© Sociedad Española de Malacología Iherus, 30 (2): 97-106, 2012 Reproductive cycle of Scrobicularia plana (da Costa, 1778) (Bivalvia: Semelidae) in two Moroccan lagoons: Khnifiss and Oualidia Ciclo reproductor de Scrobicularia plana (da Costa, 1778) (Bivalvia: Semelidae) en dos lagunas marroquíes: Khnifiss y Oualidia Latifa LEFRERE*, Abdellatif MOUKRIM*', Zaina IDARDARE*, Hafida BERGAYOU* and Abderrazak KAAYA* Recibido el30-VII1-2011. Aceptado el 6-VI-2012 ABSTRACT The gametogenic cycle of Scrobicularia plana (da Costa, 1778) (Mollusca: Bivalvia) was studied in two Moroccan lagoons, both of them exposed to upweiling influence but with dif- ferent climate and environmental characteristics (Oualidia located in Centre near an indus¬ trial orea, and Khnifiss in saharian zone). The gonadal development was studied in both populations by histology and gonadic Índex. At both lagoons, the sex ratio averaged 2:1 in favor of femóles (at Oualidia, X^= 36.4150; df= 24; p= 0.05, and at Khnifiss, 31.4104; df== 20; p= 0.05). The gametogenesis cycle began at Oualidia in September, while at Khnifiss in October. Two periods of spawning in spring and summer months were observed in both sites with small differences. Gonadic Índex never reached the valué 1, and in the gonad of all individuáis different stages of gametogenesis were found. RESUMEN El ciclo gametogénico de Scrobicularia plana (da Costa, 1778) (Mollusca: Bivalvia) fue estu¬ diado en dos lagunas de Marruecos, ambas expuestas a la influencia de upweiling, pero con distintos climas y características ambientales (Oualidia situada en la parte mediana de la costa cerca de una zona industrial y Khnifiss en la zona sahariana). El desarrollo de las gónadas se ha estudiado en las dos poblaciones por histología y por el índice gonadal. En ambas lagunas, la proporción de sexos era en promedio 2:1 a favor de las hembras (en Oualidia, 36,4150, df- 24, p= 0,05 y en Khnifiss, X^- 31,4104, df- 20, p= 0,05). El ciclo de gametogénesis comenzó en septiembre en Oualidia y en octubre en Khnifiss. Dos períodos de puesta en los meses de primavera y verano se observaron en ambos sitios con pequeñas diferencias. El índice gonádico nunca ha alcanzado el valor 1, y en la gónada de todos los individuos se han encontrado distintas etapas de la gametogénesis. INTRODUCTION The lagoons are part of Coastal envi- remain the weakest and most vulnerable ronments, and are among the most pro- because of natural and human effects. In ductive natural marine ecosystems but Morocco, there are four lagoons, with * Laboratory Ecosystémes Aquatiques : Milieu marin et continental, Sciences Faculty, Ibn Zohr University, BP. 32/S, Agadir, 80 000, Morocco. ^ Correspondance to Abdellatif Moukrim ([email protected]) 97 Iberus, 30 (2), 2012 different bio-ecological and climatic In the present work, we study the characteristics: Nador lagoon (on the reproductive biology of this species by Mediterranean coast) and Moulay Bous- histological techniques from two selham, Oualidia, and Khnifiss (located lagoons, Oualidia (northern industrial on the Atlantic coast). They have impor- area) and Khnifiss (saharan zone), dif¬ tant ecological, biological and socio-cul- ferent by their climate and environmen- tural valúes, and are most importan! tal characteristics, but both of them wetlands as stopover and wintering exposed to the influence of upwellings. sites for thousands of migratory birds (Lakhdar Idrissi, Orbi, Zidane, Hilmi, Sarf, Massik and Makaoui, 2004). MATERIALS AND METHODS The few studies realized on the Moroc- can lagoons, have been limited in time and Study sites (Fig. 1) to some aspects: Chemical contamination Oualidia lagoon (32° 44' 42" N, 9° 02' (Cheggour, Chafik, Langston, Burt, 50" W) is located between El Jadida and Benbrahim and Texier, 2001), avifauna Safi in a highly industrialized urban area (Radi, Bergier, El Idrissí, Qninba, on the Atlantic coast. This lagoon is 7 km Zadane and Dakki, 2009; Zadane, long and on average 0,5 km wide, and Qninba, Ibn Tattou and Bergier, 2009), exchanges water with the ocean through hydrology (Lakhdar Idrissi et al., 2004). a major inlet about 150 m wide and 2 m In the last years, a multidisciplinary deep. Rainfall over the región accounts program (physical chemistry, structure of only for 1% of the fresh water entering the macrobenthic communities, pollutants, lagoon. The annual average rainfall, esti- ecotoxicology and microbiology) has been mated from 1977 to 1998, is about 390 mm, carried out by our laboratory in two la¬ with a máximum in December and no rain goons: Khnifiss and Oualidia (Id arad are, in the dry period from autumn (October) Chiffoleau, Moukrim, Allá, Auger, until spring. The drought began in June Lefrere and Rozuel, 2004). As a part of and continued until September. There are this research program, we have studied the two large industrial complexos around reproductive cycle of : Scrobicularia plana this coast: Jorf Lasfar and Safi. Banaoui, (da Costa, 1778) an importan! and char- Chiffoleau, Moukrim, Burgeot, Kaaya, acteristic species of lagoon ecosystems. Auger and Rozuel (2004) have reported Scrobicularia plana is a common inter¬ a high contamination of Cd (29 jUg/g dw) tidal sentinel species inhabiting soft sub¬ in Perna perna near the main discharges straía in estuarios and Coastal areas from from these industrial complexos. Similar the Atlantic and the Mediterranean, with a results were reported by Chafik, Cheg¬ wide range of distribution (Tebble, 1976). gour, COSSA AND SiFEDDINE (2001) who Because of this many studies have involved studied the contamination of Mytilus gal- it (Paes-Da-Franca, 1956; Hughes, 1971; loprovincialis in the same sites. Worrall, Widdows and Lowe, 1983; The Khnifiss lagoon (20 km long and Zwarts, 1991; Essink, Beukema, Coosen, 65 km2 surface area) is located between Craeymeersch, Ducrotoy, Michaelis Tantan and Tarfaya (28° 02' 54" N, 12° 13' AND Robineau, 1991; Sola, 1997; 66" W). It opens up into the Atlantic Guerreiro, 1998; Rodríguez de la Rúa, Ocean through a narrow inlet called Prad, Romero and Bruzón, 2003; "Foum Agoutrir", about 100 m wide. This Raleigh and Keegan, 2006). lagoon, far from anthropogenic activity is In Morocco, studies on the biology part of the national biological and eco¬ of Scrobicularia plana have concerned the logical reserve created on September 2006 dynamics of population monitoring (Pare National de Khnifiss, décret n° (Kourradi, 1987; Cheggour, 1988; 2.06.461 of 26 September 2006).The lagoon Bazairi, 1999). The reproductive cycle is the only one located in the Saharian bio- of S. plana was studied at the estuary of climatic level. The water circulation to the Oued Souss (Agadir) through histologi- lagoon is rich in nitrogen and phosphate cal studies (Bergayou, 2006). components, especially during spring 98 Lefrere ETal.'. Reproductive cycle of Scrobiculariaplana in two Moroccan lagoons Figure 1: Location of the lagoons of Oualidia (1) and Khnifiss (2). Figura 1: Situación de las lagunas de Oualidia (1) y Khnifiss (2). tides. The high amount of chlorophyll in Reproductive cycle parameters the lagoon is related to the presence of up- studied welling in the Coastal area during spring In total 905 specimens were and summer months. Previous studies sampled, 582 from Oualidia and 323 have shown that the lagoon of Khnifiss is from Khnifiss (shell length 23 to 32 an environment recommended for shell- mm). For histological study of gonads, fish (Lakhdar Idrissi et al., 2004). shells of S. plana were opened and soft parts were fixed in Bouin for 24 h. In the Sampling laboratory, the shell of each bivalve was Samples of Scrobicularia plana were removed and small pieces of soft parts collected from January 2005 to January were post-fixed in a new solution of 2006 in Oualidia, and Khnifiss, except Bouin. The central región of the foot was January and September for the latter removed before being dehydrated lagoon. Samples were taken in mud flats through a graded series of ethanol and on a monthly frequence. Water tempera- butanol, and finally embedded in wax. ture was recorded in each sampling Sections 7 pm in thickness were then cut period. and stained with Flematoxilin of 99 íberus, 30 (2), 2012 Table I. Gametogenic scale used to determine histological stage of the gonadic developmental in S. plana according to Lubet (1959). Tabla /. Escala gametogénica utilizada para determinar el estadio histológico de desarrollo de la gónada en S. plana, según LuBET (1959). Stage Bríef descríptíonaf gonad Stage 0 Sexual rest Stage 1 Early gametogenesis Stage IIID Spent, completely empty lumina Stage II Actively developing gonads but mature gametes were not observed Stage IIIA Near ripe follicles with mature gametes Stage IIIB Spawning follicles distended Stage IIIC Partial spawning, partially empty lumina Carazzii/ eosin (Martoja et Martoja, ratio was determined during the months 1967). The different stages of gonadal of sexual activity, when the sexes are development were scored according to easily recognizable. In Oualidia, 546 Lubet (1959) (Table I). specimens were analysed; the percentage Quantitative analysis of the repro- of females and males was respectively 63 ductive cycle was estimated from the and 37 %. The sex ratio averaged 2:1 in gonadic índex. This índex (Seed, 1975) favour of females (X^= 36.4150; df= 24; P= indícales the State of gonad maturity for 0.05). At Khnifiss, a total of 299 individu¬ each populatíon and ít ís obtaíned from áis were analysed. The males represented histological data. It was determíned by 37.8 % and females 62.2 %. The sex ratio gíving a number to each of the gameto- is in favour of females 2:1 {y}= 31.4104; genic stages of Lubet (1959): stage 0 df= 20; P= 0.05). (number 1), stages I and II (number 2), stage IIIA (number 3), stages IIIB and Gametogenic cycle IIIC (number 2) and stage IIID (number The distribution of the gametogene- 1). For each sample of clams, the sis stages in Scrohicularia plana (both fe- number of gonads showing a gameto- males and males) of Oualidia or Khnifiss genic stage is multiplied by the corre- lagoon, according to Lubet's scale (1959) sponding number. The figures obtaíned is given in Figures 2 and 3. The gameto¬ were then added and the sum was then genic cycle of the populations from both divided by the total number of clams sites shows few differences. studied. This índex broadly defines the In clams from Oualidia lagoon, the reproductive condítion of the popula- stage 0 (sexual rest) and 1 (early game- tion at any particular time. An increas- togenesis) seems to begin from Septem- ing Índex in successive samples indi- ber (20% SO, 25% SI) to December cates that gonads are developing, while (39.13% SI) in females. Developing a falling Índex means that spawning is gonads with mature gametes, stages II in progress. (16.67% in January) and IIIA (41.67% in May) occurred from January to August with peaks of spawning in both females RESULTS and males. In this period, males from Oualidia were either ripe (IIIA stage) or Sex ratio in spawning (IIIB stage). From April to During this study, approximately August, females were also either ripe or 6.18% and 7.43% of the sampled popula- spawning. In males, we observed IIIC tion, at respectively Oualidia and stage (17.64%) from April and IIID Khnifiss, could not be sexed. The sex (33%) stage from May. 100 Lefrere ETal.: Reproductive cycle of Scrobiculariaplana in two Moroccan lagoons The population of Khinifiss showed Oualidia lagoon (Fig 4A), the tempera- stages 0 and 1 from October to Decem- ture shows increasing levels from ber (as revealed in males). Some indi¬ January to April. Another peak has been viduáis in development of gonad were detected in October. also found in this period. Stage IIIA In Khnifiss lagoon, the temperature (15%) was observed in early October increases from February to April fol- and continued with importan! percent- lowed by a small decrease until July. ages of females until March (23%).Peaks Máximum valué was also observed in of spawning (ÍIIB stage) occurred in August. August and November-December. The spawning of August was the most importan! in both females and males DISCUSSION (50%). Increasing percentages of Stages IIIC and IIID have been observed from Over the course of our investigations early April. the reproductive cycle of Scrobicularia plana was studied in Oualidia and Gonadic Índex Khnifiss lagoons. We have used speci- In Oualidia lagoon, gonadic Índex mens with shell length ranging between shows increasing valúes from February 20 and 32 mm (both sites considered). to April (stage I and II). Principal Raleigh and Keegan (2006) had spawning occurred in March which reported that sexual maturity was seems to be related to an increase in attained at approximately 22 mm in temperature levels. From April, there shell length in Mweelon Bay (Galway, was a decrease in gonadic indices (stage west coast of Ireland). A similar valué IIIB) together with a decrease of sea was also reported by Paes-da-Franca water temperature. After spawning, a (1956), Sola (1997) and Guerreiro reconstruction of the gonad and addi- (1998). Hughes (1971) observed that S. tional spawning were observed, plana reaches sexual maturity in the (optional periods of spawning were second summer of life, in the animáis observed in September and November) with a shell length of 20 mm. (Figure 4). Rodríguez de la Rúa et al. (2003) In Khnifiss lagoon, gonadic Índex reported that the smallest size analyzed decreases between February and April, measured 23 mm in the Guadalquivir which corresponded to a spawning estuary (South West of Spain). period and was coincident with a No hermaphroditic animáis were decrease of the temperature valúes. In observed during our study. Hughes July, when temperature levels increase, a (1971), Sola (1994) and Rodríguez de further spawning event was recorded. LA Rúa (2003) obtained the same results, The rest of the active period corre- and established that S, plana is predomi- sponds to reconstructions of the gonad nantly a dioecious species. However, and additional spawning. Paes-da-Franca (1956) reported a In both sites, the gonadic Índex máximum of 4.42% showing this condi- never reached 1. This shows that the tion in a Portuguese population, and resting period is reduced in Scrobicularia Raleigh and Keegan (2006) indícate plana in Oualidia and Khnifiss lagoons. one hermaphroditic condition in a Mweelon Bay (Galway, west coast of Temperature Ireland) population. Although this con¬ Figure 4 shows the variations of tem¬ dition is rare in S. plana, Lammens perature along the sampling period. A (1967) indicates that it is usual to find a similar temporal pattern was observed small number of hermaphrodite speci- in both lagoons. The lowest valúes (15 mens in gonochoristic bivalve species, °C) were observed in December whereas like in the case of Anodonta cygnea for the warm period (April-October), (Linné), Mytilus edulis (Linnaeus) and valúes were between 20 and 30°C. In Dreissena polymorpha (Pallas). 101 Iberus, 30 (2), 2012 (cid:9632) S3 D S3C m S3B m S3A (cid:9633) S2 (cid:9633) SI A (cid:9633) SO >• Months S3 (cid:9632) D S3C S3B (cid:9632) S3A (cid:9633) S2 (cid:9633) SI (cid:9633) SO o<-^’ /(cid:9632) Months Figure 2. Percentage of occurrence of different stages of gametogenesis in Scrobicularia plana sampled from Oualidia lagoon (A: females; B: males). The cumulated frequencies of the different developmental stages corresponded to ali bivalves studied (100%). Figura 2. Porcentaje de ocurrencia de las diferentes etapas de la gametogénesis en Scrobicularia plana maestreada en la laguna de Oualidia (A: hembras, B: machos). Las frecuencias acumuladas de las dis¬ tintas etapas de desarrollo corresponden al total de los bivalvos estudiados (100%). Ai both lagoons, the overall sex ratio In this study, we observed two prin¬ recorded by the current study indicates cipal periods of spawning in popula- a predominance of females over males tions, the first in spring and the second (at Oualidia: 63 % to 37 %, x2= 36.4150; in summer. In Oualidia lagoon, gonad df= 24; P= 0.05; at Khnifiss: 62.2 % to development in Scrobicularia plana began 37.8 %, 31.4104; df= 20; P= 0.05). in September (early autumn), and the Otherwise, in other studies, Paes-da- spawning period began in March Franca (1956) had also found a slightly (spring). S. plana from this lagoon higher number of females than males showed an extended period of gamete (1.2:1). By the same token, Raleigh and release, from March to August. Addi- Keegan (2006) reported a rate of 1.1:1, tional spawning periods have been but balanced it to 1:1. recorded along the study period (espe- 102 Lefrere ETal.: Reproductive cycle of Scrobiculariaplana in two Moroccan lagoons (cid:9632) S3 D (cid:9632) S3C El S3B (cid:9632) S3A (cid:9633) S2 (cid:9633) SI (cid:9633) SO 70- 60- ^ 50- 40- 30- 20- 10- Months Figure 3. Percentage of occurrence of different stages of gametogenesis in Scrobicularia plana sampled from Khnifiss lagoon (A: females; B: males). The cumulated frequencies of the different developmental stages correspond to all bivalves studied (100%). Figura 3. Porcentaje de ocurrencia de las diferentes etapas de la gametogénesis en Scrobicularia plana maestreada en la laguna de Khnifiss laguna (A: hembras, B: machos). Las frecuencias acumuladas de las etapas de desarrollo diferentes corresponden al total de los bivalvos estudiados (100%). cially in September (late summer) and According to Fíughes (1971) and in November (autumn). In Khnifiss, the Essink et al., (1991), the differences in gonad development began in October the prolongation of the reproductive and the spawning occurred in April and cycle of S. plana, would be due to latitu¬ July (it seems that this is caused by an dinal and thermal differences along the increase of temperature valúes). Active Atlantic coast (Sola, 1997). At first, the gametogenesis continued with recon- start of gonad development is reached struction of gonad and additional when mean temperature was an average spawning periods. Gonadic Índex never of 20°C (Oualidia: 15°C to 25°C; reached the valué of 1, and all individu¬ Khnifiss: average of 20°C). In Spain, the áis were at various stages of gametogen¬ start of gametogenesis coincided with esis evolution. an increase of temperature in the 103 Iberus, 30 (2), 2012 Figure 4. Variation of gonadic Índex (squares) and water temperature (triangles) throughout the study period. A: Oualidia; B: Khnifiss. Figura 4. Variación del índice gonádico (cuadrados) y de la temperatura del agua (triángulos) durante el período de estudio. A: Oualidia; B: Khnifiss. months of January (Sola, 1997) and resting period in December with tem¬ Febmary (Rodríguez de la Rúa et al., perature of ca. 14 °C. The same result 2003). Fíughes (1971), in his study in was reported throughout the current North Wales, found development of study, and we found differentiated gonad to begin at a later date (April). gametes in all months of the sample Raleigh and Keegan (2006) found that period (except during the resting gonad development began in January/ period). An increase of temperature at February when the water and substrate Oualidia could be responsible for the temperature were, on average, 9°C. beginning of gametogenesis. The time Paes-da-Franca (1956), in a popula- available for gonadal development may tion of Scrobicularia plana of Portugal, decrease in relation to latitude increas- found differentiated gametes in nearly ing, until just beyond the geographical all months of the year, except a short limit of the species. 104 Lefrere ETAL.: Reproductive cycle of Scrobiculariaplana in two Moroccan lagoons According to several authors, S. plana Rodríguez de la Rúa, Romero and is a species whose reproductive cycle Prado, 2000): the first one occurring in varíes with latitude (Paes-da-Franca, spring and the second in summer. These 1956; Hughes, 1971; Bachelet, 1981; results are similar to those found in Guerreiro, 1998; Rodríguez de la Rúa Moroccan lagoons ET AL., 2003; and Raleigh and Keegan, Worrall et al. (1983), who studied 2006) with Southern populations exhibit- S. plana from three different estuarios in ing more than one annual spawning Southwest England, observed signifi- period. Studies conducted in North cant variations between local popula- Wales (Hughes, 1971), northwest Spain tion, with differences in the timing and (Sola, 1997) and the west coast of Ireland duration of the breeding cycle. It is (Raleigh and Keegan, 2006) recorded attributed to food availability, suggest- an increase in development from March ing that the shorter time window during onwards, spawning occurring from June which food was available at one site to August and gonad regression in Sep- necessitated more rapid gameto devel¬ tember. Studies carried out on Iberian opment and caused earlier spawning. populations (Paes=da-Franca, 1956; According to Hughes (1971) and Essink Guerreiro, 1998; Rodríguez de la Rúa ET AL. (1991), the differences in the pro- ET AL., 2003) reported two spawning longation of the reproductive cycle of S. periods. In Southern Spain, bivalve plana would be due to latitudinal and spawning periods are known to be longer thermal differences along the Atlantic due to latitudinal characteristics, which is coast (Sola, 1997). Paes-da-Franca consisten! with the February to Septem- (1956) and Rodríguez de la Rúa et al. ber spawning period proposed for Salen (2003) observed that variations in the marginatus from Bajo de la Cabezuela le veis of chlorophyll "a" might affect the (Bay of Cádiz, SW Spain) (Bruzón, reproduction cycle of S. plana. BIBLIOGRAPHY Bachelet G. 1981. Données préliminaires sur Chafik A., Cheggour M., Cossa D. and Sifed- l'organisation trophique d'un peuplement dine S.B.M. 2001. Quality of Moroccan Atlan¬ benthique marin. Vie et Milieu, 31: 205-213. tic Coastal waters: water monitoring and mus- Banaoui a., Chiffoleau J.-F., Moukrim A., sel watching. Aquatic Living Resources, 14: Burgeot T., Kaaya a., Auger D. and 239-249. Rozuel E. 2004. Trace metal distribution in Cheggour M. 1988. 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