Turkish Journal of Fisheries and Aquatic Sciences 11: 315-321 (2011)
www.trjfas.org
ISSN 1303-2712
DOI: 10.4194/trjfas.2011.0216
Systematic Status of Nine Mullet Species (Mugilidae) in the Mediterranean
Sea
Cemal Turan1,*, Mevlüt Gürlek1, Deniz Ergüden1, Deniz Yağlıoğlu1, Bayram Öztürk2
1
2
Mustafa Kemal University, Faculty of Fisheries, TR-31200, Iskenderun-Hatay, Turkey.
Istanbul University, Faculty of Fisheries, 34320, Avcilar, Istanbul, Turkey.
* Corresponding Author: Tel.: +90.326 6141877; Fax: +90.326 6141693;
E-mail: cturan@mku.edu.tr
Received 25 August 2009
Accepted 05 January 2011
Abstract
Systematic relationships among four genera and nine species (Mugil cephalus Linnaeus, 1758, Mugil soiuy Basilewsky,
1855, Liza ramada (Risso, 1827), Liza aurata (Risso, 1810), Liza abu (Heckel, 1843), Liza saliens (Risso, 1810), Liza
carinata (Valenciennes, 1836), Chelon labrosus (Risso, 1827), Oedalechilus labeo (Cuvier, 1829)) of the Mugilidae family
living in the Mediterranean Sea were investigated using morphological characters. Moreover the systematic relationship of M.
soiuy and L. abu among other mullet species was investigated in the present study for the first time. Hierarchical cluster
analyses of morphometric data were not concordant with the meristic data. Meristic characters in the present study were more
discriminative than morphometric characters in terms of taxonomic classification of the mullets. According to meristic data in
UPGMA tree, all nine species were grouped in two main branching. In the first branch, C. labrosus and O. labeo were
clustered as closest taxa, and being the sister group to the L. aurata. The other four Liza species produced two sub-branching
in this group; L. carinata was branched with L. saliens, which is neighbour to L. ramada. In the second branch two species,
M. soiuy and L. abu were clustered together and highly isolated from others. M cephalus was clustered as a most differentiated
species from all other Mugil species.
Keywords: Mugilidae, morphology, morphological characters, truss network system.
Akdenizde Bulunan Dokuz Barbun Türünün (Mugilidae) Sistematik Durumu
Özet
Akdeniz’de yaşayan Mugilidae familyasına ait dört cins ve dokuz kefal türü (Mugil cephalus Linnaeus, 1758, Mugil
soiuy Basilewsky, 1855, Liza ramada (Risso, 1827), Liza aurata (Risso, 1810), Liza abu (Heckel, 1843), Liza saliens (Risso,
1810), Liza carinata (Valenciennes, 1836), Chelon labrosus (Risso, 1827), Oedalechilus labeo (Cuvier, 1829)) arasındaki
sistematik ilişki morfolojik karakterler kullanarak incelenmiştir. Bu çalışmada ayrıca ilk olarak kefal türleri içerisinde M.
soiuy ve L. abu’nun sistematik durumu birlikte incelenmiştir. Morfometrik verilere dayalı hiyerarşi küme analizi meristik
verilerle aynı bulunmadı. Kefal türlerinin taksonomik sınıflandırılmasında meristik karakterler morfometrik karakterlere göre
türleri daha ayırt edici özellikteydi. UPGM ağacına göre tüm türler iki ana branş altında toplandı. İlk branşta, C. labrosus ve
O. labeo birlikte en yakın taksa olarak sınıflandırıldı ve L. aurata’da bu iki türe yakın en ilişki içerisinde sınıflandırıldı. Diğer
dört Liza türü iki alt branş olarak bu grupta sınıflandırıldı; ilk branşta L. carinat ve L. saliens birbirine en yakın türler ve
bunlara yakın olan L. ramada ile sınıflandırıldı, ikinci branşta iki tatlı su orijinli tür olan L. abu ve M. soiuy birlikte diğer
türlerden çok farklı bir şekilde sınıflandırıldı. M. cephalus ise tüm türlerden çok farklı olarak sınıflandırıldı.
Anahtar Kelimeler: Mugilidae, morfoloji, morfolojik karakterler, hiyerarşi küme analizi.
Introduction
Mullets have worldwide distribution and inhabit
tropical and temperate seas; a few spend their lives in
freshwater (Nelsonv, 2006). The Mugilidae family
includes 17 genera and 72 species in the world
(Harrison and Senou, 1999; Nelson, 2006). Eight
species of Mugilidae inhabit the Mediterranean Sea,
and originally classified as part of the single genus
Mugil, under different names (M. cephalus, M.
ramada, M. labrosus, M. labeo, M. aurata, M. abu,
M. saliens, M. carinata). Lately, the systematic
relationships of these species were revised and
subdivided into four genera, Mugil, Liza, Chelon,
Oedalechilus. After revision, the species names have
been changed as Mugil cephalus, Liza ramada,
© Published by Central Fisheries Research Institute (CFRI) Trabzon, Turkey
in cooperation with Japan International Cooperation Agency (JICA), Japan
316
C. Turan et al. / Turk. J. Fish. Aquat. Sci. 11: 315-321 (2011)
Chelon labrosus, Oedalechilus labeo, Liza aurata,
Liza abu, Liza saliens, Liza carinata, occurring along
the Mediterranean Sea (Nelson, 2006) and one
species, Mugil capurii, found at the Atlantic coast of
Morocco and southward to Senegal (Nelson, 2006).
Mugil soiuy has also recently been found in the Black
Sea (Unsal, 1992). This is native to the Amur River
estuary and brackish waters of the Sea of Japan
(Zaitsev, 1991). Mugil soiuy was introduced into the
Azov Sea during the early 1980s by Soviet scientists
(Zaitsev, 1991). This species started to reproduce in
the Sea of Azov and was reported to be very
numerous along the South Crimean coast and was
caught for the first time along the eastern Turkish
Black Sea coast (Unsal, 1992). At the present Mugil
soiuy are commonly fished in the Black Sea and
rarely found in the Aegean Sea (Kaya et al., 1998;
Golani et al., 2002). L. abu inhabit Asia: Irak and
Pakistan and is reported from the Tigris, Europhrates
and recently Orontes (connected to Mediterranean
Sea) (Turan et al., 2004) river systems in Turkey. The
geographic distribution of O. labeo is restricted to the
Mediterranean Sea. C. Labrosus and L. carinata
inhabit the Mediterranean, the Eastern Atlantic coast
and Indo-Pacific areas (Tortonese, 1975). L. ramada
is found Mediterranean and the Black Sea (BenTuvia, 1986) and L. saliens inhabit Eastern Atlantic,
Mediterranean Sea, Black Sea, Sea of Azov and
Atlantic coasts from Morocco to France, Caspian Sea
(Baltz, 1991). M. cephalus is the only worldwide
species occurring on several continental waters
(Crosetti et al., 1994).
To date limited number of studies on
morphologic between species and genera in the
Mugilidae family in the Mediterranean Sea has been
found (Schultz, 1946; Corti and Crosetti, 1996;
Trewavas and Ingham, 1972; Harrison and Howes,
1991; Stiassny, 1993; Turan et al., 2000). Turan et al.
(2000) investigated four species (Mugil cephalus,
Chelon labrosus, Liza aurata, Liza ramada) of the
Mugilidae family with morphologic data. On the other
hand, it appears that there is lack of systematic studies
comprising all the species using morphometric and
meristic data together in the Mediterranean Sea. Also
the systematic position of M. soiuy and L. abu among
other mullet species was investigated in the present
study for the first time.
The aim of this study is to contribute to the
understanding of the systematic relationship of the
Mediterranean
grey
mullet
species
using
morphometric and meristic characters.
Material and Methods
Laboratory Procedures
Individual samples from each species were
collected from Iskenderun Bay in North-eastern
Mediterranean Sea and Trabzon Seaport in the Black
Sea. Certain biological aspects of the samples are
given in Table 1.
Morphometric
The truss network system described for fish
body morphometrics (Strauss and Bookstein, 1982)
was used to construct a network on mullet’s body.
Thirteen landmarks determining 24 distances were
chosen and measured on the body, as illustrated in
Figure 1. Fish were thawed, placed on their right side
on acetate sheets, and body posture and fins were
teased into a natural position. Each landmark was
obtained by piercing the acetate sheet with a
dissecting needle, and additional data such as eye
diameter (ED), head width (HW), pectoral fin length
(PFL) were also recorded with digital calliper. Only
undamaged fish were included in the analyses. There
were no significant correlation (P>0.05) between the
standardized truss measurements and standard length,
indicating that the size effect was successfully
removed with the allometric transformation (Somers,
1986).
Meristic
Five meristic characters commonly used to
describe mullets were examined using the number of:
first dorsal fin rays (DFR1), second dorsal fin rays
(DFR2), ventral fin rays (VFR), anal fin rays (AFR),
pectoral fin rays (PFR), pyloric caeca (PC) under a
binocular microscope.
Table 1. Location and biological features of mullet species. Standard deviations of mean stanfad length (STL) of samples are
given brackets
Species
Chelon labrosus
Oedalechilus labeo
Mugil cephalus
Mugil soiuy
Liza aurata
Liza abu
Liza carinata
Liza ramada
Liza saliens
Locations
36°02' N 35°57' E
36°05' N 35°55' E
36°22' N 35°50' E
41°01' N 39°35' E
36°25' N 35°53' E
36°04' N 36°01' E
36°36' N 35°30' E
36°49' N 36°09' E
36°45' N 36°10' E
Collection
Time
07.06.2007
21.05.2007
15.05.2007
14.07.2007
04.06.2007
16.07.2007
24.11.2007
09.07.2007
14.07.2007
Gear
Gill Net
Gill Net
Gill Net
Gill Net
Gill Net
Gill Net
Gill Net
Gill Net
Gill Net
Sample
size
25
25
25
10
25
25
25
25
25
Mean STL (cm) (± SD)
(Min-Max)
13.75±3.03 (9.6-19.2)
21.50±2.24 (17.7-27.7)
15.70±0.90 (14.1-17.2)
39.33±1.51 (37.0-41.2)
14.03±3.05 (9.8-18.0)
13.67±1.99 (11.5-17.0)
11.59±0.82 (10.1-13.2)
13.20±0.82 (12.0-14.7)
22.28±5.39 (15.4-29.7)
C. Turan et al. / Turk. J. Fish. Aquat. Sci. 11: 315-321 (2011)
statistical package program. The DFA combines a
selection of body measures in a linear fashion to
produce a mathematical function, which can be used
to classify individuals into groups. In hierarchical
cluster analyses, UPGMA dendogram based on
Squared Euclidean distance was constructed to
monitor taxonomic relationships among the species
that does not plot actual distances but rescales the
distance to numbers between 0 and 25.
Multivariate Analyses
Morphometric and meristic characters were used
separately in the multivariate analyses, though these
variables are different both statistically and
biologically (Allendorf et al., 1987; Ihssen et al.,
1981). Body measurements strongly correlate with
body size, while in most fish meristic characters do
not change during growth beyond some threshold
body size (Strauss, 1985). Therefore allometric
growth can result in heterogeneity of shape without
providing information on differences in body
proportion among populations (Reist, 1985). In the
present study, there were significant correlations in
size only for morphometric characters between the
samples. Therefore transformation of absolute
measurements to size–independent shape variables
was accomplished by using the formula by Elliott et
al. (1995);
Results
Morphometric
Univariate statistics (ANOVA) revealed highly
significant (P<0.001) differences between species
from all truss measurements. The canonical
discriminant function analysis produced 8 functions
(DFs). The first DF explained 49% and second and
third DFs explained 20% and 12% of between-group
variability respectively. The overall random
assignment of individuals into their original group by
the DFA was 100%. In order to illustrate which
morphometric characters are playing role to
differentiate species contribution of each variable to
the canonical functions were examined, and high
contribution from measurements 2_3, 3_12, 1_2, PFL,
HW, ED were observed (Table 2).
The UPGMA cluster analysis of morphometric
data did not cluster species on the bases of current
meristic status of Mugilidae (Figure 2). Three main
branching were produced: in the first branch, C.
labrosus was clustered as a closest taxa to L. ramada,
being the sister group to O. labeo, and L. aurata and
M. cephalus were branched more divergently from
these three species. In the second group, L. carinata
was clustered together with L. abu, being sister to M.
soiuy. L. saliens seen to be morphometrically most
divergent from the other species and was branched as
a third group.
Madj = M (Ls / Lo)b
where M: original measurement, Madj: size
adjusted measurement, Lo: standard length of fish, Ls:
overall mean of standard length for all fish from all
samples in each analysis. Parameter b was estimated
for each character from the observed data as the slope
of the regression of logM on logLo, using all fish in
all groups. Correlation coefficients between
transformed variables and standard length were
calculated to check if the data transformation was
effective in removing the effect of size in the data.
The effectiveness of size transformations was
evaluated by testing the significance of correlation
between transformed variables and standard length. A
significant correlation indicated an incomplete
removal of size effects from the data. Size adjusted
data were standardized and submitted to a canonical
discriminant function analysis (DFA), and
discriminant function (DF) scores were used in
hierarchical cluster analyses using SPSSv13.0
3
317
4
5
2
6
7
8
1
10
9
13
12
11
Figure 1. Locations of the 13 landmarks for constructing the truss network on fish (●) and morphometric lengths between
dots. Landmarks refer to (1) anterior tip of snout at upper jaw, (2) most posterior aspect of neurocranium (beginning of scaled
nape), (3) origin of dorsal fin, (4) insertion of dorsal fin, (5) origin of 2 nd dorsal fin, (6) insertion of 2nd dorsal fin, (7) anterior
attachment of dorsal membrane from caudal fin, (8) posterior end of vertebrae column, (9) anterior attachment of ventral
membrane from caudal fin, (10) insertion of anal fin, (11) origin of anal fin, (12) insertion of pelvic fin, (13) posteriomost
point of maxillary. Picture modified from Bauchot (1987).
318
C. Turan et al. / Turk. J. Fish. Aquat. Sci. 11: 315-321 (2011)
Meristic
Observed meristic characters of nine mullet
species (Table 3) were in the range of their
description given by Nelson (2006). Highly
significant (P<0.001) differences between species
were observed from all meristic characters. Dorsal
(DFR1) and ventral fin rays (VFR) were constant in
each group and could not be computed in the
Univariate analysis.
Table 2. Contribution of morphometric and meristic variables to the canonical functions. Variables ordered by size of
correlation within the functions *, indicate largest correlation between each variable and any discriminant function
Morphometric
2_3
3_12
1_2
PFL
ED
HW
6_9
7_9
5_9
1_12
12_13
10_11
6_7
2_12
2_11
3_4
4_10
4_11
3_10
4_9
1_13
5_10
3_11
2_13
4_5
11_12
9_10
Meristic
PFR
PC
DFR2
AFR
1
-0.065
-0.232
-0.125
0.008
-0.202
-0.015
-0.163
-0.028
-0.146
0.026
0.042
-0.163
-0.026
0.047
0.078
0.055
0.073
0.026
0.105
0.064
-0.064
-0.195
0.126
-0.072
0.172
-0.061
-0.051
2
0.416*
-0.345*
-0.213*
0.177
0.076
-0.234
0.008
-0.213
-0.005
0.062
0.019
0.118
0.025
0.083
0.131
-0.311
-0.034
-0.181
-0.159
0.018
0.018
-0.146
-0.230
-0.116
-0.017
-0.029
0.046
3
-0.126
0.137
0.129
0.438*
0.422*
0.268*
-0.079
-0.297
-0.107
-0.064
-0.178
0.055
-0.041
-0.018
-0.071
-0.097
0.003
0.071
0.032
-0.022
0.198
-0.075
0.035
0.122
0.088
-0.093
-0.052
4
0.076
0.258
0.095
0.233
0.302
-0.134
0.476*
0.372*
0.313*
0.251*
0.225*
-0.221*
0.211*
0.196*
0.189*
0.152
0.068
0.168
0.169
0.151
0.011
0.139
0.262
-0.064
-0.036
0.174
0.174
0.950*
0.228
0.021
0.087
-0.177
0.833*
-0.273
-0.042
0.100
0.381
0.896*
0.570
-0.239
-0.330
-0.349
0.816*
Function
5
-0.029
0.129
-0.076
-0.026
-0.369
-0.149
-0.023
0.060
-0.134
0.014
0.068
-0.035
0.183
0.176
-0.131
0.492*
-0.402*
-0.308*
-0.285*
-0.285*
-0.128
-0.332
-0.103
0.017
-0.298
-0.104
0.170
Figure 2. UPGMA tree of Squared Euclidiean distances based on morphometric data.
6
-0.051
-0.225
0.056
-0.028
0.142
-0.019
0.323
0.186
0.280
-0.002
-0.107
0.197
0.105
0.011
-0.110
0.058
0.251
0.241
0.020
0.181
0.462*
0.343*
0.160
-0.100
0.197
0.002
0.173
7
0.097
-0.068
0.163
0.056
0.006
0.121
0.080
0.133
-0.144
0.212
0.137
0.051
0.046
0.152
-0.044
-0.188
0.068
-0.149
-0.053
-0.050
0.299
-0.051
-0.352*
0.240*
0.097
-0.174
-0.203
8
0.022
0.128
0.196
-0.070
-0.030
0.031
-0.058
-0.247
-0.084
0.227
0.005
-0.179
-0.111
0.014
0.104
0.040
0.203
0.129
0.024
0.216
-0.048
-0.072
0.273
0.035
0.309*
0.277*
0.238*
C. Turan et al. / Turk. J. Fish. Aquat. Sci. 11: 315-321 (2011)
319
Table 3. Observed meristic counts of the nine mullet species.
Species
Chelon labrosus
Oedalechilus labeo
Mugil cephalus
Mugil soiuy
Liza aurata
Liza abu
Liza carinata
Liza ramada
Liza saliens
DFR 1
IV
IV
IV
IV
IV
IV
IV
IV
IV
DFR 2
I 8
I 8
I 8
I 8-9
I 8
I 7-8
I 7
I 7-8
I 7
The first discriminant function explained 63% of
between group variability and the second, third and
fourth explained 29%, 6%, 2% respectively.
Component loadings showed that PFR, PC, DFR2,
AFR characters are playing key role to differentiate
species respectively (Table 2).
Hierarchical cluster analyses of meristic data
clustered O. labeo and C. labrosus as a closest taxa
being the sister group to L. aurata. The neighbouring
branch is made up of L. carinata, L. saliens and L.
ramada. M. cephalus was most divergently clustered
in the dendogram and close to its sister species M.
soiuy and L. abu (Figure 3).
Discussion
Taxonomic description of fishes has commonly
relied on the description of unique sets of
morphological characters. Meristic characters in the
present study were rather more discriminative than
morphometric characters in terms of taxonomic
classification of the mullets. Segmented rays in the
dorsal (DFR2) and anal fins and pectoral fins, and
also pyloric caeca were most discriminative
characters in the present classification of mullets.
Such characters are phylogenetically informative to
distinguish between species of the Mugilidae.
The present meristic analysis within the family
Mugilidae did not reveal similar pattern of
morphologic results among the species. On the other
hand, morphometric data were not congruent with
meristic data. Based on meristic data UPGMA tree
splited Liza and Mugil genera species into two main
clusters. In the first group, M. cephalus was clustered
with its sister species M. soiuy, supporting
monophyletic status of Mugil genera. The results
revealed that M. cephalus was morphologically more
divergent than M. soiuy from the other Mediterranean
taxa. On the other hand, L. abu is grouped within the
Liza genera and sister group into three Liza species
(L. ramada, L. saliens, L. carinata). However O.
labeo and C. labrosus species was clustered together
and included within the Liza genera. Similar
controversy was also reported in connection with
chromosome analysis by Cataudella et al. (1974) who
did not find significant differences in the karyotype of
VFR
I 5
I 5
I 5
I 5
I 5
I 5
I 5
I 5
I 5
AFR
III 8-9
III 8-10
III 8-9
III 8-9
III 8-9
III 8
III 7
III 8-9
III 7-8
PFR
17
16-17
17
16
16
11-12
15
16-17
16
PC
6-7
6
2
4-5
7-8
3-5
5
6-8
7-9
C. labrosus compared to the three Mediterranean
species of the Liza genus. Several studies have also
questioned the present systematic status of the
Mugilidae. Turan et al. (2000) analyzed by using
Truss network system and 10 meristic characters of
four grey mullets and all mullet species (M. cephalus,
C. labrosus, L. aurata, L. ramada) were clearly
different from each other. Antovic and Simonovic
(2006) investigated interspecific variability and
phenetic relationships in six southern Adriatic mullet
species (M. cephalus, C. labrosus, L. aurata, L.
ramada, L. saliens and O. labeo), and as a result M.
cephalus was clearly separated from the other species
and the species of the genus Liza were phenetically
most similar.
Caldara et al. (1996) compared DNA sequences
of mitochondrial cytochrome b and 12S rRNA genes
for six mullets species and observed lowest genetic
distance between C. labrosus and L. saliens.
Papasotiropoulos et al. (2002) investigated
phylogenetic relationship of five mullet species (M.
cephalus, C. labrosus, L. aurata, L. ramada and L.
saliens) with PCR-RFLP of mtDNA gene segments
and found that L. saliens and C. labrosus were the
closely related species while M. cephalus was the
most distinct one. A similar result reported by Rossi
et al. (2004) using allozyme data and 16s mt-rRNA,
reffered to M. cephalus as being the most divergent
species and the existence of a main cluster including
all the Mediterranean species of Liza and C. labrosus.
Also, Rossi et al. (2004) indicated that the
Mediterranean species of Liza did not form a
monophyletic group exclusive of Chelon and thus, the
monophyly of the whole genus should be
reconsidered.
In addition to several previous studies (Harrison
and Howes, 1991; Caldara et al., 1996; Murgia et al.,
2002; Gornung et al., 2001, 2004), and this study is
consistent in not identifying the Mediterranean Liza
species as a monophyletic group. This is in agreement
with our previous studies based on allozyme data
(Turan et al., 2005). Morever, Turan et al. (2005)
reported that C. labrosus and O. labeo clustered as
closest taxa and were sister group to L. ramada. M.
cephalus and M. soiuy, clustered together and were
clearly isolated from the other three genera. It is
320
C. Turan et al. / Turk. J. Fish. Aquat. Sci. 11: 315-321 (2011)
Figure 3. UPGMA tree of Squared Euclidiean distances based on meristic data.
reported in a recent phylogenetic study by
Papasotiropoulos et al. (2007) using three (12s rRNA,
16s rRNA, and COI) mtDNA segments that the
greatest genetic differentiation was observed between
M. cephalus and all the other species studied, while C.
labrosus and L. aurata were the closest taxa.
Our present study, indicated that Liza
monophyly were not supported, allowing room for the
plea to get more data to resolve the systematics of
mullets. M. cephalus and M. soiuy supported
monophyletic status of Mugil genera, which had
higher morphologic compared to other Mediterranean
taxa. However, Chelon and Oedalechilus genera
species were clustered within the Liza genera. The
separation of Liza, Chelon and Oedalechilus might be
unnatural, and that the monophyletic origin of the
genus Liza is questionable. However the existence of
such differences in morphologic and phylogenetic
studies of Mugilidae in the literatures is not
uncommon (Cataudella et al., 1974; Menezes et al.,
1992; Caldara et al., 1996; Rossi et al., 1998; Fraga et
al., 2007). Therefore, more studies are needed to
integrate not only more species but also different
genetic data (mtDNA, nDNA vs.).
In conclusion, we did not detect any appreciable
degree of morphologic differentiation between Liza,
Chelon and Oedalechilus species. This was strongly
supported by our previous genetic study (Turan et al.,
2005) based on allozymic data. At the same time,
other similar studies based on mtDNA and allozyme
data (e.g., Caldara et al., 1996; Rossi et al., 2004;
Papasotiropoulos et al., 2007) seem to be in
agreement with our current findings, leaving room for
reconsidering the modern systematic classification of
those species. The lack of congruence in the
morphologic results of mullet species suggests us
scrutinizing the present status of Mugil species with
more comprehensive investigations using molecular
genetic and morphologic markers together.
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