NORTH AFRICAN COASTAL LAGOONS

Environmental influences on the qualitative and quantitativecomposition of phytoplankton and zooplankton in NorthAfrican coastal lagoons

M. Ramdani Æ N. Elkhiati Æ R. J. Flower ÆJ. R. Thompson Æ L. Chouba Æ M. M. Kraiem ÆF. Ayache Æ M. H. Ahmed

Published online: 22 January 2009

� Springer Science+Business Media B.V. 2009

Abstract Within the framework of the international

research project MELMARINA, seasonal dynamics of

plankton communities in three North African coastal

lagoons (Merja Zerga, Ghar El Melh, and Lake

Manzala) were investigated. The sampling period

extended from July 2003 to September 2004 with the

aim of evaluating hydrological and other influences on

the structure, composition and space-time develop-

ment of these communities in each lagoon.

Phytoplankton in Merja Zerga showed a quasi-perma-

nent predominance of marine diatoms in the open sea

station and in the marine inlet channel. Dinoflagellates

were abundant in summer and early autumn in the

marine inlet and extended into the central lagoon

station. In Ghar El Melh, marine species (especially

diatoms and dinoflagellates) dominated despite occa-

sional winter inflows of freshwater. In Lake Manzala,

freshwater species generally predominated and the

planktonic communities were comparatively very

diverse. Chlorophyceae contributed 39% of the total

species recorded and diatoms and cyanophyceans were

also common; the Dinophyceae, Euglenophyceae,

Chrysophyceae and Cryptophyceae less so. Zooplank-

ton communities in both Ghar El Melh and Merja

Zerga were dominated by marine copepods. Rotifera,

Copepoda, Ostracoda, and Cladocera were recorded in

both lagoons as were meroplanktonic larvae of Poly-

chaeta, Cirripedia, Mysidacea and Gastropoda and free

living nematodes. Ghar El Melh was the more

productive of these two lagoons with spring and early

Guest editors: J. R. Thompson & R. J. Flower

Hydro-ecological Monitoring and Modelling of North African

Coastal Lagoons

Electronic supplementary material The online version ofthis article (doi:10.1007/s10750-008-9678-4) containssupplementary material, which is available to authorized users.

M. Ramdani (&)

Department of Zoology & Animal Ecology, Institut

Scientifique, University Mohamed V, Charia Ibn Batouta,

Rabat Agdal BP703, Morocco

e-mail: mramdani@israbat.ac.ma

N. Elkhiati

Faculte des Sciences, Biologie, Universite Hassan II Ain

Chock, Km 8, Route El Jadida, Casablanca, Morocco

R. J. Flower � J. R. Thompson

UCL Department of Geography, Environmental Change

Research Centre/Wetland Research Unit, University

College London, Gower Street, London WC1E 6BT, UK

L. Chouba � M. M. Kraiem

INSTM, Rue de 2 mars 1934, No. 28, Salammbo, Tunis

2025, Tunisia

F. Ayache

Department de Geography, Faculte des Lettres & Sciences

Humaines, Universite de Sousse, Sousse 4029, Tunisia

M. H. Ahmed

Department of Marine Resources, National Authority for

remote sensing and Space Sciences, 23 Josef Burrows

Tito Street, El Nozha, Al Gadida, PO Box 1654, Cairo,

Egypt

123

Hydrobiologia (2009) 622:113–131

DOI 10.1007/s10750-008-9678-4

summer being the productive seasons. Zooplankton

communities in Lake Manzala were generally domi-

nated by rotifers and highest zooplankton abundances

occurred in April (2003). Sampling stations near the

marine inlets showed the highest diversity and the

zooplankton communities showed considerable spatial

variation within this large lagoon. The three lagoons

represent very different water bodies contrasted

strongly in terms of tidal effects and freshwater

availability. Yet, there are some similarities in eco-

system structure. Space-time development of the

plankton communities was similar especially in Merja

Zerga and Ghar El Melh. Species abundances and

specific diversities indicated that seasonal changes in

salinity and nutrient concentrations were the main

influential factors. Lake Manzala was the most

productive lagoon and all the three sites supported

toxic algal species. Relatively low plankton biomass in

Merja Zerga and Ghar El Melh probably resulted from

a combination of factors including highly episodic

nutrient inputs, light suppression (by turbidity) and

nutrient competition with benthic algae. Water quality

variables were largely driven by the hydrological

regime specific to each lagoon. Nutrient enrichment

and, particularly for Lake Manzala, sea level rise

threaten the sustainability of the planktonic ecosys-

tems in all three lagoons.

Keywords Coastal lagoons � Water chemistry �Plankton � Hydrology � Monitoring

Introduction

Plankton communities in coastal lagoons are of major

importance in food web structures and for ecosystem

health. Coastal lagoons are often heavily impacted by

human activities and eutrophication is one of the

several processes that can degrade water quality and so

alter plankton species abundances (e.g. Delgado,

1990). Precise species changes are difficult to predict

(e.g. Gamito et al., 2005), but hydrological modifica-

tions of freshwater inflows and of marine inlet channels

can bring about major changes in lagoon ecosystems

and particularly in the plankton (Borja, 2005). The

structure of plankton communities in any coastal water

body is especially important, not the least for com-

mercial fisheries in relation to environmental change.

Phytoplankton is the main primary producer in most

lagoon ecosystems (Khalil, 1990; Romdhane et al.,

1998; Scheffer, 1998; Daly Yahia et al., 2001; Sakka

Hlaili et al., 2003; Mageed, 2006) and, as well as

biomass, the species composition of phytoplankton

communities influences the ecological status of a site,

with particular species being good indicators of either

high or low ecological status (Hutchinson, 1967, 1975;

Talling, 1976; Talling & Lemoalle, 1998; Fathi et al.,

2001; Borja, 2005; EC Water Framework Directive -

2000/60/E).

As a consequence of a dry climate and intensive

land use, coastal lagoons in the Southern Mediterra-

nean Region (SMR) are particularly vulnerable to

disturbance and environmental change. Notably, agri-

cultural exploitation of land around many SMR lakes

and lagoons has expanded strongly during the twen-

tieth Century (e.g. Flower, 2001). Freshwater

resources in the region have been generally impacted

by increasing water demand from a growing local

population and associated land use changes (Ayache

et al., 2009; Thompson et al., 2009). In the future these

impacting factors will be exacerbated by predicted

global climate change, including sea level rise.

Relatively little research has been undertaken on

aquatic ecosystems within SMR lagoons, although

some environmental factors influencing aquatic com-

munities have been investigated. Some studies

demonstrated human pressures and declining envi-

ronment quality in some lagoons (e.g. Meininger &

Mullie, 1981; Saad et al., 1985). In the late 1990s, the

CASSARINA Project (Flower, 2001) used sediment

records to reveal past changes in aquatic communities

in several North African lagoons (e.g. Birks et al.,

2001; Flower et al., 2001) and linked studies

evaluated the status of plankton (Fathi et al., 2001;

Ramdani et al., 2001a, b, c) and fish (Kraıem et al.,

2001). In 2002, follow-up work was initiated as part

of the MELMARINA (Monitoring and Modelling

Coastal Lagoons: Making Management Tools for

Aquatic Resources in North Africa) Project (Flower

& Thompson, 2009). The project (funded through the

EU INCO-Med programme) set base lines and

undertook integrated hydro-ecological monitoring at

selected sites to ascertain the impacts of environment

and management changes and to enable setting of

future scenarios through hydroecological modelling.

This article undertakes assessment of water quality

and describes the results of qualitative and quantita-

tive sampling of both phytoplankton and zooplankton

114 Hydrobiologia (2009) 622:113–131

123

communities in three lagoons, Merja Zerga (Mor-

occo), Ghar El Melh (Tunisia) and Lake Manzala

(Egypt).

Sites, materials and methods

The MELMARINA primary lagoons

Detailed accounts of the three MELMARINA

primary lagoons are provided by Ayache et al.

(2009). All the three lagoons have considerable value

for biodiversity, which include both fish and birds.

The Moroccan site, Merja Zerga (Fig. 1a), is linked

to the Atlantic Ocean by a single channel (the

‘‘gullet’’), that is strongly tidal and, at high tide, is

connected with a smaller lagoon, the Merja Khala.

Open water area at high tide is approximately

13.2 km2 (2003) and at low tide, large areas of mud

flats are exposed. Macroalgae (Enteromorpha and

Ulva) are very common on these mud flats and in

intertidal depressions. The mud flats are exploited for

edible molluscs (Ruditapes decussatus). The margins

of the lagoon are managed for agriculture, including

cattle and sheep grazing and cash crops. Merja Zerga

is well known as a bird reserve and as an area of

outstanding natural beauty. Its hydrology and vege-

tation have been studied since the 1970s and the

plankton since 1986 (Ramdani, 1988; Ramdani et al.,

2001a, b; Fraikech et al., 2005).

Ghar El Melh, on the northeast coast of Tunisia

(Fig. 1b), has also received considerable attention

regarding water quality and plankton and the large

migrant bird populations (Morgan & Boy, 1980; Daly

Yahia & Romdhane, 1994; Souissi et al., 2000; Daly

Yahia et al., 2001; Benrejeb-Jenhani & Romdhane,

2002). The lagoon, which has a total area of approx-

imately 35.6 km2, is separated from the Mediterranean

by sand bars through which there is one main and

several smaller connections to the sea. The lagoon is

subject to the relatively small Mediterranean tidal

regime. It is mainly surrounded by agricultural land

and the littoral margins support abundant growth of

macroalgae (Enteromorpha and Ulva), especially on

the north and western shores. In summer months, a

mat of filamentous green algae develops over much

of the submerged surface sediments. Occasional large

winter freshwater inflows from the diverted Mejerda

River occur (Ayache et al., 2009) and can temporarily

lower lagoon salinity. In general, however, salinity

remains near that of seawater, fluctuating between 27

and 48 % annually. The freshwater inflows deliver

sediment and agro-chemicals from farmland. Birds

frequent the shallow SE part of the lagoon and the

small fishery comprises eel, mullet, sea-bass and sole

(Kraıem et al., 2009).

Egyptian Lake Manzala is the largest of the four

Nile Delta lakes with an area of c. 700 km2 (Fig. 1c). It

has been much reduced by twentieth Century recla-

mation, and Meininger & Mullie (1981) noted that the

lake formerly occupied 1710 km2. It is shallow

(average depth c. 1 m with 25% of the area \ 60 cm

deep, Shaheen & Yosef, 1987). The lake is linked to

the Mediterranean by several channels the largest of

which is at El Gamil. In the southern sector, there are a

number of drains, including the grossly polluted Bahr

Fig. 1 Sample locations within the MELMARINA lagoons (a) Merja Zerga (Morocco), (b) Ghar El Melh (Tunisia), (c) Lake

Manzala (Egypt)

Hydrobiologia (2009) 622:113–131 115

123

El Baqar, which discharge freshwater to the lake.

Much of the northwestern and eastern sectors are now

wholly or partly reclaimed or converted to fish

farming. Similarly, extensive areas of reclaimed lake

bed, which are not intensively farmed, border the lake

to the south. The lagoon still retains extensive

emergent and submerged aquatic plant communities

and provides approximately 50% of the total inland

fisheries within Egypt. It is highly threatened by

pollution (Khalil & Salib, 1986; Shaheen and Yosef,

1987), and sea level rise and geological subsidence

(Stanley & Warne, 1994; Saad et al., 1985). A number

of studies of Lake Manzala’s plankton have been

undertaken (El-Hawary 1960; Samaan & Aleem,

1972; Samaan, 1977; El-Sherif & Aboul-Ezz, 1988;

Radwan & Popiolek, 1989; Khalil, 1990; Guerguess,

1993; Aboul-Ezz, 1995; El-Naggar et al., 1997;

Gharib & Soliman, 1998; Aboul-Ezz & Soliman,

2000; Zaghloul & Hussein, 2000; El-Sherif & Gharib,

2001; Fathi et al., 2001, Khalifa & Mageed, 2002;

Abdel-Aziz & Aboul-Ezz, 2004, Mageed, 2006;

Zakaria et al., 2007).

Water quality monitoring

Within each lagoon representative water sampling

stations were selected: four in Merja Zerga, five in

Ghar El Melh, and ten in Manzala. All stations were

sampled at approximately monthly intervals from July

2003 to September 2004. For tidal Merja Zerga,

sampling was undertaken at approximately the same

time in the tidal cycle. Water clarity was assessed by

Secchi disc. Dissolved oxygen was determined by the

azide modification of the Winkler method (according

to APHA, 1995). Water temperature, pH, conductiv-

ity, total dissolved solids (g l-1) and dissolved oxygen

were measured using field probes (EXTECH, YSI or

Mettler Toledo). Water quality and phytoplankton

samples were collected from the subsurface water

column by hand dipping a one-litre sample bottle.

Samples for nitrate, total nitrogen (TN), inorganic

phosphorus and chlorophyll-a were treated according

to Grasshoff (1976). Before assay, samples were

filtered through 47 mm GF/C filters (nominal porosity

1.2 lm). In the laboratory, analyses were made using

a LKB 4050 spectrophotometer according to standard

procedures (Parsons et al., 1984) and results were

expressed in mg l-1. Total phosphorus (TP) was

assayed by spectrophotometry after reaction with

ammonium molybdate and reduction by ascorbic acid

(Murphy & Riley, 1962). Nitrate was assayed by ionic

chromatography using a Shimadzu ion chromatograph

HIC-6A (limit of detection for NO3 was less than

1.0 mg l-1). This apparatus was equipped with an ion-

exchange resin that is stable to a wide range of salt

concentrations. Appropriate blanks and standards

were used to calibrate each analytical method (APHA,

1995; Souissi et al., 2000; Fathi et al., 2001).

Plankton sampling

Phytoplankton samples were concentrated by sedi-

mentation (Sournia 1986; Hallegraeff et al., 1995).

Identification and enumeration were done under an

inverted microscope (Axiovert 25C—Egypt and

Olympus C-K2—Morocco and Tunisia) at 6009

magnification. Identification of the species and their

taxonomic categories were according to Tregouboff &

Rose (1957), Sournia (1986), Ricard (1987), Delgado

& Fortuna (1991), Hallegraeff et al. (1995) and Tomas

(1997). All cell counts were corrected to abundances in

1 litre original sampling volume. Zooplankton sam-

ples were collected at the same time as phytoplankton.

For Ghar El Melh and Merja Zerga, plankton samples

for Copepods, Cladocera and Rotifera were collected

with a standard 20 cm diameter plankton net (55-lm

mesh size) drawn through c. 20 m of open water at

each water quality sampling station (Fig. 1). For Lake

Manzala, zooplankton samples were collected by

filtering 50 l of lake water through a standard plankton

net (55-lm mesh size) and fixing in 4% formalin. A

Dollfus Vat was used to fractionate the samples and to

facilitate counting of the zooplankton (Ramdani, 1988;

Paterson, 1993, Ramdani et al., 2001b). The number of

species of Copepoda, Cladocera and Rotifera as well

as other zooplanktoners was estimated using tech-

niques from Dussart (1969), Rougier & Lam Hoai

(1997) and Ramdani et al. (2001c). For Manzala,

samples were concentrated to 100 ml prior to micro-

scopical examination. For specific enumeration

purposes, at least two 2-ml aliquots were used and

the total number of zooplankton determined so that

abundances and total numbers per m-3 could be

calculated. Species identifications and their taxonomic

categories were according to Tregouboff & Rose

(1957), Hutchinson (1967, 1975) and Dussart (1969).

Toxic phytoplankton species were identified using the

Hallegraeff et al. (1995) classification.

116 Hydrobiologia (2009) 622:113–131

123

Statistical analyses

A matrix of the normalized physical, chemical and

biological data was produced and analysed by means

of principal components analysis (PCA) using SPSS

software version 9.01n. This type of statistical

analysis is used when uniform linear relationships

are likely to exist between variables (Doledec &

Chessel, 1989). Differences between the three study

lagoons were tested by one-way analysis of variance

(ANOVA).

Results

Hydrochemistry

Water quality data are summarized for each sampling

station at all three sites in Fig. 2 and Supplementary

Material Table 1. This figure provides the maximum,

minimum and average values. The principal charac-

teristics of these data are described as follows:

Merja Zerga: Water temperature (12.1–23.5�C)

and pH values (7.7–8.4) varied seasonally. Open water

salinity was higher in summer (35.7 %) and the lowest

in autumn (13.2 %) in station Z1. Open water showed

only slight variations in salinity during the year (c. 35

%). Sample sites Z2 and Z3 near drainage inflows

were fresher and the salinity fluctuated between 2 and

12 % (Fig. 2). The maximum oxygen concentration

was recorded in autumn (12.6 mg l-1). Chlorophyll-a

peaked in spring–summer at 7.6 lg l-1. Total soluble

salts were higher in summer but dropped to minimum

levels through the autumn. Total phosphorus concen-

trations showed no regular trend but were the lowest in

the autumn (at c. 0.5 mg l-1). The maximum nitrate

concentration (10.7 mg l-1) was recorded in spring

adjacent to the Nador Canal (Fig. 2). Water transpar-

ency was higher in summer and lower in autumn and

winter at all stations and, during the flood period

(November and December); Secchi disc depth at Z2

and Z3 was nearly 1 cm but reached 45 cm in the

summer period.

Ghar El Melh: The maximum water temperature

(32�C) was recorded in summer (July). Water pH

values were from 7.3 (winter) to 9.3 (summer) and

salinities ranged from 43.5 % (summer) to below 29

% (winter). Oxygen concentration was around

15 mg l-1 in late autumn but increased during summer

when phytoplankton activity was high. Chlorophyll-a

values showed only small fluctuations during the year

(3.0–12.3 lg l-1). Total phosphorus concentrations

were higher (0.36–7.04 mg l-1) than in Merja Zerga

(0.5–1.6 mg l-1). Maximum nitrate concentrations (c.

50 mg l-1) were recorded in spring. Water transpar-

ency was greater during spring and summer when

Secchi disc depths were[50 cm.

Lake Manzala: Water temperature ranged from

15�C in winter to a maximum of 31.3�C in summer.

pH varied from 6.3 to 9.3. Salinity was low and

varied from 1.4 % in spring to 20.3 % in summer (at

station M2). Open water was always well oxygenated

during day time and varied from 6.7 mg l-1 in

summer to 15.3 mg l-1 in winter. The total soluble

salts were higher in summer and dropped to minimum

levels through the autumn. Total phosphorus concen-

trations showed no regular trends but were high at all

stations at around 8.5 mg l-1. The highest nitrates

concentration (10.7 mg l-1) was recorded in spring.

Water transparency was higher in the northwest part

of the lagoon where macrophytes were present

(Secchi disc depth usually[60 cm or to the sediment

surface) and lower in the turbid eastern part of the

lake (typically \25 cm).

Phytoplankton composition and abundance

A total of 314 phytoplankton taxa were identified at

the three lagoons. These included 68 Dinophyceae,

131 Bacillariophyceae, 29 Cyanophyceae, 67 Chlo-

rophyceae, 8 Euglenophyceae, 3 Chrysophyceae, 6

Cryptophyceae and 2 Silicoflagellate taxa (see

Supplementary Material Tables 2–5).

Merja Zerga and Ghar El Melh: Diatoms were

dominant in terms of the number of species and

abundance in these two lagoons (Fig. 3). The highest

number of species occurred in spring and summer in

both lagoons, but in summer and autumn the number

of Dinophyceae species usually exceeded that of the

diatoms. The lowest number of phytoplankton species

in Merja Zerga occurred in November and December

(Fig. 4). In terms of phytoplankton species succession,

the diatoms were most abundant during April–May

(Pseudonitzschia pseudodelicatissima, Nitzschia spp.,

Rhizosolenia sp.) as was the dinophyceaean Ceratium.

In early April, species of Chaetoceros and Navicula

were dominant in terms of both abundance and

the number of the species. In summer the diatoms

Hydrobiologia (2009) 622:113–131 117

123

Licmophora spp, Navicula spp, Nitzchia spp. and

Pleurosigma elongatum, together with the dinophy-

ceaeans Ceratium spp and Protoperidinium spp., were

most common. Nitzchia was of particular significance

with 31 species identified at all the sites and Navicula

with 15 species. In summer (June–August), Ceratium

and Protoperidinium (Dinophyceae) were usually the

dominant species. The genus Protoperidinium

attained the highest diversity (11 species) at Ghar El

Melh in November–January when Dinoflagellate cell

numbers were at their lowest (7 9 104 cells m-3).

Only in September did dinoflagellate cell numbers

exceed those of diatoms at the open sea sampling

station. This was due to a predominance of Peridinium

spp. and Scrippsiella trochoidea. In both lagoons,

Dinoflagellate cell numbers reached 12 9 106 cells

Fig. 2 Water chemistry in the three lagoons: Z—Merja Zerga, G—Ghar El Melh, M—Lake Manzala; Vertical bars = maximum,

minimum and average values (July 2003–September 2004)

118 Hydrobiologia (2009) 622:113–131

123

m-3 at this time, but in November they declined (to

c. 25 9 103 cells m-3). The highest cell concentration

in Merja Zerga was 7 9 106 cells m-3 in June whereas

for Ghar El Melh the highest concentration (9 9 107

cells m-3) was in July. In Ghar El Melh, dinoflagellates

were the most abundant, especially Alexandrium

foedum, Ceratium furca, Coolia monotis, Peridinium

quinquecorne, Prorocentrum compressum and

Prorocentrum concavum. Some of these species are

toxic (see Table 1). In June, the diatoms were mainly

dominated by benthic species (Licmophora gracilis and

Navicula cocconeiformis). The central lagoon areas

were more productive during spring and summer, but

Merja Zerga was more influenced by brackish species

than Ghar El Melh lagoon, which was characterized by

marine forms.

0

200

400

600

800

1000

1200

1400

1600

Z1 Z2 Z3 Z4 G1 G2 G3 G4 G5 M1 M2 M3 M4 M5 M6 M7 M8 M9 M10

Num

ber

of c

ells

x 1

05 m-3 Chlorophyceae Bacillariophyceae

Euglenophyceae Cyanophyceae

Dinophyceae Cryptophyceae

Silicoflagellates

Fig. 3 Mean

phytoplankton biomass at

each monitoring stations

within the three

MELMARINA lagoons

(July 2003–September

2004)

0

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40

60

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100

120

140

160

Jul-0

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ber

of c

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x 1

06m

-3N

umbe

r of

cel

ls x

105

m-3

Num

ber

of c

ells

x 1

05m

-3

Bacillariophyceae Dinophyceae

Silicoflagellates Euglenophyceae

Cyanophyceae

0

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Bacillariophyceae DinophyceaeSilicoflagellates Euglynophyceae

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Bacillariophyceae Euglenophyceae

Cyanophyceae Chlorophyceae

Cryptophyceae

No Data

(a)

(b)

(c)

Fig. 4 Phytoplankton

biomass during the

MELMARINA monitoring

period (July 2003–

September 2004). (a) Merga

Zerge Z1. (b) Ghar El Melh

G1. (c) Lake Manzala (M3)

Hydrobiologia (2009) 622:113–131 119

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The phytoplankton communities at Lake Manzala

were diverse and were of essentially freshwater

species. They were represented by 163 species

belonging to seven classes (Supplementary Material

Tables 2–5). The green algae were dominant, but

diatoms and cyanophytes were common at stations

M6–M10 (Fig. 3). Other groups (7 Dinophyceae, 5

Euglenophyceae, 2 Chrysophyceae, 2 Cryptophyceae

and 1 Silicoflagellate species) were minor constitu-

ents of the phytoplankton. The green algae

constituted c. 48% of the total species recorded (67

species) and c. 77% of the total phytoplankton

abundance during spring with 91 9 106 cells m-3

at station M4. The western part of Lake Manzala

(stations M7, M8 and M9) supported lower phyto-

planktonic abundances compared to the other

stations, while stations 1, 2 and 5 attained maximum

population densities during the period of investiga-

tion. A gradual increase in phytoplankton population

densities was observed from March till June; the

highest density (780 9 107 cells m-3) was recorded

in April at M3. Diatoms ranked second in terms of

both species occurrence (c. 27%; 48 species) and the

total abundance (c. 18%; 98 9 107 cells m-3)

(Fig. 4). Cyanophytes formed c. 15% of the total

species recorded and c. 4 9 107 cells m-3 of the total

phytoplankton abundance. The green algae Ankis-

trodesmus spp, Dictyosphaerium pulchellum,

Kirchneriella spp, Pyramimonas spp, Scenedesmus

spp and Selenastrum spp were the most important

algae in the Lake Manzala communities. Diatoms

were typically freshwater or brackish water species

and mainly represented by the three taxa Cyclotella

meneghiniana, Nitzschia closterium and N. frustulum

var. perpusilla (at stations M3, M4 and M5). The

most important cyanophyceans were Microcystis aeru-

ginosa, Rhabdoderma lineare var. unicella and

Spirulina major and these characterized the western

part of the lake (stations M7 to M10). Cryptophyceae

were represented by Chroomonas acuta, C. erosa,

C. vata, Cryptomonas sp. and Rhodomonas sp. Euglen-

ophyceae (Euglena acus, E. clara, E. hemichromata,

E. proxima and E. viridi) were also represented, mostly

in the western and central parts of the lake.

Toxic species of phytoplankton were recorded in

all the three lagoons and, following the UNESCO

(Hallegraeff et al., 1995) classification, seven groups

of harmful algae were identified (Table 1). These

occurred mainly during summer and autumn. Dino-

flagellates and, to a lesser extent cyanophyceans,

comprised the most harmful groups and particularly

noteworthy are the dinoflagelate Gonyaulax spinifera

Table 1 Phytoplankton toxic species identified in the three lagoons following the classification of UNESCO (Hallegraeff et al.,

1995)

Useful,

but mostly

harmless

Oxygen

depletion

Paralytic

shellfish

poisoning

Diarrheic

shellfish

poisoning

Neurotoxic

shellfish

poisoning

Amnesic

shellfish

poisoning

Ciguatera

fish

poisoning

Gonyaulax spinifera GEM

Prorocentrum micans GEM, Zerga

Dinophysis caudata GEM, Zerga

Alexandrium tamarense GEM

Gymnodinium catenatum Zerga

Dinophysis acuminata GEM, Zerga

Dinophysis caudata GEM, Zerga

Gymnodinium breve Zerga

Pseudonitzschia spp GEM, Zerga

Coolia monotis GEH

Osteopsis sp. Zerga

Prorocentrum lima GEM, Zerga

Amphidinium sp. Zerga

Microcystis flos-aque Manzala

Microcystis aeruginosa Manzala

120 Hydrobiologia (2009) 622:113–131

123

in Ghar El Melh, Dinophysis species in both Ghar El

Melh and Merja Zerga, and Microcystis aeroginosa

and M. flos-aquae in Lake Manzala.

Zooplankton composition and abundance

Analysis of the zooplankton communities in the three

lagoons revealed five major groups: Copepoda,

Rotifera, Cladocera, Ostracoda and Protozoa

(Supplementary Material Tables 6–8). Other marine

representatives (meroplanktonic larval Polychaeta,

Cirripedia, Mysidacea and Gastropoda and the free-

living nematods) were also occasionally encountered

in some samples. Merja Zerga and Ghar El Melh

lagoons were both dominated by copepods (48 and 55

species, respectively). Copepods were mainly marine

species (Supplementary Material Table 6) in both

these lagoons, but more freshwater Cladocera and

rotifers were found in samples from the stations (Z2

and Z3) near the Oued Drader and Nador Canal in

Merja Zerga (Supplementary Material Tables 7–8).

These taxa were either very rare or totally absent in

Ghar El Melh. The minimum zooplankton standing

crop was 75 ind m-3 in Merja Zerga (Z1) during

November and December (Fig. 5). Peaks occurred

during spring and early summer, with a minimum

standing crop of 130 ind m-3 and maximum abun-

dance of c. 700 ind m-3 in April, May and June.

Open sea stations in both Merja Zerga and Ghar El

Melh were often more diverse and more productive

than in the central areas of each lagoon.

At Lake Manzala, Rotifera were remarkably abun-

dant and constituted the main group of zooplanktoners

comprising c. 80% of the total number in all the

sampled stations (Fig. 5). Five species dominated the

Rotifera: Brachionus angularis, B. urceolaris,

B. calyciflorus, B. plicatilis and Colurella adriatica

and were most common in the southern part of the

lagoon. The genus Brachionus was represented by

eight species in the western part of the lake (stations

M6–M10). The Copepods constituted the second most

abundant group forming c. 14% of the total number of

zooplankton individuals. The average zooplankton

standing crop at Manzala was relatively high with a

minimum of 50 9 104 ind m-3 in February and

August and a maximum of c. 300 9 104 ind m-3 in

April at M6. The marine copepod species Euterpina

acutifrons and Oithona nana were only recorded in

the northern part of the lake near the El Gamil

connection with the Mediterranean.

Discussion

All the three of the MELMARINA primary lagoons

share some similarities in terms of location and near

catchment landscape. They all occur at the termini of

inland drainage systems where land is modified

principally for agriculture by land drainage. Hydrol-

ogy exerts a major influence on the environmental

conditions at each lagoon. Merja Zerga is subjected to

daily flushing by Atlantic tides whereas tidal effects

are much less at Ghar El Melh and Lake Manzala

because of the smaller Mediterranean tidal regime.

Lake Manzala is differentiated by its freshwater

character as a result of large discharges from land

drains along the lake’s southern margin (Ayache

et al., 2009; Thompson et al., 2009). These differ-

ences have major implications for both the water

quality and the plankton of the three lagoons, and

these are now considered and relationships are

evaluated using statistical methods.

Water quality

The concentrations of nutrients in the three lagoons

and their variations are largely controlled by the

quality of drainage water entering and leaving the

lagoon and the uptake of nutrients by plant assimila-

tion. The concentrations and distribution of nutrients

can be strongly affected by the mixing of the water

through the lagoon–sea connection (Thompson et al.,

2009). Absorption on suspended sediment and sub-

sequent deposition/resuspension may also play an

important role in determining nutrient concentrations

in lagoon water. Significant sources of nitrate and total

phosphorus for Merja Zerga are the drainage waters

from the Nador Canal and Oued Drader inflows. For

Ghar El Melh, nutrients enter from drainage of the

agricultural Utica floodplain as well from several

significant point sources that include the town of Ghar

El Melh and, exceptionally, from overflow of the

Mejerda River. Within Lake Manzala, the Bahr El

Baqar drain is a well-known source of urban waste

water with high concentrations of total phosphorus

and nitrate (Fathi et al., 2001; Mageed, 2006). Except

during freshwater floods and otherwise poor weather,

Hydrobiologia (2009) 622:113–131 121

123

water transparency was generally higher in Merja

Zerga and Ghar El Melh than at most stations in

Manzala Lake. However, suspended sediments and

therefore transparency in Merja Zerga varied daily

according to the tidal cycle and both the lagoons were

subject to wind-induced sediment resupension (cf.

Flower et al., 2009). In Lake Manzala, in those areas

that have retained submerged macrophytes communi-

ties, the water was very clear and the emergent

macrophyte beds offered protection from high winds.

Elsewhere in the Nile Delta lagoons water transpar-

ency is now generally low (Mageed, 2006) due to their

shallowness, frequent sediment resuspension as well

as to high phytoplankton productivity. It is likely that

Lake Manzala is currently switching from a sub-

merged macrophyte-dominated clear water system to a

turbid phytoplankton-dominated system, according to

alternative equilibrium state theory (Scheffer et al.,

1993, Scheffer, 1998). The lower dissolved oxygen

values in southern Manzala (stations WQ6–10)

0

200

400

600

800

Z1 Z2 Z3 Z4 G1 G2 G3 G4 G5

Indi

vidu

als

m-3

Indi

vidu

als

m-3

Indi

vidu

als

m-3

OthersOstracodsRotiferaCladoceraCopepoda

0

500

1000

1500

2000

2500

3000

M1 M2 M3 M4 M5 M6 M7 M8 M9 M10

Indi

vidu

als

m-3

0

200

400

600

800

Jul-0

3

Aug

-03

Sep

-03

Oct

-03

Nov

-03

Dec

-03

Jan-

04

Feb

-04

Mar

-04

Apr

-04

May

-04

Jun-

04

Jul-0

4

Aug

-04

Sep

-04

0

200

400

600

800

Jul-0

3

Aug

-03

Sep

-03

Oct

-03

Nov

-03

Dec

-03

Jan-

04

Feb

-04

Mar

-04

Apr

-04

May

-04

Jun-

04

Jul-0

4

Aug

-04

Sep

-04

0

500

1000

1500

2000

2500

3000

Jul-0

3

Aug

-03

Sep

-03

Oct

-03

Nov

-03

Dec

-03

Jan-

04

Feb

-04

Mar

-04

Apr

-04

May

-04

Jun-

04

Jul-0

4

Aug

-04

Sep

-04

Indi

vidu

als

103m

-3

(a) (b)

(c)

(d)

(e)

Fig. 5 Zooplankton biomass during the MELMARINA mon-

itoring period (July 2003–September 2004). (a) Mean values at

each station within Merga Zerga and Ghar El Melh. (b) Mean

values at each station within Lake Manzala. (c) Monthly values

at Merja Zerga Z1. (d) Monthly values at Ghar El Melh G1. (e)

Monthly values at Lake Manzala (M3). Note: different y-axis

scales for Lake Manzala

122 Hydrobiologia (2009) 622:113–131

123

provide further evidence of eutrophication and decom-

position of excess organic matter. Because of its size

and array of nutrient sources, Lake Manzala showed

the highest values and the greatest spatial variation in

nutrients compared to the Merja Zerga and Ghar El

Melh lagoons.

The concentrations of total phosphorus indicated

the pattern of drainage water distribution in Lake

Manzala. Higher concentrations of total phosphorus

generally occurred in the southern and eastern zones of

the lake (near to the drainage canals and to the waste

water treatment works). Nitrate concentrations were

also relatively high in stations near the drains. They

reached their highest values during spring–summer

while total phosphorus concentrations peaked after-

wards. Nutrient concentrations in general declined in

late summer probably due to increased uptake by

phytoplankton and benthic algae and by the sub-

merged and emergent macrophytes. In Lake Manzala,

nutrient concentrations generally decreased towards

the sea connections and probably indicate several

processes: adsorption and sedimentation, plant assim-

ilation and flushing through the El Gamil channels.

Guerguess (1993) and Ahmed et al. (2009) identify the

drains as the main source of phosphate to the lake, and

the data presented here indicate that the nutrient-rich

drainage water is diluted and distributed across the

lake in a northerly direction. This pattern is modified

by emergent vegetation stands and water circulation

(Rasmussen et al., 2009a, b). Contaminated freshwater

is undoubtedly the major source of nutrients in all the

lagoons although in some periods nutrients may be

transported in from the coastal zone (i.e. as suspected

for Ghar El Melh, Rasmussen et al., 2009b). Nutrient

concentrations recorded in Ghar El Melh were lower

than the previous findings for Bizerte lagoon (Sakka

Hlaili et al., 2003). For Merja Zerga, the highest

nutrient concentrations were recorded adjacent to the

Canal Nador and Oued Drader. As indicated by

modelling results (Rasmussen et al., 2009a, b),

reduction of nutrient inputs, especially phosphorus,

is needed in these coastal lagoons.

In order to reveal correlations between the various

physico-chemical parameters measured in the three

lagoons, ADE4 software (Data Analysis functions to

analyse Ecological and Environmental data in the

framework of Euclidean Exploratory methods) was

applied. Twelve environmental variables (descriptors)

were used: temperature (�C), pH, salinity (%),

dissolved oxygen (mg l-1), suspended sediment

(mg l-1), nitrate (mg l-1), total nitrogen (mg l-1),

total phosphorus (mg l-1), chlorophyll-a (lg l-1),

alkalinity (mg l-1), mean depth (cm) and transparency

(cm). A correlation matrix between the components

was constructed which gave each variable equal

importance and simplified analysis of a large data set

(Ayadi et al., 2002). The relationship of these variables

with the first two axes of variation indicates the most

influential variables. Principal Component Analysis

(PCA) was applied and the environmental data com-

ponents biplot of the first two axes are shown in Fig. 6.

These highlight the close correlation between salinity

and transparency, which is in contrast to alkalinity,

chlorophyll-a, total phosphorus, nitrate and total nitro-

gen along the first axis. Mean depth, salinity and

temperature are more correlated with the second axis.

Variables associated with axis 1 indicate a eutrophica-

tion gradient and the analysis illustrates clearly the

tendency of Lake Manzala towards eutrophication.

Axis 2 is related to hydrologically linked factors

(Fig. 6, left). PCA ordination of the data according to

the 19 reference stations (Fig. 6, right) highlights the

water quality differences between both the sites and the

sampling stations. Sample points are all well discrim-

inated according to each lagoon. In Lake Manzala,

stations are clearly discriminated by being fresher and

richer in nutrients (phosphate and nitrate). The Merja

Zerga sampling stations are differentiated by salinity

and (moderate) nutrient concentrations; similarly Ghar

El Melh stations are characterised by (lower) nutrients

and salinity differences.

Phytoplankton

Phytoplankton abundance in all the three lagoons

displayed significant fluctuations according to season

and to location. Cell numbers decreased in November

and January and then increased in March. The highest

cell concentrations were found during the summer

period when relatively large individuals dominated.

The summer increases were attributed to higher cell

numbers of Pseudonitzschia spp, Licmophora spp,

Navicula spp and Pleurosigma elongatum. These

diatoms reached 24,400 cells l-1 in Ghar El Melh and

35,000 cells l-1 in Merja Zerga. The latter three

species are predominantly benthic in habit, and their

abundance in the plankton samples probably reflects

benthic productivity and turbulent suspension of the

Hydrobiologia (2009) 622:113–131 123

123

shallow water surface sediments. Pseudonitschia spp

have long needle-like cells, and Sournia (1986) noted

that larger phytoplankton species respond more

quickly to favourable conditions and tend to domi-

nate the community at the time of bloom. Diatoms

and dinoflagellates comprised 82.5% and 15.5% of

cell numbers, respectively, and their diversity was the

lowest in winter. The 211 identified phytoplankton

taxa (Supplementary Material Table 3) include spe-

cies previously identified elsewhere in Mediterranean

lagoons and bays by Delgado (1990), Fathi et al.

(2001), Benrejeb-Jenhani & Romdhane (2002), Sakka

Hlaili et al. (2003) and Fraikech et al. (2005).

Overall, phytoplankton cell numbers recorded in

this study for Ghar El Melh and Merja Zerga were

lower than those previously reported by Sakka Hlaili

et al. (2003) for the Gulf of Tunis. In general, large

phytoplankton species were dominant but they did

not reach high concentrations in Merja Zerga. In Ghar

El Melh, the concentrations reached 9 9 105 cells l-1

during July–August when benthic diatoms (Licmo-

phora gracilis and Navicula sp. were common).

However, it is likely that the small size groups, such

as picophytoplankton (\2 lm), have great impor-

tance in these warm water sites (cf. Agawin et al.,

2000). Dinoflagellate abundance diversity was quite

low during the study period but, on a seasonal basis,

overall phytoplankton species diversity was the

highest in spring and summer. Delgado & Fortuna

(1991) also noted that one or a few species were

dominant in phytoplankton blooms in the early winter

period. In contrast to other findings (Delgado, 1990;

Ayadi et al., 2002) from the Mediterranean, a

significant positive relationship was found in the

SMR lagoons between temperature and phytoplankton

abundance (r = 0.72, P \ 0.01).

Combined ordinations (DCA) of the phytoplank-

ton data (samples and species) for the three lagoons

(Fig. 7) clearly separated Merja Zerga and Ghar El

Melh where the marine species (dinoflagellates and

diatoms) were often dominated from Lake Manzala

where the freshwater species (Chlorophyceae, fresh-

water diatoms and Cyanophyceae) were abundant.

Zooplankton

Zooplankton can influence the phytoplankton com-

munity through preferential grazing. In turn, nuisance

cyanobacteria (e.g. Microcystis aeroginosa) may

affect copepod community structure by allowing

certain species to out-compete others (Bautista &

Harris, 1992). Many authors have reported a direct

M8

Z4

G4

G3G1

G5

Component 1 C

ompo

nent

2 Z3

Z2

Z1

G2

M9

M7

M6 M5

M4M3

M1

M2

M10

Transparency

pH

Depth

Com

pone

nt 2

Total Nitrogen

Salinity Nitrates

Dissolved Oxygene

Total Phosphorus

Chlorophyll

Temperature

Alkalinity

Suspended matter

Component 1

Fig. 6 Left: PCA components projection on the Axis 1 and

Axis 2. Chlorophyll, Temperature and Total Phosphorus are

most closely related to PCA Axis 1 and salinity and nitrates to

Axis 2. Right: PCA stations projection in the Axis 1 and Axis 2

(Z—Merja Zerga, G—Ghar El Melh, M—Lake Manzala)

124 Hydrobiologia (2009) 622:113–131

123

relationship between phytoplankton cell size and

copepod feeding. Copepods feed inefficiently on

particles \10 lm (Bautista & Harris, 1992) and

show a preference for particles larger than 5–10 lm

(Harris, 1982). Examination of copepod–phytoplank-

ton grazing interactions at Merja Zerga (MZ1) during

spring–summer 2003 indicates that individuals at

different stages of dominance in the different samples

(Calanus helgolandicus, Pseudocalanus elongatus,

Oithona sp, Acartia clausi, Ternora longicornis,

Paracalanus parvus and Centropages typicus) were

characterized by body pigment colouration. Phyto-

plankton bloom periods appeared to enhance copepod

grazing, as indicated by increased pigments in gut

contents. The abundances of most of zooplankton

species tended to increase to maximum values during

April after the spring phytoplankton bloom (Fig. 5).

Calanus helgolandicus increased again at the end of

June. Generally, when numbers of diatoms were high,

copepods were more diverse and comprised larger

species.

According to Dowidar & El-Maghraby (1970),

Guerguess (1993), Ramdani et al. (2001b), Abdel-

Aziz & Aboul-Ezz (2004) and Zakaria et al. (2007)

freshwater rotifers in Lake Manzala have increased

markedly in recent years, possibly as a result of

eutrophication and high abundance of aquatic bacte-

ria. Indeed, Mostafa et al. (2003) noted that the

biological activity of sulphate-reducing bacteria was

very high in water and sediment of Lake Manzala.

Total bacterial count (TBC—total coliforms, fecal

coliforms) in lake water can reach 1–3 105 CFU ml-1

-1

Axi

s 2

+1

Axis 1+1 0

242

239

236

235

233

231

230

229

227

225

220

219

218

217

216

215

212

210

209

208

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205

203

202

196

195

193

191

190

189

188

187

186

185

184

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181

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179

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173

172 171

170

169

168 167

166

165

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162

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150

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136

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129

128

127

126125

124

123

122

121

120

118

117 116 115

114

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111

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108

107

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102 101

100

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67

66

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61

60

59

58

57

56

5554

53

52 51

50

49

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47

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42

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40

39

38

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35

34

33

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20

19

18

17

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15

14

13

10

9

8

7

6

5

4

3

2

1

Fig. 7 (DCA) phytoplankton species projection on Axis 1 and

Axis 2. Numbers refer to phytoplankton species named from 1

to 250 as in Supplementary Material Tables 2–5. Axis 1 is

most related to salinity, Axis 2 to nutrients and transparency.

Dinoflagellates species—upper left, Chlorophyceae species—

most upper right and Diatoms species—downside of the figure

Hydrobiologia (2009) 622:113–131 125

123

in summer (Mostafa et al., 2003 and Sabae, 2006). In

the other two lagoons, Merja Zerga and Ghar El

Melh, the zooplankton are mainly marine species,

and compared to other Meditterean lagoons there was

a slight tendency towards species poor-communities.

Salinity and nutrients probably have the greatest

effect on intra-annual changes in each lagoon.

Combined ordinations (DCA) of the zooplankton

data (samples and species) for the three MELMARI-

NA primary lagoons (Fig. 8) indicated the species

difference between the lagoons. The Lake Manzala

stations were dominated by rotifers and cladocerans

and constituted a heterogeneous group. Merja Zerga

and Ghar El Melh stations were dominated by marine

copepods (Acartia clausi, Calanus helgolandicus,

Pseudocalanus elongatus, Oithona nana, Ternora

longicornis, Paracalanus parvus and Centropages

typicus) and constituted the second group within

Fig. 8. Stations Z2 and Z3, which were under more

freshwater influence, constituted the intermediate

group characterized by brackish and freshwater

species Acanthocyclops robustus and Acanthocyclops

speratus.

Controls on plankton

Space–time development of the phytoplankton com-

munities in the three lagoons indicated that seasonal

changes in salinity and nutrient concentrations were

the main determining factors, but grazing effects

were less clear. No relationship was found between

salinity and phytoplankton abundance in the three

lagoons although the overall availability of freshwa-

ter imparts a major control on species occurrences.

So, Lake Manzala, with the largest freshwater inputs,

has by far the highest proportion of freshwater taxa.

All the water quality variables were under strong

hydrological influences and these include the effects

of freshwater inflows and the exchange of lagoon

water with the sea (Thompson et al. 2009). Phyto-

plankton seasonality was largely a function of

nutrient supply and probably grazing in Merja Zerga

with the former being linked with the Nador Canal

and Qued Drader inflows. This freshwater linkage

was less evident in Ghar El Melh. However, fresh-

water inflows to these two sites were very episodic

with distinct peaks associated with individual rainfall

events (Thompson et al., 2009). Because of the

monthly sampling frequency, it is possible that peak

conditions were missed for both plankton abundance

and water quality extremes. More regular sampling

and the provision of in situ multi-parameter moni-

toring instrumentation would enable better temporal

resolution of plankton changes in future studies. As

noted above, abundant year-round freshwater inflows

to Lake Manzala were provided by drains so that

these issues were less problematic.

Significant negative relationships were found

between phytoplankton and nutrients. In Ghar El

Melh, the value of the correlation coefficient (r) for

the relationship between phytoplankton abundance

(4–16 9 106 cells m-3) and nutrient concentration

(nitrates ? nitrites) was -0.47 (P \ 0.01). For the

relationship with total phosphorus, r was -0.58,

(P \ 0.01). In Merja Zerga, relationships between

phytoplankton abundances (4–12 9 106 cells m-3)

and nutrients (nitrates) and total phosphorus were

Factor 1 420-2-4

4

2

0

-2

100

99

9897 9

695

94

93

92

91

90

89

88

87

8685

84

83

82

81 80

79

78

77

76

7574

73

72 71

69

6867

6665

64

6362

6160

59

58

57

56

55

54

5352

51

50

49

484746

45

4443

42

41

40

39

3837

36

35

34

33

32

31

30

29

28

27

2625

24

2322

21

20

19

1817

1615

14

13

1211

10

9

8

7

6

5

4

3

2 1

Fac

tor

2

G1

1.0Axis 1

.50.0-.5

Axi

s 2

1.0

.5

0.0

-.5

-1.0

M10

M8M7

M6

M5

M4M3

M1

M2

Z3

Z1

Z4

G5

G4G3

G2

Z2

M9

Fig. 8 Top: DCA zooplankton projection on the Axis 1 and

Axis 2. Numbers refer to zooplankton species named in order

from 1 to 96 as in Tables 6 and 8. Bottom—DCA stations

projection on the Axis 1 and Axis 2

126 Hydrobiologia (2009) 622:113–131

123

-0.53 (P \ 0.01) and -0.42, (P \ 0.01), respec-

tively. The corresponding values for Lake Manzala,

where phytoplankton abundances were between 40

and 110 9 107 cells m-3, were -0.67, (P \ 0.01)

and -0.58 (P \ 0.01). These relationships suggest

that phytoplankton development accounts for the

decline in dissolved nutrient concentrations in each

lagoon. Nutrient fluxes in the drainage water were not

measured, but it seems very likely that little nutrient

transport into Merja Zerga and Ghar El Melh

occurred during the dry season. This was in sharp

contrast to the situation in Lake Manzala where

perennial irrigation means that the nutrient-rich

freshwater was available throughout the year and

the phytoplankton was clearly the most eutrophic in

nature. At the other two sites, phytoplankton abun-

dance was generally low with relatively small

seasonal changes. The daily flushing of Merja Zerga

diminishes any significant crop development. Ghar El

Melh normally receives very little freshwater inflow,

so nutrients were not regularly distributed within the

lagoon and, even though the tidal range was small,

additional nutrient input from the Bay of Tunis

(Rasmussen et al., 2009b) (as well as from sediments

and domestic drainage water) is suspected.

Recent changes in plankton communities

Evidence from previous studies indicates that the

plankton, especially the phytoplankton, has changed

significantly in many North African lagoons during

the twentieth Century. During this time, both hydro-

logical modifications and excess nutrients arising

from agricultural development increased markedly in

the region (e.g. Flower, 2001, Ayache et al., 2009).

Sediment records (Flower, 2001; Ramdani et al.,

2001a) indicate a trend towards more freshwater

plankton species within Lake Manzala from the 1960s

onwards. Documentary records show that the density

of zooplankton in Lake Manzala also increased over

the last few decades. In 1987, the zooplankton density

was 100–200 9 103 ind m-3 (El-Sherif & Gharib,

2001). Results from this study indicate densities in the

range 50–300 9 104 ind m-3. This particular ecosys-

tem is highly productive when compared with other

Mediterranean lagoons (Aboul-Ezz, 1995; Daly

Yahya et al., 2001; Mageed, 2006). Khalil (1990)

showed that the phytoplankton communities in Lake

Manzala were dominated by diatoms (68%), followed

by Chlorophyceae (22%) and Cyanophyceae (3%).

Dinoflagellates and Euglinophyceae were rarely and

sporadically present. Previous work indicated that the

diatoms were mainly represented by the genera

Synedra, Nitzschia, Melosira [Aulacoseira] and Cos-

cinodiscus, the Chlorophyceae by Tetraspora,

Scenedesmus and Pediastrum and the Cyanophyceae

by the filamentous Spirulina and Anabaena. El-Sherif

& Gharib (2001) suggested that there has been a

continuous increase in the standing crop of phyto-

plankton in this lake. They identified 129 species that

were either fresh or brackish, whereas 12 species were

purely marine, supporting the suggestion of a move

towards lower salinity conditions. Elsewhere in

Egypt, Zaghloul & Hussein (2000) studied the impact

of the large inputs of pollutants on the phytoplankton

communities in Lake Edku. They suggested that

nutrient pollution created a rich resource spectrum for

algal growth making the lake biologically productive.

In Merja Zerga, a trend to more freshwater conditions

in the south of the lagoons has also been noted

(Ayache et al., 2009). Sediment cores from this

location (Ramdani et al., 2001a; Flower et al., 2001)

showed a decline in marine species and a change from

attached diatoms to those indicative of soft sediments.

Implications

Pollution and salinity changes have already brought

about major shifts in the occurrence of both planktonic

and benthic species in coastal lagoons of the SMR (e.g.

Birks et al., 2001; Reynolds et al., 2002) and without

water quality regulation these changes will become

increasingly detrimental to aquatic resources, espe-

cially to fisheries and biodiversity. The drainage

systems to all the three lagoons have been strongly

modified through construction of barrages, abstraction

and drainage. It is likely that availability of silica, an

essential nutrient for diatom phytoplankton, has

declined at all the three sites (cf. Humborg et al.,

1997). One consequence of this silica depletion

hypothesis is that non-diatom phytoplankton are

favoured, and these algae (especially the dinoflagel-

lates) are often less favourable to lagoon ecosystems.

Toxic phytoplankton species identified in this study

included Gymnodinium catenatum, Alexandrium spp.,

Dinophysis spp. Lingulodinium polyedra, Pseudo-

nitzschia ssp. Gymnodinium aureolum, G. sanguineum,

Prorocentrum micans, P. depressum, Ceratium furca,

Hydrobiologia (2009) 622:113–131 127

123

Gyrodinium spirale, G. impudicum and Scrippsiella

spp. It is thought possible that the presence of these

species is encouraged in the SMR lagoons by changing

nutrient ratios as well as by increasing enrichment and

salinity.

Excess nutrients and discharge of waste or agri-

cultural return water together with land reclamation

are probably the most serious current and common

problems confronting sustainability of the SMR

lagoons. Such changes have caused eutrophication

and loss of ecological capacity in all the three

monitored lagoons. Climate change further threatens

to degrade these lagoon ecosystems as the twenty-first

Century progresses. Lagoon ecosystem surveillance

through regular monitoring is needed not only to better

understand the relationships between phytoplankton

and environmental change, but also for detecting

invasive species. Predictive models to aid water body

management will benefit from the enhanced field data,

especially regarding the plankton. Also, deployment of

automated water quality loggers is a key requirement in

future studies. Similarly, enhanced spatial studies using

remote sensing applications will facilitate monitoring

of phytoplankton distributions (cf. Simis et al., 2005,

Ahmed et al., 2009). Nevertheless, species level

information can only be provided by microscopical

examination, and this remains an essential tool for

monitoring planktonic communities.

Conclusions

Although Merja Zerga, Ghar El Melh and Lake

Manzala displayed major differences in their hydro-

logical regimes which influence salinity and suspended

sediment dynamics, they all were affected to some

extent by excess nutrients. The relatively high inflows

of both freshwater and nutrients into Lake Manzala

produced a rich phytoplankton community dominated

by green algae. At the more saline lagoons, Merja

Zerga and Ghar El Melh, diatoms often predominated

in the phytoplankton during the summer period.

Harmful species in the two latter lagoons were

identified, and these species raise phytosanitation

issues. Future management options would need to

curb the development of harmful blooms by, in the first

instance, reducing nutrient enrichment locally and in

the coastal zone more generally. Zooplankton showed

a high marine influence at Merja Zerga and Ghar El

Melh, but the densities of zooplanktoners tended to be

low in comparison with Lake Manzala and other

Mediterranean lagoons. A major influence by fresh-

water occurs at Lake Manzala with a high diversity of

rotifers, cladocerana and green algae. The historical

records for Lake Manzala indicate that zooplankton

density has increased strongly since the 1970s,

confirming the trend towards eutrophication. The

status of planktonic communities is of crucial impor-

tance for maintaining ecosystem quality. Not only are

the plankton communities a keystone component of

aquatic food webs that support fisheries but they also

function for the dispersal of many delicate larval forms

that are essential for the survival of communities

elsewhere. Careful surveillance of these communities

in relation to water quality and freshwater availability

is required to form environmental management deci-

sions that must be taken in the near future, if these

coastal resources are to be sustained.

Acknowledgements The MELMARINA Project was financed

by the EU Framework V INCO-Med Programme under their

Grant No. ICA3-CT2002-10009. The authors acknowledge the

assistance of all the partner institutions involved in this project.

The generous help provided by the enthusiastic field teams from

each of the countries in North Africa, where the studies were

conducted is also duly acknowledged. Several individuals, in

particular, Dr A. Berraho and Dr. M. Serghini (INRH), Dr S.

Duvail and Ms C. Chambers (UCL), Dr S. Zaghloul (NARSS),

Mr M. Mansour (Merja Zerga), R. M’Rabet (INSTM) also

deserve the authors’ gratitude for their special contributions to

the success of this study.

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