Environ. Sci. Technol. 2008, 42, 86–92
High-Frequency Archives of Manganese Inputs To Coastal Waters (Bay of Seine, France) Resolved by the LA-ICP-MS Analysis of Calcitic Growth Layers along Scallop Shells (Pecten maximus) A . B A R A T S , † D . A M O U R O U X , * ,† C. PÉCHEYRAN,† L. CHAUVAUD,‡ AND O. F. X. DONARD† Laboratoire de Chimie Analytique Bio-Inorganique et Environnement, IPREM UMR 5254, CNRS - Université de Pau et des Pays de l’Adour, Hélioparc Pau-Pyrénées, 2 avenue du Président Angot, 64053 Pau Cedex 9, France, and Laboratoire des Sciences de l’Environnement Marin, IUEM UMR 6539, CNRS - Université de Bretagne Occidentale, Technopole Brest-Iroise, Place Nicolas Copernic, 29280 Plouzané, France
Received January 17, 2007. Revised manuscript received September 14, 2007. Accepted September 25, 2007.
During their growth, bivalves are recognized to archive minor and trace elements within their shells which may reflect environmental conditions at the sediment-water interface (SWI). Shells from juvenile Great Scallops (Pecten maximus (L.)), which develop a daily calcite growth layer, were collected in the Bay of Seine (France) and examined by matrixmatched Laser Ablation ICP-MS analysis for Mn concentrations along their growth period, from April to October (year 2004). The backdated Mn concentration profiles were compared with environmental variables (e.g., temperature, salinity, chlorophyll a, oxygen, etc.) measured continuously at monitoring stations in riverine, estuarine, and coastal waters. The objective was first to perform microanalyses of Mn composition along the shell reflecting episodic enrichment or depletion in such environment, and second, to depict Mn cycling and inputs at the SWI according to the measured profiles. Basically, Mn concentration profiles mostly depend on established estuarine and coastal biogeochemical processes that lead to an increase of dissolved Mn concentration available for shell uptake. Potential particulate Mn fluxes from the Seine River, that control both particulate and dissolved Mn input to the bay, are strongly correlated with shell Mn concentrations from April to July (r2 ) 0.95, n ) 8, p < 0.05). In late summer, riverine inputs can not only provide an explanation for the shell Mn enrichments which suggest additional sources of Mn. During this period, two other processes also contribute to the release of dissolved Mn in coastal waters and the increase of shell Mn content: (1) successive redox oscillations within the high turbidity zone of the macrotidal Seine estuary and (2) postbloom reductive * Corresponding author e-mail:
[email protected]; tel: +33 559 407 756; fax: +33 559 407 781. † CNRS - Université de Pau et des Pays de l’Adour. ‡ CNRS - Université de Bretagne Occidentale. 86
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conditions developed at the SWI of the Seine Bay under periodic seasonal eutrophication. This study demonstrates that incremental Mn concentrations profiles in scallop shells are a relevant natural archive to evaluate the processes governing Mn inputs into coastal environments at a daily scale.
Introduction Manganese is an element involved in redox processes which exhibits a relatively high mobility in estuarine and marine waters (1–4). Chemical Mn speciation is essential to understand redox processes in gradually changing chemical environments such as estuaries and oxic-anoxic interfaces (5, 6). The cycling of Mn in estuaries is rather dominated by natural processes such as river inputs, particle desorption, and sediment remobilization (7). In oxygenated seawaters, the most stable Mn form is the insoluble MnIV which occurs as MnO2(s) (4, 8). In estuarine and coastal waters, permanently oxygenated conditions are not remaining and by consequence, occurrence of transient reducing conditions can favor the dissolution of particulate MnO2(s) into dissolved MnII as Mn2+ (3). The slow kinetic of the Mn oxidation can account for the persistence of this meta-stable ionic specie in oxic waters (9). Dissolved Mn is particle reactive and can be removed from the water column by oxidation, sorption onto inorganic and organic particles, or bacteria and phytoplankton uptake (5, 6, 10, 11). Dissolved Mn was reported to increase during important Mn inputs of nonsaline waters (freshwater runoff and wastewaters) (8, 12). Mn release from riverine suspended particles in the estuarine mixing zone, especially in the high turbidity zone (HTZ) of macrotidal estuaries, was evidenced in various studies (3, 13). Benthic inputs of Mn at the sediment-water interface (SWI) can also increase the dissolved Mn concentration in the water column (14). These seasonal inputs were attributed to the diagenetic remobilization of Mn under reducing conditions during summer when intense benthic respiration leads to decreased dissolved oxygen concentrations (8, 15, 16). As a result, Dellwig et al. demonstrated that the total Mn inventory in the German Wadden Sea shallow water column was respectively influenced by reductive benthic remobilization in summer and by freshwater discharge in winter (17). Measurements of benthic Mn fluxes at the SWI were already performed and were correlated to the global benthic respiration rate (O2 consumption) both in a shallow eutrophic bay (18) and in a deep coastal bay (19). It is now well established that the speciation of Mn is a prominent indicator of redox conditions at the SWI in coastal environments (4). The cycling of Mn has been already investigated in dissolved and particulate phases of both the Seine estuary (2, 3) and adjacent coastal waters (20, 21). Mn partition between dissolved and particulate phases in the Seine estuary was reported to be strongly influenced by the formation of inorganic complexes (e.g., carbonate) which decreases dissolved Mn concentrations, and by the increase of salinity and suspended matter concentrations which increase the dissolved Mn concentrations (3). Significant benthic fluxes from sediment and the HTZ in the Seine estuary have also been reported due to dissolved Mn release from the solid phase to the pore water by reductive dissolution of Mn oxides, and further reinjection to the water column during the sediment erosion periods (2, 3, 22–24). In coastal waters from the adjacent English channel, significant increases of dissolved Mn were measured during the summer period and were also associated with the benthic release of dissolved Mn to the coastal water column (20, 21). 10.1021/es0701210 CCC: $40.75
2008 American Chemical Society
Published on Web 12/06/2007
Mn/Ca ratios in calcite shells of Mytilus edulis and Isognomon ephippium were first reported to be respectively related to seasonal changes in primary production (25), and to increased riverine discharge and subsequent phytoplankton bloom events (26), suggesting a trophic uptake of Mnenriched particles. Mn2+ uptake by the Crassostrea gigas calcite bivalves was suggested to be enhanced in summer at higher seawater temperature promoting aqueous Mn2+ bioavailability and biomineralization rates (27). Seawater temperature was however reported to have a minor influence on Mn contents in aragonite bivalve shells (Mesodesma donacium and Chione subrugosa) from the Peruvian Coast (28) and in calcite bivalve shell (Pecten maximus) (29). In Pecten maximus originating from the Menai Strait (Wales, UK), seasonal variations of shell Mn/Ca ratios were suggested to reflect the intra-annual variation of seawater-dissolved Mn2+ (29). This result suggests a preferential uptake of dissolved Mn into the shell, although it has not been experimentally demonstrated. The shell of the Great Scallop (Pecten maximus) was already promoted as a valuable archive of environmental changes in temperate environment (30–34). Chauvaud et al. demonstrated that the isotopic oxygen composition of the daily calcite striae accurately tracks the seawater temperature measured in situ in bottom waters at a daily resolution which underscored a daily deposition of calcite striae on Pecten maximus shells (32). The variations of trace element concentrations in this daily calcite growth layer (stria) may provide significant high-frequency archived information to especially constrain biogeochemical processes at the SWI (33, 34). The laser ablation-inductively coupled plasma-mass spectrometry coupling (LA-ICP-MS) was previously developed for the quantitative microanalysis of trace elements in calcium carbonate (CaCO3) matrices by the use of matrixmatched standards (35). Quantitative analyses of trace elements along the daily calcite striae of the Great Scallop shells (Pecten maximus) provided then chronological profiles at high temporal resolution. In this study, backdated shell Mn concentration profiles are first examined along 3 shells covering the growth period of the year 2004 (from April to October). The variability of the shell Mn content is then compared to environmental variables providing the temporal biogeochemical status along the investigated period. The reconstruction of shell Mn profiles in relation to major potential processes leading to Mn inputs at coastal SWI is further established. The aim of this study is thus to mainly demonstrate the usefulness of exploring Mn concentration variations in scallop shell, especially in coastal areas for which continuous and longterm high-resolution monitoring of Mn can not be easily achieved.
Materials and Methods The Seine River (France) is the largest freshwater outflow into the English Channel (Figure A in the Supporting Information). Its length is 780 km and its catchment area is 75000 km2 in which 40% of the French population and economic activity are located (2). The annual mean water discharge ranges from 200 to 650 m3 s-1 with significant seasonal fluctuation (from 60 to 2000 m3 s-1) (36). The suspended particulate matter concentrations of the river mostly depend on the water inflow, leading to a mean annual flux to estuarine waters of about 5 × 108 kg y-1 (37). This macrotidal estuary is characterized by a high turbidity zone (up to several g L-1), related to the large tidal range (3 m at neap tide to 7.5 m at spring tide) coupled with relatively shallow depths (37). Freshwater turnover time in the estuary is ranging from 2 to 30 days depending on freshwater runoff and tidal range. The Bay of Seine is usually considered one
FIGURE 1. Shell Mn concentrations (µg g-1) along shell growth layers (backdated from April to mid-October 2004) of 3 Pecten maximus shells collected in the Bay of Seine compared to environmental variables collected at monitoring stations upstream and downstream to the Seine estuary and in the Bay of Seine. The flow rate (m3 s-1) and the particulate flux (kg s-1) were measured at the Seine River end-member (Poses); the seawater temperature (°C) and the oxygen saturation (%) were measured in surface seawater at Honfleur station (Seine estuary, high-turbidity zone); and the chlorophyll concentrations were measured in surface seawater and the oxygen saturation (%) was measured in bottom water at Luc buoy (Bay of Seine). The dashed lines indicate maxima of Mn shell concentrations. The grey zones represent the maxima of shell Mn concentrations which are not mainly influenced by the upstream particulate Mn inputs from the Seine River. of the most eutrophicated coastal ecosystems in Europe, due to large nutrient loadings from the Seine River (38). This ecosystem is mainly influenced by material load from the VOL. 42, NO. 1, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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Seine River, with the inputs induced by the other coastal rivers being negligible. Only one-year-old scallops (class 1) were collected in the Bay of Seine (France) by dredging trail onboard a professional fishing vessel (L. Chauvaud, personal communication). The sampling area, shown in Figure A in the Supporting Information, is characterized by one of the highest scallop densities in the bay and has a total depth ranging between 20 and 30 m. Other sampling sites of Western Europe (Atlantic Ocean) were described by Barats et al. (33, 35). The shells were cleaned with glacial acetic acid (Merck, analysis grade) for 60 s, thoroughly rinsed with 18.2 MΩ milli-Q water and dried overnight. Only the top side of the flat valve part and its juvenile stage (second year of growth) were considered for LA-ICP-MS analysis because of their long growth period (April to November). A 45 × 10 mm2 cross section corresponding to the year 2004 was then cut along the axis of maximum growth rate with a diamond saw to fit into the ablation cell of the laser. Quantitative analyses of 55Mn and 43Ca, within the shell striae, were performed by a LA-ICP-MS method consisting of coupling a UV laser ablation unit (LSX 100 UV 266 nm, Cetac Tech.) to an ICP-MS (X7 serie, Thermo Fisher). The methodology and its validation are described by Barats et al. (35). The intensity of the 55Mn isotope signal was first normalized against the 43Ca signal to compensate for instrumental drift and instability. A matrix-matched external calibration was then performed with laboratory-prepared CaCO3 pellets with Mn concentrations ranging from 0.289 to 20.8 µg g-1 (35). This Mn calibration displayed a good linearity (r2 < 0.999), sensitivity (DL ) 14 ng g-1), analytical repeatability (5 integration zones during 1 analysis), and reproducibility (5 successive independent analyses) (%RSD < 5) (35). Shell analyses were performed each third striae to obtain a temporal resolution of 3 days. A date can be then assigned to each ablated striae by backdating from the harvest date. An estimate of the shell growth rate, expressed in µm d-1, was made for each shell by measuring distances between successive striae (30). For a better interpretation of Mn profiles, all hydrological (temperature, salinity, turbidity, suspended particulate matter), biological (chlorophyll a), and chemical variables (oxygen, ammonium, nitrates, phosphates) were examined upstream and downstream of the Seine estuary, respectively, in the Seine River end-member (Poses dam), in the Seine estuary (Honfleur, HTZ), and in the Seine Bay (Luc buoy, near shell sampling zone). This environmental database originated from different coastal monitoring programs: GIP Seine-Aval, Agence de l’eau Seine Normandie, database QUADRIGE of the French Research Institute for Exploitation of the Sea (IFREMER: MAREL, RHLN programs) (Supporting Information). The particulate flux was estimated as the product of the freshwater discharge by the suspended particulate matter (SPM) concentrations at Poses station (upstream river end-member). Further, Mn particulate fluxes from the Seine River were also evaluated at Poses (2) using a rather constant particulate Mn concentration of 416 ( 75 mg kg-1, averaged over a 10-year period (1993–2003).
Results and Discussion Significance and Variations of Shell Mn Concentration Profiles. Figure 1 presents shell Mn concentration profiles along the growth period (backdated Julian days) for three shells which are characterized by similar concentrations along the shell with Mn/Ca ratio averaging 7 ( 3 µmol mol-1 (Table A in the Supporting Information). Mn concentration profiles also exhibit well correlated seasonal variations between two different shells (r2 > 0.56, n ) 47, p < 0.05). Such intershell comparison (n ) 3) confirms that variations of Mn concentrations with a 3-day resolution are reproducible among 88
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various shells belonging to the same population and location (Figure B in the Supporting Information). The reproducibility of shell Mn profiles among scallop populations (n ) 21) has also been demonstrated in the Bay of Brest over a 7-year period (1998–2004) (33). Shell Mn profiles in the Bay of Seine can be divided into four main periods from April to October 2004. Shell Mn concentrations are first decreasing in April from 4 to 1 µg g-1, remain low from May to mid-June (n ) 3) (averaging 1.9 ( 0.3 µg g-1), increase dramatically at end of June to reach higher Mn contents from July to September (averaging 5.1 ( 0.9 µg g-1), and finally decrease in early October until the end of the shell growth period (Figure 1, Table A in the Supporting Information). Such shell enrichment of Mn during the summer period exhibits, however, a significant variability of Mn concentrations punctuated by four maxima occurring the 08/07 (4.6 ( 0.8 µg g-1), the 20/07 (5.8 ( 0.5 µg g-1), the 09/08 (6.1 ( 1.0 µg g-1), and the 25/08 (5.7 ( 1.2 µg g-1) (date uncertainty ( 3 days) (Figure B in the Supporting Information). In September, shell Mn concentrations decreased moderately down to 3.4 ( 1.0 µg g-1 (14/09) to subsequently increase end of September to reach a maximum value of 5.7 ( 2.7 µg g-1 (26/09). The comparison between seasonal variations of shell Mn concentrations in the Bay of Seine and the shell growth rate (Figure A in the Supporting Information) agreed with previous studies on biogenic calcium carbonate which demonstrated that shell Mn uptake was not significantly influenced by seawater temperature or shell growth rate (25, 26, 29). In Table 1, Mn concentrations in Pecten maximus shells from the Bay of Seine are compared with the results obtained for different coastal ecosystems in Europe (33) and with similar investigations involving either scallop or mussel shells (25, 29). This comparison first reveals that shell Mn concentrations usually exhibit summer enrichments, especially for ecosystems subjected to riverine inputs. These previous studies performed in coastal environments underlined summer shell enrichments of similar amplitude (ca. 2 times the mean concentrations) (25, 29). Because such relative Mn enrichments remain independent from the analytical methodology or shell characteristics, similar biogeochemical processes are suggested to increase shell Mn uptake in these coastal environments. Freitas et al. previously considered that shell Mn concentrations in Pecten maximus reflect mainly dissolved Mn variations in coastal waters of the Menai strait (UK) (29). Scallops, standing at the SWI, were considered to be highly sensitive to redox benthic release of dissolved Mn, although a direct relationship between shell and dissolved Mn concentrations was not demonstrated. Langlet et al. determined by cathodoluminescence analysis intense Mn enrichment layers along a large mussel shell corresponding to summer hypoxic or anoxic Mn remobilization taking place in a eutrophic coastal lagoon (27). Finally, our seven year survey (1998–2004) on scallop shells from the Bay of Brest did not exhibit any significant or reproducible (n ) 3) variations of shell Mn concentration along the year (Table 1). Although this ecosystem is subjected to large phytoplankton blooms, no significant oxygen undersaturation was ever observed in the water column of the Bay of Brest, suggesting that benthic inputs of dissolved Mn were restricted in this area (33). In the Bay of Seine, the ecological constrains are dramatically different with significant seasonal river inputs and benthic reducing conditions that will enhance dissolved Mn concentrations at the SWI. This comparison suggests that shell Mn variations in the Bay of Seine are also closely linked to dissolved Mn cycling and benthic remobilization at the SWI. Although Mn is an essential micronutrient taken up by the phytoplankton (10, 11), major phytoplankton blooms in the Bay of Seine, as highlighted by chlorophyll a measurements at Luc Buoy station and occurring both in spring and
TABLE 1. Manganese Mean Concentrations and Their Specific Enrichments Archived in Different Bivalve Shells from Different Coastal Ecosystems
bivalves
species
location
investigated period
scallop Pecten maximus Bay of Seine, France 2004
Mn shell enrichment period
max [Mn]/[Ca]/ mean [Mn]/[Ca]
6.5 ( 1.7
summer
1.9
references
Bay of Brest, France
1998–2004
6.9 ( 1.5
none
-
Quiberon, France
2000
18 ( 9
summer
1.8
Belle Ile, France
1999–2001
12 ( 2
summer (2000)
2.4
Ria de Vigo, Spain
2000
7.5 ( 2.9
none
-
1994–1995
50
spring-summer
2.2
this study (n ) 3)a this study (n ) 20)a this study (n ) 3)a this study (n ) 10)a this study (n ) 3)a (29)
1995–1996
100
spring-summer
5
(25)
scallop Pecten maximus Menai Strait, Wales, UK mussel Mytilus edulis Schelde estuary, The Netherlands a
mean Mn/Ca shell concentrations (µmol/mol)
Analyses performed with matrix-matched standards.
summer, are not concomitant with any shell Mn enrichment (Figure 1). Shell Mn enrichment related to phytoplankton bloom was, however, previously proposed for other types of bivalves (e.g., mussel) in various coastal environments (25, 26). Our results confirm the findings from Freitas et al. (29), and suggest that direct biogenic particulate uptake is a negligible source for shell Mn uptake during the enrichment period. From our study, shells from Quiberon or Belle Ile exhibit 2–3 times higher Mn/Ca mean molar ratios than for shells originating from the Bay of Seine (France), the Bay of Brest (France), and the Ria de Vigo (Spain). Both Quiberon and Belle Ile locations are dramatically influenced by the Loire River which induces average Mn inputs to the coastal zone 6 times higher than those related to the Seine River (39). Such a large difference in Mn load from upstream river inputs may account for the geographic variability of shell Mn contents. Further comparison of shell Mn/Ca content with previous investigations, shown in Table 1, exhibit 10 times lower Mn concentrations in P. maximus shells analyzed by our matrixmatched LA-ICP-MS method (35). For similar P. maximus shells, Freitas et al. used an indirect drilling sampling method which collects a larger fraction of the shell and thus may affect the final concentrations (29). For mussel shells investigated by Vander Putten et al., Mn enrichment can be drastically different in relation to the bivalve species, habitat, feeding exposure, growth rate, and shell matrix properties (i.e., calcite versus aragonite) (25). Finally, significant biases induced when using different laser ablation wavelength (UV versus IR) and matrix- or non-matrix-matched standards (i.e., NIST glass CRM), may also explain concentration discrepancies among the different studies (35). Shell Mn Concentration Profiles in Relation To Estuarine and Coastal Mn Cycling. Influence of Upstream Seine River Inputs on Shell Mn Enrichment. Figure 1 presents the variations of shell Mn concentrations according to the Seine River upstream flow rate and particulate flux. Variations of shell Mn concentrations seem to follow the temporal trend of particulate flux from the Seine River. In opposition, river discharge and other environmental variables do not agree with shell Mn profiles. In April, the riverine particulate flux is decreasing from 3.6 to 1.6 kg s-1 similarly to shell Mn concentrations (Table B in the Supporting Information). From May to mid-June, lower particulate flux averaging 2 kg s-1, corresponds with lowest shell Mn concentrations over the entire shell growth period (Figure 1). In addition, the slight increase of shell Mn concentrations observed early in May
FIGURE 2. Mean shell Mn concentrations as a function of the river particulate Mn flux from April to July (full triangle) and the representation of the other points obtained from August to mid October (empty square) in 2004. Shell Mn concentrations were averaged from the three shells analysis (n ) 3 shells) taking into account all the measurements within the week consecutive to the Seine flow rate measurement (n ) 3 LA-ICPMS analysis). The uncertainty on shell Mn concentration was considered as the standard deviation of the three mean shell Mn concentrations. The particulate Mn fluxes from the Seine River were evaluated at Poses using a mean particulate Mn concentration of 416 ( 75 mg kg-1 (1993–2003). The uncertainty on Mn fluxes was determined as the product of the standard deviation on the mean particulate Mn concentration over a 10-year period (1993–2003) by the Mn flux determined at Poses. agrees with a simultaneous increase of the particulate inputs from the Seine River. In July, periods of significant riverine particulate inputs are occurring concomitantly to specific higher Mn shell enrichments, respectively, 4.6 ( 0.8 µg g-1 and 5.8 ( 0.5 µg g-1 on the 08/07 and 20/07 ((3 days) (Figure 1). From August to mid-October, the river discharge and its subsequent particulate flux are not further delineated by shell Mn concentrations during the same period (Figure 1). To confirm the significant trend observed between the temporal variations of upstream particles inputs and shell Mn concentrations, Figure 2 presents the mean shell Mn concentration (n ) 3) according to the estimated Mn particulate flux from the Seine River (database in Table B of the Supporting Information). From April to July, a significant linear relationship (r2 ) 0.95, n ) 8, p < 0.05) is obtained and supports that particulate flux from the Seine River is the dominant source VOL. 42, NO. 1, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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for the variations of shell Mn concentrations. This evaluation of the riverine particulate fluxes is, however, not sufficient to accurately underscore shell Mn concentrations all along the growth period. Shell Mn enrichments occurring especially in summer and early fall (i.e., August to October) can not be directly explained by increases of particulate river inputs (Figures 1 and 2). Figure 2 clearly exhibits an additional enrichment of Mn in the shell for all the period taking place in late summer (i.e., 2-3 times higher) relative to the linear trend observed with the riverine particulate flux. Significant river discharges were previously recognized to bring large inputs of particulate Mn into the Seine Bay and estuary (3). Particulate Mn concentrations are mostly derived from the erosion of the drainage basin and exhibit homogeneous concentration in the suspended particulate matter from the Seine River (416 ( 75 mg kg-1, 1993–2003). The further transport of Mn from the Seine estuary to the coastal zone is mainly controlled by the dynamics of the HTZ (2, 3, 22). Chiffoleau et al. estimated that Mn inputs into the Seine estuary in spring were dominated at 90% by particulate transport (214–444 kg/day), which in turn was directly converted into dissolved Mn output to the coastal zone of similar amplitude (100–300 kg/day) (2). During higher river discharge, the residence time of water and particles in the estuary remains low (i.e., few days), suggesting a direct contribution of particulate Mn input to coastal waters as delineated in Figure 2. In these conditions, the lag between Mn transport to the estuary and subsequent shell uptake at the SWI is assumed to be less than a week. During estuarine mixing, the particulate Mn flux from the Seine River and the subsequent Mn release with increasing salinity (22) mainly govern dissolved Mn abundance in the bay from April to July (3), and its further uptake in the Pecten maximus shell. At low river discharge, water and particle turnover is longer and directly related to the tidal range within the Seine estuary (40), affecting the fate of dissolved Mn in the HTZ (2, 3). In the Seine estuary, Mn is reported to have a nonconservative behavior during the low discharge period in summer that revealed supplementary inputs of Mn in the Seine estuary and bay (2, 3). In summer, shell Mn enrichments are not only related to upstream inputs from the Seine River, but also to downstream release of dissolved Mn under seasonal reducing conditions. Influence of Seasonal Eutrophication and Reductive Processes in the Seine Estuary and Bay on Shell Mn Enrichment. The variations of shell Mn concentrations were examined according to the estuarine water temperature and oxygen saturation within the estuarine HTZ (Honfleur station) and to bay water temperature, salinity, oxygen saturation, chlorophyll a concentration, turbidity, and ammonium concentration (Luc Buoy station) (Figures 1, 2, and 3, and Table B in the Supporting Information). From this data set, both major pelagic and benthic processes were examined in relation to the estuarine HTZ and coastal dynamics, established to affect dissolved Mn fate in the Seine Bay under low discharge regime (2, 3, 22). During summer, eutrophication of the Seine River promotes estuarine heterotrophic activity and the formation of hypoxic to anoxic conditions in the HTZ (2, 24, 41). Usually, the most reducing conditions are obtained under the spring tide regime increasing the suspended matter load in the HTZ. As a result, severe depletions in oxygen occur in estuarine surface waters in late summer (100). Such conditions were found to increase dissolved Mn concentrations compared to neap tide regime in the Seine estuary (22). In the Bay of Seine, large summer blooms are usually dominated by dinoflagellates (42). The subsequent organic matter mineralization in the bay requires a significant fraction 90
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FIGURE 3. Variations of Mn shell concentrations (µg g-1) obtained for 3 Pecten maximus shells from the Seine bay according to salinity (PSU), temperature (°C) measured in bottom seawater; ammonium concentrations (µmo L-1), and turbidity (NTU) measured in surface seawater at Luc buoy (Seine bay), from April to mid-October 2004. The dashed lines indicated maxima of Mn shell concentrations. The grey zones represent the maxima of shell Mn concentrations which are not mainly influenced by the particulate upstream Mn inputs from the Seine River. of dissolved oxygen from the water column that may drastically promote the development of reductive conditions at the SWI (24, 38). In comparable shallow waters from the Wadden sea as influenced by the Elbe estuary, most of the dissolved Mn contribution under summer conditions originated from benthic reductive conditions (17). Several measurements performed in coastal waters of the English channel highlighted also the contribution of benthic inputs during summer time with increasing dissolved Mn concentrations (20, 21). A similar dynamic is occurring in the Bay of Seine, in which a significant summer bloom at the end of July (Chl a max: 5.06 µg L-1, 26/07) is subsequently followed by a minimum of oxygen saturation (78.6%, 09/08) (Figure 1; Table B in the Supporting Information). This marked oxygen depletion in coastal waters is also simultaneous with a severe spring-tide-induced oxygen undersaturation in the estuarine HTZ (64.6%, 09/08, Figure 1). Both processes stimulated by higher ambient temperature are suggested to provide significant inputs and stable conditions for further dissolved Mn shell uptake. Shell Mn concentrations exhibit the highest concentration of the entire growth period on the 09/08 ((3 days) reaching 6.1 ( 1.0 µg g-1 (n ) 3). The estuarine contribution to the Bay of Seine is also tracked by a minimum of salinity and a maximum of temperature (32.6 PSU, 02/08; 19.5 °C, 09/08, Figure 3) corresponding to intense spring tidal cycle. In addition, Figure 3 exhibits a 10 times increase
of ammonium (NH4+) concentrations in surface seawater, from 0.33 µm (26/07) to 3.66 µm (16/08). Increases of ammonium concentrations in the water column of similar environments are generally induced by anaerobic mineralization of the organic matter and often correlated to dissolved Mn concentrations (24). This result confirms thus the contribution of both estuarine and benthic release of reduced species, such as Mn2+, to the bay water column beginning of August. In September, another spring tide regime induces a drastic minimum oxygen saturation in the estuary HTZ (61.2%, 06/09, Figure 1). Potential exchanges between estuarine water and bay waters are also exhibited by minimum of salinity and maximum of temperature in the bay (33.2 PSU; 19.6 °C, 06/09, Figure 3). Simultaneously, chlorophyll a surface concentrations in the bay depict a large summer bloom reaching a maximum value of 7.82 µg L-1 on the 06/09 (Figure 1). In this case, the intense primary productivity induces an oxygen supersaturation in bottom waters of the bay (137%, 06/09, Figure 1). Although estuarine inputs of dissolved Mn can be considered, redox conditions in the bay water resulting from a large oxygen production are not favorable to the benthic release of Mn at the SWI and the stability of Mn2+ in the water column (3, 22). As a result, shell Mn concentrations observed during early September are reaching the lowest content for the entire summer period at about 3.4 ( 1.0 µg g-1 on the 14/09. This result also confirms that pelagic biogenic particles provided by a large bloom are not resulting in direct shell Mn enrichment for the scallop Pecten maximus. Mn release from the HTZ may also occur in September due to an oxygen depletion (81.8%, 27/09) in relation to a spring tidal regime. Any decrease of salinity is however observed in the bay during this period (Figure 3), indicating no significant exchange of estuarine waters to the bay. Although no oxygen depletion is detected in the water column of the bay, a significant increase of ammonium concentrations is measured in surface seawater from 0.41 to 5.77 µmol L-1 (06/09 – 05/10) (Figure 3). It is thus expected that a significant release of dissolved reduced components, such as Mn2+, occurs at the end of September and accounts for the maximum of shell Mn concentration on the 26/09. In similar coastal environments, the ongoing oxidation of organic matter settling on the sediments, subsequently to major blooms, was demonstrated to sustain reducing conditions at the SWI in summer and to promote Mn remobilization as a major source to the water column (1).
Acknowledgments We acknowledge Antoine Huguet (IFREMER, Dpt Dynamique de l’Environnement Côtier, Nantes, France) and the Laboratoire Environnement et Ressources de Normandie (IFREMER, Port-en-Bessin, France) for providing monitoring data from the QUADRIGE database. This work is a contribution to the ACI PECTEN research program (French Ministère de la Recherche). Thermo Fisher Company is thanked for the loan of the ICP-MS. A.B. acknowledges the Aquitaine Region (ORQUE project) for her Doctoral fellowship.
(2)
(3)
(4)
(5)
(6)
(7)
(8)
(9) (10)
(11)
(12)
(13)
(14)
(15)
(16)
(17)
(18)
(19)
Supporting Information Available Environmental data, Table A (annual variations of Mn shell concentrations), Table B (hydrological, biological, and chemical data in the Seine River, Seine estuary, and Bay of Seine), Figure A (map of the investigated area), and Figure B (variations of average Mn shell concentrations). This material is available free of charge via the Internet at http:// pubs.acs.org.
Literature Cited (1) Dehairs, F.; Baeyens, W.; van Gansbeke, D. Tigh coupling of iron and manganese in North Sea suspended matter and
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