CALIGUS TURKIYENSIS N. SP.
(COPEPODA: CALIGIDAE) ON THE FLATHEAD GREY MULLET, MUGIL CEPHALUS (LINNAEUS) (MUGILIFORMES: MUGILIDAE)
FROM THE SEA OF MARMARA, TURKEY
INTRODUCTION
Members of the Caligidae family are ectoparasite
copepods on fish. There are 269 valid species listed in the genus Caligus, belonging to the family Caligidae (Walter & Boxshall 2024).
Species belonging to Caligus are known as sea
lice. These parasites are of global importance, because sea lice cause
high levels of mortality as well as catastrophic losses in salmonid
aquaculture. As a result, the direct and indirect effects of fish lice
are economic losses in aquaculture (Johnson et al. 2004).
The number of Caligus species in
the Mediterranean increased to 32, after the record of Caligus tunisiensis Hamdi, Benmansour, Zouari-Tlig,
Kamanli, Özak, Boxshall, 2021 on Serranus scriba
(Linnaeus, 1758) from the Mediterranean Sea. So far, 20 species
of Caligus have been reported from the fishes
of the Aegean Sea and Mediterranean Sea of Turkey: Caligus adenensis Özak, Sakarya & Boxshall
2019, Caligus apodus (Brian 1924), Caligus bonito
C. B. Wilson 1905, Caligus brevicaudatus A.
Scott 1901, Caligus dakari van Beneden 1892,
Caligus diaphanus von Nordmann 1832, Caligus lagocephali Pillai 1961, Caligus lichiae Brian 1906, Caligus ligusticus Brian 1906, Caligus macrurus Heller 1865, Caligus minimus Otto, 1821, Caligus mulli Rodrigues, Özak, Silva & Boxshall
2018, Caligus pageti Russel 1925, Caligus pelamydis Krøyer, 1863, Caligus quadratus Shiino, 1954, Caligus scribae Essafi, Cabral & Raibaut 1984,
Caligus solea Demirkale, Özak, Yanar &
Boxshall 2014, Caligus temnodontis Brian 1924
and Caligus vexator Heller,1865. Five species
of Caligus are known from the Sea of Marmara:
C. apodus, C. bonito,
C. diaphanus, Caligus
minimus and Caligus zei Norman & T.
Scott 1906 (Özak 2020).
Eighteen species of Caligus from
Mugil cephalus Linnaeus, 1758 are listed in the
world (Table I, WoRMS 2024),
but only four of them are known on M. cephalus
from the Mediterranean Sea. These species are C. apodus, C. minimus, C. mugilis and C. pageti
(see Raibaut et al. 1971, Raibaut & Ben Hassine 1977, Raibaut et al.
1998, Kabata
2003). This paper describes a new species, Caligus turkiyensis n. sp. from the body surface
and fins of the flathead grey mullet, M.
cephalus, collected in the Sea of Marmara of Turkey. Two other
Caligus species were identified in this survey:
Caligus apodus and Caligus
pageti on the body surface and fins of Chelon
auratus (Risso, 1810) and M. cephalus from
the Sea of Marmara, Turkey.
MATERIALS AND METHODS
One hundred and thirty specimens of the flathead grey
mullet, Mugil cephalus and 63 of the golden
grey mullet, Chelon auratus were caught by rod
and line from Bandırma Bay, Turkey (the Sea of Marmara) in 2022. The
parasites collected were fixed in 70 % ethanol. Some of the specimens
were later cleared in lactic acid for 2 h before dissection of the
appendages. The samples were dissected using an Olympus SZH10 and a
Wild M5 stereomicroscope. The appendages were mounted on slides in a
glycerin-gelatine mounting medium following Pritchard & Kruse
(1982). The drawings of
appendages were made with the aid of a drawing tube (Olympus® BH-DA).
Microscope images were drawn on tracing paper, and the drawings were
scanned and digitized. Additionally, microphotographs were taken with
the aid of a Canon camera (EOS 1100D) connected to an Olympus CH30
phase contrast microscope. The scientific names and synonyms for
parasites and hosts were checked with WoRMS (2024), and Froese & Pauly (2024), respectively. The
nomenclature of copepod body parts follows Boxshall (1990) and Huys & Boxshall
(1991). Samples of C. turkiyensis n. sp. in this study were compared
with samples of Caligus minimus previously
collected from Köyceğiz Dalyan Lagoon (Figs. 2, 6). Type and voucher specimens are deposited
in the Zoology Collection of the İstanbul University, Faculty of
Science, İstanbul, Turkey.
RESULTS
In this study, three species of Caligus were identified: Caligus
apodus, Caligus pageti and Caligus turkiyensis n. sp.
Locality: Bandırma Bay (Balıkesir, Sea of Marmara,
Turkey; 40°21’12.8” N 27°58’04.7” E); depth range: 1-3 m
Locality properties: A region where flows the sewage
waters of Bandırma City Site on host: body surface, pectoral, ventral
and caudal fins
Prevalence of infection: 21 %, Mean intensity: 1.3
Material examined: 1 female and 1 male deposited in the Zoology
Collection of the Istanbul University, Faculty of Science (IUSHM
20231007-07, IUSHM 20231007-08)
Adult female: Body (Fig. 1a) consists of a caligiform
cephalothorax shield, a fourth pedigerous somite, a genital complex,
and 1-segmented abdomen with paired caudal rami. Total body length
3.72 mm (3.33-4.26, n=4) caudal rami, excluding setae. Dorsal
cephalothoracic shield is subcircular and slightly longer 1.74 mm
(1.57-1.91) than wide 1.63 mm (1.40-1.81). Fourth pedigerous somite
wider 0.37 mm (0.27-0.42) than long 0.21 mm (0.15-0.25), distinctly
separated from the cephalothorax and genital complex. Genital complex
subcircular, is wider 1.07 mm (0.84-1.23) than long 0.90 mm
(0.73-1.12), about 1.3 times longer than the abdomen. Abdomen
subrectangular and elongated, 1-segmented, longer 0.69 mm (0.66-0.72)
than wide 0.37 mm (0.290.42). Caudal ramus subrectangular, slightly
longer 0.19 mm (0.14-0.31) than wide 0.15 mm (0.11-0.20), each armed
with six plumose setae. Egg sac long 2.39mm (1.98-3.21), wide 0.33 mm
(0.31-0.42). Setal and spinal formula of 1-4 legs are given in Table II.
Adult male: Body (Fig. 1b)
consists of a caligiform cephalothorax shield, fourth pedigerous
somite, genital complex and 1-segmented abdomen with paired caudal
rami. Total body length 3.57 mm, (3.52-3.62, n = 2) caudal rami,
excluding setae. Dorsal cephalothoracic shield subcircular, slightly
longer 1.91 mm (1.901.92) than wide 1.72 mm (1.70-1.74). Fourth
pedigerous somite wider 0.42 mm (0.41-0.42) than long 0.22 mm
(0.21-0.22), distinctly separated from the cephalothorax and genital
complex. Genital complex subcircular, is slightly wider 0.71 mm
(0.7-0.72) than long 0.61 mm (0.590.62), about as long as the abdomen.
Abdomen subrectangular 1-segmented, longer 0.62 mm (0.60-0.63) than
wide 0.32 mm (0.31-0.32). Caudal ramus subrectangular, slightly longer
0.23 mm (0.22-0.23) than wide 0.12 mm (0.110.12) and each armed with
six plumose setae.
Remarks: Brian (1924) first described C. apodus (as syn Pseudocaligus
apodus) on M. cephalus from Mauritania.
This species is easily distinguished from the other caligid species by
the absence or presence of the vestigial fourth leg in female and male
samples. Ben Hassine (1983)
mentioned the presence of vestigial fourth legs in both females and
males of C. apodus from Tunisia. Özak et al. (2013) did not observe a vestigial fourth leg in
female samples from Turkey. They also found a minute, rod-like trace
of a possible fourth leg in one of the two females in Brian’s (1935) samples from Italy. No
evidence of the fourth leg in female individuals was found in the
present study.
Özak et al. (2013) also compared male samples
of C. apodus from Turkey and Brian’s (1935) samples from Italy. Özak et al. (2013) found three unequal and spiniform elements at
the apex in the samples from Turkish Mediterranean Sea Coasts and two
spiniform terminal elements in Italian material. The fourth leg with
three terminal spiniform elements in the male samples (Fig. 1c) in this study is also
compatible with those of Özak et al. (2013).
The total body length of females in this study was
smaller than in Brian’s (1935) length of 4.3-5.00 mm and Özak et al.’s (2013) of 4.30 mm. The total body length of males in
this study was greater than Özak et al.’s (2013) of 3.19 mm and smaller than
in Brian’s (1935) of
3.19-4.00 mm.
Locality: Bandırma Bay (Balıkesir, Sea of Marmara,
Turkey; 40°21’12.8”N 27°58’04.7”E); depth range: 1-3 m
Locality properties: A region where flows the sewage
waters of Bandırma City Site on host: body surface, pectoral, ventral
and caudal fins
Prevalence of infection: 10 %, Mean intensity: 1.2
Material examined: 1 female and 1 male deposited in the Zoology
Collection of the Istanbul University, Faculty of Science (IUSHM
2023100709, IUSHM 20231007-10)
Adult female: Body (Fig. 1d)
consists of a caligiform cephalothorax shield, a fourth pedigerous
somite, a genital complex and 1-segmented abdomen with paired caudal
rami. Total body length 4.17 mm (3.42-5.07, n = 4). Dorsal
cephalothoracic shield subcircular, is slightly longer 2.40 mm
(2.02-2.93) than wide 2.28 mm (1.87-2.81). Fourth pedigerous somite
wider 0.64 mm (0.51-0.81) than long 0.25 mm (0.22-0.29), distinctly
separated from the cephalothorax and genital complex. Genital complex
subrectangular, wider 1.35 mm (0.911.71) than long 0.89 mm
(0.62-1.12); about 2.3 times longer than the abdomen, and with
slightly lobate posterolateral corners of genital complex and
extending to middle of abdomen. Abdomen subrectangular, 1-segmented,
slightly wider 0.44 mm (0.38-0.51) than long 0.39 mm (0.35-0.46).
Caudal ramus subrectangular, longer 0.24 mm (0.21-0.27) than wide 0.16
mm (0.120.20), each armed with six plumose setae. Egg sac long 2.79 mm
(1.72-3.62), wide 0.39 mm (0.31-0.42). Setal and spinal formula of 1-4
legs are given in Table
II.
Adult male: Body (Fig. 1e) consists of a caligiform
cephalothorax shield, a fourth pedigerous somite, a genital complex
and 1-segmented abdomen with paired caudal rami. Total body length
4.49 mm (4.21-4.63, n = 3). Dorsal cephalothoracic shield subcircular,
slightly longer 2.63 mm (2.41-2.75) than wide 2.57 mm (2.31-2.72).
Fourth pedigerous somite, wider 0.66 mm (0.61-0.69) than long 0.32 mm
(0.31-0.33), distinctly separated from the cephalothorax and genital
complex. Genital complex subcircular, wider 0.98 mm (0.91-1.02) than
long 0.70 mm (0.67-0.72), about 1.3 times longer than abdomen. Abdomen
subrectangular and 1-segmented, slightly wider 0.55 mm (0.51-0.61)
than long 0.52 mm (0.51-0.52). Caudal ramus subrectangular, longer
0.32 mm (0.31-0.34) than wide 0.22 mm (0.22-.0.24), each armed with
six plumose setae.
Remarks:Caligus pageti was first described on M. cephalus from Egypt by
Russel (1925). The most
distinguishing characteristic of C. pageti is
the fourth leg, which is serrated to middle of inner and outer margins
of fourth leg. The fourth leg is 3-segmented, with a protopodal
segment and 2-segmented exopodal segment; protopodal segment with a
plumose first exopodal segment with outer spine; second exopodal
segment with long outer apical spine and one subapical spine about
one-third the length of the apical spine; long apical spine serrated
to the middle of inner and outer margins (Fig. 1f).
Type host: Mugil cephalus
Linnaeus, 1758(Mugilidae) (n = 130)
Locality: Bandırma Bay (Balıkesir, Sea of Marmara,
Turkey; 40°21’12.8”N 27°58’04.7”E); depth range: 1-3 m
Locality properties: A region where flow the sewage
waters of Bandırma City
Site on host: body surface, fins
Prevalence of infection: 22 %, Mean intensity: 1.1
Type Material: Holotype female and paratype male deposited in the
Zoology Collection of the Istanbul University, Faculty of Science
(IUSHM 20231007-03, IUSHM 20231007-04)
Etymology: The species name refers to Turkey, close to
where the material was collected.
Description
Adult female: Cephalothorax
subcircular, dorsoventrally flattened, lateral zones of dorsal
cephalothoracic shield associated with welldeveloped marginal
membranes. Body consists of a caligiform cephalothorax shield, a
fourth pedigerous somite, a genital complex and an indistinctly
2-segmented abdomen with paired caudal rami. Total body length 3.79
mm (3.134.61, n = 7) (Fig. 2a, 3a).
Dorsal cephalothoracic shield subcircular, longer at 1.82 mm
(1.52-2.01) than wide 1.61 mm (1.34-1.73). Fourth pedigerous somite
is wider at 0.46 mm (0.24-0.61) than long 0.23 mm (0.14-0.32),
distinctly separated from the cephalothorax and genital complex.
Genital complex subcircular, is slightly wider at 1.04 mm
(0.77-1.52) than long 0.94 mm (0.741.31), about 1.6 times longer
than the abdomen and with nonlobate posterolateral corners of
genital complex. Abdomen subrectangular, indistinctly with two
somites, first abdominal somite slightly wider at 0.31 mm
(0.21-0.41) than long 0.18 mm (0.12-0.22), anal somite longer at
0.41 mm (0.280.48) than wide 0.33 mm (0.28-0.42). Egg sac 2.11 mm
(1.82-2.51) long by 0.36 mm (0.31-0.42) wide.
Antennule (Fig.
3b) 2-segmented; proximal segment distinctly larger than
distal, armed with 24 setae; distal segment armed with isolated
subterminal seta on posterior margin and 11 naked setae plus two
aesthetascs around the apex. Antenna (Fig. 3f, 6e) uniramous, 3-segmented; proximal segment
subrectangular with rounded margins and a short process; middle
segment subrectangular and armed with a large corrugated adhesion
pad on the dorsal surface; terminal segment forming a recurved claw
armed with a seta near the middle area and posterior margin.
Post-antennal process (Fig.
3f, 6g)
well-developed, slender and slightly curved, ornamented with two
trisensillate papillae on the basal part and a single similar
trisensillate papilla on the adjacent ventral cephalothoracic
surface near the base of the post-antennal process. Mandible (Fig. 3c, 6m) stylet-like, armed with 13 marginal teeth on
inner side near the apex. Maxillule (Fig. 3h, 6k) comprising an anterior papilla bearing three
naked setae (one medial long seta and two lateral small setae), and
an anterior process with folding, and posterior process slender with
rounded margin. Maxilla (Fig.
3g) 2-segmented and brachiform; proximal segment (lacertus)
unarmed; distal segment (brachium) slender, bearing subterminal
hyaline membrane on the inner margin plus short canna and long
calamus distally. Maxilliped (Fig. 3e,
6a) subchelate, protopodal segment (corpus) elongate and
bearing a slight expansion on myxal surface; distal subchela
representing endopodal segments plus claw; small seta at the concave
margin of claw base. Sternal furca (Fig. 3d,
6c) with subrectangular box, elongated and parallel tines with
little divergence. Leg 1 (Fig.
4a) biramous with sympods joined by a slender intercoxal
sclerite; sympod with inner and outer plumose seta, plus a setule;
and endopod represented by a process on the posterior margin of
basis, bearing two-minute vestigial setae on the apex. Exopod
2-segmented, with first exopodal segment robust, about 2.7 times
longer than wide, armed with a small outer spine at the distal
corner and ornamented with a row of setules along the mid-section of
the posterior margin. Distal exopodal segment with three plumose
setae posteriorly plus four distal margin elements; spine 1
(outermost) and seta 4 smooth and longer than spines 2-3; spines 2
and 3 about equal in length, both lacking accessory process and
arcuated with blunt ends. Leg 2 (Fig. 4b) biramous, with distinct coxa and basis;
coxa short, bearing a long plumose inner seta and a sensillium on
the ventral surface; basis armed with a short naked seta on the
outer distal corner plus extensive marginal membrane along the
posterior margin and a sensillium near the mid-length of the
anterior margin. Exopod 3-segmented: first exopodal segment with
inner plumose seta, an outer spine, extending to the middle of the
third exopodal segment and with a row of setules on the inner
margin; the second exopodal segment is the smallest, with an inner
plumose seta and an outer distal spine and not extending across to
the anterior margin of the third segment. Third exopodal segment
with three outer spines and five inner plumose setae; first spine
simple and smallest; second spine slightly longer than first spine
and third spine with an outer marginal membrane and fine setules
along the inner margin. Endopod 3-segmented; first endopodal segment
subrectangular, armed with an inner plumose seta and ornamented with
a row of setules along the outer margin; second segment elongated,
armed with two inner plumose setae plus ornamented with a row of
setules along the outer margin; third segment smallest, with six
plumose setae. Leg 3 (Fig.
4c) protopodal part flattened and joined by plate-like
intercoxal sclerite, forming an apron ornamented with marginal
membrane posteriorly and along the lateral margin anterior to the
exopod: bearing inner plumose seta at the junction with intercoxal
plate and an outer plumose seta dorsal to the base of the exopod;
sensillae located adjacent to the inner coxal seta and adjacent to
the origin of endopod. Exopod 3-segmented: first segment with a
large, recurved outer spine; a hyaline flap and sensillium along the
corner of spine; second segment with an outer spine, inner plumose
seta and setules along outer margin; the third segment with three
outer spines (third spine slightly longer than the other two) and
four short plumose setae. Endopod 2-segmented: first segment is
armed with a long inner plumose seta; second segment is armed with
six plumose setae, ornamented with rows of setules along the outer
margin. Leg 4 (Fig. 4d,
6o) uniramous. Protopodal
segment with an outer seta derived from the basis. Exopod
2-segmented; first segment bearing a short, slender, outer distal
spine, not extending to the middle part of second exopodal segment;
second segment with three apical spines increasing in length from
outer to inner; first spine slightly shorter than second and third
spine three times as long as. Leg 5 (Fig. 4e) is represented by three plumose setae.
Setal and spinal formula of 1-4 legs are given in Table II.
Caudal ramus (Fig. 4f)
subrectangular, longer 0.19 mm (0.13-0.27) than wide 0.14 mm
(0.10-0.25), each armed with three distal setae the longest on the
outer margin, a median size seta, and other the two located opposed,
and with a row of setules on inner margin.
Adult male: Cephalothorax
subcircular, dorsoventrally flattened, lateral zones of dorsal
cephalothoracic shield associated with welldeveloped marginal
membranes. Body consists of a caligiform cephalothorax shield, a
fourth pedigerous somite, a genital complex and 1-segmented abdomen
with paired caudal rami. Total body length 3.67 mm (3.30-4.69, n =
7) (Fig. 2c, 5a). Dorsal cephalothoracic
shield subcircular, is slightly longer 2.12 mm (1.82-2.71) than wide
1.75 mm (1.52-2.22). Fourth pedigerous somite at wider 0.49 mm
(0.41-0.61) than long 0.29 mm (0.21-0.35), distinctly separated from
the cephalothorax and genital complex. Genital complex subcircular,
is slightly at wider 0.69 mm (0.56-0.92) than long 0.56 mm
(0.46-0.72), and about 1.2 times longer than abdomen. Abdomen
subrectangular, 1-segmented, longer at 0.46 mm (0.41-0.60) than wide
0.34 mm (0.30-0.42). Caudal ramus subrectangular, longer at 0.23 mm
(0.200.31) than wide 0.13 mm (0.11-0.22), each armed with six
plumose setae. Antennule, mandible, post-antennal process and
maxilla as in female. Maxilliped (Fig. 5b, 6i) protopod (corpus) is slightly swollen and armed
with one small process at distal part and one big process as bifid
at posterior part of myxal surface opposing tip of subchela; distal
subchela armed with a short seta at the concave margin of claw base
and a spine at posterior margin. Antenna (Fig. 5c) 3-segmented; proximal segment elongated
and unarmed; middle segment reflexed, swollen proximally, with
corrugated adhesion pads on medial and distal surfaces; distal
segment with four plates on trifid direction and with basal seta.
Maxillule (Fig. 5d)
comprising an anterior papilla bearing three naked setae (one long
and two small) and reduced posterior process. Legs 1 to 4, as in
female. Leg 5 and 6 (Fig.
5e) are represented by three plumose setae and a minute spine,
respectively.
Remarks: The report of C. mugilis from M.
cephalus caught in Bandırma Bay (Sea of Marmara) by Alaş &
Öktener (2017) is erroneous
according to Özak (2020)
for the following reasons: the female had an abdomen as long as the
genital complex; the female maxilliped had a distinct, subtriangular
myxal process; the posterolateral corners of the genital complex
were indistinctly lobate and did not extend beyond the posterior
margin of the genital complex. This study provided an opportunity to
collect and examine the specimens of Alaş & Öktener (2017) again. The morphology of
the new species appears to have the closest similarity to the four
species Caligus curtus Müller O.F., 1785, Caligus dicentrarchi Cabral & Raibaut, 1986,
C. minimus and C.
mugilis (Table IV).
Caligus mugilis was described for the first
time from the mucous membrane of the mouth of M.
cephalus from Portoferraio, Italy by Brian (1935), but he considered it to
be a subspecies of Caligus minimus and named
it as Caligus minimus var. n. mugilis. Later, Raibaut & Ben Hassine (1977) accepted C. mugilis as a different species from Chelon labrosus (Risso, 1827) and described it
from only female specimens. They also compared females of C. mugilis from C.
labrosus and C. minimus from Dicentrarchus labrax (Linnaeus, 1758) in Tunisia.
The female of the new species differs from C.
mugilis in having a smaller body at 3.79 mm (5.33 mm in C. mugilis); a genital complex which is about 1.6
times longer than the abdomen (3.2 times in C.
mugilis); an abdomen with two indistinct somites (one somite in
C. mugilis); tines of sternal furca little
divergent, slightly elongated (divergent, short tines in C. mugilis); number of teeth on mandible as 13
(12 in C. mugilis); posterolateral corners of
genital complex indistinctly lobate not extending to middle or
anterior of the abdomen (distinctly lobate, extending slightly
beyond the middle of abdomen in C. mugilis);
ratio of length/anterior margin of maxillule endopodite is 1.45 (1.1
in C. mugilis); myxal surface of maxilliped
with a slight process (absent in C. mugilis);
and ratio of first spine/third spine on fourth leg is 3.2 (3.4 in
C. mugilis). The male of the new species
could not be compared as the male of C.
mugilis was not described. The other species reported from M. cephalus is Caligus minimus
which was described on D. labrax by Otto
(1821). The female of the new species differs from C. minimus in having a smaller body 3.79 mm in
comparison with 4.38 mm in C. minimus;
genital complex is about 1.6 times longer than abdomen (2.3 times in
C. minimus); abdomen with indistinctly two
somites (one somite in C. minimus); tines of
sternal furca are little divergent, slightly elongated (slightly
divergent short in C. minimus) (Fig. 6d); number of teeth on
mandible is 13 (12 teeth in C. minimus) (Fig. 6m); posterolateral corners
of genital complex indistinctly lobate not extending to middle or
anterior of the abdomen (distinctly lobate, extend slightly beyond
one third of abdomen in C. minimus); terminal
segment of antenna and postantennal process slightly recurved
(strongly recurved in C. minimus) (Fig. 6f, h); ratio of
length/anterior margin of maxillule endopo.
Male of the new species differs from C. minimus in having a smaller body 3.67 mm (4-5
mm in C. minimus); myxal surface of
maxilliped with one small process in distal and one large bifid
process in proximal (one large process in proximal of C. minimus) (Fig. 6j); terminal segment of antenna with
quadrifid plate and a basal seta (quadrifid plate in C. minimus).
Caligus curtus was described
from Merlangius merlangus (Linnaeus, 1758) in
Denmark and Norway waters by Müller (1785). It can be distinguished
from C. turkiyensis n. sp. in having: a
greater body, 8.7 mm in comparison to 3.79 mm; a genital complex
about 2.5 times longer than the abdomen (1.6 times in C. turkiyensis n. sp.); an abdomen with one
somite (indistinctly two somites in C.
turkiyensis n. sp.); tines of sternal furca slightly divergent,
short parallel (little divergent, slightly elongated in C. turkiyensis n. sp.); number of teeth on
mandible 12 (13 teeth in C. turkiyensis n.
sp.); posterolateral corners of genital complex distinctly lobate,
extend slightly beyond one third of abdomen (indistinctly lobate not
extending to middle or anterior of the abdomen in C. turkiyensis n. sp.); terminal segment of
antenna and postantennal process strongly recurved (slightly
recurved in C. turkiyensis n. sp.); ratio of
length/anterior margin of maxillule endopodite of 0.8 (1.45 in C. turkiyensis n. sp.); and ratio of first
spine/third spine on fourth leg of 5 (3.2 in C.
turkiyensis n. sp.). Male of C. curtus
differs from C. turkiyensis n. sp. in having
a greater body of 7.93 mm in comparison to 3.67 mm in C. turkiyensis n. sp.; myxal surface of
maxilliped with one large process in both proximal and distal (one
small process in distal and one large bifid process in proximal of
C. turkiyensis n. sp.); and terminal segment
of antenna with bifid plate and a basal seta (quadrafid plate and a
basal seta in C. turkiyensis n. sp.) and
denticles on first spine of fourth leg present (absent in C. turkiyensis n. sp.). Caligus
dicentrarchi was found on D. labrax
farmed in Corsica and Sete by Cabral & Raibaut, 1986. The
female of the new species can be differentiated from C. dicentrarchi in having: a smaller body of 3.79
mm in comparison to 6.2 mm in C.
dicentrarchi; genital complex is about 1.6 times longer than
the abdomen (2.6 times in C. dicentrarchi);
abdomen with indistinctly two somites (one somite in C. dicentrarchi); tines of sternal furca little
divergent, slightly elongated (short parallel in C. dicentrarchi); number of teeth on mandible 13
(12 teeth in C. dicentrarchi); posterolateral
corners of genital complex indistinctly lobate not extending to
middle or anterior of the abdomen (distinctly lobate, extend
slightly beyond one-third of abdomen in C.
dicentrarchi); ratio of length/anterior margin of maxillule
endopodite of 1.45 (1.2 in C. dicentrarchi);
myxal surface of maxilliped with a slight process (absent in C. dicentrarchi); and ratio of first spine/third
spine on fourth leg of 3.2 (4.5 in C.
dicentrarchi). Male of the new species differs from C. dicentrarchi in having a smaller body of 3.67
mm (6.5 mm in C. dicentrarchi); myxal surface
of maxilliped with one small process in distal and one large bifid
process in proximal (one large process in proximal of C. dicentrarchi); terminal segment of antenna
with quadrifid plate and a basal seta (trifid plate in C. dicentrarchi). Boxshall (2018) classified some Caligus species in 5 groups according to a
combination of several morphological characters, such as leg 1, 2
and 4, antenna, maxilla, and abdomen of female. These groups are Caligus bonito-group, Caligus
confusus-group, Caligus diaphanus-group,
Caligus macarovi-group, and Caligus productus-group. The number of these
groups reached 7 with the revision of Caligus
pseudorhombi-group and Caligus
undulatus-group by Ohtsuka & Boxshall (2019) and Ohtsuka et al. (2020), respectively. Caligus
turkiyensis n.sp. may also be closely related to the C. macarovi-group. First and second exopodal
segments of 3-segmented leg 4 with I and III spines in this group
are the same in the new species. The proximal segment of female
antenna has a posterior process, as in this group. The new species
differs from the C. macarovi-group: female
abdomen is 2-segmented indistinctly in the new species, but group
carries 1-segmented. Distal of maxilla brachium in this group has
marginal serrations, but is absent in the new species. Structure of
setal and spinal of leg 1 in new species is similar to the rest
group. This species has also the distal exopodal segment of leg 1
bears 3 plumose setae and 4 distal elements. Spines 1-3 are all
subequal in length and seta 4 is markedly longer than spines in this
group. Spine 1 (outermost) and seta 4 are smooth and longer than
spines 2-3; spines 2 and 3 are about equal in length in new species.
Only spines 2 and 3 carry accessory processes in this group, but
spines 2 and 3 both lack accessory process and arcuated with blunt
ends. Many morphological characters of the new species are different
from the C. macarovi-group. Therefore, it is
likely that it does not belong to this group.
DISCUSSION
Caligus apodus, C. mugilis and C. pageti
have been reported mostly from countries along the Mediterranean
coast, except for one report from the Atlantic Ocean (Angola) for C. apodus and from Ireland and South Africa for C. pageti (Fig.
7). Considering the geographical distribution of these
parasites, this distribution suggests they are mostly specific to the
Mediterranean.
The Sea of Marmara, where the new species discovered
in this study was found, is a transitional area between the Black Sea
and the Mediterranean, and is under the influence of both these seas.
The Sea of Marmara has unique hydrographic, hydrological and
oceanographic features. In addition, there is a dense human population
around the Sea of Marmara and Bandırma Bay, which are then affected by
both domestic and industrial pollution (Öztürk 2021). Due to the unique environmental
characteristics of the Sea of Marmara, speciation may have occurred in
Caligus parasites in link geographical
isolation.
Caligus apodus, C. mugilis and C. pageti
have high host specificity and have been reported mostly from 5
species of mugilids: Mugil cephalus, Chelon auratus, C. labrosus,
C. ramada (Risso, 1827) and C. saliens (Risso, 1810). In addition, C. apodus has been reported from Crenimugil crenilabis (Forsskål, 1775), Planiliza carinata (Valenciennes, 1836), and Crenimugil seheli (Fabricius, 1775) in Israel by
Paperna & Overstreet (1981) (Table
III).
Apart from mullets, C. apodus
was reported from different hosts, such as the common sole, Solea solea (Linnaeus, 1758) from Iskenderun Bay,
Turkey by Özak et al. (2013). The reason why this parasite has been
reported from the common sole as well as mullets is probably because
the habitats of these hosts are similar. Common sole live in demersal
habitats, while C. labrosus and C. saliens live in demersal, M.
cephalus in benthopelagic and C. auratus
and C. ramada in pelagic-neritic habitats (Froese & Pauly 2024). Apart
from pelagic-neritic, the presence of these fish in similar habitats
increases the possibility of parasites changing hosts between mullets
and common sole.
Venmathi Maran et al. (2016) reviewed the presence and
explaining factors of caligid copepods in coastal and marine plankton.
Caligids may be found in plankton, because they escape from their
host, host switch or search for a new host, change of mode of life,
and accidental detachment from the host. This behavior supports the
possibility to be found on different hosts.
Due to their host specificity, Boualleg et al. (2011) and Ben Mansour & Ben Hassine (1998) defined C.
mugilis and C. pageti as stenoxenous
species, respectively. Ragias et al. (2004) only reported it from sea
bass, for the same reasons as above.
Caligus minimus has been
mainly reported from the North Atlantic Ocean, Mediterranean,
Adriatic, Sea of Marmara and Black Sea (Radujkovic & Raibaut 1989, Özak 2020). In addition, there are reports of C. minimus from perciforms other than sea bass,
such as Alosidae, Moronidae, Gadidae, Labridae, Mugilidae, Sparidae,
Percidae, and Sciaenidae.
The geographical distribution of C.
curtus includes the Arctic-Boreal region of the Atlantic Ocean
and contiguous waters. It is mainly a typical parasite of marine
gadids, but has been reported from marine fish from various families,
including elasmobranchs (see Parker
et al. 1968). Considering the host
specificity of C. curtus and C. minimus, they may be defined as euryxenous
parasite species.
The number of studies on species of Caligus in the Mediterranean and Aegean coasts of
Turkey is higher than in the Marmara Sea and Black Sea. Twenty of Caligus have been recorded hitherto from Turkish
Coasts, of which 19 are from Mediterranean and Aegean Coasts, 5 from
Sea of Marmara and 1 from Black Sea Sea (Özak 2020). This parasitological study still
includes species of Caligus of mullets in a
limited region. The discovery of Caligus turkiyensis
n.sp. increases the 21st species of Caligus for Turkish fauna.
Information about the host specificity, host-parasite
relationship and zoogeography of parasites of mullets is very
important from zoological and ecological point of view. Parasites
cause mass and serious fish deaths (Paperna & Lahav 1974). Infections by monoxenous
parasites such as monogenea, parasitic crustaceans are more effective
in farmed fish (Bragoni et al. 1984, Paperna 1987, Stella et al. 2023). Mullet
is the close contact of with farmed fish, which can transmit pathogens
such as parasites, viruses, bacteria, etc. to these fish and cause
infection, leading to serious economic losses (Johnson et al. 2004, Paladini et al.
2017, Assane et al. 2022). It is also important to
identify parasites for fish farming to take precautions against
possible infections in the future
CONCLUSION
Although Caligus apodus and
C. pageti were known as specific to the coasts
of the Mediterranean Sea and Aegean Sea, there are uncertainties about
the morphological characters and geographic distribution of the
caligids in the Sea of Marmara. This study presented C. apodus, C. pageti and the
morphological characters of a new species
Caligus turkiyensis n. sp.
from the sea of Marmara. Although morphological characters of this new
species are described in this study, molecular studies are needed to
confirm its species status.
Acknowledgements: The first
author gratefully acknowledges the following individuals for
technical and facility support: Dr. Mike Robertson for scientific
support, Ömer Öktener who provided the phase contrast condenser for
Olympus CH30 Light microscope, Dr. Argun Özak for criticism,
fisherman Nilufer Torpilli for helping to catch the fishes,
mechanical engineer Mr. Vedat Kızılkaya for repairing the
stereomicroscope, Dr. Olivier Brosseau for obtaining an article
about Caligus dicentrarchi and Dr. Cigdem
Akduman for providing the chemical solutions, the anonymous
reviewers and Dr. Yves Desdevises, Dr. Elodie Magnanou, Dr. Franck
Lartaud the editors, and Mrs Véronique Arnaud, Editorial Secretary
of Vie et Milieu, for the valuable, critical and helpful comments
and corrections on the manuscript. This article is dedicated to
Prf.Dr. Zbigniew Kabata, Prf.Dr. André Raibaut, and Prf.Dr. Murat
Sezgin
Indistinctly lobate, not extend to
anterior of the abdomen
Distinctly lobate, extend
slightly beyond the middle of
abdomen
Distinctly lobate, extend slightly beyond one
third of abdomen
Distinctly lobate, extend
slightly beyond one third of
abdomen
Distinctly lobate, extend slightly
beyond one third of abdomen
Terminal claw of antenna
Slightly recurved
Slightly recurved
Strongly recurved
Strongly recurved
Slightly recurved
Postantennal process
Slightly recurved
Slightly recurved
Strongly recurved
Strongly recurved
Slightly recurved
Length/ Anterior margin of maxillule endopodite
1.45 times
1.1 times
1.6 times
0.8 times
1.2 times
Process on myxal surface of
maxilliped
A slight process
Absent
Absent
A slight process
Absent
First spine/ Third spine on fourth
leg
3.2 times
3.4 times
5 times
5 times
4.5 times
Denticles on first spine of fourth
leg
Absent
Unknown
Absent
Present
Absent
Male
Length of total body
3.67 mm (3.30-4.69)
Unknown
4-5mm
7.93 mm (5.38-12.3)
6.5 mm
Process on myxal surface of
maxilliped
One small process in distal and one large bifid
process in proximal
Unknown
One large process in proximal
One large process in both proximal
and distal
One large process in proximal
Terminal segment of antenna
Quadrafid plate and a basal seta
Unknown
Quadrafid plate
Bifid plate and a basal seta
Trifid plate
1
From Raibaut & Ben Hassine (1977)
; 2
From Raibaut & Ben Hassine (1977) and Kabata
(1979)
; 3
From Parker et al. (1968); 4From Cabral & Raibaut
(1986)
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CALIGUS TURKIYENSIS N. SP. (COPEPODA: CALIGIDAE) ON
THE FLATHEAD GREY MULLET, MUGIL CEPHALUS (LINNAEUS) (MUGILIFORMES:
MUGILIDAE) FROM THE SEA OF MARMARA, TURKEY