples were collected at other depths in various stations. Some observations made in November 2006 along a short section of the Guadalquivir estuary are also included, as well as some measurements made at longitudinal transects along Río San Pedro tidal creek (September 2003) and Guadalete River (January 2004). Water samples for methane analysis were carefully drawn in airtight glass bottles, preserved with saturated mercuric chloride to inhibit microbial activity, sealed with Apiezon® grease to prevent gas exchange, and stored in the dark until analysis in the laboratory within a month of collection. Methane was determined using a gas chromatograph equipped with flame ionization detector (300 °C) using helium as carrier gas (30 mL min− 1). Gases were separated in a 4.5 m × 1/8-in. stainless steel column packed with 80/100 Porapack N and a 1.5-m × 1/8-in. Molecular Sieve 5A column. The detector was calibrated using three standard gas mixtures which were made and certified by Air Liquide (France), with certified CH4 concentrations of 0.489 ppmv, 1.07 ppmv and 2.53 ppmv. The precision of the method, including the equilibration step and expressed as the coefficient of variation based on replicate analysis (n = 25), was 4.8%. Dissolved CH4 concentrations in the water samples were calculated by applying the solubility equation given by Wiesenburg and Guinasso (1979). 3.2. CH4 benthic fluxes In addition, benthic fluxes of dissolved CH4 were measured in situ at nine sampling sites (see Fig. 1) in June 2006, November 2006 and February 2007 (Ferrón et al., 2009). Benthic fluxes were determined by benthic chamber incubations, using an opaque cylindrical stirred chamber that covers 0.50 m2 of sediment and which is described in detail by Ferrón et al. (2008). The incubations were performed during the day and they lasted approximately 8 h. Samples were collected by a multiple water sampler provided with 50 mL-syringes (KCDenmark), and they were carefully drawn right after chamber recovery in 25 mL air-tight glass bottles, preserved with saturated mercuric chloride and sealed with Apiezon® grease and stored in the dark until analysis in the laboratory. Fluxes across the sediment– water interface were calculated as the product of the chamber height and the slope of the linear regression of the time series concentration evolution. 3.3. Saturation ratio and flux calculations Saturation values, expressed in %, were calculated as the ratio of the concentration of dissolved gas to the expected equilibrium water
where k (cm h− 1) is the gas transfer velocity, Cw is the concentration of dissolved gas in the water (mol L− 1), α is the Bunsen solubility and Ca is the atmospheric gas concentration. A positive flux indicates a transfer of gas from the water to the atmosphere. Gas transfer velocities were calculated using the tri-linear wind speed parameterization proposed by Liss and Merlivat (1986) (hereinafter referred to as LM86) and also the quadratic wind speed relationship established by Wanninkhof (1992) (hereinafter referred to as W92). The k coefficients were adjusted by multiplying with (Sc/600)n for LM86 (n = 2/3 for wind speeds ≤ 3.6 m s− 1 and n = 1/2 for wind speeds N 3.6 m s− 1) and (Sc/660)n for W92 (n = 1/2), where Sc is the Schmidt number for CH4, which was calculated according to Jähne et al. (1987). Wind speed data, recorded at the Seawatch buoy station (Fig. 1; 36°28.6′N; 6°57.8′W), were provided by the Spanish Puertos del Estado network (available at http://www.puertos.es/es/oceanografia_y_ meteorologia/banco_de_datos/index.html), and normalized to 10 m height by using the relationship of Garratt (1977). Daily averaged wind speeds were used for the calculation of gas transfer velocities. 3.4. Statistical analysis Statistical analyses were performed using Statgraphics Plus 5.1 software. Differences were analysed by one-way ANOVA followed by the Bonferroni post-hoc test. When data did not fulfil ANOVA requirements, differences were determined by Kruskal–Wallis test. The threshold value for statistical significance was assumed to be p b 0.05. 4. Results 4.1. Surface waters Fig. 2 shows the distribution of temperature, salinity and dissolved CH4 concentration in surface waters for the four periods sampled. Temperature and salinity in surface waters presented a wide range of variation (Table 1). Surface water temperature varied significantly among the different surveys (p b 0.001), whereas salinity was significantly higher in June 2006 (p b 0.001) relative to the other surveys, when the influence of freshwater inputs was more evident. In June 2006, surface water temperature, ranging from 21.1 to 24.2 °C, was higher in the northern part, whereas salinity, which ranged between 35.9 and 36.4, showed less spatial variability. In November 2006, surface water temperature ranged from 18.4 to 19.9 °C and a marked salinity gradient was observed near the mouth of the Guadalquivir estuary, with salinities decreasing northwards and onshore (range: 35.0–36.4). In February 2007, surface temperature showed a strong offshore–onshore gradient, with values decreasing from 16.0 °C to 12.6 °C towards the coast. The fluvial discharge in this period was manifested by a rapid decrease of salinity down to 33 near the mouth of the Guadalquivir estuary; a smaller salinity decrease was also evident near the Bay of Cádiz. In May 2007, surface temperatures increased northwards and varied between 17.6 and 20.3 °C, whereas salinity ranged from 35.7 to 36.1, showing a slight decrease towards the north.
216
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
Fig. 2. Surface water distributions of temperature, salinity and dissolved methane concentration for the different surveys. A: June 2006; B: November 2006; C: February 2007; D: May 2007.
The distribution of CH4 in coastal waters showed strong temporal and spatial variabilities (Fig. 2). CH4 concentrations in surface waters varied significantly among the surveys (p b 0.001), ranging from 8.4 to Table 1 Range of temperature, salinity, dissolved CH4 concentration and CH4 saturation measured during the four surveys in surface waters (excluding Station BC). In brackets: mean ± standard deviation. In italics: values corresponding to Station BC, located within the Bay of Cadiz (see Fig. 1).
June 2006 Stn BC November 2006 Stn BC February 2007 Stn BC May 2007
T (°C)
Salinity
CH4 (nM)
% CH4
21.14–24.24 (22.41 ± 0.81) 22.32 18.02–19.92 (19.17 ± 0.45) 18.33 12.55–15.97 (14.65 ± 0.89) 12.01 17.59–20.28 (18.59 ± 0.62)
35.89–36.44 (36.33 ± 0.08) 36.67 33.76–36.45 (35.93 ± 0.51) 35.73 34.51–36.36 (36.05 ± 0.41) 34.05 35.71–36.15 (36.04 ± 0.10)
8.40–14.94 (11.06 ± 1.60) 38.74 4.73–10.97 (6.69 ± 1.23) 26.22 2.46–18.55 (5.29 ± 3.54) 51.11 1.64–8.73 (3.63 ± 1.26)
370–690 (495 ± 75) 1725 200–440 (280 ± 50) 1080 95–690 (200 ± 130) 1820 70–365 (150 ± 50)
14.9 nmol L− 1 in June 2006, from 4.7 to 11.0 nmol L− 1 in November 2006, from 2.5 to 18.5 nmol L− 1 in February 2007 and from 1.6 to 8.7 nmol L− 1 in May 2007, corresponding to saturations of 370–690%, 200–440%, 95–690% and 70–365%, respectively (Table 1). Station BC, which was located outside the sampling grid, within the external Bay of Cádiz and near the mouths of Guadalete River and San Pedro tidal creek (see Fig. 1), showed significantly higher CH4 concentrations relative to the other sampling stations, ranging from 26.2 to 51.1 nmol L− 1, which corresponded to saturations of up to 1823%. In general, a clear onshore–offshore gradient was observed in all the surveys, with the concentrations decreasing rapidly offshore, indicating a coastal source (Fig. 2). The highest variability in surface CH4 concentration was observed in February 2007, with concentrations markedly increasing towards the coast. 4.2. Bottom waters The distributions of temperature, salinity and dissolved CH4 concentration in near-bottom waters for the four periods sampled are plotted in Fig. 3. Water temperature decreased offshore towards
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
217
Fig. 3. Bottom water distributions of temperature, salinity and dissolved methane concentration for the different surveys. A: June 2006; B: November 2006; C: February 2007; D: May 2007.
the deeper stations and showed the smallest gradient in February 2007, when water mixing was more effective. Near-bottom salinity tended to increase offshore, due to the influence of freshwater inputs in the shallower stations, except in June 2006. Near-bottom CH4 distributions measured during the four surveys (Table 2) ranged from 5.7 to 18.8 nmol L− 1 in June 2006, from 5.5 to 12.1 nmol L− 1 in November 2006, from 2.8 to 10.2 nmol L− 1 in February 2007 and from 2.5 to 28.6 nmol L− 1 in May 2007, corresponding to saturations of 215–825%, 230–495%, 105–390% and 100–1080%, respectively (station BC not included). Station BC presented the highest CH4 concentrations, ranging from 14.0 to 39.0 nmol L− 1 and corresponding to saturations of 580 to 1730%. Whereas the ranges of CH4 concentration in bottom waters were rather similar to those measured in surface waters for June and November 2006, in February and May 2007 bottom water CH4 concentrations were significantly higher than those in surface waters (p b 0.001). CH4 concentrations in bottom waters were significantly higher in June and November 2006 relative to February 2007 (p b 0.001); CH4 concentrations in June 2006 were also significantly higher than those measured in May 2007 (p b 0.01). In general, bottom
CH4 concentrations increased towards the coast, especially in June 2006 when the strongest offshore–inshore gradient was observed. In May 2007 a plume of CH4-enriched bottom water was observed in the southern part, with concentrations of up to 28.6 nmol L− 1. Table 2 Range of temperature, salinity, dissolved CH4 concentration and CH4 saturation measured during the four surveys in bottom waters (excluding Station BC). In brackets: mean ± standard deviation. In italics: values corresponding to Station BC, located within the Bay of Cadiz (see Fig. 1).
June 2006 Stn BC November 2006 Stn BC February 2007 Stn BC May 2007
T (°C)
Salinity
CH4 (nM)
% CH4
14.16–23.42 (18.41 ± 2.42) 21.96 15.35–19.60 (18.12 ± 1.19) 18.38 12.79–15.29 (14.32 ± 0.54) 12.17 13.48–19.19 (16.46 ± 1.56)
36.04–36.55 (36.32 ± 0.14) 36.67 35.49–36.40 (36.19 ± 0.23) 35.83 35.67–36.37 (36.21 ± 0.14) 35.20 35.90–36.16 (36.08 ± 0.06)
5.68–18.79 (9.11 ± 3.18) 39.05 5.47–12.12 (8.01 ± 1.59) 14.01 2.83–10.21 (5.66 ± 1.61) 30.55 2.48–28.61 (7.06 ± 4.26)
215–825 (370 ± 140) 1730 230–495 (325 ± 70) 580 105–390 (215 ± 60) 1100 100–1080 (275 ± 160)
218
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
4.3. Vertical distribution Figs. 4 and 5 show, as examples, the water column temperature, salinity and CH4 distribution along two transects perpendicular to the coast, one starting from station BC (the solid line representing the threshold of the Bay of Cádiz) (Fig. 4) and the other near the mouth of the Guadalquivir River (Fig. 5). Water temperature showed a marked decrease with depth in all cases, except for February 2007 when it was vertically rather uniform due to more effective vertical mixing of the water column. The presence of freshwater inputs from land was evident mainly in November 2006 and February 2007. CH4 concentrations in the water column showed a marked increase towards the shallower coastal stations. In November 2006 and February 2007, local CH4 enrichment was observed locally in near-bottom layers (Figs. 4 and 5), whereas in May 2007, a CH4-enriched water layer was observed at medium depths along the vertical transect off the Guadalquivir estuary, with concentrations decreasing again towards deeper waters (Fig. 5). Fig. 6 shows a vertical transect parallel to the coast at the deepest stations. CH4 concentrations in these waters were significantly lower in February and May 2007 relative to both June and November 2006 (p b 0.05). In June 2006, there was a marked vertical gradient with concentrations increasing rapidly towards the surface, possibly due to a more stratified water column and less advective mixing. In the other three surveys, there was a general increase of dissolved CH4 concentration towards the bottom.
an annual average of 280 ± 150% (Station BC not included) (Table 1). These values are within the range reported by Bange (2006) for European shelf waters, which present an average CH4 saturation of 224 ± 142% (range: 100–567%). The annual average of CH4 surface saturation for the external Bay of Cádiz, based on the samples taken at station BC, was 1540 ± 330%, which is more in the range of the values reported for estuarine systems and river plumes (Bange, 2006). The distribution of CH4 observed in the water column is the balance between inputs (land drainage and tidal exchange), benthic supply, in situ biological production and consumption, and removal by physical processes of diffusion, advection and gas exchange. 5.1. Water column production Water column CH4 production has been observed previously and can be related to methanogenesis in anoxic microniches of sinking organic particles (Sansone et al., 2001) or production of CH4 by zooplankton grazing (De Angelis and Lee, 1994). There was no evidence for in situ CH4 production in the study site. For example, no consistent correlations were found between CH4 concentration and parameters such as turbidity and chlorophyll a. However, such associations can often be masked by CH4 oxidation or air–sea exchange and, therefore, it is not possible to assess the potential importance of in situ water column production as a source of CH4 with the available data. 5.2. Estuarine inputs
5. Discussion Shelf waters in the north-eastern shelf of the Gulf of Cádiz were in general supersaturated with CH4. Mean surface saturations in the study site ranged from 150% in May 2007 to 495% in June 2006, with
The general CH4 onshore–offshore gradients observed in this study indicated an important coastal source. Tidal exchange through the rivers that discharge into the Gulf of Cádiz and inside the Bay of Cádiz has a significant influence on the physicochemical characteristics of
Fig. 4. Water column distribution of temperature, salinity and dissolved methane concentration in a transect perpendicular to the coast off the Bay of Cádiz (T3) A: June 2006; B: November 2006; C: February 2007; D: May 2007. Solid line represents the threshold of the Bay of Cádiz.
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
219
Fig. 5. Water column distribution of temperature, salinity and dissolved methane concentration in a transect perpendicular to the coast off the Guadalquivir estuary (T6). A: June 2006; B: November 2006; C: February 2007; D: May 2007.
Fig. 6. Water column distribution of temperature, salinity and dissolved methane concentration along a transect parallel to the coast at the deepest stations. The position corresponding to transects T1 to T9 are indicated on the X-axis (see Fig. 1).
220
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
nearby waters (García-Lafuente et al., 2006). According to these authors, the presence of localised spots of warm water off the mouth of Guadalquivir River and the Bay of Cádiz is linked to the propagation of heat from land, which is the result of inland propagation of the tides along the Guadalquivir River and associated arms and marshes, as well as along the marshes around the Bay of Cádiz and minor rivers. This heat export does not depend on the net freshwater discharge, which is negligible during the dry season (spring/summer), but rather on the tidal dynamics and the heating of land relative to water. Furthermore, the same mechanism was used to explain the nutrient pumping from land into the sea (Reul et al., 2006), and could therefore be extensible to CH4, partly explaining the strong onshore–offshore CH4 gradients found in the study site, a pattern observed regardless of the freshwater input. Surface water CH4 concentrations along transects T3 and T6 (see Fig. 1), the former starting near the mouths of the Guadalete River and Río San Pedro creek and the latter near the mouth of Guadalquivir estuary, were found to correlate with salinity (Fig. 7), indicating an estuarine input for dissolved CH4. The relationships between CH4 and
salinity for T3 were strongly nonlinear, being better described by a second-order polynomial. These deviations from conservative behaviour imply a substantial removal during mixing between waters from the Bay of Cádiz and nearby shelf waters. Note that these correlations were not always negative, due to an increase of salinity inside the Bay of Cádiz during the dry season. On the other hand, CH4 distribution along T6 showed a more conservative behaviour. The large estuarine input is further supported by the data collected within the Guadalquivir estuary, the Guadalete River and Río San Pedro creek (Fig. 8). CH4 concentrations in the lower part of the Guadalquivir estuary and its plume, measured in November 2006, were linearly correlated with salinity, indicating a conservative behaviour in that part of the estuary (Fig. 8A) with concentrations reaching up to 50.3 nmol L− 1 at a salinity of 15.8, which corresponded to a saturation of 1740%. Unfortunately, no samples were taken at lower salinities. Ferrón et al. (2007) investigated CH4 seasonal and tidal variability in Río San Pedro creek and found CH4 concentrations that ranged from 13 to 88 nmol L− 1, corresponding to saturations ranging from 500 to
Fig. 7. Surface water CH4 concentration versus salinity along transects T3 and T6 (see Fig. 1).
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
221
southern North Sea (Upstill-Goddard et al., 2000). It should be noted that if the low-salinity CH4 end-member measured did not represent the maximum CH4 concentration (no samples were collected upstream of this station), the removal calculated would be a minimum estimate. Although our estimation is based on a single campaign and, therefore, cannot be extrapolated to the annual situation, it highlights the importance of CH4 removal during estuarine mixing, which can be through microbial oxidation or air– sea exchange. Whereas CH4 oxidation is known to be an important estuarine sink of CH4 at low salinities (b6) (De Angelis and Scranton, 1993), a large fraction of the CH4 carried out by rivers or advected from tidal marshes has been found to be physically ventilated to the atmosphere in many inner estuaries (Upstill-Goddard et al., 2000; Middelburg et al., 2002) or adjacent plumes at sea (Bange et al., 1994). Summarizing, the tidal exchange between waters from the bay and waters from the river, the creeks and the surrounding salt marshes, together with enhanced land drainage during rainy periods and direct wastewater outlets, are important factors controlling CH4 saturation in near-shore waters of the Gulf of Cádiz. 5.3. Air–sea fluxes
Fig. 8. Dissolved CH4 concentration versus salinity along: (A) a longitudinal transect in Guadalquivir estuary (November 2006) and (B) a longitudinal transect in Guadalete River (January 2004); (C) CH4 concentration versus distance to the mouth in Río San Pedro tidal creek (September 2003).
5000%. Major processes controlling CH4 variability in this system were related to tidal advection and mixing with seawater coming from the Bay of Cádiz, and the range of variation was related to the amplitude of the tides. On a seasonal time scale, CH4 variations were associated with the dependence of respiratory processes on temperature, as well as seasonal changes in the fish farm discharges. Fig. 8C shows dissolved CH4 distribution measured in the creek along a longitudinal transect in September 2003. Dissolved CH4 concentrations increased, almost linearly with salinity (r2 = 0.77), towards the location of the main fish farm (about 10 km upstream of the mouth) going from 30 to 58 nmol L− 1. High CH4 concentrations were found in the Guadalete River along a longitudinal transect that took place in January 2004, ranging from 25 to 1841 nmol L− 1 and corresponding to saturations of 920–58,800%. These values are within the range reported by other authors in rivers (for a review refer to Upstill-Goddard et al., 2000), which are generally characterized by large and variable CH4 supersaturations. The CH4 versus salinity distribution along the Guadalete River (Fig. 8B) showed a clear non-conservative behaviour, with the highest concentration located upstream at the lower salinity, which corresponds to the location of the effluent from the wastewater treatment plant. The degree to which this high CH4 concentration is removed along the river was estimated by the tangent of the CH4 versus salinity plot at the seawater end-member (the first four points) extrapolated to the low-salinity end-member, as proposed by Upstill-Goddard et al. (2000). The extrapolated CH4 concentration for the low-salinity endmember estimated in this way was 285.5 nmol L− 1, implying an estuarine removal of about 84%.This is consistent with the percent of CH4 removal reported for other estuaries that discharge into the
During the four surveys, surface waters of the north-eastern shelf of the Gulf of Cádiz were found to be oversaturated with CH4 relative to the atmosphere, indicating that this region represents a source of this gas to the atmosphere. Table 3 summarizes the range, mean and standard deviation of CH4 flux densities derived from LM86 and W92 parameterizations. Although there is considerable uncertainty associated with existing air–sea exchange models, estimates of gas transfer velocities obtained from LM86 and W92 often fall within the upper and lower ranges of other gas exchange parameterizations (Nightingale et al., 2000; Upstill-Goddard, 2006) and, therefore, fluxes calculated from LM86 and W92 can be considered as lower and upper estimates, respectively. CH4 air–sea fluxes in the study site showed high spatial and temporal variabilities. Average CH4 fluxes for each survey ranged from 0.8 µmol CH4 m−2 d− 1 in May 2007 to 11.3 µmol CH4 m−2 d− 1 in June 2006, when applying LM86 parameterization, and from 1.7 to 19.7 µmol CH4 m−2 d− 1 for W92. The temporal variability in air–sea CH4 fluxes was mainly dominated by the variability of surface CH4 saturation values. The mean CH4 fluxes for the four surveys were 4.7 ± 4.6 µmol m−2 d− 1 and 8.4 ± 7.8 µmol m−2 d− 1, for LM86 and W92 respectively. These values fall within the range reported for other coastal and shelf areas (e.g. Bange et al., 1994; Patra et al., 1998; Amouroux et al., 2002). 5.4. Sedimentary supply CH4 supply from the sediments can have a biogenic or a thermal origin. In deeper areas of the Gulf of Cadiz (N400 m depth) there is an extensive field of mud volcanoes and diapiric structures hosting methane-hydrates which have been intensely surveyed (e.g. Somoza Table 3 Range of daily averaged wind speed (normalized to 10 m height) and calculated CH4 air–sea fluxes (± SD) derived from LM86 and W92 parameterizations. In brackets: mean ± standard deviation.
June 2006 November 2006 February 2007 May 2007 Mean ± SD
U10 (m s− 1)
CH4 flux LM86 (µmol m− 2 d− 1)
CH4 flux W92 (µmol m− 2 d− 1)
3.08–6.17 (5.10 ± 1.16) 2.09–6.40 (3.94 ± 1.61) 1.61–8.33 (5.27 ± 2.20) 3.54–5.86 (4.49 ± 0.93) 4.70 ± 0.61
0.7–22.7 (11.3 ± 7.1) 0.2–19.3 (3.2 ± 4.0) − 0.2–42.5 (3.6 ± 7.6) − 0.6–4.4 (0.8 ± 1.0) 4.7 ± 4.6
4.4–35.4 (19.7 ± 9.3) 1.0–37.1 (6.2 ± 6.2) − 0.3–68.1 (6.2 ± 12.0) − 1.0–7.0 (1.7 ± 1.8) 8.4 ± 7.8
222
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
et al., 2002; Pinheiro et al., 2003). However, the geochemical and microbial activity in these sites and their potential methane emission to the hydrosphere remain poorly understood. Recent studies indicate that methane is anaerobically consumed in subsurface sediments of several mud volcanoes from the Gulf of Cádiz before reaching the hydrosphere, suggesting that the emission of methane from these sites may be insignificant at present (Niemann et al., 2006; Stadnitskaia et al., 2006). While seepage from mud volcanoes and diapiric structures is limited to specific and deeper regions, biogenic methane production in sediments may be more widespread. Ivanov et al. (2002) demonstrated that, in the north-western shelf of the Black Sea, a considerable portion of the biogenic CH4 produced in the sediments escaped to the atmosphere. Water column CH4 distributions (Figs. 4–6) showed that bottom sediments could often be significant sources of CH4 to shelf waters. Biogenic methane is produced in anoxic sediments in the last step of organic matter mineralization, normally after the sulphate pool has been exhausted, as sulphate reducing bacteria compete with methanogens for the same substrates (Martens and Berner, 1974). CH4 fluxes across the sediment–water interface are then controlled by CH4 transport to the sediment surface, which can be through molecular diffusion and/or bubble ebullition, and are mainly limited by CH4 anaerobic oxidation in the sulphate reducing zone (Valentine, 2002). Apart from dissolved CH4 diffusing from sediments, near-bottom enrichment could be a consequence of resuspension events that could liberate CH4 accumulated in porewaters and also provide favourable microniches for potential water column methanogenesis (UpstillGoddard et al., 2000). However, no correlations were observed between bottom CH4 concentration and turbidity, making this option rather improbable during the sampling periods. Dissolved CH4 fluxes across the sediment–water interface were measured in situ at nine near-shore locations in the near-shore north-eastern shelf of the Gulf of Cádiz during the first three cruises (June 2006, November 2006 and February 2007) (Ferrón et al., 2009). Benthic CH4 fluxes were highly variable, not showing any spatial or temporal trend, and ranged from 0.5 to 24.1 µmol CH4 m−2 d− 1, although on most occasions they were below 10 µmol CH4 m−2 d− 1 (average ± SD; 5 ± 6 µmol CH4 m−2 d− 1). These values, although measured only for the shallower stations (depth range: 8– 34 m), are of the same order of magnitude as estimated air–sea fluxes for the study site, indicating that sediments are potentially important sources of CH4 to these coastal waters. 5.5. Temporal variability Although this study did not have enough seasonal coverage to explain the seasonal patterns of dissolved CH4 variability, the results indicate strong temporal fluctuations in CH4 distribution and emission to the atmosphere, which highlights the importance of having long time series of dissolved CH4 measurements in coastal waters to fully understand the biogeochemistry of CH4 in these systems and to resolve its seasonality. In the north-eastern shelf of the Gulf of Cádiz, higher concentrations were observed during June and November 2006 compared to February and March 2007. A strong positive correlation was observed between surface water CH4 saturations and temperature for the warmer surveys (June 2006, November 2006 and May 2007) (Fig. 9). The seasonal variability of dissolved CH4 concentrations in coastal temperate systems is often attributed to the enhancement of methanogenesis with temperature, as well as the seasonality of organic matter availability (e.g. Bange et al., 1998; Ferrón et al., 2007). In February 2007, when water temperatures were lower, CH4 saturations did not follow the thermal relationship observed for the other 3 surveys (Fig. 9). This survey showed the greatest CH4 variability and, despite the fact that water column was considerably well mixed (see Figs. 4 and 6), there were strong horizontal onshore– offshore gradients, with CH4 concentrations rapidly increasing
Fig. 9. CH4 saturation versus surface water temperature for the surveys in June 2006, November 2006 and May 2007 (open circles) (r2 = 0.78), and February 2007 (triangles).
towards the coast. The increase of CH4 saturations coincided with a decrease in salinity as a consequence of significant estuarine freshwater inputs (Figs. 2, 4 and 5). Therefore, the temporal variability of CH4 saturation in the study site was influenced by both the observed temperature and the magnitude of freshwater inputs. The CH4 accumulation observed in February 2007 could also be partly explained by seasonal changes in the hydrography of the northeastern shelf of the gulf. In this sense, the cyclonic circulation over the eastern shelf seems to be driven by the pool of warm water observed off the Guadalquivir River mouth and Cádiz embayment, which presumably produces the necessary sea-level slope to drive the coastal counter current that closes the cell at the north (GarcíaLafuente et al., 2006). Sánchez et al. (2006) observed winter changes in the coastal counter current which were not correlated to local wind stress but were probably linked to seasonal fluctuations of the basinscale wind-driven circulation (Machín et al., 2006). Moreover, the buoyancy input at the mouth of the Guadalquivir River stops in the winter, which would imply that the alongshore sea-level slope that drives the coastal current and, hence, the coastal counter current itself would both disappear. This would imply a less effective transport of water towards the north, which together with the enhanced freshwater inputs would lead to the accumulation of CH4 in the shallower stations. 6. Conclusions The distribution of CH4 in the north-eastern shelf of the Gulf of Cádiz showed great spatial and temporal variabilities. Surface waters were in all cases supersaturated with respect to the atmosphere, indicating that the area studied behaves as an atmospheric source of CH4 during the whole year. The magnitude of CH4 saturation in shelf waters was directly influenced by the continental inputs and varied seasonally depending on water temperature and the magnitude of freshwater discharge. CH4 benthic fluxes, although subjected to high variability, seemed to be another considerable CH4 source to bottom waters. Overall, annual CH4 emission was estimated to range from 0.04 (LM86) to 0.08 (W92) Gg CH4 yr− 1 for the area studied (1586 km2). Acknowledgments The authors would like to thank the crew of the R/V Mytilus and R/ V Ucádiz for their valuable assistance during the cruises, M. Fernández Díez-Picazo for his advice on how to treat and analyse the samples and S. Smith for language correction. The authors also acknowledge Spanish Puertos del Estado for providing meteorological data. This work was supported by the Spanish CICYT (Spanish Program for Science and Technology) under contract CTM2005-01364/MAR. S.F.
S. Ferrón et al. / Journal of Sea Research 64 (2010) 213–223
was funded by a grant from the Spanish MECD. The manuscript benefited from the comments provided by two anonymous reviewers. References Bange, H.W., 2006. Nitrous oxide and methane in European coastal waters. Estuar. Coast. Shelf Sci. 70, 367–374. Bange, H.W., Bartel, U.H., Rapsomanikis, S., Andreae, M.O., 1994. Methane in the Baltic and North Seas and reassessment of the marine emissions of methane. Glob. Biochem. Cycles 8, 465–480. Bange, H.W., Dahlke, S., Ramesh, R., Meyer-Reil, L.-A., Rapsomanikis, S., Andreae, M.O., 1998. Seasonal study of methane and nitrous oxide in the coastal waters of the Southern Baltic Sea. Estuar. Coast. Shelf Sci. 47, 807–817. Bates, T.S., Kelly, K.C., Johnson, J.E., Gammon, R.H., 1996. A reevaluation of the open ocean source of methane to the atmosphere. J. Geophys. Res. 101, 6953–6961. Crutzen, P.J., 1991. Methane's sinks and sources. Nature 350, 380–381. De Angelis, M.A., Scranton, M.I., 1993. Fate of methane in the Hudson river and estuary. Glob. Biogeochem. Cycles 7, 509–523. De Angelis, M.A., Lee, C., 1994. Methane production during zooplankton grazing on marine phytoplankton. Limnol. Oceanogr. 39, 1298–1308. De la Paz, M., Gómez-Parra, A., Forja, J., 2007. Inorganic carbon dynamic and air–water CO2 exchange in the Guadalquivir Estuary (SW Iberian Peninsula). J. Mar. Syst. 265–277. Ferrón, S., Ortega, T., Gómez-Parra, A., Forja, J.M., 2007. Seasonal study of dissolved CH4, CO2 and N2O in a shallow tidal system of the Bay of Cádiz (SW Spain). J. Mar. Syst. 66, 244–257. Ferrón, S., Alonso-Pérez, F., Castro, C.G., Ortega, T., Pérez, F.F., Ríos, A.F., Gómez-Parra, A., Forja, J.M., 2008. Hydrodynamic characterization and performance of an autonomous benthic chamber for use in coastal systems. Limnol. Oceanogr. Methods 6, 558–571. Ferrón, S., Alonso-Pérez, F., Ortega, T., Forja, J.M., 2009. Benthic respiration in the northeastern shelf of the Gulf of Cádiz (SW Iberian Peninsula). Mar. Ecol. Prog. Ser. 392, 69–80. Folkard, A.M., Davies, P.A., Fiúza, A.F.G., Ambar, I., 1997. Remotely sensed sea surface thermal patterns in the Gulf of Cadiz and the Strait of Gibraltar: variability, correlations, and relationships with the surface wind field. J. Geophys. Res. 102, 5669–5683. García-Lafuente, J., Ruiz, J., 2007. The Gulf of Cádiz pelagic ecosystem: a review. Prog. Oceanogr. 74, 228–251. García-Lafuente, J., Delgado, J., Criado-Aldeanueva, F., Bruno, M., del Río, J., Miguel Vargas, J., 2006. Water mass circulation on the continental shelf of the Gulf of Cádiz. Deep-Sea Res. Part II 53, 1182–1197. Garratt, J.R., 1977. Review of the drag coefficients over oceans and continents. Mon. Weather Rev. 105, 915–929. Huertas, I.E., Navarro, G., Rodríguez-Gálvez, S., Lubián, L.M., 2006. Temporal patterns of carbon dioxide in relation to hydrological conditions and primary production in the northeastern shelf of the Gulf of Cádiz (SW Spain). Deep-Sea Res. Part II 53, 1344–1362. IPCC, 2007. Climate change 2007: the physical science basis. In: Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L. (Eds.), Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel of Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, USA. 996 pp. Ivanov, M.V., Pimenov, N.V., Rusanov, I.I., Lein, A.Yu., 2002. Microbial processes of the methane cycle at the north-western shelf of the Black Sea. Estuar. Coast. Shelf Sci. 54, 589–599. Jähne, B., Heinz, G., Dietrich, W., 1987. Measurements of the diffusion coefficients of sparingly soluble gases in the water. J. Geophys. Res. 92, 10767–10776. Liss, P.S., Merlivat, L., 1986. Air–sea exchange rates: introduction and synthesis. In: Buat-Ménard, P. (Ed.), The Role of Air–Sea Exchanges in Geochemical Cycling. Reidel, Dordrecht, The Netherlands, pp. 113–127. Machín, F., Pelegrí, J.L., Marrero-Díaz, A., Laiz, I., Ratsimandresy, A.W., 2006. Nearsurface circulation in the southern Gulf of Cádiz. Deep-Sea Res. Part II 53, 1161–1181. Manzano Harriero, J.C., Naranjo Márquez, J.M., Aguilar Perea, M., Sánchez-Lamadrid, A., Jiménez Peral, T., Ruiz Segura, J., Gutiérrez Mas, J.M., Muñoz Pérez, J.L., Saavedra Martín, M., Juárez Dávila, A., Pérez Pastor, A., Romero Romero, Z. 2002. Bahía de
223
Cádiz: Protección de los recursos naturales pesqueros y aplicaciones para instalaciones acuícolas. Dirección General de Pesca y Acuicultura. Consejería de Agricultura y Pesca. Junta de Andalucía. Sevilla, España: 198 pp. Martens, C.S., Berner, R.A., 1974. Methane production in the interstitial waters of sulfate depleted marine sediments. Science 185, 1167–1169. Middelburg, J.J., Nieuwenhuize, J., Iversen, N., Høgh, N., De Wilde, H., Helder, W., Seifert, R., Christof, O., 2002. Methane distribution in European tidal estuaries. Biogeochem 59, 95–119. Navarro, G., Ruiz, J., 2006. Spatial and temporal variability of phytoplankton in the Gulf of Cádiz through remote sensing images. Deep-Sea Res. Part II 53, 1241–1260. Navarro, G., Ruiz, J., Huertas, I.E., García, C.M., Criado-Aldeanueva, F., Echevarría, F., 2006. Basin-scale structures governing the position of the deep fluorescence maximum in the Gulf of Cádiz. Deep-Sea Res. Part II 53, 1261–1281. Niemann, H., Duarte, J., Hensen, C., Omoregie, E., Magalhães, V.H., Elvert, M., Pinheiro, L.M., Kopf, A., Boetius, A., 2006. Microbial methane turnover at mud volcanoes of the Gulf of Cadiz. Geochim. Cosmochim. Acta 70, 5336–5355. Nightingale, P.D., Malin, G., Law, C.S., Watson, A.J., Liss, P.S., Liddicoat, M.I., Boutin, J., Upstill-Goddard, R.C., 2000. In situ evaluation of air–sea gas exchange parameterizations using novel conservative and volatile tracers. Global Biogeochem. Cycles 14, 373–387. Patra, P.K., Lal, S., Venkataramani, S., Gauns, M., Sarma, V.V.S.S., 1998. Seasonal variability in distribution and fluxes of methane in the Arabian Sea. J. Geophy. Res. 103, 1167–1176. Pinheiro, L.M., Ivanov, M.K., Sautkin, A., Akhmanov, G., Magalhães, V.H., Volkonskaya, A., Monteiro, J.H., Somoza, L., Gardner, J., Hamouni, N., Cunha, M.R., 2003. Mud volcanism in the Gulf of Cadiz: results from the TTR-10 cruise. Mar. Geol. 195, 131–151. Reeburgh, W.S., 2007. Oceanic methane biogeochemistry. Chem. Rev. 107, 486–513. Reul, A., Muñoz, M., Criado-Aldeanueva, F., Rodríguez, V., 2006. Spatial distribution of phytoplankton b 13 μm in the Gulf of Cádiz in relation to water masses and circulation pattern under westerly and easterly wind regimes. Deep-Sea Res. Part II 53, 1294–1313. Ruiz, J., Garcia-Isarch, E., Huertas, E., Prieto, L., Juárez, A., Muñoz, J.L., Sánchez-Lamadrid, A., Rodríaguez-Gálves, S., Naranjo, J.M., Baldó, F., 2006. Meteorological and oceanographic factors influencing Engraulis encrasicolus early life stages and catches in the Gulf of Cádiz. Deep-Sea Res. Part II 53, 1363–1376. Sánchez, R.F., Mason, E., Relvas, P., da Silva, A.J., Peliz, A., 2006. On the inner-shelf circulation in the northern Gulf of Cádiz, southern Portuguese shelf. Deep-Sea Res. Part II 53, 1198–1218. Sansone, F.J., Popp, B.N., Gasc, A., Graham, A.W., Rust, T.M., 2001. Highly elevated methane in the Eastern tropical North Pacific and associated isotopically enriched fluxes to the atmosphere. Geophys. Res. Lett. 28, 4567–4570. Somoza, L., Gardner, J.M., Díaz-Del-Río, V., Vazquez, J.T., Pinheiro, L.M., HernandezMolina, F.J., 2002. Numerous methane gas-related sea floor structures identified in Gulf of Cádiz. EOS 83, 541–547. Stadnitskaia, A., Ivanov, M.K., Blinova, V., Kreulen, R., van Weering, T.C.E., 2006. Molecular and carbon isotopic variability of hydrocarbon gases from mud volcanoes in the Gulf of Cadiz, NE Atlantic. Mar. Petrol. Geol. 23, 281–296. Tovar, A., Moreno, C., Manuel-Vez, M.P., García-Vargas, M., 2000. Environmental implications of intensive marine aquaculture in earthen ponds. Mar. Pollut. Bull. 40, 981–988. Upstill-Goddard, R.C., Barnes, J., Frost, T., Punshon, S., Owens, N.J.P., 2000. Methane in the southern North Sea: low-salinity inputs, estuarine removal, and atmospheric flux. Global Biogeochem. Cycles 14, 1205–1217. Upstill-Goddard, R.C., 2006. Air–sea gas exchange in the coastal zone. Estuar. Coast. Shelf Sci. 70, 388–404. Valentine, D., 2002. Biogeochemistry and microbial ecology of methane oxidation in anoxic environments: a review. Antonie Van Leeuwenhoek 81, 271–282. Van Geen, A., Adkins, J.F., Boyle, E.A., Nelson, C.H., Palanques, A., 1977. A 120 yr record of widespread contamination from mining of the Iberian pyrite belt. Geology 25, 291–294. Vargas, J.M., García-Lafuente, J., Delgado, J., Criado, F., 2003. Seasonal and wind-induced variability of Sea Surface Temperature patterns in the Gulf of Cádiz. J. Mar. Syst. 38, 205–219. Wanninkhof, R., 1992. Relationship between wind speed and gas exchange over the ocean. J. Geophys. Res. 97, 7373–7382. Wiesenburg, D.A., Guinasso, N.L., 1979. Equilibrium solubilities of methane, carbon monoxide, and hydrogen in water and seawater. J. Chem. Eng. Data. 24, 356–360.