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ecological indicators 9 (2009) 982–991

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Simple tools for assessing water quality and trophic status in


transitional water ecosystems

G. Giordani a,*, J.M. Zaldı́var b, P. Viaroli a


a
Department of Environmental Sciences, University of Parma, Via Usberti 11/A, I-43100 Parma, Italy
b
European Commission, Joint Research Centre, Institute for Health and Consumer Protection, Via E. Fermi 2749, TP 272. I-21027 Ispra
(VA), Italy

article info abstract

Article history: In this study we have developed an index for assessing trophic status and water quality in
Received 4 March 2008 transitional aquatic ecosystems of Southern Europe. The index has been developed from the
Received in revised form water quality index of the U.S. National Sanitation Foundation and integrates the main
10 November 2008 causal factors (inorganic nutrients), the key biological elements (primary producers) and
Accepted 12 November 2008 indicator of effects (oxygen) of eutrophication. Six main variables have been used: relative
coverage of benthic phanerogams and opportunistic macroalgae species, and concentra-
tions of dissolved oxygen, phytoplankton chlorophyll-a, dissolved inorganic nitrogen and
Keywords: phosphorus. Non-linear functions are used to transform each measured variable into its
Phanerogams quality value. Each quality value is then multiplied by a weighting factor, to take into
Opportunistic macroalgae account the relative contribution of each variable to the overall water quality. Finally, the
Phytoplankton chlorophyll-a index value is calculated as the sum of the weighted quality values, ranging from 0 (poorest
Nutrients state) to 100 (best condition). The index has been tested and validated in six transitional
Oxygen water ecosystems which differ in anthropogenic pressures and eutrophication levels, for
Water quality index which data sets were available from 1989 to 2004: Sacca di Goro (Northern Adriatic Sea, Italy),
Lesina Lagoon (Southern Adriatic Sea, Italy), Ria Formosa (Algarve, Southern Portugal), Mar
Menor (Murcia, Southern Spain), Etang de Thau (Herault, Southern France) and Gulf of Gera
(Lesvos Island, Greece). The index assessments have been compared with evaluations from
the IFREMER (French Research Institute for the Exploitation of the Sea) classification scheme
(France) and the trophic index TRIX (Italy), which are currently used for national monitoring
of coastal waters and lagoons. Based on the conclusions of this study we suggest to use the
index for monitoring water quality in shallow coastal transitional waters, where benthic
vegetation controls primary productivity, which makes indices based on phytoplankton
only (e.g., TRIX) unsuitable.
# 2008 Elsevier Ltd. All rights reserved.

1. Introduction 2008). Nonetheless, little attention has been given to the


development of specific tools for transitional waters (TW),
Several indicators and indices are available for assessing despite their ecological and economical importance (Basset
trophic status and quality of aquatic ecosystems and their et al., 2006). TW comprise shallow aquatic ecosystems, which
evolution under different anthropogenic pressures and inher- are highly dynamic and heterogeneous (McLusky and Elliott,
ent threats (Jørgensen et al., 2005; Niemeijer and de Groot, 2007), thus indicators and indices developed for deeper

* Corresponding author. Tel.: +39 0521 905976; fax: +39 0521 905402.
E-mail address: giordani@nemo.unipr.it (G. Giordani).
1470-160X/$ – see front matter # 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecolind.2008.11.007
ecological indicators 9 (2009) 982–991 983

ecosystems (e.g., coastal marine waters and lakes) are (Portugal), Mar Menor (Spain) and Gulf of Gera (Greece). The
unsuitable for monitoring TW. Furthermore, the existing tools TWQI assessments were then compared with the evaluations
specific for TW are generally currently under new develop- from the IFREMER (French Research Institute for the Exploita-
ment or their validity is restricted to areas/habitats where they tion of the Sea) classification scheme and the TRIX index,
have been developed (Jørgensen et al., 2005; Magni et al., 2005). considering also other eight French Mediterranean lagoons
The implementation of the Water Framework Directive described by Souchu et al. (2000).
(WFD) in the European Union is supporting the development of
assessment tools specific for TW, here considered as an
ecosystem distinct from coastal waters (McLusky and Elliott, 2. Materials and methods
2007) and from which they have to be evaluated separately for
their ecological and chemical status (Borja, 2005). TW 2.1. Assumptions and metrics of Transitional Water
monitoring requires indicators and descriptors that incorpo- Quality Index (TWQI)
rate the specific ecosystem features, mainly shallowness and
degree of confinement. Moreover, they have to consider TWQI was implemented using six variables, namely: dissolved
ecosystem status and vulnerability to specific perturbations oxygen (DO), phytoplankton chloropyll-a (Chl-a), dissolved
such as nutrient loadings, contamination of toxic compounds inorganic nitrogen (DIN) and phosphorus (DIP) concentrations
and resource exploitation, e.g., aquaculture (Rice, 2003). plus coverage of benthic phanerogams (Ph) and opportunistic
Presently, aggregated indices would meet most of above macroalgae (Ma) species. These variables represent the main
criteria, depending on the selected variables and algorithms causal factors (inorganic nutrients), the key biological ele-
used in the integration processes. Among them, a series of ments (primary producers) and indicator of effects (oxygen) of
water quality indices (WQIs) have been developed for aquatic eutrophication and water quality in shallow transitional
ecosystems in which simple quality vectors are obtained from waters (Vollenweider et al., 1998; Orfanidis et al., 2003; Viaroli
several measured variables (Štambuk-Giljanović, 1999; Cude, et al., 2008). As for the other WQIs, non-linear functions were a
2001). WQIs are user-friendly and can be easily handled in priori established and applied to transform each measured
automatic systems and computational tools (Mocenni et al., in variable into its quality value (QV). Each QV was then
press). multiplied by a weighting factor, to take into account the
The idea to use an integrated index that reflects the relative contribution of each variable to the overall water
composite influence of significant variables on water quality quality. Both utility functions and weighting factor were
was firstly proposed by Brown et al. (1970) and later improved derived from literature and expert assessment. Finally, TWQI
by the National Sanitation Foundation (McClelland, 1974). This was calculated as the sum of the weighted QVs, ranging from 0
index, called the National Sanitation Foundation Water (poorest state) to 100 (best condition).
Quality Index (NSFWQI), is actually used for water quality The QV assigned to DO (QVDO) increased from 0 to 100,
monitoring of different U.S. water supplies. Recently, many spanning complete anoxia to 100–125% oxygen saturation
different types of WQIs have been developed but there is still a (Fig. 1a). DO values higher than 125%, common in highly
need to develop new WQIs based on fewer variables which can productive transitional ecosystems, were also considered
be used to compare sites with similar water quality char- critical, since oversaturation is often coupled to phytoplank-
acteristics (Said et al., 2004). ton or macroalgal biomass accumulation. The accumulated
Vollenweider et al. (1998) developed a trophic index (TRIX) biomass fuels respiration processes, which in turn can lead to
which integrates oxygen saturation, phytoplankton chloro- complete anoxia (Viaroli and Christian, 2003). Therefore, at
phyll-a, nitrogen and phosphorus concentrations to assess the oxygen saturation greater than 125%, QVDO decreased with
trophic state of coastal marine waters, this is presently also QVDO = 0 at 250%, according to previous studies (Vollenweider
applied to coastal lagoons. TRIX is founded on the assumption et al., 1998; Štambuk-Giljanović, 1999; Cude, 2001).
that eutrophication processes depend primarily on phyto- Chl-a is a measure of the active phytoplankton biomass,
plankton community, and assumes the reference system although the cellular Chl-a content is often species-specific
proposed by Vollenweider et al. (1992) and Nixon (1995). and depends on the physiological status of phytoplankton
Pettine et al. (2007) recently developed a new TRIX version in cells (Felip and Catalan, 2000). In this study, we used
order to fulfil the WFD requirements for marine coastal waters thresholds and fixed boundaries from common classification
dominated by phytoplankton. In the last few years, other criteria for eutrophication (Vollenweider and Kerekes, 1982).
multi-metric indices were developed including benthic com- QVchla = 0 was attained at concentrations Chl-a > 30 mg m 3,
ponents, however, they required high numbers of variables to whilst optimal conditions (QVchla = 100) were assigned to Chl-
be measured. A comprehensive review on indicators and tools a < 6 mg m 3 (Fig. 1b). The concentration range proposed here
for assessing eutrophication and water quality in transitional is typical of Mediterranean coastal lagoons and continental
aquatic ecosystems is reported by Zaldı́var et al. (2008). estuaries (Giordani et al., 2005; EPA, 2005).
In the present study, we implemented an index that is DIN and DIP concentrations result from external loadings
tailored for transitional ecosystems, adopting the WQI and internal recycling and have been widely used as criteria
approach: the Transitional Water Quality Index (TWQI). The for assessing trophic status in lentic water bodies (Vollen-
TWQI approach has been tested and validated at different weider and Kerekes, 1982). DIN is now recognised as the
temporal and spatial scales in six transitional water ecosys- main driver of coastal eutrophication, whilst DIP is often
tems which differ in levels of eutrophication: Sacca di Goro assumed as the main limiting factor (de Jonge et al., 2002;
and Lesina lagoons (Italy), Etang de Thau (France), Ria Formosa Howarth and Marino, 2006). For this reason, simple models
984 ecological indicators 9 (2009) 982–991

have been developed which allow for estimating the net Moreover, other classification schemes report DIN = 20 mM
ecosystem metabolism from DIP as a measures of lagoon as a critical threshold for coastal lagoons (Souchu et al.,
trophic potential (Giordani et al., 2008a). Utility functions for 2000; EPA, 2005). A similar utility function was set for DIP,
DIN and DIP were established considering the main criteria with QVDIP = 100 at DIP = 0 mM and QVDIP = 0 at DIP > 6 mM
for trophic status classification (Vollenweider and Kerekes, (Fig. 1d). The use of total nitrogen (TN) and phosphorus (TP),
1982; Vollenweider et al., 1998). QVDIN was assumed to be in place of DIN and DIP, would be recommended if such data
inversely related to DIN concentrations with QVDIN = 100 at are available, because dissolved organic and particulate
DIN = 0 mM and QVDIN = 0 at DIN > 100 mM (Fig. 1c). The most species can greatly contribute to the nitrogen and phos-
significant decrease of QVDIN was imposed in the 0–20 mM phorus bulk. Utility functions for TN and TP follow similar
range, because the main transformation in the productivity patterns as for DIN and DIP, except for the wider ranges
assets usually occurs within this range (Viaroli et al., 2008). (Fig. 1c and d).

Fig. 1 – Relationships among analytical measurements of (a) dissolved oxygen saturation (DO), (b) chlorophyll-a (Chl-a), (c)
dissolved inorganic and total nitrogen (DIN-TN), (d) dissolved inorganic and total phosphorus (DIP-TP), (e) macroalgal
coverage (Ma), (f) phanerogam coverage (Ph) and respective TWQI Q values (QV). wf: weighting factors used in TWQI
calculation.
ecological indicators 9 (2009) 982–991 985

Table 1 – Trophic state, geographical and morphometric data of the TW ecosystems considered in this study. t: theoretical
water residence time.
System Country Symbol Latitude t (d) Area Mean Trophic Reference
and longitude (km2) depth (m) level

Sacca di Goro Italy SG 44.78–44.848N 3 26 1.5 Very high Viaroli et al. (2006)
12.26–12.398E

Lagoon of Lesina Italy LE 41.85–41.928N 100 52 0.8 Low Manini et al. (2005)
15.31–15.578E

Ria Formosa Portugal RF 36.96–37.168N 1 105 3.5 Medium Newton and


Mudge (2005)
08.25–07.518W

Mar Menor Spain MM 37.63–37.828N 190 135 3.6 High Pérez-Ruzafa


et al. (2005)
00.72–00.868W

Etang du Thau France ET 43.33–43.468N 56 75 4.5 Medium Plus et al. (2006)


03.53–03.708E

Gulf of Gera Greece GG 39.00–39.128N 8 43 10 Very low Arhonditsis et al. (2003)


26.44–26.538E

The main functional groups of the benthic vegetation the main driver of the lagoon water quality and trophic status
community and their relative coverage were considered for (Viaroli et al., 2008). A lower weight (0.15) was used for
TWQI, assuming that each of them was associated with phytoplankton chlorophyll-a, phytoplankton being less
different stages of the eutrophication development in TW important due to the shallow depth. Also DO was rated with
(Orfanidis et al., 2003; Nielsen et al., 2004; Hauxwell and 0.15, assuming that it depends primarily on benthic vegetation
Valiela, 2004). The general assumption was that phanerogams and phytoplankton. The lowest weight (0.12) was assigned to
prevailed in pristine and unaltered ecosystems, whilst dissolved nutrients, as they represent the causal factor of
opportunistic macroalgae species became dominant in vegetation status rather than a direct estimate of trophic
eutrophic and dystrophic TW (Schramm, 1999; Viaroli et al., status and water quality. DIN and DIP concentrations are also
2008). The opportunistic macroalgae species considered in this linked to several biogeochemical processes.
study were among those listed in the ESGII group of the TWQI was then obtained as the sum of weighted QVs. The
Ecological Evaluation Index (Orfanidis et al., 2003). We sum was considered more appropriate than the unweighted
considered the presence and abundance of the functional harmonic mean (Cude, 2001), because QVs close to zero – as
groups as sufficient to discriminate the trophic status, often occurs for QVMa or QVPh – can result in unsuitable values
although we recognize that the eco-physiological conditions (TWQI < 1).
of benthic vegetation could add information on buffering
capacity, resistance and resilience of benthic community 2.2. Data sources for TWQI testing
(Juanes et al., 2008). The coverage by macroalgae and
phanerogams (Ph) was expressed as % of surface area TWQI was tested in six coastal lagoons in the Southern
colonised by a permanent meadow/stand using an ordinal European Arc, which differ in trophic status and water quality,
transform scale based on an extended Braun-Blanquet cover- namely Sacca di Goro (SG), Lagoon of Lesina (LE), Etang du
abundance scale (Braun-Blanquet, 1964). Both macroalgae and Thau (ET), Ria Formosa (RF), Mar Menor (MM) and Gulf of Gera
phanerogams are known to out-compete phytoplankton, thus (GG) (Table 1).
measures of their density and biomass were considered as A detailed analysis of spatial and temporal variations of
complementary to Chl-a measurements. Furthermore, we TWQI was performed in SG. Complete datasets for TWQI
assumed that the maximum coverage by benthic vegetation applications to the whole SG were available for seven periods
could not exceed 80% of the total lagoon surface, 20% being from 1991 to 1994. QVs were obtained from averages of
accounted for as unsuitable areas, e.g. deep canals, intertidal variables measured at eight stations representative of the
mudflats, etc. For this reason, QVMa = 0 was assigned to a lagoon (Colombo et al., 1994) and benthic vegetation coverage
macroalgal coverage >80% (Fig. 1e). Conversely, the highest was obtained from Viaroli et al. (2006).
QVMa was assigned to a coverage range <10%, assuming that A more detailed analysis of the seasonal evolution of TWQI
small amounts of opportunistic macroalgae can be found in SG was performed for a fixed station (st. 17) located in the
under pristine conditions. The utility function representing confined eastern sub-basin of the lagoon where huge blooms
phanerogam coverage was set symmetric of that of macro- of floating macroalgae occurred (Viaroli et al., 2006).
algae, with QVPh = 100 corresponding to 80% coverage, and TWQI and TRIX responses were tested and compared with
QVPh = 0 at 0–10% coverage (Fig. 1f). the 0D biogeochemical model developed for SG by Zaldı́var
Weighing factors were selected based on the ecological et al. (2003a,b). Simulations were run with input data from
relevance of the considered variables. The highest values (0.23) 1997, which represented the average meteorological condi-
were set for benthic vegetation, assuming that it represented tions, nutrient loads and water flushing values of the last two
986 ecological indicators 9 (2009) 982–991

decades (Viaroli et al., 2005, 2006). Additional data were


provided by the Regional Environmental Protection Agency
(http://www.arpa.emr.it) and the Coastal Waters and Fishery
unit of the Province of Ferrara (http://www.provincia.fe.it/
acquecostiere).
In spring and summer 2004, TWQI was further compared
between SG and LE. Four stations were selected in each lagoon
in order to discriminate among the main pressures and
trophic conditions (Giordani et al., 2008b). In LE, station LE1
was close to the town of Lesina, and had bare sediment with
high nutrient concentrations in the water column. Station LE2
was mainly influenced by marine water inflow. Stations LE3
and LE4 were colonized by dense meadows of Zostera noltii and
Ruppia cirrhosa. In SG lagoon, station SG1 was located in the
plume zone of the Po di Volano river, station SG2 was in the Fig. 2 – TWQI values estimated for the whole Sacca di Goro
central part of the lagoon, where mussel farming was Lagoon on 18/6/91, 27/11/91, 5/5/92, 27/10/92, 24/11/93, 16/
performed until 2002, station SG3 was close to the sea mouth 3/94, 7/6/94. Legend as Fig. 1.
in a sandy area exploited for clam farming, and station SG4
was located in a sheltered and muddy-sand zone impacted by
both clam farming and macroalgal blooms. classification scheme and the French lagoons considered in
A wider comparison was performed among LE, SG, RF, MM, this study are reported by Souchu et al. (2000).
ET and GG. The data source for the latter five lagoons was the
EU-funded DITTY project (Aliaume et al., 2007; Giordani et al.,
2008b; Table 1). 3. Results
Relationships between TWQI and IFREMER quality scheme
and TWQI and TRIX were analysed for RF, MM, ET, SG, GG and 3.1. TWQI estimations in the Sacca di Goro lagoon
for additional 13 sites in 8 coastal lagoons located in the
Southern Mediterranean French coast, namely: Etang de l’Or The TWQI evaluation of the whole SG lagoon for the 1991–1994
(E, W), Grec, Ingril (N, S), Bages (N, C, S), Campignol, l’Ayrolle, period is shown in Fig. 2. TWQI spanned 39–48 in the May–June
Gruissan and Leucate (N, S). Details on the IFREMER periods when macroalgal blooms occurred. Values slightly

Fig. 3 – Seasonal evolution of (a) dissolved oxygen (DO), (b) phytoplankton chlorophyll-a (Chl-a), (c) dissolved inorganic
nitrogen (DIN), (d) dissolved inorganic phosphorus (DIP), (e) macroalgal coverage (Ma) and the respective Q values at station
17 of the Sacca di Goro lagoon from 1990 to 1992. (f) comparison between TWQI estimations based on dissolved inorganic
nitrogen and phosphorus (DIN,DIP) and total nitrogen and phosphorus (TN,TP).
ecological indicators 9 (2009) 982–991 987

essential dynamics of the water quality and trophic status.


Water quality varied seasonally with 25 < TWQI < 75. The
lowest values were detected in early summer each year.
Overall, these findings conformed to previous assessments
achieved with conventional descriptors, namely community
productivity and respiration (Viaroli and Christian, 2003;
Viaroli et al., 2005) and sedimentary biogeochemical indicators
(Azzoni et al., 2005; Giordani et al., 2008b).
The 0D model runs for 1997 also provided evidence that
under typical meteorological and hydrological conditions
TWQI ranged from 42 to 65 (Fig. 4), which was close to values
estimated from experimental data (Fig. 2). As usual, the lowest
TWQI occurred in June, during the early phase of the
dystrophic outbreak (Viaroli et al., 2005). QVMa, QVcha and
Fig. 4 – Annual evolution of Ulva coverage, TWQI and TRIX
QVDO were the main drivers of water quality in the lagoon.
values simulated with the 0D model of Zaldı́var et al.
QVMa and QVcha were complementary, whilst QVDO was
(2003a,b) for a normal year in the Sacca di Goro lagoon.
mainly associated with QVMa.
The TRIX scale is reversed to have higher quality values
upwards for both indexes.
3.2. TWQI application to lagoons with different
eutrophication levels
higher (60 < TWQI < 64) were found in the other periods.
TWQI was very sensitive to macroalgal blooms, whilst The comparison of SG and LE provide evidence of clear
phanerogams had negligible effects, as they have nearly differences between lagoons, with 40 < TWQI < 70 in SG and
disappeared since the late 80s. QVs of the other variables TWQI > 70 in LE, in agreement with the expected trophic status
underwent opposite patterns. The lowest QVDIN and QVDIP of the two ecosystems (Fig. 5; Table 1). Differences between
were attained in autumn and winter (i.e., highest concentra- lagoons were greater in summer, when in SG TWQI decreased to
tions), whilst DO and Chl-a had low QVs in spring and 40 at SG1, SG2 and SG4, due to phytoplankton and Ulva blooms,
summer. whilst at SG3, TWQI was almost constant, likely due to marine
The contribution of individual QVs to TWQI and their water flushing. In LE, no seasonal differences were found, whilst
timing over three years (1990–1992) were analyzed at station 17 within-lagoon differences were observed with lower TWQI at
in SG (Fig. 3). Overall, TWQI was driven by macroalgal biomass, LE1 and LE2, these stations receiving sewage from the urban
with water quality deterioration during bloom events and area of Lesina, and TWQI peaks up to 98 at LE3 and LE4, where
subsequent dystrophic outbreaks. The total TWQI was kept large meadows of benthic phanerogams developed out-com-
low by QVMa in spring and by QVDO and QVDIP in early summer. peting phytoplankton and leading to oxygen saturation.
Summer phytoplankton blooms also affected TWQI with The sensitivity of TWQI was assessed through its applica-
QVchla close to zero. By contrast, in late autumn and winter, tion in six lagoons with a wide range of trophic conditions
TWQI was influenced by high DIN loadings with very low (Table 1). The highest TWQI were found in GG (TWQI = 99), RF
QVDIN. Basically, one can argue that TWQI responses to the (TWQI = 95) and LE (TWQI = 85), which conformed to hydro-
within system variability were robust and captured the dynamics and the healthy status of benthic vegetation (Fig. 5).

Fig. 5 – TWQI values in 4 stations of the SG in May (M) and August (A) 2004, in 4 stations of the LE in May (M) and July (J) 2004
and, in the right box, TWQI values based on annual mean values for RF in 1999 (RF99), MM in 1988 (MM88), ET in 1998
(ET98), SG in 1990–1993 (SG90-93) and GG in 1996 (GG96). Legend as Table 1.
988 ecological indicators 9 (2009) 982–991

Intermediate conditions were observed in ET (TWQI = 77),


which was assessed as mesotrophic, being colonized by large
meadows of Z. marina and Z. noltii, but with an increasing
impact of chlorophyceans (Plus et al., 2005). Lower TWQI was
estimated for MM (TWQI = 68) due to high DIP concentrations
and significant losses of benthic vegetation following the huge
development of the urban area, tourism and agriculture. The
worst conditions were found in SG (TWQI = 52), conforming to
the observations reported above.

4. Discussion and conclusions

4.1. Comparison of TWQI with other indices

TWQI was compared with the IFREMER classification scheme


and with TRIX index. The IFREMER classification scheme was
Fig. 7 – Relationships between TRIX and TWQI for systems
implemented as an operational tool to assess the eutrophica-
not colonized by benthic vegetation (bare) and colonized
tion level in French Mediterranean lagoons (Souchu et al.,
by macroalgae (Ma) or phanerogams (Ph) with coverage
2000). This tool adopted a classification grid with five classes,
>10%. Data relative to the systems considered in this study
spanning ‘‘very good’’ to ‘‘very bad’’, according to the EU Water
listed in Fig. 5. TRIX scale is reversed to have the higher
Framework Directive (2000/60/EC). The IFREMER tool com-
quality values upwards for both indexes.
prises of 21 descriptors referring to phytoplankton, macro-
phytes, macro-zoobenthos, sediment and water column. A
simplified version was also developed and applied to the
lagoons listed in Table 1, except for LE (Austoni et al., 2004). On with the lowest quality (Fig. 6). Once again, differences
average TWQI was directly comparable with the IFREMER between tools depended on the different metrics, the IFREMER
quality classes, with RF as an exception, it being only included approach being more restrictive and driven by single variables,
in the IFREMER ‘‘sufficient’’ class, whereas, it obtained a high whilst TWQI was based on the integration of all the considered
TWQI value (Fig. 6). The IFREMER classification is based on the variables.
worst partial value among the descriptors mentioned above. TRIX integrates several state variables, mainly with linear
Although water quality was good on average, in summer metrics (Vollenweider et al., 1998). The main assumption is
ammonium concentrations significantly increased causing a that eutrophication depends primarily on phytoplankton
decrease from good to sufficient status (Duarte et al., 2007). A community (Vollenweider et al., 1992; Nixon, 1995). Therefore,
similar scenario was obtained by comparing summer TWQI TRIX and TWQI have similar data requirements, except for
with the IFREMER classification in 13 sites of 8 Mediterranean benthic vegetation, which is used only in TWQI, and Secchi
coastal lagoons (Souchu et al., 2000). A good agreement was depth which is used only in TRIX as an optional parameter.
found between IFREMER classes and TWQI, except for the sites Thus both indices can be applied using the same datasets with
some integrations. Responses of TRIX and TWQI show good
agreements for sites without benthic vegetation (bare sedi-
ments), whilst when benthic vegetation is present the two
indices give contrasting assessments, with TWQI peaks
coinciding with low TRIX values (Fig. 7). Basically, the
difference is due to the inclusion of benthic vegetation in
TWQI, which is not considered in TRIX, it being developed for
deep coastal waters rather than for shallow TW. In TW the
dominance of benthic vegetation within the primary producer
community can alter the TRIX response, due to oxygen
production and nutrient uptake by macroalgae (Viaroli and
Christian, 2003; Viaroli et al., 2005). For example, lagoons with
high Ulva biomass, which is detrimental for ecosystems
quality, can be rated as ‘‘good status’’ by TRIX due to high
Fig. 6 – Relationship between TWQI values and IFREMER oxygen, and low DIN and chlorophyll-a concentrations. TWQI,
quality classes estimated for DITTY sites from Austoni which includes macroalgal coverage as a negative factor, can
et al. (2004) and 13 sites of 8 Mediterranean French Coastal lead to the opposite status, capturing the community
lagoons for water column compartment in summer 1999, degeneration that can be caused by the occurrence of blooms
Souchu et al. (2000). IFREMER scheme classification ranges of opportunistic macroalgal species (Nielsen et al., 2004;
from 1 to 5 which correspond to bad (1), sufficient (2), Viaroli et al., 2008). The different responses of TWQI and TRIX
discrete (3), good (4) and very good (5) conditions. Legend can be more clearly shown using 0D model simulations
as Table 1. (Fig. 4). Whilst the TWQI signals a progressive water quality
ecological indicators 9 (2009) 982–991 989

deterioration following macroalgal growth, TRIX indicates an When using simple metrics, large and heterogeneous
improvement of water quality during the growth season of datasets are likely to be generated; thus the final assessment
macroalgae. Furthermore, TWQI seems to better represent the of environmental quality is often made considering large
most critical period when the macroalgal biomass begin to intervals of variation, thus loosing much of the detailed
decompose and dystrophic crisis have the highest probability information collected (Viaroli et al., 2004). This is particularly
of occuring. Also TRIX is less sensitive to changes driven by the true for TW ecosystems, as has been discussed above, where
benthic component of the system and remains rather constant few specific indicators are available and, where often, those
when the benthic community undergoes sudden changes due that have been developed in other types of water bodies (rivers
to the collapse of macroalgal stands. The main reason is that and coastal waters) are manipulated to be used in TW.
TRIX does not contain indicators of benthic metabolism, We believe that the use of simple indices such as TWQI are
which are included in TWQI. Due to its structure, which is meaningful for rapid assessments and repeated surveillance
tailored for benthic dominated TW, TWQI is less sensitive to programs rather than for highly detailed quality evaluations.
changes in nutrient and chlorophyll-a concentrations, which Detailed quality assessments require more sensitive tools,
can be induced by external inputs to TW. This behaviour effect which are clearly very difficult to apply at large scale and over
can be seen from late summer onwards when water quality is repeated surveys (because of the need of highly trained
mainly affected by DIN concentrations. specialists, expensive instrumentation and due to their
generally time consuming application). Finally rapid and
4.2. Reliability of TWQI for monitoring TW ecosystems simple assessment tools are especially useful in systems
having long time series of measurements of a few selected
TWQI seems suitable for monitoring eutrophication processes variables of high ecological relevance.
in transitional water ecosystems, where, due to the shallow
depth benthic vegetation controls primary productivity,
making ineffective indices based on phytoplankton only. Acknowledgements
TWQI integrates the main causal factors (inorganic nutrients),
the key biological elements (primary producers) and an This research was partially supported by the European
indicator of eutrophication effects (oxygen). The metrics we Commission under contract n8 EVK3-CT-2002-00084 ‘‘Devel-
have adopted are simple and allow the contribution of each opment of an Information Technology Tool for the Manage-
component of the index to be taken into account, thus ment of European Southern Lagoons under the influence of
capturing the intrinsic variability of each of them. The utility river-basin runoff (DITTY)’’ and by the Italian Ministry of
functions we adopted also consider the potential variability of Research and Education under the PRIN project ‘‘Nuovi
index components. For example, oxygen concentration is Indicatori di stato Trofico e d’Integrità ecologica Di Ambienti
extremely sensitive to temporal changes due to the natural marini costieri e ambienti di transizione (NITIDA)’’. We are
dynamics of primary productivity and community respiration very indebted to Nicholas Murray and the two anonymous
(Viaroli and Christian, 2003). Thus, instantaneous oxygen referees for reviewing and commenting on the manuscript.
concentrations are not suited for assessing the oxygenation
status of a given aquatic ecosystem. Nonetheless, concentra-
tions measured around mid-day may be considered as a good references
approximation of oxygen availability, as when oxygen
saturation is either low or very high, an oxygen deficit can
be predicted within the system (see Fig. 1a). Repeated Aliaume, C., Do Chi, T., Viaroli, P., Zaldı́var, J.M., (Eds.), 2007.
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et al., 2001; Viaroli et al., 2008). However, one has to avoid the using the IFREMER classification scheme for coastal
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