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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.
* 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
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
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
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
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
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