Research Article

Occurence of Scoliosis, Pugheadness and Disappearance of Pelvic Fin in Three Marine Fish Species from Turkey  

Laith A. Jawad1 , Murat ÇELİK2 , Celal ATEŞ2
1 Flat Bush, Manukau, Auckland 2016, New Zealand
2 Muğla Sıtkı Koçman University, Faculty of Fisheries, 48000, Kötekli, Muğla, Turkey
Author    Correspondence author
International Journal of Marine Science, 2017, Vol. 7, No. 28   doi: 10.5376/ijms.2017.07.0028
Received: 12 Jul., 2017    Accepted: 28 Jul., 2017    Published: 03 Aug., 2017
© 2017 BioPublisher Publishing Platform
This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Preferred citation for this article:

Jawad L.A., ÇELİK M., and ATEŞ C., 2017, Occurrence of scoliosis, pugheadness and disappearance of pelvic fin in three marine fish species from Turkey, International Journal of Marine Science, 7(28): 275-283 (doi:  10.5376/ijms.2017.07.0028)


Skeletal deformities such as scoliosis, pugheadness and complete absence of pelvic fins have been described in three specimens of Mugil cephalus Linnaeus, 1758, Nemipterus randalli Russell, 1986 and Sparus aurata (Linnaeus, 1758). The cases of scoliosis were with 4 lateral bends, pugheadness with a significant absence of bones from the preorbital region of the fish skull and the complete absence of pelvic fins accompanied with absence of pelvic girdle.

Skeletal anomalies; Abnormalities; Environmental pollution; Vertebral column; Fins; Mediterranean Sea


Skeletal deformities are among the fundamental problems in the developmental phase of the fish life, which can influence morphology, growth and survival of the individuals. Skeletal abnormalities in wild fish populations are rarely observed either because they are less abundant or because of the decreased viability of the abnormal fish in their natural habitat (Gavaia et al., 2009; Bogutskaya et al., 2011; Jawad et al., 2015; 2016).


Scoliosis, i.e. the side curvature of the vertebral column, is one severe anomaly that affects this part of the fish skeleton. It is considered less common than lordosis (Boglione et al., 2013) and it can be found in pre-haemal and haemal positions (Boglione et al., 1995). Among the cases of vertebral anomalies, scoliosis is the most easily recognizable in live fish. To confirm such case, the fish needs to be looked at dorsal-ventrally (Boglione and Costa, 2011).


Hickey (1972) described pugheadness deformity as an abnormal osteological condition that results in the aberration of the maxilla, premaxilla, or infraorbital bones, with variable degrees of severity. The affected specimens often show bulging eyeballs, acutely steep foreheads, and incomplete mouth closure (Shariff et al., 1986). Pugheadness is infrequently observed in the wild, particularly in large estuarine systems (Catelani et al., 2017), but higher incidences of this case were revealed from more polluted waters (Slooff, 1982). Fish specimens with this type of anomaly can have their mouth partially closed (Jawad and Hosie, 2007; Branson and Turnbull, 2008), which can affect the feeding procedure and hindered growth rate (Shariff et al., 1986).


Aberration or absence of pelvic fins in teleost species has been previously documented and attributed to congenital or postnatal malformations (Papern, 1978; Alvarez-Leόn, 1980; Graham et al., 1986; Petriki and Bobori, 2014), as well as to chemical pollution (Slooff, 1982). The entire absence of this pair of fins raises questions on further acquired functional changes in body morphology as a consequence of environmental adaptation (Graham et al., 1986). Pelvic fins are generally considered as maneuvering structures. However, their hydrodynamic function has received little attention compared to the pectoral and median fins (Lauder and Drucker, 2004; Yamanoue et al., 2010).


The present study describes abnormalities that have either rarely or never been reported before in the three fish species studied. Scoliosis has been reported from specimens of Mugil cephalus collected from North California (Schwartz, 2000) and Mie Prefecture, Japan (Maeno et al., 2000), but not from the Mediterranean Sea. The threadfin bream, Nemipterus randalli is a fairly new resident in the eastern Mediterranean Sea and its presence was first reported by Golani and Sonin (2006), while its presence in Turkey were reported by Bilecenoglu and Russell (2008), Gokoglu et al. (2009) and Gulsahin and Kara (2013). Therefore, this the first ever case of abnormality to be reported for this species. Finally, the absence of pelvic fins in Sparus aurata is rare and the present record adds information to the marine fish anomalies data base.


The aim of the present study was to document the cases of scoliosis, pugheadness and absence of pelvic fins observed in M. cephalus, N. randalli and S. aurata.


1 Materials and Methods

Three specimens of the teleost fishes, M. cephalus (Mugilidae, Total length, TL: 291 mm, Standard length, SL: 261 mm), N. randalli (Nemipteridae, TL: 150 mm, SL: 130 mm) and S. aurata (Sparidae, TL: 224 mm, SL: 197 mm,) suffering different skeletal aberration were captured from the Turkish waters (during 1st October 2014 to 19th August 2015). Specifically, M. cephalus was caught in the protected nature reserve of Köyceğiz-Dalyan, while N. randalli and S. aurata were captured in Gökova Bay (Figure 1). The M. cephalus specimen was caught by set net and specimens of N. randalli and S. aurata by trammel net. Ten normal specimens of each species were obtained from the same fishing lot at the same fishing localities for comparison issues. Specimens’ body and fins were examined carefully for malformations, amputations and any other morphological anomalies.



Figure 1 Map showing sampling localities


For the case of scoliosis, the length of the vertebral column from the anterior margin of the first vertebra to the posterior margin of the last vertebra was divided by fish total length to produce a ratio that is used to compare abnormal with normal fish (Jawad et al., 2014). The angles formed at each side bend of the vertebral column were measured using digital protractor. To assess the degree of deformity in the distorted individuals, the height of the curvature of the spinal column (HC) was measured. This represents the depth of the curvature formed by the abnormal vertebrae. The measurements were made using a digital caliper with accuracy of 0.01 mm. The depth of curvature (DC) was calculated by the equation (Louiz et al., 2007):


DC = (HC / SL) × 100

where SL is the standard length of the fish.


To describe vertebral shape changes, the following five ratios from 7 vertebral measurements were calculated:


Length ratio = Dorsal length of the vertebra / Ventral length of vertebra for estimating wedging along vertebral length;

Width ratio = Anterior width of the vertebra / Posterior width of the vertebra for assessing wedging along the vertebral width;

Height ratio = Dorsal height of the vertebra / Ventral height of the vertebra for assessing the distortion of the amphicoelous shape;

Thickness ratio = Middle line width of the vertebra / Posterior width of the vertebra for estimating the mid-centrum thickness;

Slenderness ratio = Dorsal length of the vertebra / Posterior width of the vertebra for estimating the ventral slenderness


All measurements were made to the nearest mm.


All specimens were deposited in the fish collection of the Faculty of Fisheries, Muğla Sıtkı Koçman University, Turkey.


2 Results

2.1 Scoliosis

The deformed M. cephalus specimen (Figure 2Figure 3) showed a clear external sign of scoliosis, with the spine curved sideway at 3 places compared with the normal specimen (Figure 4). The fish body curved started from just anterior to the spinous dorsal fin and ended at the commencing line of the caudal peduncle. The radiograph (Figure 2B) showed that scoliosis deformity is clear even the x-ray was taken on the lateral side of the fish (Figure 3B). The radiography that revealed that there were 4 curvatures in the vertebral column, 2 curves to the right and 2 others to the left. The right curvature was the 1st from the head. The following vertebrae were involved in the 4 curvatures: 4th–7th abdominal vertebrae (1st curvature); 8th–11th abdominal vertebrae (2nd curvature); 9th–14th abdominal vertebrae (3rd curvature); and 15th abdominal–6th caudal vertebrae (4th curvature). The angles between the two lines passing through the sides of the curvature a, b, c and d were of 120°, 98°, 105° and 170 respectively. The depth of the curvatures (DC) a, b, c, and d were: 3, 4, 3.5 and 1.5 mm respectively.



Figure 2 Abnormal Mugil cephalus, 291 mm TL

Note: A: external morphology; B: radiograph showing the scoliosis case



Figure 3 Abnormal Mugil cephalus, 291 mm TL

Note: A: dorsal view; B: radiograph showing dorsal view of the scoliosis case



Figure 4 Normal specimen of Mugil cephalus, 291 mm TL


2.2 Pugheadness

The pug-headed N. randalli specimen (Figure 5A-C) had 150 mm Fork length (FL) and 130 mm SL, 4.2 mm preorbital length and 10.2 mm postorbital length. This specimen was compared to normal fish having 175 mm total length, 145 mm standard length, 5 mm preorbital length and 15 mm postorbital length.



Figure 5 Nemipterus randalli

Note: A: normal specimen 175 mm TL; B: abnormal specimen 150 mm TL, left side; C: abnormal specimen 150 mm TL, right side


The abnormal specimen had short skull and normal upper and lower jaws. The mouth was widely open when the fish was caught suggesting that the deformity has not affected the mechanism of opening and shutting the mouth. The snout shortening had brought the steep forehead close to the eye.


2.3 Absence of the pelvic fins

Externally, the deformed fish (Figure 6) showed complete absence of pelvic fins. The area where the pelvic fins should be present was very soft and there was no indication of presence of any internal bony materials. This suggests that the pelvic girdle supporting the pelvic fins was completely missing too.



Figure 6 Abnormal specimen of Sparus aurata, 224 mm TL showing complete absence of pelvic fins


3 Discussion

The present study reports skeletal deformities in three adult specimens of wild teleost fish species in the Turkish waters.


Skeletal deformities were documented for wild species of fish (Divananch et al., 1996; Jawad et al., 2013; Jawad and Liu, 2015) and were attributed to both genetic (Ishikawa, 1990) and epigenetic factors (Chatain, 1994; Fjelldal et al., 2009; Gavaia et al., 2009).


The specimen of M. cephalus suffering scoliosis faced an anterior-posterior (i.e. cranial-caudal) compression along the spine. Structural sign was present in the x-ray of the specimen showing that the normal amphicoelous (hour-glass) shape of vertebrae was distorted so that vertebral height was reduced on the convex and was greater on the concave side of curvature. In addition, vertebrae at the middle of the curvature were wedged so that the length on the concave side of the curve was reduced relative to the convex length. Also, the midline width was significantly reduced for some vertebrae. Similar changes were observed in Poecilia reticulata by Gorman et al. (2010), who attributed them to either (1) distortion of normal vertebral shape or (2) active remodeling of vertebral osteoid bone as a consequence of extrinsic forces. The formation of asymmetrical vertebrae demonstrates changes in growth rate along their growth plates, causing uneven progression in longitudinal growth and consequential shape distortion in the form of wedging (Mente et al., 1997).


Another evidence for the severity of the case of M. cephalus is provided from the depth of the 4 curvatures that represented by the DC factor calculated. Both B and C curvatures fall in the middle of the vertebral column were deeper than the other two curvatures a condition indicating the extreme extent of the curvature of the vertebral column at these points.


The present case of severe pugheadness anomaly in N. randalli is different from the other cases of pugheadness reported from wide range of fish species (AL-Hassan, 1988; Jawad and Hosie, 2007; Macieira and Joyeux, 2007; Francini-Filho and Amado-Filho, 2013; Jawad et al., 2014), the present case characterizes  in having normal both upper and lower jaw.


It is unknown whether the observed deformity in the specimen of N. randalli has reduced its survival potential; however, the pugheadness individual showed no obvious signs of poor health, so feeding was obviously unrestricted due the open mouth. Escaping from the predators was also not likely deterred by the observed abnormality, because the body of the deformed fish was robust.


Unlike the situation in the hatchery, the frequency of pugheadness deformity in wild fish populations is rare (Bortone, 1971; Riehl and Schmitt, 1984). This is probably due to the fact that the abnormal individuals in the hatcheries are sheltered and the predation factor is nil. Therefore, aberrant individuals may have a higher survival rate there and hence a higher frequency among hatchery-reared adults (Cobcroft et al., 2001). Other researchers suggested that such deformities are more frequent due to overcrowding (Shariff et al., 1986), xenobiotics (Haga et al., 2003), nutrition (Cobcroft et al., 2001), inbreeding (Sadler and King, 2001) and dietary deficiencies (Takeuchi et al., 1998).


The causes of the observed pugheadness anomaly in the specimen of N. randalli are unknown, but they probably arise during early development (Cobcroft et al., 2001). Genetic and epigenetic factors could cause pugheadness deformity (Dahlberg, 1970; Sloof, 1982). Exposure to contaminants such as cadmium, zinc, lead, mercury, or other contaminants, where the specimen caught (Davies and Everhart, 1973; Nakamura, 1974; Valentine, 1975) may affect the skeletal development. As a result, the concentration of the mobilized calcium will be reduced within the body and inhibit enzymes necessary for bone metabolism (Valentine, 1975; Yamashita and Hayashi, 1985; Ludwig et al., 1995).


Pelvic fins have a certain important role in fish movement; therefore it must be constructed so as to cope with hydrodynamic stresses with the least possible expenditure of energy (Boglione et al., 1993). Any anomaly in the pelvic fins will impair fish flexibility so hinder the performance of the fish.


The combination of genetic and environmental factors could cause a complete absence of the pelvic fins (Scheiner, 1993). It is clear that diversities in the genetic pool can determine variations in the developmental pattern.


Skeletal abnormalities observed in the present study can be induced during embryonic and postembryonic periods of life through a complicated mechanism (Koumoundouros et al., 1995; Cataudella et al., 1996). Establishment of both nutritional and abiotic parameters involved in the mechanisms leading to the appearance of these deformities must be determined in order to prevent a high incidence of malformations.


Authors’ contributions

All authors have contributed equally toward the publication of this paper.



Our sincere thanks are due to the Scientific and Technological Research Council of Turkey (TUBITAK) for funding this study (project number 213O263) and to Göksel Bayramli for the help in the x-ray.



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