Syst Parasitol (2009) 74:29–39
DOI 10.1007/s11230-009-9186-6
The translocated Liza haematocheila (Teleostei: Mugilidae)
as a new host of four species of Saturnius Manter, 1969
(Digenea: Hemiuridae) within its invasive range in the Black
Sea
Plamen Pankov Æ David I. Gibson Æ
Aneta Kostadinova
Received: 19 November 2008 / Accepted: 16 February 2009
Ó Springer Science+Business Media B.V. 2009
Abstract This paper presents the first documented
record of four species of Saturnius Manter, 1969 in
Liza haematocheila (Temminck & Schlegel) in its
invasive Pontic range. S. papernai Overstreet, 1977,
S. dimitrovi Blasco-Costa, Pankov, Gibson, Balbuena,
Raga, Sarabeev & Kostadinova, 2006, S. minutus
Blasco-Costa, Pankov, Gibson, Balbuena, Raga,
Sarabeev & Kostadinova, 2006 and Saturnius sp. are
described and compared with existing data by means
of multivariate morphometric analysis. The morphological and morphometric similarities between the
specimens of Saturnius sp. from L. haematocheila and
a small form of S. papernai from L. aurata indicate the
possible existence of another, cryptic species.
Although having acquired at least three species of
Saturnius since its establishment in the Black Sea
region, there is no evidence that a Pacific congener has
P. Pankov A. Kostadinova (&)
Central Laboratory of General Ecology, Bulgarian
Academy of Sciences, 2 Gagarin Street, 1113 Sofia,
Bulgaria
e-mail: Aneta.Kostadinova@uv.es
D. I. Gibson
Department of Zoology, Natural History Museum,
Cromwell Rd, London SW7 5BD, UK
A. Kostadinova
Institute of Parasitology, Biology Centre of the Czech
Academy of Sciences, Branišovská 31, 370 05 České
Budějovice, Czech Republic
been introduced with this fish. This is the first report of
S. minutus from the Black Sea.
Introduction
Liza haematocheila (Temminck & Schlegel) (syn.
Mugil soiuy Basilewsky; see e.g. Parin, 2003; Fricke
et al., 2007; Eschmeyer, 2008) is a mugilid fish native
to the Western North Pacific. Following numerous
deliberate introduction attempts to support commercial fisheries, this species established a successful
breeding population in the Sea of Azov during the
early 1980s (Occhipinti-Ambrogi & Savini, 2003) and
is now the most abundant mugilid species present
(Kottelat & Freyhof, 2007). L. haematocheila has
already become established in the north-eastern Black
Sea, where it has been subjected to commercial fishing
by Russia and the Ukraine since 1995. A small stock
has also been exploited along the Turkish coasts since
the 1990s. The environmental conditions of its Black
Sea range appear to favour this exotic species, whose
growth rate exceeds that of the native mullet species
(Okumus & Bascinar, 1997). Furthermore, its expansion in the Black Sea coincides with a decline in the
native mullet species, which it apparently replaces
(Kottelat & Freyhof, 2007). More recently, L. haematocheila has been recorded from the Aegean Sea
(Kaya et al., 1998), and Starushenko & Kazanski
(1996) have predicted its ongoing invasion towards the
Western Mediterranean.
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Syst Parasitol (2009) 74:29–39
Until the recent description of Saturnius overstreeti
Blasco-Costa, Montero, Gibson, Balbuena, Raga,
Shvetsova & Kostadinova, 2008 from the Russian
coast of the Sea of Japan (Blasco-Costa et al., 2008),
no bunocotyline hemiurids have been reported from
L. haematocheila in its native range. Domnich &
Sarabeev (1999) described Bunocotyle constrictus
Domnich & Sarabeev, 1999 from this host collected
in the Sea of Azov, which they later assumed to be a
mis-identification of Saturnius papernai Overstreet,
1977 (see Domnich & Sarabeev, 2000a, b, c, d;
Sarabeev, 2000; Sarabeev & Domnich, 2000). However, Blasco-Costa et al. (2008), based on the
re-examination of type- and voucher material, considered B. constrictus a species inquirenda and rejected
its identification as S. papernai. Material from
subsequent records of S. papernai in L. haematocheila
from the Black and/or Azov Seas (Dmitrieva &
Gaevskaya, 2001; Gaevskaya & Korniychuk, 2003)
was not described, and these records are, therefore,
questionable.
In a study of the parasites of mullets (Mugilidae)
from two localities off the Bulgarian Black Sea coast,
we collected four different forms of Saturnius Manter,
1969 from L. haematocheila. Three were identified as
S. papernai Overstreet, 1977, S. dimitrovi BlascoCosta, Pankov, Gibson, Balbuena, Raga, Sarabeev &
Kostadinova, 2006 and S. minutus Blasco-Costa,
Pankov, Gibson, Balbuena, Raga, Sarabeev & Kostadinova, 2006, whereas the fourth, Saturnius sp.,
exhibited differences from existing species of Saturnius (recently revised by Blasco-Costa et al., 2008).
This paper presents the first documented record of four
species Saturnius in L. haematocheila in its invasive
Pontic range and includes morphological descriptions
and multivariate morphometric analysis supporting
the identifications.
examined as permanent mounts in Canada balsam.
Worms from frozen fish were stored in 70% ethanol
and processed as above. Measurements are taken
from illustrations, which were made using a drawing
apparatus attached to an Olympus-BX51 microscope
at 9400 magnification. Fully-developed, non-collapsed eggs were measured using an Olympus
ColorView III digital camera and Olympus Cellp
software (ver. 2.4). All measurements are in micrometres; mean values in the text are given within
parentheses.
The data for 28 metrical variables (see e.g.
Table 1; the length of the oesophagus and egg-size
were excluded) were ln-transformed and a principal
components analysis (PCA) run to examine the
multivariate relationship between the specimens of
Saturnius ex L. haematocheila [22 specimens identified as S. minutus (n = 9), Saturnius sp. (n = 11),
S. papernai (n = 1) and S. dimitrovi (n = 1)] and
those of the dataset of Blasco-Costa et al. (2008)
[i.e. S. minutus (n = 12); S. dimitrovi (n = 26);
S. papernai ex M. cephalus (n = 31) and S. papernai
ex L. aurata (n = 36)].
The following abbreviations for ratios are used in
the text and tables: FO/BL, forebody as a percentage
of body length; LSL/BL, posteriormost pseudosegment length as a percentage of body length; LSW/
LSL, posteriormost pseudosegment width as a
percentage of its length; MFL/VSL, muscular flange
length as a percentage of ventral sucker length;
LSW/BW, posteriormost pseudosegment width as a
percentage of body width; VSW/BWVS, ventral
sucker width as a percentage of body width at the
level of the anterior margin of the ventral sucker;
MFW/BWVS, muscular flange width as a percentage of body width at the anterior border of ventral
sucker.
Materials and methods
Saturnius dimitrovi Blasco-Costa, Pankov, Gibson,
Balbuena, Raga, Sarabeev & Kostadinova, 2006
A total of 96 Liza haematocheila was collected and
examined during 2004–2005 from off the Bulgarian
Black Sea coast. Trematodes were recovered from
fresh and frozen fish. Live worms were fixed by being
pipetted into nearly-boiling saline solution (c.80°C)
and immediately transferred to 70% ethanol, stained
with iron acetocarmine, dehydrated through a series
of alcohols, cleared in dimethyl phthalate and
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Host: Liza haematocheila (Temminck & Schlegel).
Locality: River Kamchia estuary (Bulgarian Black
Sea coast).
Site: Embedded in the cardiac stomach lining.
Prevalence: 4.2%.
Intensity: 1–20 (mean 7.5).
Voucher material: BMNH 2009.1.27.5.
Syst Parasitol (2009) 74:29–39
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Table 1 Morphometric data for Saturnius minutus and Saturnius sp.
Species
S. minutus
S. minutus
Saturnius sp.
Host
Mugil cephalus
Liza haematocheila
L. haematocheila
Locality
Western Mediterranean
Black Sea (off Sozopol)
Black Sea (River Kamchia)
Source
Blasco-Costa et al. (2006)
Present study (n = 9)
Present study (n = 11)
Range
Mean
Range
Mean
Range
Mean
Body length
Body width (at ventral
sucker flange)
364–542
73–115
431
92
405–523
87–112
461
99
400–540
66–108
474
87
Body width (at anterior margin
of ventral sucker)
–
74
61–80
72
62–101
79
Forebody length
133–184
155
139–186
164
143–187
164
Oral sucker
31–54 9 39–70
41 9 56
40–53 9 50–67
45 9 57
36–58 9 32–64
50 9 53
Measurements
Ventral sucker
56–74 9 56–74
67 9 66
58–75 9 57–72
67 9 65
46–56 9 47–58
51 9 52
Pharynx
20–32 9 19–31
25 9 25
18–33 9 26–31
29 9 29
26–35 9 21–32
30 9 28
Oesophagus length
Sinus-sac
7–29
23–41 9 15–26
19
32 9 21
17–29
24–37 9 19–31
23
29 9 24
17–29
23–40 9 18–34
22
32 9 26
Pars prostatica
18–38 9 12–24
27 9 17
22–41 9 15–26
30 9 20
23–42 9 13–29
31 9 19
Seminal vesicle
12–47 9 11–37
33 9 22
28–52 9 18–40
38 9 29
21–46 9 19–41
32 9 28
Anterior testis
22–47 9 22–47
33 9 33
28–35 9 24–40
32 9 30
23–35 9 22–44
31 9 32
Posterior testis
22–45 9 20–57
34 9 35
18–38 9 21–44
30 9 33
26–43 9 22–43
34 9 29
Ovary
22–37 9 21–46
30 9 33
23–55 9 31–47
35 9 40
20–49 9 40–63
38 9 46
Vitellarium
29–64 9 22–51
42 9 37
27–53 9 32–53
43 9 42
37–63 9 32–46
50 9 40
Last pseudosegment
65–150
86 9 63
97–130 9 71–85
108 9 77
114–158 9 84–116
137 9 97
Ventral sucker flange cone
34–59
46 9 23
36–50 9 16–24
46 9 21
27–39 9 9–16
34 9 13
Eggs
19–24 9 9–12
21 9 10
–a
–a
22–27 9 11–14
24 9 13
Sucker length ratio
1:1.21–2.25
1:1.66
1:1.23–1.76
1:1.55
1:0.91–1.21
1:1.02
Sucker width ratio
1:0.90–1.82
1:1.19
1:1.07–1.37
1:1.17
1:0.78–1.56
1:1.01
BW/BL (%)
19–25
21
18–25
22
15–22
18
VSW/BWVS (%)
–
89
80–103
91
52–81
66
FO/BL (%)
MFL/VSL (%)
28–39
–
36
69
31–39
62–81
36
69
32–38
54–78
35
66
MFW/BWVS (%)
–
31
22–33
29
9–22
16
Ratios
LSL/BL (%)
17–29
20
21–26
24
26–35
29
LSW/BW (%)
–
68
71–86
78
100–135
112
LSW/LSL (%)
–
73
65–82
71
61–85
71
a
Eggs collapsed
Description (Fig. 1B)
[Based on 30 specimens. Measurements from single
well-fixed adult specimen.] Body elongate, cylindrical, 678 long, with maximum width of 121 at level of
ventral sucker flange; width at mid-level of ventral
sucker 86. Tegument unarmed, with slight longitudinal and transverse striations. Three circular muscular
flanges present around body: oral sucker flange
located at posterior level of oral sucker; strongly
developed ventral sucker flange (MFL/VSL = 85%;
MFW/BWVS = 27%) in third pseudosegment, with
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32
Fig. 1 Saturnius spp. ex
Liza haematocheila from
the Bulgarian Black Sea
coast. A. S. papernai,
ventral view; B.
S. dimitrovi, dorsal view;
C. S. minutus, dorsal view;
D. Saturnius sp., dorsal
view. Scale-bar: 200 lm
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Syst Parasitol (2009) 74:29–39
2 lateral nipple-shaped conical protuberances [cone
length (anterior-posterior) 68; width (lateral) 23];
well-developed third flange located in posterior third
of last pseudosegment.
Body with 7 pseudosegments separated by 6
transverse fibrous septa. First, second and third
pseudosegments similar in length; fourth smallest;
last largest, 194 9 89 (LSL/BL = 29%; LSW/BW =
100%). Oral sucker thick-walled, with terminal opening and flared anterior border, 61 9 74. Ventral sucker
strongly muscular (VSW/BWVS = 93%), spherical,
larger than oral sucker (sucker length ratio 1:1.31;
sucker width ratio 1:1.08), in middle third of body,
80 9 80. Forebody 195 (29% of body length). Prepharynx absent; pharynx muscular, subglobular,
40 9 37. Oesophagus thick-walled, shorter than pharynx, 27. Intestinal bifurcation just anterior to genital
pore. Caeca relatively wide, not observed posterior to
ventral sucker (masked by uterus filled with eggs).
Testes 2, subtriangular, smooth, oblique, slightly
separated; anterior testis in fifth pseudosegment,
55 9 33; posterior testis in sixth pseudosegment,
50 9 34. Seminal vesicle thick-walled, elongateoval, antero-dorsal to ventral sucker, larger than
sinus-sac, 74 9 55. Pars prostatica external, oval,
vesicular, with lining of anuclear blebs, slightly
smaller than sinus-sac, 31 9 18, surrounded by large
prostatic cells. Sinus-sac subglobular, 40 9 35, contains hermaphroditic duct lined by small cells.
Genital pore a wide transverse slit, submedian, at
level of first septum.
Ovary elongate-oval, in anterior part of last
pseudosegment, contiguous with posterior testis,
overlaps anterior margin of vitellarium, 69 9 38.
Uterine seminal receptacle present; Laurer’s canal
not observed. Vitellarium compact, elongate-oval,
large, 82 9 53. Uterus thin-walled, forms numerous
coils in hindbody. Eggs numerous (c.162), 22–25
(24) 9 11–14 (12) (n = 8).
Excretory system not visible; pore wide, terminal.
Remarks
These specimens key down to S. dimitrovi using the
key to species of Saturnius in Blasco-Costa et al.
(2008) due to the strong development of the second
muscular flange and the two anterior transverse fibrous
septa. Other characteristic features of S. dimitrovi and
these Black Sea specimens include: body with seven
33
pseudosegments separated by strongly muscular transverse septa; ventral sucker large in relation to body;
and a large saccular seminal vesicle. The metrical data
for the measured specimens from L. haematocheila
fall within the range of measurements and ratios
given for S. dimitrovi by Dimitrov et al. (1998) (as
S. papernai) and Blasco-Costa et al. (2006) with the
exception of the slightly smaller testicular width (33
and 34 vs 42–80 and 44–84 lm, respectively).
To date, S. dimitrovi has been recorded from Mugil
cephalus L., Liza aurata (Risso), L. ramado (Risso)
and Chelon labrosus (Cuvier) in the Black Sea (the
first host) and the western Mediterranean (the last
three hosts) (Dimitrov et al., 1998; Blasco-Costa
et al., 2008). L. haematocheila is a new host record
for S. dimitrovi.
Saturnius minutus Blasco-Costa, Pankov, Gibson,
Balbuena, Raga, Sarabeev & Kostadinova, 2006
Host: Liza haematocheila (Temminck & Schlegel).
Locality: Off Sozopol (Bulgarian Black Sea coast).
Site: Embedded in the cardiac stomach lining.
Prevalence: 3.1%.
Intensity: 1–8 (mean 3.7).
Voucher material: BMNH 2009.1.27.6.
Description (Fig. 1C; Table 1)
[Based on 11 worms. Measurements for 9 well-fixed,
whole-mounted adult specimens.] Body minute, elongate, cylindrical, with rounded posterior extremity and
maximum width at level of ventral sucker flange.
Tegument unarmed, with fine longitudinal and transverse striations. Three circular muscular flanges present around body: oral sucker flange weakly developed,
located posterior to mid-level of oral sucker; ventral
sucker flange strongly muscular, located in posterior
third of second pseudosegment, with 2 lateral nippleshaped conical protuberances; third flange relatively
well developed, located in posterior third of last
pseudosegment.
Body with 6 pseudosegments separated by 5 very
thin transverse fibrous septa, with anteriormost septum
being particularly thin; no septum present at level of
ventral sucker. Oral sucker simple, transverse-oval,
with slightly flared anterior border in some specimens and terminal opening. Ventral sucker strongly
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Syst Parasitol (2009) 74:29–39
6
5
S. dim itrovi
4
S. m inutus
3
Factor 2: 9.44%
2
1
0
Saturnius sp.
-1
S. papernai
ex M. cephalus
-2
S. papernai
ex L. aurata
-3
-4
-5
-14
-12
-10
-8
-6
-4
-2
0
2
4
6
8
10
12
Factor 1: 66.31%
Fig. 2 Plot of the 127 specimens of Saturnius spp. in the first plane of the PCA. Legend: S. minutus (triangles); S. dimitrovi
(diamonds); S. papernai ex Mugil cephalus (circles); ‘Small form’ of S. papernai ex Liza aurata (squares; frozen specimens in grey).
Black symbols indicate specimens from L. haematocheila in the Black Sea
muscular, subspherical, larger than oral sucker, at
about mid-body. Prepharynx absent; pharynx muscular, subspherical. Oesophagus short. Intestinal bifurcation at about mid-distance between genital pore and
pharynx. Caeca form ‘Drüsenmagen’ anterior to first
septum and cyclocoel dorsally to posterior third of
vitellarium (observed in single specimen).
Testes 2, subspherical to elongate-oval, smooth,
oblique, contiguous or slightly separated, in fourth
and fifth pseudosegments. Seminal vesicle thinwalled, elongate-oval, antero-dorsal to ventral sucker,
similar in size to or larger than sinus-sac. Pars
prostatica external, elongate-oval, similar in size to
sinus-sac, lined with anuclear blebs, surrounded by
small number of large prostatic cells. Sinus-sac thinwalled, subglobular, contains hermaphroditic duct
lined by small intensely staining cells. Genital pore a
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wide transverse slit, submedian, at level of first
septum.
Ovary oval, in anterior part of last pseudosegment,
overlaps vitellarium antero-ventrally. Uterine seminal receptacle present; Laurer’s canal not observed.
Vitellarium compact, elongate-oval. Uterus thinwalled, occupies free space in hindbody; metraterm
not seen. Eggs not numerous, large in relation to body
size.
Excretory vesicle Y-shaped; arms unite dorsally at
level of pharynx; stem subspherical; pore relatively
wide, terminal.
Remarks
This material from L. haematocehila keys down to,
and exhibits the characteristic features of, S. minutus,
Syst Parasitol (2009) 74:29–39
i.e. small size, large muscular ventral sucker, long
forebody and well-developed ventral sucker with
nipple-shaped muscular lateral cone (Blasco-Costa
et al., 2006, 2008). Comparison with the data of
Blasco-Costa et al. (2006) revealed an overlap in the
ranges for all metrical features, the material from
L. haematocheila exhibiting higher upper size limits
(and subsequently slightly higher means) for the length
of the forebody and the size of the seminal vesicle,
ovary and last pseudosegment; the latter was also
larger in relation to body size, which results in higher
means for the ratios LSL/BL and LSW/BW (Table 1).
S. minutus was originally described from
M. cephalus and has subsequently been recorded from
L. aurata and L. saliens in the Spanish Mediterranean
(Blasco-Costa et al., 2006, 2008). Our study represents
the first record of S. minutus from the Black Sea, and
L. haematocheila is a new host record for this species.
Saturnius papernai Overstreet, 1977
Host: Liza haematocheila (Temminck & Schlegel).
Locality: River Kamchia estuary (Bulgarian Black
Sea coast).
Site: Embedded in the cardiac stomach lining.
Prevalence: 8.3%.
Intensity: 1–5 (mean 2.6).
Voucher material: BMNH 2009.1.27.4.
Description (Fig. 1A)
[Based on 21 worms. Measurements for 2 well-fixed,
whole-mounted adult specimens.] Body large, elongate, cylindrical, 722–916 long, with maximum width
of 113 at level of ventral sucker flange; width at midlevel of ventral sucker 96. Tegument unarmed, with
slight longitudinal and transverse striations. Three
circular muscular flanges present around body: oral
sucker flange located at mid-level of oral sucker;
ventral sucker flange relatively poorly developed
(MFL/VSL = 117–123%; MFW/BWVS = 20–24%)
in third pseudosegment, with 2 lateral mound-shaped
conical protuberances [cone length (anterior-posterior)
63–75; width (lateral) 19–23 (MFW/VSW = 34–
39%)]; third flange well developed, located in posterior
third of last pseudosegment.
Body with 7 pseudosegments separated by 6
thick transverse fibrous septa. First and second
35
pseudosegments similar in length; fourth smallest;
last largest, 238–299 9 115–121 (LSL/BL = 33%;
LSW/BW = 102–107%). Oral sucker thick-walled,
with terminal aperture, 53–63 9 62–63. Ventral
sucker relatively small (VSW/BWVS = 58–60%),
spherical, similar in size to or smaller than oral sucker
(sucker length ratio 1:0.91–1.00; sucker width ratio
1:0.70–0.92), in middle third of body, 53–61 9
56–58. Forebody 247–305 (33–34% of body length).
Prepharynx absent; pharynx muscular, subglobular,
34–42 9 31–39. Oesophagus shorter than pharynx,
29–38. Intestinal bifurcation anterior to first septum.
Caeca relatively wide, not observed posterior to testes
(masked by uterine coils filled with eggs).
Testes 2, subtriangular, smooth, oblique, slightly
separated; anterior testis in fifth pseudosegment,
40–73 9 37–55; posterior testis in sixth pseudosegment, 47–71 9 32–59. Seminal vesicle thick-walled,
elongate-oval, antero-dorsal to ventral sucker, larger
than sinus-sac, 69–76 9 44–47. Pars prostatica external, large, 44-62 9 37–40, larger than sinus-sac,
elongate-oval, vesicular, lined with large anuclear
blebs; prostatic cells relatively large, surrounding
base of and partly overlapping sinus-sac. Sinus-sac
elongate-oval, 44–47 9 35, contains hermaphroditic
duct lined by small cells. Genital pore median, at
level of first septum.
Ovary elongate-oval to subtriangular, in anterior
third of last pseudosegment, overlaps anterior margin
of vitellarium, 66–93 9 60–71. Uterine seminal receptacle large, postero-dorsal to vitellarium; Laurer’s
canal not observed. Vitellarium compact, elongateoval, large, 50–95 9 46–93. Uterus thin-walled,
strongly developed, extends to near posterior extremity. Eggs numerous (c.167), 20–28 (23) 9 12–16 (13)
(n = 22).
Excretory system not visible; pore wide, dorsosubterminal.
Remarks
These specimens from L. haematocheila key down to
S. papernai using the key of Blasco-Costa et al. (2008)
due to: (i) the poor development of the ventral sucker
flange, with two mound-shaped protuberances visible
in lateral view; (ii) the presence of six thick transverse
fibrous septa which divide the body into seven
pseudosegments; (iii) the sucker ratios; and (iv) the
large sizes of the pars prostatica and seminal vesicle
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36
(in relation to the sinus-sac). All metrical data fall
within the ranges given for S. papernai by Overstreet
(1977) and Blasco-Costa et al. (2006, 2008).
S. papernai was originally described from Mugil
cephalus in Bardawil Lagoon (Sinai coast, Eastern
Mediterranean, see Overstreet, 1977). This description
and two recent studies (Blasco-Costa et al., 2006,
2008) represent the only documented record of this
species in the Mediterranean basin, the latter authors
adding four additional hosts (i.e. Liza aurata,
L. ramado, L. saliens and Chelon labrosus). L.
haematocheila is a new host record for S. papernai.
Saturnius sp.
Host: Liza haematocheila (Temminck & Schlegel).
Locality: River Kamchia estuary (Bulgarian Black
Sea coast).
Site: Embedded in the cardiac stomach lining.
Prevalence: 0.9%.
Intensity: 123.
Voucher material: BMNH 2009.1.27.1-3.
Description (Fig. 1D; Tables 1, 2)
[Based on 25 worms. Measurements for 11 dorsoventrally mounted adult specimens.] Body minute,
elongate-oval, with rounded posterior extremity and
maximum width at mid-level of last pseudosegment.
Tegument unarmed, with longitudinal and transverse
striations. Three circular muscular flanges present
around body: oral sucker flange poorly developed,
located at mid-level of oral sucker (when protruded;
n = 2); ventral sucker flange small, located in middle
of second pseudosegment, with 2 lateral moundshaped conical protuberances; third flange well
developed, located just posterior to mid-length of
last pseudosegment.
Body with 7 pseudosegments separated by 6 thick
transverse fibrous septa. Oral sucker simple, subglobular, with terminal opening. Ventral sucker muscular,
spherical, similar in size to or larger than oral sucker,
in middle third of body. Prepharynx absent; pharynx
muscular, subspherical. Oesophagus short. Intestinal
bifurcation at level of genital pore. ‘Drüsenmagen’
and cyclocoel not seen.
Testes 2, subspherical, smooth, oblique, contiguous or slightly separated, in fourth and fifth
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Syst Parasitol (2009) 74:29–39
pseudosegments. Seminal vesicle thick-walled, subspherical, antero-dorsal to ventral sucker, similar in
size to sinus-sac. Pars prostatica external, elongateoval, similar in size to sinus-sac, lined with anuclear
blebs, surrounded by large number of large prostatic
cells. Sinus-sac thick-walled, subglobular, contains
eversible hermaphroditic duct lined by relatively
large intensely staining cells. Genital pore median, at
level of first septum.
Ovary transversely elongate-oval, in anterior third
of last pseudosegment, overlaps vitellarium anteroventrally. Uterine seminal receptacle present; Laurer’s
canal not observed. Vitellarium compact, elongateoval. Uterus thin-walled, occupies almost entire hindbody; metraterm not seen. Eggs numerous, large in
relation to body size.
Excretory system not observed; pore wide, dorsosubterminal.
Remarks
This material from L. haematocheila exhibits the
diagnostic characteristics of Saturnius and keys down
to S. papernai using the key to species of BlascoCosta et al. (2008) due to: the less well-developed
ventral sucker flange with mound-shaped lateral
cones; the body divided into seven pseudosegments;
similar sucker ratios; and a sinus-sac similar in size to
the pars prostatica and seminal vesicle. However, the
specimens studied, which we denote as ‘Saturnius
sp.’ here, are on average only half the size of those
recently described from mullets in both the Mediterranean and Black Seas (Blasco-Costa et al., 2006),
with the measurements for a number of features
varying outside the lower limits for S. papernai.
Examples of the latter are: the size of the body, oral
sucker, testes and ventral sucker flange; the length of
the forebody, pars prostatica and seminal vesicle; and
the width of the ventral sucker and vitellarium. A
further set of metrical characters exhibits smaller
lower limits in Saturnius sp.: the size of the sinus-sac
and ovary; the width of the body at the mid-level of
the ventral sucker, pars prostatica and seminal
vesicle; and the length of the vitellarium and last
pseudosegment. Finally, the ventral sucker and the
last pseudosegment in Saturnius sp. are larger in
relation to body size, which result in higher upper
limits and means for the ratios VSW/BWVS, LSW/
LSL and LSW/BW (Table 2).
Syst Parasitol (2009) 74:29–39
37
Table 2 Comparative data for S. papernai and Saturnius sp.
Species
S. papernai
Saturnius sp.
Blasco-Costa et al. (2006)
S. papernai (small form,
frozen material)
Blasco-Costa et al. (2008)
Source
Range
Range
Range
Mean
Present study (n = 11)
Mean
Measurements
Body length
687–1,183
994
454–593
400–540
474
Body width (at ventral
sucker flange)
107–165
141
81–104
66–108
87
Body width (at anterior
margin of ventral sucker)
95–136
119
72–93
62–101
79
Forebody length
240–412
326
160–233
143–187
164
Oral sucker
55–91 9 57–91
71 9 78
38–57 9 38–56
36–58 9 32–64
50 9 53
Ventral sucker
47–79 9 57–84
66 9 73
38–47 9 44–62
46–56 9 47–58
51 9 52
Pharynx
27–65 9 27–48
44 9 40
25–37 9 23–33
26–35 9 21–32
30 9 28
Oesophagus length
–
37
–
17–29
22
Sinus-sac
37–74 9 27–45
54 9 37
29–39 9 19–31
23–40 9 18–34
32 9 26
Pars prostatica
40–77 9 23–54
62 9 38
37–49 9 16–28
23–42 9 13–29
31 9 19
Seminal vesicle
52–109 9 32–81
82 9 57
33–67 9 23–45
21–46 9 19–41
32 9 28
Anterior testis
Posterior testis
34–113 9 44–94
38–105 9 42–105
72 9 67
73 9 70
23–53 9 19–52
24–59 9 24–58
23–35 9 22–44
26–43 9 22–43
31 9 32
34 9 29
Ovary
42–101 9 36–120
62 9 71
28–44 9 32–48
20–49 9 40–63
38 9 46
Vitellarium
45–124 9 50–103
87 9 76
37–61 9 26–56
37–63 9 32–46
50 9 40
Last pseudosegment
176–358 9 80–173
278 9 141
120–160 9 81–105
114–158 9 84–116
137 9 97
Ventral sucker flange cone
46–91 9 19–36
65 9 28
35–54 9 12–21
27–39 9 9–16
34 9 13
Eggs
21–26 9 9–14
24 9 12
20–26 9 10–15
22–27 9 11–14
24 9 13
Ratios
Sucker length ratio
1:0.91–0.92
1:0.93
1:0.7–1.1
1:0.91–1.21
1:1.02
Sucker width ratio
1:0.70–1.20
1:0.95
1:0.9–1.3
1:0.78–1.56
1:1.01
BW/BL (%)
12–19
14
15–19
15–22
18
VSW/BWVS (%)
52–71
61
55–68
52–81
66
FO/BL (%)
30–37
33
34–42
32–38
35
MFL/VSL (%)
76–118
99
77–123
54–78
66
MFW/BWVS (%)
17–32
23
13–26
9–22
16
MFW/VSW (%)
28–49
–
21–39
17–30
24
LSL/BL (%)
LSW/LSL (%)
25–35
31–72
28
51
23–30
60–78
26–35
61–85
29
71
LSW/BW (%)
51–120
101
94–114
100–135
112
However, the material described above resembles
the ‘small form’ of S. papernai from L. aurata
distinguished by Blasco-Costa et al. (2008) in its
longer forebody, relatively wider last pesudosegment,
and the size of the body and most other metrical
features. A morphometrical comparison between the
present specimens, originating from a single frozen
fish, and the frozen material of Blasco-Costa et al.
(2008) revealed slightly higher upper limits of variation in the latter for the size of the testes and muscular
flange at ventral sucker level (also in relation to the
body and ventral sucker width, i.e. MFW/BWVS and
MFW/VSW), and the lengths of the forebody, pars
prostatica and seminal vesicle (Table 2).
A comparison with S. minutus is also necessary
here, especially because of the small size of the worms
123
38
from L. haematocheila (body length \550 lm).
Although many metrical features exhibit a range
overlap, Saturnius sp. can be clearly distinguished
from this species by having: a body comprised of
seven pseudosegments formed by six strongly developed fibrous septa; a less developed ventral sucker
flange (also narrower in relation to the body, see
MFW/BWVS in Table 1); a distinctly smaller ventral
sucker (also in relation to the body size, resulting in
values for VSW/BWVS below the lower range of
S. minutus); a much larger posterior segment; and
larger eggs.
Saturnius sp. resembles the third species parasitising mullets in the Mediterranean basin, S. dimitrovi, in the number of septa/pseudosegments, but
differs in the remaining distinguishing features listed
in the comparison with S. minutus above. Overall, the
above comparisons suggest that Saturnius sp. and the
‘small form’ of S. papernai ex L. aurata described by
Blasco-Costa et al. (2008) may in fact represent a
new species more closely related to S. papernai than
to the other Mediterranean species of Saturnius.
However, the lack of ample, well-fixed material
prevents its delineation at present.
Statistical comparisons
The first two principal components of a PCA run
using the correlation matrix between 28 metrical
variables of the 127 specimens of Saturnius in the
combined dataset explained 75.7% of the variation in
the data-set. The length of the body, forebody and last
pseudosegment, as well as body width at both the
anterior margin of the ventral sucker and the ventral
sucker muscular flange, exhibited a greater contribution to the separation along the first axis, which
explained 66.3% of the total variance, whereas the
size of ventral sucker and ventral sucker flange had
important contributions to the second principal component, explaining a further 9.4% of the variance. A
plot of the specimens in the first plane of the PCA
shows three well-separated groups that correspond to
the three Mediterranean species of Saturnius; these
included the specimens from L. haematocheila identified as S. dimitrovi, S. minutus and S. papernai. The
specimens of Saturnius sp. grouped together with the
specimens of S. papernai denoted as the ‘small form
ex L. aurata’ in Blasco-Costa et al. (2008) (Fig. 2).
123
Syst Parasitol (2009) 74:29–39
As in the latter study, no clear hiatus exists in the
two-dimensional plane between the samples from
M. cephalus, L. aurata and L. haematocheila.
Concurrent infections
Although the overall prevalence of infection of
L. haematocheila with Saturnius spp. was low
(13.5%), the frequency of concurrent infections was
quite high (38%). Thus combinations of two species
(S. papernai ? S. dimitrovi and S. papernai ?
S. minutus) were found in each of two fish (of 13
infected) and one fish harboured individuals of
three species (5 S. papernai, 20 S. dimitrovi and 8
S. minutus). To the best of our knowledge, this is the
first record of co-occurrence of Saturnius spp. in
individual fish. Blasco-Costa et al. (2008) compared
the prevalence patterns of the three Saturnius spp. in
a large sample (676 fish) from the western Mediterranean and indicated that S. dimitrovi and S. minutus
attain their highest prevalence in M. cephalus in two
different ecosystems and that S. papernai reaches a
maximum prevalence in L. aurata; no concurrent
infections were reported in the latter study. It is,
therefore, possible that our data reflect a trophic
overlap between L. haematocheila and both M.
cephalus and Liza spp. in the Black Sea.
Concluding remarks
This increased sampling effort and detailed morphological study have revealed that Liza haematocheila
has acquired at least three species of Saturnius in its
invasive range, and that this example of transfaunation does not appear to have introduced any Pacific
species, such as S. overstreeti, into the Pontic region.
However, the levels of infection of this host along the
Bulgarian Black Sea coast are rather low. Further
sampling and re-identification of existing material
from other regions of the Black Sea may reveal the
patterns of exchange of Saturnius spp. between
the sympatric mullet populations and the role of
L. haematocheila in the cycling of these parasites
in the local communities. The morphological and
morphometric similarity between the specimens of
Saturnius sp. from L. haematocheila and the small
form of S. papernai from L. aurata indicates the
Syst Parasitol (2009) 74:29–39
possible existence of a cryptic species whose delineation might be enhanced by a molecular study.
Acknowledgements This study was supported by Institute of
Parasitology (Academy of Sciences of the Czech Republic)
(grants Z60220518 and LC522 to AK); and the material was
collected within the framework of an INTAS project (03-515998).
References
Blasco-Costa, I., Pankov, P., Gibson, D. I., Balbuena, J. A.,
Raga, J. A., Sarabeev, V. L., et al. (2006). Saturnius
minutus n. sp. and S. dimitrovi n. sp. (Digenea: Hemiuridae) from Mugil cephalus L. (Teleostei: Mugilidae),
with a multivariate morphological analysis of the Mediterranean species of Saturnius Manter, 1969. Systematic
Parasitology, 65(7), 7–91.
Blasco-Costa, I., Montero, F. E., Gibson, D. I., Balbuena, J. A.,
Raga, J. A., Shvetsova, L. S., et al. (2008). A revision
of the species of Saturnius Manter, 1969 (Digenea:
Hemiuridae), parasites of mullets (Teleostei: Mugilidae).
Systematic Parasitology, 71, 53–74.
Dimitrov, G. I., Arapoglou, F. K., & Georgiev, B. B. (1998).
First record of Saturnius papernai Overstreet, 1977 in the
Black Sea, with a review of the genus Saturnius Manter,
1969 (Digenea, Bunocotylidae). Systematic Parasitology,
40, 43–48.
Dmitrieva, E. V., & Gaevskaya, A. V. (2001). Parasitological
aspects of mugilids mariculture and of their introduction
into the Sea of Azov and the Black Sea. Ekologiya Morya,
Kiev, 55, 73–78. (In Russian).
Domnich, I. F., & Sarabeev, V. L. (1999). Trematodes of the
genus Bunocotyle (Trematoda, Halipegidae) from the
haarder (Mugil so-iuy) acclimatized in the Azov Sea.
Parazitologiya, 33, 67–70. (In Russian).
Domnich, I. F., & Sarabeev, V. L. (2000a). Forming of the
parasitic fauna of the pilengas in the Azov Sea. Acta
Parasitologica, 45, 265–266.
Domnich, I. F., & Sarabeev, V. L. (2000b). The trematodes of
the Far-East-mullet-pelingas (Mugil soiuy) in the Azov
Sea aquatories. Vestnik Zoologii, 34, 7–15. (In Russian).
Domnich, I. F., & Sarabeev, V. L. (2000c). Contemporary
fauna of fish parasites in the northern part of the Azov
Sea. Visnik Zaporiz’kogo Derzhavnogo Universitetu, 1,
224–230. (In Ukrainian).
Domnich, I. F., & Sarabeev, V. L. (2000d). Parasitic fauna
structure of the pilengas in the Azov Sea. Acta Parasitologica, 45, 268.
Eschmeyer, W. N. (2008). Catalog of fishes electronic version
(updated 23 April 2008). [http://www.calacademy.org/
research/ichthyology/catalog/fishcatsearch.html].
39
Fricke, R., Bilecenoglu, M., & Musa Sari, H. (2007).
Annotated checklist of fish and lamprey species
(Gnathostomata and Petromyzontomorphi) of Turkey,
including a Red List of threatened and declining species.
Stuttgarter Beiträge zur Naturkunde. Ser A (Biologie),
706, 1–174.
Gaevskaya, A. V., & Korniychuk, Y. M. (2003). Parasitic
organisms as a component of ecosystems of the Black Sea
near-shore zone of Crimea. In V. N. Eremeev & A. V.
Gaevskaya (Eds.), Modern condition of biological diversity in near-shore zone of Crimea (Black Sea sector)
(pp. 425–490). Sevastopol: EKOSI-Gidrophizika.
Kaya, M., Mater, S., & Korkut, A. Y. (1998). A new grey
mullet species ‘‘Mugil so-iuy Basilewsky’’ (Teleostei:
Mugilidae) from the Aegean Coast of Turkey. Turkish
Journal of Zoology, 22, 303–306.
Kottelat, M., & Freyhof, J. (2007). Handbook of European
freshwater fishes. Cornol, Switzerland: Publications
Kottelat, 646 pp.
Occhipinti-Ambrogi, A., & Savini, D. (2003). Biological invasions as a component of global change in stressed marine
ecosystems. Marine Pollution Bulletin, 46, 542–551.
Okumus, I., & Bascinar, N. (1997). Population structure,
growth and reproduction of introduced pacific mullet,
Mugil soiuy, in the Black Sea. Fisheries Research, 33,
131–137.
Overstreet, R. M. (1977). A revision of Saturnius Manter, 1969
(Hemiuridae: Bunocotylinae) with descriptions of two
new species from the striped mullet. In: Excerta parasitológica en memoria del doctor Eduardo Caballero y
Caballero. Instituto de Biologı´a, Universidad Nacional
Autónoma de Me´xico. Publicaciones Especiales, 4,
273–284.
Parin, N. V. (2003). An annotated catalogue of fish-like vertebrates and fishes of the seas of Russia and adjacent
countries: Part 3. Orders Perciformes (excluding suborders Gobioidei, Zoarcoidei and Stichaeoidei) and Tetraodontiformes. Voprosy Ikhtiologii, 43 (Suppl 1), S1–S40.
Sarabeev, V. L., & Domnich, I. F. (2000). Age-related
dynamics of parasitic infection of the pilengas (Mugil
soiuy) in the Molochny Estuary of the Sea of Azov.
Vestnik Zoologii, 14, 6–12. (In Russian).
Sarabeev, V. (2000). [Seasonal dynamics of the parasitic
infection of the pilengas in the northern part of the Azov
Sea.]. In: Materials of the international scientific conference of young scientists. Aquatic biological resources and
ways of their rational use. Kiev, pp. 97–98. (In Russian).
Starushenko, L. I., & Kazanski, A. B. (1996). Introduction of
mullet haarder (Mugil so-iuy Basilewsky) into the Black
Sea and the Sea of Azov. General Fisheries Council for
the Mediterranean. Studies and Reviews, 67, 1–29.
123