Reproduction of the cockle Cerastoderma edule (Linne, 1758) in the estuary of Oued Souss (southwestern Morocco)

2008·8.3 MB·English

by  Hafida Bergayou

,
© SociedadEspañoladeMalacología Iberus, 26 (1): 29-42, 2008
Reproduction of the cockle Cerastoderma edule (Linné,
1758) in the estuaryofOued Souss (southwestern Morocco)
Reproducción del berberecho Cerastoderma edule (Linné, 1758) en
el estuario del Oued Souss (suroeste de Marruecos)
Hafida BERGAYOU**, AbdellatifMOUKRIM*1 Michel MATHIEU** and
,
GIMAZANE**
Jean-Pierre
Recibidoel14-11-2006.Aceptadoel3l-X-2007
ABSTRACT
Field and laboratory investigations were carried out from 2001 to 2003 on a population
of Cerastoderma edule living ¡n the estuary of Oued Souss, ¡n order to determine the
impact of domestic wastewater discharges on the biology of this species. During waste-
water discharges, several episodes of partial spawning occurred from November to
March, followed by another in April-May. The main spawning occurred nevertheless in
August. The gonadic Índex was always higher than 1, so that the period of sexual rest
was short. The period of recruitment (from June to October) was mainly correlated with
spawning peaks. The renewal of the population was ensured by the recruitment ofJune-
July, whereas young cockles recruited from August to October only represented 9.2% of
the population at the end of autumn. Most 1-year-old cockles disappeared during the sum-
mer of the second year following their recruitment. After wastewater pollution stopped, an
important recruitment of young cockles occurred. The spatial distribution of this species
progressed upstream and the biomass of cockles had strongly increased. Because of its
reproduction which takes place throughout the year, C. edule as an opportunistic
species, succeeded in colonizing this site.
RESUMEN
Se realizaron, entre 2001 y 2003, estudios de campo y de laboratorio sobre una pobla-
ción de Cerastoderma eduledel estuario del Oued Souss, con el objetivo de determinar el
impacto de los vertidos de aguas residuales sobre la biología de esta especie. Coinci-
diendo con los vertidos, se produjeron varios episodios de puesta parcial entre Noviem-
bre y Marzo, seguidos de otro en Abril-Mayo. La puesta principal, sin embargo, se pro-
dujo en Agosto. El índice gonádico fue siempre superior a 1, indicando que el periodo de
reposo sexual fue corto. El periodo de reclutamiento (deJunio a Octubre) estuvo esencial-
mente relacionado con picos de puesta. La reposición de la población fue asegurada por
el reclutamiento de Junio-Julio, mientras berberechos jóvenes reclutados entre Agosto y
Noviembre representaban tan solo el 9,2% de la población a finales de otoño. La mayor
parte de los berberechos con un año de edad desaparecieron durante el verano del
segundo año después de su reclutamiento. Al finalizar los vertidos se produjo un impor-
tante reclutamiento de berberechos jóvenes. La especie se extendió río arriba y la bio-
* LaboratoryAquaticEcosystems : MarineandContinentalField, BiologyDepartment, Sciences Faculty, Ibn
ZohrUniversity, BP8106, 80000,Agadir,Morocco.
**LaboratoryofMarineBiologyandBiotechnology,UniversityofCaen, F-14000, Caen, France.
1Correspondingauthor
29
Iberus, 26 (1), 2008
masa de berberechos aumento fuertemente. Por su reproducción que se extiende sobre
todo el año, C. edule, como especie oportunista, fue exitosa en la colonización de este
lugar.
KEYWORDS: Cerastodermaedule,estuary,OuedSoussriver,pollütion,recruitment,reproductivecycle,waste-
waterdischarges.
PALABRASCLAVE: Cerastodermaedule,estuario,OuedSouss,contaminación,reclutamiento,cicloreproductor,
INTRODUCTION
In marine environment, many biotic nation stopped. In view of these objec-
and abioticfactorsmayinfluencethelife tives, the following two questions aróse:
cycle of bivalves. If temperature, salin- Had the discharge of wastewater before
ity, food supply, and tidal exposure are November 2002 caused repercussions
the most important causes known to onthe reproductive cycle ofC. edule and
modulate development in mytilids on the dynamics of this population?
(Seed, 1975), other elements, such as What consequences did thepresence of
intraspecific competition or environ- sea water in the estuary after November
mental contaminants, can result in great 2002 have on the spatial distribution
variations in growth rate of bivalves and biomass of C. edule? To answer the
(Seed and Suchanek, 1992). These first question, monthly investigations
factors also have an effect on the repro- from January 2001 to December 2002
duction, settlement, recruitment, and were carried out in the habitat of C.
production of these molluscs so that edule i) to follow the different stages of
their variations directly affect the devel- sexual maturity in males and females,
opment of beds for each species of andii) to specifythe developmentofthe
bivalve (WiddowsandDonkin, 1992). different generations and cohorts of
Contrary to numerous ecological cockles. To tackle the second question,
reports ontheeffectsofcontaminantson two surveys in 2002 and 2003 during
different marine bivalves, the recovery summer months were performed in the
of mollusc populations after the disap- estuaryofOuedSoussriver.
pearance of pollütion has been less This study complements other
investigated. reports made by our research team in
Theimplantationofawastewaterpu- the same ecosystem (Mouneyrac, Pel-
rification plant since November 2002 LERIN, MOUKRIM, AlTALLA, DUROUAND
alongtheestuaryofOuedSouss, at4km Viault, 2005; Ait Allá, Mouneyrac,
from the mouth of the estuary, had re- Durou, Moukrim and Pellerin, 2005;
sulted inthefactthatthefreshwaterstill Ait Allá, Gillet, Deutsch, Moukrim
running in the river and the decanted and Bergayou, 2005; Bergayou and
wastewaterwerenolongerdischargedin Moukrim, 2003 and Gillet, Gorman,
the estuary but diverted to another Tallec, Moukrim, Mouloud, Anajjar,
Coastalsite:M'Zar,locatedat3kmsouth. AitAllá, BergayouandKaaya,2003).
For this reason, the estuary, upstream to
thepurificationplant,wasonlysweptby
MATERIALS AND METHODS
seatideatthepresenttime.
As there existed a population of
Cerastoderma edule living in the estuary The estuaryofOued Souss is located
of the Oued Souss river, it was interest- on the Atlantic coast, in southwestern
ing to determine the physiological State Morocco and is subjected to an arid
of these cockles during the pollütion climate. The mouth is swept by an
period by wastewater and the changes intense marine hydrodynamism,
which have occurred after this contami- responsible of the presence of great
30
BergayouETAL.: Reproduction ofCerastodermaedulein Southwestern Morocco
Figure 1. Location ofsamplingsites along the estuaryofOued Souss in the BayofAgadir, south-
westernMorocco.
Figura 1. Situacióndelaslocalidadesdemaestreoalo largodelestuariodelOuedSouss, en la bahíade
Agadir, suroestedeMarruecos.
sandbanks in the estuary, with currents respectively, 30 and 100 cockles (length,
linked to high or low tides, and with 20 to 30 mm) were collected by hand at
highsalinity (from31.2to34.2%o). low tide, at monthly intervals (respec-
tively, a total of about 450 and 1300
Reproductive cycle accumulatedcockleswasexamined).
The study of reproductive cycle and Forthefirststudy(histologicalstudy
population dynamics for C. edule were of gonads), the shells of C. edule were
carried out at station 2 (30° 21.97'N opened and soft masses were prefixed
north,9o35.98'Wwest), (Fig. 1). Selected in the Gendre's fixative for 24 h. In the
because ofitshighbiomass ofthecockle laboratory, the shell ofeachbivalve was
population, this station was character- removed and smallpiecesofsoftmasses
ized by fine silty sand 2-5% of organic were post-fixed in a new solution of
matter in the substratum and 340-440 Gendre's fixative for 48 h before being
mg/1ofsuspendedmatterinthewater. dehydrated through a graded series of
Twomethodsforstudyingtherepro- ethanol andbutanol, and finallyembed-
ductive cycle of C. edule were used. The ded in cytoparaffin (56°-58°C). Serial
firstwas a classical histological study of sections (thickness, 5 pm) were made
gonads and was performed from before being stained with Gabe's
January 2001 to March2002. The second trichrome, hemalun-eosin, or Mann-
was a complementary study of condi- Dominici's method (Gabe, 1968). The
tion Índex and microscopic examination maturity of gonads was determined
of gonad smears (Guillou, Bachelet, using the scale proposed by Lubet
and Glémarec, 1991) and was per- (1959) forMytilusedulis (TableI).
formed from August 2001 to August The gonadic Índex (Seed, 1975) indi-
2002. For the first and second study. cates the State of gonad maturity for
31
Iberus, 26 (1), 2008
Table I.Terminologyused byLUBET (1959) and LUCAS (1965) to studymorphologicallyand his-
tologicallythegonadicdevelopmentalstages in bivalves.
TablaI. Terminología empleadaporLubet(1959)yLucas (1965)para elestudio morfológicoyhis-
tológicodeestadiosdedesarrollogonadalen bivalvos.
Lubft'sscale(1959) Lucas'sscale(1965)
Staqe0:sexualrest. StaqeA:sexundetectable.Ihisstagecancorrespondto
Staae1:earlvqametoaenesiswithnumerousqoniae. sexualrest,previtellogenesis,orgameteresorption.
StaqeIII D:spent,completelvemptvlumina.
StaqeII:activelvdevelopinqqonadsbutmatureqametes StaqeB:sexdetectablewithdifficullytothenakedeye.
werenotobserved.
StaqeIIIA:nearripefollideswithmatureqametes. StaqeC:identifiablegonad.Ihefootissalmon-stainedin
StaqeIIIB:spawninq,folliclesdistended. malesandpearlywhiteinfemales.Gonadmaturation
andspawningoccurredduringthisstage.
StaqeIIIC:partialspawninq,partiallvemptvlumina. StaqeD:gonadicreconstitutionwithco-existenceofempty
folliclesandoftubulesshowingnumerousgoniae.
each population and is evaluated from and spermatogoniae, primary and sec-
histological slides. Itwas determinedby ondary spermatocytes, and, lastly, sper-
giving a number to each of Lubet's matids and spermatozoa. The meanper-
gametogenic stages: stage 0 (number 1), centage of each cell category was calcu-
stages I and II (2), stage IIIA (3), stages lated in relation to the total number of
IIIB and IIIC (2), and stage IIID (1). For cells counted. Mean valúes and corre-
each sample of cockles, the number of sponding S.D. were established for each
gonads showing a gametogenic stage is cellcategory.
multiplied by the corresponding For the second study, gonad smears
number; the figures obtained were then and the determinationofsex ratioswere
added and the sumwas thendividedby madeby removing eachbivalve fromits
the totalnumberofcockles studied. This shellandbyrubbing softmasses against
gonad Índex varied from 1 (all gonads a histological slide. The microscopic
were spent, with completely empty examination was made using the scale
lumina) to3 (allgonadswereripe). of Lucas (1965) adapted for C. edule by
The stereological analysis was made Fernandez-Castro, Guillou, Le
onthewholebivalvesusedforthehisto- Pennec, and CARDENAS López (1989)
logicalexaminationsofgonads. Foreach (see table I). The sex ratio (number of
C. edule, three histological slides were females in relation with the total
randomly chosen through the antero- number ofbivalvs with a recognizable
posterior axis. The different cell cate- sex) was performed when this identifi-
gories present in gonadic follicles were cation was easy. A x2test was used to
counted onfiveocularfields (magnifica- determine levels of statistical signifi-
tion: x 100 for females, and x 400 for cance.
males) randomly selected in the visceral The condition Índex represents the
mass. In females, four categories: oogo- variations of dry weight for a standard
niae, vitellogenic oocytes, ripe oocytes, bivalve and aims to elimínate the effect
and atresic oocytes, were considered. In of mollusc growth while revealing an
males, the cells were classified into the accumulationoralossoforganic matter,
following three categories: protogoniae associated with reproduction. A single
32
BergayouETAL.: Reproduction ofCerastoderma edulein Southwestern Morocco
size class (20-30 mm) was considered wastewater, and in 2003, when the dis-
and 30 bivalves were randomly chosen charge stopped) gives insights on the
to determine this condition Índex. The wastewater pollution impact and the
índex selected was that proposed by reestablishment of the ecosystem when
Lucasand Beninger (1985): IC = [(dry this pollution stopped. These investiga-
weight of soft masses) / (dry weight of tions were made in a total of 8 stations
valves) x 1000]. The dry weight was (27 sampling sites) located at 400-500 m
obtained using a dehydration of soft intervals from the estuary mouth up to
masses (or shell) in a desiccator (60°C, the wastewater outlet (Fig. 1). In each
24h). site, four to six sediment samples
m
(surface, 0.0625 2 height, 20 cm) were
,
Populationdynamics collected at low tide according to the
To study the dynamics of the popu- method of quadrats used by Elliott
lation and to specify the period ofjuve- and Decamps (1973, in Bayed, 1982).
nile recruitment, samplings of C. edule These samples were sieved (square
were performed from January to meshes, 1 mm) to recupérate and count
December 2002. This study was also cockles,asabove.
carried out in the station 2. Monthly, Ash-free dry weight (AFDW) was
sixteen sediment samples (surface, determined by dipping molluscs in a
m
0.0625 2 height, 20 cm) were collected solution of 10% HC1 until the shell was
,
at low tide according to the method of completely dissolved. Then, the soft
quadratsusedbyElliottandDecamps parts were dried for 48 h at 80°C,
(1973, in Bayed, 1982). These samples weighed, placed at 600°C for 2 h and
were sieved (square meshes, 1 mm) to weighed again. Theweightlossat600°C
recover and count cockles. The antero- was considered to represent the AFDW
posteriorlengthofeachcocklewasmea- of individuáis and was expressed in
suredusinga calliperrule (precisión, 0.1 g/m2 (Bachelet, Bouchet and
mm). For mollusc sizes less than 5 mm, Lissalde, 1980-1981).
a stereomicroscope equipped with a
micrometric ocular was used. The indi-
vidual valúes recorded for the length of RESULTS
bivalves and sampling dates were com-
pared using the FISAT software Effects of pollution on the biology
(Gayanilo, Sparke and Pauly, 1996) to ofthespecies
draw size histograms in relation to the Reproductive cycle: The study of
frequency of animáis and to make a gonad smears from August 2001 to
modal analysis based on the algorithm August 2002 had allowed to recognize
according to the method by Battacharya sex in 1138 bivalves (87.5%). Within this
(1967). This comparison, with the use of group, the sex ratio of C. edule was
the x2test (at P<0.05) allows to distin- 51.1% ± 2.6%, and was well-balanced at
guish the different size classes in each 1:1 (x2 = 2.5, P < 0.05). No hermaphro-
monthly sample, to determine mollusc dite individuáis were found in this pop-
densities, and to specify recruitment ulation. In September, the A stage
periods. (undetectable sex) was observed in 75%
of cockles and might correspond to a
Spatial distribution, density and previtellogenic phase rather than a
biomass sexual rest, as the percentage of C. edule
To determine the spatial distribu- showingtheC stage (gonad maturation)
tion, density, and biomass (ash-free dry increased in October to reach about50%
weight, AFDW) of cockles, two surveys in November. The frequency of C stage
were carried out in 2002 and 2003 was above 50%between November and
(duringsummerperiod). Thereplication April (Fig. 2A), and subsequently
of this study during these two periods decreased inMay (from 75 to20%), thus
(in 2002, when the estuary received the corresponding to a slightdecreaseofthe
33
Iberus, 26 (1), 2008
Figure2. Distribution ofsexual-developmentstages (A) accordingto thescaleofLUCAS (1965) and
annual cycle ofcondition indexes (B) in the populations ofC. edulestudied fromAugust 2001 to
August2002.Thecumulatedfrequenciesofthedifferentsexual-developmentstagescorrespondedto
thetotalofbivalvesstudied(100%). Fordetailsofeachstage,seeMaterialsandMethods (TableI).
Figura2. Distribución de los estadiosdedesarrollo sexual(A) según la escala deLUCAS (1965)y ciclo
anualdeíndicesdecondición (B) en laspoblacionesdeC. edule estudiadasentreagosto2001yagosto
2002. Lasfrecuencias acumuladas de distintos estadios de desarrollo sexualcorresponden altotalde
bivalvosestudiados(100%). VéaseMaterialyMétodos (TablaL)paralosdetallesdecadaestadio.
condition Índex (Fig. 2B). An episode of 2001- March 2002) than the analysis of
pardal spawning had thus occurred gonad smears. Mature gonads (IIIA
during this last period. In May, the fre- stage)wereoftenobservedonmorethan
quency ofthe D stage (80%) proved that 50% of cockles studied from January to
gametogenesis had resumed. In June April (Fig. 3). Episodesofpardalspawn-
and July, the C stage was the most fre- ingoccurred fromJanuarytoMarch;fol-
quent (65 to 75%) and was followed in lowedbyanotherspawninginApriland
August by a more marked decrease of May (inMay, the IIIB stagewasnoted in
the condition Índex (from 80 to 50%o) 60% of males, Fig. 3A). The reconstitu-
thus indicating an important release of tion of the gonad (IIIC stage) is more
gametes. It may be concluded that two marked in females (Fig. 3B) in May
periods of gamete maturation (C stage), (80%) and seems more precocious in
the first ranging from November to males. In both sexes, this stage devel-
April and the other occurring in June- opedinparallelfromMaytoJulysothat
July,weredifferentiated. pardal spawning occurred during these
The histological study was carried months. In August, the IIIB stage was
outoveralongerperiodoftime (January preponderant in both sexes (80% of
34
BergayouETAL.: Reproduction ofCerastodermaedulein Southwestern Morocco
StaIIID
m
Sta MIC
El Sta IIIB
m
Sta IIIA
Sta II
E
Sta
1
Sta0
A
2001 Months 2002
Sta IIID
m
Sta MIC
E
Sta IIIB
m
Sta IIIA
a
Sta II
Sta
Sta0
B
2001 Months 2002
Figure3. Distributionofgonadic-developmentstagesover2001-2002inthemales (A) andfemales
(B) ofC. edule. The cumulated frequencies ofthe different developmental stages corresponded to
thewholebivalvesstudied(100%). Fordetailsofeachstage,seeMaterialsandMethods (TableI).
Figura3. Distribucióndelosestadiosdedesarrollogonadalsobreelperiodo2001-2001 en machos(A)y
hembras (B) de C. edule. Lasfrecuencias acumuladas de distintos estadios dedesarrollo sexualcorre-
spondenaltotaldebivalvosestudiados (100%). VéaseMaterialyMétodos (TablaI)paralosdetallesde
cadaestadio.
males, 60% offemales), proving that the between January and April, thus con-
main spawning episode had happened. firming the presence of ripe gonads
The resorption of gonads (IIID stage) during this period. The lowest valúes
was observed in a few individuáis after (1.7)werefoundfromJunetoAugust. In
the spawning ofMay and was less than both sexes, the gonadic Índex was
25% from June to August. Several always higher than 1 so that the period
females in IIID stage were noted during ofsexualrestwasshort.
the other months, but they never Gametogenesis in the population ofC.
exceeded 5%. In September, gametogen- edule: Figure 5 gives the results ofstere-
esis started inboth sexes (I and II stages ological analysis. From January to
were found in 95% ofcockles). The mat- March, the percentages of mature
uration of the gonad (IIIA stage) was gametes increased to peak in April.
observed in the first bivalves from Another episode of gametogenesis
OctobertoDecemberandpartialspawn- began in May, as demonstrated by the
ingoccurredfromNovembertoMarch. highfrequenciesofyounggerminalcells
The highest valúes (2.7) of the during this month in both sexes. In
gonadic Índex (Fig. 4) were noted males, the effectofthis developingsper-
35
b
Iberas, 26 (1), 2008
—°"“a —
Figure 4. Annual cycle ofthe gonadic Índex in the males (A) and females (B) ofC. edule over
2001-2002
.
Figura4. Cicloanualdelíndicegonádicoen machos (a)yhembras (b)deC. edule en elperiodo2001-
2002.
matogenesis was high rates of sper- January to April, in July, and from
matids and spermatozoa in June or JanuarytoMarch.
August (grouped frequencies, 75% and Population dynamics: The lengths of
85%, respectively). Infemales,animpor- C. edule measured from January to
,
tant vitellogenesis was observed in May December 2002, are given in Figure 6.
and June so that the highest frequency Theperiod ofrecruitment spanned from
of mature oocytes (55%) was noted in the end of spring to the onset of
July and that of degenerated oocytes autumn. The first settlement ofjuvenile
(60%) in August. In September, the cockles occurred in June. A second
highest percentages of spermatogoniae cohortappearedinJuly, athirdcohortin
(29%) in males and ofoogoniae (37%) in August, and a fourth one in October. At
females were noted, thus indicating the the end of autumn, the individuáis
starting of another gametogenetic wave. recruited in June-July had a length of
mm
From September to December, the 18.3 ±1.8 and constituted 71.6% of
gonadic tissue of males was important, the population. By contrast, those origi-
as the grouped frequencies ofspermato- nating from the grouped cohorts of
goniae and of spermatocytes were more August and October only had a length
mm
than 47%. The same finding was noted of 11.1 ± 1.1 and represented 9.2%
in females during this period (grouped of the population. In addition to these
rates of oogoniae and of vitellogenic recruitments; a few young cockles (2-
oocytes, >70%). Low percentages of 3%) were found for each date of sam-
atresic oocytes (5-25%) were always pling. In summer, there was a strong
observed in females throughout the decrease in the number of cockles mea-
mm
year. suring 24.6 ±1.9 in length. This
From the above study, it can be con- diminution is followed by the almost
cluded that three successive gametoge- complete disappearance ofadultcockles
netic waves were differentiated: the first just after the period of recruitment
one from January to April, the second (August 2002) so that the population of
one from May to July, and the third one C. edulein2002wasmainlycomposed of
from September to March. Ripe cockles young individuáis which are being
for both sexes were predominant from renewedeachyear.
36
BERGAYOUETAL. Reproduction ofCerastodermaedulein Sourhwestern Morocco
:
Spz
Hfl Spc
EH3 Spg
JFMAMJ JASONDJFM
B
2001 Months 2002
Figure 5. Frequencies ofdifferent cell categories in themale (A) andfemale (B) gonads ofC. edule
collectedbetweenJanuary2001 andMarch2002. Maleline: Spc (primaryandsecondarysperma-
tocytes), Spg (protogoniae and spermatogoniae), Spz (spermatids and spermatozoa). Female line:
D (degenerated oocytes), Og (oogoniae), R (mature oocytes), V (vitellogenic oocytes).The cumu-
latedfrequenciesofthedifferentcellcategoriescorrespondedtothewholebivalvesstudied(100%).
Figura 5. Frecuencia dedistintas categorías de células engónadas de machos (A)y hembras (B) de C.
edule recolectadosentreenero2001y marzo2002. En machos: Spc (Espermatocitosprimariosysecun-
D
darios), Spg(protogoniasyespermatogonias), Spz(espermatidiosyespermatozoos);enhembras: (ovoc-
itos degenerados), Og (oogonias), R (ovocitos maduros), V(ovocitos vitelogénicos). Lasfrecuenciasacu-
muladasdedistintosestadiosdedesarrollosexualcorrespondenaltotaldebivalvosestudiados(100%).
Spatial distribution, biomass, and did not exceed 320 individuals/m2 in
structure of population of C. edule 2002, and strongly increased in 2003 to
before and afterwastewaterdischarges reach valúes higher than 4,900
The spatial distribution of C. edule cockles/m2 in several places (these
along the estuary, its density and its valúeswerefound duringtheperiods of
biomass are given in Table II for the recruitment). The mean biomass
summer surveys (2002 and 2003). (AFDW) calculated on the cockle
During the period of wastewater dis- samples collected during summer
charge, the species was confined down- surveys, increased from 2.54 g/m2 in
stream (stations 1 and 2). By contrast, in 2002to 14.87g/m2in2003.
2003, its distribution had extended with Table III shows the different groups
an upstream penetration of cockles up ofcockles constituting the populationin
to the station 5. The density of C. edule summer surveys (2002 and 2003).
37
Iberus, 26 (1), 2008
Length (mm)
0 10 20 30
N=171
N=182
N=207
N=242
N=300
N=244
N=114
N=119
N=256
N=92
N=119
Figure 6. Size distribution of C. edule in the estuary ofOued Souss from January to December
2002 and theprincipal normal components. Month and numbers ofindividuáis measured (N) are
givenforeachsampling.
Figura 6. DistribucióndetallasdeC. edule enelestuariodelOuedSoussentreeneroydiciembre2002
y componentes normalesprincipales. Mesesy número de ejemplares medidos (N) están indicadospara
cadamuestra.
Duringthewastewater discharges inthe DISCUSSION
estuary (July 2002), individuáis are dis-
tributed amongfourgroups: two classes The results reported in the present
mm
withlowestlengths (6.81 ± 1.53 and study on the gonochorism of C. edule
9.97 ± 0.83mm), derivingfroma recruit- agreewiththe reports ofseveral authors
ment in May and June; and two classes (Gimazane, 1971; Kingston, 1974).
mm
ofoíd cockles (24,72 ±2.17 and 27.5 Several cases of accidental hermaphro-
± 0,76 mm). In July 2003, the most fre- dism (4%0) were also noted by Fernan-
quent group (89.2%) was composed of dez Castro, Guillou, Le Pennec and
young individuáis (length, 6.55 ± 1.17 Cárdenas López (1989). In the estuary
mm; 11.76 ± 1.63 mm) originating from of Oued Souss, the sex ratio of cockles
a recruitment in May and June. Another was well-balanced so that pollution did
group ofmédium size (36.25 ± 1.73 mm) not have an influence on the distribu-
appeared for the first time and probably tion of males and females. This finding
comprised cockles more than one year agrees with studies that some authors
oíd, as the absence of growth lines on have performed in other populations of
cockle valves did not allow to easily C. eduleatdifferentlatitudes, suchas the
identify the different age subgroups report by Kingston (1974) along the
constitutingthislastsizegroup. coasts of Kent (UK), that of Ivell (1981)
38