ANNALES · Ser. hist. nat. · 29 · 2019 · 2 211 received: 2019-09-16 DOI 10.19233/ASHN.2019.21 MORPHOLOGICAL DEFORMITIES IN A STRIPED SEA BREAM LITHOGNATHUS MORMYRUS (OSTEICHTHYES: SPARIDAE) FROM NORTHERN TUNISIAN WATERS (CENTRAL MEDITERRANEAN SEA) Sihem RAFRAFI-NOUIRA Université de Carthage, Unité de Recherches Exploitation des Milieux aquatiques, Institut Supérieur de Pêche et d’Aquaculture de Bizerte, BP 15, 7080 Menzel Jemil, Tunisia Christian REYNAUD & Christian CAPAPÉ Laboratoire d’Ichtyologie, case 104, Université de Montpellier, 34 095 Montpellier cedex 5, France e-mail: capape@univ-montp2.fr ABSTRACT Abnormalities of the lateral line and the vertebral column are described in a specimen of striped sea bream Lithognathus mormyrus (Linnaeus, 1758) collected from the northern coast of Tunisia. Despite these deformities, the specimen was able to live in the wild together with normal specimens. The origin of these abnormalities are commented and discussed. Key words: Lithognathus mormyrus, hyperkyphosis, lordosis, environmental pollution, length-weight relationship DEFORMAZIONI MORFOLOGICHE IN UNA MORMORA, LITHOGNATHUS MORMYRUS (OSTEICHTHYES: SPARIDAE), IN ACQUE DELLA TUNISIA SETTENTRIONALE (MEDITERRANEO CENTRALE) SINTESI L’articolo riporta anomalie della linea laterale e della colonna vertebrale in un esemplare di mormora, Lithognathus mormyrus (Linnaeus, 1758), proveniente dalle acque al largo della costa settentrionale della Tunisia. Nonostante queste deformità, l’esemplare è stato in grado di vivere allo stato libero insieme ad individui normali. Gli autori commentano e discutono l’origine di queste anomalie. Parole chiave: Lithognathus mormyrus, ipercifosi, lordosi, inquinamento ambientale, relazione lunghezza-peso ANNALES · Ser. hist. nat. · 29 · 2019 · 2 212 Sihem RAFRAFI-NOUIRA et al.: MORPHOLOGICAL DEFORMITIES IN A STRIPED SEA BREAM LITHOGNATHUS MORMYRUS ..., 211–218 INTRODUCTION The striped sea bream Lithognathus mormyrus (Lin- naeus, 1758) is a sparid species inhabiting shallow coastal waters of the eastern Atlantic from the Bay of Biscay to South Africa, and from the south-western areas of the Indian Ocean to the Red Sea (Bauchot & Hureau, 1986). L. mormyrus occurs throughout the Mediter- ranean Sea, where it is abundantly captured by anglers for local consumption especially in the Strait of Sicily (Vitale et al., 2011). Additionally, the species has been recently found in the Black Sea (Aydin, 2018). It lives on sandy and rocky bottoms partially covered by seagrass and algae, to a maximum depth of 80 m (Bauchot & Hureau, 1986), and feeds on crustaceans, small teleosts and molluscs (Chessa et al., 2005). L. mormyrus is one of the 21 sparid species, all hav- ing economic importance, that are commonly caught throughout the Tunisian coast. Populations of this spe- cies can also be found in brackish areas, such as Bahiret el Bibane, in the southern region, and the Lagoon of Bizerte, in the northern region, where they live and reproduce (Hammami et al., 2013). Additionally, the species is rather abundant in southern Tunisia, where it is targeted by fishermen, as its flesh is appreciated by the local population (Bradaï, 2000). During investigations conducted in the northern Tunisian area since 2006, focusing primarily on elasmobranch species (El Kamel et al., 2009a, b) and then on all fish species (Rafrafi-Nouira, 2016), several L. mormyrus have been collected, among them a specimen displaying morphological deformi- ties. Comprehensive published scientific references of recorded abnormalities in teleost species do not report any case in L. mormyrus (see Dawson, 1964, 1966, 1971; Dawson & Heal 1971; Jawad & Hosie, 2007; Jawad et al., 2010; Jawad & Ibrahim, 2018). The aim of this note is to describe this abnormal specimen and comment on similar abnormalities previously observed in teleost species. MATERIAL AND METHODS A total of 32 specimens of L. mormyrus were col- lected during years 2013 and 2014, off Ras Jebel, located on the northern Tunisian coast, among them a specimen found on 23 June 2014 presenting abnormalities on the body. All specimens were caught by commercial gillnet with a stretched mesh size of 26 mm, at 37° 14’ 57.53” N and 10°11’ 52. 85” E, on sandy bottom, together with other sparid and labrid species (Fig. 1). The fresh specimens were measured for total length (TL) recorded to the nearest centimetre and weighed for total body weight (TBW) to the nearest gram. Mor- phometric measurements and meristic counts followed Bauchot & Hureau (1986) and Aydin (2018); they were recorded in the abnormal specimen and compared with those recorded in 2 of the normal specimens (see Tab. 1). The 3 specimens were fixed in 10% buffered forma- lin, preserved in 75 % formaldehyde and deposited in the Ichthyological Collection of the Institut Superieur de Pêche et d’Aquaculture de Bizerte (Tunisia), under catalogue numbers ISPAB-Lith mor 01 for the abnormal specimen, and ISPAB-Lith mor 02 ISPAB-Lith mor 03, for the 2 normal specimens, respectively. The abnormali- ties of the vertebral column, such as scoliosis (lateral curvature), lordosis (ventral curvature), kyphosis (dorsal curvature) and ankylosis (fusion of vertebrae), reported in many species, cultured and from the wild, were de- scribed following the Elie & Girard (2014) and Jawad & Ibrahim (2018) definitions. Additionally, three regions were taken into consideration, partially following Louiz et al. (2007): the anterior or cephalic region, the inter- mediate or abdominal region and the terminal or caudal region. A t-test was performed to point out the differences in the number of line scales and vertebrae between the abnormal L. mormyrus and the normal specimens. The relation between the total length (TL) and the total body weight (TBW) was used as a complement following Froese et al. (2011), including all specimens, normal and Fig. 1: Map of Tunisia indicating the capture area (rec- tangle) of Lithognathus mormyrus from the northern Tu- nisian coast. GT, Gulf of Tunis; GH, Gulf of Hammamet; GG, Gulf of Gabès. Sl. 1: Zemljevid Tunizije z označenim predelom (pra- vokotnik), kjer je bil ujet primerek ovčice na severni obali. Legenda: GT, Tuniški zaliv; GH, Hamameški zaliv; GG, Gabeški zaliv. ANNALES · Ser. hist. nat. · 29 · 2019 · 2 213 Sihem RAFRAFI-NOUIRA et al.: MORPHOLOGICAL DEFORMITIES IN A STRIPED SEA BREAM LITHOGNATHUS MORMYRUS ..., 211–218 abnormal, to show if this latter was able to develop in the wild like other normal specimens. This LWR is TBW = aTLb, and was converted into its linear regression, ex- pressed in decimal logarithmic coordinates, correlations were assessed by least-squares regression as log TBW = log a + b log TL. The significance of constant b differ- ences was assessed to the hypothesis of isometric growth if b = 3, positive allometry if b > 3, negative isometry if b < 3 (Pauly, 1983). These two latter tests were performed by using the logistic model STAT VIEW 5.0. Tab. 1: Morphometric measurements in millimeters (mm), with percentages of standard length (% SL), meristic counts and total body weight in grams (g), recorded in an abnormal and 2 normal specimens of Lithognathus mormyrus from northern Tunisian waters. Tab. 1: Morfometrične meritve v milimetrih (mm), z odstotki standardne dolžine (% SL), merističnim štetjem in skupno telesno maso v gramih (g), zabeležene v neobičajnem in dveh normalnih primerkih vrste Lithogna- thus mormyrus iz severno tunizijskih voda. References ISPAB-Lit-mor01 ISPAB-Lit-mor02 ISPAB-Lit-mor03 Condition Abnormal Normal Normal Morphometric measurements mm %SL mm %SL mm %SL Total length 168 124.4 160 125.0 163 125.4 Fork length 149 110.4 142 110.9 144 110.4 Standard length 135 100.0 128 100.0 130 100.0 Head length 47 35.1 44 34.3 43 33.1 Eye diameter 10 7.5 11 8.3 10 7.7 Pre-orbitary length 20 14.7 19 14.5 17 13.2 Post-orbitary length 19 13.7 17 13.6 17 13.4 Dorsal fin length 68 50.5 61 47.6 61 47.2 Pectoral fin length 8 5.9 6 4.6 7 5.3 Pelvic fin length 11 8.2 9 6.9 9 7.0 Anal fin length 29 21.4 23 18.1 22 17.2 Caudal fin length 15 11.3 14 11.3 14 10.5 Snout length 18 13.2 18 13.7 17 12.8 Body height 53 39.5 40 31.1 40 31.0 Pre-dorsal fin length 56 41.8 53 41.2 53 41.0 Pre-pectoral fin length 47 34.7 43 33.4 43 33.2 Pre-pelvic fin length 51 37.4 51 39.5 49 37.8 Pre-anal fin length 89 65.8 87 67.9 88 67.9 Length of the largest spine of the pectoral fin 34 25.3 30 23.5 30 23.4 Thickness 23 17.2 19 14.7 19 14.9 Meristic counts Lateral line scales 68 60 60 Total number of vertebrae 27 24 24 Dorsal fin rays XI+12 XI+12 XIII+10 Pectoral fin rays 14 13 13 Pelvic fin rays II+10 II+10 II+10 Anal fin rays III+10 III+10 III+10 Caudal fin rays 19 20 20 Total body weight (g) 68.6 48.3 48.4 ANNALES · Ser. hist. nat. · 29 · 2019 · 2 214 Sihem RAFRAFI-NOUIRA et al.: MORPHOLOGICAL DEFORMITIES IN A STRIPED SEA BREAM LITHOGNATHUS MORMYRUS ..., 211–218 RESULTS AND DISCUSSION All collected specimens were identified as L. mormyrus following the combination of main morpho- logical characters from Bauchot & Hureau (1986) and Engin et al. (2015), such as: body elongated, ovoid and compressed, snout elongate and pointed, posterior nos- tril an oblique slit, in front the of eyes, scales on check and opercle, preopercle broad, scaleless, livery with a fundamental silver-grey colouration, more or less dark, broken by a dozen of blackish or grey vertical lines. The abnormal specimen exhibited an upper margin devel- oped and arched, forming a hump, and the upper profile of the head was strongly curved, the lateral obviously sinuous, while it was only slightly curved in the normal specimens, mainly in the caudal region (Fig. 2). On an X-ray photograph, the abnormal specimen appeared to display three visible deformities. At the level of cephalic and caudal regions, the vertebral col- umn was strongly arched, forming hyperkyphosis. The abdominal region displayed lordosis with a somewhat smaller arch than the other two deformities (Fig. 3). No scoliosis was observed in the abnormal specimen. The number of lateral line scales in the abnormal specimen was 68, significantly outnumbering those of the normal specimens, 60 (t-test = 16, df = 1, p = 0.03). Following Bauchot & Hureau (1986) the normal range is from 59 to 65. Similarly, the number of vertebrae in the abnormal specimen, 27, significantly outnumbered those of the normal specimens, 24, (t-test = 17, df = 1, p = 0.03). Such increased numbers are probably due to the curves of the lateral line and the deformities of the vertebral column. This also means that the vertebrae were not fused and the specimen did not display any signs of ankylosis. Lateral line deformation is the main consequence of vertebral column malformation, as observed in the present specimen exhibiting hyperkyphosis. Similar pat- terns were reported by Jardas & Homen (1977) in the whiting Merlangius merlangus (Linnaeus, 1758) and the bogue Boops boops (Linnaeus, 1758). The same authors considered such anomalies not to be that rare in teleost species from the Adriatic, and suggested that parasitic in- fection could also be the cause of skeletal deformations. Jawad et al. (2010) noted that anomaly in fins could hinder the performance of the specimen, especially af- fecting its capacity to obtain food and avoid predators. In the case presented herein, the deformities observed did not affect the life of the abnormal specimen in the wild, it functioned as well as other normal specimens from the same size class, as shown by the relation between total length versus total body weight (TM, in g) plotted in Fig. 4, with: log TBW = 3.150 * log TL +5.161; r = 0.973, n = 32, displaying a positive allometry. Similar patterns were observed by Khenfech et al. (2011) in the annular sea bream Diplodus annularis (Linnaeus, 1758). Conversely, Matsuoaka (1987) and Boglione et al. (2006) noted a Fig. 2: Lithognathus mormyrus specimens from the northern Tunisian coast. A: Abnormal specimen. B: Normal specimen, scale bar = 40 mm. Sl. 2: Primerki ovčice iz severne tunizijske obale. A: Deformirani primerek. B: normalni primerek, merilo = 40 mm. Fig. 3: An X-ray photograph of Lithognathus mormyrus from the northern Tunisian coast. A: Abnormal speci- men. B: Normal specimen, scale bar = 30 mm. Sl. 3: Rentgenski posnetek ovčice iz severne tunizijske obale. A: Deformirani primerek. B: Normalni primerek, merilo = 30 mm. ANNALES · Ser. hist. nat. · 29 · 2019 · 2 215 Sihem RAFRAFI-NOUIRA et al.: MORPHOLOGICAL DEFORMITIES IN A STRIPED SEA BREAM LITHOGNATHUS MORMYRUS ..., 211–218 lethal effect caused by severe skeletal deformities in teleost species living in natural conditions. Abnormalities in fish species occur during the early stages of development and could have a genetic origin. A mechanical origin cannot be totally ruled out either. For instance, when specimens entangled in gillnets successfully escape, they can suffer morphological deformations and distortions of the normal vertebral shape, essentially a remodelling of the vertebral col- umn, as a consequence of extrinsic forces (Jawad & Ibrahim, 2018). On the other hand, these deformities could constitute an important indicator of adverse en- vironmental conditions and pollutants, and stress in the wild induced in other ways (Sfakianakis et al., 2004). Several cases of abnormalities were described among the animal species collected in the Lagoon of Bizerte, a restricted brackish area polluted by both inorganic and organic nutriments and heavy metals (Mzoughi et al., 2002). The global warming of marine waters in the various seas throughout the world could also play a role in skeletal deformities (Jawad & Ibrahim, 2018). The entire Mediterranean has been facing this major problem for several decades (Francour et al., 1994), including the Tunisian coast with the spread of alien species incom- ing from the Red Sea through the Suez Canal and/or from the eastern tropical Atlantic through the Strait of Gibraltar (Ounifi-Ben Amor et al., 2016). The northern coast of Tunisia is progressively invaded by such species and cases of abnormalities in fish are more frequent than previously recorded in the area (Rafrafi-Nouira, 2016). However, thorough investigations are needed and should be conducted together with environmental monitoring to locally delineate the role of temperature in deformities among fish species. Fig. 4: The relation between total length (TL) and total body weight (TBM) in specimens of Lithognathus mor- myrus from the northern Tunisian coast. Sl. 4: Odnos med totalno dolžino telesa (TL) in tel- esno težo (TBM) pri primerkih ovčice iz severne obale Tunizije. ANNALES · Ser. hist. nat. · 29 · 2019 · 2 216 Sihem RAFRAFI-NOUIRA et al.: MORPHOLOGICAL DEFORMITIES IN A STRIPED SEA BREAM LITHOGNATHUS MORMYRUS ..., 211–218 MORFIOLOŠKE DEFORMACIJE PRI OVČICI LITHOGNATHUS MORMYRUS (OSTEICHTHYES: SPARIDAE) IZ SEVERNO TUNIZIJSKIH VOD (OSREDNJE SREDOZEMSKO MORJE) Sihem RAFRAFI-NOUIRA Université de Carthage, Unité de Recherches Exploitation des Milieux aquatiques, Institut Supérieur de Pêche et d’Aquaculture de Bizerte, BP 15, 7080 Menzel Jemil, Tunisia Christian REYNAUD & Christian CAPAPÉ Laboratoire d’Ichtyologie, case 104, Université de Montpellier, 34 095 Montpellier cedex 5, France e-mail: capape@univ-montp2.fr POVZETEK Avtorji opisujejo anomalije v pobočnici in na hrbtenici, opažene na primerku ovčice Lithognathus mormyrus (Linnaeus, 1758), ujete ob severni obali Tunizije. Kljub tem deformacijam je primerek uspel živeti v naravi skupaj z drugimi, normalnimi primerki. Avtorji nadalje razpravljajo o izvoru teh anomalij. 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