diversity of the digenean fauna in sparid fishes from the lagoon of bizerte in tunisia
TRANSCRIPT
DOI: 10.2478/s11686-011-0007-0© W. Stefanski Institute of Parasitology, PASActa Parasitologica, 2011, 56(1), 34–39; ISSN 1230-2821
Diversity of the digenean fauna in sparid fishes from the Lagoon of Bizerte in Tunisia
Lamia Gargouri Ben Abdallah*, Rym Antar and Fadhila MaamouriReasearch Unit: Animal Bio-Ecology and Systematic Evolutionary, Faculty of Sciences, University of Tunis El Manar, 2092, Tunis, Tunisia
AbstractA total of 24 digenean species belonging to 10 distinct families (Derogenidae, Faustulidae, Fellodistomidae, Gyliauchenidae,
Hemiuridae, Lepocreadiidae, Mesometridae, Monorchiidae, Opecoelidae and Zoogonidae) were recorded in sparid fishes from
Bizerte Lagoon (northern Tunisia). The diversity of the digenean fauna of sparid fishes from this locality is compared to that
recorded from the Gulf of Tunis. Prodistomum polonii, not detected before, was found in Sarpa salpa. Aphallus rubalo, Dero-genes latus, Holorchis micracanthum and Pachycreadium carnosum previously recorded from sparid fishes on the Tunisian
coasts were absent during this study. Allopodocotyle pedicellata, Lepocreadium pegorchis, L. album, Proctoeces maculatus,
Magnibursatus bartolii and Macvicaria maillardi were reported in hosts not previously reported for the Gulf of Tunis. Gener-
ally, prevalence was higher in fishes from Bizerte Lagoon but abundance and mean intensity were higher in Gulf of Tunis. Ex-
cept for Lithognathus mormyrus, Sarpa salpa and Sparus aurata from Bizerte Lagoon, which show higher digenean diversity,
the other sparid fishes have a lower diversity compared to those from Gulf of Tunis. The species richness of digeneans in
B. boops was the same in the two areas studied.
KeywordsDigenea, diversity, epidemiologic values, sparid fishes, comparative analysis, Bizerte Lagoon, Tunisia
Introduction
In the Mediterranean Sea, the digenean fauna of sparid fishes
has aroused the interest of numerous parasitologists (Prévôt
and Bartoli 1967; Papoutsoglou 1976; Bartoli and Prévôt
1978; Orecchia and Paggi 1978; Fischthal 1980, 1982; Saad
Fares 1985; Bartoli 1987 a, b; Bartoli and Gibson 1989; Bar-
toli and Bray 1996; Bartoli et al. 1989a, b, 2005; Sasal et al.1999; Ternengo et al. 2005; D’Amico et al. 2006; Pérez-del
Olmo et al. 2006, 2007, 2008; Kostadinova and Gibson 2009).
In consequence, many digenean species have been recorded
and described from this region. On the Tunisian coasts, this
fauna remains poorly known and is represented by three stud-
ies, that of Anato et al. (1991), concerning the description of
digeneans of only one species of sparid fish, Boops boops, the
other of Gargouri Ben Abdallah and Maamouri (2008) on the
digenean diversity in 13 species of sparid fishes from the Gulf
of Tunis and recently that of Antar and Gargouri Ben Abdal-
lah (in press) on the digenean parasites in fishes of the genus
Diplodus from the Bizerte Lagoon. To remedy this deficiency
and in order to make a comparative analysis with the avail-
able data on the Gulf of Tunis, we have studied the digenean
fauna of sparid fishes from Bizerte Lagoon, a confined and
favourable environment for the circulation of the parasites and
the completion of their life cycles.
Materials and methods
During the sampling period (October 2008-October 2009),
a total of 277 sparid fishes represented by 9 species (30 Boopsboops (Linnaeus, 1758), 100 Lithognathus mormyrus (L.,
1758), 7 Pagellus acarne (Risso, 1826), 16 Pagellus erythri-nus (L., 1758), 3 Pagrus auriga (Valenciennes, 1843), 7 Pa-grus pagrus (L., 1758), 10 Sarpa salpa (L., 1758), 86 Sparusaurata L., 1758 and 18 Spondyliosoma cantharus (L., 1758)
were collected from Bizerte Lagoon situated in northern
Tunisia between 37°8΄N, 9°46΄E and 37°16΄N, 9°56΄E and oc-
cupying an area of 15 × 106 m2 (Dellali et al. 2001).
The fish nomenclature is taken from Fischer et al. (1987).
These species, living on various bottoms (sand, mud, rocks,
gravels, conglomerates, posidonia) are gregarious or solitary.
*Corresponding author: [email protected]
Digenean fauna of sparid fishes in Tunisia 35
They live at depths varying from 20 to 420 m. Sexual matu-
rity is reached during the first or the second year of life. They
feed on algae, worms, molluscs, small crustacean, echino-
derms, larvae of fishes, cephalopods and bivalves (Fischer etal. 1987).
The fishes collected were kept on ice and brought to the
laboratory as soon as possible. The trematodes were obtained,
after dissection of freshly killed fish, from various parts of the
digestive tract (oesophagus, stomach, pyloric caeca, duode-
num, mid-intestine, posterior intestine, and rectum) and in the
gall bladder. Parasites were examined and identified under the
binocular microscope. Sites and number of each species of
parasite were noted. Some of them were examined while still
alive. The others were killed and fixed in Bouin-Holland. They
were stained with borax carmine, dehydrated through a graded
alcohol series, cleared and mounted in Canada balsam. Draw-
ings were made using a light microscope equipped with a
drawing tube.
The parasitological terminology (prevalence, abundance
and mean intensity) followed the definitions of Margolis et al.(1982) and Bush et al. (1997). As mentioned by Holmes and
Price (1986), satellite species represents parasites with a
prevalence varying from 6 to 40% and rare species, those with
frequency less than 6%.
Results
The digenean fauna of sparid fishes from Bizerte Lagoon con-
sists of the 24 species belonging to 10 distinct families: Dero-
genidae Nicoll, 1910; Faustulidae Poche, 1926; Fellodisto-
midae Nicoll, 1909; Gyliauchenidae Fukui, 1929; Hemiuridae
Looss, 1899; Lepocreadiidae Odhner, 1905; Mesometridae
Poche, 1926; Monorchiidae Odhner, 1911; Opecoelidae Ozaki,
1925 and Zoogonidae Odhner, 1902 (Table I). These species
were recorded from only 7 species of fish hosts investigated;
Pagellus acarne and Pagrus auriga were digenean free due
probably to their small sample size. These fishes, preferring a
rocky bottom and living in greater depth, are scarce in Bizerte
Lagoon. The highest proportion (33.33%) of species richness
was found in Lithognathus mormyrus, Sarpa salpa and Sparusaurata; 20.83% was found in Boops boops and 12.5% in
Spondyliosoma cantharus. Pagellus erythrinus and Pagruspagrus harboured only 8.33% of the species.
Majority of recorded digeneans colonize two or more parts
of the digestive tract of the host. However, Hemiuris commu-nis Odhner, 1905, Bacciger israelensis Fischthal, 1980, Diph-terostomum brusinae Stossich, 1889 and Prodistomum poloniiMolin, 1859 seem to show clear ecological preferences and
limit their distribution to only one niche (Table I). The distri-
bution of digeneans in the host species shows that Aphanurusstossichi Monticelli, 1891, Bacciger israelensis Fischthal,
1980, Centroderma spinosissima (Stossich, 1883) Lühe, 1901,
Elstia stossichianum (Monticelli, 1892) Bray, 1984, Mesome-tra brachycoelia Lühe, 1901, Mesometra orbicularis (Rudol-
phi, 1819) Lühe, 1901, Robphildollfusium martinezgomeziLópez-Román et al., 1992, Robphildollfusium fractum Rudol-
phi, 1819 and Wardula capitellata (Rudolphi, 1819) Poche,
1926 were collected in only one host species and the other
species seem to be more generalist and were recorded from
several host species.
The examination of the ecological parameters of different
parasites shows that Bacciger israelensis, Hemiuris commu-nis, Robphildollfusium martinezgomezi, Diphterostomumbrusinae, Magnibursatus bartolii Kostadinova et al., 2003,
Pycnadenoides senegalensis Fischthal et Thomas, 1972 at-
tained low prevalences of less than 6% and were considered as
rare species. Allopodocotyle pedicellata (Stossich, 1887)
Pritchard, 1966, Lepocreadium album Stossich, 1890, Macvi-caria maillardi Bartoli et al., 1989 and Proctoeces maculatusLooss, 1901 showing lower level of prevalence in Lithogna-thus mormyrus, were most prevalent in the other hosts. All
other parasites were satellite species. The highest value of in-
fection was generally recorded for digeneans from S. salpa,
characterized generally by specialist species.
The infracommunities of L. mormyrus, S. aurata and
S. salpa reveal that the most of these hosts harboured 1 (50%,
40% and 25%) or 2 (35.71%, 38.18% and 37.5%) and more
rarely 3 (10.71%, 20% and 12.5%) or 4 species of parasites
(3.57%, 9.09% and 12.5%); these values were surpassed on
occasion in S. aurata (maximum 5 species) and in S. salpa(maximum 7 species). Furthermore, 62.5% of S. cantharusand 42.85% of B. boops were infested with 1 species; 37.5%
of the first host and 42.85% of the second host accumulated 2
parasites species. Pagellus erythrinus and Pagrus pagruswhich were less heavily infested harbouring mostly 1 species.
Discussion
The local digenean fauna of the sparids of Bizerte Lagoon
consists of 24 parasite species which were found in 7 of the 9
fish hosts investigated; a few of these parasites were recur-
rently rare species; all other digenean fauna were satellite
species. The examination of the distribution of the parasites
in the host species shows that only Aphanurus stossichi, Bac-ciger israelensis, Centroderma spinosissima, Elstia stossichia-num, Mesometra brachycoelia, Mesometra orbicularis,
Robphildollfusium martinezgomezi, Robphildollfusium frac-tum and Wardula capitellata are oioxenic species; other
helminths are known as generalists and do not have the same
prevalence among their various hosts; this is undoubtedly re-
lated to the large morphological variations of the teleost ali-
mentary tract and the ecological preferences of the parasites.
Hemiuris communis, Monorchis monorchis, Pycnadenoidessenegalensis, Steringotrema pagelli, Magnibursarus bartolii,Prodistomum polonii, recorded from one host species in
this study have been reported from other host species in other
studies (Bray and Gibson 1990, Kostadinova et al. 2004,
Gargouri Ben Abdallah and Maamouri 2008). We think, as
Lamia Gargouri Ben Abdallah et al.36
Table I. Epidemiologic values – prevalence: P (%), abundance: A and mean intensity – MI of Digenea in sparid fishes from Lagoon of Bizerte and Gulf ofTunis (Gargouri Ben Abdallah and Maamouri 2008). A, oesophagus; B, stomach; C, pyloric caeca; D, duodenum; E, mid-intestine; F, posterior intestine; G,rectum; H, gall bladder. Derogenidae1, Cryptogonimidae2, Faustulidae3, Fellodistomidae4, Gyliauchenidae5, Hemiuridae6, Lepocreadiidae7, Mesometridae8,Monorchiidae9, Opecoelidae10 and Zoogonidae11
Fish species Parasites speciesPresent work Gulf of Tunis
Bizerte Lagoon (Gargouri & Maamouri 2008)
Sites P (%) A MI Sites P (%) A MI
Aphanurus stossichi6 AB 16.66 0.43 2.6 AB 26.13 0.9 3.45
Arnola microcirrus1 B 1 0.01 1
Boops boops Bacciger israelensis3 D 3.33 0.03 1 CD 3.6 0.05 1.25
Hemiuris communis 6 B 3.33 0.03 1 B 2.7 0.04 1.33
Lepocreadium pegorchis7 C 3.33 0.03 1Robphildollfusium martinezgomezi5 E 3.33 0.03 1 E 2.7 0.06 2.33
Derogenes latus1 H 1.11 0.01 1
Allopodocotyle pedicellata 10 EG 2 0.02 1
Diphterostomum brusinae11 F 3 0.03 1 G 3.33 0.06 1.66
Lithognathus Holorchis pycnoporus7 DEFG 31 1.27 4.09 DEF 27.78 1.45 5.24
mormyrus Lepocreadium album7 DE 2 0.13 6.5
Lepocreadium pegorchis7 BDF 19 0.76 4 CDE 15.56 0.84 5.42
Macvicaria maillardi 10 D 2 0.03 1.5
Macvicaria mormyri 10 DEF 19 0.52 2.73 DE 8.89 0.47 5.37
Proctoeces maculatus4 FG 5 0.06 1.2
Pycnadenoides senegalensis10 E 3.33 0.08 2.33
Derogenes latus1 H 0.6 0.01 1
Holorchis micracanthum 7 DEF 12.36 0.24 1.95
Holorchis pycnoporus 7 EF 12.5 0.25 2 DEF 14.04 0.38 2.72
Pagellus Lepocreadium album 7 D 2.81 0.06 2.2
erythrinus Lepocreadium pegorchis 7 E 6.25 0.12 1
Macvicaria crassigula 10 DE 5.06 0.12 2.33
Pachycreadium carnosum10 D 5.62 0.07 1.3
Pycnadenoides senegalensis10 D 1.12 0.01 1
Aphallus rubalo 2 E 4 0.12 1
Holorchis micracanthum 7 E 4 0.04 1
Holorchis pycnoporus 7 EF 16 0.24 1.5
Lepocreadium album 7 D 14.28 0.14 1
Pagrus pagrus Lepocreadium pegorchis 7 E 14.28 0.14 1
Macvicaria crassigula 10 DE 10 0.18 1.8
Proctoeces maculatus4 G 2 0.02 1
Zoogonus rubellus11 G 2 0.04 2
Centroderma spinosissima 8 DEF 10 2.6 26 DEF 12.5 1 .22 9.8
Elstia stossichianum 8 EF 40 1.7 4.25 EF 10 0.63 6.25
Lepocreadium pegorchis 7 C 30 7.4 24.66 DE 2.5 0.10 4
Mesometra brachycoelia 8 CDEF 40 2.3 5.75 CDEF 17.5 1.17 6.71
Sarpa salpa Mesometra orbicularis 8 CDEF 30 3.1 10.33 CDEF 22.5 3.55 15.77
Prodistomum polonii7 F 10 0.1 1
Robphildollfusium fractum5 F 10 0.1 1 ABCDE 42.5 4.50 10.58
Wardula capitellata 8 EF 10 0.3 3 DEF 12.5 0.20 1.33
Allopodocotyle pedicellata10 CDFG 25.58 0.56 2.22 DEFG 17.92 0.38 2.11
Diphterostomum brusinae 11 F 4.72 0.10 2.2
Lepocreadium album 7 D 3.48 0.12 3.66
Lepocreadium pegorchis 7 CDF 19.76 2.86 14.47
Macvicaria maillardi DEFG 24.41 0.54 2.23 DEF 17.92 0.38 2.11
Sparus aurata Macvicaria obovata10 DEF 34.88 1.05 3.03 DEF 12.26 0.42 3.38
Magnibursatus bartolii1 A 3.48 0.08 2.33
Proctoeces maculatus 4 DFG 18.60 0.9 4.87
Pycnadenoides senegalensis10 D 1.16 0.01 1 E 10 0.05 2
Zoogonus rubellus11 F 1 0.09 2
Arnola microcirrus1 B 2.5 0.02 1
Lepocreadium album7 CD 22.22 0.44 2 D 5 0.07 1.5
Spondyliosoma Macvicaria crassigula10 DE 5 0.05 1
cantharus Monorchis monorchis9 CD 16.66 1.44 8.66 C 7.5 0.1 1.33
Steringotrema pagelli4 CDF 33.33 0.55 1.66 CDEF 17.5 2.95 16.85
Digenean fauna of sparid fishes in Tunisia 37
proposed by Bartoli (1987b) that the restriction of some dige-
neans to only one host species relates to the transmission
modality of the infective stages of parasites and with the diet
of the host. This hypothesis is in perfect agreement with oiox-
enic parasites of S. salpa (Centroderma spinosissima, Elstiastossichianum, Mesometra brachycoelia, Mesometra orbicu-laris, Robphildollfusium fractum, Wardula capitellata). In-
deed, these parasites encyst as metacercariae usually upon
vegetation which constitute the diet of the herbivorous defin-
itive host, S. salpa. Moreover, we think that the morphology
of the digestive tract and the availability of adequate food
seem to influence the specificity of the parasite to the host.
The other parasites of S. salpa (Lepocreadium pegorchis and
Prodistomum polonii), encysted on epiphytic lamellibranch
molluscs, seem to be fortuitously transmitted to S. salpa after
accidental ingestion of parasitized molluscs. Moreover, these
species do not have the accessory adhesive organ found in
other specific parasites of S. salpa, allowing their establish-
ment in the smooth digestive gut wall of this herbivorous fish.
Contrary to the parasites previously cited in this host, these
two species seems to be very generalist. Indeed, Lepocreadiumpegorchis has been reported from Sparidae, Labridae,
Blennidae and Centracanthidae. Prodistomum polonii has
been found in a wide variety of fish families (Carangidae,
Centracanthidae, Gadidae, Engraulidae, Mullidae, Pomato-
midae, Scorpaenidae, Soleidae and Zeidae) but never previ-
ously in sparid fishes. If Prodistomum polonii is an accidental
parasite in S. salpa its occurrence in sparid fishes is confirmed;
indeed, this parasite was also reported from another sparid
species (Diplodus annularis) from Bizerte Lagoon (Antar and
Gargouri Ben Abdallah, in press). However, this species seem
to be predominantly reported in carangid fishes of the genus
Trachurus (see Bray and Gibson 1990).
The examination of the ecological terms shows that the
highest level of infection was generally recorded for digeneans
from S. salpa; this is undoubtedly connected with diet, be-
haviour and interactions of parasites in the digestive tract of
the host. Indeed, the digeneans of this sparid, feeding upon in-
testinal chyme and not permanently attached to the digestive
wall of their host, seem to be slightly or not immunogenic
(Bartoli 1987b). Moreover, we think that the length of the di-
gestive tract is relatively important in this herbivorous host
and so the availability of food can influence the abundance
values for parasites of S. salpa.
The digenean faunal composition of the sparid fishes from
Bizerte Lagoon is compared with those recorded from Gulf of
Tunis (Gargouri Ben Adallah and Maamouri 2008); we found
that, Prodistomum polonii, recorded in S. salpa from Bizerte
Lagoon, has not been previously collected from sparid fishes
in the Gulf of Tunis. Some parasite species (Aphallus rubalo,
Derogenes latus, Holorchis micracanthum and Pachycread-ium carnosum) which were previously found in sparid fishes
on the Tunisian coasts were not collected during this study.
This result cannot be solely attributed to the small host sam-
ple sizes but also to the scarcity of these parasite species.
Arnola microcirrus, Macvicaria crassigula and Zoogonusrubellus absent in the fishes of the current study were found in
this environment in Diplodus fishes (Antar and Gargouri Ben
Abdallah, in press). Lepocreadium pegorchis was previously
not found from B. boops, P. erythrinus and S. aurata in the
Gulf of Tunis. Lepocreadium album was also detected in Pa-grus pagrus and S. aurata, Proctoeces maculatus in L. mor-myrus and S. aurata, Allopodocotyle pedicellata and Macvicariamaillardi in L. mormyrus from the Bizerte Lagoon. Mag-nibursarus bartolii, recorded for the first time in the Mediter-
ranean in Oblada melanura (Gargouri Ben Abdallah and
Maamouri 2008), colonizes another host (S. aurata) in the
Bizerte Lagoon.
Concerning the level of infection we note that, except for
Aphanurus stossichi, B. israelensis, Centroderma spinosis-sima, Diphterostomum brusinae, Holorchis pycnoporus, Pyc-nadenoides senegalensis, Robphildollfusium fractum and
Wardula capitellata which were more frequent in the Gulf of
Tunis, the other parasites were predominant in the Bizerte La-
goon; this may be connected with the successful completion of
life cycles of these parasites in Bizerte Lagoon, a confined en-
vironment limiting the dispersal of the larval stages. Indeed,
Maillard (1976) showed that a digenean which completes its
life cycle in the ponds and the lagoons has a higher chance of
completion than that having a marine life cycle. The values of
abundance and mean intensity were generally lower in the
Bizerte Lagoon. This can be due to unfavourable living con-
ditions for intermediate host or for free larval stages in this
environment. Indeed, Bizerte Lagoon, being a subject to eu-
trophication, is susceptible also to anthropogenic disturbances
of various origins (domestic and industrial wastes released by
the neighbouring towns and agricultural waste run-off) (Del-
lali et al. 2001, Ben Said et al. 2010). This polluted environ-
ment may reduce the lifespan of cercaria (Morley et al. 2003)
and decrease their success in infecting the second host (Cross
et al. 2005). Indeed, Cross et al. (2001) showed that there is a
reduction in the speed of swimming and longevity of the cer-
caria Cryptocotyle lingua infesting a bivalve, Littorina littorealiving in polluted environment. Sures (2004, 2008) supposed
that pollution can affect the health of the intermediate host and
cause their scarcity or loss.
The niche dimensions of the parasites collected within the
host digestive system were generally the same for lagoonal
and marine sparid fishes (Table I). However, we note that the
increase of the individual numbers of parasites (Bacciger is-raelensis in B. boops, Holorchis pycnoporus in P. erythrinusand Robphildollfusium fractum in S. salpa from the Gulf of
Tunis) led to the extension of the niche dimensions. This can
undoubtedly buffer the parasite against intraspecific competi-
tion.
If we compare digenean species richness of sparid fishes
from Bizerte Lagoon and from Gulf of Tunis, we note that
L. mormyrus, S. aurata and S. salpa from the first biotope
have the most diverse digenean fauna (8 species). However,
this diversity, is lower (not exceeding 2 and 3 species) for Page-
Lamia Gargouri Ben Abdallah et al.38
llus erythrinus, Pagrus pagrus and Spondyliosoma cantharusfrom Bizerte Lagoon, but is higher for the same fishes from
Gulf of Tunis. B. boops shows the same specific richness in
the two Tunisian localities. Examination of the parasite species
found in fishes from lagoonal environment and absent in the
same host from the Gulf of Tunis shows that they generally
present low frequencies. However, Lepocreadium pegorchisand Proctoeces maculatus collected from S. aurata have
greater epidemiological values; this is undoubtedly in relation
with the preference of these parasites for the final host, their
specificity to the first intermediate host and with the trans-
mission strategies selected by larval stages. As far as we know
specificity to the first intermediate host is usually oioxenic for
Digenea. However, for L. pegorchis sporocyst and cercaria
have been reported from two species (gastropods) of interme-
diate hosts, Nassarius corniculum (Olivi), N. mutabilis (L.)
(Bartoli 1966); this undoubtedly increases the number of the
larvae emitted and so the success of the life cycle. Proctoecesmaculatus is also reported from two species of the first inter-
mediate host, Mytilus galloprovincialis and M. edulis(Stunkard and Uzmann 1959, Martinez 1972). Cercariae of
this species are characterized by a very small tail; so it moves
short distances and encysts (as metacercaria) on the fauna as-
sociated with the mussels; this reduces the loss of the larvae
and decreases the time of exposure to the environmental con-
ditions. The life cycle of this parasite was elucidated in Bizerte
Lagoon; sporocyst and cercaria were recorded from M. gallo-provincialis; the metacercaria was found in associated fauna,
Chlamys varia and Sabella pavonina (Chargui et al. 2010).
The frequency of the first host is important since culture under
shellfish tables or on long-lines of this mollusc is practised in
Bizerte Lagoon. All these factors can increase the epidemio-
logic values of this parasite species.
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