Range Extension of Egyptian Sole Solea Aegyptiaca (Soleidae: Pleuronectiformes), in the Red Sea

Home , Egyptian sole, Pegusa, Solea (fish), Solea senegalensis

Range extension of Egyptian sole Solea aegyptiaca (Soleidae: Pleuronectiformes), in the Red Sea

Bruno Chanet* (1), Martine Desoutter-Meniger (1) & Sergey V. Bogorodsky (2)

RÉSUMÉ. - Extension géographique en mer Rouge de la sole égyptienne Solea aegyptiaca (Soleidae; Pleuronectiformes). Des captures récentes de soles égyptiennes, Solea aegyptiaca Chabanaud, 1927, dans le golfe de Suez confirment que cette espè- ce est anti-lessepsienne. Les migrations de téléostéens par le canal de Suez sont discutées. Key words. - Soleidae - Solea aegyptiaca - Red Sea - Anti-Lessep- sian migrant.

The Egyptian sole, Solea aegyptiaca Chabanaud, 1927, is one of the 16 soleid species (Soleidae, Pleuronectiformes) inhabit- ing the Mediterranean Sea (Desoutter-Meniger, 1997). It is often confused with the common sole, Solea solea (Linnaeus, 1758), its sympatric species in the Mediterranean Sea (Quignard et al., 1984, 1986). The differentiation between these species has been both assessed through molecular data studies (She et al., 1987b; Borsa and Quignard, 2001) and using morphological data (Vachon et al., 2008). The Egyptian sole represents an important and overexploited species in the Egyptian Mediterranean fisheries (Mehanna, 2007; Ahmed et al., 2010). S. aegyptiaca is present in Mediterranean Sea, from Tunisia, southern extremity of the Adriatic Sea to Egypt (Desoutter-Meniger, 1997; Vachon et al., 2008), but considered as less frequent along the southern shores of the Mediterranean Sea. A specimen of S. aegyptiaca (MNHN 1995-0899) was reported by Chabanaud (1930) to have been caught inland, in Lake Nass- er, southwest of Cairo, but the putative presence in this artificial lake needs to be confirmed. Tillier (1902) mentioned that in 1900, between 500 to 600 soles were sold during the summer at the mar- ket of Ismailia on the west bank of the Canal of Suez (Fig. 1). He identified them asSolea lascaris, a species currently placed in the genus Pegusa. Norman (1927) identified these soles asS. solea, but Chabanaud (1930) reviewed these specimens and recognized them as S. aegyptiaca. Despite the fact that these specimens have only been collected at Ismailia, about halfway between the Mediterra- nean and the Red Sea, he suggested that S. aegyptiaca crossed the Suez Canal to reach the Red Sea. This suggestion was repeated in the species lists of the Mediterranean and Red seas (see for instance Steinitz, 1967 mentioning Solea vulgaris, a junior synonym of Solea solea) without further reference to captured specimens or reliable field data. Egyptian sole and common sole were mentioned as sympatric species in the Suez Canal by She et al. (1987a), while Figure 1. - Egypt map showing the capture site (*) of the two Solea aegyp- Mosaad and El-Sayed (1991) studied the biology of Solea vulgar- tiaca in the Gulf of Suez (17 July 2009). is (= Solea solea) from the northwestern part of the Red Sea. We have been unable to find this work despite important bibliographic one of us (SB) collected two specimens of soles captured by local researches and the presence of this species in the Red Sea has not fishermen in the northwestern part of the Gulf of Suez. The objec- been yet documented or confirmed. Yet recently (17 July 2009), tive of this study paper is to document the identification of these

(1) Muséum national d’Histoire naturelle, Département systématique et évolution, UMR 7138, Équipe phylogénie, CP 30, 57 rue Cuvier, 75231 Paris c e d e x 05, France. [[email protected]] (2) station of Naturalists, Tulenina str., Omsk, Russia. [[email protected]] * Corresponding author [[email protected]]

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using a 3-digit formula (Chapleau, 1989). The first digit indicates the number of pterygiophores associated with the erisma (first mod- ified pterygiophore). The next digit indicates the number of pterygiophores inserted on the cranium. The last digit gives the number of pterygiophores inserted on the posterior side of the second vertebrae. The angle between ventral and dorsal branches of the urohyal was measured following Chabanaud (1929) and Desoutter-Meniger (1997).

Figure 2. - Solea aegyptiaca. Specimen MNHN 2010-0447, ocular side. RESULTS Scale bar: 10 mm. The collected specimens have been compared to the two soleid specimens and the resulting range extension of this Mediterranean species present in the Eastern Mediterranean Sea: Solea solea and species in the Red Sea. S. aegyptiaca. Table I indicates meristic and morphometric data for the examined specimens and data from the literature. All the specimens present the same pattern of supracranial Material and methods portion of the dorsal fin (0-1-(2-4)-(0-1), corresponding to pattern A defined by Chapleau (1989), and which is present in the The two Solea specimens collected in the Red Sea are regis- genus Solea. Moreover, the examination of the studied parameters tered in the MNHN collection under the references: MNHN 2010- (Tab. I) shows that the specimens collected in the Gulf of Suez 0446, Red sea, 1 ex., alcohol, SL: 232 mm; MNHN 2010-0447, 1 can be placed in precise species of the genus Solea. On the basis ex. alcohol, SL: 227 mm (Fig. 2). They have been compared with of the number of vertebrae (precaudal and caudal), the number of literature data and the following specimens: dorsal-fin rays (Tab. I), MNHN 2010-0446 and MNHN 2010-0447 Solea aegyptiaca Chabanaud, 1927: MNHN1902-0009, neotype desig- differ from the common sole and are Egyptian soles, Solea aegypti- nated by Vachon et al. (2008), Ismailia, Egypt, coll. Tillier, 1 ex., alcohol, aca. Nevertheless, the numbers of lateral line scales in the Red sea 213 mm SL; MNHN 1899-0135, Ismaïlia, Egypt, coll. Tillier, 1 ex., alco- specimens are out of the range identified by Vachon et al. (2008) hol, 236 mm SL; MNHN 1995-0899, Lac Nasser, coll. POM, 2 ex., alcohol, for S. aegyptiaca and may lead to consider these specimens as rep- 195-292 mm SL; MNHN 1958-0022, coast of Israel, Mediterranean Sea, 1 resentatives of S. solea (Tab. I). But the numbers of vertebrae are ex alcohol, 167 mm SL. quite unequivocal, while the number of lateral line scales is sub- Solea solea (Linnaeus, 1758): MNHN 2000-5638, Pertuis Breton, coast jected to losses and miscounts. We consider that this later character of Atlantic Ocean, coll. Lagardère, 1 ex, alcohol, 149 mm SL. is informative in a purely descriptive approach, but cannot be really Abbreviations of institutions follow Eschmeyer (1998). Char- useful to discriminate S. solea from S. aegyptiaca. These observa- acters used to identify the Solea species are from the species tions lead us to confirm the presence ofSolea aegyptiaca in the Red descriptions of Desoutter-Meniger (1997) and Vachon et al. (2008). Sea. Methods for meristics and morphometrics follow Hubbs and Lagler (1947) except for eye diameter, which was measured on the ventral eye. These characters are: standard length (SL), head length DISCUSSION (H), body depth (D), number of dorsal-, anal- and caudal-fin rays, number of pectoral-fin rays on both sides of the body, number of Solea aegyptiaca is a well-known Mediterranean species, and lateral line scales, number of precaudal and caudal vertebrae, angle its documented presence in the Red Sea (MNHN 2010-0446 and of the urohyal. All meristic features, except for scale counts and the MNHN 2010-0447) is an element to consider it as an anti-Lessep- number of pectoral-fin rays were observed and determined from sian species, i.e., a species which had a range extension from the radiographs. The supracranial portion of the dorsal fin was codified Mediterranean Sea to the Red Sea through the Suez Canal (Golani,

Table I. - Meristic features for the studied specimens. *: data from Vachon et al. (2008); +: data from Desoutter-Meniger (1997). Specimens collected Solea solea Solea aegyptiaca in the Gulf of Suez 2010-0446 2010-0447 2000-5638 Range* 1902-0009 Range* Number of dorsal fin rays 70 72 88 74-89 70 65-76 Number of anal fin rays 60 60 72 60-74 59 53-62 Number of caudal fin rays 20 20 20 17-20 20 17-20 Number of eyed side pectoral fin rays 7 8 8 7-9 9 7-10 Number of blind side pectoral fin rays b.s. 7 7 7 7 7 7 Number of lateral line scales (straight portion) 148 146 123 104-164 126 111-134 Number of precaudal vertebrae 9 9 10 10 9 9 Number of caudal vertebrae 33 33 39 36-41 33 32-34 SL/D 3.26 3.24 3.13 2.4-3.4 3.12 2.8-3.5 SL/H 5.64 5.00 4.96 4.2-5.8 5.21 4,2-5,6 Angle of the urohyal (°) 80 86 86 87* (55-94)+ 77 87* (70-90)+

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1998a, 1998b; Boudouresque, 1999, 2008). Even if Lessepsian AZZURRO E., GOLANI D., BUCCIARELLI G. & BERNADI G., and anti-Lessepsian migrants are not true migrants from a biologi- 2006. - Genetics of the early stages of invasion of Lessepsian cal perspective, as eels or salmons, but rather extensions of geo- rabbit fishSiganus luridus. J. Exp. Mar. Biol. Ecol., 333: 190- graphical distribution dues to species dispersion; this corroborates 201. the observations of Chabanaud (1930) and Steinitz (1967). This is BERNARDI G., GOLANI D. & AZZURRO E., 2010. - The genet- the first confirmed mention of flatfish species that have expanded ics of Lessepsian bioinvasions. In: Fish Invasions of the Medi- their range from the Mediterranean Sea to the Red Sea as a result of terranean Sea: Change and Renewal (Golani D. & Appelbaum- the construction of the Suez Canal. Por (1978) and Boudouresque Golani B., eds), pp. 71-84. Sofia-Moscow: Pensoft Publishers. (1999, 2008) indicate that range extension of animals and plants in BILECENOGLU M., YOKEŞ M.B. & ERYIGIT A., 2008. - First the Mediterranean Sea (referred to as Lessepsian species) are more record of Vanderhorstia mertensi Klausewitz, 1974 (Pisces, numerous than range extension from the Mediterranean (referred Gobiidae) in the Mediterranean. Aquat. Inv., 3: 487-490. as anti-Lessepian species). Galil (2009) and Bernardi et al. (2010) indicated the presence of 300 Lessepsian species of metazoans, BONHOMME F., BARANES A., GOLANI D. & HARMELIN- including 85 fish species (Bilecenoglu et al., 2008; Lipej et al., VIVIEN M., 2003. - Lack of mitochondrial differentiation between rabbit fish, Siganus rivulatus (Perciformes: Sigani- 2008) in the Red Sea and 10 were anti-Lessepsian species in the dae). Sci. Mar., 67(2): 215-217. Mediterranean Sea, such as Muraena helena (Randall and Golani, 1995) Serranus cabrilla, Dicentrarchus labrax and D. punctatus BORSA P. & QUIGNARD J.P., 2001. - Systematics of the Atlantic- (Dor, 1984). The reasons of such an asymmetric species movements Mediterranean soles Pegusa impar, Pegusa lascaris, Solea have been discussed by Boudouresque (1999). They can be placed aegyptiaca, S. senegalensis, and S. solea (Pleuronectiformes: in two broad categories: hydrogeological and biological. From Soleidae). Can. J. Zool., 79: 2297-2302. a hydrological perspective, the level of the Red Sea is 30-40 cm BOUDOURESQUE C.F., 1999. - The Red Sea-Mediterranean link: (average level) higher than the Mediterranean Sea (Tillier, 1902; Unwanted effects of canals. In: Invasive Species and Biodiver- Boudouresque, 1999). Consequently, the water tends to flow north- sity Management (Sandlund O.T., Schei P.J. & Viken A., eds), ward, at least 8 months a year, from November to the end of July pp. 213-228. Dordrecht: Kluwer Academic Publishers. (Tillier, 1902; Morcos, 1967; 1980; Boudouresque, 1999, 2008). BOUDOURESQUE C.F., 2008. - Les Espèces introduites et invasi- This northward flow would have facilitated the migration of Red ves en Milieu marin. 3e édit., 201 p. Marseille: GIS Posidonie Sea species into the Mediterranean. In addition, the high salinity publ. (45 ppt) of the Red Sea is an effective barrier for Mediterranean species that live in a less saline environment (39 ppt) (Tillier, 1902). CHABANAUD P., 1929. - Observations sur la taxonomie, la mor- phologie et la binomie des Soléidés du genre Pegusa. Bull. Inst. From a biological perspective, species diversity is much higher in Oceanogr. Monaco, 7(6): 215-261. the Red Sea than in the eastern Mediterranean Sea (Golani, 1998a, 1998b; Boudouresque, 1999). As a consequence, these two authors CHABANAUD P., 1930. - Sur la répartition géographique de suggested that there are very few ecological niches vacant in Red divers poissons de la famille des Soléidés. Bull. Soc. Zool. Fr., Sea and that the opening of Suez Canal in 1869 has been and still 55: 222-224. is a gateway for Red Sea species to colonize the more depauperate CHAPLEAU F., 1989. - Étude de la portion supracrânienne de la ecosystems of the eastern part of the Mediterranean Sea. Neverthe- nageoire dorsale chez les Soleidae (Téléostéens, Pleuronecti- less, these statements remain highly speculative and are difficult to formes). Cybium, 13(3): 271-279. verify. DESOUTTER-MENIGER M., 1997. - Révision systématique des The details of the processes of the geographical extension of genres de la famille des Soleidae présents sur les côtes de l’Est anti-Lessepsian teleost species have not been yet studied in detail, Atlantique et de la Méditerranée. Thèse de doctorat, 182 p. as it has been for few Lessepsian fish species. Using molecular Muséum national d’Histoire naturelle, Paris. analyses, Hassan et al. (2003) on Upeneus moluccensis, Bonhom- me et al. (2003) and Azzurro et al. (2006) on Siganus rivulatus pro- DOR M., 1984. - CLOFRES, Checklist of the Fishes of the Red Sea. 437 p. Tel Aviv: Israel Academy of Sciences and Humani- vided information about the dynamics of these range extensions. ties. We hope that similar studies could be performed on S. aegyptiaca and other anti-Lessepsian species for a better understanding of the ESCHMEYER W.N., 1998. - Catalog of Fishes (with update 2011 dynamics of their southern range extension as a consequence of the online version www.calacademy.org). Cent. Biodiv. Res. Inf. construction of the Suez Canal. Calif. Acad. Sci., Spec. Publ. n° 1, 3 vol., 2905 p. San Francis- co: California Academy of Sciences. 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