Internat. Rev. Hydrobiol.
90
2005
4
376–391
DOI: 10.1002/iroh.200410767
CATERINA CASAGRANDA*, 1, 2 and CHARLES FRANÇOIS BOUDOURESQUE1
1
UMR CNRS 6540 Dimar “Diversité, Evolution et Ecologie fonctionnelle marine”,
Centre d’Océanologie de Marseille, Université de la Méditerranée, Campus de Luminy,
case 901, 13288 Marseille Cedex 9, France; e-mail: [email protected]
2
Department of Biology, University of Freiburg, Germany
Abundance, Population Structure and Production of Scrobicularia
plana and Abra tenuis (Bivalvia: Scrobicularidae)
in a Mediterranean Brackish Lagoon, Lake Ichkeul, Tunisia
key words: Scrobicularia plana, Abra tenuis, population structure, secondary production,
Mediterranean lagoon
Abstract
Abundance, growth and production of the deposit-feeding bivalves were studied in the Ichkeul wetland, northern Tunisia, from July 1993 – April 1994. Scrobicularia plana (DA COSTA, 1778) occurred
at annual mean densities (biomasses) of 299 ± 65 to 400 ± 100 individuals/m2 (22.54 ± 3.00 to
34.27 ± 3.96 g ash-free dry mass (AFDM)/m2) depending on the study area. The annual mean density
of Abra tenuis (MONTAGU, 1803) amounted to 640 ± 74 individuals/m2 during the whole study period,
in contrast the biomass rose from 2.87 g AFDM/m2 in July to 10.29 g AFDM/m2 in April. Both species were largely dominated by age class I. Although not very successful, recruitment presented a twoperiod pattern: the main period at the beginning of spring, and a secondary one in late summer/autumn.
S. plana rarely exceeded 40 mm and lived for only 2 years, while most individuals of A. tenuis lived
for only 15–18 months growing to a length of 12 mm. The annual bivalve deposit-feeder production for
–
the whole lagoon system (90 km2) was 8.24 g AFDM/m2 (5.26 g C/m2, 0.65 g N/m2). The annual P/B
ratio was about 0.4 and therefore in the same order of magnitude as estimates from other brackish coastal waters.
1. Introduction
Scrobicularia plana (DA COSTA, 1778) and Abra tenuis (MONTAGU, 1803) are ecologically
closely related marine infaunal bivalves of the family Scrobicularidae. Their main ecological characteristics are tolerance of physical and chemical changes in the sediment and rapid
demographic adaptability to variations in the environment (HUGHES, 1970a; NOTT, 1980).
They both inhabit similar types of soft bottoms of clay or mud, with abundant organic detritus, where freshwater input produces conditions of varying salinity. Their range extends
from the Norwegian Sea to Senegal including the Mediterranean (TEBBLE, 1976). But they
differ with regard to habitat preference. A. tenuis is localized in its distribution, tending to
occur in lagoons or sites partly cut off from the sea, just below the surface of the sediment
or amongst macrophytes. S. plana is more widely distributed, inhabits the intertidal coastal
waters in great abundance and is often the dominant species of shallow water benthic communities (TEBBLE, 1976). In many of these coastal waters, benthic macrophytes form large
dense stands from late spring to early autumn. Often only a small proportion of this biomass
is directly consumed by herbivores, the remaining part enters the detritical pool and becomes
* Corresponding author
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 1434-2944/05/408– 376
Bivalvia in a Mediterranean Brackish Lagoon
377
available to deposit-feeders. Living micro-organisms are commonly much better absorbed
than detritus, suggesting that they constitute the main food source of deposit-feeding bivalves (MATTHEWS et al., 1989). Although they primarily suck up surface deposits, S. plana
and A. tenuis obtain some of their food by filtering suspended matter from the water column
(HUGHES, 1970a; HUGHES, 1973). The bivalves play an important role in the coupling between the benthic and pelagic systems by removing large amounts of particulate material
from the water column (ALPINE and CLOERN, 1992), partly sequestrating the nitrogen and
phosphorus (NALEPA et al., 1991) and releasing inorganic nutrients into the water column
from direct excretion and from production of pseudofeces (PRINS and SMAAL, 1994). The
sediment enrichment with biodeposits provides a nutrient source for other biotic components
such as macrophytes and epibenthic deposit-feeders.
An estimate of the annual bivalve deposit-feeder production is needed in order to obtain a
quantitative measure of their role in the benthic-pelagic coupling in the Ichkeul ecosystem.
Secondary production of Scrobicularia plana has been investigated by HUGHES (1970a, b),
WARWICK and PRICE (1975), BACHELET (1982), GUELORGET and MAZOYER-MAYÈRE (1983),
SOLA (1997) and GUERREIRO (1998). Abra alba (WOOD, 1802) has received a lot of attention
on account of its wide geographical distribution and its high density permitting production studies (HILY, 1976; MENESGUEN, 1980; WARWICK and GEORGE, 1980; BACHELET, 1981b; GLÉMAREC and MENESGUEN, 1980; CORNET, 1986; DAUVIN, 1986; FRANCESCH and LOPEZ-JAMAR,
1991; LASTRA et al., 1993). Little is known about the secondary production of Abra ovata (PHILIPPI, 1893) (GUELORGET and MAZOYER-MAYÈRE, 1982; KEVREKIDIS and KOUKOURAS, 1992)
and Abra nitida (MÜLLER, 1776) (BUCHANAN and WARWICK, 1974; FRANCESCH and LOPEZJAMAR, 1991). No production investigation of Abra tenuis was found in the literature.
The present study is part of a more extensive research programme on the functioning of
the Ichkeul (Tunisia) which has the objective of identifying the ecological and physical characteristics of the ecosystem in order to draw up a predictive forecasting model with a view
to devising a conservation management programme which takes into account the social and
economic development of the region. The Ichkeul lagoon is a rare example of an oligotrophic functioning coastal lagoon in the Mediterranean basin (TAMISIER and BOUDOURESQUE,
1994). What is the fate of the macrophyte biomass since a dystrophic crisis has never been
described at Ichkeul lagoon? We investigate the contribution of the deposit-feeding bivalves
to the functioning of the ecosystem. Our study describes the abundance and biomass of Scrobicularia plana and Abra tenuis, and estimates their life span, growth and production in this
temperate brackish lagoon which harbours a conspicuous population of wintering waterfowl
(TAMISIER et al., 1987; TAMISIER and BOUDOURESQUE, 1994; TAMISIER et al., 2000).
2. Materials and Methods
2.1. Study Site
The study was carried out at Lake Ichkeul, an inland brackish lagoon of 9000 ha surrounded by
3000 ha of temporary marshes on the northern coast of Tunisia (Fig. 1). It is linked by a narrow channel
(Tinja channel) to the Lagoon of Bizerte which in turn has an outlet to the Mediterranean sea. The wetland is shallow with a mean depth of 2–3 m in winter and 1 m in summer. It is filled up with freshwater
from autumn and winter rainfall (from 7 wadis, i.e. temporary rivers) that overflows into the Lagoon of
Bizerte. In summer, high evaporation lowers the water level and allows seawater to enter the lagoon. Salinity displays considerable seasonal changes from 3 psu in the innermost parts in spring to 38 psu at the
mouth of the Tinja channel in autumn. The western and the southern areas, supplied with freshwater
from the wadis, are covered by extensive beds of Potamogeton pectinatus L. The eastern area close to
the Tinja channel and supplied with seawater is covered by a meadow of Ruppia cirrhosa (PETAGNA)
GRANDE. The central area of the Ichkeul lagoon is completely vegetation-free. The faunal investigation
carried out by HOLLIS (1986) by means of two cores in the eastern and central lagoon areas dated in a
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
378
C. CASAGRANDA and C. F. BOUDOURESQUE
Figure 1. The Ichkeul lagoon, with location of the sampling sites. Location of 7 wadis (i.e. temporary
rivers), the connecting channel to the Lagoon of Bizerte (Tinja channel), the meadows of Potamogeton
pectinatus and Ruppia cirrhosa are indicated.
210
Pb analysis showed that before the widening of the channel which links the Bizerte lagoon to the sea
during the 1880’s, the bivalve community of Ichkeul was represented by two species, Cerastoderma
glaucum (POIRET, 1789) and A. tenuis. In the strata following the 1890’s, S. plana was then present and
has progressively replaced A. tenuis since then. A. tenuis nowadays inhabits the eastern area of the Ichkeul lagoon whereas S. plana occupies the eastern and the central area (HOLLIS, 1986).
During the study period from July 1993 to April 1994 mean aboveground macrophyte biomass was
maximum in September (BCEOM et al. 1995) followed by the macrophyte fall from October onward.
Only negligible autumn and winter rainfall was registered, the inflow of seawater into the lagoon continued from summer to winter and was reversed only in February and March 1994 (2 months instead of
8 in average years). While water temperature did not deviate from its usual mean values (27.2 ± 0.8 °C
in August and 10.6 ± 0.2 °C in January), salinity continued to increase from 26.0 ± 4.1 psu in August
to 36.2 ± 1.1 psu (BCEOM et al. 1995) in December with a slight decrease during January and February
due to some precipitation. In December the P. pectinatus meadow had completely disappeared at Sejnene and Joumine and did not regrow in spring. Thick layers of dead vegetation piled up in particular
along the southern shores. The R. cirrhosa meadow reached its minimum in February and regrew from
March onward. At the end of the study period in April 1994, unusually high average salinity of
28.3 ± 0.4 psu (BCEOM et al. 1995) and low water level were observed. The mean salinity rose to
43.2 ± 0.5 psu in June 1994 (BCEOM et al. 1995). C. glaucum and other endobenthic deposit-feeder
species such as Cyathura carinata (KRØYER, 1847), Corophium volutator (PALLAS, 1766) and Nereis
diversicolor MÜLLER, 1776 were also present in the lagoon but occurred in too low density to allow
demographic studies and were therefore not taken into consideration.
2.2. Sampling
The lagoon was divided into 4 study areas on the basis of the macrophytal cover (Fig. 1). The western
and the southern areas were called “Sejnene” and “Joumine” after the main wadi supplying the lagoon
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
Bivalvia in a Mediterranean Brackish Lagoon
379
with freshwater. The eastern area close to the Tinja channel was henceford called “Tinja” and the vegetation free area “Centre”. From July 1993 to April 1994, three replicate samples were taken monthly
(with the exception of August and September 1993) at a total of 21 sites, at Sejnene 6 (sites 1–5), in
the Centre 3 (sites 6–8), at Tinja 6 (sites 9–14) and at Joumine 6 ( sites 15–20) (Fig. 1) using a 15 cm
inner diameter cylindrical Plexiglas coring tube containing a 20 cm thick substrate layer. The sediment
cores were rinsed in a 300 µm gauze hand-net. All samples were preserved in 75% ethanol.
2.3. Size Frequency Distribution, Biomass and CHN Content
Only live bivalves were measured and counted. In the Ichkeul lagoon clear visible growth rings on
the S. plana and A. tenuis shells are produced between July and August when water temperature and
salinity are highest. These summer rings are often accompanied by weak extra rings produced during
winter. The group of specimens which had not yet passed its first summer has been classified as age
class 0; age class I is the group which had passed only one summer, etc. The ash-free dry mass (AFDM)
[g] was estimated as a general power function of shell length (SL) [mm].
Scrobicularia plana:
AFDM = e–11.2009 · SL2.64089 (R2 = 85.21%, n = 18)
Abra tenuis:
AFDM = e–10.7109 · SL2.8038 (R2 = 61.19%, n = 38)
The AFDM was measured as weight loss after 4 h of incineration at 600 °C (BACHELET, 1982) of
unconserved specimens dried at 60 °C for 48 h. The average CHN content was measured with a LECO
800 analyser as described by CASAGRANDA and BOUDOURESQUE (2002). The C- and N-content for
S. plana yielded 64.3% C and 8.0% N of the AFDM, for A. tenuis 29.4% C and 2.9% N respectively.
The significance of the temporal variation in abundance and biomass of each species in each area was
tested by a Kruskal-Wallis analysis followed by a Student-Newman-Keuls (SNK) test. A Mann-Whitney
test was performed to compare the temporal S. plana abundance and biomass between the areas studied.
2.4. Production
The different age classes were regarded as separate cohorts, and production was calculated separately for each of these cohorts. The cohorts were separated according to HARDING (1949), assuming that
the size-frequency distributions of the cohorts were normally distributed. Production was estimated by
two methods using (1) the loss summation method described by BOYSEN-JENSEN (1919) and (2) the
increment summation method which MASSÉ (1968) derived from the BOYSEN-JENSEN (1919) method.
Another method, the mass specific growth rate method (CRISP, 1984; BREY, 2001) was not considered
here since comparing methods was not the aim of the present work and results from direct methods are
usually equivalent (MEDERNACH and GREMARE, 1999).
(1) According to BOYSEN-JENSEN (1919), the production ∆P of a cohort can be calculated as the sum
of the standing stock gain (∆B) and the biomass produced but eliminated (E) due to mortality or emigration from time t to time t + ∆t:
∆P = ∆B + E
– where ∆N = N – N
– 1
with ∆B = Bt + ∆t – Bt and E = ∆N · w
t
t + ∆t and w = /2 (wt + wt + ∆t). N is the individual number and w the mean individual biomass. Total cohort production is expressed as the sum of
all produced biomass over all time intervals:
P1 = ∑ (Bt + ∆t – Bt) + (Nt –Nt + ∆t) · 1/2(wt + wt + ∆t).
(2) According to MASSÉ (1968), the production ∆P of a cohort can be calculated as biomass gain
from time t to time t + ∆t:
–
∆P = N · ∆w
– 1
with N = /2 (Nt + Nt + ∆t) and ∆w = wt + ∆t – wt. The total production of the cohort is calculated as the
sum of the production increments over all time intervals:
P2 = ∑ (1/2(Nt + Nt + ∆t)) · (wt + ∆t – wt).
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
380
C. CASAGRANDA and C. F. BOUDOURESQUE
The energy budget of the deposit-feeding bivalves was estimated from literature using the calorific
value of 18.74 kJ/g AFDM, the growth efficiency (P/A) of 21.07% and 12.78% consumption (C) used
for production according to HUGHES (1970b). The organic income from the macrophyte meadows of the
Ichkeul lagoon was calculated to be 5306 kJ/m2 (BOUDOURESQUE et al., 1994; BCEOM et al., 1995;
DEFOSSE and POYDENOT, 1995).
3. Results
3.1. Spatial and Temporal Fluctuations of Abundance and Biomass
S. plana and A. tenuis were never found at Sejnene and Joumine. S. plana occurred at
annual mean densities (biomasses) of 400 ± 100 individuals/m2 (34.27 ± 3.96 g AFDM/m2)
at Centre and 299 ± 65 individuals/m2 (22.54 ± 3.00 g AFDM/m2) at Tinja. At the Centre
(3 sites*3 replicates) S. plana was the most abundant in November and December with a
mean density (biomass) of 577 and 621 individuals/m2 (22.75 and 36.61 g AFDM/m2), respectively (Fig. 2). At Tinja (6 sites*3 replicates), the maximum was reached in July with a
mean density (biomass) of 515 individuals/m2 (27.22 g AFDM/m2) and the minimum in
October with a mean density (biomass) of 146 individuals/m2 (9.96 g AFDM/m2) when the
autumnal macrophyte fall started. Monthly estimates of density were highly variable during
the macrophyte fall in autumn and stabilized once the leaf fall finished, i.e. from January.
A. tenuis was only present at Tinja. Mean density (6 sites*3 replicates) was around 640 ± 74
individuals/m2 during the whole study period; in contrast the biomass rose from 2.87 g
AFDM/m2 in July to 10.29 g AFDM/m2 in April. The abundance and biomass of S. plana
were only significantly higher in July, that of A. tenuis only in October (Table 1). No significant difference in the temporal variation of S. plana was found between the Centre and
Tinja by the Mann-Whitney test.
3.2. Population Structure and Growth
Both species were largely dominated by age class I composed of 2 cohorts (I–1 and I–2)
(Figs. 3 and 4). Specimens which had passed the second summer merged into a single class.
This is due to the lowering of the growth rate as the animals become larger so that younger
and faster growing animals could catch them up. In October, an increase of large numbers
of one-year-old S. plana individuals was observed in the central lagoon (Fig. 3). For
S. plana, a first spat settlement (0–1 cohort) was observed in October at Tinja (Fig. 4), in
November through December in the Centre, which was eliminated during winter, and a
second settlement (0–2 cohort) in March only in the Centre. For A. tenuis, a first recruitTable 1. Kruskal-Wallis analysis of temporal variation in abundance [individuals/m2] and
biomass [g AFDM/m2] of each species in each area. H = Kruskal-Wallis test statistic,
p = probability, SNK test = Student-Newman-Keuls test.
Species
Area
Centre
Scrobicularia
plana
Tinja
Abra tenuis
Tinja
Data
H
p
Abundance 6.95 0.33
Biomass 11.24 0.08
Abundance 9.69 0.21
Biomass
9.16 0.24
Abundance 8.99 0.25
Biomass
9.03 0.25
SNK test between months
Jul > Oct = Nov = Dec = Jan = Feb = Mar = Apr
Jul > Oct = Nov = Dec = Jan = Feb = Mar = Apr
Jul > Oct = Nov = Dec = Jan = Feb = Mar = Apr
Jul > Oct = Nov = Dec = Jan = Feb = Mar = Apr
Jul < Oct > Nov = Dec = Jan = Feb = Mar = Apr
Jul < Oct = Nov = Dec = Jan = Feb = Mar = Apr
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
Bivalvia in a Mediterranean Brackish Lagoon
381
Figure 2. Over time changes in abundance [individuals/m2] and biomass [g AFDM/m2] of Scrobicularia plana and Abra tenuis at each study area. Bars = standard error. No samples were taken in August
and September nor in January for Centre due to stormy weather.
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
▲
Figure 3. Over time changes in size-frequency distribution and growth of age classes of Scrobicularia
plana at Centre. Bars = standard error. Cohorts detected by the HARDING (1949) method are indicated. No
samples were taken in August and September nor in January due to stormy weather.
382
C. CASAGRANDA and C. F. BOUDOURESQUE
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
Bivalvia in a Mediterranean Brackish Lagoon
383
Figure 4. Over time changes in sizefrequency distribution of Scrobicularia
plana and Abra tenuis at Tinja. Cohorts
detected by the HARDING (1949) method
are indicated. No samples were taken in
August and September.
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
384
Figure 5.
C. CASAGRANDA and C. F. BOUDOURESQUE
Growth of age classes of Scrobicularia plana and Abra tenuis at Tinja. Bars = standard error,
no samples were taken in August and September.
ment was recorded in October (0–1 cohort) and a second one in April (0–2 cohort) (Fig. 4).
Although not very successful, recruitment of both species presented two periods: the main
period at the beginning of spring, and a second one in late summer/autumn. The data set
indicated high losses during summer. The youngest age class (0) underwent high losses
during winter, resulting in a dominance of age class I in both species. S. plana rarely exceeded 40 mm and lived 2 years although maximum life span observed was 5 years with
growth to a length of 52 mm (Fig. 5). The maximum life span of A. tenuis was 2 years, and
the maximum length observed 15 mm respectively, but most individuals lived only 15–18
months growing to a length of 12 mm.
3.3. Production
Production estimates for S. plana varied according to the area. The S. plana production achieved by loss summation was 13.45 g AFDM/m2 in the Centre and 21.23 at Tinja (Table 2). The
A. tenuis production at Tinja amounted to 3.44 g AFDM/m2. The major production (81–94%)
of the deposit-feeding bivalves took place in age class I. Within this age class, about 60%
was achieved in S. plana by the second recruited cohort (I–2) (Table 2). In A. tenuis, 67%
was achieved by the first recruited cohort (I–1). Production mainly occurred before November, when growth ceased. During winter, production was almost zero. Production of the
–
remaining age classes was negligible. The P/B values decreased whereas age increased
(Table 2). A mean estimate of bivalve deposit-feeder production and biomass was determined for the whole lagoon. In order to obtain this overall figure, the production and biomass
estimates for each sampling area were weighted by their contribution (Centre, 55%; Tinja,
3%) to the total surface area of the wetland (Table 2). Mean production (biomass) from July
to April for the deposit-feeding bivalves achieved by loss summation amounted to 8.24 g
AFDM/m2 (19.90 g AFDM/m2). The mean C- and N-production from July to April yielded
–
5.26 g C/m2 and 0.65 g N/m2 in the lagoon. The resulting turnover (P/B ratio) was about 0.4
(Table 2). The estimate according to MASSÉ’s (1968) method, 7.40 g AFDM/m2, was about
10% lower. The total bivalve deposit-feeding production (biomass) over the whole lagoon
surface was 741 t AFDM (1791 t AFDM).
The calorific value of the infaunal tissue production was calculated to be 154 kJ/m2. The
total bivalve deposit-feeder assimilation amounted to 733 kJ/m2 and the total consumption
(C) was to 1208 kJ/m2. On the basis of this value the deposit-feeding bivalves would have
consumed 23% of this energy income during the study period. The elimination (E) calcula-
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
385
Bivalvia in a Mediterranean Brackish Lagoon
Table 2. Mean biomass [g AFDM/m2], production during the study period [g AFDM/m2]
–
and P/B ratio of Scrobicularia plana and Abra tenuis at each study area and in the lagoon
as a whole. P1 = production as loss summation (BOYSEN-JENSEN, 1919), P2 = production as
increment summation (MASSÉ, 1968).
Age class
Biomass
P1
P2
–
P1/B
–
P2/B
S. plana
Centre
(49.6 km2)
III
II
I–1
I–2
0–1
total AFDM
total C
total N
3.25
13.66
10.28
7.03
0.05
34.27
22.06
2.74
0.43
2.09
3.14
7.70
0.09
13.45
8.66
1.08
0.43
2.09
3.14
6.46
0.05
12.17
7.84
0.98
0.13
0.15
0.31
1.10
1.83
0.39
0.39
0.39
0.13
0.15
0.31
0.92
1.04
0.36
0.36
0.36
S. plana
Tinja
(3 km2)
IV
III
II
I–1
I–2
0–1
total AFDM
total C
total N
2.78
1.94
1.98
8.79
7.03
0.01
22.54
14.51
1.81
0.35
0.60
0.76
6.09
13.43
0.01
21.23
13.67
1.70
0.35
0.60
0.76
6.09
9.60
0.01
17.41
11.21
1.39
0.13
0.31
0.38
0.69
1.91
0.51
0.94
0.94
0.94
0.13
0.31
0.38
0.69
1.37
0.35
0.77
0.77
0.77
A. tenuis
Tinja
(3 km2)
II
I–1
I–2
0–1
0–2
total AFDM
total C
total N
0.64
6.08
1.01
0.04
0.01
7.78
2.29
0.23
0.06
2.30
0.94
0.12
0.01
3.44
1.01
0.10
0.06
2.30
0.79
0.07
0.01
3.24
0.95
0.09
0.10
0.38
0.93
3.00
1.00
0.44
0.44
0.44
0.10
0.38
0.79
1.77
0.50
0.42
0.42
0.42
Lagoon
(90 km2)
mean AFDM
mean C
mean N
19.90
12.72
1.58
8.24
5.26
0.65
7.40
4.73
0.59
0.41
0.41
0.41
0.37
0.37
0.37
Area
ted by the BOYSEN-JENSEN (1919) method amounted to 104 kJ/m2, rendering the ecological
efficiency (E/C) of the deposit-feeding bivalves as 9%.
4. Discussion
4.1. Spatial and Temporal Fluctuations of Abundance and Biomass
Density and biomass of the deposit-feeding bivalves in the Ichkeul lagoon are high compared with results from other studies (GUELORGET and MAZOYER-MAYÈRE, 1982; GUERREIRO,
1998; HUGHES, 1970b; KEVREKIDIS and KOUKOURAS, 1992; SOLA, 1997). Among the local
factors that could influence high abundance in the Ichkeul lagoon, we can point to (1) the
stability of the sediment; (2) the high organic matter content of the sediment favouring the
development of bacterial populations that form the basis of the diet of deposit-feeders; (3)
the low number of competing bivalve species and predators on adult individuals (BCEOM
et al., 1995).
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
386
C. CASAGRANDA and C. F. BOUDOURESQUE
The reproductive strategies differ considerably for the two species. S. plana has a planktotrophic development with a long pelagic stage (HUGHES, 1970a). The unfavourable environmental conditions at Sejnene and Joumine such as low salinity, dense Potamogeton pectinatus stands, coarser sediment, high temperature and low dissolved oxygen especially at
the time of settlement in summer prevent S. plana from colonizing these areas. A. tenuis has
a lecithotrophic development (NOTT, 1980) which is interpreted as ensuring the maintenance of populations but population dispersal is very limited.
The strong biomass decrease observed in October can be interpreted as the result of lower
condition factor linked with spawning. Gamete release significantly affects biomass. HUGHES (1970b) estimated that gametic production could account for 24 to 52% of the total production which is in line with BACHELET (1982). However, in the Ichkeul lagoon the effect
of summer stress on biomass outweighed the effect of spawning on biomass. S. plana is unable to osmoregulate physiologically (HUGHES, 1970a) and highest mortality occurred essentially during summer when temperature, salinity and macrophyte development were highest
and dissolved oxygen lowest in the lagoon (BCEOM et al., 1995). High mortality following
spat settlement and spawning is not unusual. The S. plana population of the Prévost lagoon
(GUELORGET and MAZOYER-MAYÈRE, 1983) was almost eliminated during summer. HUGHES
(1970a) found in an S. plana population a mortality rate of 50% that he attributed to unfavourable environmental conditions which is consistent with the results of BACHELET (1982)
and SOLA (1997).
4.2. Life History and Recruitment
The high density and biomass of the Ichkeul deposit-feeding bivalves could also be related to the temperature regime in the southern part of the geographical range of both S. plana
and A. tenuis. This may result in faster growth, higher density of individuals of smaller size
and a shorter life span. Although S. plana is obviously capable of substantial horizontal
migration it appears to do so only rarely (HUGHES, 1970a; BACHELET, 1982; GUELORGET and
MAZOYER-MAYÈRE, 1983). In October, the arrival in the central lagoon of large numbers of
one-year-old S. plana individuals which had already passed a summer (Fig. 3) can only be
explained by migration as a response to unfavourable conditions. The highly adverse environmental conditions during late summer eliminate the possible interpretation of the rapid
growth of a new settlement.
The Ichkeul population of S. plana showed a reproduction pattern similar to that of the
Arcachon bay population (BACHELET, 1981a) and the Tagus and Mira estuary populations
(GUERREIRO, 1998) with two recruitment events, one in spring and one in autumn. The reproduction pattern of the Ichkeul A. tenuis population differs from that of northern regions
(NOTT, 1980; GIBBS, 1984; DEKKER and BEUKEMA, 1993) by the occurrence of 2 recruitments
in spring and autumn. According to HUGHES (1970a) the differences in the reproductive
cycle of S. plana may be due to latitudinal, i.e. thermal differences along the Atlantic coast.
Northern populations of S. plana are characterised by short, mid-summer spawning periods
(HUGHES, 1970a; WARWICK and PRICE, 1975). Further south, spawning periods are extended
and occur later, sometimes throughout the winter, but with negligible or no activity in midsummer (SOLA, 1997). One cohort per year occurs mostly in northern areas (HUGHES, 1970a;
WARWICK and PRICE, 1975), versus 2–3 cohorts per year in southern regions (BACHELET,
1981a; GUERREIRO, 1998). DAUVIN (1986) compared his results to other A. alba populations
and his conclusions seem to confirm this pattern.
These latitudinal differences in reproductive cycles are related to varying local conditions
at times of settlement and during the first six months after settlement which affect the success of recruitment (HUGHES, 1970a). At densities found in the Ichkeul lagoon, pediveliger
or spats could be consumed by adults while deposit-feeding. Thus the poor recruitment has
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
Bivalvia in a Mediterranean Brackish Lagoon
387
lead to a dominant age class at Ichkeul. In fact, if one very successful spawning event takes
place, recruitment in the following years may be suppressed due to intraspecific competition for food and space. HUGHES (1970a) and GUERREIRO (1998) postulated a dominant age
class phenomenon where a population may be numerically dominated by one or a few large
older classes. Successful recruitment does not seem to be a regular annual phenomenon
(DEKKER and BEUKEMA, 1993; GUERREIRO, 1998). In southern Europe, the pattern of population dynamics of at least S. plana may possibly be dominated by periods of highly successful recruitment and high production followed by large periods of unsuccessful recruitment and low production (GUERREIRO, 1998; this study).
4.3. Production
–
The S. plana P/B ratio in the Centre was much lower (0.39) than at Tinja (0.94, Table 2)
due to a faster growth in age class I from March on at Tinja (Fig. 5) than in the Centre (Fig. 3).
At Tinja, growth is favoured by much better food availability in spring than in the vegeta–
tion-free Centre. The P/B of A. tenuis at Tinja is in the same order as that of S. plana in the
Centre which is interpreted as a consequence of the poor recruitment during the study period. As has been pointed out by SIEGISMUND (1982), the method described by MASSÉ (1968)
underestimates the production of a cohort during a period of recruitment in which the density is increasing. The SIEGISMUND (1982) modification probably still underestimates production as it neglects the production of individuals recruited during the period of increasing
density and eliminated before observation at the end of the period. For these reasons and
also because of migration phenomenon within the system, the production estimates achieved by the loss summation method (BOYSEN-JENSEN, 1919) were favoured here. The production of S. plana from July 1993 to April 1994 amounted to 17.34 g AFDM/m2, and that of
A. tenuis to 3.44 g AFDM/m2 (Table 3). Although determined for only 10 months, this probably approximates the total annual production since the highly adverse environmental con–
ditions from October onward did not improve but worsened. The P/B ratio estimates of
S. plana in the Ichkeul lagoon were of the same order of magnitude as estimates in other
brackish coastal areas (HUGHES, 1970b; WARWICK and PRICE, 1975; BACHELET, 1982; GUERREIRO, 1998) (Table 3). In the Prévost lagoon, GUELORGET and MAZOYER-MAYÈRE (1983)
–
found exceptionally high P/B values which are due to particularly fast growth and short but
–
very abundant recruitment. The P/B ratio of A. tenuis in the Ichkeul lagoon is low compared to other Abra species which may be due to the weak recruitment during the study period and a very slow growth rate of the settling juveniles until a length of 1 mm was reached
(BACHELET, 1989). Along the Atlantic coast, a southward increase in secondary production
–
can be observed for populations of S. plana whereas P/B is constant (Table 3). This could
be related to faster growth in southern latitudes (BACHELET, 1981a), high densities of small
individuals, more than one annual generation and a shorter life span.
The high energy flow through the deposit-feeding bivalves indicates the importance of
this functional group in the Ichkeul ecosystem. HUGHES (1970b) estimated as much as 1336
and 1407 kJ/m2 for S. plana on a Welsh tidal flat, which seems to be very high. The assimilation in the Ichkeul lagoon was locally close to the above values but weighted to the
whole lagoon surface, the estimate of the average energy flow amounted to 733 kJ/m2 during
the study period. The consumption was 23% of the total energy input from the lagoon
macrophytes during the study period. Other energy sources may be available in the Ichkeul
lagoon, e.g. the excrements of the wintering waterfowl and the input through the Tinja channel. As the autumn and winter rainfall was very low during the study period, the nutrient
input from the wadis was negligible. Input of inorganic nutrients can also be attributed to
bivalve activity. Through their feeding and burrowing activities, Scrobicularids stimulate
mineralization processes in the adjacent sediment. In addition to mixing nutrient-rich pore
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
388
C. CASAGRANDA and C. F. BOUDOURESQUE
–
Table 3. Comparison of published data on mean biomass (B in g AFDM/m2), annual pro–
2
duction (P in g AFDM/m ) and P/B ratios. AFDM = ash-free dry mass, DM = dry mass.
a
= loss summation method, b = increment summation method, c = instantaneous growth
method, d = size-frequency method.
–
B
Study area
Abra tenuis
Ichkeul lagoon (Tunisia)
AFDM
Abra ovata
Prévost lagoon (France)
Mauguio lagoon (France)
Evros Delta (Greece)
DM
DM
DM
Abra alba
Charente straits (France)
Concarneau Bay (France)
Bristol channel (U.K.)
Gironde estuary (France)
Concarneau Bay (France)
Arcachon Bay (France)
Gironde estuary (France)
Morlaix Bay (France)
Ria de La Coruna
(Spain)
Santander Bay (Spain)
Abra nitida
Northumberland coast
(U.K.)
Ria de La Coruna
(Spain)
Scrobicularia plana
Conway Bay, marshward
(U.K.)
Conway Bay, seaward
(U.K.)
Lynher estuary (U.K.)
Gironde estuary (France)
Arcachon Bay (France)
Prévost lagoon, marshward (France)
Prévost lagoon, seaward
(France)
Bidasoa estuary (Spain)
Mira estuary (Portugal)
Tagus estuary (Portugal)
Ichkeul lagoon (Tunisia)
P
–
P/B
Authors
3.44
0.44
this study
0.70 1.50
14.33 26.10
29.22 17.09
2.14
1.82
0.59
GUELORGET and MAZOYER-MAYÈRE (1982)b
GUELORGET and MAZOYER-MAYÈRE (1982)b
KEVREKIDIS and KOUKOURAS (1992)c
7.78
a
DM
DM
AFDM
AFDM
DM
AFDM
AFDM
DM
1.04
0.35
0.30
0.80
0.72
0.81
4.44
0.77
0.81
1.34
0.41
2.91
1.45
2.34
7.31
1.58
0.77
3.83
1.35
3.63
2.01
2.87
1.65
2.04
HILY (1976)b
MENESGUEN (1980)b
WARWICK and GEORGE (1980)b
BACHELET (1981b)b
GLÉMAREC and MENESGUEN (1980)b
CORNET (1986)d
CORNET (1986)b,d
DAUVIN (1986)b
AFDM
AFDM
2.86
0.30
8.80
0.85
3.08
2.82
FRANCESCH and LOPEZ-JAMAR (1991)b
LASTRA et al. (1993)b
AFDM
0.11
0.12
0.11
BUCHANAN and WARWICK (1974)b
AFDM
0.35
0.93
2.63
FRANCESCH and LOPEZ-JAMAR (1991)b
AFDM
4.37
2.97
0.68
HUGHES (1970 b)a
ADFM 46.24 13.41
ADFM 2.15 0.48
ADFM 11.60 9.13
ADFM 9.65 12.28
0.29
0.22
0.79
1.27
HUGHES (1970 b)a
WARWICK and PRICE (1975)b
BACHELET (1982)a,b
BACHELET (1982)a,b
ADFM
3.97
GUELORGET and MAZOYER-MAYÈRE (1983)b
3.68
1.21
0.58
0.85
0.61
GUELORGET and MAZOYER-MAYÈRE (1983)b
SOLA (1997)b
GUERREIRO (1998)c
GUERREIRO (1998)c
this studya
7.98 31.69
ADFM 122.87
ADFM 69.20
ADFM 7.29
ADFM 28.93
ADFM 28.40
451.92
83.62
4.20
24.71
17.34
waters with overlying waters, the deposit-feeders remove organic material from the water
column and excrete remineralized nutrients in form of pseudofeces and through direct excretion (ALPINE and CLOERN, 1992). Bivalves can also sequestrate nitrogen and phosphorus. The
reduction of total phosphorus (TP) content in the Centre and at Tinja during winter (e.g.,
from 142 µg TP/l in August to 70 µg TP/l in October throughout the winter; BCEOM et al.,
1995) indicated a high potential for phosphorus storage in the bivalves. The nutrient cycling
© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
Bivalvia in a Mediterranean Brackish Lagoon
389
and the phosphorus storage by bivalves has been described for different aquatic ecosystems
(NALEPA et al., 1991; PRINS and SMAAL, 1994) suggesting the potential of bivalves for eutrophication control. It is difficult to quantify the amount of ingested material derived from the
sediment. More studies are necessary to determine food preferences and to quantify actual
ingestion rates. However, our study allowed quantification of the amounts of organic matter which passed through the deposit-feeding bivalves (short-term energy budget). Only 9%
of the bivalve deposit-feeding production was available to the next trophic level such as
common pochards, oystercatchers, eels and gilthead seabream.
5. Acknowledgements
This study was carried out within the international programme “Etude pour la sauvegarde du Parc
National de l’Ichkeul” financed by the Kreditanstalt für Wiederaufbau (KfW) under the aegis of the
Tunisian authorities, in particular the Agence Nationale pour la Protection de l’Environnement. Thanks
are due to members of the Groupement d’Intérêt Scientifique (GIS) Posidonie for field assistance, to
the colleagues at UMR 6540 CNRS Dimar (Diversité, Evolution et Ecologie fonctionnelle marine) for
advice and work facilities, and to Prof. GERHARD BAUER of the University of Freiburg for critical revision of the manuscript. The present research was supported by a Ph. D. grant from the Landesgraduiertenförderungsgesetzes (LGFG) Germany. The study would not have been possible without the support of Prof. JÜRGEN SCHWOERBEL, mentor and friend. Finally, the authors are grateful to two anonymous referees for very valuable comments and to MICHAEL PAUL for improving the English text.
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Manuscript received July 24th, 2004; revised February 19th, 2005; accepted March 9th, 2005
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