ICES Journal of Marine Science, 54: 905–916. 1997
Seasonal changes of nutrients in water and sediment in a
Mediterranean lagoon with shellfish farming activity (Thau
Lagoon, France)
M.-L. De Casabianca, T. Laugier, and
E. Marinho-Soriano
De Casabianca, M.-L., Laugier, T., and Marinho-Soriano, E. 1997. Seasonal changes
of nutrients in water and sediment in a Mediterranean lagoon with shellfish farming
activity (Thau Lagoon, France). – ICES Journal of Marine Science, 54: 905–916.
The French Mediterranean lagoon of Thau is characterized by an important eutrophication dominated by shellfish farming (ca. 15 times the terrestrial inputs). On the basis
of increasing eutrophication, three areas were identified and monitored for one year
(overlying and sediment pore water nutrients, macrophytic biomass and water column
chlorophyll a). Though some parameters show similar changes in the three areas
(salinity, temperature), others are elevated in eutrophicated sites, e.g. organic content
and siltation of the sediments, dissolved inorganic nitrogen (136.1 ìmol l "1 overlying
water, and 1185 ìmol l "1 pore water), dissolved reactive phosphorus (DRP)
(20.9 ìmol l "1 overlying water), the summer oxygen depletion (1.1 mg l "1), the peak
of macrophytic biomass (8 kg w · wt m "2) and phytoplanktonic bloom (14 ìg l "1).
Differences in DRP levels arise from sediment release during the summer anoxia; DRP
appeared to play a key role as a limiting factor, and regulates competition between
macrophytes and phytoplankton in spring. The macrophytes (seagrass Zostera and
seaweeds Gracilaria and Ulva) may sustain the environment they are living in, acting as
additional eutrophication sources.
? 1997 International Council for the Exploration of the Sea
Key words: lagoon, shellfish, farming, eutrophication, nutrients, sediments, macrophytes.
Received 2 May 1996; accepted 7 October 1996.
M.-L. De Casabianca, T. Laugier, and E. Marinho-Soriano: Centre National de la
Recherche Scientifique, Laboratory ‘‘Eutrophisation et Macrophytes’’, Station Méditerranéenne de l’Environnement Littoral, 1 Quai de la Daurade, 34200, Sète, France.
Correspondence to M.-L. De Casabianca: tel: +330467463380; fax: +330467460256;
email: [email protected]
Introduction
Currently, Mediterranean coastal lagoons are not spared
the eutrophication processes which generally result from
increasing anthropogenic pressures such as urban, agricultural and industrial sewages. This situation is usually
characterized by an increased level of nutrients (NH4,
NO3, PO4) and suspended particulate matter in the
water column, by nitrogen and phosphorus enrichment
of sediments, by dissolved oxygen depletion which
can lead to anoxic crisis in summer, and the frequent
occurrence of macroalgal blooms (Zaouali, 1977; De
Casabianca, 1983; Comin, 1984; Sfriso et al., 1988;
Viaroli et al., 1993; Lundin and Linden, 1993; De
Casabianca et al., 1994). If water inputs and their high
nutrient loads are generally used to explain eutrophi1054–3139/97/050905+12 $25.00/0/jm960201
cation in coastal lagoons, primary productivity, sediments and occasionally secondary productivity, also play
a key role in nutrient recycling, and thus play a great
part in sustaining eutrophic conditions. Indeed, several
authors have shown that the macroalgal biomass, which
is very important in eutrophic ecosystems, acts as a
major sink or source of nutrients during its growth or
decay stages (Sfriso et al., 1989; De Casabianca, 1989;
Pugnetti et al., 1992). These degradation processes generally enhance the development of anoxic events, and
thus the release of nutrients from sediments (Callame,
1961; Berner, 1977; De Casabianca, 1979; Rosenfeld,
1979). On the other hand, secondary productivity can
also be a major source of eutrophication in the case of
intensive aquaculture (Kaspar et al., 1988; Chua et al.,
1989; Carr and Goulder, 1990; Lombardo et al., 1993).
? 1997 International Council for the Exploration of the Sea
906
M.-L. De Casabianca et al.
Balaruc-les-bains
´
Meze
Site 3
Site 2
8m
Thau lagoon
Marseillan
5m
´
Sete
Site 1
Channel
MEDITERRANEAN SEA
2°
Shellfish farming areas
4°
6°E
49°N
Urban areas
Industrial areas
47°
Sampling sites
45°
2 km
Figure 1. The Thau Lagoon. Location of the three sampling sites.
Thau Lagoon (Fig. 1), located on the French
Mediterranean coast, is a large (75 km2) and rather deep
lagoon (average depth 4.5 m) with a strong marine
influence (salinity ranging from 35.9 to 40.5) and a
wind-induced hydrodynamic pattern (Tournier et al.,
1983; Millet, 1989). In this lagoon, oyster and mussel
farming is intensively developed and fills about 20% of
the whole lagoon area and yearly produces about 35 000
tonnes of shellfish (Hamon and Tournier, 1981). This
shellfish biomass produces a biodeposition accounting
for 500 kg ha "1 yr "1 of nitrogen and 3000 kg ha "1
yr "1 of carbon (De Casabianca, 1977). Inputs of nitrogen (30 kg N ha "1 yr "1) and phosphorus (10 kg N
ha "1 yr "1) mostly come from urban sewage but also
from agricultural activity (Agence De l’Eau, 1981).
Shellfish farming (tables and farms where oysters and
mussels are depurated with lagoon waters) is mostly
located in the northern part of the lagoon and appears
to be the main factor in the spatial variation of the water
and sediment characteristics (Casellas et al., 1990; Pena
and Picot, 1991; De Casabianca et al., 1994).
In this paper, the results of one year’s sampling of
physical and chemical parameters, nutrient concen-
trations in water and sediment pore water and phytoplanktonic and macrophytic biomass at three sites under
different eutrophication influences are reported.
Materials and methods
From January 1994 to January 1995, sampling was
carried out fortnightly at three sites (average depth
1.5 m) marked with buoys anchored to bottom (Fig. 1):
- Site 1 is located in the southern part of the lagoon
which is free from shellfish aquaculture and where a
mixed seagrass bed (Zostera noltii Horn. and Zostera
marina L.) prevails.
- Site 2 is located in an area without oyster tables and
under urban influence (Mèze); the benthic vegetation
is mainly characterized by the green macroalgae Ulva
rigida C. Agardh.
- Site 3 is situated in a shellfish farming zone and
characterized by the seaweed Gracilaria bursa-pastoris
(Gmelin) Silva.
Temperature (to 0.1)C), salinity (to 0.1) and dissolved
oxygen (to 0.01 mg l "1) were measured in situ in both
Seasonal nutrient changes in a lagoon
907
Table 1. Grain size (% g dry weight) and organic matter content of the surface sediment
(0–5 cm) at the three studied areas in Thau Lagoon (mean&standard deviation, n=3).
Grain size
Site 1
Site 2
Site 3
Shell (%)
(<1·5 mm)
Sand (%)
(400 ìm–1.5 mm)
Silt (%)
(<400 ìm)
Organic matter
content
(% g d.wt)
0.6&0.3
0.2&0.2
0
87.6&3.5
91.8&4.3
23.8&2.8
11.7&1.8
8.0&1.1
76.2&2.3
1.33&0.17
1.66&1.27
4.96&2.46
surface and bottom water with a multi-parametric lead
(Horriba). Water transparency was evaluated by measuring the irradiance (in lux) above the water surface (Io)
and at the bottom (Ip) with a light meter and the light
extinction coefficient (LEC) was computed according to
the formula: LEC=Ln (Ip/Io)/p where p is the depth in
metres.
Water samples were also taken at both surface and
bottom with a Kemmerer bottle. At the laboratory,
water was immediately filtered through a GF/C
Whatmann glass filter for nutrient and chlorophyll a
(Chl a) analyses. Chlorophyll a was determined in three
aliquots of 100 ml water samples. The filters were pulverized in acetone and stored at 5)C for 12 h. After
centrifugation, the overlying solutions were analysed by
fluorimeter (Turner 112). Results are presented as a
mean between surface and bottom waters. Dissolved
reactive phosphorus (DRP:P-PO4) and total inorganic
dissolved nitrogen (TIN calculated as a sum of
N-NO2 +N-NO3 +N-NH4) were assayed in triplicate
within 24 h by colorimetric methods (Strickland and
Parsons, 1972) using a microplate reader (Galgani and
Bocquene, 1989). N:P atomic ratios were calculated
from the monthly mean in TIN and DRP.
Surface sediments (0–5 cm) were sampled by free
diving with a corer and stored in a cold box. At the
laboratory, they were immediately centrifuged (5000 r
min "1, 10 min, 0)C); the extracted pore water was
filtered through a GF/C Whatmann glass filter and
assayed for DRP and TIN (same methods as for water
samples) within 24 h. The remained sediments were
freeze-dried and then burned at 500)C for 6 h in order to
determine the percentage of organic matter, as dry
weight.
Three times a year, granulometry was determined at
the three sampling sites. Aliquots of wet surface sediments were passed through two sieves of 1.5 mm and
400 ìm mesh in order to determine the percentage (dry
weight) of shell fragments, sand and silt, after drying.
Benthic macrophytes were sampled monthly with a
metallic frame (0.25 m2) according to the permanentquadrat method (Nienhuis, 1978). Macrophyte fresh
biomass was determined from three repeated samplings.
Results
Sediment characteristics
The granulometric determinations (Table 1) showed that
the surface sediments of sites 1 and 2 were mostly sandy
(87.6% and 91.8% of sand respectively). In contrast, the
surface sediments at site 3 were mainly comprised of silt
(76.2%) and shell fragments (23.8%). The percentage of
organic matter in surface sediments showed a similar
trend with higher values in silty sediments (site 3) than
sandy ones (sites 2 and 3).
Biotic factors
Every month, macrophyte biomass was always highest
at site 3 (Gracilaria) although it declined greatly in
spring, from 7.04 to 0.97 kg w · wt m "2, and remained
minimal throughout summer (Fig. 2). At site 2, the
macrophytic biomass, mostly Ulva rigida, decreased
gently during summer from 1.84–0.34 kg w · wt m "2
becoming zero in October. At site 1, macrophytic biomass (Zostera noltii and Z. marina) remained almost
stable showing two annual peaks in August and October
(1.36 and 1.38 kg w · wt m "2 respectively).
Phytoplanktonic biomass (Fig. 2), expressed as
chlorophyll a concentration in water column, was low
from mid-autumn to end of spring (0.001–0.790 ìg l "1)
in the whole lagoon. It rose strongly in June (site 3)
or July (sites 1 and 2) to reach a maximum in
August–September with 3–4 times higher concentrations
at site 3 (14.044 ìg l "1) than at sites 1 and 2 (9.658 and
9.951 ìg l "1 respectively).
Water characteristics
The differences between surface and bottom waters were
generally not significant; thus, only results from the
bottom water will be presented in detail.
The water temperature, the salinity and the dissolved
oxygen showed almost the same seasonal evolution at
the three stations (Fig. 3). The water temperature
increased from January (minimum 3.2)C) until August
908
M.-L. De Casabianca et al.
16
[Chlorophyll a] in water (µg l–1)
14
12
10
8
6
4
2
1
F
M
A
M
J
J
A
S
O
F
M
A
M
J
J
A
S
O
N
D
J
F
N
D
J
F
Macrophyte biomass (kg w.wt m–2)
9
8
7
6
5
4
3
2
1
0
"1
Figure 2. Seasonal changes (1994–1995) in chlorophyll a concentration in water (ìg l ) and macrophytic biomass (kg w · wt
m "2) at the three studied areas in Thau Lagoon (—— site 1, – – – site 2, · · · site 3). Vertical bars represent standard deviations.
(maximum 26.5)C) when salinity was also maximum
(43). The seasonal minimum of salinity (30.7) occurred
in November during the annual rainfall maximum; this
drop in salinity was less marked at sites 2 and 3 which
are in closest connection with the sea. The dissolved
oxygen concentration decreased from the end of the
winter (maximum 14 mg l "1) leading to anoxic conditions in July (Fig. 3). This depletion was more drastic at
site 3 (minimum 1.1 mg l "1). A second oxygen depletion
occurred in the two eutrophic areas during the October
rains. It must be pointed out that dissolved oxygen
concentration was elevated at sites 2 and 3 (February
and January respectively) when maximum growth of
macrophytes occurred.
The light extinction coefficient (Fig. 3) was quite
stable at site 1 and more variable and higher at sites 2
and 3. The seasonal peaks occurred in spring at site 2
(1.45 m "1) and in summer at site 3 (1.75 m "1) when
chlorophyll a was highest.
Nutrients
Total dissolved inorganic nitrogen (TIN) showed almost
similar fluxes and levels in all areas and mostly comprised ammonium (Fig. 4). While the seasonal maximum
occurred in July (136.1 ìmol l "1) at all sites, eutrophic
areas (sites 2 and 3) had already shown increasing and
higher levels since the early spring. Moreover, there was
a short rise in TIN during the rains at these two sites.
Meanwhile, TIN in the sediment pore water (Fig. 5) was
approximately ten-fold higher than in the overlying
water and followed a similar annual trend, but with a
Water temperature (°C)
30
25
20
15
10
5
0
F
M
A
M
J
J
A
S
O
N
D
J
F
F
M
A
M
J
J
A
S
O
N
D
J
F
F
M
A
M
J
J
A
S
O
N
D
J
F
F
M
A
M
J
J
A
S
O
N
D
J
F
45.0
42.5
Salinity
40.0
37.5
35.0
32.5
30.0
27.5
25.0
16
Dissolved oxygen (mg l–1)
14
12
10
8
6
4
2
0
Light extinction coef. (m–1)
2.5
2.0
1.5
1.0
0.5
0.0
Figure 3. Seasonal changes (1994–1995) in temperature ()C), salinity, dissolved oxygen (mg l
(m "1) at the three sampling sites in Thau Lagoon (—— site 1, – – – site 2, · · · site 3).
"1
) and light extinction coefficient
910
M.-L. De Casabianca et al.
120
[NH +3] in µmol l–1
100
80
60
40
20
0
F
M
A
M
J
J
A
S
O
N
D
J
F
F
M
A
M
J
J
A
S
O
N
D
J
F
F
M
A
M
J
J
A
S
O
N
D
J
F
140
120
[TIN] in µmol l–1
100
80
60
40
20
0
25
[DRP] in µmol l–1
20
15
10
5
0
"1
"1
Figure 4. Seasonal changes (1994–1995) in ammonia (ìmol l ), TIN (ìmol l ) and DRP (ìmol l
bottom waters at the three sampling sites in Thau Lagoon (—— site 1, – – – site 2, · · · site 3).
"1
) concentrations of the
Seasonal nutrient changes in a lagoon
911
900
600
450
+
[NH 3] in µmol l
–1
750
300
150
0
F
M
A
M
J
J
A
S
O
N
D
J
F
F
M
A
M
J
J
A
S
O
N
D
J
F
F
M
A
M
J
J
A
S
O
N
D
J
F
1200
[TIN] in µmol l
–1
1000
800
600
400
200
0
120
[DRP] in µmol l
–1
100
80
60
40
20
0
"1
"1
Figure 5. Seasonal changes (1994–1995) in ammonia (ìmol l ), TIN (ìmol l ) and DRP (ìmol l
pore water at the three sampling sites in Thau Lagoon (—— site 1, – – – site 2, · · · site 3).
"1
) concentrations in sediment
912
M.-L. De Casabianca et al.
10 000
N:P atomic ratio
in overlaying water
1000
100
10
1
F
M
A
M
J
J
A
S
O
N
D
J
F
F
M
A
M
J
J
A
S
O
N
D
J
F
N:P atomic ratio
in sediment pore water
10 000
1000
100
10
1
Figure 6. Annual changes (1994–1995) in monthly mean of N:P atomic ratio (logarithmic scale) in overlying and sediment pore
waters at the three sampling sites in Thau Lagoon (—— site 1, – – – site 2, · · · site 3).
much greater variability. At sites 2 and 3, the annual
maximum which occurred in July (1185 and 993 ìmol
l "1 respectively) was mostly due to nitrate and nitrite
and followed the decaying stage of the macrophytic
biomass.
Dissolved reactive phosphorus (DRP, Fig. 4) rose
from mid-spring with increasing temperature at sites 2
and 3 to reach a maximum in June–July (18.1 and
20.9 ìmol l "1 respectively). Moreover, DRP at site 2
which was under urban influence, showed several annual
peaks. In the oligotrophic area (site 1), increased DRP
occurred later, in July–September, with a weaker amplitude (maximum 5 ìmol l "1). In all areas, DRP was
lowest in winter and ranged from 0.1 to 5 ìmol l "1. In
sediment pore water (Fig. 5), DRP followed the reverse
trend from the overlying water as it greatly decreased
while water temperature increased (March). Minimum
levels occurred from the end of the spring to the end of
the summer and varied from 0.5 to 33.6 ìmol l "1. The
highest concentrations were observed at site 2 (urban
influence) and at site 1 (maximum 107 ìmol l "1) where
rooted macrophytes (Zostera) prevailed.
From these nutrient levels, a regular decrease of
the N:P atomic ratio followed from February until
September (Fig. 6) with higher ranges at sites 2 and 3
(1010–5) than at site 1 (60–20). However, in sediment
pore water, the N:P atomic ratio was lower and did not
often exceed 40. Between the three areas studied, the
N:P ratio in pore water was always higher in the two
eutrophic areas. In either overlying water or in sediment
Seasonal nutrient changes in a lagoon
913
Table 2. Salinity TIN (ìmol l "1) and DRP (ìmol l "1) concentrations in some Mediterranean coastal lagoons. Annual means and
ranges (in parentheses).
Lagoons
Lac Mellah
(Algeria)
Urbino
(Corsica, Fr.)
Biguglia
(Corsica, Fr.)
Prévost
(Hérault, Fr.)
Venice
(Italy)
Sacca di Goro
(Italy)
Thau
(Hérault, Fr.)
Rhône Delta
(Bouches-du-Rhône, Fr.)
Salinity
TIN
(ìmol l "1)
DRP
(ìmol l "1)
27
(24–32)
28.5
(26.5–30)
12.6
(3.5–23.5)
25
(16–36)
28
(25–31)
—
—
36
(32.5–43.2)
—
—
—
(3.1–5.2)
10.46
(0–20)
11.02
(0–36)
12.62
(0.99–16.98)
21
(2–41.5)
20.2
(7.1–37.1)
55.14
(20.7–136.1)
—
(50–120)
—
(1–5)
0.62
(0–1.45)
0.82
(0–4.13)
5.86
(2.1–13.2)
1.2
(0.3–2.9)
15
(3.2–21.4)
13.87
(0.1–20.9)
—
(3–8)
pore water, the N:P ratio was strongly correlated to
DRP (r=0.82).
Discussion
The waters of Thau Lagoon are characterized by a
rather high level of dissolved inorganic nitrogen and
phosphorus. Indeed, if these results are compared with
those of other Mediterranean lagoons, classified by
increasing eutrophication (Table 2), it appears that TIN
and DRP levels encountered in Thau Lagoon are some
of the highest. They are twice those observed in the
lagoon of Venice (Sfriso et al., 1988) and in the Po River
Delta lagoon (Pugnetti et al., 1992), and they are close to
those noted in the Rhône Delta waters (Coste, 1985). On
the other hand, if one examines the annual nitrogen and
phosphorus inputs (Fig. 7), they are about ten times
lower than those of the lagoons of Prévost (Agence de
l’Eau, 1981) and Venice (Andreottola et al., 1990) in
which nutrient levels are lower. Inputs that are usually
postulated to explain eutrophication do not therefore
suffice in the present case.
In the Thau Lagoon, shellfish farming seems to be the
major source of eutrophication as shown by the comparative survey of the three areas. The shellfish biomass
in culture releases to the environment, in terms of
nitrogen, are about 500 kg ha "1 yr "1 as biodeposition
(De Casabianca, 1977) and 5 kg ha "1 yr "1 as ammoniotellic excretion (Outin, 1990), i.e. about fifteen times
the inputs. To this must be added the water pumped
from the lagoon and used to depurate shellfish, but there
are no available data about the additional loads of
nitrogen and phosphorus this could represent.
References
De Casabianca et al., 1990
De Casabianca, 1982
De Casabianca, 1982
De Casabianca, 1983
Sfriso et al., 1989
Varioli et al., 1993
Present study
Coste, 1985
Moreover, in shellfish farming areas, sediments are
silty and rich in organic matter. Though these differences
do not seem to interfere markedly in TIN and DRP
concentrations in sediment pore water they clearly affect
the release processes which occurred earlier and with
greater amplitude in eutrophic sites (2 and 3) with
increased temperatures. Indeed, nutrient fluxes from
sediments to overlying water show much higher rates
below shellfish tables than elsewhere (Baudinet et al.,
1990).
With regard to nitrogen, exchangeable nitrogen, especially ammonia, is predominantly associated with
organic matter (Berner, 1977; Rosenfeld, 1979) and thus
sediment-water fluxes may be greater in eutrophic areas.
On the other hand, Grenz et al. (1992) estimated that
nitrogen coming from sediments does not represent
more than 30% of that excreted by shellfish. The increase
in TIN in spring and summer in the whole Thau Lagoon
thus mostly results from the increasing metabolism of
shellfish with increasing temperature (Outin, 1990).
Phosphorus originates mainly from sediments as was
shown by the opposite fluctuations of DRP in pore
water and overlying water. This phenomenon is heightened during the warm season (April–September) in
eutrophic sites. During autumn and winter (October–
February), DRP in pore water shows higher levels and
fluctuations in sandy sediments (sites 1 and 2). Though
the role of particle grain size and the nature of the
sediment is obvious, the presence of rhizophytes (site 1)
and the vicinity of urban sewage (site 2) must also be
taken into account.
On the other hand, the different origins of eutrophication determine the nature of macrophyte communities
as observed in the three sites: annual nitrophilous
914
M.-L. De Casabianca et al.
Nitrogen annual loads (kg ha–1 year–1)
300
250
200
150
100
50
0
Thau
Venice
Prévost
Thau
Venice
Prévost
Phosphorus annual loads (kg ha–1 year–1)
50
45
40
35
30
25
20
15
10
5
0
Figure 7. Nitrogen and phosphorus annual loads in Thau, Prévost (Agence de l’Eau, 1981) and Venice Lagoons (Andreottola
et al., 1990). . Rains, agricultural, / industrial, domestic.
seaweeds in eutrophic areas (Gracilaria and Ulva) and
perennial seagrass (Zostera) in the oligotrophic site (De
Casabianca et al., 1994). In addition to the ecological
interest, macrophyte populations which grow in
eutrophic areas show higher biomass peaks and variations; this means a larger amount of nutrients recycled,
and obviously released in water and surface sediment
where they will decompose (De Casabianca, 1989; Sfriso
et al., 1989). Thus, the macrophytes might sustain the
eutrophic conditions they are living in.
Moreover, this sudden availability of nutrients
released in water by the macrophyte degradation precedes and triggers phytoplanktonic blooms as described
in other coastal lagoons (Pugnetti et al., 1992; Viaroli
et al., 1993; Sfriso and Pavoni, 1994). In Thau Lagoon,
this succession macro–microphytes can be explained by
the limiting role of phosphorus. Indeed, the optimum
N:P ratio for macrophytes is about 30:1 (Atkinson and
Smith, 1983) vs. 16:1 for phytoplankton (Redfield,
1958); thus phytoplanktonic blooms can only occur in
summer when the N:P ratio of water is lower than 20:1.
The eutrophication in the Thau Lagoon, which is one
of the most eutrophic Mediterranean coastal lagoons,
thus arises from inner sources which are mainly shellfish
farming (nitrogen) and indirectly from sediments (phosphorus). Phosphorus therefore plays a key role (by
Seasonal nutrient changes in a lagoon
excess of nitrogen) as a limiting factor and regulates the
competition between macrophytes and phytoplankton.
Climatic factors, especially temperature, which determine phosphorus availability, could be responsible for
the inter-annual fluctuations in water eutrophication.
The macrophytes play, in Thau Lagoon, a secondary
role in eutrophication processes; they may sustain the
environment they are living in, for instance, as a stabilizing role for seagrasses (Zostera) or as additional
eutrophication sources (Ulva and Gracilaria algae). The
higher the nutrient recycling by shellfishes, sediments
and macrophytes the higher are the nutrient levels. It is
now necessary to quantify this recycling in order to
control eutrophication in coastal lagoons.
Acknowledgement
This work was carried out in the framework of an EEC
program ‘‘EUMAC’’ (EV5V-CT93-0290).
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Atkinson, M. J. and Smith, S. V. 1983. C:N:P ratios of benthic
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Baudinet, D., Alliot, E., Berland, B., Grenz, C., Plante-Cuny,
M. R., Plante, R., and Salen-Picard, C. 1990. Influence of
mussel culture on biogeochemical fluxes at the sedimentwater interface. Hydrobiologia, 207: 187–196.
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