diversity of the digenean fauna in sparid fishes from the lagoon of bizerte in tunisia

6
DOI: 10.2478/s11686-011-0007-0 © W. Stefan´ski Institute of Parasitology, PAS Acta 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 Maamouri Reasearch Unit: Animal Bio-Ecology and Systematic Evolutionary, Faculty of Sciences, University of Tunis El Manar, 2092, Tunis, Tunisia Abstract A 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. Keywords Digenea, 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 Boops boops (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 Sparus aurata 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 × 10 6 m 2 (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]

Upload: lamia-gargouri-ben-abdallah

Post on 29-Jul-2016

215 views

Category:

Documents


2 download

TRANSCRIPT

Page 1: Diversity of the digenean fauna in sparid fishes from the Lagoon of Bizerte in Tunisia

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]

Page 2: Diversity of the digenean fauna in sparid fishes from the Lagoon of Bizerte in Tunisia

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

Page 3: Diversity of the digenean fauna in sparid fishes from the Lagoon of Bizerte in Tunisia

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

Page 4: Diversity of the digenean fauna in sparid fishes from the Lagoon of Bizerte in Tunisia

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-

Page 5: Diversity of the digenean fauna in sparid fishes from the Lagoon of Bizerte in Tunisia

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.

References

Anato C.B., Ktari M.H., Dossou C.H. 1991. La parasitofaune méta-zoaire de Boops boops (Linné, 1758), poisson téléostéen Spa-ridae des côtes tunisiennes. Oebalia, 17, 259–266.

Antar R., Gargouri Ben Abdallah L. Digenean parasites in fish ofDiplodus genus (Teleost, Sparidae) from the Lagoon of Bi-zerte in Tunisia. Hydrobiologia (in press).

Bartoli P. 1966. Sur le cycle vital de Lepocreadium pegorchis (M.Stossich, 1900) M. Stossich, 1903 (Trematoda, Digenea, Lepo-creadiidae). Comptes Rendus de l’Académie des Sciences,Paris, 263, 1398–1400.

Bartoli P. 1987a. Les Trématodes digénétiques parasites des poissonsSparidés de la Réserve Naturelle de Scandola. Travaux Scien-tifiques du Parc Naturel Régional et des Réserves Naturellesde Corse, 10, 1–158.

Bartoli P. 1987b. Caractères adaptatifs originaux des Digènes intes-tinaux de Sarpa salpa (Teleostei, Sparidae) et leur interpréta-tion en termes d’évolution. Annales de Parasitologie Humaineet Comparée, 62, 542–576.

Bartoli P., Bray R.A. 1996. Description of three species of HolorchisStossich, 1901 (Digenea: Lepocreadiidae) from marine fishesoff Corsica. Systematic Parasitology, 35, 133–143. DOI: 10.1007/BF00009822.

Bartoli P., Bray R.A., Gibson D.I. 1989a. The Opecoelidae (Dige-nea) of sparid fishes of the western Mediterranean. III. Mac-vicaria Gibson & Bray, 1982. Systematic Parasitology, 13,167–192. DOI: 10.1007/BF00009743.

Bartoli P., Bray R.A., Gibson D.I. 1989b. The Opecoelidae (Dige-nea) of sparid fishes of the western Mediterranean. II. Pycnadenoides Yamaguti, 1938 and Pseudopycna denaSaad-Fares & Maillard, 1986. Systematic Parasitology, 13,35–51. DOI:10.1007/BF00006949.

Bartoli P., Gibson D.I. 1989. Wardula sarguicola n. sp. (Digenea,Mesometridae), a rectal parasite of Diplodus sargus (Teleo-stei, Sparidae) in western Mediterranean. Annales de Parasi-tologie Humaine et Comparée, 64, 20–29.

Bartoli P., Gibson D.I. 2007. Synopsis of the life cycles of Digenea(Platyhelminthes) from lagoons of the northern coast of thewestern Mediterranean. Journal of Natural History, 41, 1553–1570. DOI: 10.1080/00222930701500142.

Bartoli P., Gibson D.I., Bray R.A. 2005. Digenean species diversityin teleost fish from a nature reserve off Corsica, France (west-ern Mediterranean), and a comparison with other Mediter-ranean regions. Journal of Natural History, 39, 47–70. DOI:10.1080/00222930310001613557.

Bartoli P., Prévôt G. 1978. Le cycle biologique de Holorchis pycno-porus M. Stossich, 1901 (Trematoda, Lepocreadiidae). Zeit-schrift für Parasitenkunde, 58, 73–90. DOI: 10.1007/BF00930794.

Ben Said O., Goñi Urriza M., El Bour M., Duran R., Aissa P. 2010.Diversité des bactéries capables de dégrader les hydrocarburesaromatiques polycycliques et résistantes aux métaux et auxantibiotiques isolés à partir des sédiments de la lagune de Bi-zerte, Tunisie. Revue de Microbiologie, Industrie, Santé et En-vironnement, 1, 32–48.

Bray R.A., Gibson D.I. 1990. The Lepocreadiidae (Digenea) of fishesof the north-east Atlantic: review of the genera OpechonaLooss, 1907 and Prodistomum Linton, 1910. Systematic Par-asitology, 15, 159–202.

Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. 1997. Parasitologymeets ecology on its own terms: Margolis et al. Revisited. Jour-nal of Parasitology, 83, 575–583. DOI: 10.2307/3284227.

Chargui T., Antar R., Trigui El Menif N., Gargouri Ben Abdallah L.2010. Identification du cycle de vie de Proctoeces maculatus(Digenea, Fellodistomidae) récolté dans la lagune de Bizertesituée au Nord Est de la Tunisie. Rapport de la CommissionInternationale de la Mer Méditerranée, 39, 474.

Cross M.A., Irwin S.W.B., Fitzpatrick S.M. 2001. Effects of heavymetal pollution on swimming and longevity in cercariae ofCryptocotyle lingua (Digenea: Heterophyidae). Parasitology,123, 499–507. DOI: 10.1017/S0031182001008708.

Cross M.A., Irwin S.W.B, Fitzpatrick S.M. 2005. Effects of host habi-tat quality on the viability of Cryptocotyle lingua (Trematoda:Digenea) cercariae. Parasitology, 130, 195–201. DOI: 10.1017/S0031182004006419.

D’Amico V., Canestri Trotti G., Culurgioni J., Figus V. 2006.Helminth parasite community of Diplodus annularis L. (Os-teichthyes, Sparidae) from Gulf of Cagliari (Sardinia, southWestern Mediterranean). Bulletin of the European Associa-tion of Fish Pathologists, 26, 222–228.

Dellali M., Gnassia Barelli M., Romeo M., Aissa P. 2001. The use ofacetylcholinesterase activity in Ruditapes decussates andMytilus galloprovincialis in the biomonitoring of Bizerta la-goon. Comparative Biochemistry and Physiology, 130, 227–235. DOI: 10.1016/S1532-0456(01)00245-9.

Fischer W., Seneider M., Bauchaut, M.L. 1987. Fiches F.A.O. d’iden-tification des espèces pour les besoins de la pêche. Méditer-ranée et Mer noire (zone de pêche 37) Vertébrés. Vol. II,1359–1361. Rome, FAO.

Page 6: Diversity of the digenean fauna in sparid fishes from the Lagoon of Bizerte in Tunisia

Digenean fauna of sparid fishes in Tunisia 39

Fischthal J.H. 1980. Some digenetic trematodes of marine fishes fromIsrael’s Mediterranean coast and their zoogeography, espe-cially those from Red Sea immigrant fishes. ZoologicaScripta, 9, 11–23. DOI: 10.1111/j.1463-6409.1980.tb00647.x.

Fischthal J.H. 1982. Additional records of digenetic trematodes ofmarine fishes from Israel’s Mediterranean coast. Proceedingsof the Helminthological Society of Washington, 49, 34–44.

Gargouri Ben Abdallah L., Maamouri F. 2008. Digenean fauna di-versity in sparid fish from Tunisian coasts. Bulletin of the Eu-ropean Association of Fish Pathologists, 28, 129–137.

Holmes J.C., Price P.W. 1986. Communities of parasites. In: (Eds.D.J. Anderson and J. Kikkawa) Community biology: patternand processes. Blackwell, Oxford, 187–213.

Kostadinova A., Bartoli P., Gibson D.I., Raga J.A. 2004. Redescrip-tions of Magnibursatus blennii (Paggi & Orechhia, 1975) n.comb. and Arnola microcirrus (Vlasenko, 1931) (Digenea:Derogenidae) from marine teleosts off Corsica. SystematicParasitology, 58, 125–137. DOI: 10.1023/B:SYPA.0000029421.06547.0.

Kostadinova A., Gibson D.I. 2009. New records of rare derogenids(Digenea: Hemiuroidea) from Mediterranean sparids, includ-ing the description of a new species of Magnibursatus Naide-nova, 1969 and redescription of Derogenes adriaticusNikolaeva, 1966. Systematic Parasitology, 74, 187–198. DOI:10.1007/s11230-009-9214-6.

Maillard C. 1976. Distomatose de poissons en milieu lagunaire. Doc-torat es-Sciences Naturelles, Université des Sciences et Tech-niques de Languedoc, Montpellier.

Margolis L., Esch G.W., Holmes J.C., Kuris A.M., Schad G.A. 1982.The use of ecological terms in parasitology. Journal of Para-sitology, 68, 131–133.

Martinez J.C. 1972. Recherches sur quelques stades larvaires deDigènes parasites de Mytilus galloprovincialis Lmk. Thèse deDoctorat, Université des Sciences et Techniques de Langue-doc, Montpellier.

Morley N.J., Crane M., Lewis J.W. 2003. Toxicity of cadmium andzinc to the decaudised cercarial life-span of Diplostomumspathaceum (Trematoda: Diplostomidae). Parasitology, 127,497–506. DOI: 10.1017/S0031182003003949.

Orecchia P., Paggi L. 1978. Aspetti di sistematica e di ecologia degli el-minti parassiti di pesci marini studiati pressol’Instituto di Pa-rassitologia dell Universito di Roma. Parassitologia, 20, 73–89.

(Accepted November 23, 2010)

Papoutsoglou S.E. 1976. Metazoan parasites of fishes from Saroni-cos Gulf Athens-Greece. Thalassographica, 1, 69–102.

Pérez-del Olmo A., Fernández M., Gibson D.I., Raga J.A., Kostadi-nova A. 2007. Descriptions of some unusual digeneans fromBoops boops L. (Sparidae) and a complete checklist of itsmetazoan parasites. Systematic Parasitology, 66, 137–157.DOI: 10.1007/s11230-006-9063-5.

Pérez-del Olmo A., Fernández M., Raga J.A., Kostadinova A., Pou-lin R. 2008. Halfway up the trophic chain: development ofparasite communities in the sparid fish Boops boops. Para-sitology, 135, 257–268. DOI: 10.1017/S0031182007003691.

Pérez-del Olmo A., Gibson D.I., Fernández M., Sanisidro O., RagaJ.A., Kostadinova A. 2006. Descriptions of Wardula bartoliin. sp. (Digenea: Mesometridae) and three newly recorded ac-cidental parasites of Boops boops L. (Sparidae) in the NE At-lantic. Systematic Parasitology, 63, 99–109. DOI: 10.1007/s11230-005-9003-9.

Prévôt G., Bartoli P. 1967. Nouvelle contribution à l’étude de Mo-norchiidae (Odhner, 1911), (Trematoda: Digenea) parasitesdes Poissons du golfe de Marseille (France). Annales de Para-sitologie Paris, 42, 621–632.

Saad Fares A. 1985. Trématodes de poissons des côtes du Liban.Thèse Doctorat d’Etat, Université des Sciences et Techniquesdu Languedoc, Montpellier.

Sasal P., Niquil N., Bartoli P. 1999. Community structure of dige-nean parasites of sparid and labrid fishes of the MediterraneanSea: a new approach. Parasitology, 119, 635–648. DOI:10.1017/S0031182099005077.

Stunkard H.W., Uzmann J.R. 1959. The life-cycle of the digenetictrematode, Proctoeces maculatus (Looss, 1901) Odhner, 1911,[syn. P. subtenuis (Linton, 1907) Hanson, 1950], and de-scription of Cercaria adranocerca n. sp. Biological BulletinWoods Hole, 116, 184–193.

Sures B. 2004. Environmental parasitology: relevancy of parasitesin monitoring environmental pollution. Trends in Parasitol-ogy, 20, 170–177. DOI: 10.1016/j.pt.2004.01.014.

Sures B. 2008. Environmental parasitology. Interactions between par-asites and pollutants in the aquatic environment. Parasite, 15,434–438.

Ternengo S., Levron C., Marchand B. 2005. Metazoan parasites insparid fish in Corsica (Western Mediterranean). Bulletin ofthe European Association of Fish Pathologists, 25, 262–269.