In order to manage the different kinds of malformations in fishes, it is vital to have a thorough information about the normal skeletal structure of the fish. A large number of such studies are available for many species of fish (Bogutskaya, 1991; Kas’yanov et al., 2001; Kozhara, 2005; Bogutskaya and Iliadou, 2006).
Lordosis is among the common deformities in fishes (Boglione et al., 2009). It is one of the most severe deformities observed in fishes; it develops either at the pre-hemal vertebrae due to non-inflation of the swimbladder (Chatain and Dewavrin, 1989) or at the hemal vertebrae as a result of the intense water-current velocity facing larval stages rearing (Kihara et al., 2002). The severity of the case of lordosis ranges from slight axial modification to acute lordosis angles (Divanach et al., 1996) and, therefore, study of the effects of deformity on body shape is of primary importance for fisheries and hatcheries (Sfakianakis et al., 2004).
Kyphosis is usually exist in the pre-haemal and haemal positions while ankylosis is a result of the changes in vertebral bodies due to deformation. It can be a combination of compression and ankylosis (Berg et al., 2006; Witten et al., 2006). In the most difficult conditions, various groupings of these three anomalies occur (Afonso et al., 2009).
This study was designed to describe the morphology of a case of lordosis-kyphosis-ankylosis in the teleosts species Mullus barbatus collected from a wild population. This is the first report about this abnormality in this species from Turkey. However, the stages of skeletal deformations have not been fully determined.
1 Materials and Methods
On 1st July 2016 one specimen of M. barbatus showing a continuous case of lordosis-kyphosis-ankylosis and other minor anomalies. This specimen was caught by a bottom trawl (44 mm mesh size in cod-end) at depth of 60 m from Gerence Bay, off Çeşme, Izmir (38°25’ N - 26°16’ E). A normal specimen 130 mm total length was also obtained from the same fishing lot used for comparison (Figure 1; Figure 2). The specimens were fixed in 70% ethanol and included in the fish collection of the Ege University, Fisheries Faculty (ESFM-PIS/2016-08).
Figure 1 Mullus barbatus, abnormal specimen, 135 mm Total length
Figure 2 Mullus barbatus, normal specimen, 130 mm Total length
The skeleton of both normal and abnormal specimens were examined by x-ray. The length of the vertebrae were divided by the total lengths to obtain a proportional relationship value between spinal lengths and total lengths of fish with normal and unusual vertebrae. The angle of vertebral deformation was measured from the centre of the deformity. The height of the curvature of the spinal column (HC) is equal to the distance between the tangent to the apical vertebra and a straight line which passes to the base of the two vertebrae limiting the curvature. Digital caliper with accuracy of 0.01 mm was used in all measurements. The depth of curvature (DC) according to Louiz et al. (2007):
DC = (HC / SL) × 100 (SL = Standard Length)
The following five ratios from 7 vertebral measurements were calculated to aid the description of the vertebral column.
Length ratio = Dorsal length of the vertebra / Ventral length of vertebra
Width ratio = Anterior width of the vertebra / Posterior width of the vertebra
Height ratio = Dorsal height of the vertebra / Ventral height of the vertebra
Thickness ratio = Middle line width of the vertebra / Posterior width of the vertebra
The anomaly fish has the following body measurements: 135 mm total length; 115 mm forked length; 104 mm standard length; and 36 mm head length.
Morphologically, the fish body is distended ventrally in the area of the caudal peduncle starting from the posterior tip of the anal fin to the base of the caudal fin (Figure 1). The two skeletons of the normal and abnormal specimens were compared (Figure 3). Two flexions of the vertebral column were observed, one in the abdominal region and the other in the caudal region of the vertebral column.
Figure 3 Radiograph of Mullus barbatus; A, normal; B, abnormal
The uprising part of the arch is formed of the abdominal vertebrae 6-9 and the descending arm is formed of the caudal vertebrae 4-8. The caudal vertebrae 1-3 are on the top of the arch with curved centra. The anterior part of the centrum of the 1st caudal vertebra shown raise upward.
The ratio of the vertebral column to the total length of the deformed specimen is 0.5, while it is 0.9 in the normal specimen. The value of the angle “A1” is 92°. The depth of the curvature of angle “A1” is 10.4 mm. The value of the angle “A2” is 110° and the depth of the curvature of angle “A2” is 5.3 mm. The value of the angle “A3” is 103˚ and the depth of the curvature of angle “A3” is 8.3 mm.
The 9th abdominal vertebra and 2nd- 5th caudal vertebrae have showed an increased in their height on the ventral side (0.021 and 0.023-0.025, respectively) (Figure 3B) and reduced on the dorsal side (1.130 and 1.135-1.256, respectively). Abdominal vertebrae 5 and 6 are wedged (1.245-1.265) (have a reduced ventral length relative to their dorsal length). The 6th abdominal and caudal vertebrae have reduced midline widths (0.023 and 0.029). The caudal vertebrae 1-4 are wedged such that the dorsal length is reduced relative to the ventral and the amphicoelous centra of the 9th abdominal vertebra and caudal vertebrae 2-5 are distorted such that the height is increased on the dorsal side (0.002 and 0.002-0.003). Slenderness and thickness were less in abdominal vertebrae 7-9 (0.001-0.003) and in caudal vertebrae 4-10 (0.002-0.005) (Figure 3B).
The fish specimen also showed a deformed pre-operculum and operculum bones, where the surface of these two bone appeared to be heavily scratched. The last 3 lateral line scales appeared distorted. Due to the curvature caused by angle “A1” the dorsal profile of the body below the dorsal fin appeared slightly curved.
No other anomalies were observed on the body of the fish.
This is the first study investigating the lordosis-kyphosis-ankylosis deformities that are observed in the examined adult wild teleosts Mullus barbatus from the Turkish waters. Anomalies in wild fish species have been well documented (Jawad et al., 2013; Jawad and Liu, 2015), where the causes of different deformities have been presented. Such causes include both genetic (Ishikawa, 1990) and epigenetic factors (Fjelldal et al., 2009), as well as environmental factors (Gavaia et al., 2009).
Structural indication was presented in the x-ray taken for the specimen (Figure 3B) that the normal shape of vertebrae is distorted. In addition, vertebrae at the estimated apex of curvature (lordotic vertebrae) are impacted so that the length on the concave side of the curve is decreased relative to the convex length. For some of the vertebrae, the midline width is appeared to be significantly. Such changes were observed by Gorman et al. (2010). Jardas and Morovic (1975) reported scoliosis and kyphosis cases in M. barbatus from the Adriatic Sea. In the kyphosis case they reported, the vertebrae were not deformed as in the case given in the present study. Therefore, the fish in our study experienced a severe abnormality than those of Jardas and Morovic (1975).
Any deformity in the shape of the vertebrae, which include remodeling will have a direct impact on the swimming ability of the fish and its survival (Başaran et al., 2007), and there was a significant relationship between the lordosis severity and swimming performance in sea bass (Dicentrarchus labrax) at least in juveniles (Sfakianakis et al., 2006; Peruzzi et al., 2007).
The multi-cases of vertebral fusion observed in the present study can be explained as a result of the study of Ytteborg et al. (2012). It might be possible that the deformed specimen of M. barbatus has lived in an unfavourable environmental conditions that might cause this type of vertebral abnormality. The case of the deformation was not fatal since the deformed specimen was an adult, but it certainly affected the mobility in some way. Except for the distorted two dorsal fins, the other fins were found in apparently in perfect condition.
From the present study, it is clear that the fish teratology is very complex and cannot be attributed to a single factor but it would have been due to the effect of multiple factors such as pollution, salinity fluctuations, low level of dissolved oxygen, radiation etc.
It is obvious that any morphological anomalies in any fish specimen offered from sale I the fish market will pull away the buyers. Therefore, there will be a commercial impact on the fishermen that happened to have deformed samples. For such reason and to decrease the presence of the deformed specimens among the fish offered in the market for the sale, further efforts such as enhancements of administration of the fisheries industries should be made to discover the various etiological causes of the anomalies before further serious choices are made.
In conclusion, there is a good possibility for the anomalous cases of lordosis, kyphosis, and ankylosis to occur in one fish specimen and such specimen could survive these vertebral deformities and reaches to the adulthood. Since these types of vertebral column abnormalities have shown to be related to pollution in other fish species, further studies are needed to relate specific pollutants with the observed types of deformity.
All authors have contributed equally toward the publication of this paper.
The authors would like to thank Faculty of Fisheries, Ege University, 35440 Urla, Izmir, Turkey for using its facilities during this study.
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