Abrupt changes in Potamogeton and Ruppia beds in a

Aquatic Botany 87 (2007) 181–188
www.elsevier.com/locate/aquabot
Abrupt changes in Potamogeton and Ruppia beds
in a Mediterranean lagoon
Abdessalem Shili a,b,*, Naceur Ben Maı̈z c, Charles François Boudouresque a,
El Bahri Trabelsi c
a
UMR CNRS 6540 ‘‘Diversité, évolution et écologie fonctionnelle marine’’, Centre d’Océanologie de Marseille,
Campus de Luminy, 13288 Marseille Cedex 9, France
b
Institut National Agronomique de Tunisie, 43 Avenue Charles Nicolle, 1082 Tunis Mahrajène, Tunisia
c
Société de Promotion du Lac de Tunis, BP 36, Tunis El Bouhaira, 1080 Tunis Cedex, Tunisia
Received 12 August 2005; received in revised form 20 March 2007; accepted 27 March 2007
Available online 25 April 2007
Abstract
Until the early 1990s, the Ichkeul lagoon (80 km2, Tunisia) was characterised by the seasonal alternation of low and high salinity and by the
presence (mainly in summer and autumn) of more or less extensive Potamogeton pectinatus beds (western and south-eastern zones). The yield was
largely consumed by wintering waterfowl populations (almost exclusively phytophagous), making this lagoon one of the most important wintering
places in northern Africa, and recognized as a high ecological value World Heritage site. Ruppia cirrhosa (together with Chaetomorpha linum
floating mats) was confined to a small north-eastern or eastern zone of the lagoon. This is the distribution which the authors observed in 1993, in the
course of a study running through 1998, with P. pectinatus covering 37 km2 (28,236 t DW) and 30 km2 (20,139 t DW) in summer and autumn,
respectively. In 1994, P. pectinatus had disappeared, an event which had already occurred in the past; however, this situation was still apparent in
1998; such a 5 year absence had never been reported since at least the early 1960s. From 1996 onwards, R. cirrhosa and C. linum ‘‘moved’’ to the
sites formerly occupied by P. pectinatus. Direct causes (shortage of freshwater input, salinity increase) and indirect ones (construction of dams in
the water catchment area of the lagoon, a relative drought) can account for these abrupt changes. The persistence of this situation could threaten the
Ichkeul lagoon, as a major site for the wintering of phytophagous waterfowl.
# 2007 Elsevier B.V. All rights reserved.
Keywords: Brackish lagoon; Potamogeton pectinatus; Ruppia cirrhosa; Cartography; Biomass; Tunisia
1. Introduction
The Ichkeul lagoon (80 km2) is located in northern Tunisia
(378100 N, 98330 E). It receives freshwater from a 8000 km2
catchment area via seven wadis and is linked by a small channel
(Tinja) to the lagoon of Bizerte which in turn opens into the
Mediterranean Sea (Fig. 1). Because of the high value of the
Ichkeul lagoon as a wintering place for large waterfowl
populations (180,000–230,000 birds), several national (National
Park) and international (Ramsar Convention List, MAB
Biosphere Reserve, UNESCO World Heritage List) designations
* Corresponding author at: Institut National Agronomique de Tunisie, 43
Avenue Charles Nicolle, 1082 Tunis Mahrajène, Tunisia. Tel.: +216 71 289 431;
fax: +216 71 799 391.
E-mail address: [email protected] (A. Shili).
0304-3770/$ – see front matter # 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.aquabot.2007.03.010
have been applied for protection purposes since the early 1980s
(Hollis, 1978; Tamisier and Boudouresque, 1994). The most
abundant waterfowl species are phytophagous: greylag goose
Anser anser (L.), European wigeon Anas penelope L., common
pochard Aythya farina (L.) and European coot Fulica atra L.
(Tamisier and Boudouresque, 1994; Tamisier, 1999; Tamisier
et al., 2000).
Through the early 1990s, autumn and winter rainfalls filled
up the wadis and the lagoon with freshwater that overflowed
into the lagoon of Bizerte through the Tinja channel (Fig. 1). In
summer, high evaporation favoured by hot easterly winds
lowered the water level and allowed seawater to enter Ichkeul
lagoon. The mean freshwater load was 340 Mm3/a (Zaouali,
1974; Lemoalle, 1983a,b; Hollis et al., 1986; Ennabli and
Kallel, 1990; Tamisier and Boudouresque, 1994; BCEOM
et al., 1995). A primary characteristic of the Ichkeul lagoon thus
was an annual alternation of high water levels (up to 2–3 m
182
A. Shili et al. / Aquatic Botany 87 (2007) 181–188
Fig. 1. Localisation of the study area.
depth) and low salinity (3 psu) in winter and low water level
(1 m mean depth) and high salinity (30–50 psu) in summer
(Zaouali, 1975a; Savoure, 1977; Hollis, 1978; Hollis et al.,
1986; Ben Rejeb and Kartas, 1988; Ben Rejeb-Jenhani, 1989;
Tamisier et al., 2000; Ben M’Barek, 2001). An additional
feature was a west-east gradient from lower to higher mean
salinity (Ben Rejeb-Jenhani, 1989).
In order to supply freshwater for northern Tunisian
agriculture and the human population, three dams were built
on the wadis Joumine (1984), Ghezala (1988) and Sejnane
(1994, Fig. 1), which represent 46% of the water catchment area
of the lagoon. This resulted in a dramatic reduction of
freshwater input into the Ichkeul lagoon and the increase in the
seawater volume entering the lagoon via the Tinja channel. In
order to control the influx of seawater, a lock was subsequently
built on the Tinja channel in 1996.
Until the early 1990s, the Ichkeul lagoon was mainly
occupied by extensive meadows of Potamogeton pectinatus L.,
whose surface area conspicuously changed over the seasons
(maximum in summer and autumn, minimum in late winter)
and years. The yield of P. pectinatus was consumed largely by
wintering birds. Ruppia cirrhosa (Petagna) Grande was also
present (Hollis et al., 1986; BCEOM et al., 1995; Tamisier,
1999; Tamisier et al., 2000). Here, we describe the subsequent
changes in the extension of Potamogeton, Ruppia and other
macrophyte beds (1993–1998), and then we analyse the reasons
for these changes and their possible consequences.
2. Material and methods
Macrophyte beds were mapped in summer and autumn when
their extension is at its maximum during 1993, 1994, 1996 and
1998. Maps were based on visual observation from a small boat
along transects perpendicular to the shore, and on snorkelling
between transects and following the bed limits, using a Global
Positioning System (GPS) for positioning the observations.
Aerial photography and satellite imagery were not used, due to
the difficulty of discriminating species and water turbidity
which screens deeper parts of the meadows, especially when
the water level is high. Some ancient maps used for the purpose
of comparison (Table 1), based upon satellite (LANDSAT)
imagery, underestimate the meadow surface area (Hollis et al.,
1986). No accurate cartography was performed in 1995 and
1997 because cursory exploration of the lagoon did not reveal
conspicuous changes compared to the previous year.
Only dominant macrophytes were taken into consideration
for cartographical purposes: P. pectinatus, R. cirrhosa, Zostera
noltii Hornemann, Chaetomorpha linum (O.F. Müller) Kützing
and Lamprothamnion papillosum J. Groves.
Cover (percent of sediment surface covered by macrophytes,
to the nearest 10%) and biomass were measured at sites
randomly distributed within bed limits (at least 2 sites/km2, 3
replicates per site). Above-ground biomass was collected
within 0.5 m 0.5 m frames. Below-ground biomass was
collected by means of a 0.16 m-diameter core down to 30 cm
Table 1
Change in Potamogeton pectinatus and Ruppia cirrhosa extension in the Ichkeul lagoon, as a percentage of the surface area (80 km2) of the lagoon
Years
Surface area (%)
Potamogeton pectinatus
Summer
SE
Total
2.0
2.0
4.6
2.4
2.3
2.5
1.8
3.8
3.0
6.4
13.6
17.4
20.5
16.1
21.6
4.1
3.3
12.4
15.6
1983
1985
1987
1989
1992
1993
1994
1995
1996
1997
1998
29.3
9.0
0.0
+
38.1
0.0
0.0
0.0
0.0
0.0
0.0
+
8.6
0.0
0.0
0.0
0.0
0.0
38.3
23.8
56.3
0.0
41.3
46.8
0.0
0.0
0.0
0.0
0.0
W
Summer
SE
Total
21.8
16.6
41.3
2.5
26.8
19.3
+
+
+
+
+
+
W
Hollis et al. (1986)
Hollis et al. (1986)
Hollis et al. (1986)
Hollis et al. (1986)
Hollis et al. (1986)
Hollis et al. (1986)
Hollis et al. (1986)
Hollis et al. (1986)
Hollis et al. (1986)
Lemoalle (1983b),
Hollis et al. (1986)
Hollis et al. (1986)
Kartas and Zaouali (1990)
Kartas and Zaouali (1990)
F. Aubry (unpublished data)
Niéri et al. (1992)
Present study
Present study
Present study
Present study
Present study
Present study
Aerial photography
Landsat imagery
Landsat imagery
Landsat imagery
Landsat imagery
Landsat imagery
Landsat imagery
Landsat imagery
Landsat imagery
Landsat imagery and fieldwork
Autumn
SE
NE
Total
0.0
0.0
+
+
+
+
+
+
W
SE
+
29.0
0.0
0.0
0.0
0.0
0.0
8.0
0.0
0.0
0.0
0.0
0.0
37
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
+
+
+
0.0
0.0
0.0
0.0
0.0
0.0
0.0
2.5
2.0
2.8
+
0.0
0.0
0.0
2.5
2.0
2.8
+
+
+
+
0.0
+
0.0
0.0
+
+
+
0.0
0.0
0.0
0.0
0.0
0.0
+
NE
Total
+
+
2.5
+
2.6
+
0.0
0.0
+
2.5
6.6
2.6
+
+
+
32.5
Fieldwork
Fieldwork
Fieldwork
Fieldwork
Fieldwork
Fieldwork
Fieldwork
Fieldwork
Fieldwork
Fieldwork
Fieldwork
(accurate observations)
(cursory observation)
(cursory observation)
(cursory observation)
(accurate observations)
(accurate observations)
(accurate observations)
(cursory observation)
(accurate observations)
(cursory observation)
(accurate observations)
A. Shili et al. / Aquatic Botany 87 (2007) 181–188
W
11.6
15.4
15.9
13.8
19.4
1.6
1.5
8.6
12.6
Methods
Ruppia cirrhosa
Autumn
1963*
1973
1975
1976
1977
1978
1979*
1980*
1981
1982
References
W: West sector. SE: South-East sector (Joumine). NE: North-East sector (Tinja). Blank: no data. +: Potamogeton or Ruppia present, but not any evaluation of its surface area. *: Measured on the authors’ figure (late
spring).
183
184
A. Shili et al. / Aquatic Botany 87 (2007) 181–188
depth within the sediment. At the laboratory, species were
sorted into three categories, P. pectinatus, R. cirrhosa and other
macrophytes, dried at 80 8C to constant weight and weighed.
Salinity, rainfall, evaporation, air temperature and water
level data (minimum monthly mean, maximum monthly mean,
year mean, winter mean, spring mean, March mean) come from
published (Lemoalle, 1983b; Hollis et al., 1986; Ben RejebJenhani, 1989; BCEOM et al., 1995; Ben M’Barek, 2001) and
unpublished (B. Chaouachi, A. Ben Rejeb-Jenhani, ANPE and
the meteorological station of Tinja) data. Salinity was measured
every month with WTW-LF 1961 conductivity meter, at five
sectors of the lagoon (NE, SE, centre, NW, SW). The
meteorological station of Tinja, where rainfall, evaporation
and air temperature were measured, is located near the entrance
of the Tinja channel (NE of the lagoon). The water level (above
NGT datum; NGT = Nivellement Général de la Tunisie) was
also measured at Tinja (ANPE, unpublished data). This data set
(1980 through 1998), together with the percentage of the
surface area of the lagoon covered in summer by P. pectinatus,
was analysed by means of a forward stepwise regression
(Statistica version 6, statsoft1).
3. Results and discussion
In 1993, the surface area occupied by the P. pectinatus
meadow was extensive and localised in shallow areas of the
western, south-western and south-eastern parts of the lagoon
(Fig. 2). The deeper areas of the central lagoon were devoid of
macrophytes, in relation with sediment resuspension during
wind episodes and turbidity. This is the picture which had
prevailed since the early 1960s, despite inter-annual fluctuations (Table 1, Zaouali, 1980; Hollis et al., 1986; Kartas and
Zaouali, 1990; Niéri et al., 1992). In 1994, P. pectinatus
abruptly disappeared and this new situation lasted until 1998. In
1996 and 1998, only isolated shoots (a few meters square) were
present near the mouth of Wadi Morra. So, a complete decline
of P. pectinatus had never been observed since the 1960s, with
the exception of the year 1989 (Table 1). However, the time
sequence since the early 1960s is not complete, and other years
without P. pectinatus may actually have occurred.
In contrast with P. pectinatus in 1993, R. cirrhosa was
mainly located in a relatively small area in the north-eastern
part of the lagoon, close to the entrance of the Tinja channel
(Fig. 3). Previous data dealing with this species are scarce
(Zaouali, 1975a; Hollis et al., 1986; Niéri et al., 1992; Alain
Tamisier, unpublished data). However, they allow the inference
that this was the pattern of localisation since at least the 1970s.
A conspicuous change occurred from 1996 to 1998: R. cirrhosa
meadows established in the western part of the lagoon, with just
a scattered population or complete loss in other parts (Fig. 3).
The distribution of Z. noltii in 1993 and 1994 was similar to
that of R. cirrhosa (data not presented). As for the latter species,
this picture had probably lasted since the 1970s (Zaouali,
1975a; Niéri et al., 1992). Subsequently, Z. noltii more or less
disappeared. Small patches of another species, Cymodocea
nodosa (Ucria) Ascherson, have been mentioned near the very
entrance of the Tinja channel (Cuenod, 1954; Zaouali, 1974,
1975a; Niéri et al., 1992); we were unsuccessful in finding it
again.
Finally, floating mats of C. linum developed, in autumn
1994, in the R. cirrhosa meadow, close to the entrance of the
Tinja channel. In autumn 1998, these mats still accompanied R.
cirrhosa, but at its new location, at the western end of the
lagoon (data not presented), and became denser. In addition,
stands of L. papillosum developed in the south-western part of
the lagoon. Several macroalgae were observed during the study
period, though in small amounts: Cladophora spp., Ulva
intestinalis L., Rhizoclonium sp., Ceramium siliquosum
(Kützing) Maggs et Hommersand, Gracilaria cf gracilis
(Stackhouse) Stenfolt, Irvine et Farnham, Hypnea musciformis
(Wulfen) Lamouroux and Polysiphonia sp. (Rhodobionta),
most of them dwelling in shallow waters fringing the shoreline.
To sum up, between 1994 and 1996, the pattern of
macrophyte distribution which had prevailed for decades, i.e.
extensive P. pectinatus beds occupying the west, south-west
and south-east parts of the lagoon, and more localised meadows
of R. cirrhosa and Z. noltii with mats of C. linum in its northeastern part, close to the entrance of the Tinja channel, abruptly
changed. R. cirrhosa and C. linum ‘‘moved’’ to the sites
formerly occupied by P. pectinatus, while the latter species,
Fig. 2. Potamogeton pectinatus extension and density (coverage, in %) in summer (left) and autumn (right) of 1993 in the Ichkeul lagoon. 1994, 1996 and 1998 maps
are not shown, as P. pectinatus was almost absent (isolated shoots in 1996 and 1998; see text).
A. Shili et al. / Aquatic Botany 87 (2007) 181–188
185
Fig. 3. Change of Ruppia cirrhosa extension and density (coverage, in %) in summer from 1993 to 1998 in the Ichkeul lagoon.
together with Z. noltii declined abruptly to virtual disappearance. The question which arises is: what may have caused these
changes?
A stepwise regression of the whole data set (independent
variables: hydrological and meteorological parameters; dependent variables: P. pectinatus and R. cirrhosa cover) failed to
identify significant parameters affecting R. cirrhosa cover due
to missing data. From 10 independent variables (Table 2), only
three significantly affected P. pectinatus cover. Spring mean
salinity (standard partial regression coefficient b = 0.58),
annual rainfall (b = 0.54), and maximum monthly air temperature (b = 0.41) are shown as significant explanatory
parameters (N = 12; R2 = 0.79; d.f. = 3, 80; p = 0.004) for P.
pectinatus cover.
Both P. pectinatus and R. cirrhosa can dwell at low
salinity; however, a suite of life history traits make the
former more competitive than the latter at low salinity
(<10 psu) (De Casabianca et al., 1973; Verhoeven, 1979,
1980; van Wijk et al., 1988; van Wijk, 1989; Kantrud, 1990).
The growth of P. pectinatus at Ichkeul appears to have an
upper tolerance of salinity of 10 psu (Fig. 4), though it is
reported to survive at higher salinity (Conover, 1964; Hollis
et al., 1986). R. cirrhosa is reported to survive and even
produce seeds between 1.5 and 80 psu (Tallon, 1957;
Molinier and Tallon, 1970; Brock, 1979; Verhoeven, 1980;
Comı́n et al., 1991, 1995; Ben Maı̈z, 1999; Shili et al., 2002),
which gives it a competitive advantage at higher salinity. The
rainfall regime in the study area is characteristic of the
Mediterranean climate, with sharp differences from year to
year (Table 2); rainfall was relatively low between 1994 and
1998, but similar or even more severe drought episodes have
occurred in the past decades. Probably more relevant is the
decline of the freshwater input of the wadis into the lagoon,
which dropped from 340 Mm3 y1(up to the early 1990s;
Tamisier and Boudouresque, 1994) to 65 Mm3 y1 (1993–
1998; data from ANPE) average annual values. The effect of
186
A. Shili et al. / Aquatic Botany 87 (2007) 181–188
Table 2
Hydrological and meteorological data of the Ichkeul lagoon
Year
1980
1981
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
Water level (m)
Salinity (psu)
Mean monthly air temperature (8C)
Winter
Spring
March
Minimum
Maximum
Spring
Minimum
Maximum
Year mean
0.75
1.19
0.52
1.59
0.28
1.24
0.56
1.08
0.33
0.21
0.65
2.09
0.28
0.67
0.20
0.25
0.40
0.30
0.76
0.58
0.45
0.69
0.61
0.38
0.69
0.38
1.02
0.28
0.31
0.83
1.12
0.33
0.41
0.12
0.12
0.65
0.13
0.48
0.70
0.72
1.05
0.72
0.38
0.99
0.72
1.62
0.28
0.24
0.75
1.59
0.36
0.58
0.15
0.18
0.91
0.14
0.70
md
4.7
5.9
3.0
md
3.8
md
2.5
5.1
9.0
11.9
md
7.9
6.2
24.0
40.2
19.3
28.1
15.6
md
34.4
30.6
md
md
31.2
30.6
9.7
34.0
45.9
30.1
md
13.8
38.3
67.0
73.5
55.0
48.3
32.5
md
5.1
7.3
3.1
md
4.1
md
3.6
5.5
19.3
md
md
9.6
13.1
31.0
37.5
19.2
33.4
16.8
9.9
9.4
11.6
11.1
10.6
9.7
11.2
10.9
11.6
11.1
9.4
8.9
10.3
9.4
11.9
10.0
10.2
11.6
11.6
26.2
25.9
28.7
27.6
26.2
27.0
28.1
28.4
27.7
27.7
24.3
28.2
25.1
26.9
29.2
26.0
25.6
27.4
26.5
17.3
18.4
17.9
18.8
16.5
18.4
18.6
18.9
19.1
21.1
17.4
17.1
17.0
17.8
19.2
18.4
16.8
18.7
18.2
Rainfall (mm y1)
550
244
721
345
718
541
682
482
385
272
742
624
715
467
406
532
594
467
406
Winter: December (previous year), January and February. Spring: March, April and May. Minimum and maximum are minimum monthly mean and maximum
monthly mean, respectively. md: Missing data.
moderate drought probably combined with the impact of the
dams, the last of which was put into service in 1994, to a
dramatically increased salinity. In addition, the dams
sequestrate a large amount of sediment, reduce the sediment
load of waters entering the lagoon and therefore probably
have improved water transparency. R. cirrhosa is considered
to be favoured more by transparent water than P. pectinatus
(Menéndez and Comı́n, 1989), so that the reduction of the
turbidity may have improved the competitiveness of the
former (Richardson, 1980).
P. pectinatus is considered to be preferred by waterfowl
(Jonzén et al., 2002), and some species totally avoid R. cirrhosa
(Tamisier and Boudouresque, 1994). Furthermore, the primary
production of R. cirrhosa is far lower than that of P. pectinatus
(Verhoeven, 1980). The overall phytomass declined by more
than 50% in 1998 when compared with that of 1993 (Table 3),
explaining in part why the wintering bird population
dramatically decreased during the study period (Adel Allouch,
personal communication). Similar changes concerning fish and
invertebrate fauna (Ben Hassine and Raibaut, 1975; Zaouali,
1975a, 1975b; Chaouachi and Ben Hassine, 1998; Casagranda
and Boudouresque, 2004) are to be expected.
Though individual years characterised by a marked P.
pectinatus decline had already occurred in the past decades
(e.g. 1978 and 1989), sometimes coinciding with a relatively
dry year (1989), these have been followed by a rapid recovery
Fig. 4. Mean salinity of the Ichkeul lagoon from 1992 through 1998. Data from Ben M’Barek (2001), B. Chaouachi and ANPE (unpublished). Salinity limits for
Potamogeton pectinatus germination and survival according to Hollis et al. (1986).
A. Shili et al. / Aquatic Botany 87 (2007) 181–188
Table 3
Macrophyte biomass (metric ton dry weight) in the Ichkeul lagoon
Species
Potamogeton pectinatus
Ruppia cirrhosa
Zostera noltii
Other macrophytes
1993
1994
1998
Summer
Autumn
Summer
Autumn
Autumn
28,236
1000
md
+
20,139
1916
md
38
0
138
133
4
0
134
0
20
+
7604
25
2425
Zostera noltii and other macrophytes are mixed with Ruppia cirrhosa within the
R. cirrhosa meadow. Other macrophytes: mainly Chaetomorpha linum and
Lamprothamnion papillosum. +: < 1 t. md: Missing data.
of P. pectinatus. The total disappearance of the meadow lasting
for 5 consecutive years, and its replacement by an extensive R.
cirrhosa meadow, had never been observed previously
(Table 1). It cannot be ruled out that P. pectinatus disappeared
for several years between 1964 and 1972; however, we can only
argue that the recollections of elderly local farmers do not
support this hypothesis; their testimony may be dubious for P.
pectinatus (possible confusion with R. cirrhosa) but may be
more reliable as far as the abundance of P. pectinatus eating
birds are concerned.
Existing dams already control 46% of the water catchment
area of the Ichkeul lagoon. Several new dams are planned
(wadis Melah, Tine and Douimis), which represent a further
25% of the catchment area. It is to be feared that the situation
which prevailed until the early 1990s, i.e. generally extensive P.
pectinatus beds only declining during some years, will be
replaced by a new one, with P. pectinatus generally absent,
though possibly briefly recovering in wet years. The probability
of recovery is based on the persistence within the sediment of
seeds (up to 9000 m2), able to germinate (under laboratory
conditions; 1998 pers. observations). These seeds may have
survived unfavourable years within the sediment (seed bank) or
may originate in the reservoirs via the wadis.
Acknowledgements
The authors acknowledge with thanks the help of L. Baccar,
N. Ben M’Barek, C. Casagranda, B. Chaouachi, A. Defosse, L.
Frigola-Girones, S. Garin, V. Gravez, M. Niéri, F. Poydenot and
J. Zaouali who participated in field work, data collection or in
an early 1990s programme which constituted the starting point
of the present study, M.J. Elloumi (Agence Nationale de
Protection de l’Environnement, ANPE) for providing field
facilities and hydrological data, ANPE, BCEOM, Fresenius
Consult, CES Salzgitter and Studi for funding or coordinating
the 1993 field work, Sandrine Ruitton for statistical analysis,
Michael Paul for improving the English text and finally Jan
Vermaat (co-editor in chief) and two anonymous reviewers for
helpful comments and suggestions.
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