Download Parasites of wild European sea bass Dicentrarchus labrax

ITTIOPATOLOGIA, 2010, 7: 123-133
Parasites of wild European sea bass
Dicentrarchus labrax (Linnaeus, 1758) from St. Gilla lagoon
(Sardinia, South western Mediterranean)
Parassiti in spigole selvatiche
Dicentrarchus labrax (Linnaeus, 1758) della laguna
di Santa Gilla (Sardegna, Mediterraneo sud-occidentale)
Jacopo Culurgioni 1*, Riccardo De Murtas 2,
Simonetta Cannella 1, Vincenza Figus 1
1
Dipartimento di Biologia Animale ed Ecologia, Università di Cagliari, via T. Fiorelli, 1 - 09126 Cagliari;
2
Consorzio Ittico di Santa Gilla, Località Sa Illetta, Strada Statale 195, Km. 3,500 - 09122 Cagliari.
_______________________________
SUMMARY – In a preliminary survey (February - April 2010) of 25 wild European sea bass Dicentrarchus
labrax (Linnaeus, 1758) from St. Gilla lagoon seventeen parasite taxa were found. The metazoan detected were:
the copepods Lernanthropus kroyeri and Caligus minimus; the monogenean Diplectanum aequans; the digeneans
Bucephalus labracis, B. baeri, B. minimus, Timoniella imbutiforme, T. praeterita, Cainocreadium labracis,
Monascus sp., Galactosomum lacteum; the nematodes Contracaecum rudolphii L3 and adults of Philometra sp.;
Cestoda Tetraphyllidaea larvae; the acanthocephalans Acanthocephaloides propinquus and Southwellina hispida.
The only myxosporean parasite observed was Henneguya sp. (Myxozoa). The results show that the parasite
infections were due mainly to the monogenean D. aequans (P% = 96.0). Henneguya sp., Monascus sp.,
G. lacteum and S. hispida are firstly reported in wild European sea bass.
RIASSUNTO – In uno studio preliminare (Febbraio – Aprile 2010) riguardante 25 spigole selvatiche
Dicentrarchus labrax (Linnaeus, 1758) pescate nella laguna di S.ta Gilla, sono stati individuati 17 taxa di
parassiti. I metazoi riscontrati sono stati: i copepodi Lernanthropus kroyeri e Caligus minimus; il monogeneo
Diplectanum aequans; i digenei Bucephalus labracis, B. baeri, B. minimus, Timoniella imbutiforme, T. praeterita,
Cainocreadium labracis, Monascus sp., Galactosomum lacteum; larve L3 del nematode Contracaecum rudolphii e
adulti di Philometra sp.; larve di Cestoda Tetraphyllidaea; gli acantocefali Acanthocephaloides propinquus e
Southwellina hispida. Il solo mixosporidio osservato è stato Henneguya sp. (Myxozoa). I dati raccolti mostrano
che le infezioni hanno riguardato principalmente il monogeneo D. aequans (P% = 96,0). La presenza di
Henneguya sp., Monascus sp., G. lacteum e S. hispida è riportata per la prima volta in spigole selvatiche.
Key words – Dicentrarchus labrax; European sea bass; Metazoan parasites; Contracaecum rudolphii;
Myxosporea; South western Mediterranean; Santa Gilla lagoon.
______________________________
* Corresponding Author: c/o Dipartimento di Biologia Animale ed Ecologia, Via T. Fiorelli, 1 - 09126 Cagliari.
Tel.: 070-6758057; E-mail: [email protected].
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INTRODUCTION
The European sea bass Dicentrarchus labrax (Linnaeus, 1758) (Moronidae) is an
euryhaline and eurythermic marine fish, distributed in Eastern Atlantic from Norway to
Senegal, and in the Mediterranean basin. During the breeding season, Mediterranean stocks
are able to over-winter near to river mouths or estuaries or lagoons. It is one of the most
appreciated fish in Europe and in Mediterranean area, particularly in Italy, where it is usually
fished by line and trammel net, as in St. Gilla lagoon. In this area, the mean annual amount
of D. labrax fished in the last six years is about 1,600 kg (official data restricted to the
fishing activity of the “Consorzio Ittico di Santa Gilla”).
In order to meet its great demand, this species is successfully cultured in lagoons and
brackish valleys by extensive farming, as in offshore and inshore cages with intensive
techniques. Because of its economic importance, a lot of attention is given to the parasitic
infections of wild and farmed European seabass in Mediterranean (Paperna & Baudin
Laurencin, 1979; Čož-Rakovac et al., 2002; Mladineo, 2005; Fioravanti et al., 2006; Bartoli
& Boudouresque, 2007).
In Sardinia, a parasitological survey was pursued in specimens of D. labrax farmed in cage
located in north, east and west coast (Merella et al., 2006) but to date there are no detailed
reports on parasitic communities of wild specimens of southern Sardinian lagoons.
Therefore, the aim of this study was to describe and to characterize the parasite species of
sea bass inhabiting the St. Gilla lagoon (Sardinia, South western Mediterranean).
MATERIALS AND METHODS
From February to April 2010 a total of 25 European sea bass were examined for metazoan
and protozoan parasites. The samples were fished in the St. Gilla lagoon (South Sardinia).
The specimens were transported to the laboratory, measured, weighed and sexed, then
examined by necropsy. Parasitological inspection of the skin, gills, viscera, abdominal cavity
and muscles was performed. Parasites were collected, processed by standard methods for
light microscopy, identified, counted and preserved in 70% or 90% ethanol or AFA
(Alcohol, Formalin and Acetic Acid). Prevalence (%) and its confidence interval, mean
intensity (MI) ± SE and mean abundance (A) ± SE were calculated according to Bush et al.,
(1997).
RESULTS
Seventeen parasite taxa, thirteen of which identified to the species level, were recorded. All
the examined fishes were infected by at least three parasite species, reaching 100% of total
prevalence of infection. Their list, life stage and the site of infection in the hosts are reported
in Table 1.
The only myxozoan parasite detected was the Myxosporea Henneguya sp., infecting the
bulbus arteriosus of the 12.0% of fish examined (Figures 1; 2). This is the first report of this
myxosporean parasite in wild European sea bass.
The ectoparasites were represented by the monogenean Diplectanum aequans (Wagener,
1857) which showed the highest prevalence of infection (96.0%). The mean intensity of this
infection was 17.0, ranging from 1 to 112 parasites per host. Two copepod species were
found: Lernanthropus kroyeri van Beneden, 1851 attached to the gill filaments (P% = 76.0)
and Caligus minimus Otto, 1821 in the mouth cavity and on the gill arches (P% = 20.0).
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N. of sea bass
25
Length range (cm)
17.3-59
Weight range (g)
49-2498
PARASITE
Stage
Site
P% (CI)
MI ± SE
IR
A ± SE
20.0 (8.2-39.8)
4.2 ± 1.8
1-10
0.8 ± 0.5
Crustacea
Caligus minimus
J, A M, GA
A
GF
76.0 (56.1-89.0)
5.4 ± 0.7
1-11
4.1 ± 0.7
J, A
GF
96.0 (80.4-99.8)
17.0 ± 5.0
1-112
16.3 ± 4.8
Bucephalus labracis
A
AI
24.0 (11.0-43.9)
3.8 ± 2.3
1-15
0.9 ± 0.6
Bucephalus baeri
A
PI
8.0 (1.5-25.6)
1.0 ± 0.0
1
0.1 ± 0.1
Bucephalus (Labratrema)
minimus
Cainocreadium labracis
A
AI, MI
36.0 (19.6-56.1)
6.0 ± 2.0
1-17
2.2 ± 0.9
A
MI, PI
36.0 (19.6-56.1)
14.1 ± 6.7
1-60
5.1 ± 2.7
Timoniella imbutiforme
A, MC
PI
52.0 (31.7-70.4)
3.3 ± 1.4
1-20
1.7 ± 0.8
Timoniella praeterita
A
PC
20.0 (8.2-39.8)
1.4 ± 0.4
1-3
0.3 ± 0.1
Monascus sp.
A
PI
4.0 (0.2-19.6)
1.0
1
0.0 ± 0.0
Galactosomum lacteum
MC
MI
4.0 (0.2-19.6)
1.0
1
0.0 ± 0.0
P
AI, MI
8.0 (1.5-25.6)
1.0 ± 0.0
1
0.1 ± 0.1
Contracaecum rudolphii
L3
IW, AC
92.0 (10.4-47.5)
80.6 ± 21.8
1-327
74.1 ± 20.5
Philometra sp.
A
O
8.0 (1.5-25.6)
9.0 ± 6.0
3-15
0.7 ± 0.6
Acanthocephaloides propinquus
A
MI, PI
24.0 (11.0-43.9)
3.3 ± 0.9
1-16
1.5 ± 0.7
Southwellina hispida
C
AC
8.0 (1.5-25.6)
2.0 ± 1.0
1-3
0.2 ± 0.1
S
BA
12.0 (3.4-30.6)
-
-
-
Lernanthropus kroyerii
Monogenea
Diplectanum aequans
Digenea
Cestoda
Tetraphyllidea sp.
Nematoda
Acanthocephala
Myxosporea
Henneguya sp.
TOTAL
100 (86.7-100)
109.2 ± 21.5 13-400 109.2 ± 21.5
Table 1 - Parasites of wild sea bass Dicentrarchus labrax from St. Gilla lagoon.
P%: prevalence; CI: confidence interval; MI: mean intensity; IR: intensity range; A: abundance; SE: standard error. A: adult;
C: cystacanth; J: juvenile; L3: third-stage larva; MC: metacercaria; P: plerocercoid; S: spore. AI: anterior intestine;
AC: abdominal cavity; BA: bulbus arteriosus; GA: gill arch; GF: gill filament; IW: intestinal wall; M: mouth; MI: middle
intestine; O: ovary; PC: pyloric caeca; PI: posterior intestine.
Tabella 1 - Parassiti di spigole (Dicentrarchus labrax) selvatiche della laguna di Santa Gilla.
P%: prevalenza; CI: limiti fiduciali; MI: intensità media; IR: intervallo di intensità; A: abbondanza; SE: errore standard.
A: adulto; C: cistacanto; J: giovanile; L3: larva al 3° stadio; MC: metacercaria; P: plerocercoide; S: spora. AI: intestino
anteriore; AC: cavità addominale; BA: bulbus arteriosus; GA: arco branchiale; GF: filamento branchiale; IW: parete
intestinale; M: bocca; MI: intestino medio; O: ovario; PC: ciechi pilorici; PI: intestino posteriore.
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1
3
5
2
4
6
Figure 1 - Heart of sea bass infected by Henneguya sp. on the bulbus arteriosus. Figure 2 - Henneguya sp.: spores
with their typical two caudal appendages. Figure 3 - Timoniella imbutiforme: adult found in the posterior
intestine. Figure 4 - Timoniella praeterita: adult extracted from a pyloric caecum. Figure 5 - Sea bass abdominal
cavity heavily infected by Contracaecum rudolphii L3 larvae. Figure 6 - Southwellina hispida: cystacanth from
the abdominal cavity.
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Figura 1 - Cuore di spigola infetto da Henneguya sp. nel bulbus arteriosus. Figura 2 - Henneguya sp.: spore
caratterizzate da due appendici caudali. Figura 3 - Timoniella imbutiforme: adulto ritrovato nell’intestino
posteriore. Figura 4 - Timoniella praeterita: adulto estratto da un cieco pilorico. Figura 5 - Cavità addominale
di spigola pesantemente infestata da larve L3 di Contracaecum rudolphii. Figura 6 - Southwellina hispida:
cistacanto da cavità addominale.
Among endoparasites, 8 species of Digenea, 2 of Nematoda, 2 of Acanthocephala and 1
species of Cestoda larva belonging to Tetraphyllidea were found.
Digenea was the most represented taxa with 7 adult and/or preadult species, one of which
detected also as metacercaria, and 1 larval metacercaria. Within this group, the Bucephalidae
were Bucephalus (syn. Labratrema) minimus (Stossich, 1887) Maillard, 1975, localized in
the anterior and middle portion of the intestine (P% = 36.0); B. labracis Paggi and Orecchia,
1965, observed mainly in the pyloric portion of the gut with a prevalence of 24.0%; B. baeri
Maillard and Saad-Fares, 1981, in the rectum (P% = 8.0).
Two species of Acanthostominae (Cryptogonimidae), Timoniella imbutiforme (Molin,
1859) Brooks, 1980 (Figure 3) and T. praeterita (Looss, 1901) Maillard, 1974 (Figure 4)
were found as adults in the rectum/posterior intestine (P% = 52.0) and in the pyloric
caeca/anterior intestine (P% = 20.0) respectively. T. imbutiforme was also found as
metacercaria in the pharynx musculature of one fish.
Adults of Cainocreadium labracis (Dujiardin, 1845) Nicoll, 1909 (Opecoelidae) were
detected mainly in the rectum, while sexually immature specimens were observed in the
middle intestine, with a total prevalence of 36.0% and a mean intensity of 14.1.
One preadult specimen of Monascus sp. Looss, 1907 (Fellodistomidae) infected the rectum
of one fish, as one metacercaria of Galactosomum lacteum (Jägerskiöld, 1896)
(Heterophyidae) was detected in the middle intestine of another sea bass.
Plerocercoids of Cestoda Tetraphyllidea were detected in the anterior and middle intestine
of 8.0% of sea bass.
Two taxa of Nematoda were individuated: Contracaecum rudolphii Hartwich, 1964
L3 (Anisakidae) were observed in the posterior intestine wall, on the viscera, and more
heavily in the connective tissues of the visceral cavity (Figure 5). This infection showed a
prevalence of 92.0% and a mean intensity of 80.6.
Adults of the genus Philometra Costa, 1845 (Philometridae) occurred in the ovaries of two
D. labrax (P% = 8.0), with a mean intensity of 9.0.
Two Acanthocephala species were observed: adults of Acanthocephaloides propinquus
(Dujiardin, 1845) (Arhythmacanthidae) in the posterior intestine of the 24.0% of examined
fish, and cystacanths of Southwellina hispida (Van Cleave, 1925) Wittenberg, 1932
(Polymorphidae) (Figure 6) adhering to the intestinal mesenteries with a prevalence of
16.7%.
DISCUSSION AND CONCLUSION
Results obtained in this study indicate that all the parasite species recognized in D. labrax
from St. Gilla lagoon were already reported in specimens from different areas of
Mediterranean Sea, except for Henneguya sp., G. lacteum, Monascus sp., and S. hispida,
new records for Mediterranean sea bass populations.
Myxosporean infections reported in Mediterranean wild and farmed sea bass are those by
Myxobilatus sp., Sphaerospora dicentrarchi, S. testicularis, Ceratomyxa labracis,
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C. diplodae, Enteromyxum leei (Alvarez-Pellitero & Sitjá-Bobadilla, 1993; Fioravanti et al.,
2006; Merella et al., 2006).
There are no previous references to the presence of the genus Henneguya in European sea
bass, while the species H. lateolabracis was described in the Chinese sea bass Lateolabrax
sp. as the causative agent of cardiac henneguyosis (Yokoyama et al., 2003). The same genus
was observed in other teleosts worldwide (Moser & Love, 1975; Meyers et al., 1977;
Yokoyama et al., 2005), and in Mediterranean Symphodus tinca (Bahri et al., 2010) and
Sparus aurata (Caffara et al., 2003). In north Sardinia, Henneguya sp. was already reported
by Merella et al. (2006) in cultured inshore S. aurata.
The occurrence of the Copepoda L. kroyeri attached to the gills, and of C. minimus in the
mouth cavity was observed. L. kroyeri is a new finding in wild D. labrax from the south
western Mediterranean while its presence was already reported in farmed specimens from
different areas, mainly of the eastern Mediterranean and the Aegean Sea (Manera & Dezfuli,
2003; Özel et al., 2004; Tokşen et al., 2008).
The monogenean D. aequans resulted the dominant species, with the prevalence of 96.0%,
higher than those of 80.2% and 24.2% detected by Merella et al. (2006) in farmed sea bass
respectively in northern and eastern Sardinia. Values of prevalence considerably lower have
been reported also in farmed and wild D. labrax from the Adriatic Sea (Gonzalez-Lanza et
al., 1991; Čož-Rakovac et al., 2002; Mladineo, 2005; Fioravanti et al., 2006).
Among Digenea the three congeneric species detected, B. baeri, B. minimus and
B. labracis were already observed in Mediterranean sea bass (Paggi & Orecchia, 1965;
Maillard & Saad-Fares, 1981; Muñoz et al., 1989). B. baeri and B. labracis, morphologically
very similar, were distinguished according to Maillard & Saad-Fares (1981) by the length of
excretory vesicle and their different localization in the host’s digestive tract. In St. Gilla
lagoon, metacercariae of B. labracis were observed in the muscular tissue of Liza aurata and
L. saliens (Culurgioni et al., 2010a) and the same larval stages of B. baeri and B. labracis
were detected in the heart of Sparus aurata (unpublished data). Regarding B. minimus, its
occurrence in this sample of D. labrax was expected, since the metacercarial stage was
observed in several teleost species living in St. Gilla as Aphanius fasciatus, Atherina boyeri,
Gobius niger, G. paganellus (Figus et al., 2002; D’Amico et al., 2007; 2008), as the
sporocysts and cercariae were found infecting the bivalve Cerastoderma glaucum
(Culurgioni et al., 2006).
Adults and sexually immature specimens of C. labracis (Dujiardin, 1845) Nicoll, 1909
were classified according to the morphologic features reported by Jousson & Bartoli (2001).
These flukes were detected in the 36% of fish examined, particularly in the middle and
posterior portion of the intestine, with the highest mean intensity (14.1) among digenean
species. The site of infection and the values of prevalence and intensity observed in this
study differ from those reported by Bartoli et al. (2005) in Scandola Nature Reserve
(Corsica) who found this parasite in duodenum and middle intestine, with higher prevalence
(100%) and intensity (MI = 20.2). In sea bass from Sardinian brackish waters, Arru et al.
(1988) previously reported the occurrence of C. labracis.
T. imbutiforme and T. praeterita were determined basing on some morphological
differences, as the structure of the caeca and the number of the circumoral spines, 18 and 21
respectively, according to Brooks (1980). Therefore the shape of the oral sucker, more
elongated in T. imbutiforme, the size ratio between acetabulum and oral sucker (about 1 in
T. imbutiforme and 0.5 in T. praeterita) and in addiction the site of infection, as reported
above and according to Maillard & Saad-Fares (1981). Among the digenean species,
T. imbutiforme reached the highest prevalence of 52%. Its unusual finding also as
metacercaria encysted in the muscular tissue of one sea bass suggests that D. labrax could
occasionally play a role as second intermediate host. In fact, this role is normally performed
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ITTIOPATOLOGIA, 2010, 7: 123-133
in St. Gilla lagoon by other teleosts as A. boyeri, G. niger and Solea solea (Culurgioni et al.,
2010a).
It is noticeable that the other two digenean species observed, G. lacteum and Monascus sp.,
are here reported for the first time in D. labrax. Concerning the first species, it has been
already found in the brain, optic nerve and pharynx of several marine teleosts from the gulf
of Cagliari (Culurgioni et al., 2007). The site of infection other than those above cited, i.e.
the intestine, indicates that the sea bass can be paratenic host for G. lacteum.
The presence of a single, non ovigerous specimen of the genus Monascus in one fish,
currently suggests that this infection may have an occasional feature; in Mediterranean
M. filiformis is reported on Carangidae and Cepolidae (Orecchia et al., 1985; Radujković et
al., 1989; Bartoli et al., 2005).
Plerocercoid larvae of Tetraphyllidea were the only cestodes represented in the sea bass
examined. The low values of prevalence and intensity recorded were similar to those
observed in other teleosts from the same lagoon, as G. niger (D’Amico et al., 2007) and
Anguilla anguilla (Culurgioni et al., 2010b).
Concerning the Nematoda infections, it is remarkable the very high values of prevalence
and intensity of C. rudolphii larvae, especially taking into account its potential zoonotic
character. This species is characterized by a worldwide distribution and, in brackish fish
species, it is warranted by the occurrence of a large variety of fish-eating birds such as
cormorants, herons, as reported by Farjallah et al. (2008) who observed this anisakid
infection in Phalacrocorax aristotelis of northern Sardinian environments. In support of this
consideration and according to Mattiucci et al. (2007), it is presumable that the specimens
observed in this survey belong to the C. rudolphii sibling species A, observed by the same
authors in sea bass from brackish coastal lagoons of Italy.
Belonging to the same taxa, adult specimens of Philometra spp. were detected in the
ovaries of two adult female sea bass. Unfortunately, one of them harbored only male worms,
and the other only females, so that makes more difficult an exact morphological
determination of one/two species. Gonad-infecting Philometridae may cause serious damage
to the fish ovaries and may thus affect fish reproduction. Philometra sp. had already been
observed in wild D. labrax from Sardinian lagoons (Moscato et al., 2005) and from northern
Adriatic Sea by Čož-Rakovac et al. (2002) with prevalences of 15.4% and 3.3%, respectively
higher and lower than that of 8.0% calculated in this survey. As reported by Moravec et al.
(2003) the occurrence of P. lateolabracis was discovered in several Mediterranean regions in
the gonads of Epinephelus marginatus and Seriola dumerili. Afterwards, Merella et al.
(2005) identified P. jordanoi in E. marginatus from Mallorca island, and females of P.
filiformis were found in the gonads of Pagellus erythrinus (Moravec et al., 2008).
Concerning the adults of A. propinquus, it’s important to underline that its occurrence is
widespread in several fish as Gobius spp., A. fasciatus, S. solea in St. Gilla lagoon (D’Amico
et al., 2007; 2008; unpublished data). This new report in D. labrax from Sardinian waters
provides a further confirm on the low specificity of this parasite. During this study, these
worms were found in the intestine of sea bass as well as in that of some preyed gobies. This
suggest that not only the larval forms, but also the adults of A. propinquus are able to transfer
from a host species to another, by predation.
The cystacanths found in the abdominal cavity were morphologically attributed to the
species Southwellina hispida according to Schmidt (1973), in particular due to the number
and arrangement of the spines of the proboscis armature (>20 rows of 15 spines).
Furthermore, adults of this species are known to infect cormorants in Italy (Dezfuli et al.,
2002) and several species of fish-eating birds in the northern hemisphere (Schmidt, 1973;
Richardson & Cole, 1997). In Europe, Belofastova (2005) observed S. hispida cystacanths in
Liza aurata in the Black Sea.
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ITTIOPATOLOGIA, 2010, 7: 123-133
The occurrence of this acanthocephalan in European sea bass is here reported for the first
time.
Considering the restricted size of the sample examined, it is remarkable the high parasite
species richness detected, moreover it is likely that further investigation may help to enlarge
the current knowledge, in particular on the determination of Philometra and Henneguya at
species level.
ACKNOWLEDGEMENTS
Research supported by MIUR-PRIN 2008.
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