Comparative Morphometric Study of the Invasive Pearl Oyster Pinctada Radiata Along the Tunisian Coastline

Biologia 65/2: 294—300, 2010 Section Zoology DOI: 10.2478/s11756-010-0023-9

Comparative morphometric study of the invasive pearl oyster Pinctada radiata along the Tunisian coastline

Sabiha Tlig-Zouari, Lotﬁ Rabaoui,IkramIrathni,MoctarDiawara & Oum Kalthoum Ben Hassine

Unité de Recherche de Biologie, Ecologie et Parasitologie des Organismes Aquatiques, Campus Universitaire, Université Tu- nis El Manar, Faculté des Sciences de Tunis, Département de Biologie, 2092 Tunis, Tunisie; e-mail: [email protected]

Abstract: In order to study the relative growth of the pearl oyster Pinctada radiata in Tunisia, a total of 330 individuals of this species were collected from six sites along the Tunisian coastline. Quantitative measurements of collected oysters were conducted for shell height, shell length, shell width, hinge length, height and width of the nacreous part and wet weight. The size structure of the sampled populations was described and the relative growth between different morphometric characteristics was estimated as allometric growth lines for the six P. radiata samples. It appeared that the majority of examined samples were dominated by large individuals that exceed a shell height of 42 mm. The maximum size (100.5 mm), recorded in Bizerta lagoon, is bigger than that recorded elsewhere in particular in the Red Sea. Size distribution analysis also showed that the majority of P. radiata samples were dominated by two or more size groups. Differences of allometric regression were found between the examined samples for the tested relationships. Moreover, the Factorial Discriminant Analysis, coupled with Ascending Hierarchic Classification, classified the sub-populations according to geographic locations. Key words: morphometry; pearl oyster; Pinctada radiata; Tunisian coastline

Introduction dric hermaphrodite species and the size of first sexual maturity happens at a size of 17 mm. It was reported in The pearl oyster Pinctada radiata (Leach, 1814) is Tunisia that sex inversion occurs in shells of 32–57 mm one of the first exotic immigrants that arrived to the length and gonad maturity is controlled by temperature Mediterranean Sea through the Suez Channel (Mon- (Tlig-Zouari 1993; Tlig-Zouari & Zaouali 1994). Stud- terosato 1878). This indo-pacific bivalve has success- ies carried out on P. radiata outside its original area fully passed through this Canal and spread through- are scarce (Tlig-Zouari 1993; Yassien et al. 2000; Mo- out the Mediterranean basin colonizing continually new hammed & Yassien 2003) and ecological and biological habitats. Indeed, this species has been recorded sev- characteristics of this species within its new habitats eral times in both eastern and western basins (Galil are spatially and temporally limited. & Zenetos 2002; Gofas & Zenetos 2003; Zenetos et al. Pinctada radiata is consumed and appreciated in 2005). It was also mentioned in the Adriatic (Vio & some Tunisian coastal regions such as Kerkennah is- De Min 1996). In Tunisia, P. radiata was reported, lands, the island of Djerba and in the region of Bizerta. for the first time, by Bouchon-Brandely & Berthoule Thus, it can be an interesting and complementary food (1891) and Vassel (1897) in the Gulf of Gabes (Southern source. However, biological and ecological characteris- coastline) where it had confined and proliferated form- tics of the species, in Tunisia, remain poorly known. ing very dense populations (Tlig-Zouari 1993). In fact, The only studies about Tunisian P. radiata popula- outside the gulf of Gabes, the presence of this bivalve tion were carried out in the Archipelago of Kerkennah is very sporadic along the eastern Tunisian coastline and interested the species reproduction, its growth and (Ktari-Chakroun & Azzouz 1971; Tlig-Zouari 1993). its demographic and biometric features (Tlig-Zouari P. radiata is now established along nearly the entire 1993; Tlig-Zouari & Zaouali 1994, 1995, 1998). The Tunisian coastline, from the Libyan frontier to Bizerta knowledge-gap about relative growth and stocks of P. lagoon which represents the northern limit of its cur- radiata along the Tunisian coastline, in particular the rent distribution. P. radiata abounds in many areas of northern and eastern sectors, led us to make a research the Tunisian coastline: the Gulf of Gabes, Monastir Bay about this bivalve. The present study aims to character- and the Gulf of Tunis (Tlig-Zouari et al. 2009). ize the morphometry and compare the relative growth Pinctada radiata is an epifaunal suspension feeder of 6 Tunisian P. radiata populations from the northern of the subtidal zone and a fouling species. It is a protan- and eastern coasts of the country.

c 2010 Institute of Zoology, Slovak Academy of Sciences Morphometry of Pinctada radiata along the Tunisian coasts 295

Fig. 1. The sampling sites of the six studied Pinctada radiata samples: N1 – Bizerta lagoon (in Bizerta coast), N2 – Tunis north lagoon, N3 – La Marsa (in Tunis gulf), E1 – Hammamet harbour (in Hammamet coast), E2 – Monastir and E3 – Stah Jaber (in Fig. 2. Morphological measurements of the shell in Pinctada ra- Monastir bay). diata.

Material and methods graphic structures of the considered sub-populations were Six samples (N1: Bizerta lagoon, N2: Tunis north lagoon, represented by histograms. Shell heights of samples were N3:LaMarsa,E1: Hammamet harbour, E2: Monastir and compared using the non-parametric test of Kruskal-Wallis. E3: Stah Jaber) of wild P. radiata specimens were collected Relative growth between different morphometric char- by divers at 3–6 m depths in 6 sites from the northern and acteristics was investigated using the shell height (SH) as eastern coasts of Tunisia (Fig. 1). At each site, 55 specimens reference variable. The relative growth was then represented were randomly collected within an area of 200 m2 which was as allometric growth regressions (lines) for the six P. radi- randomly chosen (Tlig-Zouari & Zaouali 1995, 1998). A to- ata samples by applying the linear least squares method tal of 330 specimens, ranging 18–100.51 mm shell height for log-transformed data of each characteristic (Schwartz (SH), were used in this study. Morphological measurements 1963; Sokal & Rholf 1994). A single allometric relationship of live oysters were conducted after shell cleaning. Speci- between wet weight (WW) and shell height (SH) was also mens were measured for shell height (SH), shell length (SL), performed for each P. radiata sample. The parameters a, b shell width (SW), height and width of the nacreous part of allometric equations were estimated and analysis of co- (Hpn and Lpn) and hinge length (HL) on the left shell to variance (ANCOVA) was used to compare the difference in the nearest 0.01 mm by a digital vernier calliper (Fig. 2). tested variables among populations. Factorial Discriminant Parts of the measurement were done similarly to previous Analysis (FDA) and the Ascending Hierarchic Classification studies about Pinctada genus (Hynd 1955; Hwang & Oku- (AHC) were also applied using the log-transformed morpho- tani 2003). Wet weight (WW) including shell and soft body metric data to check differences among the studied samples. was weighted to the nearest 0.01 g by an electronic scale. Statistical analyses of the data were performed using Excel, The samples were grouped by size classes and the demo- SPSS 11.5 and Rgui package softwares. 296 S. Tlig-Zouari et al.

Fig. 3. Distribution of Pinctada radiata individuals according to the total shell height (SH) in six examined populations.

Table 1. Estimated parameters of allometric growth (for the relationships ln (SL)–ln (SH), ln (SW)–ln (SH), ln (Hpn)–ln (SH), ln (Lpn)–ln (SH), ln (HL)–ln (SH) and ln (WW)–ln (SH)) of Pinctada radiata in the six examined populations at 95% conﬁdence intervals.

Metric N1 N2 N3 E1 E2 E3 characters (Y–X) abR2 abR2 abR2 abR2 abR2 abR2 ln(SL)–ln(SH) 0.718 1.095 0.860 0.748 0.889 0.848 0.967 0.103 0.809 0.927 0.235 0.949 1.027 0.149 0.968 0.972 0.093 0.884 ln(SW)–ln(SH) 1.095 1.476 0.850 0.892 0.715 0.753 0.766 0.106 0.579 1.387 2.624 0.936 1.162 1.709 0.908 1.111 1.518 0.836 ln(Hpn)–ln(SH) 0.988 0.192 0.980 0.986 0.238 0.893 0.896 0.176 0.918 0.943 0.023 0.079 1.003 0.264 0.981 0.996 0.233 0.943 ln(Lpn)–ln(SH) 0.851 0.275 0.927 0.823 0.305 0.860 0.871 0.220 0.773 0.849 0.261 0.914 1.068 0.620 0.968 1.008 0.347 0.839 ln(HL)–ln(SH) 0.497 1.864 0.577 0.747 0.833 0.825 0.720 0.979 0.483 0.692 0.981 0.901 0.778 0.630 0.829 0.638 1.212 0.715 ln(WW)–ln(SH) 2.673 7.764 0.822 2.554 7.485 0.898 1.784 4.526 0.522 3.613 11.60 0.943 3.086 9.640 0.974 2.663 8.148 0.889

Explanations:SH–shellheight(mm);SL–shelllength(mm);SW–shellwidth(mm);HL–hingelength(mm);Hpn–heightof nacreous part (mm); Lpn – width of nacreous part (mm); WW – wet weight (g).

Results Marsa (N3) showed lower average values of total height. They were distinguished by specimens whose size did Total SH average values of the examined samples not exceed 42 mm (Fig. 3). It is worth noting that the ranged between 33.57 ± 10.13 mm and 63.50 ± 16.09 maximum size (100.51 mm) recorded during the present mm. The majority of the analyzed P. radiata sub- study was recorded in N1 (Bizerta lagoon). Although populations were dominated by large individuals whose normality assumption of shell height (SH) data of the size were equal or exceeded 42 mm (Fig. 3). In con- whole sample was satisﬁed (Shapiro-Wilk test = 0.956; trast, the samples of Tunis north lagoon (N2) and La P < 0.001), some samples did not show a normal distri- Morphometry of Pinctada radiata along the Tunisian coasts 297

Fig. 4. Comparison of relative growth of the different measurements taken on Pinctada radiata individuals from six populations considering the shell height (SH) as a variable reference. For explanations see Table 1. bution, e.g., N1 and E1. In addition, a non-parametric variables were highly correlated (high R2 values) for procedure using Kruskal-Wallis test showed a signifi- all examined samples (Table 1). Significant differences cant difference between the examined samples (H = in the tested relationships between samples were found 151.364; P < 0.001). with analysis of covariance (ANCOVA, P < 0.0001), The parameters of allometric lines among ln(SL), although some overlaps in the plot area were observed ln(SW), ln(Hpn), ln(Lpn), ln(HL), ln(WW), and (Table 2). It is worth noting that for the majority of ln(SH), estimated at 95% confidence intervals, are tested relationships, the regression line of the sample shown in Table 1. The relationships between these vari- N1 was obtained separated from those of other sam- ables, except for ln(WW) and ln(SH), exhibited close ples. These latter showed always overlaps in the plot linear regressions, with exponent (b) 0.093–1.095 for area. The larger overlaps in the plot area was especially ln(SL) vs ln(SH), 0.106–2.624 for ln(SW) vs ln(SH), observed, between N2, N3, E1, E2 and E3, with the 0.023–0.264 for ln(Hpn) vs ln(SH), 0.220–0.347 for relationships ln(SL)–ln(SH), ln(SW)–ln(SH), ln(Hpn)– ln(Lpn) vs ln(SH) and 0.630–1.864 for ln(HL) vs ln(SH). ln(SH), ln(Lpn)–ln(SH), and ln(WW)–ln(SH) (Fig. 4). Exponents in allometric relationships for ln(WW) vs Factorial Discriminant Analysis (FDA) done based ln(SH) were comprised between 4.526 (N3) and 11.60 on the same data gave a better discrimination (Fig. 5). (E1) (Table 1). Morphological comparisons of relation- The first two axes explained 64% of the variability in ships between P. radiata samples are presented in Ta- the data (38% for axis 1 and 26% for axis 2). In spite ble 1 and Figure 4. of the overlap observed between the samples, it is pos- With the exception of the morphometric relation- sible to see that the sample E1 tend to be separated ship ln(HL)–ln(SH) within N3 (La Marsa), all tested from the rest of samples. High overlap was observed be- 298 S. Tlig-Zouari et al.

Table 2. Results of statistical analysis on log linear relationships of morphological characters between Pinctada radiata populations by ANCOVA.

Metric relationships df Sum of squares Average squares F Pr >F

ln(SL)–ln(SH) 12 4787.852 398.988 85700.378 < 0.0001 ln(SW)–ln(SH) 12 2563.676 213.640 17769.451 < 0.0001 ln(Hpn)–ln(SH) 12 4242.084 353.507 126450.372 < 0.0001 ln(Lpn)–ln(SH) 12 4080.250 340.021 67488.236 < 0.0001 ln(HL)–ln(SH) 12 4459.662 371.639 44492.364 < 0.0001 ln(WW)–ln(SH) 12 2101.650 175.138 3158.842 < 0.0001

For explanations see Table 1.

Fig. 5. Scatterplot of the first two FDA (Factorial Discriminant Analysis) axes of the log-transformed data of the six Pinctada radiata populations. tween the samples E2 and E3. N2 and N3 individuals were grouped separately in both sides of axis 1. In addition, FDA separated the six samples and a Student– Neuman–Keuls multiple-range test separated four ho- mogenous groups: E1, N2, N3 and E2+E3+N1. A better separation was obtained with the Ascending Hierar- chic Classification which showed two clusters. The first was represented by the Northern samples (N1, N2 and N3) with a separation of the population N1. As for the second cluster, it was formed by the Eastern samples (E1, E2 and E3) and it consisted of two sub-clusters, one represented by E1 and another by E2 + E3 (Fig. 6).

Discussion Fig. 6. Ascending Hierarchic Classification of the six Pinctada The size structure of the six P. radiata samples showed radiata populations. Morphometry of Pinctada radiata along the Tunisian coasts 299 that with the exception of the two sub-populations of that such variability could be in relation with individu- Tunis Gulf (N2 & N3) characterized by the dominance als’ size (SH) and the availability of food resources. The of small specimens (Ht ≤ 42 mm), the other samples latter authors also explained that within large-sized in- were dominated by large pearl oysters (Ht ≥ 42 mm) dividuals, the growth of SH is highly reduced but their (Fig. 3). Not similarly to the latter result, the study shells became wider. carried out about P. radiata sub-populations in the The comparison of the relationship SW-SH inves- Archipelago of Kerkennah (Gulf of Gabes, Southern tigated during this study with that of other species be- coast of Tunisia) showed that the majority of individu- longing to the same genus from different areas showed als had a size lower than 42 mm with individuals rang- that P. radiata in Monastir (E2) has a higher SW in- ing between 1 and 74 mm (Tlig-Zouari 1993). The lat- crease against SH than those of P. fucata (Gould, 1850), ter author explained this fact by a continuous recruit- P. margaritifera (L., 1758) and P. sugillata (Reeve, ment of the species in Kerkennah islands which is due 1857) in Taiwan (Hwang et al. 2007), Korea (Shimizu to a continuous reproduction activity along the year 1999) and Japan (Wada 1984). Furthermore, it is worth (Tlig-Zouari & Zaouali 1994). Size distribution analy- noting that the variable SW was also considered as the sis also showed that the majority of P. radiata samples most important morphological character in the aqua- were dominated by 2 or more size groups. Differences culture of other pearl oyster species; e.g., P. fucata, P. in size distribution might be due to various environ- margaritifera and P. sugillata since it greatly affects the mental factors, such as temporally and spatially vari- number and size of the inserted pearl nuclei (Hwang et able predation or exploitation or adverse environmental al. 2007). These differences could be in relation to en- episodes. Otherwise, similar observations were found in vironmental and therefore nutritional factors or to ge- the Archipelago of Kerkennah where P. radiata popu- netic ones as was reported for P. fucata populations in lations were reported to be dominated by four cohorts Japan (Wada 1984). However, because it has a thicker during most of the year; such an observation was ex- SW, the species P. radiata has great potential for use plained by an irregular seasonal growth and continuous as a supplementary edible resource and also as a nacre reproduction activity and recrutement of the species resource. (Tlig-Zouari & Zaouali 1994, 1995). Morphometric differences in relation to genetic fac- It is worth noting that the maximum size (100.5 tors have been reported with P. radiata (mentioned as mm), recorded in Bizerta lagoon (N1) is higher than P. imbricata and P. albina) in Australia (Colgan & Pon- that observed by Seurat (1929) (85 mm) in Gabes Gulf der 2002). Otherwise, the study of P. radiata (men- (south of Tunisia) and Tlig-Zouari (1993) in Kerkennah tioned as P. imbricata) populations of Japan (Wada islands (74 mm). This size is larger than that recorded 1975, 1982) and Bahrain (Beaumont & Khamdan 1991) by Yassien (1998) and Yassien et al. (2000), respec- showed the existence of morphometric variations. The tively, in the Red Sea (93.2 mm) and Eastern Mediter- latter authors have not excluded the hypothesis that ranean (64 mm). these morphometric differences may be also related to The comparison of relative growth features of P. environmental conditions, in particular the exposure to radiata showed differences between the studied samples. wave action, salinity and temperature. Moreover, the Larger differences were observed in the relationships temperature also affects the size of pearl oysters. In ln(SW)–ln(SH) (Fig. 4). This result indicated that SW, the Gulf of Mexico, for example, the size of oysters de- among the six characters examined (SH, HL, SL, SW, creases at low latitudes because the elevated tempera- Hpn, Lpn), greatly differs between samples, because ture reduces the allocation of energy to growth somatic larger overlaps in the plot area of the log-linear relation- (Klinck et al. 1992). Similar relative growth differences ships were observed by other combinations of characters have been mentioned among the stocks of P. margari- (ln(SL)–ln(SH), ln(Hpn)–ln(SH) and ln(Lpn)–ln(SH)). tifera in French Polynesia (Pouvreau & Prasil 2001). High correlation was also found between SW and SH According to these authors, such relative growth dif- within the sub-populations of Kerkennah Islands (Tlig- ferences are probably due to temperature, the renewal Zouari & Zaouali 1998). The latter authors also men- rate of water and food availability around the bivalves. tioned significant differences in this relationship be- The four sub-population assemblages, obtained tween the examined samples. Other large differences with FDA and CHA, almost matched with geographi- were observed with the relationship ln(SH)–ln(WW). cal separation of the six samples. This could be in re- These differences could be caused by WW, which dif- lation with environmental conditions which differ from fered from one sample to another due to the variabil- one sector to another. In fact, N1 is localized in Bizerta ity of environmental conditions and availability of food lagoon, N2 + N3 in Tunis Gulf, E1 in Hammamet Gulf resources. This study also revealed a variable relative and E2 + E3 in Monastir bay (Fig. 1). growth of SW between the different prospected locali- Summarising, the present study described the rel- ties and indicated that the pearl oysters of Hammamet ative growth of the alien species P. radiata in North- harbour (E1) and Stah Jaber (E3) have the widest SW ern and Eastern Tunisian coastline. Except for La than those recorded in the other sites. Similar variabil- Marsa sample (N3), all populations showed high cor- ity in length-weight relationships was previously ob- relations between the various combined variables, with served in the south Tunisian coastline by Tlig-Zouari some variability from one station to another. The (1993) and Tlig-Zouari & Zaouali (1994) who explained most significant differences between samples were es- 300 S. Tlig-Zouari et al. pecially obtained with the relationships ln(SW)–ln(SH) Schwartz D. 1963. Méthodes statistiques à l’usage des médecins et des biologistes. Troisième édition. Editions Médicales and ln(WW)–ln(SH). Multivariate analyses (FDA and ◦ ◦ CHA) enabled to classify the samples in four sub- Flammarion. Flammarion et Cie, éditeur (N 9005) – N d’impression: 18353, 318 pp. groups. Such differences might be due to the difference Seurat L.G. 1929. Observations sur les limites, les faciès et les in geographic locations. 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Received April 28, 2009 DOI 10.1016/S0990-7440(01)01120-2 Accepted August 28, 2009