ANNALES · Ser. hist. nat. · 21 · 2011 · 2 
161
Short scientific article                        UDK 591.159:597.556.221.1(262.26)
Received: 2011-10-03
MORPHOLOGICAL ABNORMALITIES IN THE ANNULAR SEA BREAM 
DIPLODUS ANNULARIS (OSTEICHTHYES: SPARIDAE) 
FROM THE LAGOON OF BIZERTE (NORTHEASTERN TUNISIA, 
CENTRAL MEDITERRANEAN)
Nour El Houda KHENFECH & Moncef BOUMAÏZA
Laboratoire d’Hydrobiologie Littorale et Limnique, Université du 07 novembre à Carthage, Faculté des Sciences, Zarzouna, 7021 
Bizerte, Tunisia
Christian REYNAUD & Christian CAPAPÉ
Laboratoire interdisciplinaire de Recherche sur la Didactique, l’Éducation et la Formation, E. A. 3749, case 77, Université Montpellier 
II, Sciences et Techniques du Languedoc, 34095 Montpellier cedex 5, France
E-mail: capape@univ-montp2.fr
ABSTRACT
Morphological abnormalities observed in annular sea bream Diplodus annularis (Linnaeus, 1758) collected in 
the Lagoon of Bizerte (northern Tunisia), such as abnormal body shape, skeletal deformities and a reduced anal fin 
are presented in this paper. The origins of these abnormalities are commented and discussed.
Key words: lateral line, vertebral column, hyperkyphosis, scale, environmental pollution
ANORMALITÀ MORFOLOGICHE IN SARAGO SPARAGLIONE DIPLODUS ANNULARIS 
(OSTEICHTHYES: SPARIDAE) DELLA LAGUNA DI BIZERTE (TUNISIA NORD-ORIENTALE, 
MEDITERRANEO CENTRALE)
SINTESI
Diverse anormalità morfologiche sono state osservate in esemplari di sarago sparaglione Diplodus annularis (Lin-
naeus, 1758), catturati nella Laguna di Bizerte (Tunisia settentrionale). Nell’articolo vengono presentate deformità 
scheletriche, forme corporee anormali e pinne anali ridotte. L’origine di tali anormalità morfologiche viene commen-
tata e discussa. 
Parole chiave: linea laterale, colonna vertebrale, ipercifosi, scaglie, inquinamento ambientale
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Nour El Houda KHENFECH et al.: MORPHOLOGICAL ABNORMALITIES IN THE ANNULAR SEA BREAM DIPLODUS ANNULARIS ..., 161–166
INTRODUCTION
According to Bradaï (2000), at least 21 sparid speci-
es, all economically important, are commonly collected 
all along the Tunisian coast (Fig. 1); some of them enter 
brackish areas, such as the Bahiret El Biban in the south 
and the Lagoon of Bizerte in the north, where they live 
and reproduce. Sustainable populations, established 
in the Lagoon of Bizerte (Fig. 2), are targeted by fisher-
men throughout the year. Sparid production of the area 
ranges between 2.8% and 7.7% of the total producti-
on of sparids for Tunisian waters with mean 4.8 ± 1.5% 
(Anonymous, 2008). During investigations conducted 
in the area since 2006, focusing primarily on elasmo-
branch species (El Kamel et al., 2009a, b), an annular 
sea bream exhibiting morphological deformities was 
captured. Comprehensive bibliographies of recorded 
abnormalities in teleost species did not report any case 
in Diplodus annularis (see Dawson, 1964, 1966, 1971; 
Dawson & Heal, 1971; Jawad & Hosie, 2007; Jawad et 
al., 2010). The aim of this note is therefore to describe 
an abnormal specimen and comment on similar abnor-
malities previously observed in teleost species. Additi-
onally, we try to explain the cause of such deformities 
in a specimen captured in a restricted area submitted to 
intense pollution. The role of pollution on fish species 
and consequently on fishery production could constitu-
te one of the most important pieces of information for 
improving fishery monitoring and management in the 
study area.
MATERIAL AND METHODS
On 15 August 2010, one annular sea bream pre-
senting an abnormal body shape was collected in the 
northern region of the Lagoon of Bizerte, off Menzel 
Abderrahman, (37°13’31.34’’ N, 9°50’28.79’’ E), with 
commercial gill-net, having 26 mm of mesh size, at a 
depth of 9 m approximately, on sandy-muddy bottom, 
with other annular sea breams (Fig. 2).
The fresh specimen was measured to the nearest mm 
and weighed to the nearest gram. Eviscerated mass, liver 
mass and gonad mass were also recorded, the stomach 
content was removed, sorted, weighed and prey items 
identified whenever possible. Morphometric measure-
ments and meristic counts followed Bauchot & Hureau 
(1986); they were recorded in the abnormal specimen 
and compared with those recorded in 3 normal speci-
mens (Tab. 1). Twelve scales were removed from the 
lateral line of the abnormal specimen and a normal 
Fig. 2: Map of the Lagoon of Bizerte, showing the cap-
ture site (black star) of the abnormal Diplodus annularis 
(FSB-Dip-ann. 01).
Sl. 2: Zemljevid Lagune Bizerte z označeno točko ulova 
(črna zvezda) abnormalnega primerka Diplodus annula-
ris (FSB-Dip-ann. 01).
Fig. 1: Map of the Mediterranean Sea showing the Tu-
nisian coast and map of Tunisia showing the location of 
the Lagoon of Bizerte.
Sl. 1: Zemljevid Sredozemskega morja s tunizijsko oba-
lo in zemljevid Tunizije z označeno Laguno Bizerte.
ANNALES · Ser. hist. nat. · 21 · 2011 · 2 
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Nour El Houda KHENFECH et al.: MORPHOLOGICAL ABNORMALITIES IN THE ANNULAR SEA BREAM DIPLODUS ANNULARIS ..., 161–166
specimen, and measured from the anterior edge to the 
posterior edge to the nearest 0.001 mm, by micrometric 
calliper under binocular microscope.
Some specimens used in this paper were preserved 
in 10% buffered formalin and deposited in the Ichthyo-
logical Collection of the Faculté des Sciences of Bizerte 
(Tunisia), receiving the catalogue numbers: FSB-Dip-
ann 01 for the abnormal specimen, and FSB-Dip-ann 
02, FSB-Dip-ann 03, FSB-Dip-ann 04, for the 3 normal 
specimens, respectively. To study the relationship total 
length (TL, in mm) vs. total mass (TM, in g), 21 speci-
mens were used including the abnormal specimen.
Reference FSB-Dip-ann01 FSB-Dip-ann 02 FSB-Dip-ann 03 FSB-Dip-ann04
Weight (g) 45.7 35.9 32.9 37.5
Morphometric counts mm % SL mm % SL mm % SL mm % SL
Total length 138 120.0 134 114.5 135 120.2 136 119.3
Standard length 115 100.0 117 100.0 113 100.0 114 100.0
Anal fin base 3 2.9 23 19.8 25 22.8 24 21.4
Body depth at anal fin origin 17 14.9 40 34.5 41 36.8 36 31.6
Width at anal fin origin 8 7.3 13 11.2 12 11.2 11 10.0
Maximum body width 15 13.3 14 12.4 13 12.2 12 10.6
Anal fin length 10 8.9 31 26.5 30 26.7 31 27.5
Caudal fin length 26 22.9 26 22.8 25 23.1 25 22.4
Caudal peduncle length 10 9.1 9 8.3 9 8.8 9 8.1
Caudal peduncle depth 4 3.3 3 3.2 3 3.2 3 3.1
Dorsal fin base 48 42.1 54 46.7 57 51.0 56 49.6
Cheek depth 11 9.7 11 9.5 10 9.3 9 8.4
Head length 30 26.3 30 25.9 30 27.2 31 27.2
Head width 17 15.6 14 12.4 14 12.8 13 11.7
Eye diameter 4 3.6 4 3.9 4 3.6 3 3.4
Interorbital width 8 7.1 7 6.7 7 6.8 8 7.4
Postorbital length 18 16.3 19 16.7 19 17.3 19 17.4
Pectoral fin length 34 30.3 38 33.2 37 33.3 38 34.1
Length of pelvic fin 24 21.2 23 20.3 22 20.2 25 22.4
Snout length 14 12.7 12 10.5 11 10.6 12 10.8
Distance from snout to anal fin origin 88 77.2 70 60.1 70 62.4 68 60.3
Distance from snout to anus 47 41.1 64 54.7 63 56.3 62 54.9
Distance from snout to dorsal fin origin 37 32.5 35 30.1 36 32.2 39 34.4
Distance from snout to pelvic fin origin 32 28.3 36 31.4 37 33.6 37 33.1
Distance from pelvic fin origin to anus 19 17.1 28 24.8 28 25.1 25 22.3
Body depth at pelvic fin origin 15 13.9 14 12.6 13 11.7 13 11.8
Meristic counts FSB-Dip-ann01 FSB-Dip-ann 02 FSB-Dip-ann 03 FSB-Dip-ann04
Dorsal fin rays XI + 11 XI + 11 XI + 11 XI + 11
Pectoral fin rays 11 12 11 12
Pelvic fin rays I + 5 I + 5 I + 5 I + 5
Anal fin rays 6 III + 11 III + 11 III + 11
Caudal fin rays 18 16 16 16
Scales in lateral line 54 46 46 45
Scales in transversal line 21 18 20 18
Tab. 1: Morphometric measurements and meristic counts recorded in the abnormal Diplodus annularis (FSB-Dip-
-ann. 01), and 3 normal D. annularis (FSB-Dip-ann. 02. 03 and 04).
Tab. 1: Morfometrični in meristični podatki za abnormalen primerek Diplodus annularis (FSB-Dip-ann. 01), in 3 
normalne primerke D. annularis (FSB-Dip-ann. 02. 03 in 04).
ANNALES · Ser. hist. nat. · 21 · 2011 · 2 
164
RESULTS AND DISCUSSION
The abnormal Diplodus annularis exhibited an irregu-
lar and sinuous lateral line (Fig. 3A, a), while in normal 
specimens it is regular and curved at pectoral fin level 
(Fig. 3A, b). The specimen was photographed with soft X-
rays in order to point out a potential correlation between 
lateral line and osteological malformations (Fig. 3B). The 
abnormal specimen presented hyperkyphosis, defined as 
an exaggerated curvature of the vertebral column at the 
thoracic region level (Fig. 3B, a), with vertebrae fused and 
apparently less developed than those observed in the nor-
mal specimen (Fig. 3B, b). The number of scales of the lat-
eral line, 54, was higher in the abnormal specimen than 
in 3 other normal ones, all having 46 scales. Such differ-
ence was probably due to the fact that the sinuous lat-
eral line was relatively longer in the abnormal specimen 
(Tab. 1). Additionally, scales of lateral line removed from 
each specimen were not morphologically different, but 
significantly smaller in the abnormal specimen (paired 
t-test, t = 4.31, df = 11, p = 0.007), and consequently 
more numerous (Fig. 3C, a, b). The anterior belly of the 
abnormal specimen was hyper developed as an effect of 
the deformed vertebral column, while the posterior re-
gion was strongly reduced, especially in the terminal part. 
The anal fin of the abnormal specimen was considerably 
reduced; it was smaller than that of the normal specimen, 
representing 8.9% SL in the former and 26.5-27.7% SL in 
the latter, respectively (Tab. 1). Additionally, the pterygi-
ophore supporting the anal fin lacked, no spinous ray was 
found; only 6 soft rays were counted in the anal fin of the 
abnormal specimen while all normal specimens had 11 
soft rays in the anal fin (Tab. 1, Fig. 3D).
Lateral line deformation and scale deformity were 
the result of irregular scalation, mechanical dysfunction 
in ontogeny, and probably environmental and genetic 
factors according to Jawad et al. (2006-2007). They 
could also be due to skeletal malformation, as observed 
in the present specimen having a hyperkyphosis; similar 
patterns were reported by Jardas & Homen (1977) in the 
whiting Merlangius merlangus (Linnaeus, 1758) and the 
bogue Boops boops (Linnaeus, 1758). Jardas & Homen 
(1977) added that such anomalies were not very rare 
in teleost species from the Adriatic, and suggested that 
parasitic infection could be also the cause of skeletal 
deformations.
Jawad et al. (2010) noted that anomaly in fins could 
hinder the performance of the specimen especially its 
capacity to get food and to avoid predators. In the case 
presented herein, the observed deformities did not af-
fect the life of the abnormal specimen which lived and 
developed in the wild as other normal specimens of the 
same size class, as shown by the relation between TL 
vs. TM plotted in Fig. 4, with TM = 0.267 TL + 0.579; 
r = 0.827. Similar patterns were observed by Al-Mamry 
et al. (2010) in silver pomfrets Pampus argenteus (Eu-
phrasen, 1788). In contrast, Matsuoaka (1987) and Bo-
glione et al. (2006) noted a lethal effect caused by severe 
skeletal deformities in teleost species living in natural 
conditions. Similar patterns concerning fin absence, re-
duction of fin, or abnormal fin were listed by Dawson 
(1964, 1966, 1971) and Dawson & Heal (1971). Biotic 
factors such as an attack of aquatic organisms cannot be 
totally excluded (Dulčić & Soldo, 2005), even if it did 
not concern the studied specimen.
Abnormalities in fish species occur during the early 
stages of development and could constitute an impor-
tant indicator on unfavourable environmental conditions 
and pollutants, induced stress in the wild (Sfakianakis et 
al., 2004). Heavy metals such as Cd, Pb, Zn and Cu are 
suspected to cause reduction or absence of fins (Sloof, 
Fig. 3: (A) Diplodus annularis, both specimens were 
caught in the lagoon of Bizerte, scale bar 25 mm; a 
- abnormal specimen (FSB-Dip-ann. 01); b - normal 
specimen (FSB-Dip-ann. 02). (B) X-Ray photograph of 
D. annularis, scale bar 20 mm; a - abnormal specimen 
(FSB-Dip-ann. 01) with arrow pointing out the hyper-
kyphosis of the vertebral column; b - normal specimen 
(FSB-Dip-ann. 02). (C) Scales of lateral line removed 
from D. annularis, scale bar 1 mm; a - abnormal speci-
men (FSB-Dip-ann. 01); b - normal specimen (FSB-Dip-
ann. 02). (D) Terminal region of the abnormal D. annu-
laris (FSB-Dip-ann. 01), arrow showing the reduced anal 
fin, scale bar 20 mm.
Sl. 3: (A) Diplodus annularis, oba primerka ulovljena v 
Laguni Bizerte, merilo 25 mm; a - abnormalen primerek 
(FSB-Dip-ann. 01); b - normalen primerek (FSB-Dip-
-ann. 02). (B) Rentgenski posnetek D. annularis, merilo 
20 mm; a - abnormalen primerek (FSB-Dip-ann. 01), 
puščica kaže na hiperkifozo hrbtenice; b - normalen 
primerek (FSB-Dip-ann. 02). (C) Luske s pobočnice D. 
annularis, merilo 1 mm; a - abnormalen primerek (FSB-
-Dip-ann. 01); b - normalen primerek (FSB-Dip-ann. 
02). (D) Zadnji del abnormalnega primerka D. annula-
ris (FSB-Dip-ann. 01), puščica kaže na zmanjšano pod-
repno plavut, merilo 20 mm.
Nour El Houda KHENFECH et al.: MORPHOLOGICAL ABNORMALITIES IN THE ANNULAR SEA BREAM DIPLODUS ANNULARIS ..., 161–166
ANNALES · Ser. hist. nat. · 21 · 2011 · 2 
165
1982), vitamin C deficiency has been associated with ca-
udal fin degeneration (Havler, 1972). Several cases of ab-
normalities were described in animal species collected in 
the Lagoon of Bizerte, a restricted brackish area polluted 
by both inorganic and organic nutriments and heavy me-
tals (Mzoughi et al., 2002). Such pollution could explain 
the specimens of Torpedo torpedo from the Lagoon of 
Bizerte presenting abnormalities (Ben Brahim & Capapé, 
1997; Ben Brahim et al., 1998; El Kamel et al., 2009b; 
Mnasri et al., 2010; El Kamel-Moutalibi et al., 2011). The 
common torpedo lives buried in sandy bottoms, where 
pollutants are accumulated. Louiz et al. (2007) noted that 
skeletal deformities observed in 3 gobiid species were 
significantly higher in the severely polluted areas. Ad-
ditionally, gastropods are collected in the area, such as 
the purple dye murex Bolinus brandaris (Linnaeus, 1758) 
and the banded dye murex Hexaplex trunculus (Linnaeus, 
1758). Both species, at present, exhibit the development 
of imposex in females, a phenomenon linked to the use of 
organic biocides, such as tributyltin, the consequence of 
environmental pollution (Abidli et al., 2008). The annular 
sea bream described in this note probably constitutes a 
new instance of abnormality induced by environmental 
pollution in the Lagoon of Bizerte.
MORFOLOŠKE NEPRAVILNOSTI PRI ŠPARU DIPLODUS ANNULARIS (OSTEICHTHYES: 
SPARIDAE) IZ LAGUNE BIZERTE (SEVEROVZHODNA TUNIZIJA, 
OSREDNJE SREDOZEMLJE)
Nour El Houda KHENFECH & Moncef BOUMAÏZA
Laboratoire d’Hydrobiologie Littorale et Limnique, Université du 07 novembre à Carthage, Faculté des Sciences, Zarzouna, 7021 
Bizerte, Tunisia
Christian REYNAUD & Christian CAPAPÉ
Laboratoire interdisciplinaire de Recherche sur la Didactique, l’Éducation et la Formation, E. A. 3749, case 77, Université Montpellier 
II, Sciences et Techniques du Languedoc, 34095 Montpellier cedex 5, France
E-mail: capape@univ-montp2.fr
POVZETEK
Članek obravnava morfološke nepravilnosti pri šparu Diplodus annularis (Linnaeus, 1758), ulovljenem v Laguni 
Bizerte (severna Tunizija), npr. nepravilno obliko telesa, deformacije skeleta in zmanjšano podrepno plavut, ter mož-
ne izvore teh nepravilnosti.
Ključne besede: pobočnica, hrbtenica, hiperkifoza, luska, okoljsko onesnaženje
Fig. 4: Relationship total length (TL) vs. total mass (TM) 
in 21 specimens of Diplodus annularis collected in the 
Lagoon of Bizerte.
Sl. 4: Razmerje celotna dolžina (TL) vs. celotna masa 
(TM) 21 primerkov Diplodus annularis, ulovljenih v La-
guni Bizerte.
Nour El Houda KHENFECH et al.: MORPHOLOGICAL ABNORMALITIES IN THE ANNULAR SEA BREAM DIPLODUS ANNULARIS ..., 161–166
ANNALES · Ser. hist. nat. · 21 · 2011 · 2 
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