abundance, population structure and production of

© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 1434-2944/05/408– 376

CATERINA CASAGRANDA*, 1, 2 and CHARLES FRANÇOIS BOUDOURESQUE1

1UMR 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] of Biology, University of Freiburg, Germany

Abundance, Population Structure and Production of Scrobiculariaplana 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 wet-land, 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 to34.27 ± 3.96 g ash-free dry mass (AFDM)/m2) depending on the study area. The annual mean densityof 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 spe-cies were largely dominated by age class I. Although not very successful, recruitment presented a two-period 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 livedfor only 15–18 months growing to a length of 12 mm. The annual bivalve deposit-feeder production forthe 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 coas-tal waters.

1. Introduction

Scrobicularia plana (DA COSTA, 1778) and Abra tenuis (MONTAGU, 1803) are ecologicallyclosely related marine infaunal bivalves of the family Scrobicularidae. Their main ecologi-cal characteristics are tolerance of physical and chemical changes in the sediment and rapiddemographic 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 detri-tus, where freshwater input produces conditions of varying salinity. Their range extendsfrom the Norwegian Sea to Senegal including the Mediterranean (TEBBLE, 1976). But theydiffer with regard to habitat preference. A. tenuis is localized in its distribution, tending tooccur in lagoons or sites partly cut off from the sea, just below the surface of the sedimentor amongst macrophytes. S. plana is more widely distributed, inhabits the intertidal coastalwaters in great abundance and is often the dominant species of shallow water benthic com-munities (TEBBLE, 1976). In many of these coastal waters, benthic macrophytes form largedense stands from late spring to early autumn. Often only a small proportion of this biomassis directly consumed by herbivores, the remaining part enters the detritical pool and becomes

Internat. Rev. Hydrobiol. 90 2005 4 376–391

DOI: 10.1002/iroh.200410767

* Corresponding author

Bivalvia in a Mediterranean Brackish Lagoon 377

© 2005 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

available to deposit-feeders. Living micro-organisms are commonly much better absorbedthan detritus, suggesting that they constitute the main food source of deposit-feeding bival-ves (MATTHEWS et al., 1989). Although they primarily suck up surface deposits, S. planaand 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 be-tween the benthic and pelagic systems by removing large amounts of particulate materialfrom the water column (ALPINE and CLOERN, 1992), partly sequestrating the nitrogen andphosphorus (NALEPA et al., 1991) and releasing inorganic nutrients into the water columnfrom direct excretion and from production of pseudofeces (PRINS and SMAAL, 1994). Thesediment enrichment with biodeposits provides a nutrient source for other biotic componentssuch as macrophytes and epibenthic deposit-feeders.

An estimate of the annual bivalve deposit-feeder production is needed in order to obtain aquantitative 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 attentionon account of its wide geographical distribution and its high density permitting production stu-dies (HILY, 1976; MENESGUEN, 1980; WARWICK and GEORGE, 1980; BACHELET, 1981b; GLÉ-MAREC 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 (PHI-LIPPI, 1893) (GUELORGET and MAZOYER-MAYÈRE, 1982; KEVREKIDIS and KOUKOURAS, 1992)and Abra nitida (MÜLLER, 1776) (BUCHANAN and WARWICK, 1974; FRANCESCH and LOPEZ-JAMAR, 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 ofthe Ichkeul (Tunisia) which has the objective of identifying the ecological and physical char-acteristics of the ecosystem in order to draw up a predictive forecasting model with a viewto devising a conservation management programme which takes into account the social andeconomic development of the region. The Ichkeul lagoon is a rare example of an oligotro-phic 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 beendescribed at Ichkeul lagoon? We investigate the contribution of the deposit-feeding bivalvesto the functioning of the ecosystem. Our study describes the abundance and biomass of Scro-bicularia plana and Abra tenuis, and estimates their life span, growth and production in thistemperate 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 wet-land is shallow with a mean depth of 2–3 m in winter and 1 m in summer. It is filled up with freshwaterfrom autumn and winter rainfall (from 7 wadis, i.e. temporary rivers) that overflows into the Lagoon ofBizerte. In summer, high evaporation lowers the water level and allows seawater to enter the lagoon. Sali-nity displays considerable seasonal changes from 3 psu in the innermost parts in spring to 38 psu at themouth of the Tinja channel in autumn. The western and the southern areas, supplied with freshwaterfrom the wadis, are covered by extensive beds of Potamogeton pectinatus L. The eastern area close tothe 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 investigationcarried out by HOLLIS (1986) by means of two cores in the eastern and central lagoon areas dated in a

378 C. CASAGRANDA and C. F. BOUDOURESQUE


210Pb analysis showed that before the widening of the channel which links the Bizerte lagoon to the seaduring the 1880’s, the bivalve community of Ichkeul was represented by two species, Cerastodermaglaucum (POIRET, 1789) and A. tenuis. In the strata following the 1890’s, S. plana was then present andhas progressively replaced A. tenuis since then. A. tenuis nowadays inhabits the eastern area of the Ich-keul 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 wasmaximum 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 con-tinued from summer to winter and was reversed only in February and March 1994 (2 months instead of8 in average years). While water temperature did not deviate from its usual mean values (27.2 ± 0.8 °Cin August and 10.6 ± 0.2 °C in January), salinity continued to increase from 26.0 ± 4.1 psu in Augustto 36.2 ± 1.1 psu (BCEOM et al. 1995) in December with a slight decrease during January and Februarydue to some precipitation. In December the P. pectinatus meadow had completely disappeared at Sej-nene and Joumine and did not regrow in spring. Thick layers of dead vegetation piled up in particularalong the southern shores. The R. cirrhosa meadow reached its minimum in February and regrew fromMarch onward. At the end of the study period in April 1994, unusually high average salinity of28.3 ± 0.4 psu (BCEOM et al. 1995) and low water level were observed. The mean salinity rose to43.2 ± 0.5 psu in June 1994 (BCEOM et al. 1995). C. glaucum and other endobenthic deposit-feederspecies such as Cyathura carinata (KRØYER, 1847), Corophium volutator (PALLAS, 1766) and Nereisdiversicolor MÜLLER, 1776 were also present in the lagoon but occurred in too low density to allowdemographic 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 westernand the southern areas were called “Sejnene” and “Joumine” after the main wadi supplying the lagoon

Figure 1. The Ichkeul lagoon, with location of the sampling sites. Location of 7 wadis (i.e. temporaryrivers), the connecting channel to the Lagoon of Bizerte (Tinja channel), the meadows of Potamogeton

pectinatus and Ruppia cirrhosa are indicated.



with freshwater. The eastern area close to the Tinja channel was henceford called “Tinja” and the vege-tation 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), inthe Centre 3 (sites 6–8), at Tinja 6 (sites 9–14) and at Joumine 6 ( sites 15–20) (Fig. 1) using a 15 cminner diameter cylindrical Plexiglas coring tube containing a 20 cm thick substrate layer. The sedimentcores 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 onthe S. plana and A. tenuis shells are produced between July and August when water temperature andsalinity are highest. These summer rings are often accompanied by weak extra rings produced duringwinter. The group of specimens which had not yet passed its first summer has been classified as ageclass 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) ofunconserved specimens dried at 60 °C for 48 h. The average CHN content was measured with a LECO800 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 wastested by a Kruskal-Wallis analysis followed by a Student-Newman-Keuls (SNK) test. A Mann-Whitneytest 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 separate-ly for each of these cohorts. The cohorts were separated according to HARDING (1949), assuming thatthe size-frequency distributions of the cohorts were normally distributed. Production was estimated bytwo methods using (1) the loss summation method described by BOYSEN-JENSEN (1919) and (2) theincrement 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 consideredhere since comparing methods was not the aim of the present work and results from direct methods areusually equivalent (MEDERNACH and GREMARE, 1999).

(1) According to BOYSEN-JENSEN (1919), the production ∆P of a cohort can be calculated as the sumof the standing stock gain (∆B) and the biomass produced but eliminated (E) due to mortality or emi-gration from time t to time t + ∆t:

∆P = ∆B + E

with ∆B = Bt + ∆t – Bt and E = ∆N · w– where ∆N = Nt – Nt + ∆t and w– = 1/2 (wt + wt + ∆t). N is the indivi-dual number and w the mean individual biomass. Total cohort production is expressed as the sum ofall 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 gainfrom time t to time t + ∆t:

∆P = N–

· ∆w

with N–

= 1/2 (Nt + Nt + ∆t) and ∆w = wt + ∆t – wt. The total production of the cohort is calculated as thesum of the production increments over all time intervals:

P2 = ∑ (1/2(Nt + Nt + ∆t)) · (wt + ∆t – wt).



The energy budget of the deposit-feeding bivalves was estimated from literature using the calorificvalue of 18.74 kJ/g AFDM, the growth efficiency (P/A) of 21.07% and 12.78% consumption (C) usedfor production according to HUGHES (1970b). The organic income from the macrophyte meadows of theIchkeul 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 atannual 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 amean density (biomass) of 577 and 621 individuals/m2 (22.75 and 36.61 g AFDM/m2), res-pectively (Fig. 2). At Tinja (6 sites*3 replicates), the maximum was reached in July with amean density (biomass) of 515 individuals/m2 (27.22 g AFDM/m2) and the minimum inOctober with a mean density (biomass) of 146 individuals/m2 (9.96 g AFDM/m2) when theautumnal macrophyte fall started. Monthly estimates of density were highly variable duringthe 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 ± 74individuals/m2 during the whole study period; in contrast the biomass rose from 2.87 gAFDM/m2 in July to 10.29 g AFDM/m2 in April. The abundance and biomass of S. planawere only significantly higher in July, that of A. tenuis only in October (Table 1). No sig-nificant difference in the temporal variation of S. plana was found between the Centre andTinja 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 youngerand faster growing animals could catch them up. In October, an increase of large numbersof 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), inNovember through December in the Centre, which was eliminated during winter, and asecond settlement (0–2 cohort) in March only in the Centre. For A. tenuis, a first recruit-

Table 1. Kruskal-Wallis analysis of temporal variation in abundance [individuals/m2] andbiomass [g AFDM/m2] of each species in each area. H = Kruskal-Wallis test statistic,

p = probability, SNK test = Student-Newman-Keuls test.

Species Area Data H p SNK test between months

Centre Abundance 6.95 0.33 Jul > Oct = Nov = Dec = Jan = Feb = Mar = AprScrobicularia Biomass 11.24 0.08 Jul > Oct = Nov = Dec = Jan = Feb = Mar = Aprplana Tinja Abundance 9.69 0.21 Jul > Oct = Nov = Dec = Jan = Feb = Mar = Apr

Biomass 9.16 0.24 Jul > Oct = Nov = Dec = Jan = Feb = Mar = AprAbra tenuis Tinja Abundance 8.99 0.25 Jul < Oct > Nov = Dec = Jan = Feb = Mar = Apr

Biomass 9.03 0.25 Jul < Oct = Nov = Dec = Jan = Feb = Mar = Apr



Figure 2. Over time changes in abundance [individuals/m2] and biomass [g AFDM/m2] of Scrobicula-ria 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.

Figure 3. Over time changes in size-frequency distribution and growth of age classes of Scrobiculariaplana 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.

▲



Figure 4. Over time changes in size-frequency distribution of Scrobiculariaplana and Abra tenuis at Tinja. Cohortsdetected by the HARDING (1949) methodare indicated. 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 mainperiod at the beginning of spring, and a second one in late summer/autumn. The data setindicated high losses during summer. The youngest age class (0) underwent high lossesduring winter, resulting in a dominance of age class I in both species. S. plana rarely excee-ded 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, andthe maximum length observed 15 mm respectively, but most individuals lived only 15–18months growing to a length of 12 mm.

3.3. Production

Production estimates for S. plana varied according to the area. The S. plana production achie-ved by loss summation was 13.45 g AFDM/m2 in the Centre and 21.23 at Tinja (Table 2). TheA. 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 Novem-ber, when growth ceased. During winter, production was almost zero. Production of theremaining 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 determi-ned for the whole lagoon. In order to obtain this overall figure, the production and biomassestimates 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 Julyto April for the deposit-feeding bivalves achieved by loss summation amounted to 8.24 gAFDM/m2 (19.90 g AFDM/m2). The mean C- and N-production from July to April yielded5.26 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 about10% lower. The total bivalve deposit-feeding production (biomass) over the whole lagoonsurface was 741 t AFDM (1791 t AFDM).

The calorific value of the infaunal tissue production was calculated to be 154 kJ/m2. Thetotal 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 haveconsumed 23% of this energy income during the study period. The elimination (E) calcula-

Figure 5. Growth of age classes of Scrobicularia plana and Abra tenuis at Tinja. Bars = standard error,no samples were taken in August and September.



ted by the BOYSEN-JENSEN (1919) method amounted to 104 kJ/m2, rendering the ecologicalefficiency (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 com-pared with results from other studies (GUELORGET and MAZOYER-MAYÈRE, 1982; GUERREIRO,1998; HUGHES, 1970b; KEVREKIDIS and KOUKOURAS, 1992; SOLA, 1997). Among the localfactors that could influence high abundance in the Ichkeul lagoon, we can point to (1) thestability of the sediment; (2) the high organic matter content of the sediment favouring thedevelopment 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 (BCEOMet al., 1995).

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 lagoonas a whole. P1 = production as loss summation (BOYSEN-JENSEN, 1919), P2 = production as

increment summation (MASSÉ, 1968).

Area Age class Biomass P1 P2 P1/B– P2/B

–

S. plana III 3.25 0.43 0.43 0.13 0.13Centre II 13.66 2.09 2.09 0.15 0.15(49.6 km2) I–1 10.28 3.14 3.14 0.31 0.31

I–2 7.03 7.70 6.46 1.10 0.920–1 0.05 0.09 0.05 1.83 1.04

total AFDM 34.27 13.45 12.17 0.39 0.36total C 22.06 8.66 7.84 0.39 0.36total N 2.74 1.08 0.98 0.39 0.36

S. plana IV 2.78 0.35 0.35 0.13 0.13Tinja III 1.94 0.60 0.60 0.31 0.31(3 km2) II 1.98 0.76 0.76 0.38 0.38

I–1 8.79 6.09 6.09 0.69 0.69I–2 7.03 13.43 9.60 1.91 1.370–1 0.01 0.01 0.01 0.51 0.35


A. tenuis II 0.64 0.06 0.06 0.10 0.10Tinja I–1 6.08 2.30 2.30 0.38 0.38(3 km2) I–2 1.01 0.94 0.79 0.93 0.79

0–1 0.04 0.12 0.07 3.00 1.770–2 0.01 0.01 0.01 1.00 0.50


Lagoon mean AFDM 19.90 8.24 7.40 0.41 0.37(90 km2) mean C 12.72 5.26 4.73 0.41 0.37

mean N 1.58 0.65 0.59 0.41 0.37



The reproductive strategies differ considerably for the two species. S. plana has a plank-totrophic development with a long pelagic stage (HUGHES, 1970a). The unfavourable envi-ronmental conditions at Sejnene and Joumine such as low salinity, dense Potamogeton pec-tinatus stands, coarser sediment, high temperature and low dissolved oxygen especially atthe time of settlement in summer prevent S. plana from colonizing these areas. A. tenuis hasa lecithotrophic development (NOTT, 1980) which is interpreted as ensuring the maintenan-ce of populations but population dispersal is very limited.

The strong biomass decrease observed in October can be interpreted as the result of lowercondition factor linked with spawning. Gamete release significantly affects biomass. HUG-HES (1970b) estimated that gametic production could account for 24 to 52% of the total pro-duction which is in line with BACHELET (1982). However, in the Ichkeul lagoon the effectof summer stress on biomass outweighed the effect of spawning on biomass. S. plana is un-able to osmoregulate physiologically (HUGHES, 1970a) and highest mortality occurred essen-tially during summer when temperature, salinity and macrophyte development were highestand dissolved oxygen lowest in the lagoon (BCEOM et al., 1995). High mortality followingspat 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 unfa-vourable 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 relat-ed to the temperature regime in the southern part of the geographical range of both S. planaand A. tenuis. This may result in faster growth, higher density of individuals of smaller sizeand a shorter life span. Although S. plana is obviously capable of substantial horizontalmigration it appears to do so only rarely (HUGHES, 1970a; BACHELET, 1982; GUELORGET andMAZOYER-MAYÈRE, 1983). In October, the arrival in the central lagoon of large numbers ofone-year-old S. plana individuals which had already passed a summer (Fig. 3) can only beexplained by migration as a response to unfavourable conditions. The highly adverse envi-ronmental conditions during late summer eliminate the possible interpretation of the rapidgrowth of a new settlement.

The Ichkeul population of S. plana showed a reproduction pattern similar to that of theArcachon 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 repro-duction 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 recruitmentsin spring and autumn. According to HUGHES (1970a) the differences in the reproductivecycle 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 extendedand occur later, sometimes throughout the winter, but with negligible or no activity in mid-summer (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 populationsand his conclusions seem to confirm this pattern.

These latitudinal differences in reproductive cycles are related to varying local conditionsat times of settlement and during the first six months after settlement which affect the suc-cess of recruitment (HUGHES, 1970a). At densities found in the Ichkeul lagoon, pediveligeror spats could be consumed by adults while deposit-feeding. Thus the poor recruitment has



lead to a dominant age class at Ichkeul. In fact, if one very successful spawning event takesplace, recruitment in the following years may be suppressed due to intraspecific competiti-on for food and space. HUGHES (1970a) and GUERREIRO (1998) postulated a dominant ageclass phenomenon where a population may be numerically dominated by one or a few largeolder classes. Successful recruitment does not seem to be a regular annual phenomenon(DEKKER and BEUKEMA, 1993; GUERREIRO, 1998). In southern Europe, the pattern of popu-lation dynamics of at least S. plana may possibly be dominated by periods of highly suc-cessful recruitment and high production followed by large periods of unsuccessful recruit-ment 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 peri-od. 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 den-sity is increasing. The SIEGISMUND (1982) modification probably still underestimates pro-duction as it neglects the production of individuals recruited during the period of increasingdensity and eliminated before observation at the end of the period. For these reasons andalso because of migration phenomenon within the system, the production estimates achiev-ed by the loss summation method (BOYSEN-JENSEN, 1919) were favoured here. The produc-tion of S. plana from July 1993 to April 1994 amounted to 17.34 g AFDM/m2, and that ofA. tenuis to 3.44 g AFDM/m2 (Table 3). Although determined for only 10 months, this pro-bably 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 otherbrackish coastal areas (HUGHES, 1970b; WARWICK and PRICE, 1975; BACHELET, 1982; GUER-REIRO, 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 compar-ed to other Abra species which may be due to the weak recruitment during the study peri-od 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 productioncan 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 smallindividuals, more than one annual generation and a shorter life span.

The high energy flow through the deposit-feeding bivalves indicates the importance ofthis functional group in the Ichkeul ecosystem. HUGHES (1970b) estimated as much as 1336and 1407 kJ/m2 for S. plana on a Welsh tidal flat, which seems to be very high. The assi-milation in the Ichkeul lagoon was locally close to the above values but weighted to thewhole lagoon surface, the estimate of the average energy flow amounted to 733 kJ/m2 duringthe study period. The consumption was 23% of the total energy input from the lagoonmacrophytes during the study period. Other energy sources may be available in the Ichkeullagoon, e.g. the excrements of the wintering waterfowl and the input through the Tinja chan-nel. As the autumn and winter rainfall was very low during the study period, the nutrientinput from the wadis was negligible. Input of inorganic nutrients can also be attributed tobivalve activity. Through their feeding and burrowing activities, Scrobicularids stimulatemineralization processes in the adjacent sediment. In addition to mixing nutrient-rich pore



waters with overlying waters, the deposit-feeders remove organic material from the watercolumn and excrete remineralized nutrients in form of pseudofeces and through direct excre-tion (ALPINE and CLOERN, 1992). Bivalves can also sequestrate nitrogen and phosphorus. Thereduction 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

Table 3. Comparison of published data on mean biomass (B– in g AFDM/m2), annual pro-duction (P in g AFDM/m2) 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.

Study area B– P P/B– Authors

Abra tenuisIchkeul lagoon (Tunisia) AFDM 7.78 3.44 0.44 this study a

Abra ovataPrévost lagoon (France) DM 0.70 1.50 2.14 GUELORGET and MAZOYER-MAYÈRE (1982)b

Mauguio lagoon (France) DM 14.33 26.10 1.82 GUELORGET and MAZOYER-MAYÈRE (1982)b

Evros Delta (Greece) DM 29.22 17.09 0.59 KEVREKIDIS and KOUKOURAS (1992)c

Abra albaCharente straits (France) DM 1.04 0.81 0.77 HILY (1976)b

Concarneau Bay (France) DM 0.35 1.34 3.83 MENESGUEN (1980)b

Bristol channel (U.K.) AFDM 0.30 0.41 1.35 WARWICK and GEORGE (1980)b

Gironde estuary (France) AFDM 0.80 2.91 3.63 BACHELET (1981b)b

Concarneau Bay (France) DM 0.72 1.45 2.01 GLÉMAREC and MENESGUEN (1980)b

Arcachon Bay (France) AFDM 0.81 2.34 2.87 CORNET (1986)d

Gironde estuary (France) AFDM 4.44 7.31 1.65 CORNET (1986)b,d

Morlaix Bay (France) DM 0.77 1.58 2.04 DAUVIN (1986)b

Ria de La Coruna (Spain) AFDM 2.86 8.80 3.08 FRANCESCH and LOPEZ-JAMAR (1991)b

Santander Bay (Spain) AFDM 0.30 0.85 2.82 LASTRA et al. (1993)b

Abra nitidaNorthumberland coast

(U.K.) AFDM 0.11 0.12 0.11 BUCHANAN and WARWICK (1974)b

Ria de La Coruna (Spain) AFDM 0.35 0.93 2.63 FRANCESCH and LOPEZ-JAMAR (1991)b

Scrobicularia planaConway Bay, marshward

(U.K.) AFDM 4.37 2.97 0.68 HUGHES (1970 b)a

Conway Bay, seaward (U.K.) ADFM 46.24 13.41 0.29 HUGHES (1970 b)a

Lynher estuary (U.K.) ADFM 2.15 0.48 0.22 WARWICK and PRICE (1975)b

Gironde estuary (France) ADFM 11.60 9.13 0.79 BACHELET (1982)a,b

Arcachon Bay (France) ADFM 9.65 12.28 1.27 BACHELET (1982)a,b

Prévost lagoon, marsh-ward (France) ADFM 7.98 31.69 3.97 GUELORGET and MAZOYER-MAYÈRE (1983)b

Prévost lagoon, seaward (France) ADFM 122.87 451.92 3.68 GUELORGET and MAZOYER-MAYÈRE (1983)b

Bidasoa estuary (Spain) ADFM 69.20 83.62 1.21 SOLA (1997)b

Mira estuary (Portugal) ADFM 7.29 4.20 0.58 GUERREIRO (1998)c

Tagus estuary (Portugal) ADFM 28.93 24.71 0.85 GUERREIRO (1998)c

Ichkeul lagoon (Tunisia) ADFM 28.40 17.34 0.61 this studya



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 eutro-phication control. It is difficult to quantify the amount of ingested material derived from thesediment. More studies are necessary to determine food preferences and to quantify actualingestion rates. However, our study allowed quantification of the amounts of organic mat-ter 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 ascommon pochards, oystercatchers, eels and gilthead seabream.

5. Acknowledgements

This study was carried out within the international programme “Etude pour la sauvegarde du ParcNational de l’Ichkeul” financed by the Kreditanstalt für Wiederaufbau (KfW) under the aegis of theTunisian authorities, in particular the Agence Nationale pour la Protection de l’Environnement. Thanksare due to members of the Groupement d’Intérêt Scientifique (GIS) Posidonie for field assistance, tothe colleagues at UMR 6540 CNRS Dimar (Diversité, Evolution et Ecologie fonctionnelle marine) foradvice and work facilities, and to Prof. GERHARD BAUER of the University of Freiburg for critical revi-sion of the manuscript. The present research was supported by a Ph. D. grant from the Landesgradu-iertenförderungsgesetzes (LGFG) Germany. The study would not have been possible without the sup-port of Prof. JÜRGEN SCHWOERBEL, mentor and friend. Finally, the authors are grateful to two anony-mous 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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