JOURNAL OF PLANKTON RESEARCH j VOLUME 26 j NUMBER 6 j PAGES 669–679 j 2004

Structure of the phytoplankton

communities in two lagoons of different
salinity in the Sfax saltern (Tunisia)
HABIB AYADI, OLFA ABID, JANNET ELLOUMI, ABDERRAHMEN BOUAÏN AND TÉLESPHORE SIME-NGANDO1,*

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LABORATOIRE D’ECOLOGIE ANIMALE ET DE PLANCTONOLOGIE, DEPARTEMENT DES SCIENCES DE LA VIE, FACULTE DES SCIENCES DE SFAX, BP 802,
CP 3018, SFAX, TUNISIA AND 1LABORATOIRE DE BIOLOGIE DES PROTISTES, UMR CNRS 6023, UNIVERSITE BLAISE PASCAL (CLERMONT-FERRAND II),
63177 AUBIERE CEDEX, FRANCE
*CORRESPONDING AUTHOR: telesphore.sime-ngando@univ-bpclermont.fr

Received on September 4, 2003; accepted on February 2, 2004; published online on April 5, 2004

The structure and ecophysiological characteristics of phytoplankton assemblages were studied for 10
months in two lagoons of different salinity (40 and 90) in the saltern of Sfax (Tunisia), in relation to
environmental factors. These assemblages were largely dominated by diatoms and dinoflagellates, which
accounted for >90% of total abundance. A principal components analysis clearly differentiated the
observations made in the two lagoons, the dominant correlate being the salinity. Euryhaline species and
particularly diatoms developed preferentially in the less saline lagoon, and were largely replaced by
stenohaline species represented by dinoflagellates, which were dominant in the more saline lagoon.
Calculation of the pigment diversity index and the species diversity index showed that the phytoplankton
assemblages studied were permanently in a juvenile stage, as the species restructuring related to
environmental constraints did not allow them to reach the climax stage at any given time in their
development. Despite the heavy constraint imposed by the salinity, it is evident that other environmental
factors, e.g. temperature, play a role in the regulation of the planktonic communities. Finally, the
difference in the size distribution of the total microbial biomass, estimated by the assay of particulate
proteins, showed that there was a significant change in the community structure and the planktonic
trophic networks, in parallel with the increase in salinity.

INTRODUCTION
Marine coastal ecosystems, and especially coastal wet-
lands, are now better understood and are managed
relatively well (Sadoul et al., 1999). However, most scien-
tific research that has allowed such management to be
put into practice has not taken into account saline habi-
tats and particularly salterns, which are now threatened
biotopes mainly because of urbanization (Sadoul et al.,
1999). It is, therefore, necessary to rehabilitate and
restore these ecosystems, which are usually biologically
very rich and harbour unusual birds, fish, plants and
micro-organisms, in addition to having considerable
landscape and economic value.
Salines or salterns are either natural or man-made, so-
called ‘paralic’ coastal ecosystems. Artificial salterns are
generally formed of lagoons of increasing salinity that
are used for salt production. These lagoons have a low
thermal inertia (because the volume of water is very low
compared with the surface area exposed to evaporation)
and a low biological diversity that can be compensated
for by high production (Dussart, 1977). Along the sali-
nity gradient in different lagoons, a zonal biological
organization forms, consisting of ecological entities that
can be relatively autonomous and stable ( Joint et al.,
2002). The formation of such biological entities along a
longitudinal salinity gradient ranging from seawater to
the extreme environments of the salt crystallizing pans
gives salterns a high ecophysiological and ecological
value. The exchanges with the sea (Kiener, 1978), the
hydrology, salinity and nutrients play a determinant role
in the development of the biological communities (Davis,
1978, 1980, 1990).
However, most biological studies on salterns have dealt
with the ecology and the biogeography of the anostracan
Artemia (Dobbelier et al., 1980; Persoone et al., 1980) and
with halophilic bacteria (Oren, 1999, 2000). Other micro-
organisms, and especially phytoplankton communities,
have been given little attention in these environments

doi: 10.1093/plankt/fbh047, available online at www.plankt.oupjournals.org

Journal of Plankton Research Vol. 26 No. 6 Ó Oxford University Press 2004; all rights reserved
 JOURNAL OF PLANKTON RESEARCH j VOLUME
[reviewed in Davis (Davis, 2000)]. To our knowledge, only
the studies of Clastère (Clastère, 1984) and Noel (Noel,
1982) in the Salins de Giraud in the Camargue (France),
and of Campbell and Davis (Campbell and Davis, 2000) in
the salterns at Port Elizabeth in South Africa, have pro-
vided information on the phytoplankton of salterns. How-
ever, most of these studies were concentrated on only one
phytoplankton group, notably diatoms. It is important to
emphasize that it is now known that micro-organisms form
most of the biomass living in the marine environment in
general and in hypersaline environments in particular
(Oren, 1999; Pedros-Alio et al., 2000), where they are
organized into a trophic network that is responsible for:
(i) the transformation of the organic matter (OM) excreted
by the phytoplankton into bacterial biomass; (ii) the recy-
cling of part of this OM into inorganic nutrients (re)used by
photoautotrophs; and (iii) the transfer of another fraction
of this OM into the upper trophic levels, especially through
the bacterivorous activity of protozoa (Amblard et al.,
1998; Sime-Ngando et al., 1999).
In this work, we examine the species composition,
structure and physiological characteristics of the phyto-
plankton assemblages in two lagoons of different salinity
in the Sfax saltern (Tunisia). The chlorophyll and parti-
culate protein concentrations were used as indicators of
the microbial biomass. The physiological state of the
phytoplankton communities was estimated using the pig-
ment diversity index, and the structure of the assem-
blages (Margalef and Ryther, 1960) was analysed using
the species diversity index of Shannon and Weaver
(Shannon and Weaver, 1949).
METHOD
Study site
The Sfax saltern is an artificial system formed of intercon-
necting lagoons extending over a total area of 1500 ha,
along the coast to the south of Sfax (Tunisia) over a distance
of 12 km (Figure 1). This body of water is separated from
the sea by a dyke of red clay
4 m high. Because of its
geographical position, this is a paralic system, i.e. a transi-
tion between the marine and the terrestrial environments.
There is an annual evapotranspiration deficit favouring the
installation of hypersaline conditions. The seawater is
therefore concentrated by evaporation until saturation,
crystallization and precipitation of NaCl occur in the har-
vesting pans. For more details on the characteristics of the
saltern, see Ayadi et al. (Ayadi et al., 2002).
Sampling
Two lagoons of very different salinity were chosen for the
samplings. The A1 lagoon of 40 median salinity is part of
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26 j NUMBER 6 j PAGES 669–679 j 2004
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Fig. 1. Maps of the geographical location of the salt works along the
coast to the South of Sfax (Tunisia).
the series of preliminary concentration lagoons in the
saltern. These lagoons, which receive seawater directly, are

50 cm deep, have a muddy bottom and are constantly
turbid because of the pumping of seawater. The second
lagoon studied is the C2-1 lagoon of 90 median salinity. It
is situated in the intermediate zone of the salt production
chain, among lagoons called the ‘partènements exterieurs’.
These lagoons are
30 cm deep and also have a muddy
bottom, but are richer in OM than the preliminary con-
centration lagoons.
Samples were collected with a Van Dorn-type closing
bottle in the central part of each of the two lagoons,
every 3 weeks, between the months of August 1999 and
May 2000. The sampling period was chosen because of
accessibility and in order to include the three main
seasons (i.e. spring, summer and autumn) for biological
activity in the saltern. All of the samples were first
filtered through a nylon net of 160 mm mesh to eliminate
most of the metazoan zooplankton. Samples of variable
volume (depending on the variables measured) were
collected and stored separately in the dark and cold,
for the analysis of biotic and abiotic variables, except
for temperature, which was measured in the field using a
portable digital display thermometer. For the microbial
community, three series of samples were collected: the
first series was fixed in Lugol’s iodine (final concentration
1% v/v) for identification and counts of phytoplankton
cells, the second series was used for assaying pigments
(total chlorophyll and carotenoids) and the third series
for assaying particulate proteins. Two size fractions
of proteins were assayed, <20 mm (nanoplankton) and
<160 mm (microplankton), in two samples collected in
autumn 1999 and spring 2000.
 H. AYADI ETAL. j PHYTOPLANKTON STRUCTURE IN SFAX SALTERN
Analysis of physico-chemical variables
The methods for measuring the temperature ( C), sali-
nity, pH and suspended solids (SS) concentrations
(mg L1) have been described previously in Ayadi et al.
(Ayadi et al., 2002). The nutrient concentrations that
were analysed were nitrates and total phosphorus.
These nutrients were analysed in a series of four samples
collected in August, November, February and May,
considered representative of the different seasons of the
year. Before the assays, the samples were filtered through
GF/C glass fibre filters 47 mm in diameter (nominal
porosity 1.2 mm). The total phosphorus was assayed by
spectrophotometry after reaction in the presence of
ammonium molybdate and reduction by ascorbic acid
(Murphey and Riley, 1962), whereas the nitrates were
assayed by ionic chromatography carried out using a
Shimadzu ion chromatograph HIC-6A. This apparatus
is equipped with an ion-exchange resin (i.e. the station-
ary phase) that is extremely stable to a wide range of salt
concentrations and can function well within the pH
range of 2–12 (limit of detection for NO3
0.07 mM).
Analysis of biotic variables
The phytoplankton counts were conducted using an
inverted microscope, according to Utermöhl’s method
(Utermöhl, 1958). The different species encountered
were identified from morphological criteria, after consulta-
tion of various works on identification. The structure of
the phytoplankton assemblages was studied by calculating
the species diversity index (H 0 ; bits cell1), using Shannon
and Weaver’s formula (Shannon and Weaver, 1949).
Total chlorophyll and carotenoids were assayed by spec-
trophotometry, after extraction of the pigments in acetone.
The concentrations were then estimated using the equa-
tions of SCOR-UNESCO (SCOR-UNESCO, 1966). The
absorbance of the pigment extracts was measured by spec-
trophotometry at 430 and 665 nm, in order to calculate the
values of the ratio OD430:OD665, which enabled us to
estimate the pigment diversity index according to the for-
mula of Margalef and Ryther (Margalef and Ryther, 1960).
This pigment index provides information on the physiolo-
gical state of the assemblages: values <5 are characteristic
of assemblages in a juvenile growth stage, whereas values
>5 are more characteristic of climax or senescent commu-
nities (Margalef and Ryther, 1960; Margalef, 1965).
Particulate protein concentrations were measured by
spectrophotometry. Two size classes considered as nano-
plankton (<20 mm) and microplankton (<160 mm) were
also separated on two different occasions, in autumn
1999 and spring 2000. For the assay of proteins, the
plankton particles contained in a 100–200 mL sample
were retained on a GF/C filter (
1.2 mm) that had
671
previously been heated at 450 C for 4 h in a muffle
furnace. The proteins were then extracted and assayed
according to the protocol of Lowry et al. (Lowry et al.,
1951). During the assays, interference caused by the
presence of salts was controlled by means of a solution
of distilled water with NaCl added to make it the same
salinity as that of the samples analysed.
Statistical analyses
A matrix of previously normalized physical, chemical and
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biological data was produced and analysed by means of a
principal components analysis (PCA). This type of statis-
tical analysis between the biological, physical and chemical
descriptors is suitable when a uniform linear relationship is
likely to exist between variables (Dolédec and Chessel,
1989). The differences between the two study lagoons
were tested by one-way analysis of variance (ANOVA).
The potential relationships between variables were tested
by Pearson’s correlation coefficient.
RESULTS
Physico-chemical environment
The lagoons of the Sfax saltern are so shallow that no
thermal stratification occurs. During this study, the
waters of the shallower lagoon (C2-1) were warmer
(14–33 C) than those (10–32 C) of the deeper lagoon
(A1). However, the extreme temperature values were
recorded on the same dates in both lagoons: 23 August
1999 for the maximum values and 6 January 2000 for
the minimum values. The seasonal temperature varia-
tions in the two lagoons were characteristic of semi-arid
to arid zones of the northern hemisphere, with a warm-
ing starting in spring and a maximum at the end of July
to early August, followed by a cooling and a seasonal
minimum in January (Figure 2A and E).
The salinity of the water increased from lagoon A1
(range of salinity variation 38.7–43.5) to lagoon C2-1 (64–
95) in parallel with the increase in temperature. The sea-
sonal variations in salinity were relatively small (Figure 2B
and F). As with the salinity, the pH increased from lagoon
A1 (5.95–8.05) to lagoon C2-1 (7.8–8.35), the temporal
variations in each lagoon being small (Figure 2C and G).
The SS concentrations were lower in lagoon A1,
where they fluctuated from 10 mg L1 (January) to
270 mg L1 (November), than in lagoon C2-1 where
the values were between 25 mg L1 (January) and 480
mg L1 (September). The temporal variations of this
variable were erratic, the lowest values generally being
recorded in spring (Figure 2D and H).
The nutrient concentrations measured on individual
dates in each season of the year are shown in Table I. In
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Fig. 2. Seasonal variations of physico-chemical parameters.

all seasons, the nitrates and total phosphorus concen- summer in lagoon A1, but in winter in lagoon C2-1.
trations were significantly higher (ANOVA, P < 0.01) The concentrations of total phosphorus in summer in
in lagoon A1 than in lagoon C2-1. The highest con- both lagoons were much higher than those recorded in
centrations of nitrates were recorded in spring and other seasons.

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 H. AYADI ETAL. j PHYTOPLANKTON STRUCTURE IN SFAX SALTERN

Table I: Seasonal variations of nitrate and 32% of total phytoplankton abundance in lagoons A1
phosphorus (DIP) concentrations in lagoons and C2-1, and dinoflagellates 12 and 67%. The various
A1 and C2-1 of the Sfax saltern genera of diatoms and dinoflagellates encountered in the
two lagoons in the different seasons of the year are
Lagoon A1 Lagoon C2-1 shown in Table II. It appears that the centric diatoms
that were present in lagoon A1 disappeared completely
Nitrate Total phosphorus Nitrate Total phosphorus in lagoon C2-1; this explains the negative correlation
(mM) (mM) (mM) (mM) between these diatoms and dinoflagellates, which were
more abundant in lagoon C2-1 (Table III). Depending
Summer 130.00 83.87 14.29 8.39 on the season, the summer period (23 August 1999

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Autumn 22.14 0.32 15.00 ND sample) was characterized by a small number of genera,
Winter 57.14 11.29 21.43 2.26 especially in lagoon A1 where only two genera of
Spring 85.71 29.03 5.71 1.29 dinoflagellates developed.
The values of the species diversity index calculated
ND, not determined.
from the genera or species belonging to the two domi-
nant taxonomic groups (diatoms and dinoflagellates)
Phytoplankton communities were higher in lagoon A1 than in lagoon C2-1. This
Microscopic examination enabled us to identify
40 index varied between 0.32 (October) and 0.96 (January)
phytoplankton genera, belonging to seven taxonomic bits cell1 in lagoon A1, and between 0.04 ( June) and
groups: diatoms, dinoflagellates, Chlorophyceae, Eugle- 0.8 (March) bits cell1 in lagoon C2-1. In lagoon A1, the
nophyceae, Euchlorophyceae, Cyanobacteria and Dic- values of this index increased more or less regularly
tyophyceae. In both lagoons, almost all of the species between September and January, and fell from January
counted were diatoms and dinoflagellates (>90% of total to April (Figure 3A). In lagoon C2-1, the diversity index
numeric abundance). Diatoms accounted for 82 and of the phytoplankton communities fluctuated slightly

Table II: Seasonal specific composition of phytoplankton communities in lagoons A1 and

C2-1 of the Sfax saltern
Summer Autumn Winter Spring

Lagoon A1
Pennate diatoms Navicula Nitzschia Nitzschia
Pleurosigma Stenopterobia Pinnularia
Diatomella Diatomella Pleurosigma
Surirella Surirella
Centric diatoms Thalassiosira Biddulphia Biddulphia
Skeletonema Rhizozolenia Chaetoceros
Coscinodiscus
Dinoflagellates Prorocentrum Gymnodinium Prorocentrum Prorocentrum
Protoperidinium Oxyrrhis Gonyaulax Scrippsiella
Peridinium Peridiniopsis Peridiniopsis
Lagoon C2-1
Pennate diatoms Nitzschia Gyrosigma Nitzschia Navicula
Gyrosigma Gyrosigma Gyrosigma
Pinnularia Pleurosigma
Stenopterobia
Dinoflagellates Protoperidinium Gymnodinium Gymnodinium Gymnodinium
Gymnodinium Oxyrrhis Oxyrrhis Oxyrrhis
Gonyaulax Peridinium Peridinium Protoperidinium
Protoperidinium Gonyaulax
Gonyaulax

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 JOURNAL OF PLANKTON RESEARCH j VOLUME 26 j NUMBER 6 j PAGES 669–679 j 2004

Table III: Correlation matrix for physical, chemical and biological variables under study
in the Sfax saltern

C pH Salinity SS Proteins Chl. Caroten. P. diatoms C. diatoms Dinoflag.


C 1
pH 0.235 1
Salinity 0.071 0.597** 1
SS 0.013 0.338 0.382* 1
Proteins 0.067 0.190 0.062 0.302 1

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Chl. 0.117 0.049 0.110 0.062 0.471* 1
Caroten. 0.026 0.171 0.206 0.228 0.502** 0.796*** 1
P. diatoms 0.441* 0.145 0.045 0.148 0.044 0.026 0.109 1
C. diatoms 0.076 0.157 0.456* 0.232 0.064 0.352 0.144 0.065 1
Dinoflag. 0.220 0.187 0.524** 0.355 0.130 0.177 0.051 0.097 0.689*** 1

*P < 0.05; **P < 0.01; ***P < 0.001; df = 26. SS, suspended solid concentration; Chl., chlorophyll a concentration; Caroten., carotenoid concentration;
P. diatioms, abundance of pennate diatioms; C. diatioms, abundance of centric diatioms; Dinoflag., abundance of dinoflagellates.

In both lagoons, the total phytoplankton abundance

Fig. 3. Seasonal variations of the species diversity index (H0 ) within
the phytoplankton communities.
from September to February, reaching a maximum in
March, and then decreased more or less progressively up
to the end of the study (Figure 3B).
fluctuated from values of <104 cells L1 to values >2 
106 cells L1. In temporal terms, the total abundance in
lagoon A1 reached its maximum (1.98  106 cells L1) on
5 October 1999, this being mainly the result of the devel-
opment of diatoms. The values then remained very low
until spring, when diatoms and dinoflagellates developed,
but at lower levels of abundance, <1  106 cells L1
(Figure 4A). In lagoon C2-1, the highest total phytoplank-
ton abundance (3.8  106 cells L1) was recorded on 20
June 2000, due to the development of pennate diatoms. In
contrast to lagoon A1, diatoms and dinoflagellates devel-
oped in winter (especially in January and February for
dinoflagellates and in February for pennate diatoms), the
spring abundances being generally low (Figure 4B). For all
the observations, positive (+) correlations were recorded
between the abundance of pennate diatoms and the tem-
perature, and between salinity and dinoflagellates (+) and
centric diatoms (–) (Table III ).
The pigment concentrations analysed were very low
in both lagoons studied, the concentrations being
<0.4 mg L1 for total chlorophyll and <0.2 mg L1 for
carotenoids (Figure 5A and B). In contrast to the
chlorophyll contents, which were similar in both lagoons,
the carotenoid concentrations were significantly higher
(ANOVA, P < 0.05) in lagoon C2-1 (mean 0.06 mg
L1) than in lagoon A1 (0.03 mg L1). In lagoon A1,
the highest values for the concentrations of these two
pigments were recorded in summer (August) and in
spring (May), whereas in lagoon C2-1, the highest values
were measured in autumn/winter. The pigment diversity
index was generally low in both lagoons (<5). The values
of this index fluctuated slightly around 3 in both lagoons,

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Fig. 4. Seasonal variations of the phytoplankton numerical abundance.

if the exceptionally high value (6.5) recorded in winter

(6 January) in lagoon A1 (Figure 5C) is excluded.
Particulate proteins
The total protein concentrations were similar in both
lagoons. They fluctuated from 0.1 to 4.3 mg L1
(mean = 1.71 mg L1) in lagoon A1, and from 0.074 to
5.2 mg L1 (mean = 1.81 mg L1) in lagoon C2-1. The
highest values were recorded in spring in lagoon A1 and in
winter in lagoon C2-1. A more or less regular increase in
these values was observed in autumn in lagoon A1 and Fig. 5. Seasonal variations of pigment concentrations (A and B) and
of the pigment diversity index (C).
in spring in lagoon C2-1 (Figure 6). The two size fractions
analysed on individual dates in autumn 1999 and spring
2000 showed that most of the particulate proteins in selected the salinity and abundance of dinoflagellates at
both lagoons (>98% of the total) were contained in the the positive end, and centric diatoms at the negative end
<160 mm size fraction. However, the relative importance (Figure 7A). The second axis distinguished pennate
of proteins of nanoplankton origin (<20 mm) increased diatoms and the temperature, with negative coordinates,
with salinity: from values <30% of the total in lagoon A1 from the chlorophyll, carotenoids and proteins, with
to values of
80% in lagoon C2-1. For all the observations, positive values. The plot of the field observations showed
a positive correlation was recorded between total proteins a clear segregation between the observations made in the
and both chlorophyll and carotenoid concentrations. two study lagoons, especially on axis 1 which, in relation
to the salinity, explained
30% of the observed vari-
Principal components analysis ance. The observations made in lagoon A1 are grouped
The plot of the descriptors on axes 1 and 2, which in the negative part of this axis together with the abun-
explained 50% of the total variance, showed that axis 1 dance of centric diatoms, in contrast to the observations

675
 JOURNAL OF PLANKTON RESEARCH
Fig. 6. Seasonal variations of particulate protein concentrations.
made in lagoon C2-1 which tended to group in the
positive part of this axis, together with the salinity and
the density of dinoflagellates (Figure 7B).
DISCUSSION
In this study, we have demonstrated the relationship
between the structure of phytoplankton assemblages
and environmental variables in two lagoons of very
different salinity in the Sfax saltern. The seasonal varia-
tions in temperature were naturally characteristics of a
semi-arid to arid Mediterranean climate. The differences
between the two lagoons, in terms of temperature and
the main chemical variables (salinity, pH, SS), were
mainly related to the depth of the lagoons, in relation
to the biology of the communities. In the salterns, the
lagoons situated in the intermediate zone of the halite
concentration chain, such as lagoon C2-1, are kept
artificially shallower than those situated at the beginning
of the concentration process, such as lagoon A1, in order
to increase the evaporation process leading to the pro-
duction of salts in the crystallizing pans (Davis, 2000).
This acceleration of the evaporation related to the shal-
low water in lagoon C2-1 did not result in a simple
mechanical concentration of the plankton communities
present but, apparently, an active response of these
communities to the increasing salinity conditions and
undoubtedly other environmental factors.
For example, although the increase in the tempera-
ture and salinity between lagoons A1 and C2-1 is
directly related to the evaporation process, that of the
pH and SS is on the other hand apparently related to
biological activity. The development of macroalgae
belonging especially to the genera Enteromorpha, Chondria
and Cladophora in lagoon C2-1 undoubtedly contributes
to the increased alkalinity of the water by photosynthesis,
but also to an increase in suspended particles related
to the bacterial degradation of the products of this
j VOLUME 26 j NUMBER 6 j PAGES 669–679 j 2004
photosynthetic production. This observation is similar
to that reported in other salterns, where the phytoplank-
tonic activity plays an important role in the changes in
pH (Clastère, 1984). As far as the SS are concerned, it is
well known that the development of halophilic bacteria
(notably belonging to the family Halobacteriaceae) in
salterns increases significantly with salinity (Rodriguez-
Valera et al., 1999). This was so in lagoon C2-1 of the Sfax
saltern, where the waters already started to take on the
pinkish colour characteristic of the carotenoid pigments of
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the halobacteria in the water column (Trabelsi, 1996)
The quantitative abundance of these pigments in this
lagoon was significantly higher than in lagoon A1. The
most saline lagoons in salterns are also generally furthest
from the sea and therefore receive more terrestrial inputs,
which would also tend to increase the SS concentration
from lagoon A1 to lagoon C2-1.
Given the similarity of the chlorophyll biomass in the
two lagoons studied, these terrestrial inputs and the recy-
cling of OM by bacteria undoubtedly represent a minor
source of nutrient enrichment. In fact, the nitrate and total
phosphorus concentrations measured on a single date in
the four seasons of the year were up to 15 times (for the
nitrates) and 22 times (for the total phosphorus) higher in
lagoon A1 than in lagoon C2-1, these differences being
much more pronounced in summer and spring (Table I).
Compared with nitrates, phosphorus concentrations were
substantially high in both lagoons sampled, where they
were generally characteristics of eutrophic to hypereu-
trophic inland aquatic systems. This is probably related
to the existence of anthropogenic sources of phosphorus
inputs in the Sfax coastal waters (Hamza, 2003). For
nitrates, our concentrations in Lagoon A1 were somewhat
typical of nutrient-rich inland waters, especially in spring
and summer. This contrasts with the concentrations
recorded in lagoon C2-1, which were characteristic of
oligotrophic inland waters for all the four seasons [(Orga-
nization for Economic Cooperation and Development
(OECD), 1982)]. The nitrate and phosphorus content
ranges that we measured were close to those recorded
from other salterns [reviewed in Litchfield et al. (Litchfield
et al., 1999)], and correspond to the values typical of
nutrient-rich eutrophic to hypereutrophic inland aquatic
ecosystems (OECD, 1982). The review by Litchfield et al.
shows that, with one exception ( Javor, 1983), the nitrogen
and phosphorus concentrations in salterns are higher in
the less saline lagoons [see table 4.1 in (Litchfield et al.,
1999)].
In contrast to the nutrient concentrations, the chloro-
phyll biomasses in the two lagoons studied (<0.4 mg L1)
are typical of nutrient-poor environments (OECD, 1982),
whereas the phytoplankton abundances (>5 mm) reached
106 cells L1 on some occasions (Figures 4 and 5). Species
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 H. AYADI ETAL. j PHYTOPLANKTON STRUCTURE IN SFAX SALTERN
Fig. 7. Results of the PCA obtained from the main variables under
study in the two sampled lagoons (A), and from the observations made
during the different sampling dates (ranked from 1 to 14, see dates on
the other figures) in each of the two sampled lagoons (A1 and C2-1) (B).
with frustules (diatoms) or thecae (dinoflagellates), which
largely dominate the phytoplankton assemblages in the
Sfax saltern (>90% of total abundance during our study),
visibly have less chlorophyll per unit biomass than most
other phytoplankton groups. In addition, many species of
dinoflagellates are aplastid and therefore strict hete-
rotrophs, whereas others are capable of exercising a
mixotrophic metabolism following partial or total regres-
sion of their chloroplasts (Sanders and Porter, 1988).
The examination of the seasonal variations in cell
abundance showed that the relative importance of the
two dominant groups differed from one lagoon to the
other. In lagoon A1, the phytoplankton mainly consisted
of diatoms, which developed in spring and autumn. In
lagoon C2-1, diatoms also occurred but dinoflagellates
tended to dominate the phytoplankton community,
677
especially in autumn and winter. This difference in the
relative composition of the phytoplankton, where steno-
haline species (dinoflagellates) developed to the detri-
ment of euryhaline species (diatoms) as the salinity
increased, was confirmed by the PCA. This analysis
showed a clear segregation between the observations
made in the two lagoons studied, which was related to
the development of diatoms in lagoon A1 and of
dinoflagellates in lagoon C2-1 (Figure 7).
The pigment diversity index, which according to
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Margalef (Margalef, 1965) reflects the physiological state
of the phytoplankton communities, also remained low (<5)
in this study (Figure 5C). In algal cultures, this index varies
from 5 in young and immature communities to 20 in
mature or senescent communities (Margalef, 1965). It
therefore seems that in the Sfax saltern, the phytoplankton
community is permanently in a relatively juvenile state, in
which the species turnover does not allow a climax stage to
be attained at any given time (Frontier, 1977). This is
confirmed by the species diversity index, the low values
of which in the two lagoons (<1 bits cell1) are character-
istic of pioneer communities. The constraints imposed by
the turbulence in lagoon A1 or by the salt concentration in
lagoon C2-1 are undoubtedly limiting factors for the
maturation of the phytoplankton assemblages in these
lagoons. It therefore appears that salinity is not the only
factor explaining the structure of the biological commu-
nities in the Sfax saltern, despite the fact that the abun-
dance of dinoflagellates and centric diatoms were
significantly correlated with salinity. For example, pennate
diatoms, which in contrast to centric diatoms (only occur-
ring in lagoon A1) developed in both lagoons, were posi-
tively correlated with the temperature. This suggests that
seasonal forcing, whose signal was still strong in the cli-
matic conditions at the site, had an influence on the
development of the organisms present, despite the heavy
constraint imposed by the salinity. A recent study con-
ducted on a saltern in the Camargue (France) also empha-
sized the importance of the salt concentration and
temperature in the regulation of plankton abundance
(Thiéry and Puente, 2002). In a review paper, Williams
indicated that the effects of salinity on the structure of
biological communities in salt lakes are less significant
than has been assumed (Williams, 1998). As there are
many correlates of salinity, it is not always possible to easily
distinguish the effects of these correlates from the direct
effects of salinity.
Finally, absence of relationships between the phyto-
plankton and SS (index of total microplankton biomass),
indicates the importance of particles other than phyto-
plankton in the Sfax saltern. It is well known that salterns
are sites of constant and high availability of food resources,
so that migratory birds, and particularly flamingos, are
 JOURNAL OF PLANKTON RESEARCH j VOLUME
able to use this site in large numbers throughout the year
( Johnson, 1991). The two size fractions analysed on single
dates in autumn 1999 and spring 2000 suggested that the
proteins were mainly represented by microplanktonic
organisms (<160 mm), the proportion of nanoplankton
(<20 mm) being very much higher in lagoon C2-1 than
in lagoon A1. This complements the recent finding by
Pedros-Alio et al. (Pedros-Alio et al., 2000), who were able
to show that increases in salinity resulted in a progressive
reduction in the abundance and number of different
groups of eukaryotic micro-organisms, but an increase in
the biomass of prokaryotes. These results lead us to con-
clude that a significant change is likely to appear in the
community structure and planktonic trophic networks as
the salinity increases, along the chain of halite concentra-
tion that occurs in salterns.
ACKNOWLEDGEMENTS
O.A. and J.E. were supported by postgraduate fellow-
ships from the University of Sfax. The authors are
indebted to D. Sargos for technical support. This study
was supported by the France–Tunisia CMCU Pro-
gramme. The writing-up of this paper was also sup-
ported by the CNRS Programmes PICS 1111 and
GDR 2476.
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