Benthic fluxes of inorganic carbon in shallow coastal ecosystems of the Iberian Peninsula

Marine Chemistry 85 (2004) 141 – 156 www.elsevier.com/locate/marchem

Benthic fluxes of inorganic carbon in shallow coastal ecosystems of the Iberian Peninsula Jesu´s M. Forja *, Teodora Ortega, T. Angel DelValls, Abelardo Go´mez-Parra Departamento de Quı´mica Fı´sica, Facultad de Ciencias del Mar y Ambientales, Universidad de Ca´diz, Campus Rı´o San Pedro, 11510 Puerto Real, Ca´diz, Spain Received 14 May 2002; received in revised form 7 February 2003; accepted 22 September 2003

Abstract The benthic fluxes of inorganic carbon, total alkalinity and oxygen were measured in five shallow coastal ecosystems located along the coast of the Iberian Peninsula (Southern Europe). The measured values ranged between 135 and 447 mmol m 2 day 1 for inorganic carbon, between 22 and 206 mmol m 2 day 1 for total alkalinity, and between 98 and 199 mmol m 2 day 1 for oxygen. These are higher than most fluxes reported previously in other coastal systems. They presented a linear correlation with the organic carbon content of surface sediments found in the systems studied. For the two sampling stations situated in the Bay of Ca´diz, a significant dependence of the benthic fluxes on the temperature has been observed, with an activation energy value ranged between 45 and 53 kJ mol 1 based on inorganic carbon flux data, and ranged between 34 and 44 kJ mol 1 based on oxygen flux data. The relationship between the fluxes of inorganic carbon and oxygen increases with the concentration of organic carbon in the surface sediments, from values close to 1 up to values in excess of 3, and is found to be affected by variations in temperature. From the vertical profiles in the interstitial water, sulfate-reduction appears to be one of the principal routes of anaerobic oxidation of the organic matter in these systems, and is to a large extent responsible for the variations in pH found and the variation of the ratio of DIC/DO fluxes. D 2003 Elsevier B.V. All rights reserved. Keywords: Inorganic carbon benthic fluxes; Oxygen benthic fluxes; Organic carbon; Sediments; Interstitial waters; Shallow coastal ecosystems; Iberian Peninsula

1. Introduction It is now known that the oceans, taken together, act as a sink for part of the anthropogenic emissions of CO2 to the atmosphere (IPCC, 1995). Within the oceans, coastal systems present a more variable be* Corresponding author. Tel.: +34-956-016163; fax: +34-956016040. E-mail address: [email protected] (J.M. Forja). 0304-4203/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.marchem.2003.09.007

havior (less generalizable), and there exists a certain tendency to consider them as an independent compartment within the overall biogeochemical cycle of inorganic carbon (Holligan and Reiners, 1992). For this reason, several international research programs are currently being undertaken (e.g., LOICZ, ELOISE) with the objective of characterizing the behavior of inorganic carbon in coastal systems. Although a unique form of behavior cannot be established (Walsh, 1991), experimental evidence indicates that coastal

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systems could often release CO2 to the atmosphere (Holligan and Reiners, 1992). The carbon cycle in coastal systems is affected by many different factors. Notable among these factors are the input of inorganic carbon from rivers (Gibbs, 1981), a high level of primary productivity (Portielje and Lijklema, 1995), and the influence of processes of precipitation/dissolution of CaCO3 (Mucci et al., 2000). Furthermore, coastal systems receive substantial supplies of particulate and dissolved organic matter as a consequence of anthropogenic discharges and primary productivity itself. The particulate organic matter is incorporated relatively rapidly into the marine sediments, and then undergoes processes of intensive degradation in coastal systems. As a final result, significant fluxes of inorganic carbon, oxygen and nutrients take place across the water –sediment interface (Hammond et al., 1985; Dollar et al., 1991; Go´mez-Parra and Forja, 1994; Giblin et al., 1997; Berelson et al., 1998). Organic matter diagenesis in the sediments of coastal systems results in aerobic oxidation and sulfate-reduction (Jørgensen, 1982). It may also cause steep vertical gradients in pH and in the concentration of inorganic carbon (Andersen and Kristensen, 1988). The transport of inorganic carbon by the interstitial water is initially produced by molecular diffusion, and is considerably strengthened by processes of irrigation in the first few centimeters of the sediment (Boudreau, 1998). The relative importance of the aerobic and anaerobic routes of oxidation of the organic matter has been evaluated fairly frequently, from the relationship between the benthic fluxes of inorganic carbon and oxygen (Hargrave and Phillips, 1981; Andersen and Hargrave, 1984; Andersen and Kristensen, 1988; Boucher et al., 1994). In this paper, some of the factors affecting the benthic inorganic carbon fluxes found in several shallow coastal ecosystems in the Iberian Peninsula region are discussed. From the relationship between the benthic fluxes of inorganic carbon and oxygen, the importance is demonstrated of the anaerobic routes of oxidation of the organic matter, in this type of zone. The study of the vertical profiles of concentration in the interstitial water shows a continuous production of inorganic carbon in the first 30 cm of interstitial water depth, together with the importance of sulfate-reduction in the diagenesis of

the organic matter and the control of the pH in the interstitial water.

2. Material and methods 2.1. Approach Five coastal ecosystems in the Iberian Peninsula region were selected as study sites, each having a different level of primary production and of anthropogenic organic matter inputs (Fig. 1). The first, the ‘‘Ria of Vigo’’, has an area of 19 km2. Its sediment is mainly clay with a high content of organic carbon (3 – 7%). This site is characterized by its high productivity (5– 300 mmol m 2 day 1, Tilstone et al., 1999). An abundant macrofauna exists in its sediments, composed predominantly of bivalves, gastropods and, in smaller proportions, echinoderms and crustaceans. Four different stations were selected in this area, with a representative range of water depths between 4 and 20 m. Benthic flux measurements were performed during the spring, summer and autumn in 1993. The second site, the Bay of Ca´diz, occupies an area of 38 km2 and receives urban effluents from a population of 600,000 inhabitants. Four stations were selected in this area with water depths ranging between 2 and 14 m, and these were sampled on several occasions from 1988 to 1998. The sediments are mainly of clay and sand, with an average grain size (g) ranging between 0.10 and 0.33 mm. There is abundant macrofauna in this zone, predominantly polychaetes (69%), molluscs (16%) and crustaceans (14%) (DelValls et al., 1998). The third study area selected is the estuary of the Odiel river, which has an area of 71 km2 and is strongly affected by industrial wastes. Four stations were located along the salinity gradient and ranged in depth between 3 and 8 m. Measurements were performed during spring and summer of 1996. The estuary presents a very well-defined spatial gradient in respect of the texture of the sediment, varying from silt –clay up to sand, with an average size of between 0.03 and 0.18 mm. The most abundant species of macrofauna are annelids (37.3 – 99.6%) and crustaceans (0.4 – 50.1%) (Drake et al., 1999). At the fourth site, in the Barbate river, to the south of Ca´diz, one

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Fig. 1. Map showing the locations of the littoral ecosystems along the coast of the Iberian Peninsula selected for study.

station close to the mouth of the estuary (3 m in water depth) was evaluated, and sampling was performed during the summers of 1997 and 1998. The sediments consist mainly of silt (49.5%) and sand (33.8%). The predominant species of macrofauna are oligochaetes (82 – 94%) and polychaetes (6 –18%) (DelValls et al., 1998). The fifth area was the estuary of the Palmones river and the adjacent salt marshes, covering approximately 2 km2. This ecosystem is at the mouth of a small Mediterranean river (the Palmones river), dammed 6 km above its mouth. It receives organic matter from urban and industrial sources. Sampling was performed at four selected stations (2 to 5 m of water depth) during spring, summer and autumn in 1998. The sediment is composed principally of clay and silt, with an average grain size of between 0.03 and 0.18 mm. Macrofauna is relatively scarce in this zone, consisting mainly of the Hydrobya ulvae and Nereis diversicolor species (Clavero et al., 1999). To quantify the inorganic carbon and oxygen fluxes across the sediment – water interface, benthic chambers were used. The chambers are constructed of opaque plexiglass and are ellipsoid in shape, covering an area of sediment of 0.385 m2 and containing volumes between 70 and 90 l depending on the eccentricity of the ellipsoid. The choice of chamber

size to be used at each site and time period was made on the basis of the expected magnitude of the fluxes. The chamber design included a recirculation pump to avoid stratification inside (Go´mez-Parra et al., 1987), allowing current simulation at a range of velocities from 5 to 30 cm s 1 at the outlet of three elbow tubes situated 5 cm above the sediment. The content of solids in suspension was monitored during the incubation, and those samplings where the content of solids in suspension varied by more than 20% from the initial value in the interior of the chamber, were discounted (Go´mez-Parra and Forja, 1993). At pre-set intervals of time (30 min), a fraction collector took the sample from the outflow for analysis. Two chambers were placed on the sediment simultaneously by divers. The total time duration of the chamber deployment varied between 3 and 5 h, based on the oxygen consumption inside the chambers. Oxygen concentrations were monitored in situ using an oxygen electrode, and the decrease in the oxygen concentration was never below 40% of its initial value. Samples were stored at 4 jC until the time of analysis. Sediment cores (40 – 60 mm inner diameter) were sampled by scuba divers, and were transported refrigerated to the laboratory within 3 h. Interstitial water was obtained from 1-cm-thick ‘slices’ of the core, by

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centrifugation at 24 000  g for 30 min at 10 jC. Using this procedure, it was possible to extract between 74% and 83% of the total water content of the sediment. Core transportation and subsequent treatments were performed in a nitrogen atmosphere. The sediment was dried at 80 jC, gently homogenized and sieved using a 63-Am sieve, prior to organic carbon analysis. 2.2. Analytical methods The dissolved inorganic carbon (DIC) concentrations in samples were determined by pH (SWS) and total alkalinity (TA) using a potentiometric analyzer (Metrohm 670) with glass combination electrodes (Metrohm, ref. 6.0210.100). The total alkalinity was obtained from the second point of inflection with an iterative program using the Gran functions. The algorithm includes the influence of the principal acid – base equilibria (nutrient, sulfur and sulfate) in the value of the inorganic carbon concentration (DOE, 1994). For seawater samples, the titration was carried out with 0.1 M HCl in solution of 0.7 M NaCl, whereas for estuarine samples 0.1 M HCl dissolved in pure water was used. During the titration of estuarine water samples, the dilution effect on the ionic strength was taken into account. The sample quantities analyzed from the benthic chamber and the interstitial water were around 100 g (to an accuracy of F 0.001 g) and 2 ml, respectively. The analyses were performed at constant temperature, and they were crosschecked using an inorganic carbon reference material provided by Dr. Andrew Dickson at the Scripps Institute of Oceanography (Batch #33). The results for six samples gave average values of 2010.6 F 2.9 and 2041.2 F 28.1 AM for total inorganic carbon of benthic chamber and interstitial water, respectively, while the certified value was 2009.85 F 0.85 AM. This accuracy and precision is good enough for the benthic flux calculation, taking into account that these fluxes in general result in concentration changes greater than 100 AM during the sampling by the benthic chambers. The organic carbon concentrations in surface sediments were determined by chemical oxidation (Gaudette et al., 1974; El Rayis, 1985) with a standard deviation of F 0.25%. Content of total carbon in sediments was measured using a Carlo Erba (Mod.

1106) elemental analyzer. The salinity was measured using a salinometer (Beckman, Mod. RS-10) with an accuracy of F 0.001. The sulfide concentration ( F 10 AM) in interstitial waters was determined by potentiometric titration (Metrohm, 670) using a sulfur specific electrode (Radiometer, F1212S) and a reference electrode (Metrohm, 6.0726.100). For this, 2 ml of sample had been buffered to pH of 11.5 with 15 ml of a solution containing 0.20 mM of Na2PO42H2O, 0.45 mM of NaNO3, and 0.10 mM of NaOH. The dissolved oxygen (DO) concentration inside the chambers was measured by the Winkler method in discrete samples (accuracy of F 0.1 AM) and continuously monitored with polarographic electrodes (YSI, mod. 57; WTW, CellOx 325). Sulfate concentration was measured by gravimetry (Grasshoff et al., 1983); this method has an accuracy of F 0.02 mM. The diffusive fluxes have been established from the gradients, at zero depth, of the concentration of DIC in the interstitial water, by means of the application of Fick’s first Law (Berner, 1976). For the calculation of the coefficient of diffusion in the sediment (Ds), we have employed the expression proposed by Sweerts et al. (1991), the porosity in the surface layer of the sediment, and an average diffusive coefficient for finite dilution (D0), taking into account the carbonate and bicarbonate concentrations and the D0 values for these species at 25 jC reported by Li and Gregory (1974).

3. Results and discussion 3.1. Benthic fluxes of inorganic carbon The characteristics of the benthic chambers and concentration variations over time inside the chambers have been used to quantify benthic fluxes of dissolved inorganic carbon, total alkalinity and oxygen (Forja and Go´mez-Parra, 1998). Fig. 2 shows typical evolutions of the total alkalinity, pH, inorganic carbon concentrations and O2 concentrations inside chambers, versus time. Usually, each parameter shows either a linear or an exponential change with time. In the case of exponential fits, fluxes have been calculated from the derivative of the concentration, with respect to time from the moment of positioning the chamber on the sediment.

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Fig. 2. Two typical variations (A and B) of the total alkalinity (TA) and the pH values inside the benthic chamber. The dissolved inorganic carbon (DIC) is calculated from the measured variables and the fit employed to calculate the benthic fluxes has been superimposed. Also included are the variations of the concentration of oxygen during the period of time submerged, measured in discrete samples (circle) and continuously using an oxymeter (line).

Table 1 shows the benthic fluxes of inorganic carbon and total alkalinity obtained for the five systems studied. The water depth at each station, the number of measurements carried out, the benthic oxygen demand, the diffusive fluxes of inorganic carbon, the porosity, and the organic carbon concen-

tration of surface sediments are also included. The range of variation of the benthic fluxes of inorganic carbon is very wide (135 –447 mmol m 2 day 1) as a consequence of spatial and temporal variability. In the case of stations PR and LC of the Bay of Ca´diz, a seasonal monitoring has been carried out

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Table 1 Benthic fluxes of inorganic carbon ( FDIC), alkalinity ( FTA) and oxygen ( FDO) in the five littoral ecosystems studied in the Iberian Peninsula System

Ria of Vigo

Station Water N depth (m)

I M P A Bay of PR Cadiza LC SP BN Odiel DR Estuary SC CI CB Barbate B Estuary Palmones PA Estuary PB PC PD

Temperature Salinity (C)

FDIC (mmol m day 1)

2

FTA (mmol m day 1)

2

Diffusive FDIC (mmol m day 1)

2

FDO (mmol m day 1)

2

Porosity Organic carbon (%)

7 20 12 4 3 10 2 14 8 3 7 5 3

3 3 3 3 13 14 3 3 2 2 2 2 2

15.4 – 22.7 15.2 – 23.0 15.0 – 24.4 14.8 – 21.9 12.4 – 25.3 11.4 – 27.3 15.7 – 25.0 15.1 – 23.9 17.4 – 24.2 16.9 – 25.3 17.0 – 24.1 15.9 – 22.5 21.9 – 24.6

12.3 – 28.4 32.4 – 34.2 31.6 – 34.1 29.4 – 34.3 33.8 – 37.7 30.6 – 36.8 32.2 – 37.9 33.5 – 35.7 16.4 – 29.6 5.2 – 18.4 12.3 – 32.5 31.4 – 35.6 28.4 – 33.6

447 F 57 403 F 48 445 F 36 367 F 40 295 F 82 284 F 108 224 F 19 154 F 23 178 F 26 252 F 34 205 F 17 305 F 45 216 F 29

206 F 43 153 F 41 133 F 37 172 F 29 192 F 60 204 F 78 114 F 34 154 F 23 155 F 34 61 F 27 103 F 24 192 F 43 112 F 22

– – – – 11.6 8.7 7.0 9.3 3.9 6.8 3.9 10.3 1.9

147 F 32 154 F 18 199 F 37 118 F 16 126 F 45 146 F 44 115 F 12 106 F 9 99 F 14 129 F 24 102 F 10 139 F 27 133 F 16

0.87 0.80 0.85 0.79 0.81 0.87 0.87 0.78 0.87 0.79 0.73 0.79 0.78

5.03 6.00 6.99 3.19 2.95 2.86 2.65 2.02 2.26 2.72 1.98 4.26 1.71

4 2 5 5

3 3 3 3

15.7 – 24.9 15.9 – 27.1 16.0 – 22.4 15.6 – 25.7

13.5 – 36.1 4.6 – 30.3 36.5 – 36.9 25.6 – 36.7

149 F 23 135 F 18 195 F 15 172 F 10

127 F 26 64 F 15 22 F 12 130 F 34

2.0 1.2 4.8 7.4

111 F 16 98 F 12 150 F 14 163 F 22

0.78 0.77 0.90 0.86

1.26 0.92 3.43 3.12

Included are the number of sampling (N) for each site, the range of variation for the temperature and salinity, the diffusive fluxes of inorganic carbon (diffusive FDIC), the porosity, and the organic carbon concentration in surface sediments. a Some of these data were previously reported by Forja et al. (1994) and Forja and Go´mez-Parra (1998).

over several years (Forja et al., 1994; Forja and Go´mez-Parra, 1998). For this reason, the range of temperature variation is wider than in the other zones, and therefore, the standard deviations associated with the benthic fluxes are also higher. The benthic fluxes of oxygen are also high and present a smaller range of variation than those of inorganic carbon (98 – 199 mmol m 2 day 1). A linear dependence of the average fluxes of inorganic carbon (r2 = 0.75) and the fluxes of dissolved oxygen (r2 = 0.68) with the organic carbon content in surface sediments was detected for all five of the systems studied (Fig. 3). The highest fluxes were measured at stations located at the ‘‘Ria of Vigo’’ site, where the organic carbon content in sediments can reach 7%, whereas the rest of the systems show organic carbon concentrations between 1% and 4%. In this system, the average flux of DIC is about 416 mmol m 2 day 1 and the maximum contribution to the dissolution of CaCO3 of this flux ( FTA/2) is about 86 mmol m 2 day 1. The difference (333 mmol m 2 day 1) is related to the

oxidation of the organic matter. This value is higher than the primary production in the area (5 – 300 mmol m 2 day 1) so more than half of the organic matter that is oxidised should be through other different ways. In this sense, the ecosystem studied in the Ria of Vigo receives organic matter inputs through urban waste from the city of Vigo (300 000 inhabitants) and from rivers Oitaben and Verdugo. Besides, there is an intensive aquaculture farming industry of mussels (34 500  103 T year 1) that produces local concentrations of organic matter higher than 10%. A similar dependence between fluxes and organic carbon content was found for each site. This relationship was observed for the stations selected in the Bay of Ca´diz using a smaller set of data (Forja et al., 1994). The benthic fluxes are the consequence of a complex set of processes that occur throughout the whole column of the sediment. However, based on the experimental set of data available for this study, the organic carbon content in surface sediment appears to be linked to the variables determining the exchange of

J.M. Forja et al. / Marine Chemistry 85 (2004) 141–156

Fig. 3. Relationship between the benthic fluxes of inorganic carbon and of oxygen, and the organic carbon content in surface sediments.

inorganic carbon and oxygen between the sediment and the water column. The linear dependence between the fluxes of inorganic carbon and the organic carbon content originally has a high ordinate, close to 90 mmol m2 day 1. For the dissolved oxygen, the residual flux could be related to the oxidation of reduced chemical species (basically sulphides and ammonia). This flux has also a value of about 90 mmol m2 day 1. Because the stoichiometric of these fluxes is about 1 the residual flux of DIC could be due to the dissolution of CaCO3, which is relatively abundant in the sediment of these zones (17.8% in the Bay of Ca´diz, 13.6% in the estuary of the Odiel, 5.1% in the estuary of the Barbate, and 3.3% in the estuary of the Palmones). Similarly, Hulth et al. (1997) estimated that the dissolution of CaCO3 contributed between 2.6% and 71% to the total flux of inorganic carbon in the south of the Weddel Sea (Antarctica) and Cermelj et al.

147

(2001) calculated a contribution of 40% in the Gulf of Trieste. The ratio between the fluxes of alkalinity ( FTA) and of inorganic carbon ( FDIC) has been employed to estimate the relative importance of the processes of oxidation of organic carbon and of dissolution of CaCO3. For the stations taken together, a well-defined trend between the variations of FTA and FDIC has not been found, largely due to the heterogeneity of the systems considered. The ratio between FTA and FDIC has an average value of 0.53, and varies between 0.40 in the Rı´a of Vigo, and 0.69 in the Bay of Ca´diz. From FTA/FDIC, Jahnke and Jahnke (2000) estimate the ratio of the CaCO3 dissolution rate to the organic carbon oxidation rate. Utilizing the simple model that they propose, the rate of CaCO3 dissolution is 0.25 times the rate of organic carbon oxidation, in the Rı´a of Vigo, 0.52 in the Bay of Ca´diz, 0.39 in the estuary of the Odiel, 0.35 in the estuary of the Barbate and 0.38 in the estuary of the Palmones. For all the stations taken together, an average value of 0.36 is obtained. If one considers that the average value of FDIC is 253 mmol m 2 day 1 for all the systems studied, the contribution of the dissolution of CaCO3 to this flux would be close to 90 mmol m 2 day 1, consistent with the intercept of the linear regression between the benthic fluxes of DIC and the content of organic carbon in the surface sediments (Fig. 3). In addition, the benthic fluxes of inorganic carbon and oxygen are highly dependent on temperature. The natural logarithm of the inorganic carbon fluxes and oxygen fluxes versus the inverse of the absolute temperature measured at two stations at the Bay of Ca´diz is shown in Fig. 4. The activation energy based on the benthic fluxes of inorganic carbon can be calculated from the slope of these lines, and varies between 45.2 kJ mol 1 at station PR (r2 = 0.73, n = 13) and 52.7 kJ mol 1 at station LC (r2 = 0.96, n = 14). For oxygen, the activation energy estimated is 33.9 kJ mol 1 (r2 = 0.92, n = 12) at station LC and 43.8 kJ mol 1 (r2 = 0.66, n = 13) at station PR. These values are similar to those previously reported in the Bay of Ca´diz by Forja et al. (1994), using a smaller database. Other authors, Aller (1980) and Aller and Yingst (1980), propose similar values for the activation energy of the principal enzymatic activities related to the processes of degradation of the organic

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Fig. 4. Variations of the natural logarithm of the benthic fluxes of inorganic carbon and oxygen with the inverse of the absolute temperature, at two stations located in the Bay of Ca´diz (LC and PR). The open symbols have not been considered in the fits made to calculate the activation energy.

matter in marine sediments. The seasonal variation in the benthic fluxes of inorganic carbon and oxygen depends more on the temperature than on the supplies of organic matter. In this context, the high C/N ratio (10 – 20) found in the sediment of the Bay of Ca´diz suggests that most of the organic matter is of the anthropogenic type, and therefore the supply of this matter to the medium is not subject to seasonal variation. In Table 2, the average benthic fluxes measured in this study are compared to fluxes reported by other authors for different coastal ecosystems around the world. The inorganic carbon fluxes present an extremely wide variation, from the lowest value of 3 mmol m 2 day 1 of the estuarine waters of the Parker river (Hopkinson et al., 1999), to the highest value of 732 mmol m 2 day 1 in shallow coastal ecosystems located in the Balearic Islands (Lo´pez et al., 1995). In comparison, the mean values of the inorganic carbon fluxes obtained in this study ranging between 135 and 447 mmol m 2 day 1 are relatively

high. The mean value of the benthic fluxes of inorganic carbon given in Table 2 is 103 mmol m 2 day 1, with a standard deviation of 110 mmol m 2 day 1. The benthic fluxes of oxygen measured may also be considered high in comparison with the data base given in Table 2, although fluxes of up to 433 mmol m 2 day 1 have been reported in estuarine waters of the Parker river (Hopkinson et al., 1999). The widespread of values found in this data base must be related to the heterogeneity of the coastal systems themselves, as can be observed from the interval of variation measured in each zone, but the differences in the methodology used to measure the benthic flux in each study will also be a contributing factor. On this point, the high benthic fluxes of inorganic carbon measured in the Iberian Peninsula do not include the effect of the primary benthic production (opaque chambers). The ratio between the fluxes of inorganic carbon and of the dissolved oxygen ( FDIC/FDO) is highly variable from site to site (ranging from 1.1 to 3.1) with

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Table 2 Benthic fluxes of inorganic carbon and dissolved oxygen in shallow marine ecosystems studied by various authors Site

Technique

Depth (m)

Temperature (jC)

f2

1.0 – 16.0

0.1 – 1.1

7.5 – 17.5

–

6.7 – 183.1

7.2 – 52.6

12.0 – 27.5

3.3 – 5.0

31.0 – 162.7

–

1.4

17.0 – 28.0

1.1 – 7.7

0.3 – 5.0a

30.2 – 62.9

25.4 – 54.2

–

14.4 – 26.0

3.7 – 15.0

Eastern Passage (Nova Scotia) Cobequid Bay (Nova Scotia) Cape Lookout Bight (N Carolina) San Francisco Bay (S California) Norsminde Fjord (Denmark) Tomales Bay (California) Ao Nam Bor mangrove (Thailand) Northern Adriatic Sea Lagoon of New Caledonia Ao Nam Bor mangrove (Thailand) Albufera of Majorca (Mediterranean) Boston Harbor (Massachusetts) Port Phillip Bay (Australia) Bay of Ca´diz (Spain)

Chambers

Chambers

2 – 14

Young Sound (Northeast Greenland) Plum Island Sound – River Parker estuary Gulf of Trieste (Northern Adriatic) Iberian Peninsula

Core incubations Core incubations Core incubations Chambers

36

a

Core – incubations Chambers – Chambers

Organic DIC flux carbon (%) (mmol m

1.5 – 14 14.3 – 14.5

2

day

28.6 – 95.7

DO Flux ) (mmol m

1

References 2

8.3 – 41.1

Core f 0.5 incubations Chambers 4 – 6

15.0

Core <2 incubations

28.0 – 33.0

0.6 – 1.8

69.9 – 86.1

44.7 – 61.1

Chambers

18.0 – 22.0

0.5 – 1.3

12.2 – 25.2

5.3 – 19.9

Core 10 – 17 incubations Core <2 incubations

23.9 – 27.8

–

23.0 – 124.1

20.9 – 105.1

28.0 – 33.0

0.1 – 2.5

23.0 – 31.0

23.0 – 34.0

Chambers

28.5 – 31.9

–

63.4 – 732.0

32.4 – 97.2

0.14 – 6.1

10.0 – 185.0

7.0 – 220.0

–

23.0 – 103.0

23.0 – 102.0

2.2 – 3.1

154.6 – 224.5

–

1.3

5.4 – 9.6

5.0 – 13.0 6.0 – 433.0

f 40

–

–

Core 3.5 – 13 0.0 – 20.0 incubations Chambers 14 10.0 – 13.0 18.4 F 6.8

1.2 – (

1.8)

0.5 – 4

3.6 – 28.1

0.2 – 10.3

3.0 – 520.0

–

10.0 – 20.0

–

5.0 – 10.1

–

11.4 – 27.3

0.9 – 7.0

135.0 – 447.0

98.0 – 199.0

2 – 20

Density of sediment equal to 2 g cm

3

day

1

) Hargrave and Phillips (1981) Andersen and Hargrave (1984) Martens and Klump (1984) Hammond et al. (1985) Andersen and Kristensen (1988) Dollar et al. (1991) Kristensen et al. (1991) Giordani et al. (1992) Boucher et al. (1994) Kristensen et al. (1994) Lo´pez et al. (1995) Giblin et al. (1997) Berelson et al. (1998) Forja and Go´mez-Parra (1998) Rysgaard et al. (1998) Hopkinson et al. (1999) Cermelj et al. (2001) This study

.

an average value of 1.9 F 0.2. This is related to the intensity of the different anaerobic routes taken in the mineralization of the organic matter (Hargrave and Phillips, 1981; Andersen and Kristensen, 1988). Different processes have been described that modify the relationship between the fluxes of DIC and DO. In this context, the oxidation of sulfides in the surface oxic layer of the sediment may contribute to increase

this relationship, especially during summer time (Jørgensen, 1977; Giblin et al., 1997). In addition, the production of CO2 could be affected by the activity of chemoautotrophic bacteria and/or by processes of precipitation/dissolution of CaCO3 (Anderson et al., 1986). A dependence of the mean values of the ratio FDIC/ FDO in each system with the content of organic carbon

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defined, it can be appreciated how the lowest values are produced in the winter months. Since the aerobic oxidation is limited by availability of oxygen near the bottom, an increase of the benthic metabolism with increasing temperature (Klump and Martens, 1981; Thamdrup et al., 1998) would explain a strengthening of the anaerobic routes of oxidation of the organic matter. 3.2. Interstitial waters

Fig. 5. Variation of the mean ratio of inorganic carbon flux to oxygen flux ( FDIC/FDO) of the various systems studied, with the mean organic carbon content in the sediment (EB: Estuary of Barbate; EP: Estuary of Palmones; BC: Bay of Ca´diz; EO: Estuary of Odiel and RV: Ria of Vigo). The deviations shown correspond to the standard error.

in the sediments has been observed (Fig. 5). On this point, it appears that a strengthening of the anaerobic oxidation routes takes place in proportion to the increase of the organic carbon content of the sediment. Fig. 6 shows the seasonal variation of the FDIC/ FDO at two stations of the Bay of Ca´diz. Although the dependence of their values on temperature is not well

The variables associated with inorganic carbon speciation versus the sediment depth for three different stations of the Bay of Ca´diz are shown in Fig. 7. Similar to the benthic fluxes, it shows a direct relationship between the organic carbon content in sediments and the inorganic carbon concentration in the interstitial waters. The organic carbon concentrations in these sediments are relatively constant, showing little decrease with depth. The progressive increase of DIC with depth is directly correlated with the mean organic carbon content present in each zone. This kind of pattern has been widely reported (Emerson et al., 1980; Hansen and Blackburn, 1991; Komada et al., 1998). The pH values in interstitial waters do not show a clear relationship with depth. Two opposing trends have previously been reported in other systems:

Fig. 6. Seasonal evolution of the ratio of inorganic carbon flux to oxygen flux ( FDIC/FDO) at two stations of the Bay of Ca´diz (LC and PR).

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Fig. 7. Vertical variations of the organic carbon content, pH (SWS), the concentration of inorganic carbon and sulfate, the degree of CaCO3 saturation, and the diffusion coefficient (Ds) of the inorganic carbon, in the Bay of Ca´diz (stations SP, LC and PR). The saturation percentage (X) has been estimated considering a constant Ca concentration of 10 2 M, and reflects a predicted saturation if precipitation does not occur.

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decreasing with depth (Revsbech et al., 1983; Bonanni et al., 1992) and increasing with depth (Emerson et al., 1980; Pedersen, 1984). In Fig. 7, a decrease of the pH values is found in the surface zone of the sediment for the three stations, in response to the aerobic oxidation of organic matter and the reoxidation of dissolved reduced species (Cai and Reimers, 1993; Canfield et al., 1993; Cai et al., 2000; Mucci et al., 2000). When the organic carbon content in the sediment is low and the gradient of sulfate concentration in the interstitial water is also low, the pH values are practically constant at depths below the oxic zone (station SP). On the other hand, when the organic carbon content is higher, with intensive sulfate-reduction, an increase in the pH values can be observed (stations PR and LC). This pattern is typical of coastal marine sediments (Kristensen et al., 1991; Cai et al., 2000). Plots of DIC variations vs. alkalinity variations (DDIC/DTA) in the interstitial water (Fig. 8) have been utilized to investigate the possible mechanisms by which sulfate reduction takes place. A high linearity is observed between DIC changes and TA changes, with slopes of 0.84 (r 2 = 0.905) at station SP, 0.69 (r 2 = 0.958) at PR, and 0.83 (r 2 = 0.953) at LC. Linear fits applied to the first 3 cm of sediment do not show significant changes of slope, possibly related to the shallow depth of oxygen penetration in the sediments of these stations, less than 0.3 mm if the model proposed by Cai and Sayles (1996) is used. Considering that the C/N ratio in the surface sediments of the Bay of Ca´diz varies between 10 and 20 (Forja et al., 1994), slopes of between 0.86 and 0.89 would be expected for the sulfate reduction based on degradation of organic matter with an average oxidation state of zero, and slopes of between 0.59 and 0.61 would be expected for the oxidation of less oxidized forms (CH4) of organic matter (Hammond et al., 1999). In different proportions depending on the stations, these are two mechanisms that describe most adequately the variations found in the interstitial water. Other mechanisms described, that consider the participation of elemental sulfur or the substitution of iron by Mg2 + and the subsequent precipitation of pyrites, lead to DIC/TA ratios noticeably larger than those found. In general, the stoichiometric relationship between the production of DIC and the consumption of SO42

Fig. 8. DIC changes vs. alkalinity changes observed in pore waters of the Bay of Ca´diz (stations SP, LC and PR).

(DDIC/DSO42 ) is close to 2:1 (Klump and Martens, 1989; Boudreau et al., 1992; Glud et al., 2000). In the zones of the Iberian Peninsula studied, the relationship obtained varies between 0.5 and 2, as occurs in other coastal zones (Klump and Martens, 1989; Thamdrup

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and Canfield, 1996; Mucci et al., 2000). One possible explanation for these low values of DDIC/DSO42 is the precipitation of calcium carbonate induced by the increase of the DIC concentration in the interstitial water and the increase of pH with depth. Fig. 7 shows the variation of the degree of saturation of CaCO3 (calcite) in the selected stations of the Bay of Ca´diz; these have been calculated from the apparent solubility constant of calcite proposed by Mucci (1983) at a salinity of 35 and a temperature of 25 jC, and a concentration of Ca2 + typical of seawater (10 2 M). The high degrees of saturation obtained are due fundamentally to the increase of the CO32 concentration with depth, which reaches values of up to 4 mM, and constitutes experimental evidence of the precipitation of CaCO3 in the anoxic zone of the sediments studied. Calcium carbonate formation can also control the maximum pH values measured (Luff et al., 2000). The calcite saturation values obtained could be considered an approximation because the concentration of calcium in the interstitial water was not analyzed and the potential loss of CO2 during the processing of the sample (centrifugation) could produce an increase in the pH values. The values obtained for the diffusive fluxes range between 1.2 and 11.6 mmol m 2 day 1, and are lower than those measured with the benthic chambers (Table 1). Forja and Go´mez-Parra (1998) have previously reported similar underestimation of the inorganic carbon fluxes calculated from the sediment core data for the Bay of Ca´diz. This difference is related to the influence of irrigation on the benthic fluxes and, to a less extent, to the poor depth resolution of the vertical profiles close to the interface. This phenomenon has been characterized for the exchange of other substances such as nutrients (Hopkinson, 1987). Another process to be considered is the dissolution of CaCO3 on the surface of the sediment induced by the reduction of the pH in the aerobic oxidation of the organic matter (Mucci et al., 2000). 3.3. Final remarks The benthic fluxes of inorganic carbon and oxygen in the coastal systems studied in the Iberian Peninsula are high (260 F 103 and 131 F 27 mmol m 2 day 1, respectively). Although the benthic fluxes present a wide range of variability that is a consequence of the

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intrinsic heterogeneity of coastal systems (Ver et al., 1999), a certain dependence of their values with the organic carbon content of surface sediments and with the temperature has been found. The high values of the benthic fluxes of inorganic carbon and oxygen are found to be associated with an intense oxidation of the organic matter and with the dissolution of CaCO3 in the surface sediments. In addition, the processes of exchange with the interstitial water could be found strengthened by the presence of a relatively abundant benthic macrofauna. The profiles of sulfate concentration in the interstitial water suggest that sulfate reduction, together with aerobic oxidation, constitute the principal mechanisms of degradation of the organic matter in the systems studied. This behavior has been described in many other coastal zones (Thamdrup and Canfield, 1996; Kostka et al., 1999; Glud et al., 2000), where sulfate reduction is found to be capable of re-mineralizing between 10% and 90% of the organic matter present (Jørgensen, 1982; Canfield, 1993) and exercises significant control over the pH of the interstitial water (King, 1988; Hammond et al., 1999; Mucci et al., 2000). The benthic production of inorganic carbon in coastal systems (of less than 200 m depth) has been estimated from global balances (Mackenzie et al., 1998; Ver et al., 1999). Using the Terrestrial-Ocean aTmosphere Ecosystem Model (TOTEM), Mackenzie et al. (1998) and Ver et al. (1999) have proposed a total global production of 7.6  1014 mol C per year for all these systems taken together. If a total area of 26  106 km2 is taken for the world’s coastal zones (Gattuso et al., 1998), the mean value of the benthic flux of inorganic carbon obtained from these balances is 80 mmol m 2 day 1. Mean values of global benthic fluxes of inorganic carbon obtained from experimental measurements do not exist for the coastal zones. The systems considered in Table 2 are characterized by being relatively shallow ( < 40 m) and by having high contents of organic carbon in the surface sediment. The mean benthic flux of DIC in these systems is 103 mmol m 2 day 1. This value is consistent with the flux calculated from the data of Mackenzie et al. (1998) and Ver et al. (1999), if the dependence of the benthic fluxes on depth in the transition zone of the continental shelf is considered (Thamdrup and Canfield, 1996; Hammond et al., 1999).

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Acknowledgements This work was supported by the Spanish Comisio´n Interministerial de Ciencias y Tecnologı´a (CICYT) of the Ministerio de Educacio´n y Ciencia under contract REN2001-3577/MAR. Thanks to M.F. Osta and P. Vidal for their assistance during sampling and analysis. Associate editor: Dr. Christopher Martens

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