The evolution of eutrophication parameters (i.e., nutrients and phytoplankton
biomass) during recent decades was examined in coastal waters of the Vilaine
Bay (VB, France) in relation to changes in the Loire and Vilaine rivers.
Dynamic linear models were used to study long-term trends and seasonality of
dissolved inorganic nutrient and chlorophyll a concentrations (Chl a) in
rivers and coastal waters. For the period 1997–2013, the reduction in
dissolved riverine inorganic phosphorus (DIP) concentrations led to the
decrease in their Chl a levels. However, while dissolved inorganic nitrogen (DIN) concentrations decreased only slightly in the Vilaine, they increased
in the Loire, specifically in summer. Simultaneously, phytoplankton in the VB
underwent profound changes with increase in biomass and change in the timing
of the annual peak from spring to summer. The increase in phytoplankton
biomass in the VB, manifested particularly by increased summer diatom
abundances, was due to enhanced summer DIN loads from the Loire, sustained by
internal regeneration of DIP and dissolved silicate (DSi) from sediments. The
long-term trajectories of this case study evidence that significant reduction
of P inputs without simultaneous N abatement was not yet sufficient to
control eutrophication all along the Loire–Vilaine–VB continuum. Upstream
rivers reveal indices of recoveries following the significant diminution of
P, while eutrophication continues to increase downstream, especially when N
is the limiting factor. More N input reduction, paying particular attention
to diffuse N sources, is required to control eutrophication in receiving VB
coastal waters. Internal benthic DIP and DSi recycling appears to have
contributed to the worsening of summer VB water quality, augmenting the
effects of anthropogenic DIN inputs. For this coastal ecosystem, nutrient
management strategies should consider the role played by internal nutrient
loads to tackle eutrophication processes.
Introduction
Anthropogenic eutrophication is widely regarded as one of the major problems
affecting both inland and coastal aquatic ecosystems (Downing, 2014). The
increase in phytoplankton biomass is the most common symptom of
eutrophication among the myriad responses of aquatic ecosystems to
anthropogenic inputs of nitrogen (N) and phosphorus (P) (Cloern, 2001;
Glibert et al., 2011). Since the beginning of the 1990s, measures to reduce
nutrient inputs in European rivers have been more effective for P, originating
largely from point sources, than for N, coming mainly from diffuse sources
(Grizzetti et al., 2012). However, this strong imbalance between N and P
input reduction still led to substantial decrease in phytoplankton biomass in
many European rivers (Istvánovics and Honti, 2012; Romero et al., 2013).
This result is consistent with the idea that P universally limits primary
productivity in many freshwater ecosystems (Correll, 1999). Thus, reducing P
inputs, and not N, can mitigate eutrophication of freshwater ecosystems
(Schindler et al., 2008, 2016).
Despite significant P input reduction, eutrophication persists in some rivers
(Bowes et al., 2012; Jarvie et al., 2013), and particularly in downstream
coastal ecosystems, where the primary productivity is often limited by N
(Ryther and Dunstan, 1971; Paerl, 2018). As freshwater systems drain into
coastal waters (Vannote et al., 1980; Bouwman et al., 2013), the efficient P
reduction without simultaneous N abatement may result in more N being
transported downstream, where it can exacerbate eutrophication problems in
coastal ecosystems, delaying recovery (Paerl et al., 2004), for example, the
Neuse River Estuary (Paerl et al., 2004), Belgian coastal waters (Lancelot
et al., 2007) and the Seine Bay (Romero et al., 2013). Despite more than
20 years of nutrient reduction implementation in European freshwater
ecosystems, including rivers (e.g., Nitrates Directive, 91/676/EEC, 1991;
Urban Waste Water Treatment Directive, 91/271/EEC, 1991), little measurable
progress has been observed in many European coastal waters (EEA, 2017; OSPAR,
2017).
The Loire River and the Vilaine River are among these major European
rivers whose phytoplankton biomass and P concentrations have decreased since
the early 1990s but with minor, if any, simultaneous diminution in N
concentrations (Romero et al., 2013; Minaudo et al., 2015). Affected by the
Loire and Vilaine river runoff (Guillaud et al., 2008; Gohin, 2012;
Ménesguen et al., 2018b), the Vilaine Bay (VB) is one of the European
Atlantic coastal ecosystems most sensitive to eutrophication (Chapelle et
al., 1994; Ménesguen et al., 2019). The VB coastal waters are classified
as a problem area due to elevated phytoplankton biomass, according to the
criteria established within OSPAR (OSPAR, 2017) and the European Water
Framework Directive (Ménesguen et al., 2018b). However, there is little
information on how eutrophication parameters have evolved in the VB over the
past 20 years in the light of eutrophication mitigation in the Loire and
Vilaine rivers. An approach taking into account seasonal variations is
required, as phytoplankton in many coastal ecosystems, such as the coastal
waters off the Loire and Vilaine rivers, is often limited by P in spring and
by N in summer (Lunven et al., 2005; Loyer et al., 2006).
In temperate coastal waters, diatoms and dinoflagellates constitute the two
dominant phytoplankton classes (Sournia et al., 1991). In terms of nutrient
requirements, the balance between these classes is controlled by silica (Si)
availability. Increased inputs in N and P (and not Si) in aquatic ecosystems
can lead to limitation in diatom biomass due to a lack of dissolved silicate
(Conley et al., 1993). Therefore, increasing eutrophication may favor the
development of non-siliceous algae, such as dinoflagellates and harmful
species (Billen and Garnier, 2007; Lancelot et al., 2007; Howarth et al.,
2011).
The present study investigated the long-term evolution (trend and
seasonality) of eutrophication parameters (dissolved inorganic nutrient
concentrations and phytoplankton biomass) in the VB coastal waters, in
relation to those in the Loire and the Vilaine between 1980 and 2013, using
dynamic linear models. This long-term ecosystem-scale analysis provided an
opportunity to test the hypothesis that eutrophication trajectories in the
downstream VB coastal waters during recent decades have been influenced by
those in the Loire and Vilaine rivers. We aim to establish the link between
fresh and marine water trajectories and highlight the impact of nutrient
reduction strategies in rivers on coastal water quality.
Material and methodsSites
The Loire is the longest river in France (1012 km) with a watershed of
117 000 km2, while the Vilaine watershed is only a tenth of the size, with
an area of 10 800 km2 (Fig. 1). Their catchment areas are dominated by
agricultural activity, sustaining two-thirds of the national livestock and
half the cereal production (Bouraoui and Grizzetti, 2008; Aquilina et al.,
2012). The Arzal dam, 8 km from the mouth of the Vilaine, was constructed in
1970 to regulate freshwater discharge and prevent saltwater intrusion (Traini
et al., 2015). The two studied rivers, especially the Loire, are the main
nutrient sources in the northern Bay of Biscay, which includes the VB
(Guillaud et al., 2008; Ménesguen et al., 2018a).
Map of the area studied showing Loire and Vilaine rivers and
delimitation of Vilaine Bay (inset red dotted line). Black dots mark the
sampling and gauging stations cited.
The VB, with an average depth of 10 m, is located under direct influence of
these two rivers (Fig. 1). The Loire river plume tends to spread
northwestward with a dilution of 20- to 100-fold by the time it reaches the
VB (Ménesguen and Dussauze, 2015; Ménesguen et al., 2018b). The model
ECO-MARS3D, using numerical tracers (Ménesguen et al., 2018a), estimates
that the Loire constitutes, on average, 30 % of VB dissolved inorganic
nitrogen (DIN) concentrations during floods (min–max 2 %–49 %) and
18 % during periods of low water (min–max 6 %–29 %). The
contributions of the Loire to VB dissolved inorganic phosphorus (DIP) concentrations can reach 36 % during flood periods (average 12 %) but
remain <5 % during periods of low water. The Vilaine river plume tends
to spread throughout the bay before moving westward (Chapelle et al., 1994).
The Vilaine contributions to the DIN concentrations in the VB, estimated by
the model, are slightly lower than those of the Loire whatever the period, on
average 23 % and 17 % for flood and low-water periods, respectively.
The Vilaine contributes, on average, to 5 % and 8 % of VB DIP
concentrations during flood and low-water periods respectively.
The water residence time in the VB varies between 10 and 20 days depending on
the season and tends to be longer during calm periods (Chapelle, 1991;
Chapelle et al., 1994), with tidal ranges varying between 4 and 6 m
(Merceron, 1985). The water circulation is characterized by low tidal and
residual currents, driven mainly by tides, winds and river flows (Lazure and
Salomon, 1991; Lazure and Jegou, 1998). During periods of prevailing winds,
particularly from the southwest and west, the water column of the VB is
subjected to vertical mixing, which can lead sometimes to sediment
resuspension and high turbidity (Goubert et al., 2010). Except during winter
and periods of high hydrodynamic activity, phytoplankton production in the VB
is not limited by light (Guillaud et al., 2008).
Long-term monitoring dataset: rivers and VB
The Loire Brittany River Basin Authority
(http://osur.eau-loire-bretagne.fr/exportosur/Accueil, last access:
31 March 2017) furnished dissolved inorganic nutrients and phytoplankton
biomass data (concentrations of DIP; DIN; dissolved silicate, DSi; and chlorophyll a, Chl a) in rivers, at pre-estuarine stations located closest to
the river mouth upstream of the haline intrusion (Fig. 1). DIN was defined as
the sum of nitrate, nitrite and ammonium, with nitrate as the major component
(>90 %). Sainte-Luce-sur-Loire on the Loire and Rieux on the Vilaine
provided DIP, DIN and Chl a, measured monthly since the 1980s. For
Sainte-Luce-sur-Loire, the influence of tidal dynamics was avoided by
discarding data collected during high tide. Monthly DSi data were available
from 2002 at Montjean-sur-Loire on the Loire and at Férel on the Vilaine
(Fig. 1).
In order to calculate riverine nutrient loads, gauging stations located close
to the river mouth were selected. River discharge data were extracted from
the French hydrologic “Banque Hydro” database
(http://www.hydro.eaufrance.fr/, last access: 20 May 2016). For the
Loire, river discharge measurements at Montjean-sur-Loire were used due to
the absence of data at Sainte-Luce-sur-Loire. The difference in drainage
areas between Montjean (109 930 km2) and Sainte-Luce (111 570 km2)
is negligible (ratio of 1.01) and would not have significantly changed
calculations of nutrient inputs. For the Vilaine, daily discharge data were
available at Rieux from the 1980s. DIN and DIP loads from rivers were
calculated using averaged monthly discharge and individual monthly nutrient
concentrations (Romero et al., 2013).
Nutrient and Chl a concentrations, plus phytoplankton count data in the VB,
provided by the French National Observation Network for Phytoplankton and
Hydrology in coastal waters (REPHY, 2017), were collected from Ouest Loscolo
station (Fig. 1). This station is representative of the VB coastal waters
(Bizzozero et al., 2018; Ménesguen et al., 2019) and displayed the
longest dataset (from 1983 for phytoplankton counts and 1997 for nutrient and
Chl a concentrations).
Acquisition periods, sampling frequencies and methods of analysis are
detailed in Table S1 in the Supplement. Briefly, nutrient concentrations were
measured manually or automatically in flow analysis using standard
colorimetric methods with fluorimetry or photometry detection. Chl a concentrations were
measured with either spectrophotometry or fluorimetry. Microscopic
quantitative micro-phytoplankton analyses in coastal waters were conducted on
Lugol-fixed samples and counted according to Utermöhl (1958).
Phytoplankton identification and counts were carried out for organisms whose
size is >20µm (i.e., micro-phytoplankton) and smaller species
with chain structure. Further details about sampling and processing of
phytoplankton species are available in Hernández-Fariñas et
al. (2014) and Belin and Neaud-Masson (2017). In order to account for the
role of DSi, of all the micro-phytoplankton classes, genera and species
identified in the VB, only total counts of diatoms (Bacillariophyceae) and
dinoflagellates (Dinophyceae) were used in this work. Other
micro-phytoplankton classes (Dictyophyceae, Prasinophyceae, Cyanophyceae,
Chrysophyceae and Raphidophyceae) together represented only 10 % to
15 % of the VB total counts (Belin and Soudant, 2018).
DIN:DIP, DIN:DSi and DSi:DIP molar ratios were
calculated and compared with theoretical molar N:P:Si ratios of
16:1:16 (Redfield, 1958; Brzezinski, 1985) in order to assess the potential
limitation of phytoplankton growth by nutrient in rivers and in the VB and to
investigate for trends.
Time-series analysesData preprocessing
Prior to analysis, all datasets were examined using time-scaled scatter
plots. For DIP in rivers, these showed periods during which a limited set of
values appeared repeatedly (Fig. S1 in the Supplement), which resulted from
analytical problems (Loire Brittany River Basin Authority, Sylvain Jolly, personal communication,
2016). Consequently,
these suspect data were discarded to avoid misinterpretation. The removed DIP
datasets represented 29 % and 31 % of the total number of data,
corresponding respectively to the period 1980–1989 in the Loire and
1980–1989 and 2009–2011 in the Vilaine. Trend analysis was not conducted on
DSi in rivers because the data covered the period 2002–2013 only.
Prior to time-series decomposition, a variance-stabilizing base e log
transformation was applied to all variables, except for phytoplankton counts
for which the base was 10, to ensure compliance with the constant variance
assumption (i.e., homoscedasticity).
Time-series decomposition
The time series were modeled using dynamic
linear models (DLMs; West and Harrison, 1997) with the dlm package (Petris,
2010) in R software (R Development Core Team, 2016). This tool belongs to the
family of methods which encompass, for example, state-space models,
structural time-series models, the Unobserved Components Model (Harvey et
al., 1998) and dynamic harmonic regression (Taylor et al., 2007). The model
decomposes an observed time series into component parts, typically the trend,
the seasonal component (i.e., seasonality) and the residual. The DLM approach
is particularly suitable for environmental data series characterized by
outliers, irregular sampling frequency and missing data. The last-mentioned
are taken into account by the Kalman filter (Kalman, 1960), using a prior
which replaces the missing value; i.e., no information leads to no change in
distributions for model parameters (West and Harrison, 1997). For other
examples of DLM applications, readers may refer to Soudant et al. (1997),
Scheuerell et al. (2002) and Hernández-Fariñas et al. (2014).
The model used was a second-order polynomial trend, which allows modeling
up to a quadratic trend. This was chosen because a linear trend (i.e., first-order polynomial) was too restrictive and a cubic trend (i.e., third-order
polynomial) might lead to an over-fitted model. For the seasonal component,
the model used was trigonometric with two harmonics, which considers
a potential bimodal pattern. This bimodal pattern is characterized by two
peaks per year, such as spring and autumn or summer and winter blooms. This
model specification was used for all parameters.
The time unit, defined as the smallest time interval between sampling dates
within a period of analysis (i.e., 1 year), was weekly, fortnightly or
monthly according to sampling frequencies of variables (see Table S1).
Normality of standardized residuals was checked using a Q–Q plot and their
independence using estimates of the autocorrelation function. If deviations were
suspected, outliers were identified as 2.5 % higher and lower than
standardized residuals and treated appropriately; i.e., specific
observational variances were estimated for each outlier. The DLM time-series
analysis provides figures allowing the visual identification of trends and
variations in seasonality.
Trend
The DLM trend plot displayed observed values with a shade of color for each
time unit segments: weekly, fortnightly or monthly. The trend was represented
by a dark grey line, with the shaded area indicating the 90 % confidence
interval. For the period 1997–2013, common to all variables, (“common
period” hereafter in the text), a monotonic linear trend significance test
was performed on DLM trend components using a modified nonparametric
Mann–Kendall (MK) test (Yue and Wang, 2004). When monotonic linear trends
were significant (p<0.05), changes were calculated from differences
between the beginning and the end of the common period of Sen's robust
line (Helsel and Hirsch, 2002).
Seasonality
The seasonality plot displayed the DLM seasonal component values. The figure
provides visual access to the interannual evolution of the amplitude,
corresponding to the difference between the minimum and maximum values of
each year. As dependent variables have been log-transformed, the model was
multiplicative. Therefore, when seasonal component values were equal to 1 (i.e.,
horizontal line), fitted values were equal to the trend. The seasonality plot
also allowed a visualization of how the values have evolved over the years
according to their seasonal position. The significance of changes in the
seasonality (monotonic linear increase or decrease in the value for a given
season) was assessed for the common period using the modified MK test
performed on DLM seasonal components for each season. The seasons were
defined as winter (January, February, March), spring (April, May, June),
summer (July, August, September), and autumn (October, November, December).
The interpretation of the seasonal components per se was not meaningful;
therefore changes were not calculated, but when monotonic linear trends were
significant (p<0.05), the sign and the percentage of the changes were
provided.
Correlation analysis
Spearman correlations were computed for annual median values of the common
period in order to analyze relationships between variables and tested using
STATGRAPHIC CENTURION software (Statgraphics Technologies Inc., Version
XVII, Released 2014).
ResultsLong-term trends in eutrophication parameters in river basin
outlet
The daily discharge of the Loire varied between 111 and
4760 m3 s-1 for the period 1980–2013, with the DLM trend displaying
oscillations with periodicities of 6–7 years (Fig. 2a). A significant
negative trend was detected for the common period (1997–2013), with a
decrease of 94 m3 s-1 (Table 1). The seasonality plot displayed
no marked change, with maximum values always observed in winter (blue) and
minimum in summer (orange/red; Fig. 2b) and no significant linear change
whatever the season (Table 2). The Vilaine discharge (median of
32 m3 s-1 for the period 1980–2013) corresponded to 6 % of
the Loire discharge and displayed a similar trend and seasonality to those of
the Loire (Fig. S2, Tables 1, 2), as highlighted by the significant
correlation between their annual medians (Table 3).
Long-term trend and seasonality of the Loire discharges. Dark grey
lines represent DLM trends. Shaded areas indicate the 90 % confidence
interval. Each dot in the trend plot (a) represents an observed
value, and those in the seasonality plot (b) represent values
estimated by the model. In the seasonality plot, the horizontal line (y=1.0) indicates seasonal components for which fitted values were equal to the
trend. The dashed vertical blue line indicates the beginning of the longest
common period for all studied variables in rivers and in the VB
(1997–2013).
Statistical results from the Mann–Kendall test performed on DLM trend
components of eutrophication parameters in rivers and in the VB coastal
waters for the common period 1997–2013. If the test was significant at p<0.05, differences of Sen's robust line between the beginning and the end
of the period (17 years) were calculated. Values in parentheses are
percentages of changes relative to the initial values of Sen's robust
line. Increasing or decreasing trends are indicated by + and - signs,
respectively. NS denotes non-significant values.
DIP in the Loire varied between 0.1 and 9.4 µmol L-1 for the
period 1990–2013 (Fig. 3a). A significant decrease of
0.85 µmol L-1 was detected for the common period (Table 1).
Also during this period, the seasonality plot indicated a noteworthy shift in
timing of annual DIP minima from summer to spring, as indicated by its change
in color from yellow/orange (summer) in 2000 to green (spring) from 2006
onwards (Fig. 3b). This change was accompanied by a significant negative
trend for winter–spring seasonal components and a significant positive trend
for summer–autumn ones (Table 2). DIP loads from the Loire ranged between <0.1 and 15 mol s-1 for the period 1990–2013, with the trend displaying
oscillations reflecting the influence of river discharge (Fig. 3c). For the
common period, the Loire DIP loads decreased significantly by 52 %
(Table 1). The seasonality plot of DIP loads from the Loire reflected that of
discharge, with annual minimum and maximum values always observed in summer
and winter, respectively (Fig. 3d). Trends of DIP concentration and DIP loads
for the Vilaine were similar to those for the Loire (Fig. S3, Tables 1, 2),
as indicated by a significant correlation between annual medians of DIP in
the two rivers (Table 3).
Long-term trend and seasonality of DIP in the Loire (a, b) and DIP
loads from the Loire (c, d). See Fig. 2 for details.
Statistical results of the modified Mann–Kendall test performed on DLM
seasonal components of eutrophication parameters in rivers and in the VB for
the common period 1997–2013. If the test was significant at p<0.05,
percentages of changes relative to the initial values of Sen's robust
line were calculated. Increasing or decreasing trends are indicated by +
and - signs, respectively. NS denotes non-significant values.
DIN in the Loire ranged between 11 and 489 µmol L-1 for the
period 1980–2013, with the trend displaying a decrease between the 1980s and the
early 1990s, followed by an increase (Fig. 4a). However, the increase was not
significant for the common period (Table 1). The DLM Loire DIN seasonality
plot indicated a decrease in the seasonal amplitude starting in 1990
(Fig. 4b). For the common period, this decreasing amplitude resulted from a
significant decrease in winter DIN maxima on the one hand and significant
increase in summer minima on the other hand (Table 2) by around
60 µmol L-1 (Fig. 4a). The DIN loads from the Loire varied
from <1.0 to 1142 mol s-1 and displayed a similar trend and
seasonality to those of DIN (Fig. 4c, d), with an increase in summer minima
from around 5 to 50 mol s-1 for the common period (Fig. 4c, Table 2).
The trend of DIN in the Vilaine displayed an oscillation (Fig. S4), with a
slight significant decrease over the common period (Table 1) and no marked
variation in the seasonality (Fig. S4b, Table 2). As for the Loire, the trend
and seasonality of DIN loads from the Vilaine were similar to those of DIN
(Fig. S4c, d, Tables 1, 2).
Long-term trend and seasonality of DIN in the Loire (a, b) and DIN
loads from the Loire (c, d). Black dots represent data considered as
outliers (see Sect. 2.3.2). See Fig. 2 for details.
DIN:DIP ratios in both rivers ranged between 1.0 and 1000, with >80 % of values being higher than 30, and displayed an increasing trend
between 1990 and 2013 (Fig. S5). A significant increase of 85 % and
303 %, respectively, for the Loire and the Vilaine, was detected for the
common period (Table S3). DSi in rivers ranged between 46 and
261 µmol L-1 in the Loire and from 5.0 to
201 µmol L-1 in the Vilaine for the period of available data
(2002–2013). More than 80 % of DIN:DSi ratios in rivers were
higher than the theoretical molar N:Si ratio of 1 for the potential
requirement of diatoms (data not shown).
Chl a in the Loire ranged between >200µg L-1 during the
1980s and <1.0µg L-1 in the 2010s. The Chl a trend
remained stable between 1980 and 2000 before decreasing subsequently
(Fig. 5a). For the common period, the Loire Chl a decreased by 93 %
(54 µg L-1; Table 1). The DLM Loire Chl a seasonality plot
displayed a shift in timing of the annual Chl a maximum, as indicated by
its change in color from orange/red (summer) during 1980–1990 to green
(spring) during 2005–2013 (Fig. 5b). For the common period, this change in
timing was accompanied by a significant negative trend for autumn seasonal
components and significant positive trend for winter and spring (Table 2).
Results for Chl a in the Vilaine revealed a similar trend and seasonality to
those in the Loire (Fig. S6, Tables 1, 2), as indicated by a significant
correlation between Chl a annual medians in the two rivers (Table 3).
Long-term trend and seasonality of Chl a in the Loire. See Fig. 2
for details.
Spearman's rank correlations between annual median values of river
discharge, nutrient concentrations and phytoplankton biomass in the Loire,
Vilaine and the VB for the common period 1997–2013 (n=17). Asterisks
designate significant correlations (***p<0.001, **p<0.01,
*p<0.05).
LoireVilaineDINDIPChl aDINDIPChl aDINDIPDSiChl adischargedischargeLoireLoireLoireVilaineVilaineVilaineVBVBVBVBLoire discharge1.00Vilaine discharge0.88***1.00DIN Loire0.52*0.391.00DIP Loire0.51*0.430.441.00Chl a Loire-0.08-0.060.250.351.00DIN Vilaine0.330.470.020.55*0.59*1.00DIP Vilaine0.160.240.230.77**0.65*0.541.00Chl a Vilaine-0.21-0.280.310.200.64**0.040.351.00DIN VB0.78**0.74**0.360.35-0.100.29-0.01-0.201.00DIP VB0.13-0.090.070.380.050.110.290.19-0.121.00DSi VB0.55*0.410.350.08-0.48-0.17-0.51-0.310.63*-0.021.00Chl a VB0.110.17-0.14-0.48-0.61*-0.34-0.58*-0.50*0.25-0.450.331.00Long-term trends in eutrophication parameters in the VB
DIP in the VB varied between <0.1 and >1.0µmol L-1 with
no noticeable trend (Fig. 6a). A significant decrease of
0.05 µmol L-1 was detected over the common period (Table 1).
The seasonality plot of the VB DIP revealed a change in timing of the minimum
values, as indicated by its change in color from yellow/orange (summer)
before 2006 to green (spring) afterwards (Fig. 6b). This shift was
accompanied by a significant negative linear trend for spring seasonal
components and a significant positive trend for summer (Table 2).
Long-term trend and seasonality of DIP (a, b),
DIN (c, d) and DSi (e, f) in the VB. Black dots represent
data considered as outliers (see Sect. 2.3.2). See Fig. 2 for details.
DIN in the VB varied between <1.0 and >200µmol L-1,
with the trend displaying an oscillation (Fig. 6c). A significant increase of
3.2 µmol L-1 was detected for the common period (Table 1).
The DLM seasonality indicated that this increase was focused in winter
(Fig. 6d, Table 2). Annual DIN medians in the VB were positively correlated
with those of discharge from the two rivers (Table 3).
DSi in the VB varied between <1.0 and 100 µmol L-1 without
a noticeable trend (Fig. 6e). For the common period, a significant increase of
3.6 µmol L-1 was detected, which was comparable to that of
DIN (Table 1). The seasonality did not indicate any particular change
(Fig. 6f, Table 2). Annual DSi medians in the VB were positively correlated
with those of the Loire discharge and with the VB DIN (Table 3).
DIN:DIP and DIN:DSi ratios in the VB ranged between <1.0 and
650 and from <0.1 to 44, respectively (Fig. S7). Summer values of
DIN:DIP and DIN:DSi ratios were often below theoretical values of 16 and
1, respectively, for potential requirements of diatoms (Fig. S7).
DSi:DIP ratios in the VB ranged between <5.0 and >100, with >80 % of values being above the theoretical value of 16 (Fig. S7). The
trends for dissolved inorganic nutrient ratios in the VB displayed a
significant increase for the common period (Fig. S7, Table S3).
Chl a in the VB ranged between 0.1 and 116 µg L-1, with
the trend displaying an increase (Fig. 7a). For the common period, the VB Chl a increased significantly by 126 % (2.1 µg L-1; Table 1).
The seasonality plot of Chl a in the VB displayed a shift in the timing of
the annual maximum, indicated by its change in color from green (spring)
before 2006 to orange/red (late summer) afterwards (Fig. 7b). This change was
accompanied by a significant negative linear trend for spring seasonal
components (Table 2). Annual Chl a medians in the VB were negatively
correlated with those of Chl a from both rivers and with DIP in the Vilaine
(Table 3).
Long-term trend and seasonality of Chl a(a, b),
diatom (c, d) and dinoflagellate (e, f) in the VB. Insets
display trends of diatom and dinoflagellate abundances with optimal scale.
See Fig. 2 for details.
Diatom abundances varied between 200 and 1.3×107 cells L-1
for the period 1983–2013, with the DLM trend showing an increase (Fig. 7c).
For the common period, diatom abundances increased significantly by 227 %
(90×103 cells L-1; Table 1). Although diatom abundances
continued to peak in spring (Fig. 7d), their seasonality plot indicated a
significant increase in summer seasonal components over the common period
(Table 2). Dinoflagellate abundances were about 10-fold less than those of
diatoms, with values ranging between 40 and 3.4×106 cells L-1 over the period 1983–2013. Like diatoms, the DLM
trend for dinoflagellate abundances in the VB displayed an increase
(Fig. 7d). For the common period, dinoflagellates' abundances increased by 8×103 cells L-1 (108 %; Table 1). However, the DLM seasonality plot
indicated that summer seasonal components of dinoflagellate abundances,
corresponding to the dinoflagellate annual peak, displayed a significant
decreasing trend over the common period (Fig. 7f, Table 2).
Discussion
The sequence of causes and effects between eutrophication in continental
aquatic ecosystems and in those located downstream can be studied by
observing trends of eutrophication indicators using the same tool and observing trends during
the same periods. In the present study, eutrophication trajectories in the
downstream VB coastal waters during recent decades were examined, through
long-term trends of phytoplankton biomass and nutrient concentrations, in
relation to the restoration of the eutrophic Loire and Vilaine rivers. The
DLM analysis provided the opportunity to explore trends and changes in
seasonality in a visual manner with figures displaying individual data. The
modified nonparametric Mann–Kendall test applied to DLM trend and seasonal
components of all variables over the common period has permitted corroboration
of DLM observations. Overall results demonstrate that upstream recoveries
from eutrophication were accompanied by increased eutrophication downstream.
The significant reduction in P input relative to N was not enough to
mitigate eutrophication all along this river–coastal marine continuum.
More reduction of N input, paying particular attention to diffuse N sources,
is necessary to mitigate eutrophication effectively in the VB coastal
waters.
Eutrophication trajectories at the river basin outlet
The decrease in Chl a in pre-estuarine stations on the Loire and Vilaine
rivers over the past decades reflects the global diminution in eutrophication
in North American and European rivers (Glibert et al., 2011; Romero et al.,
2013; Dupas et al., 2018). This decrease in Chl a was also observed in the
Upper and Middle Loire (Larroudé et al., 2013; Minaudo et al., 2015).
However, the Loire did not retrieve its oligotrophic state of the 1930s
(Crouzet, 1983). At the studied stations, the annual Chl a peak decreased
and shifted from late summer to spring (Fig. 8a, b). The parallel decrease of
DIP and Chl a in the Loire and Vilaine rivers underlines the role of
decreasing P in reducing phytoplankton biomass (Descy et al., 2012; Minaudo
et al., 2015), as also found in other river systems, such as the Danube
(Istvánovics and Honti, 2012), the Seine (Romero et al., 2013) and some
Scandinavian rivers (Grimvall et al., 2014). This decreasing trend of DIP is
a result of improved sewage treatment, decreased use of P fertilizers and the
removal of P from detergents (Bouraoui and Grizzetti, 2011). However, the
decline of Chl a in both studied rivers began several years after that of
DIP when the latter reached limiting concentrations for phytoplankton, as
deduced at Montjean on the Loire by Garnier et al. (2018). The change in
timing of the annual DIP minima from summer to spring in the Loire and
Vilaine rivers during the last decades of the studied period, concomitant with
that of the annual peak of Chl a, can be explained by the increasingly
early depletion of DIP by phytoplankton (see Floury et al., 2012, for the
Loire).
Graphical representation of the major changes in phytoplankton and
nutrient concentrations in rivers (a, b) and the VB coastal
waters (c, d) for the period 1997–2005 (a, c) and
2006–2013 (b, d). Downward arrows represent long-term trends.
Nutrient curves are ranked from the least limiting (below) to the most
limiting (above) according to Redfield ratios. Nutrient inputs from rivers
and sediments are also ranked according to their potential limitation for
phytoplankton using Redfield ratios. Benthic nutrient inputs were fitted
according to the measurement of benthic fluxes in summer 2015 (Ratmaya,
2018). Shaded areas underline the season of maximum Chl a.
The trend of DIN in studied rivers reveals the general trends observed in
other large European rivers, showing a slight decrease, a steady trend or
even an increase, depending on the degree of fertilizer application in
catchment areas (Bouraoui and Grizzetti, 2011; Romero et al., 2013). The
increase in summer Loire DIN since the early 1990s was offset by the decrease
in winter values, which is related to the reduction in N point source
emissions and N fertilizer application (Poisvert et al., 2016; data from
French Ministry of Agriculture, Sylvie Lesaint, personal communication,
2017). An increase in summer DIN of several tens of micromole per liter was
also reported in the Middle Loire (Minaudo et al., 2015). This increase in
summer DIN is the result of a delayed response due to the long transit time
of DIN through soils and aquifers in the Loire catchment (up to 14 years;
Bouraoui and Grizzetti, 2011). The decreasing DIN uptake by phytoplankton in
the Loire may have also contributed to the increase in summer DIN (Lair,
2001; Floury et al., 2012). Concerning the Vilaine, the slight decrease in
DIN from the early 1990s reflects the decrease in N fertilizer application in
the Vilaine catchment (Bouraoui and Grizzetti, 2011; Aquilina et al., 2012),
which is facilitated by a relatively short transit time of DIN in the Vilaine
watershed (∼5–6 years; Molenat and Gascuel-Odoux, 2002; Aquilina et
al., 2012).
DSi data series in both rivers were too short to investigate long-term trends
and seasonality but provided values in order to examine nutrient
stoichiometry. Larroudé et al. (2013) observed no significant trend in
DSi between 1985 and 2008 in the Middle Loire, as also confirmed at Montjean
station by Garnier et al. (2018). The decrease in DIP led to the increasing
trend of DIN:DIP ratios, and probably DSi:DIP, in both rivers,
as was observed in numerous rivers (Beusen et al., 2016). Based on these
trends, the DIP limitation has thus been reinforced in studied rivers during
the last decades, and potentially in receiving coastal waters, regardless of
the season.
Eutrophication trajectories in the VB
In contrast to what happened in rivers, eutrophication in the downstream VB
coastal waters has worsened during recent decades, as indicated by
a significant increase in Chl a, also confirmed by the significant
augmentation of both diatom and dinoflagellate abundances. The increase in
Chl a in the VB was accompanied by a shift in its annual peak from spring
to summer (Fig. 8c, d). This modification in the seasonal course of
phytoplankton biomass coincides with the increase in diatom abundances,
occurring mainly in summer. The dynamics of phytoplankton in the VB during
the last decade of the studied period thus underwent important changes:
(1) an increase in biomass, (2) a change in timing of the annual peak from
spring to summer and (3) a modification in the seasonal course of diatoms and
dinoflagellates.
Increased Chl a
The increase in phytoplankton biomass could result from several causes,
namely decreased predation (overfishing), a decrease in commercially grown
suspension feeders, an increase in temperature and an increase in nutrient
inputs. Increased predation on planktonic herbivores could reduce grazing on
phytoplankton (Caddy, 2000). In the VB, commercial fishing targeting small
pelagic (herbivorous) species has been banned since 1977 (Dintheer, 1980).
The decline in fisheries in the Bay of Biscay since the 1990s (Rochet et al.,
2005) was unlikely to have caused increased Chl a in the VB, since
phytoplankton biomass in these oceanic waters has always been lower than that
in the VB (Table S2). Grazing activity by bivalve suspension feeders can
modify phytoplankton biomass (Cloern, 1982; Souchu et al., 2001). In the VB,
there was an increase in commercial mussel production (Mytilus edulis) between 2001 and 2012 (Le Bihan et al., 2013). This should have led
to depletion in phytoplankton biomass; in fact the opposite trend was
observed. In regions where the phytoplankton productivity is limited by light
availability, an increase in sea surface temperature can promote
phytoplankton growth due to water column stabilization (Doney, 2006; Boyce et
al., 2010) and decreased turbidity (Cloern et al., 2014). In the VB, except
during winter and high hydrodynamic activity periods, phytoplankton
production is limited by nutrients (Guillaud et al., 2008). Therefore, the
increase in Chl a in the VB was particularly due to enhanced nutrient
availability, as also reported in Chinese coastal waters by Wang et al. (2018).
Changes in timing of annual Chl a peak
Seasonal changes in phytoplankton biomass peaks have been reported in other
aquatic ecosystems and mostly attributed to climate-change-induced
temperature (Edwards and Richardson, 2004; Racault et al., 2017). Variations
in nutrient availability can also induce a change in the seasonal pattern of
phytoplankton biomass (Thackeray et al., 2008; Feuchtmayr et al., 2012).
These authors observed that the advancement in the timing of the spring
diatom bloom in some English lakes was related to the increase in winter DIP.
In the VB, the shift in annual Chl a peak from spring to summer, coupled
with the change in position of the annual DIP minima from summer to spring,
suggests that DIP depletion by phytoplankton bloom occurred progressively
earlier during the last two decades. Based on nutrient concentrations and
stoichiometry (Justić et al., 1995), the first nutrient-limiting
phytoplankton biomass in the VB shifts seasonally from DIP in spring to DIN
in summer, as verified by bioassays (Michaël Retho et al., Ifremer,
unpublished data). The conjunction of the decrease in DIP and an increase in
DIN in the VB has probably also contributed to the shift in annual Chl a.
Role of DSi in the seasonal course of diatoms and dinoflagellates
In terms of nutrients, the balance between diatoms and dinoflagellates is
predominantly regulated by the DSi availability (Egge and Aksnes, 1992). In
the VB, based on nutrient concentrations and stoichiometry, diatoms were
rarely limited by the DSi availability, thanks probably to internal DSi
regeneration, as suggested by Lunven et al. (2005) and Loyer et al. (2006) in
the northern Bay of Biscay continental shelf. The fact that diatoms have
increased more than dinoflagellates in the VB contradicts the idea that
excessive DIN and DIP inputs favor phytoplankton species, which do not
require DSi (Conley et al., 1993; European Communities, 2009; Howarth et al.,
2011). An increase in diatom abundances during the eutrophication process was
also observed in Tolo Harbor (Yung et al., 1997; Lie et al., 2011) and the
coastal waters of the Gulf of Finland (Weckström et al., 2007).
Conversely, decreasing eutrophication in the Seto Inland Sea (Yamamoto,
2003), in the Thau lagoon (Collos et al., 2009) and in other Mediterranean lagoons (Leruste
et al., 2016) was accompanied by the increase in dinoflagellate abundances to
the detriment of diatoms. These observations and our results provide evidence
that eutrophication can be manifested by an increase in diatom abundances.
Loire–Vilaine–VB continuum
In theory, several external nutrient sources could have contributed to
nutrient availability in the VB: atmospheric, oceanic and riverine inputs.
DIN inputs from rainwater estimated by Collos et al. (1989) represent only
1 % of river inputs, while levels of nutrients and Chl a in the Bay of
Biscay always remained low during the studied period (Table S2). The
proximity of the VB to the Loire and Vilaine rivers designates riverine
inputs as main external nutrient sources in these coastal waters
(Ménesguen et al., 2018a, b).
Rivers as the main external nutrient source to the VB
Watersheds, rivers and coastal waters located at their outlet constitute a
continuum in which anthropogenic pollution, generated in watersheds, is
transported to coastal zones (Vannote et al., 1980). The transfer of
nutrients from continents to coastal waters is largely determined by
freshwater inputs, the dynamics of which depend largely on precipitation in
watersheds. Trends in the Loire and the Vilaine discharges displayed similar
oscillations to those of rivers flowing to the North Sea as reported by
Radach and Pätsch (2007), suggesting a common hydroclimatic pattern in
western Europe linked to the North Atlantic Oscillation. The decrease in the
Loire discharge observed between 1997 and 2013 was also found in the middle
section of the river for the period 1977–2008 (Floury et al., 2012) and
was attributed essentially to abstraction for irrigation and drinking water by
these authors. The strong correlation between Loire and Vilaine discharges
underlines the similarities between the two rivers concerning the
precipitation regime. However, with a 10-fold higher discharge than the
Vilaine, the Loire remains the main source of freshwater for the northern Bay
of Biscay, with a major role in the eutrophication of coastal waters in south
Brittany, including the VB (Guillaud et al., 2008; Ménesguen et al.,
2018a, 2019). Aside from flood periods, the closure of the Arzal dam during
the low-water periods (Traini et al., 2015) makes nutrient inputs into the
VB by the Vilaine negligible in summer, compared to those from the Loire.
Role of estuaries and the Vilaine dam
Biogeochemical processes within estuaries may alter the nutrient transfer
from rivers to coastal waters (Statham, 2012). Coupled
nitrification–denitrification and ammonification-anammox can be a sink of N
in estuaries (Abril et al., 2000). Inorganic nutrients in estuaries can also
be removed by phytoplankton uptake, which is nonetheless limited by turbidity
(Middelburg and Nieuwenhuize, 2000). Estuaries can also act as a source of
nutrients, resulting from mineralization of riverine phytoplankton organic
matter (Meybeck et al., 1988; Middelburg et al., 1996). However, for the
studied rivers, this process may have diminished with the decreasing trend in
riverine Chl a. The desorption of loosely bound P from suspended mineral
particles in estuaries can also be a source of DIP (Deborde et al., 2007).
Except during flood periods, the suspended particle fluxes from the Loire are
generally low (Moatar and Dupont, 2016). In addition to these biogeochemical
processes, the increase in population around the Loire estuary (ca.
1 % yr-1; INSEE, 2009) during the last decades could have
contributed to the increase in N and P inputs. However, inputs of DIN and DIP
from wastewater treatment plants in the Loire and Vilaine estuaries have not
increased due to improved treatment techniques (Loire-Brittany River Basin
Authority, Philippe Fera, personal communication, 2019). The presence of a
dam at the river outlet may increase water residence time, thus favoring
nutrient uptake by phytoplankton and loss of N via denitrification
(Seitzinger et al., 2006). Unfortunately, for these two studied rivers,
processes in estuaries and the dam are poorly investigated and quantified,
which makes it difficult to estimate their influence on nutrient transfer to
coastal zone.
Despite influences of estuaries and the dam, the increase in DIN:DIP and
DSi:DIP ratios in rivers during the last two decades, with values already
largely above the theoretical value of 16 in the 1990s, has been reflected in
the VB coastal waters (Figs. S5, S7). Moreover, significant negative
correlations between annual Chl a medians in the VB and in rivers, as well
as significant positive correlations between annual medians of DIN and DSi in
the VB with those of river discharge, suggest that changes in eutrophication
parameters in the VB (i.e., phytoplankton biomass) were related to changes in
rivers (Ménesguen et al., 2018a, b). Although biogeochemical processes in
estuaries and the Vilaine dam may introduce bias in nutrient transfer from
rivers to the VB, they are probably not intense enough to decouple the
observed trends between rivers and the VB, as suggested by Romero et
al. (2016) for the Seine River–Seine Bay continuum.
Link between eutrophication trajectories in rivers and in the
VB
During the last two decades, the downstream VB coastal waters have received
decreasing DIP inputs, increasing DIN inputs especially from the Loire during
summer and no change in DSi inputs (Fig. 8). The decrease in riverine DIP
loads was the cause of the simultaneously decreasing trend in the VB DIP and
may have reinforced spring DIP limitation, as also reported by Billen et
al. (2007) in the Seine Bay. The worsening eutrophication in the VB was the
consequence of increasing DIN inputs from the Loire. A similar observation
was reported in other coastal ecosystems, such as the Neuse River Estuary
(Paerl et al., 2004), Belgian coastal waters (Lancelot et al., 2007) and the
Seine Bay (Romero et al., 2013), where decreasing upstream Chl a, due to
DIP input reduction, was accompanied by the increase in downstream Chl a,
as a result of increasing DIN input. The seasonal change in annual Chl a
peak in the VB also resulted from the conjunction of decreasing DIP loads and
increasing summer DIN loads from the Loire. The summer limitation of
phytoplankton production by DIN, rather than a limitation by DIP and
especially DSi in the VB, cannot be explained by the stoichiometry of
nutrients in rivers. Internal sources of nutrients, especially sediments (see
below), were also likely to support a significant portion of nutrient
availability for phytoplankton production during the period of low river
discharge (Cowan and Boynton, 1996; Pitkänen et al., 2001).
Role of internal nutrient loads
In shallow ecosystems, internal nutrient recycling can regulate phytoplankton
production and potentially exacerbate eutrophication (Paerl et al., 2016), as
observed both in lakes (Jeppesen et al., 2005) and coastal ecosystems
(Pitkänen et al., 2001). Compared to freshwater, the fragility of marine
ecosystems is related to salinity (Blomqvist et al., 2004). The presence of
sulfate (a major element of salinity) decreases the efficiency of sediments to
retain DIP (Caraco et al., 1990; Lehtoranta et al., 2009) and favors the
recycling of DIP over DIN, the latter being potentially eliminated through
denitrification (Conley, 2000; Conley et al., 2009). In the VB, measurements
of benthic nutrient fluxes confirm that sediments represent a substantial DIP
and DSi source compared to riverine inputs (Ratmaya, 2018), allowing summer
phytoplankton production to benefit from surplus DIN inputs from the Loire.
The increase in summer diatom abundances in the VB was thus mainly due to
increased summer DIN loads from the Loire, sustained by internal sources of
DIP and DSi coming from sediments.
Implications for nutrient managementImpact of nutrient management strategies
The need to control both N and P inputs to mitigate eutrophication along the
freshwater–marine continuum is still debated within the scientific community
(see Schindler et al., 2008, 2016; Conley et al., 2009; Schindler, 2012;
Paerl et al., 2016). Despite the imbalance between P and N input reduction,
eutrophication in the river section of the Loire–Vilaine–VB continuum has
diminished but the increase in phytoplankton biomass in the VB provides
evidence that significant reduction of P inputs, without concomitant N
abatement, was not yet sufficient to improve water quality along the entire
continuum. Targeting N and P pollution from point sources has successfully
reduced eutrophication in marine ecosystems, as evidenced in the Tampa Bay
(Greening and Janicki, 2006) and in several French Mediterranean lagoons
(Derolez et al., 2019). However, N pollution in coastal waters from rivers
with watersheds largely occupied by intensive agriculture remain problematic
in many European countries (Bouraoui and Grizzetti, 2011; Romero et al.,
2013). Reducing diffuse N inputs through improved agricultural practices and
structural changes in the agro-food system (Desmit et al., 2018; Garnier et
al., 2018) would probably help to lessen eutrophication (Conley et al., 2009;
Paerl, 2009). Assuming that rapid and radical change in farming practices is
implemented, the delayed responses due to variations in transit time of
NO3- in aquifers should be taken into account for restoration
strategy (Bouraoui and Grizzetti, 2011).
In the VB, a reduction in DIN inputs, especially during the summer, would
probably have prevented eutrophication from worsening in this ecosystem.
Given that in many other coastal ecosystems the first nutrient-limiting
phytoplankton production tends to switch from DIP in spring to DIN in summer
(Fisher et al., 1992; Del Amo et al., 1997; Tamminen and Andersen, 2007), it
would be relevant to take into account seasonal aspects for nutrient
reduction strategy.
Influence of internal nutrient regeneration
In the VB, the internal nutrient recycling from sediments appears to have
contributed to the worsening of summer water quality during the last two
decades and augmented the effects of anthropogenic nutrient inputs. Internal
nutrient loads can delay ecosystem recovery from eutrophication following
external nutrient input reduction (Duarte et al., 2009). In lakes, this delay
induced by internal loads of P on the oligotrophication process varies from
10 to 20 years (Jeppesen et al., 2005; Søndergaard et al., 2007). In
coastal ecosystems, the delay resulting from internal nutrient loads was less
studied. However, Soetaert and Middelburg (2009), using a model in a shallow
coastal ecosystem, estimated a delay of more than 20 years following the
reduction of external N input. Therefore, for the Loire–Vilaine–VB
continuum, nutrient management strategies should consider the internal
nutrient loads in order to anticipate the delay in recovery of the VB coastal
waters from eutrophication.
Conclusions and perspectives
Parallel investigation of eutrophication parameters in the Loire and Vilaine
rivers, and coastal waters under their influence, revealed several striking
patterns and relationships, of which the most apparent were upstream
recoveries from eutrophication accompanied by increased eutrophication
downstream (Fig. 8). During the last two decades, coastal
waters off the Loire and Vilaine rivers have experienced a diminution
in DIP inputs, whereas DIN continued to increase in the Loire during summer.
While the decreasing trends in DIP were accompanied by declining
phytoplankton biomass in rivers, the seasonal cycle of phytoplankton has been
changed in downstream VB, with an increase in biomass, a shift in its annual
peak from spring to summer and a modification in the seasonal course of
diatoms and dinoflagellates. Moreover, the concept of diatom replacement by
dinoflagellates during the eutrophication process does not seem to be
applicable to all shallow coastal ecosystems.
These results open up a whole field of investigation into the effects of
changes in the phytoplankton dynamics on food webs, which is of major
importance to this flatfish nursery and commercial shellfish area
(Désaunay et al., 2006; Chaalali et al., 2017). Further studies are
necessary to investigate the modifications in the phytoplankton community,
especially the phenology of the different species, as well as the possible
consequence on food webs. Finally, the internal loads of nutrients from
sediments are suspected of counteracting the reduction of external nutrients,
thus delaying the restoration progress. During the eutrophication process,
sediments may also play an important role in the balance between diatoms and
others classes of phytoplankton. Taking into account these internal processes
in modeling studies (i.e., ECO-MARS3D; Ménesguen et al., 2018a, b,
2019), will better simulate nutrient load scenarios in shallow coastal bays
(work in progress).
Data availability
All data used in this study are available on the following
online databases: French National Observation Network for Phytoplankton and
Hydrology in coastal waters (10.17882/47248), French Oceanographic
Cruises PELGAS surveys
(http://campagnes.flotteoceanographique.fr/series/18/, last access:
23 August 2017), Loire-Brittany River Basin Authority
(http://osur.eau-loire-bretagne.fr/exportosur/Accueil, last access:
31 March 2017), French hydrologic database
(http://www.hydro.eaufrance.fr/, last access: 20 May 2016) and ICES
Oceanographic database
(http://ocean.ices.dk/HydChem/HydChem.aspx?plot=yes, last access:
23 August 2017).
The supplement related to this article is available online at: https://doi.org/10.5194/bg-16-1361-2019-supplement.
Author contributions
WR and PS designed the study. WR compiled and prepared the datasets. DS
performed statistical and time-series analyses. MP performed the model
(ECO-MARS3D) calculating the contribution of the Loire and Vilaine rivers. WR
wrote the paper with contributions from all co-authors (PS, DS, JSM, MP,
NCL, EG, FAL, LB).
Competing interests
The authors declare that they have no conflict of
interest.
Acknowledgements
This study was funded by the Loire Brittany River Basin Authority (AELB). The
authors are grateful to Sylvain Jolly from AELB for providing datasets of the
Vilaine and the Loire. The authors thank IFREMER-LER/MPL staff for their
technical contributions, especially Karine Collin, Yoann Le Merrer,
Mireille Fortune, Michaël Retho, Raoul Gabellec, Jacky Chauvin,
Isabelle Truquet and Anne Schmitt. We thank Alice Mellor for the proof
reading. The authors are grateful to F. Gerald Plumley, Anniet M. Laverman
and several anonymous reviewers for their comments on the earlier draft of
this paper. Authors acknowledge IFREMER and the Regional Council of the
Région des Pays de la Loire for the funding of Widya Ratmaya's PhD. The
authors thank Perran Cook for editing the manuscript. Our grateful
acknowledgements also go to Camille Minaudo and an anonymous reviewer for
their constructive comments and suggestions.
Review statement
This paper was edited by Perran Cook and reviewed by
Camille Minaudo and one anonymous referee.
References
91/271/EEC: Directive 91/271/EEC concerning urban waste-water treatment,
Official Journal L, 135, 40–52, 1991.
91/676/EEC: Directive 91/676/EEC concerning the protection of waters against
pollution caused by nitrates from agricultural sources, Official Journal L,
375, 1–8, 1991.Abril, G., Riou, S. A., Etcheber, H., Frankignoulle, M., de Wit, R., and
Middelburg, J. J.: Transient, tidal time-scale, nitrogen transformations in
an estuarine turbidity maximum – fluid mud system (The Gironde, South-west
France), Estuar. Coast. Shelf S., 50, 703–715, 10.1006/ecss.1999.0598,
2000.Aquilina, L., Vergnaud-Ayraud, V., Labasque, T., Bour, O., Molenat, J., Ruiz,
L., de Montety, V., De Ridder, J., Roques, C., and Longuevergne, L.: Nitrate
dynamics in agricultural catchments deduced from groundwater dating and
long-term nitrate monitoring in surface- and groundwaters, Sci. Total
Environ., 435–436, 167–178, 10.1016/j.scitotenv.2012.06.028, 2012.
Belin, C. and Neaud-Masson, N.: Cahier de Procédures REPHY, Document de
prescription, Version 1, 61 pp., Ifremer, Nantes, France, 2017 (in French).
Belin, C. and Soudant, D.: Trente années d'observation des micro-algues
et des toxines d'algues sur le littoral, Éditions Quæ, Versailles,
258 pp., 2018 (in French).Beusen, A. H. W., Bouwman, A. F., Van Beek, L. P. H., Mogollón, J. M.,
and Middelburg, J. J.: Global riverine N and P transport to ocean increased
during the 20th century despite increased retention along the aquatic
continuum, Biogeosciences, 13, 2441–2451,
10.5194/bg-13-2441-2016, 2016.Billen, G. and Garnier, J.: River basin nutrient delivery to the coastal sea:
Assessing its potential to sustain new production of non-siliceous algae,
Mar. Chem., 106, 148–160, 10.1016/j.marchem.2006.12.017, 2007.Billen, G., Garnier, J., Nemery, J., Sebilo, M., Sferratore, A., Barles, S.,
Benoit, P., and Benoit, M.: A long-term view of nutrient transfers through
the Seine river continuum, Sci. Total Environ., 375, 80–97,
10.1016/j.scitotenv.2006.12.005, 2007.Bizzozero, L., Gohin, F., Lampert, L., Fortune, M., and Cochennec-Laureau,
N.: Apport des images satellite à l'évaluation de la qualité des
masses d'eau DCE. Analyse des données de Chlorophylle a sur la
période 2011–2016 dans les masses d'eau côtière du bassin
versant Loire-Bretagne, 50 pp., Ifremer, Nantes, France, 2018 (in French).Blomqvist, S., Gunnars, A., and Elmgren, R.: Why the limiting nutrient
differs between temperate coastal seas and freshwater lakes: A matter of
salt, Limnol. Oceanogr., 49, 2236–2241, 10.4319/lo.2004.49.6.2236, 2004.Bouraoui, F. and Grizzetti, B.: An integrated modelling framework to estimate
the fate of nutrients: Application to the Loire (France), Ecol. Model., 212,
450–459, 10.1016/j.ecolmodel.2007.10.037, 2008.Bouraoui, F. and Grizzetti, B.: Long term change of nutrient concentrations
of rivers discharging in European seas, Sci. Total Environ., 409, 4899–4916,
10.1016/j.scitotenv.2011.08.015, 2011.Bouwman, A. F., Bierkens, M. F. P., Griffioen, J., Hefting, M. M.,
Middelburg, J. J., Middelkoop, H., and Slomp, C. P.: Nutrient dynamics,
transfer and retention along the aquatic continuum from land to ocean:
towards integration of ecological and biogeochemical models, Biogeosciences,
10, 1–22, 10.5194/bg-10-1-2013, 2013.Bowes, M. J., Ings, N. L., McCall, S. J., Warwick, A., Barrett, C., Wickham,
H. D., Harman, S. A., Armstrong, L. K., Scarlett, P. M., Roberts, C.,
Lehmann, K., and Singer, A. C.: Nutrient and light limitation of periphyton
in the River Thames: implications for catchment management, Sci. Total
Environ., 434, 201–212, 10.1016/j.scitotenv.2011.09.082, 2012.Boyce, D. G., Lewis, M. R., and Worm, B.: Global phytoplankton decline over
the past century, Nature, 466, 591–596, 10.1038/nature09268, 2010.Brzezinski, M. A.: The Si:C:N ratio of marine diatoms: Interspecific
variability and the effect of some environmental variables, J. Phycol., 21,
347–357, 10.1111/j.0022-3646.1985.00347.x, 1985.Caddy, J. F.: Marine catchment basin effects versus impacts of fisheries on
semi-enclosed seas, ICES J. Mar. Sci., 57, 628–640,
10.1006/jmsc.2000.0739, 2000.Caraco, N., Cole, J. J., and Likens, G. E.: A comparison of phosphorus
immobilization in sediments of freshwater and coastal marine systems,
Biogeochemistry, 9, 277–290, 10.1007/bf00000602, 1990.Chaalali, A., Brind'Amour, A., Dubois, S. F., and Le Bris, H.: Functional
roles of an engineer species for coastal benthic invertebrates and demersal
fish, Ecol. Evol., 7, 5542–5559, 10.1002/ece3.2857, 2017.
Chapelle, A.: Modélisation d'un écosystème marin côtier
soumis à l'eutrophisation: la Baie de Vilaine (Sud Bretagne). Etude du
phytoplancton et du bilan en oxygène, PhD thesis, Université Paris
VI, 214 pp., 1991 (in French).Chapelle, A., Lazure, P., and Menesguen, A.: Modelling eutrophication events
in a coastal ecosystem. Sensitivity analysis, Estuar. Coast. Shelf S., 39,
529–548, 10.1016/S0272-7714(06)80008-9, 1994.
Cloern, J. E.: Does the benthos control phytoplankton biomass in south San
Francisco Bay?, Mar. Ecol.-Prog. Ser., 9, 191–202, 1982.Cloern, J. E.: Our evolving conceptual model of the coastal eutrophication
problem, Mar. Ecol.-Prog. Ser., 210, 223–253, 10.3354/meps210223, 2001.Cloern, J. E., Foster, S. Q., and Kleckner, A. E.: Phytoplankton primary
production in the world's estuarine-coastal ecosystems, Biogeosciences, 11,
2477–2501, 10.5194/bg-11-2477-2014, 2014.Collos, Y., Souchu, P., and Tréguer, P.: Relationships between different
forms of inorganic nitrogen in rainwater of a coastal area and ground-level
gaseous nitrogen oxides, Atmos. Res., 23, 97–104,
10.1016/0169-8095(89)90001-x, 1989.Collos, Y., Bec, B., Jauzein, C., Abadie, E., Laugier, T., Lautier, J.,
Pastoureaud, A., Souchu, P., and Vaquer, A.: Oligotrophication and emergence
of picocyanobacteria and a toxic dinoflagellate in Thau lagoon, southern
France, J. Sea Res., 61, 68–75, 10.1016/j.seares.2008.05.008, 2009.Conley, D. J.: Biogeochemical nutrient cycles and nutrient management
strategies, Hydrobiologia, 410, 87–96, 10.1023/a:1003784504005, 2000.Conley, D. J., Schelske, C. L., and Stoermer, E. F.: Modification of the
biogeochemical cycle of silica with eutrophication, Mar. Ecol.-Prog. Ser.,
101, 179–192, 10.3354/meps101179, 1993.Conley, D. J., Paerl, H. W., Howarth, R. W., Boesch, D. F., Seitzinger, S.
P., Havens, K. E., Lancelot, C., and Likens, G. E.: Controlling
Eutrophication: Nitrogen and phosphorus, Science, 323, 1014–1015,
10.1126/science.1167755, 2009.Correll, D. L.: Phosphorus: a rate limiting nutrient in surface waters,
Poultry Sci., 78, 674–682, 10.1093/ps/78.5.674, 1999.Cowan, J. L. W. and Boynton, W. R.: Sediment-water oxygen and nutrient
exchanges along the longitudinal axis of Chesapeake Bay: Seasonal patterns,
controlling factors and ecological significance, Estuaries, 19, 562–580,
10.2307/1352518, 1996.
Crouzet, P.: L'eutrophisation de la Loire, Water Supp., 1, 131–144, 1983 (in
French).Deborde, J., Anschutz, P., Chaillou, G., Etcheber, H., Commarieu, M. V.,
Lecroart, P., and Abril, G.: The dynamics of phosphorus in turbid estuarine
systems: Example of the Gironde estuary (France), Limnol. Oceanogr., 52,
862–872, 10.4319/lo.2007.52.2.0862, 2007.Del Amo, Y., Le Pape, O., Tréguer, P., Quéguiner, B., Ménesguen,
A., and Aminot, A.: Impacts of high-nitrate freshwater inputs on macrotidal
ecosystems. I. Seasonal evolution of nutrient limitation for the
diatom-dominated phytoplankton of the Bay of Brest (France), Mar. Ecol.-Prog.
Ser., 161, 213–224, 10.3354/meps161213, 1997.Derolez, V., Bec, B., Munaron, D., Fiandrino, A., Pete, R., Simier, M.,
Souchu, P., Laugier, T., Aliaume, C., and Malet, N.: Recovery trajectories
following the reduction of urban nutrient inputs along the eutrophication
gradient in French Mediterranean lagoons, Ocean Coast. Manage., 171, 1–10,
10.1016/j.ocecoaman.2019.01.012, 2019.Désaunay, Y., Guérault, D., Le Pape, O., and Poulard, J.-C.: Changes
in occurrence and abundance of northern/southern flatfishes over a 20-year
period in a coastal nursery area (Bay of Vilaine) and on the eastern
continental shelf of the Bay of Biscay, Sci. Mar., 70, 193–200,
10.3989/scimar.2006.70s1193, 2006.Descy, J. P., Leitao, M., Everbecq, E., Smitz, J. S., and Deliege, J. F.:
Phytoplankton of the River Loire, France: a biodiversity and modelling study,
J. Plankton Res., 34, 120–135, 10.1093/plankt/fbr085, 2012.Desmit, X., Thieu, V., Billen, G., Campuzano, F., Duliere, V., Garnier, J.,
Lassaletta, L., Menesguen, A., Neves, R., Pinto, L., Silvestre, M., Sobrinho,
J. L., and Lacroix, G.: Reducing marine eutrophication may require a
paradigmatic change, Sci. Total Environ., 635, 1444–1466,
10.1016/j.scitotenv.2018.04.181, 2018.
Dintheer, C.: La pêche de Quiberon à la Vilaine, Vol. 1223, 93–98,
La Pêche Maritime, Paris, France, 1980.Doney, S. C.: Oceanography: Plankton in a warmer world, Nature, 444,
695–696, 10.1038/444695a, 2006.Downing, J. A.: Limnology and oceanography: Two estranged twins reuniting by
global change, Inland Waters, 4, 215–232, 10.5268/iw-4.2.753, 2014.Duarte, C. M., Conley, D. J., Carstensen, J., and Sanchez-Camacho, M.: Return
to neverland: Shifting baselines affect eutrophication restoration targets,
Estuar. Coast., 32, 29–36, 10.1007/s12237-008-9111-2, 2009.Dupas, R., Minaudo, C., Gruau, G., Ruiz, L., and Gascuel-Odoux, C.:
Multidecadal trajectory of riverine nitrogen and phosphorus dynamics in rural
catchments, Water Resour. Res., 54, 5327–5340, 10.1029/2018wr022905,
2018.Edwards, M. and Richardson, A. J.: Impact of climate change on marine pelagic
phenology and trophic mismatch, Nature, 430, 881–884,
10.1038/nature02808, 2004.
EEA: State of Europe's seas, 178 pp., European Environment Agency,
Luxembourg, 2017.
Egge, J. K. and Aksnes, D. L.: Silicate as regulating nutrient in
phytoplankton competition, Mar. Ecol.-Prog. Ser., 83, 281–289, 1992.
European Communities: Common implementation strategy for the Water Framework
Directive (2000/60/EC), Guidance Document No. 23, Guidance document on
eutrophication assessment in the context of European Water Policies, European
Communities, Luxembourg, 2009.Feuchtmayr, H., Thackeray, S. J., Jones, I. D., De Ville, M., Fletcher, J.,
James, B. E. N., and Kelly, J.: Spring phytoplankton phenology – are
patterns and drivers of change consistent among lakes in the same
climatological region?, Freshwater Biol., 57, 331–344,
10.1111/j.1365-2427.2011.02671.x, 2012.
Fisher, T. R., Peele, E. R., Ammerman, J. W., and Harding Jr., L. W.:
Nutrient limitation of phytoplankton in Chesapeake Bay, Mar. Ecol.-Prog.
Ser., 82, 51–63, 1992.Floury, M., Delattre, C., Ormerod, S. J., and Souchon, Y.: Global versus
local change effects on a large European river, Sci. Total Environ., 441,
220–229, 10.1016/j.scitotenv.2012.09.051, 2012.Garnier, J., Ramarson, A., Billen, G., Thery, S., Thiery, D., Thieu, V.,
Minaudo, C., and Moatar, F.: Nutrient inputs and hydrology together determine
biogeochemical status of the Loire River (France): Current situation and
possible future scenarios, Sci. Total Environ., 637–638, 609–624,
10.1016/j.scitotenv.2018.05.045, 2018.Glibert, P. M., Fullerton, D., Burkholder, J. M., Cornwell, J. C., and Kana,
T. M.: Ecological stoichiometry, biogeochemical cycling, invasive species,
and aquatic food webs: San Francisco Estuary and comparative systems, Rev.
Fish. Sci., 19, 358–417, 10.1080/10641262.2011.611916, 2011.Gohin, F.: Répartition spatio-temporelle de la chlorophylle a.
Sous-région marine Golfe de Gascogne, Evaluation initiale DCSMM, 13 pp.,
Ifremer, Brest, France, 2012 (in French).Goubert, E., Frenod, E., Peeters, P., Thuillier, P., Vested, H. J., and
Bernard, N.: The use of altimetric data (Altus) in the characterization of
hydrodynamic climates controlling hydrosedimentary processes of intertidal
mudflat: the Vilaine estuary case (Brittany, France), Revue Paralia, 3,
6.17–6.31, 10.5150/revue-paralia.2010.0066.1-6.15, 2010.Greening, H. and Janicki, A.: Toward reversal of eutrophic conditions in a
subtropical estuary: water quality and seagrass response to nitrogen loading
reductions in Tampa Bay, Florida, USA, Environ. Manage., 38, 163–178,
10.1007/s00267-005-0079-4, 2006.Grimvall, A., von Bromssen, C., and Lindstrom, G.: Using process-based models
to filter out natural variability in observed concentrations of nitrogen and
phosphorus in river water, Environ. Monit. Assess., 186, 5135–5152,
10.1007/s10661-014-3765-y, 2014.Grizzetti, B., Bouraoui, F., and Aloe, A.: Changes of nitrogen and phosphorus
loads to European seas, Glob. Change Biol., 18, 769–782,
10.1111/j.1365-2486.2011.02576.x, 2012.Guillaud, J.-F., Aminot, A., Delmas, D., Gohin, F., Lunven, M., Labry, C.,
and Herbland, A.: Seasonal variation of riverine nutrient inputs in the
northern Bay of Biscay (France), and patterns of marine phytoplankton
response, J. Marine Syst., 72, 309–319, 10.1016/j.jmarsys.2007.03.010,
2008.
Harvey, A., Jan Koopman, S., and Penzer, J.: Messy Time Series: A Unified
Approach, in: Messy Data, 103–143, Emerald Group Publishing Limited,
Bingley, UK, 1998.
Helsel, D. R. and Hirsch, R. M.: Statistical Methods in Water Resources,
Hydrologic analysis and interpretation: Techniques of Water-Resources
Investigations of the U.S. Geological Survey, Chapter A3, 510 pp., US
Geological Survey, Reston, VA, 2002.Hernández-Fariñas, T., Soudant, D., Barillé, L., Belin, C.,
Lefebvre, A., and Bacher, C.: Temporal changes in the phytoplankton community
along the French coast of the eastern English Channel and the southern Bight
of the North Sea, ICES J. Mar. Sci., 71, 821–833,
10.1093/icesjms/fst192, 2014.Howarth, R., Chan, F., Conley, D. J., Garnier, J., Doney, S. C., Marino, R.,
and Billen, G.: Coupled biogeochemical cycles: eutrophication and hypoxia in
temperate estuaries and coastal marine ecosystems, Front. Ecol. Environ., 9,
18–26, 10.1890/100008, 2011.
INSEE: En Pays de la Loire, une densification de la population plus loin des
villes, Étude no. 74, INSEE Pays de la Loire, Nantes, France, 2009 (in
French).Istvánovics, V. and Honti, M.: Efficiency of nutrient management in
controlling eutrophication of running waters in the Middle Danube Basin,
Hydrobiologia, 686, 55–71, 10.1007/s10750-012-0999-y, 2012.Jarvie, H. P., Sharpley, A. N., Withers, P. J., Scott, J. T., Haggard, B. E.,
and Neal, C.: Phosphorus mitigation to control river eutrophication: murky
waters, inconvenient truths, and “postnormal” science, J. Environ. Qual.,
42, 295–304, 10.2134/jeq2012.0085, 2013.Jeppesen, E., Sondergaard, M., Jensen, J. P., Havens, K. E., Anneville, O.,
Carvalho, L., Coveney, M. F., Deneke, R., Dokulil, M. T., Foy, B. O. B.,
Gerdeaux, D., Hampton, S. E., Hilt, S., Kangur, K., Kohler, J. A. N.,
Lammens, E. H. H. R., Lauridsen, T. L., Manca, M., Miracle, M. R., Moss, B.,
Noges, P., Persson, G., Phillips, G., Portielje, R. O. B., Romo, S.,
Schelske, C. L., Straile, D., Tatrai, I., Willen, E. V. A., and Winder, M.:
Lake responses to reduced nutrient loading – an analysis of contemporary
long-term data from 35 case studies, Freshwater Biol., 50, 1747–1771,
10.1111/j.1365-2427.2005.01415.x, 2005.Justić, D., Rabalais, N. N., Turner, R. E., and Dortch, Q.: Changes in
nutrient structure of river-dominated coastal waters: stoichiometric nutrient
balance and its consequences, Estuar. Coast. Shelf S., 40, 339–356,
10.1016/s0272-7714(05)80014-9, 1995.Kalman, R. E.: A new approach to linear filtering and prediction problems, J.
Basic Eng.-T. ASME, 82, 35–45, 10.1115/1.3662552, 1960.Lair, N.: Regards croisés sur l'état de la Loire Moyenne:
potamoplancton et qualité de l'eau, quel enseignement tirer de 20
années d'études?, Hydroécol. Appl., 13, 3–41,
10.1051/hydro:2001002, 2001.Lancelot, C., Gypens, N., Billen, G., Garnier, J., and Roubeix, V.: Testing
an integrated river–ocean mathematical tool for linking marine
eutrophication to land use: The Phaeocystis-dominated Belgian coastal zone
(Southern North Sea) over the past 50 years, J. Marine Syst., 64, 216–228,
10.1016/j.jmarsys.2006.03.010, 2007.Larroudé, S., Massei, N., Reyes-Marchant, P., Delattre, C., and Humbert,
J. F.: Dramatic changes in a phytoplankton community in response to local and
global pressures: a 24-year survey of the river Loire (France), Glob. Change
Biol., 19, 1620–1631, 10.1111/gcb.12139, 2013.Lazure, P. and Jegou, A.-M.: 3D modelling of seasonal evolution of Loire and
Gironde plumes on Biscay Bay continental shelf, Oceanol. Acta, 21, 165–177,
10.1016/s0399-1784(98)80006-6, 1998.
Lazure, P. and Salomon, J. C.: Etude par modèles mathématiques de la
circulation marine entre Quiberon et Noirmoutier, Oceanol. Acta, Vol. Sp.,
93–99, 1991 (in French).
Le Bihan, V., Morineau, B., and Ollivier, P.: Recensement de la
conchyliculture entre 2001 et 2012, résultats et analyses, 177 pp.,
Agreste, Ministère de l'Agriculture et de l'Alimentation, 2013 (in
French).Lehtoranta, J., Ekholm, P., and Pitkanen, H.: Coastal eutrophication
thresholds: a matter of sediment microbial processes, Ambio, 38, 303–308,
10.1579/09-A-656.1, 2009.Leruste, A., Malet, N., Munaron, D., Derolez, V., Hatey, E., Collos, Y., De
Wit, R., and Bec, B.: First steps of ecological restoration in Mediterranean
lagoons: Shifts in phytoplankton communities, Estuar. Coast. Shelf S., 180,
190–203, 10.1016/j.ecss.2016.06.029, 2016.Lie, A. A., Wong, C. K., Lam, J. Y., Liu, J. H., and Yung, Y. K.: Changes in
the nutrient ratios and phytoplankton community after declines in nutrient
concentrations in a semi-enclosed bay in Hong Kong, Mar. Environ. Res., 71,
178–188, 10.1016/j.marenvres.2011.01.001, 2011.
Loyer, S., Lampert, L., Menesguen, A., Cann, P., and Labasque, T.: Seasonal
evolution of the nutrient pattern on Biscay Bay continental shelf over the
years 1999-2000, Sci. Mar., 70, 31–46, 2006.Lunven, M., Guillaud, J. F., Youénou, A., Crassous, M. P., Berric, R., Le
Gall, E., Kérouel, R., Labry, C., and Aminot, A.: Nutrient and
phytoplankton distribution in the Loire River plume (Bay of Biscay, France)
resolved by a new Fine Scale Sampler, Estuar. Coast. Shelf S., 65, 94–108,
10.1016/j.ecss.2005.06.001, 2005.
Ménesguen, A. and Dussauze, M.: Détermination des “bassins
récepteurs” marins des principaux fleuves français de la façade
Manche-Atlantique, et de leurs rôles respectifs dans l'eutrophisation
phyto-planctonique des masses d'eau DCE et des sous-régions DCSMM. Phase
1 (2013): Calcul de scénarios optimaux à partir des “bassins
récepteurs”. Phase 2 (2014): Simulation de scénarios imposés et
des scénarios optimaux, 334 pp., Ifremer, Brest, France, 2015 (in
French).Ménesguen, A., Desmit, X., Duliere, V., Lacroix, G., Thouvenin, B.,
Thieu, V., and Dussauze, M.: How to avoid eutrophication in coastal seas? A
new approach to derive river-specific combined nitrate and phosphate maximum
concentrations, Sci. Total Environ., 628–629, 400–414,
10.1016/j.scitotenv.2018.02.025, 2018a.Ménesguen, A., Dussauze, M., and Dumas, F.: Designing optimal scenarios
of nutrient loading reduction in a WFD/MSFD perspective by using passive
tracers in a biogeochemical-3D model of the English Channel/Bay of Biscay
area, Ocean Coast. Manage., 163, 37–53, 10.1016/j.ocecoaman.2018.06.005,
2018b.Ménesguen, A., Dussauze, M., Dumas, F., Thouvenin, B., Garnier, V.,
Lecornu, F., and Répécaud, M.: Ecological model of the Bay of Biscay
and English Channel shelf for environmental status assessment part 1:
Nutrients, phytoplankton and oxygen, Ocean Model., 133, 56–78,
10.1016/j.ocemod.2018.11.002, 2019.
Merceron, M.: Impact du barrage d'Arzal sur la qualité des eaux de
l'estuaire et de la baie de la Vilaine, 31 pp., Ifremer, Brest, France, 1985
(in French).Meybeck, M., Cauwet, G., Dessery, S., Somville, M., Gouleau, D., and Billen,
G.: Nutrients (organic C, P, N, Si) in the eutrophic River Loire (France) and
its estuary, Estuar. Coast. Shelf S., 27, 595–624,
10.1016/0272-7714(88)90071-6, 1988.Middelburg, J. J. and Nieuwenhuize, J.: Uptake of dissolved inorganic
nitrogen in turbid, tidal estuaries, Mar. Ecol.-Prog. Ser., 192, 79–88,
10.3354/meps192079, 2000.Middelburg, J. J., Klaver, G., Nieuwenhuize, J., Wielemaker, A., de Haas, W.,
Vlug, T., and van der Nat, J.: Organic matter mineralization in intertidal
sediments along an estuarine gradient, Mar. Ecol.-Prog. Ser., 132, 157–168,
10.3354/meps132157, 1996.Minaudo, C., Meybeck, M., Moatar, F., Gassama, N., and Curie, F.:
Eutrophication mitigation in rivers: 30 years of trends in spatial and
seasonal patterns of biogeochemistry of the Loire River (1980–2012),
Biogeosciences, 12, 2549–2563, 10.5194/bg-12-2549-2015,
2015.
Moatar, F. and Dupont, N.: La Loire Fluviale et Estuarienne – Un Milieu en
Évolution, 320 pp., Éditions Quae, Versailles, France, 2016.Molenat, J. and Gascuel-Odoux, C.: Modelling flow and nitrate transport in
groundwater for the prediction of water travel times and of consequences of
land use evolution on water quality, Hydrol. Process., 16, 479–492,
10.1002/hyp.328, 2002.
OSPAR: Eutrophication Status of the OSPAR Maritime Area, 166 pp., OSPAR
Commission, London, UK, 2017.Paerl, H. W.: Controlling eutrophication along the freshwater–marine
continuum: dual nutrient (N and P) reductions are essential, Estuar. Coast.,
32, 593–601, 10.1007/s12237-009-9158-8, 2009.Paerl, H. W.: Why does N-limitation persist in the world's marine waters?,
Mar. Chem., 206, 1–6, 10.1016/j.marchem.2018.09.001, 2018.Paerl, H. W., Valdes, L. M., Joyner, A. R., Piehler, M. F., and Lebo, M. E.:
Solving problems resulting from solutions: evolution of a dual nutrient
management strategy for the eutrophying Neuse River Estuary, North Carolina,
Environ. Sci. Technol., 38, 3068–3073, 10.1021/es0352350, 2004.Paerl, H. W., Scott, J. T., McCarthy, M. J., Newell, S. E., Gardner, W. S.,
Havens, K. E., Hoffman, D. K., Wilhelm, S. W., and Wurtsbaugh, W. A.: It
takes two to tango: When and where dual nutrient (N & P) reductions are
needed to protect lakes and downstream ecosystems, Environ. Sci. Technol.,
50, 10805–10813, 10.1021/acs.est.6b02575, 2016.Petris, G.: An R package for dynamic linear models, J. Stat. Softw., 36,
1–16, 10.18637/jss.v036.i12, 2010.Pitkänen, H., Lehtoranta, J., and Raike, A.: Internal nutrient fluxes
counteract decreases in external load: the case of the estuarial eastern Gulf
of Finland, Baltic Sea, Ambio, 30, 195–201,
10.1579/0044-7447-30.4.195, 2001.Poisvert, C., Curie, F., and Moatar, F.: Annual agricultural N surplus in
France over a 70-year period, Nutr. Cycl. Agroecosys., 107, 63–78,
10.1007/s10705-016-9814-x, 2016.Racault, M. F., Sathyendranath, S., Menon, N., and Platt, T.: Phenological
responses to ENSO in the global oceans, Surv. Geophys., 38, 277–293,
10.1007/s10712-016-9391-1, 2017.Radach, G. and Pätsch, J.: Variability of continental riverine freshwater
and nutrient inputs into the North Sea for the years 1977–2000 and its
consequences for the assessment of eutrophication, Estuar. Coast., 30,
66–81, 10.1007/bf02782968, 2007.
Ratmaya, W.: Rôle des sédiments dans le cycle des nutriments et
impacts sur l'eutrophisation des écosystèmes côtiers, PhD Thesis,
Université de Nantes, 212 pp., 2018 (in French).R Development Core Team: R: A Language and Environment for Statistical
Computing. R Foundation for Statistical Computing, Vienna, Austria, available
at: https://www.R-project.org/ (last access: 15 June 2016), 2016.
Redfield, A. C.: The biological control of chemical factors in the
environment, Am. Sci., 46, 205–221, 1958.REPHY: REPHY dataset – French Observation and Monitoring program for
Phytoplankton and Hydrology in coastal waters, 1987–2016 Metropolitan data,
10.17882/47248, 2017.Rochet, M., Trenkel, V., Bellail, R., Coppin, F., Lepape, O., Mahe, J.,
Morin, J., Poulard, J., Schlaich, I., and Souplet, A.: Combining indicator
trends to assess ongoing changes in exploited fish communities: diagnostic of
communities off the coasts of France, ICES J. Mar. Sci., 62, 1647–1664,
10.1016/j.icesjms.2005.06.009, 2005.Romero, E., Garnier, J., Lassaletta, L., Billen, G., Le Gendre, R., Riou, P.,
and Cugier, P.: Large-scale patterns of river inputs in southwestern Europe:
seasonal and interannual variations and potential eutrophication effects at
the coastal zone, Biogeochemistry, 113, 481–505,
10.1007/s10533-012-9778-0, 2013.Romero, E., Le Gendre, R., Garnier, J., Billen, G., Fisson, C., Silvestre,
M., and Riou, P.: Long-term water quality in the lower Seine: Lessons learned
over 4 decades of monitoring, Environ. Sci. Policy, 58, 141–154,
10.1016/j.envsci.2016.01.016, 2016.Ryther, J. H. and Dunstan, W. M.: Nitrogen, phosphorus, and eutrophication in
the coastal marine environment, Science, 171, 1008–1013,
10.1126/science.171.3975.1008, 1971.Scheuerell, M. D., Schindler, D. E., Litt, A. H., and Edmondson, W. T.:
Environmental and algal forcing of Daphnia production dynamics,
Limnol. Oceanogr., 47, 1477–1485, 10.4319/lo.2002.47.5.1477, 2002.Schindler, D. W.: The dilemma of controlling cultural eutrophication of
lakes, P. Roy. Soc. B-Biol. Sci., 279, 4322–4333,
10.1098/rspb.2012.1032, 2012.Schindler, D. W., Hecky, R. E., Findlay, D. L., Stainton, M. P., Parker, B.
R., Paterson, M. J., Beaty, K. G., Lyng, M., and Kasian, S. E.:
Eutrophication of lakes cannot be controlled by reducing nitrogen input:
results of a 37-year whole-ecosystem experiment, P. Natl. Acad. Sci. USA,
105, 11254–11258, 10.1073/pnas.0805108105, 2008.Schindler, D. W., Carpenter, S. R., Chapra, S. C., Hecky, R. E., and Orihel,
D. M.: Reducing phosphorus to curb lake eutrophication is a success, Environ.
Sci. Technol., 50, 8923–8929, 10.1021/acs.est.6b02204, 2016.Seitzinger, S., Harrison, J. A., Bohlke, J. K., Bouwman, A. F., Lowrance, R.,
Peterson, B., Tobias, C., and Van Drecht, G.: Denitrification across
landscapes and waterscapes: a synthesis, Ecol. Appl., 16, 2064–2090,
10.1890/1051-0761(2006)016[2064:DALAWA]2.0.CO;2, 2006.
Soetaert, K. and Middelburg, J. J.: Modeling eutrophication and
oligotrophication of shallow-water marine systems: the importance of
sediments under stratified and well-mixed conditions, in: Eutrophication in
Coastal Ecosystems, edited by: Andersen, J. H. and Conley, D. J.,
Developments in Hydrobiology, Springer, the Netherlands, 239–254, 2009.Søndergaard, M., Jeppesen, E., Lauridsen, T. L., Skov, C., Van Nes, E. H.,
Roijackers, R., Lammens, E., and Portielje, R. O. B.: Lake restoration:
successes, failures and long-term effects, J. Appl. Ecol., 44, 1095–1105,
10.1111/j.1365-2664.2007.01363.x, 2007.Souchu, P., Vaquer, A., Collos, Y., Landrein, S., Deslous-Paoli, J. M., and
Bibent, B.: Influence of shellfish farming activities on the biogeochemical
composition of the water column in Thau lagoon, Mar. Ecol.-Prog. Ser., 218,
141–152, 10.3354/meps218141, 2001.Soudant, D., Beliaeff, B., and Thomas, G.: Explaining Dinophysis cf.
acuminata abundance in Antifer (Normandy, France) using dynamic linear
regression, Mar. Ecol.-Prog. Ser., 156, 67–74, 10.3354/meps156067, 1997.Sournia, A., Chrdtiennot-Dinet, M. J., and Ricard, M.: Marine phytoplankton:
how many species in the world ocean?, J. Plankton. Res., 13, 1093–1099,
10.1093/plankt/13.5.1093, 1991.Statham, P. J.: Nutrients in estuaries – an overview and the potential
impacts of climate change, Sci. Total Environ., 434, 213–227,
10.1016/j.scitotenv.2011.09.088, 2012.
Tamminen, T. and Andersen, T.: Seasonal phytoplankton nutrient limitation
patterns as revealed by bioassays over Baltic Sea gradients of salinity and
eutrophication, Mar. Ecol.-Prog. Ser., 340, 121–138, 10.3354/meps340121,
2007.Taylor, C., Pedregal, D., Young, P., and Tych, W.: Environmental time series
analysis and forecasting with the Captain toolbox, Environ. Modell. Softw.,
22, 797–814, 10.1016/j.envsoft.2006.03.002, 2007.Thackeray, S. J., Jones, I. D., and Maberly, S. C.: Long-term change in the
phenology of spring phytoplankton: species-specific responses to nutrient
enrichment and climatic change, J. Ecol., 96, 523–535,
10.1111/j.1365-2745.2008.01355.x, 2008.Traini, C., Proust, J. N., Menier, D., and Mathew, M. J.: Distinguishing
natural evolution and human impact on estuarine morpho-sedimentary
development: A case study from the Vilaine Estuary, France, Estuar. Coast.
Shelf S., 163, 143–155, 10.1016/j.ecss.2015.06.025, 2015.
Utermöhl, H.: Zur Vervollkommnung der quantitativen
Phytoplankton-Methodik, Mitteilungen Internationale Vereinigung Theoretische
und Angewandte Limnologie, 9, 1–38, 1958.Vannote, R. L., Minshall, G. W., Cummins, K. W., Sedell, J. R., and Cushing,
C. E.: The river continuum concept, Can. J. Fish Aquat. Sci., 37, 130–137,
10.1139/f80-017, 1980.Wang, B., Xin, M., Wei, Q., and Xie, L.: A historical overview of coastal
eutrophication in the China Seas, Mar. Pollut. Bull., 136, 394–400,
10.1016/j.marpolbul.2018.09.044, 2018.
Weckström, K., Korhola, A., and Weckström, J.: Impacts of
eutrophication on diatom life forms and species richness in coastal waters of
the Baltic Sea, Ambio, 36, 155–160, 2007.
West, M. and Harrison, J.: Bayesian Forecasting and Dynamic Models, 2nd Edn.,
Springer Series in Statistics, Springer-Verlag, New York, 682 pp., 1997.Yamamoto, T.: The Seto Inland Sea – eutrophic or oligotrophic?, Mar. Pollut.
Bull., 47, 37–42, 10.1016/S0025-326X(02)00416-2, 2003.Yue, S. and Wang, C. Y.: The Mann-Kendall test modified by effective sample
size to detect trend in serially correlated hydrological series, Water
Resour. Manag., 18, 201–218, 10.1023/B:Warm.0000043140.61082.60, 2004.Yung, Y. K., Wong, C. K., Broom, M. J., Ogden, J. A., Chan, S. C. M., and
Leung, Y.: Long-term changes in hydrography, nutrients and phytoplankton in
Tolo Harbour, Hong Kong, Hydrobiologia, 352, 107–115,
10.1023/a:1003021831076, 1997.