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Distribution, habitat and population densities of the invasive radiata (Molluca: ) along the Northern and Eastern coasts of

Article in Cahiers de Biologie Marine · January 2009

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Distribution, habitat and population densities of the invasive species Pinctada radiata (Molluca: Bivalvia) along the Northern and Eastern coasts of Tunisia

Sabiha TLIG-ZOUARI, Lotfi RABAOUI, Ikram IRATHNI and Oum Kalthoum BEN HASSINE Unité de recherche de Biologie, Ecologie et Parasitologie des Organismes Aquatiques. Campus Universitaire, Université Tunis El Manar, Faculté des Sciences de Tunis, Département de Biologie, 2092 Tunis - TUNISIE. Tel / Fax: (00216) 71881939, Mobile: (00216) 98 234 355. E-mail: [email protected]

Abstract: The Pinctada radiata (Leach, 1814) is an alien species introduced to the and recorded in Tunisia many years ago. However, since its record in Tunisian inshore areas, no studies have been carried out about the spread of this invasive mollusc. Thus, the status of this species is still poorly known and there is a knowledge- gap about its distribution and ecology. The present work is a contribution to the knowledge of the pearl oyster distribution and density of individuals along the northern and eastern Tunisian coasts, at depths situated between 0 and 6 metres. A large part of Tunisian coast was surveyed, stressing some observations concerning the species ecology and its preferred biotopes. The size structure of the five densest populations was also described. Pinctada radiata has not yet reached the northern coasts ( and Bizerta coasts). Density of individuals varied from one locality to another between 0 and 62.67 ± 6.11 individuals m-2. This mollusc prefers to be attached to vertical solid substrata (natural or artificial) within marine habitats with relatively high hydrodynamic conditions. Confined localities such as those inside lagoons seem not to be the preferred habitat for the proliferation of this immigrant species. Size structure analysis showed that the majority of the five examined populations, except for Tunis north lagoon and , were dominated by large individuals exceeding 42 mm in shell height. It is worth noting that the maximum size (100.5 mm) recorded in the lagoon of Bizerta (Njila) is higher than that recorded in previous studies, in particular in its origin habitat (Red Sea). This suggests that Pinctada radiata is well adapt- ed to Tunisian coasts.

Résumé : Distribution, habitat et densité des populations de l’espèce invasive Pinctada radiata ( : Bivalvia) le long des côtes septentrionales et orientales de Tunisie. L’huître perlière Pinctada radiata (Leach, 1814) est l’une des espèces exotiques de la Méditerranée. Elle a été signalée en Tunisie depuis plusieurs années. Toutefois, depuis son signalement sur les côtes tunisiennes, aucune étude n’a été menée sur ce mollusque invasif. Ainsi, le statut de cette espèce est encore mal connu et il existe un déficit de connaissances sur sa distribution et son écologie. Le présent travail est une contribution à la connaissance de la distribution de l’huître perlière et la détermination de sa densité le long des côtes nord et est de la Tunisie, à des profondeurs allant de 0 à 6 mètres. Une vaste partie de la côte tunisienne a été prospectée, en effectuant des observations sur l’écologie et les biotopes préférés par cette espèce. La structure en taille des cinq plus denses populations a également été décrite. Pinctada radiata ne semble pas encore franchir les côtes nord (les côtes de Tabarka et ). Sa densité varie d’une localité à une autre entre 0 et 62,67 ± 6,11 individus m-2. En outre, il semble que ce mollusque préfère être attaché à des substrats solides verticaux (naturels ou artificiels) dans des habitats soumis à des

Reçu le 7 octobre2008 ; accepté après révision le 31 mars 2009. Received 7 October 2008; accepted in revised form 31 March 2009. 132 THE INVASIVE PEARL OySTER PINCTADA rADIATA AlONG TUNISIAN COASTS conditions hydrodynamiques relativement fortes. Les milieux confinés (localités intra-lagunaires) ne semblent pas être des habitats de prédilection pour la prolifération de cette espèce exotique. La majorité des cinq populations examinées, à l’ex- ception de la lagune nord de Tunis et de La Marsa, est dominée par de grands individus dont la coquille dépasse la hauteur de 42 mm. Il est à noter que la taille maximale (100,5 mm), enregistrée dans la lagune de Bizerte (Njila) est plus élevée que celle mentionnée dans des travaux antérieures, en particulier au niveau de son habitat d’origine (mer Rouge). Cela conduit à déduire que Pinctada radiata est bien adaptée sur les côtes tunisiennes.

Keywords: Pinctada radiata l Invasive species l Bivalve l Distribution l Density l Mediterranean Sea l Habitat.

Introduction Isles complex and in Kriti (Zenetos et al., 2007). Pinctada radiata was also intentionally imported for mariculture in The colonization of marine ecosystems by newly many areas of Greece and Italy during the last century. Up introduced species is a phenomenon that has begun to be to date, it has been recorded as common in the eastern more amplified, during the last decades. It seems to be Mediterranean with sporadic occurrences in the western favoured by various anthropogenic activities and the basin (Zenetos et al., 2003). Besides its adaptation to the current global warming (Quignard, 1994; Astraldi et al., subtropical environment of the south-eastern 1995). It has been stated that this phenomenon contributes Mediterranean, its tolerance to chemical contamination has to changing faunistic and floristic composition of the enhanced its expansion in enclosed polluted ecosystems colonized ecosystems and can then affect their ecological (Zenetos et al., 2007). equilibrium (Wolfe, 2002; Torchin et al. 2003). Introduced In Tunisia, the first records of Pinctada radiata was species are common in the marine environment because made by Bouchon-Brandely & Berthoule (1891) and Vassel organisms are easily transported via shipping routes and (1897), in the Gulf of Gabes (southern coast), where it had introduced unintentionally through (Carlton, been confined and proliferated forming very dense 1996). In the Mediterranean Sea, biotopic colonization by populations (Zouari, 1985). In fact, outside the Gulf of exotic species has progressed and increased since 1970 Gabes, the presence of this bivalve is very sporadic along (Gofas & Zenetos, 2003). Thus, various exotic molluscan the eastern Tunisian coastline (Ktari-Chakroun & Azzouz, species have been recorded in different areas (Galil & 1971; Zouari, 1985; Tlig-Zouari, 1993). Research on Zenetos, 2002; Gofas & Zenetos, 2003; Zenetos et al., Pinctada radiata is very sparse and has been limited to the 2003). The Mediterranean Sea currently houses approxi- study of Kerkennah island populations (Tlig-Zouari, 1993). mately 139 exotic molluscs; among them ten species are Apart from some recent records in the inventories of locally invasive (Gofas & Zenetos, 2003; Zenetos et al., benthic macro-invertebrate communities (Diawara et al., 2005). The pearl oyster Pinctada radiata (Leach, 1814) 2008), no study has targeted the current distribution of this was among the first invasive immigrants that arrived to the species along the Tunisian coast and the density of its Mediterranean through the Suez Channel (Monterosato, populations in the habitats recently colonized. The study of 1878). Pinctada radiata is an epifaunal suspension feeder Pinctada radiata in Tunisia seems then to be important. of the subtidal zone and a fouling species, living attached The present study focuses on pearl oyster distribution on by its byssus to hard substrata. Usually it attains a length of the northern and eastern coasts of Tunisia, on the 50-65 mm, but may exceed 100 mm in length. It is a characteristics of colonized habitats, and on the protandric species with sex inversion demographic structure of its populations. occurring in shells of 32-57 mm length. Gonad maturity is controlled by temperature (Tlig-Zouari & Zaouali, 1994). Material and Methods This indo-pacific bivalve has successfully spread through- out the Mediterranean colonizing continually new habitats In the present study, systematic surveys were carried out in the eastern basin (Tlig-Zouari & Zaouali, 1994 & 1998; along the coastal region from Tabarka to Monastir. Galil & Zenetos, 2002; Gofas & Zenetos, 2003; Zenetos et Observations were made during spring 2005 (March and al., 2005) and also in the Adriatic (Vio & De Min, 1996) April 2005) at 31 stations belonging to six sectors from the and Croatia (Doğan & Nerlović, 2008). Recently, it was northern and eastern Tunisian coastline (Fig. 1 & Table 1). recorded in newly invaded Hellenic sites, e.g. the Kyklades A total of 50 surveys were conducted by SCUBA diving, S. TLIG-ZOUARI, L. RABAOUI, I. IRATHNI, O.K. BEN HASSINE 133

Figure 1. Pinctada radiata. Study area sampling stations. 1. Ancient Tabarka harbour. 2. Tabarka El Corniche beach. 3. Tabarka Island. 4. Negro Cape. 5. Sidi Mechreg. 6. Serrat Cape. 7. Enjlaa Cape. 8. Blanc Cape. 9. Bizerta El Corniche beach. 10. Sidi Salem beach. 11. Rimel beach. 12. Bizerta channel. 13. Carrier Bay. 14. Njila. 15. . 16. Ghar Elmelh Lagoon. 17. Kalaat Landalous beach. 18. La Marsa beach. 19. The entrance lock of Tunis north lagoon-Kheireddine side. 20. Entrance lock of Tunis north lagoon-lagoon side. 21. Inner part of Tunis north lagoon. 22. Sidi Rais. 23. Port Prince. 24. . 25. Hammamet harbor. 26. lagoon. 27. El Kantaoui beach. 28. Monastir harbor. 29. Stah Jaber harbor. 30. Stah Jaber. 31. harbor. Figure 1. Pinctada radiata. Stations d’échantillonnage dans la région d’étude. 1. Ancien port de Tabarka. 2. Plage de Tabarka El Corniche. 3. l’ile de Tabarka. 4. Cap Negro. 5. Sidi Mechreg. 6. Cap Serrat. 7. Cap Enjlaa. 8. Cap Blanc. 9. Plage d’El Corniche de Bizerte. 10. Plage de Sidi Salem. 11. Plage de Rimel. 12. Canal de Bizerte. 13. Baie des Carrières. 14. Njila. 15. Menzel Jemil. 16. Lagune de Ghar Elmelh. 17. Plage de Kalaat Landalous. 18. Plage de La Marsa. 19. Porte d’entrée de la lagune nord de Tunis - côté Kheireddine. 20. Porte d’entrée de la lagune nord de Tunis - côté lagune. 21. Partie intérieure de la lagune nord de Tunis. 22. Sidi Rais. 23. Port Prince. 24. Kelibia. 25. Port de Hammamet. 26. Lagune de Hergla. 27. Plage d’El Kantaoui. 28. Port de Monastir. 29. Port de Stah Jaber. 30. Stah Jaber. 31. Port de Teboulba.

calculated to see the spread time of the species and whether a relationship exists between densities and distances from the Gulf of Gabes. To better determine the environmental conditions preferred by the pearl oyster, obtained average densities were compared using a Kruskal-Wallis test taking into account the stations’ characteristics mentioned above and the distances from Gabes Gulf. The categories with one to three prospections per station, at a depth ≤ 6 considered in each of the three qualitative environmental metres, depending on the encounter of Pinctada radiata. If variables were the following: two categories of Pinctada the species was not found after three prospections at the radiata substratum (1, hard substratum i.e. rocks, bivalve same locality, no more prospections were made and the shells or hard artificial substrata, 2, root systems of divers moved to another station. Similarly to the technique seagrasses, i.e. Posidonia oceanica Delile, 1813, or used during similar studies (Tlig-Zouari & Zaouali, 1994 & Cymodocea nodosa Ascherson, 1864), four categories of 1998; Apolinário, 1999; Espinosa & Guerra-García, 2005; substratum covering i.e. dominant vegetation (1, Pinctada Diawara et al., 2008; Tlig-Zouari & Maamouri-Mokhtar, oceanica, 2, C. nodosa, 3, , 4, no vegetal cover) and 2008), the density of individuals was estimated within the three categories of wave action intensity (1, strong, 2, stations where the mollusc was present (20 localities) with moderate, 3, weak). The categories of the latter the use of a 0.25 m2 surface quadrat. Three quadrats were environmental variable were estimated based on data made randomly made in each locality and the pearl oyster density within the localities of study (e.g., Prunus & Pantoustier, was determined as the average of density values obtained in 1974; Oueslati, 1993 & 2004; Ben Charrada, 1997). As for the three quadrats. It was expressed in individuals m-2. The distances from the Gulf of Gabes, the following categories characteristics of each station were recorded, in particular were considered (1, the nearest (localities within the Bay of the sediment type, presence or absence and type of Monastir), 2, near (localities within the Gulf of dominant vegetation and the intensity of wave action. Hammamet), far (localities within the Gulf of Tunis), the Moreover, the distances between the study localities and farest (localities within Bizerta lagoon)). the centre of Gabes Gulf (city of Gabes) where Pinctada To characterize the size structure of pearl oyster radiata was first recorded in Tunisia were approximately populations, samples of Pinctada radiata were randomly 134 THE INVASIVE PEARL OySTER PINCTADA rADIATA AlONG TUNISIAN COASTS Description des différentes populations rencontrées lors de la présente étude. Description of populations encountered during the present study. Pinctada radiata. Pinctada radiata. Tableau 1. Tableau Table 1. Table S. TLIG-ZOUARI, L. RABAOUI, I. IRATHNI, O.K. BEN HASSINE 135 collected within the localities where the mollusc was The pearl oyster was observed in various substratum types. present. To ensure the collecting of juveniles and spats of Indeed, this mollusc was found attached, by its byssus, the species, the entire quadrat surface (0.25 m2) was either to rocks or to the root systems of marine seagrasses scraped carefully. The samples were taken in plastic bags Posidonia oceanica and Cymodocea nodosa (Table 1). bearing the station reference. The samples considered Pinctada radiata was also found attached to the surface of during this study were Bizerta lagoon, La Marsa, Tunis other macroinvertebrate species. The species hosting pearl north lagoon, Hammamet Gulf, and coast of Monastir. In were the bivalves Pinna nobilis Linnaeus, 1758, the laboratory, samples of each station were washed in a 0.5 Linnaeus, 1758, and Mytilus galloprovin- mm sieve. The remaining specimens were then counted and cialis Lamarck, 1819, and the ascidian Pyra microcosmus conserved. The size (total height of the shell) of each (Savigny, 1816) (Table 1). Within certain localities, individual was measured with a digital vernier calliper Pinctada radiata was found fixed to artificial substrata, the (0.01 mm accuracy). The samples were grouped by size iron doors of lagoon locks and shipwreck remains (Table class and the demographic structures of the populations 1). Regarding the substratum cover, the majority of stations were represented by histograms. Average height values hosting pearl oysters were dominated by Posidonia were compared using an Analysis of Variance (ANOVA). oceanica or Cymodocea nodosa or by mixed vegetation The comparison Post-hoc (Tukey HSD) was also applied to consisting of these two seagrasses. Some localities elucidate the differences, in size structure, between the containing Pinctada radiata were also encountered with studied Pinctada radiata populations. Statistical analysis of only algal cover (Table 1). the data was performed using SPSS 11.5 software (SPSS The average density of individuals varied significantly Inc., Chicago, Illinois). (Kruskal-Wallis: H = 5.96; p = 0.014) from one sector to another (Fig. 2), ranging between 0.00 and 62.67 ± 6.11 ind -2 Results m (Table 1). The highest densities were recorded in the localities of Stah Jaber (62.67 ± 6.11 ind m-2), the entrance lock of Tunis north lagoon-Kheireddine side (60.00 ± 10.58 Among the 31 stations, Pinctada radiata was encountered ind m-2), the port of Stah Jaber (52.00 ± 10.58 ind m-2), La at 20 localities including both lagoon and marine (Table 1).

Figure 2. Pinctada radiata. Spatial variation of density along the northern and eastern Tunisian coasts. Figure 2. Pinctada radiata. Variations spatiales des densités le long des côtes septentrionale et orientale de la Tunisie. 136 THE INVASIVE PEARL OySTER PINCTADA rADIATA AlONG TUNISIAN COASTS

Marsa beach (50.67 ± 11.55 ind m-2), Kelibia (50.67 ± 4.62 exceeded 42 mm (Table 3 & Fig. 4). In contrast, the ind m-2) and the entrance lock of Tunis north lagoon-lagoon populations of Tunis north lagoon and La Marsa showed side (48.00 ± 10.58 ind m-2). Within the localities of Bizerta lower average values of total height. They were channel and Hammamet harbor, the average density was distinguished by specimens whose size did not exceed 42 16.00 ± 4.00 ind m-2. As for the average densities recorded mm (Table 2). The maximum size (100.51 mm) noted in the rest of stations, they varied between 4.00 and 8.00 ± during the present study was recorded at Bizerta lagoon 4.00 ind m-2, except for Menzel Jemil and Kalaat Landalous (Njila station). The statistical analysis of average total where the average densities of Pinctada radiata were height showed a significant difference between the estimated to be respectively 1.67 ± 0.58 and 1.33 ± 2.31 ind examined populations (ANOVA: F = 58.718; p < 0.001). -2 m (Table 1). According to the Kruskal-Wallis test applied As for the results of Post-hoc comparison, they showed a to test the relationship between pearl oyster density and the significant difference between most of the examined station environmental characteristics that was taken into populations. The largest significant differences were found account, there was a significant difference between the between the populations of Hammamet Gulf and the other densities in relation to both substratum type (p = 0.013) and populations (Table 4). The difference was not significant hydrodynamics (p = 0.032). However, the probability expressed by the Kruskal-Wallis test showed that pearl between the populations of Bizerta lagoon and Monastir oyster densities were not significantly different in relation and between those of Tunis north lagoon and La Marsa to the dominant vegetation (p = 0.322) and distances from (Table 4). Tukey HSD test allowed classifying the Gabes Gulf (p = 0.888) (Table 2). examined populations into three groups: (1) the two Total height average values of the examined populations populations belonging to the sector of Tunis Gulf (Tunis ranged from 33.57 ± 10.13 mm and 63.50 ± 10.13 mm. The north lagoon + La Marsa), (2) the two populations of majority of the analysed Pinctada radiata populations were Bizerta lagoon and Monastir and (3) the sector of dominated by large individuals whose size equalled or Hammamet Gulf.

Table 2. Pinctada radiata. Kruskal-Wallis Test: relationship between density and observed ecological characteristics (* p < 0.05). Tableau 2. Pinctada radiata. Test de Kruskal-Wallis : relation entre la densité et les caractéristiques écologiques observées (* p < 0,05).

TESTED ECOLOGICAL VARIABLES

Pearl Oyster substrata Categories Number of stations (Total = 20) Average rank H df p Solid substrata 11 13.45 6.223 1 0.013* Seagrass Rhizomes 9 6.89

Dominant Vegetation Categories Number of stations (Total = 20) Average rank H df p Posidonia oceanica 6 9.33 3.490 3 0.322 Cymodocea nodosa 8 11.00 Algae 4 8.00 No vegetative cover 2 17.00

Hydrodynamics Categories Number of stations (Total = 20) Average rank H df p Strong 12 13.17 6.896 2 0.032*

Pearl oyster density Moderate 1 11.00 Weak 7 5.86

Distances from Gabes Gulf Categories Number of stations (Total = 20) Average rank H df p The farest 4 9.38 0.637 3 0.888 Far 8 9.81 Near 4 11.50 The nearest 4 12 S. TLIG-ZOUARI, L. RABAOUI, I. IRATHNI, O.K. BEN HASSINE 137

Discussion Regarding the substratum cover (vegetation), it seems that this parameter influences Pinctada radiata density. The The present study provided the current distribution of the non-significant result of Kruskal-Wallis for this ecological invasive species Pinctada radiata along the northern and variable (Table 2) leads to the suggestion that the presence eastern coasts of Tunisia. The pearl oyster has colonized the of this invasive species does not require a particular type of entire study area except for the coastal region between vegetation in the ecosystems where it lives. The Bizerta and Tabarka (Fig. 2 & Table 1). However, the density comparison of Pinctada radiata densities obtained during of individuals varies substantially from one locality to the present study with the results of previous work reveals another. High densities (> 45 ind m-2) were noted only at six that high densities recorded in the majority of locations stations. Pearl oyster absence from the sectors of Tabarka and remain significantly lower than those recorded by Tlig- Bizerta suggests that this species has not yet colonized the Zouari (1993). The average density found by the latter northern Tunisian coastline. The densest Pinctada radiata author was 119 individuals m-² ranging from 1 to 230 population was encountered in Stah Jaber locality (Fig. 2 & individuals m-². This indicates that within the Gulf of Table 1) where pearl oysters are fixed on Pinna nobilis Gabes, in particular at , reign good shells. Solid substrata of various types (rocks or artificial conditions for pearl oyster proliferation (Tlig-Zouari, 1993; substrata) seem to be more favorable for the settlement of Tlig-Zouari & Zaouali, 1994). very dense Pinctada radiata populations as evidenced by No relationship was found between densities and high densities observed, e.g. the entry lock of Tunis north distances from the Gulf of Gabes (Table 2). In fact, high lagoon-Kheireddine side, the entry lock of Tunis north densities were recorded at nearer (Stah Jaber, Stah Jaber lagoon-lagoon side, La Marsa and Stah Jaber harbour Harbor) and farer distances (Kelibia, entrance lock of Tunis (jetties). It can thus be deducted that Pinctada radiata north lagoon-Kheireddine side, the entrance lock of Tunis attachment on solid substrata, subjected to currents and wave north lagoon-lagoon side and La Marsa) and vice versa. actions, improves the nutritive resources and dissolved Since there are no aquaculture activities of exotic species oxygen levels. Moreover, solid substrata seem to be the along the Tunisian coastline, higher densities of Pinctada preferred substrata of this sessile bivalve, because radiata could be mainly matched to the shipping activities. attachment by its byssus on this kind of substratum is much In fact, highest densities on individuals were noted at the better than on any other type since it allows a good fixing of proximities of important harbors located in the different the species and better exposition to water currents providing sectors of study (Monastir and Stah Jaber Harbors in good feeding conditions (Ranson, 1961; Ricordi, 1993; Tlig- Monastir Bay, Kelibia and Sidi Daouad harbors in Zouari, 1993). Moreover, seagrass roots do not appear to be Hammamet Gulf, and harbor in Tunis Gulf). preferred substrata for Pinctada radiata as evidenced by the The existence of Pinctada radiata at Bizerta lagoon (upper low densities observed. This kind of substratum might not limit of its expansion) can also be due to the same factor allow sufficient nutrition or might harbour a higher level of because of the import harbour of Bizerta which is located at trophic competition with other sessile filter-feeders. the entrance of this lagoon. Similar to the present observations, the investigations of It appears from the present study that the pearl oyster Tlig-Zouari (1993) in the Kerkennah Islands (Gulf of expansion keeps increasing. Unfortunately, no similar Gabes) demonstrated that high densities of Pinctada radiata studies about biogeography and densities of Pinctada were observed at stations presenting solid and vertical radiata were done in Tunisia or elsewhere. The only data substrates (Charfia palms and Iron pickets) whereas low we found concerns Greek coasts where the species was densities were noted at stations presenting Cymodocea firstly reported close to areas where it was originally nodosa and Posidonia oceanica meadows. Otherwise, high introduced for aquaculture (mainly in the Dodekanisos densities of Pinctada radiata were recorded in the stations islands, Argolikos, the Saronikos, Evvoia, and the island of presenting a high activity of hydrodynamics in particular Lesvos in the N Aegean Sea). Recently, the species was currents and wave actions (Table 2). The latter observations also recorded in the Kyklades Isles complex (in 2006) and were confirmed by Kruskal-Wallis tests, which showed in Kriti (in 2003) (Zenetos et al., 2007; Katsanevakis et al., significant differences with this parameter. In addition, low 2008). In addition, Pinctada radiata is a successful invader Pinctada radiata densities recorded in lagoon localities lead into the Mediterranean Sea and its spatial distribution keeps the author to suggest that the harsh environmental increasing (Zenetos et al., 2003; Zenetos et al., 2007). conditions characterizing lagoon ecosystems, in particular The results of research on Pinctada radiata reproduction confinement, prevented pearl oyster proliferation. Confined have demonstrated that this species reaches its first sexual areas do not present the preferred habitats for pearl oysters maturity at a size varying from 15 to 20 mm (Tranter, 1959; that seem to be localized within open environments, i.e. Tlig-Zouari & Zaouali, 1994; Khamdan, 2001a & b). marine biotopes. Average sizes recorded here within the five analysed 138 THE INVASIVE PEARL OySTER PINCTADA rADIATA AlONG TUNISIAN COASTS

Table 3. Pinctada radiata. Variability of minimum (Min), maximum (Max), Average, Mode and Standard Deviation (SD) values of shell height (SH) within the five examined populations (N: number of measured specimens). Tableau 3. Pinctada radiata. Variabilité des valeurs minimales (Min), maximales (Max), du mode et de l’écart-type (SD) de la hauteur des coquille (SH) des cinq populations examinées (N: nombre des spécimens mesurés).

Population N Min SH (mm) Max SH (mm) Average SH (mm) SD Mode

Bizerta Lagoon 54 25.35 100.51 52.08 14.90 42.00 Tunis north Lagoon 55 18.00 69.20 33.57 10.13 22.00 La Marsa 55 29.23 47.43 38.46 4.38 40.00 Gulf of Hammamet 75 33.45 98.27 63.50 16.09 53.63 Coast of Monastir 110 23.35 81.56 49.86 11.58 63.80 populations ranged between 33.57 ± 10.13 mm (Tunis north 42 mm), the other populations were dominated by large lagoon) and 63.50 ± 16.09 mm (Gulf of Hammamet). This pearl oysters (≥ 42 mm) (Table 3 & Fig. 4). Size size varies between 18 mm (Tunis north lagoon) and 100.51 distribution analysis showed that the majority of the mm (Bizerta lagoon). It can thus be deducted that all Pinctada radiata populations were dominated by two or individuals collected during the sampling period were more size groups. The size structure of these populations adults. These values are higher than those noted by Tlig- could relate to alternating periods of good and poor Zouari (1993) in the Kerkennah Islands. That study recruitment during different years. According to Cerrato revealed a permanent presence throughout the year of all (1980), the obtained results seem to confirm that pearl evolution stages, indicating the existence of continual oyster populations on the northern and eastern Tunisian reproductive activity with two spawning peaks during coasts undergo varying recruitment from one year to summer (major spawning) and autumn (secondary spawn- another. ing) (Tlig-Zouari, 1993; Tlig-Zouari & Zaouali, 1994). The Alternatively, the absence of spat from all sampling size structure of the five Pinctada radiata populations stud- localities could be explained by the sampling period, which ied here showed that with the exception of the two was just after the hivernal sexual pause of the species (Tlig- populations of Tunis Gulf dominated by small specimens (≤ Zouari & Zaouali, 1994) or by the fluctuations of

Table 4. Pinctada radiata. Post-hoc comparison (Tukey HSD). Tableau 4. Pinctada radiata. Test de comparaison multiple (Tukey HSD).

I (V1) J (V1) Mean Difference Standard p 95% Confidence Level (I-J) Error Lower Bound Upper Bound

Bizerta lagoon Tunis north lagoon 18.51 2.36 < 0.001 12.08 24.94 La Marsa 13.62 2.36 < 0.001 7.19 20.05 Gulf of Hammamet -11.34 2.20 < 0.001 -17.42 -5.44 Coast of Monastir 2.21 2.04 0.816 -3.36 7.79 Tunis north lagoon Bizerta lagoon -18.51 2.36 < 0.001 -24.94 -12.08 La Marsa -4.89 2.35 0.226 -11.30 1.51 Gulf of Hammamet -29.94 2.18 < 0.001 -35.90 -23.98 Coast of Monastir -16.30 2.03 < 0.001 -21.84 -10.75 La Marsa Bizerta lagoon -13.62 2.36 < 0.001 -20.05 -7.19 Tunis north lagoon 4.89 2.35 0.226 -1.51 11.30 Gulf of Hammamet -25.04 2.18 < 0.001 -31.00 -19.09 Coast of Monastir -11.40 2.03 < 0.001 -16.95 -5.86 Gulf of Hammamet Bizerta lagoon 11.43 2.20 < 0.001 5.44 17.42 Tunis north lagoon 29.94 2.18 < 0.001 23.98 35.90 La Marsa 25.04 2.18 < 0.001 19.09 31.00 Coast of Monastir 13.64 1.84 < 0.001 8.62 18.67 Coast of Monastir Bizerta lagoon -2.21 2.04 0.816 -7.79 3.36 Tunis north lagoon 16.30 2.03 < 0.001 10.75 21.84 La Marsa 11.40 2.03 < 0.001 5.86 16.95 Gulf of Hammamet -13.64 1.84 < 0.001 -18.67 -8.62 S. TLIG-ZOUARI, L. RABAOUI, I. IRATHNI, O.K. BEN HASSINE 139

environmental factors that can cause variability in the Pinctada radiata sexual cycle. Indeed, the variability of cli- matic factors, in particular temperature, is in a wide rela- tionship with gametogenesis. In fact, an increase of temperature favorizes the reproduction activity and maturi- ty of the species (Tlig-Zouari, 1993; Tlig-Zouari & Zaouali, 1994). Similar observations have been mentioned for other species in this genus. e.g., Pinctada albina (Lamarck, 1819) (Tranter, 1958a, b & c) and Pinctada fucata (Gould, 1850) (Tranter, 1959). Thus, low temperatures characterizing the northern and north-eastern localities of Tunisia could be the cause of a temporally limited gonadal activity and not spread as that observed in the Kerkennah Islands (Tlig-Zouari, 1993). In Australia, O’Connor & Lawler (2004) showed that temperature and salinity signif- icantly affect the development, settlement, and survival of Pinctada radiata (mentioned as Pinctada imbricata by Röding, 1798) embryos. According to these authors, the embryo requires a temperature ranging between 18 and 26°C and salinity from 29 to 32. Beyond these limits, meta- morphosis of these embryos to the veliger stage did not occur and settlement of spat was significantly hampered. Moreover, spat scarcity could also be related to . In fact, widespread settlement of pearl oyster spat on adult shells commonly exposes them to predators. This phenom- enon was observed for (Linnaeus, 1758) whose spat and small individuals are often eaten by certain species of fish, , and gastropods, the last mainly of species of Cymatium (Haws & Ellis, 2000). This is also the case for spat of the gastropod ferruginea Gmelin, 1791, settle on adult shells and are then subjected to predation by other species (Laborel-Deguen & Laborel, 1991a & b). The comparison of Pinctada radiata average size on the northern and eastern Tunisian coasts with other Mediterranean populations (i.e., Syria and Greece) revealed that, with the exception of individuals of Njila (74.88 mm) and Hammamet (73.37 mm), collected individuals are on average smaller than that of Greek (69.68 mm) and Syrian (56.63 mm) pearl oysters. Variability in Pinctada radiata size could be related to environmental factors that vary from one habitat to another. In fact, the growth, development and survival of bivalves are in general under the control of physical and chemical parameters, in particular temperature and salinity (Tlig-Zouari, 1993; Tlig-Zouari & Zaouali, 1994). It is worth noting that the maximum size (100.5 mm), recorded in the lagoon of Bizerta (Njila) is larger than that observed by Seurat (1929) Figure 3. Pinctada radiata. Distribution of individuals accord- (85 mm) in El Bibane lagoon and Tlig-Zouari (1993) in the ing to the total height (H: shell height; N: total number of speci- mens). Kerkennah Islands (74 mm). This size is also larger than Figure 3. Pinctada radiata. Distribution des individus selon la that recorded by yassien (1998) and yassien et al. (2000) in hauteur totale (H: hauteur de la coquille; N: nombre total des the Red Sea (93.2 mm) and eastern Mediterranean (64 spécimens). mm), respectively. 140 THE INVASIVE PEARL OySTER PINCTADA rADIATA AlONG TUNISIAN COASTS

In summary, physicochemical, edaphic, trophic, and Carlton J.T. 1985. Transoceanic and interoceanic dispersal of environmental conditions of the northern and eastern coastal marine organisms: the biology of ballast water. Tunisian coasts have not reduced the invasive power of Oceanography and marine biology, an Annual review, 23: Pinctada radiata, which since its introduction, has invaded 313-371. successfully in a relatively short time into new habitats with Carlton J.T. 1987. Patterns of transoceanic marine biological invasions in the Pacific Ocean. Bulletin of marine science, 41: high densities on the eastern coasts of Tunisia from the 452-465. north (Bizerta Lagoon) to the centre (Teboulba). Other Carlton J.T. 1996. Pattern, process, and prediction in marine research on macroinvertebrate and malacofaunal communi- invasion ecology. Biological Conservation, 78: 97-106. ties in Bizerta lagoon (Zaouali, 1978 & 1980; Zaouali & Cerrato R.M. 1980. 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