Use of microbenthic algal communities in ecotoxicological tests for the assessment of water quality: the Ter river case study
ABSTRACT The tolerance of microbenthic algal communities to two model toxicants, atrazine and copper, was studied in the Ter river during spring and summer. Artificial substrata were colonised at 9 sites and used to perform short-term (1-4 h) toxicity tests in the laboratory and to obtain photon yield as the ecotoxicological endpoint. The tolerance was lower in spring than in summer for both toxic substances and varied according to the site studied. Copper toxicity was associated with physico-chemical conditions (total suspended solids and water pH) and, especially, with several biomass-related parameters, whereas atrazine toxicity was related to algal abundance and species composition. Temporal and spatial changes in nutrient concentration may alter the biomass and species composition of the communities and thus affect their tolerance to toxic substances. It has to be therefore considered that the environmental characteristics of the river system may determine relevant direct and indirect effects on the algal communities, then affecting their specific ecotoxicological responses. Once this is assumed, the empirical expressions obtained on calculating EC50 and EC10 can be used to predict the community-level transient effects of toxic exposures.
- SourceAvailable from: Ali Akbar Jamali[Show abstract] [Hide abstract]
ABSTRACT: Introduction: Diatoms are single cell eukaryotic microalgae, which present in nearly every water habitat make them ideal tools for a wide range of applications such as oil exploration, forensic examination, environmental indication, biosilica pattern generation, toxicity testing and eutrophication of aqueous ecosystems. Methods: Essential information on diatoms were reviewed and discussed towards impacts of diatoms on biosynthesis and bioremediation. Results: In this review, we present the recent progress in this century on the application of diatoms in waste degradation, synthesis of biomaterial, biomineralization, toxicity and toxic effects of mineral elements evaluations. Conclusion: Diatoms can be considered as metal toxicity bioindicators and they can be applied for biomineralization, synthesis of biomaterials, and degradation of wastes.BioImpacts. 05/2012; 2(3-3).
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ABSTRACT: Diatoms are an integral and often dominant component of the benthic microalgal assemblage in estuarine and shallow coastal environments. Different toxic substances discharged into these ecosystems persist in the water, sediments, and biota for long periods. Among these pernicious agents, the toxicity in diatoms by metal is linked to different steps in the transmembrane and internal movements of the toxicant, causing perturbations in the normal structural and functional cellular components. These changes constitute an early, nontaxonomic warning signal that could potentially serve as an indicator of this type of pollution. The aim of this work was to study the environment-reflecting short-term responses at different levels of organization of epipsammic diatoms from the Río de la Plata estuary, Argentina that had been exposed to hexavalent chromium within experimental microcosms. To this end we monitored: (i) changes in the proportion of the diatoms in relation to other algal groups at the biofilm community level; (ii) shifts in species composition at the diatom-assemblage level; (iii) projected changes in the densities of the most representative species at the population level through comparison of relative growth rates and generation times; and (iv) the cytological changes at the cellular and subcellular levels as indicated by the appearance of teratological effects on individuals and nuclear alterations. The epipsammic biofilms were exposed for 96h to chromium at a concentration similar to that measured in highly impacted sites along the coast (80μgL(-1)). Chromium pollution, at this concentration and short exposure time did not affect the algal biomass and density of these mature biofilms. The biofilm composition, however, did change, as reflected in a decline in cyanophytes and an increment in the proportions of diatoms and chlorophytes; with Hippodonta hungarica, Navicula novaesiberica, Nitzschia palea, and Sellaphora pupula being the most frequent and abundant species. The most notable shifts related to chromium exposure were a decrease in the relative abundance of H. hungarica and a significant increase in the proportion of N. palea. Moreover, the species analyzed in the treatment microcosms showed higher growth rates than in the controls - N. palea grew faster, while H. hungarica replicated more slowly. The total nuclear abnormalities - as recorded in Fallacia pygmaea and N. novaesiberica - were significantly higher in the treatment microcosms; whereas in N. palea, the dominant species in treatment microcosms, neither nuclear alterations nor abnormal frustules were observed.Aquatic toxicology (Amsterdam, Netherlands) 03/2013; 134-135C:82-91. · 3.12 Impact Factor
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ABSTRACT: Diatoms are single cell eukaryotic microalgae, which present in nearly every water habitat make them ideal tools for a wide range of applications such as oil explora-tion, forensic examination, environmental indication, biosilica pattern generation, toxicity testing and eutrophication of aqueous ecosystems. Essential information on diatoms were reviewed and discussed towards impacts of diatoms on biosynthesis and bioremediation. In this review, we present the recent progress in this century on the application of diatoms in waste degradation, synthesis of biomaterial, biomineraliza-tion, toxicity and toxic effects of mineral elements evaluations. Diatoms can be considered as metal toxicity bioindicators and they can be applied for biomineralization, synthesis of biomaterials, and degradation of wastes.BioImpacts : BI. 01/2012; 2(2):83-9.
Journal of Applied Phycology 14: 41–48, 2002.
© 2002 Kluwer Academic Publishers. Printed in the Netherlands.
Use of microbenthic algal communities in ecotoxicological tests for the
assessment of water quality: the Ter river case study
Enrique Navarro, Helena Guasch & Sergi Sabater∗
Departament d’Ecologia, Facultat de Biologia, Univ. de Barcelona. Avgda. Diagonal 645, E-08028 Barcelona,
Spain (∗Author for correspondence; e-mail: email@example.com)
Received 15 September 2000; revised 7 March 2001; accepted 7 March 2001
Key words: Atrazine, Copper, Cyanobacteria, Diatoms, Ecotoxicity, Environmental assessment, Fluorescence,
Green algae, Mediterranean, River, Photosynthesis
The tolerance of microbenthic algal communities to two model toxicants, atrazine and copper, was studied in the
Ter river during spring and summer. Artificial substrata were colonised at 9 sites and used to perform short-term
(1–4 h) toxicity tests in the laboratory and to obtain photon yield as the ecotoxicological endpoint. The tolerance
was lower in spring than in summer for both toxic substances and varied according to the site studied. Copper
toxicity was associated with physico-chemical conditions (total suspended solids and water pH) and, especially,
with several biomass-related parameters, whereas atrazine toxicity was related to algal abundance and species
composition. Temporal and spatial changes in nutrient concentration may alter the biomass and species compos-
ition of the communities and thus affect their tolerance to toxic substances. It has to be therefore considered that
the environmental characteristics of the river system may determine relevant direct and indirect effects on the
algal communities, then affecting their specific ecotoxicological responses. Once this is assumed, the empirical
expressions obtained on calculating EC50and EC10can be used to predict the community-leveltransient effects of
Most ecotoxicologicaltests areperformedinthelabor-
atory, on small populations of certain species and,
although they provide useful information on the ef-
fect of these toxicants, they are not fully reliable to
forecast effects in natural systems (Cairns and Nieder-
lehner 1995), and require complementary studies on
variance of tests involving multi-species assemblages
can bereducedwithappropriateknowledgeofthe eco-
logical function of the most relevant components of
the community (Round 1991). Therefore, the use of
natural communities from many river systems does
not imply loss of reliability. The community-scale ap-
proach is ecologically sound, since it integrates the
specific tolerances of all the taxa present in a given
community (Blanck and Wängberg 1988), as well as
their own interactions and environment-relationships.
Physiological tests are used to ascertain the im-
mediate response of algal communities to toxicants
(Blaylock et al. 1985; Tubbing et al. 1996). These
tests provide a short-term complement to the long-
term response of communities, when the exposure to
a toxicant can affect their structure (Paulsson et al.
This study was carried out in the Ter, a chemic-
ally and biologically well characterised (Caixach et
al. 1990; Espadaler et al. 1997; Sabater et al. 1991,
1995) Mediterranean river with various human in-
fluences. We selected two common model toxicants,
atrazine and copper, which result from agricultural,
farmingandindustrialinputs. Thefirst is ausualherbi-
cide whose concentrationsin river systems range from
0.017 to 0.19 µg L−1(Readman et al. 1993; Solomon
et al. 1996). The latter is a heavy metal with con-
centrations between 30 and 60 µg L−1in moderately
polluted sites (Armengol et al. 1993). Both toxicants
Figure 1. The Ter, showing the sites where the ecotoxicological
response of microbenthic communities was analysed.
can reach peak values of several orders of magnitude
higher than the above-described (Huber 1993; Van
Beelen and Doelman 1997).
The aim of this study was first to show the reli-
ability of an approachbased on communitytests in the
frameworkof a well-describedecological context; and
second, to predict easily the ecological consequences
of a given input of toxicant in a given location.
Several sites scattered throughout the main stretch of
the River Ter (Figure 1) were analysed during spring
and summer. The sites ranged from the headwaters to
the mouth, and had very distinct influences (Table 1):
nivo-pluvial in the upper stretch, strongly Mediter-
ranean in the lower stretch (Sabater et al. 1995).
Three reservoirs located in the middle part interrupt
the river and alter its physical and chemical charac-
teristics downstream (Puig et al. 1987). In the peri-
ods studied, benthic algae grow at the maximal rates
and show well-differentiated physical and chemical
characteristics (Sabater and Sabater 1992).
Materials and methods
Artificial substrata (etched glass 1.4 cm−2of surface
area) on perspex supports were placed at the sites,
and allowed to colonise for four weeks. The physical
(temperature, light transmittance, water velocity) and
chemical (pH, dissolved oxygen) parameters of the
sites were measured at the beginning and at the end of
the experiment. Chemical data (chemical water para-
were obtained from the Catalan Agency for Water,
which monitors them routinely. The artificial substrata
were placed avoiding littoral, slow-movingwaters; the
current velocity ranged from 4 cm s−1(Roda de Ter,
Flaçà) to 80–100 cm s−1(Ter headwaters: Setcases,
Camprodon).Transmittedlight at the substratasurface
was measured with an underwater light sensor, and
recordedas the differencebetween the data at the river
surface and the location of the glass.
After colonisation, the glass were transported to
the laboratory (maximum travel time of 2h) and sep-
arated for community analysis (2 glass), chlorophyll
a analysis (5 glass) and ecotoxicological tests. Com-
munity analysis included the identification of the taxa,
enumeration (following Utermöhl’s technique after
sonication, Sabater et al. 1998) and estimate of cell
biovolume (Muñoz et al. 2000). Cell counts were
used to calculate the Shannon-Wiener diversity in-
dex (Shannon and Weaver 1963). Chlorophyll-a was
estimated after extraction with 90% acetone and spec-
trophotometric measurements (Jeffrey and Humphrey
1975). For the ecotoxicological tests, two protocols
were followed. Since copper requires long-term in-
cubation, the glass were placed on artificial channels
(Navarro et al. 2000). Since the water for incubation
was from the site, the channels were used in a re-
circulation mode (4 h). Water temperature and pH
were adjusted to those of the sites at the beginning
of incubation (± 1◦C for temperature, ± 0.01 for
pH). pH was carefullycontrolledin orderto ensure the
chemical speciation of this heavy metal. Eight chan-
nels were used, including one control and 7 copper
concentrations, with five glass replicates each. For
atrazine, incubation (1h) was performed in buckets
containing the glass with the herbicide concentrations
(7) and the control. In both tests, light was provided
by halogen lamps (110 µmol photon m−2s−1at the
The photon yield (Fm’-F)/Fm’ quotient (Falkowski
and Raven 1997) was measured after incubation
Table 1. Physical and chemical characteristics of the sites on the Ter studied in spring and summer 1999. Standard deviations for mean
values are given in italics.
Roda de Ter7.9
Cellera de Ter7.9
Cellera de Ter7.6
by means of a Pulse Amplitude Modulation (PAM)
fluorometer, which is a clean, non-destructive tech-
nique. In steady light and temperature conditions, it
is proportional to the photosynthetic rate (Hofstraat et
al. 1994).Themeasurementswereusedto estimatethe
effective concentration that reduced the photon yield
by 50% (EC50) and by 10% (EC10). These paramet-
ers were quantified by log-linear interpolation, which
provides the photon yield in samples exposed to toxic
substances as a percentage of the average activity of
the controls (which is set to 100%).
The relationships between the ecotoxicological,
biological and environmental data were analysed by
Pearson Correlation tests.
Physical and chemical characteristics
several orders of magnitude (Table 1). However, the
reservoirs caused major discontinuity in this pattern
(Table 1), and also affected the total suspended solids
(TSS). The highest TSS concentrations were found at
the sites immediately upstream of the reservoirs and
at the vicinity of the river mouth, and the lowest at
the sites downstream of the reservoirs. The highest
concentrations of nutrients (422–540 µg L−1soluble
reactive P and 8–12 mg L−1nitrate-N) were detected
at the lowermost sites and upstream of the reservoirs.
Table 2. Diversity, biomass (chlorophyll-a), biovolume and percent growth forms for each algal community from the sites on the
Chlorophyll-a Shannon- Density
(cells cm−2) (µm3cm−2) Biovolume Biovolume Biovolume Biovolume Biovolume
filamentous encrusting prostrate planktonic stalked
Roda de Ter
Cellera de Ter
8.51 × 105
4.84 × 106
7.91 × 106
1.76 × 106
4.50 × 105
2.70 × 106
2.90 × 106
5.27 × 105
5.93 × 105
5.41 × 108
6.00 × 108
1.65 × 109
6.21 × 108
4.66 × 108
3.01 × 109
2.18 × 1010
5.70 × 109
8.76 × 108
Cellera de Ter
8.79 × 105
2.29 × 106
7.87 × 106
3.41 × 106
2.34 × 106
1.03 × 106
2.43 × 108
7.72 × 108
6.73 × 108
8.47 × 108
6.91 × 109
2.78 × 108
Monthly averages of basal copper concentrations
(when detectable) during the study period ranged
between 0.5 µg L−1(close to detection limit, at
Bescanó) and 4.5 µg L−1(Roda de Ter, upstream
of the reservoirs). Analogous measurements of at-
razine ranged from 0.004 µg L−1(at Montesquiu) to
0.03–0.08 µg L−1(Roda de Ter, and river mouth).
Microbenthic community parameters
During spring, the chlorophyll-a concentration in the
colonised glass substrata was higher (Table 2). Min-
imal and maximal values were detected in the head-
waters andslightly upstreamof the reservoirs, respect-
ively. In summer, the differences between sites were
more marked (Table 2). Diatoms were the dominant
algal group in all the sites studied. They accoun-
ted for 87 to 95% of the total algal biovolume. The
dominant growth forms varied according to sites and
periods (Table 2). Encrusting taxa (e.g., Chamae-
siphon polonicus) were dominant in the headwaters
duringspring. Filamentoustaxa(e.g., Phormidiumau-
tumnale) accounted for about half the total taxa from
the middle sites, upstream of the reservoirs. Prostrate
forms (Navicula spp., Cymbella spp.) were abundant
in communities at sites downstream of the reservoirs,
especially during summer. Finally, planktonic taxa
(like Cyclotella sp. and Stephanodiscus hantzschii)
were mainly found in the lowermost sites.
The mean Shannon-Wiener’ index of diversity
was similar for the two periods. However, the vari-
ation between sites was much higher during summer.
Moreover, the differences between sites were higher
upstream than downstream of the reservoirs (Table 2).
The EC50for the two toxicants at all sites and during
the two periods are shown in Table 3. In general, tol-
erance to copper was lower in spring than in summer.
The EC50for copper in spring and in summer ranged
from 20 to 50 µg Cu L−1and from 100 to 350 µg Cu
L−1, respectively. The headwaters (Camprodon) were
the most sensitive (16 µg Cu L−1) and Montesquiu
(115µg Cu L−1) themost tolerantin spring.The latter
was also the most tolerant in summer, but with a much
higher EC50(1557 µg Cu L−1).
The tolerance to atrazine toxicity was higher in
summer than in spring. Most EC50in the latter period
ranged between 6 –9 µg atrazine L−1, while in sum-
mer the usual range of values went up to 30–70 µg
atrazine L−1. The most tolerant sites were in the Ter
Table 3. EC50for copper and atrazine for photon yield (pho-
tosynthetic rate) in the sites studied.
Roda de Ter
headwaters, with EC50 values ranging from 47 to
112 µg of atrazine L−1.
The interactions between ecotoxicological parameters
and physical, chemical and biological variables were
explored by means of correlation analysis. Among
the chemical variables, pH was associated with the
EC10for copper, and SRP with the EC50for atrazine
(Table 4). However, the EC50and EC10were mainly
correlated with algal biomass and cell densities of the
growth forms (Table 4). Chlorophyll-a was signific-
for atrazine, with the cell densities of cyanobacteria,
filamentous and stalked growth forms, and with sev-
eral biovolume-related parameters (Table 4). Several
cyanobacterial and algal taxa also showed significant
correlations with the EC50 for copper and atrazine
Physiological tests were useful to determine early
effects on the algal communities of the Ter River.
However, it was clear that strong differences occurred
between the two studied periods: the algal communit-
ies were more sensitive during spring than summer to
the effects of the toxicants (Table 3). This difference
is attributable a variety of factors, both environmental
and biological, which should be considered in the use
of this type of tests in natural communities.
Among the environmental factors, flow (high dur-
ing spring and low during summer) could cause the
different spatial patterns in the two periods (Sabater et
al. 1991). Differences between sites during the sum-
mer resulted from the lower precipitation (especially
in the lower stretch), which caused water characterist-
ics to depend on local inputs. Moreover,the reservoirs
in the Ter increased the differences between the sites.
Since they are in the middle part of the river (Sabater
et al. 1995), they affect the dissolved and suspended
solids that are transported. Although their effect on
the ecotoxicological parameters of the sites upstream
or downstream of the reservoirs has not been shown,
TSS may adsorb and complexate heavy metals like
bioavailability (and hence their toxicity, Table 4). The
statistical analysis also revealed (Table 4) a signific-
ant correlation between the EC50for copper and pH.
At lower pH, the bioavailability of copper increased,
sincethereis a higheramountoffreecopper(Stadorub
et al. 1987).
Water chemicalcharacteristicscouldalso influence
the ecotoxicological responses of the algal communit-
ies by affecting their respective algal biomass accu-
mulation. Nutrients varied accordingto the season and
the site (Table 1, Sabater et al. 1995), which probably
trient availability strongly determines algal biomass
and community composition (Biggs 1995; Guasch et
al. 1995; Dodds et al. 1997). Therefore, biomass-
related parameters, except TSS and pH, were the most
clearly correlated with the EC50and EC10for copper
and atrazine (Table 4). There was a positive relation-
ship between the resistance to toxicity (higher EC50)
and the algal biomass. This relationship may be re-
lated to the influence that biomass accumulation has
on light availability within the biofilm, as well as for
that of nutrients and other dissolved substances (Hill
and Knight 1988; Mulholland et al. 1995; Steinman
et al. 1995). Moreover, the penetration of metals into
biofilms is limited by their thickness, i.e. the accu-
mulated biomass (e.g., Admiraal et al. 1999), since
polysaccharideexudatesmay efficiently adsorbmetals
(Decho 1990; Ivorra et al. 2000), and thus reduce their
penetration into algal cells.
Table 4. Significant correlations (p <0.05) between EC50and EC10for copper and
atrazine and associated chemical and biological parameters.
EC50Cu EC10Cu EC50AtrEC10Atr
Number of stalked algae
Number of filamentous algae
Number of cyanobacteria
Biovolume postrate algae
Biovolume planktonic algae
Height above sea level
Table 5. Cyanobacterial and algal taxa significantly correlated
with the EC50for copper and atrazine (p < 0.05)
Environmental factors also determine the over-
all responses of algal communities: the low light
availability (due to high shading) and the subsequent
physiological response of the algal community prob-
ably account for the minimal atrazine toxicity ob-
served in Setcases and other sites of the Ter head-
waters (Table 3). Several laboratory and field studies
indicate that atrazine toxicity is associated with pho-
toadaptation to low light intensity, when the relative
increase of carotenoids and other accompanying pig-
ments decreases the toxicant effect (Millie et al. 1992;
Guasch and Sabater 1998).
Certain algal taxa were clearly linked with the
ecotoxicological indicators. Although the density of
cyanobacteria was related to the EC50 for copper
(Table 4), the only taxa positively correlated with this
ecotoxicological parameter was the diatom Navicula
radiosa (Table 5), a common species in the middle
stretch of the Ter (Sabater et al. 1991). Cyanobacteria
have been described to tolerate high concentrations of
heavy metals such as zinc (Say and Whitton 1982,
Whitton et al. 1981), but they are not so common
in copper-polluted environments (Leland and Carter
1984). In a long-term experiment Soldo and Behra
(1990) determinedthat exposure of periphytonto high
concentrationsof copper(5 µM) caused the shift from
the Cyanobacteria to green algae dominance. In the
same experiment, diatoms remained at a similar pro-
portion with the highest copper concentrations than
in the control conditions. Takamura et al. (1989), by
measuring the effect of copper on photosynthesis,also
determined the high sensitivity of cyanobacteria to
copper, as well as the higher resistance of green algae
and of some diatom taxa. Atrazine toxicity is also as-
sociated with the higher proportion of cyanobacteria,
green algae and diatoms (Table 5). Diatom communit-
ies are more tolerant than those dominated by green
and Sabater 1998), which are 8 to 10 times more sens-
most sensitive to atrazine were dominated by green al-
gae (Bescanó, Flaçà and Torroella), whereas the least
sensitive (Setcases) had a low proportion of this algal
Our conclusions based on natural communities are
consistent with other studies carried out in more con-
trolled conditions, in the laboratory or in mesocosms.
Tests using natural communities appropriately reflect
the ecological reality of a natural system (Cairns and
Niederlehner1987),andmakethem a valuabletoolfor
Table 6. Percent decrease (negative) and increase (positive) in the
photosynthetic rate after the input of 10 µg L−1copper for 3 h or
10 µg L−1atrazine for 1 h, as deduced from the log-linear cor-
relation between photosynthesis and the toxicant concentration (for
further details see the text).
Roda de Ter
Cellera de Ter
environmental assessment. However, it is clear from
our results in the Ter that the environmental charac-
teristics of the system may determine relevant direct
and indirect effects on the algal communities, then af-
fecting their specific ecotoxicologicalresponses. Once
this is assumed, the empirical expressions obtained on
calculating EC50and EC10can be used to estimate the
effect ofa concentrationof toxicant.We describedtwo
scenarios that could affect the photon yield. The first
is highlyrealistic, since it considersthe concentrations
detected in the Ter. It describes the 3 h-effect of 10 µg
L−1copper on the algal communities of the river. The
second explores the response to a high concentration
of atrazine (10 µg L−1atrazine for 1 h) (Huber 1993)
that has never been recorded in the Ter, though has
ation to these concentrations can occur in some sites
for copper, but not for atrazine.
Each scenario shows a variety of responses. Some
communities are slightly affected by the toxicant in-
put, others show a decrease in the photosynthetic rate,
and others a moderate increase (Table 6). In the case
of atrazine, the effects on the photosynthetic rates
are devastating for many of the algal communities of
the Ter, especially during spring. Regarding copper,
the moderate amount tested can cause a remarkable
decrease (around 20% in some sites).
In conclusion, physiological tests provide an early
prospective quantification of the transient effects of
a toxic community on separate communities, predict
which of these effects are not reversibleand determine
their intensity. This procedurecouldbe followedto as-
sess the effect of toxicants on algal communities, and
thus extrapolate the effect to the whole river system.
This work is part of the project ‘Microbenthos’, fun-
ded by the European Community (project number
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