Tunisian coastal waters are located in the south-central Mediterranean Sea. Tunisia has a 1670- km coastline including 7 coastal lagoons, covering a total surface of 105200 ha and an exceptional continental shelf of 88 000 km2 (Cherif et al., 2011). It also has a large hydrographic network in the north. The surface water accommodates a relatively high faunal diversity, especially in terms of aquatic vertebrates that can host a high species richness of parasites. Among them, monogeneans (Plathyhelmintes) which are commonly found on fishes can also parasitise freshwater turtles and amphibians. These parasites are ideal for diversity investiga
tions because they are diverse both in terms of morphology and numbers. Their members are generally host specific, and their phylogeny is well resolved (Poulin, 2002). In addition, the study of monogeneans is also fundamental to aquaculture because they are known as agents responsible for many epidemics (Lia et al., 2007). In Tunisia, these flatworms were first studied by Ktari (1969) who described the species of Atrispinum salpae (Parona & Perugia, 1890) Maillard & Noisy, 1979 from Sarpa salpa (Linnaeus, 1758). After that, more than 50 studies have been published about monogenenans including description of new species and new hosts as well as locality records. Despite these parasitological surveys, there were no attempts to quantify the species richness of Monogenea of Tunisian aquatic vertebrates.
In this paper we present all the available species records of monogeneans in Tunisian waters and we incorporate new data derived from our own work on species recorded from marine fish of the Gulf of Gabes (southern coast of Tunisia) in order to make the first checklist of monogeneans as parasites of Tunisian aquatic vertebrates.
Materials and Methods
The list of Monogenea from Tunisian aquatic vertebrates was prepared based on published data and doctoral and masters theses. It is organized in both a parasite–host table (Table 1 and a host– parasite one (Table 2).The families and species of monogeneans are presented in alphabetical order followed by microhabitat, localities and references (Table 1). The nomenclatures of all taxa are presented according to WoRMS (2021). However, authors of new combinations for some very old taxa of Monogenea are lacking.
List of Monogenea parasites of Tunisian aquatic organisms. Records are listed by monogenoidean families and ordered per: parasite species (alphabetically), host species (alphabetically), reference (chronologically). NR, New record. Areas: 1, North; 2, East ; 3, South; 4. hydrographic network in the north.
Ligophorus acuminatus Euzet and Suriano, 1977; Ligophorus heteronchus Euzet and Suriano, 1977; Ligophorus macrocolpos Euzet and Suriano, 1977; Ligophorus minimus Euzet and Suriano, 1977; Solostamenides mugilis (Vogt, 1879) Unnithan, 1971
Dasyatis marmorata (Steindachner, 1892)
Heterocotyle pastinacae Scott, 1904; Heterocotyle scotti Neifar, Euzet and Ben Hassine, 1998; Merizocotyle concinna (Scott, 1904) Chisholm, Wheeler and Beverley-Burton, 1995; Neoentobdella diadema (Monticelli, 1902) Kearn and Whittington, 2005; Trimusculotrema micracantha (Euzet and Maillard, 1967) Whittington and Barton, 1990
Dasyatis pastinaca (Linnaeus, 1758)
Heterocotyle pastinacae Scott, 1904; Heterocotyle scotti Neifar, Euzet and Ben Hassine, 1998; Heterocotyle similis Neifar, Euzet and Ben Hassine, 1998; Merizocotyle concinna (Scott, 1904) Chisholm, Wheeler and Beverley-Burton, 1995; Neonchocotyle pastinacae Ktari and Maillard, 1972; Neoentobdella diadema (Monticelli, 1902) Kearn and Whittington, 2005; Trimusculotrema micracantha (Euzet and Maillard, 1967) Whittington and Barton, 1990
Dasyatis tortonesei Capapé, 1975
Heterocotyle capapei Neifar, Euzet and Ben Hassine, 2000; Neoentobdella diadema (Monticelli, 1902) Kearn and Whittington, 2005; Thaumatocotyle tunisiensis Neifar, Euzet and Ben Hassine, 2000; Trimusculotrema micracantha (Euzet and Maillard, 1967) Whittington and Barton, 1990
Dentex dentex (Linnaeus, 1758)
Gotocotyla acanthura (Parona and Perugia, 1896) Meserve, 1938
Cotyloatlantica mediterranea (Euzet and Trilles, 1960) Bravo-Hollis, 1984
Spicara maena (Linnaeus, 1758)
Bivagina alcedinis (Parona and Perugia, 1889) Yamaguti, 1963
Spicara smaris (Linnaeus, 1758)
Lamellodiscus knoepffleri Oliver, 1969
Synapturichthys kleinii (Risso, 1827)
Pseudodiplectanum syrticum Derbel, Boudaya and Neifar, 2007
Taeniura grabata Geoffroy Saint-Hilaire, 1817
Heterocotyle forcifera Neifar, Euzet and Ben Hassine, 1999; Heterocotyle mokhtarae Neifar, Euzet and Ben Hassine, 1999; Heterocotyle striata Neifar, Euzet and Ben Hassine, 1999; Neoentobdella apiocolpos (Euzet and Maillard, 1967) Kearn and Whittington, 2005
Diclidophora sp. Nudaciraxine imperium Châari, Derbel and Neifar, 2010; Pseudoaspinatrium gallieni (Euzet and Ktari, 1971) Mamaev, 1986
Umbrina cirrosa Linnaeus, 1758
Calceostomella inermis (Parona and Perugia, 1889) Palombi, 1943; Diplectanum grassei Oliver, 1974; Diplectanum melvillei Oliver and Paperna, 1984; Sciaenacotyle pancerii (Sonsino, 1891) Mamaev, 1989
Uranoscopus scaber Linnaeus, 1758
Tetraonchoides paradoxus Bychowsky, 1951
Monogenea were reported from hosts of different localities in the coast of Tunisia, at the northern area (Gulf of Tunis 37°N, 10°30’E), at the eastern area (Gulf of Hammamet 36°5’N, 10°45’E) and at the southern area (Gulf of Gabes 34°05’N, 10°26’E) (Fig. 1). In addition, fish were sampled from the Gulf of Gabes at Skhira (34°05’N; 10°01’E), Kerkennah (34°45’N; 11°17’E) and Sidi Mansour (34°46’N; 10°48’E). This fish has been caught by locals fishermen. The specimens, coming from the coastal fishing, were identified using Fisher et al. (1987) and Whitehead et al. (1984). These fish were dissected as soon as they died and examined for Monogenea. Living parasites were detached then partially compressed between slide and coverslip. They were examined using an optical microscope. Some parasites were fixed with 70 % alcohol and stained with Semichon’s acetic carmine. After dehydration using a graded ethanol series, the parasites were cleared in clove oil and mounted in Canada balsam for identification. Several specimens were fixed, stained and mounted directly in ammonium picrate glycerine after Malmberg (1957). The slides were sealed with Canada balsam. The host-parasite list of our work is arranged in alphabetical order of Monogenea-family (Table 3). Prevalence (P), mean abundance (MA) and mean intensity (MI) are determined according to Bush et al. (1997).
Fig. 1
Map of Tunisia showing sites of monogenean records.
Monogenean species diversity in the Gulf of Gabes.
Monogenean family
Monogenean species
Fish species
Number of fishes examined
P (%)
MA
Ml
Ancyrocephalidae
Haliotrema balisticus
Batistes capriscus
2
100
6
6
Ligophorus vanbenedenii
Chelon auratus
21
80
6.4
8
Ligophorus szidati
80
4.8
6
Ligophorus angustus
Chelon labrosus
4
100
3
3
Ligophorus macrocolpos
Chelon saliens
12
50
0.75
1
Ligophorus minimus
75
2
2
Ligophorus heteronchus
100
8.33
8
Ligophorus acuminatus
100
10.3
10
Capsalidae
Benedenia monticellii
Mugil cephalus
22
13.6
0.22
1
Capsala maccallumi
Euthynnus alletteratus
4
50
3
6
Diplectanidae
Diplectanum aeguans
Dicentrarchus labrax
2
100
10
10
Pseudodiplectanum syrticum
Synapturichthys kleinii
30
90
15.3
17
Lamellodiscus knoepffleri
Spicara smaris
9
88
4.4
5
Lamellodiscus elegans
Diplodus annularis
82
22
0.5
2
Lamellodiscus fraternus
71.4
4.7
6
Lamellodiscus ignoratus
Diplodus puntazzo
6
83.3
18
21
Diplodus vulgaris
5
100
28
28
Lamellodiscus theroni
Diplodus puntazzo
6
66
13
20.5
Lamellodiscus hilii
50
1
2
Lamellodisscus bidens
66
2.2
4
Lamellodiscus impervius
33
1.6
4
Lamellodiscus ergensi
Diplodus vulgaris
5
100
3.6
3
Lamellodiscus verberis
Lithognatus mormyrus
4
100
38
38
Lamellodiscus erythrini
Pagellus erythrinus
7
85.7
15.28
20
Lamellodiscus rastellus
Pagrus auriga
2
100
24
24
Lamellodiscus confusus
Sarpa salpa
14
100
12
12
Lamellodiscus parisi
28
0.5
2
Lamellodiscus echeneis
Sparus aurata
4
75
1.5
2
Hexostomatidae
Neohexostoma euthynni
Euthynnus alletteratus
4
75
6
8
Microcotylidae
Metamicrocotyla cephalus
Mugil cephalus
22
13
0.6
7
Polylabris tubicirrus
Diplodus annularis
82
2.5
1
1
Microcotyle erythrini
Pagellus erythrinus
7
42
0.85
2
Mazocraeidae
Grubea cochlear
Scomber japonicus
21
19
0.1
1
Pseudokuhnia minor
55
2.35
4
Kuhnia scombri
18
0.36
2
Pseudanthocotyloides heterocotyle
Engraulis encrasicolus
31
54
2.4
4
Mazocraes sp.
Sardinella aurita
46
8.6
0.08
1
Mazocraes pilchardi
Sardina pilchardus
63
15
0.19
1
Ethical Approval and/or Informed Consent
All applicable institutional, national and international guidelines for the care and use of animals were followed.
Results and Discussion
The checklist of Monogenea species recorded from Tunisian waters includes 153 species from 89 host species. Among them, 37 species are reported from elasmobranchs and two species, Neopolystoma euzeti Combes & Ktari, 1976 and Polystomoides ocellatus (Rudolphi, 1819) Ozaki, 1935 from the freshwater tortoise Mauremys caspica var. leprosa (Gmelin, 1774).
The diversity of Monogenea in the coast of Tunisia is similar to that of other regions of the Mediterranean. For example, in the coast of Italy, there are 141 species of Monogenea reported from 93 host species (Strona et al., 2010). However, this diversity is lower than the other regions of the World. In fact, 367 Monogenea are reported from 363 Mexican aquatic vertebrates (Mendoza-Garfias et al., 2017) and 581 species from 263 inland aquatic vertebrates in China (Xia et al., 2000). In general, the number of parasites reported must be dependent on the number of host examined as well as the number of host in the regions. Thus, areas with the highest host diversity have the highest diversity of parasites reported if the research efforts into fish parasites discovery are important. Jorge and Poulin (2018) note that there is a poor match between the host species richness and the parasite species discovery. Some areas with hotspots of host diversity, such as the tropical regions, suffer from a research deficit in parasite discovery.
In this list, twenty six families are recorded; among them the Diplectanidae Monticelli, 1903 which represents the major mono-genean family. Most species belong to the genus Lamellodiscus Johnston & Tiegs, 1922. Many phylogenetic analyses suggest that this group seem to be able to speciate rapidly, even in sympatric condition (Desdevises et al., 2002) leading to a high diversity.
This list shows that there are more species of Monopisthocotylea (93 species) than Polyopisthocotylea (60 species). Several studies of Monogenea diversity of fish from many localities show that the Monopisthocotylea is the richest group (Justine et al., 2010, 2012; Mendoza-Garfias et al., 2017). This difference is probably due to the differences in speciation rates between the two groups. In fact, sympatric speciation is important factor in parasite diversity, thus multiple congeners species in hosts are the product of speciation and diversification within the host (Poulin, 1999). Therefore, it appears that polyopisthocotyleans exhbit a lower level of speciation than monopisthocotyleans.
This difference can be also explained by the sampling effort. Indeed, examining additional hosts can probably change the number of monogeneans records and may also change the Monopisthocotylea/Polyopisthocotylea balance of recorded species. Moreover, Mendoza-Garfias et al. (2017) mentioned that the inventory of the monogeneans fauna in Mexico is not completed because a small number of aquatic vertebrates have been studied for monogeneans in this area.
We noted that the number of Monogenea recorded in the coast of Tunisia has increased in the past 2 decades and led to the description of many new species. The first species were reported by Ktari and Euzet & Ktari in the 1970s. After that, the number has increased with the studies of Neifar (1995, 2001). Since 2001, only 61 species have been reported. This diversity is related to the research effort in terms of the number of studies and the number of fish species examined each year.
The species accumulation curve of this group off the Tunisian waters shows a rising curve that is not reaching the asymptote (Fig. 2). This means that new species (or new records) of monogeneans will continue to be found when other hosts and other areas are examined. This number does not represent the real monogenean fauna of Tunisia but only the number of species reported by the few researchers who have worked in this region. Those described so far represent only a very small proportion of the real richness considering the potential host fauna. It is difficult to have an estimate of relative parasites biodiversity.
Fig. 2
Cumulative curve of monogeneans species recorded from Tunisia.
The discovery of cryptic species affects estimates of parasites diversity. Several cases show that what was once thought to be a single parasite species infecting a few host species turns out to represent on complex of cryptic species, each specific to a single host species (Poulin & Keeney, 2008). Their discovery depends mostly on the application of molecular methods.
Most Monogenea included in the checklist are restricted to fishes with high commercial value. The parasitological study of fishes with minor commercial interest allows us to complete the list of Monogenea from the coast of Tunisia. Moreover, the parasiofauna of some area such as the eastern coast is not well studied.
This list includes results from our study of Monogenea parasite of fish in the Gulf of Gabes. During this study, we have examined 22 teleost fish species belonging to nine families. A total of 37 species of Monogenea belonging to 16 genera and six families were found (Table 3). Among them 15 species are recorded for the first time off the coast of Tunisia (Table 1). The number of helminth species per host species was variable. Diplodus puntazzo (Walbaum) has the richest Monogenea fauna (5 species).
Ligophorus acuminatus Euzet and Suriano, 1977; Ligophorus heteronchus Euzet and Suriano, 1977; Ligophorus macrocolpos Euzet and Suriano, 1977; Ligophorus minimus Euzet and Suriano, 1977; Solostamenides mugilis (Vogt, 1879) Unnithan, 1971
Dasyatis marmorata (Steindachner, 1892)
Heterocotyle pastinacae Scott, 1904; Heterocotyle scotti Neifar, Euzet and Ben Hassine, 1998; Merizocotyle concinna (Scott, 1904) Chisholm, Wheeler and Beverley-Burton, 1995; Neoentobdella diadema (Monticelli, 1902) Kearn and Whittington, 2005; Trimusculotrema micracantha (Euzet and Maillard, 1967) Whittington and Barton, 1990
Dasyatis pastinaca (Linnaeus, 1758)
Heterocotyle pastinacae Scott, 1904; Heterocotyle scotti Neifar, Euzet and Ben Hassine, 1998; Heterocotyle similis Neifar, Euzet and Ben Hassine, 1998; Merizocotyle concinna (Scott, 1904) Chisholm, Wheeler and Beverley-Burton, 1995; Neonchocotyle pastinacae Ktari and Maillard, 1972; Neoentobdella diadema (Monticelli, 1902) Kearn and Whittington, 2005; Trimusculotrema micracantha (Euzet and Maillard, 1967) Whittington and Barton, 1990
Dasyatis tortonesei Capapé, 1975
Heterocotyle capapei Neifar, Euzet and Ben Hassine, 2000; Neoentobdella diadema (Monticelli, 1902) Kearn and Whittington, 2005; Thaumatocotyle tunisiensis Neifar, Euzet and Ben Hassine, 2000; Trimusculotrema micracantha (Euzet and Maillard, 1967) Whittington and Barton, 1990
Dentex dentex (Linnaeus, 1758)
Gotocotyla acanthura (Parona and Perugia, 1896) Meserve, 1938
Calicotyle palombi Euzet and Williams, 1960; Calicotyle stossichi Braun, 1899; Erpocotyle sp.; Triloculotrema euzetiBoudaya and Neifar, 2016
Mycteroperca costae (Steindachner, 1878)
Pseudorhabdosynochus bouainiNeifar and Euzet, 2007; Pseudorhabdosynochus dolicocolposNeifar and Euzet, 2007; Pseudorhabdosynochus enitsujiNeifar and Euzet, 2007; Pseudorhabdosynochus sinediscusNeifar and Euzet, 2007; Pseudorhabdosynochus sosiaNeifar and Euzet, 2007
Mycteroperca marginata (Lowe, 1834)
Echinoplectanum echinophallus (Euzet and Oliver, 1965) Justine and Euzet, 2006; Pseudorhabdosynochus beverleyburtonae (Oliver, 1984) Kritsky and Beverley-Burton, 1986; Pseudorhabdosynochus riouxi (Oliver, 1986) Santos, Buchmann and Gibson, 2000
Mycteroperca rubra (Bloch, 1793)
Pseudorhabdosynochus hayet Chaabane, Neifar, Gey and Justine, 2016; Pseudorhabdosynochus regius Chaabane, Neifar and Justine, 2015
Oblada melanura (Linnaeus, 1758)
Gotocotyla acanthura (Parona and Perugia, 1896) Meserve, 1938; Lamellodiscus elegans Bychowsky, 1957; Lamellodiscus gracilis Euzet and Oliver, 1966
Pagellus erythrinus (Linnaeus, 1758)
Lamellodiscus erythrini Euzet and Oliver, 1966; Microcotyle erythrini Van Beneden and Hesse, 1863
Pagrus auriga Valenciennes, 1843
Lamellodiscus rastellus Neifar, Euzet and Oliver, 2004
Pagrus coeruleostictus (Valenciennes, 1830)
Lamellodiscus sarculus Neifar, Euzet and Oliver, 2004; Lamellodiscus sigilatus Neifar, Euzet and Oliver, 2004
Cotyloatlantica mediterranea (Euzet and Trilles, 1960) Bravo-Hollis, 1984
Spicara maena (Linnaeus, 1758)
Bivagina alcedinis (Parona and Perugia, 1889) Yamaguti, 1963
Spicara smaris (Linnaeus, 1758)
Lamellodiscus knoepffleri Oliver, 1969
Synapturichthys kleinii (Risso, 1827)
Pseudodiplectanum syrticum Derbel, Boudaya and Neifar, 2007
Taeniura grabata Geoffroy Saint-Hilaire, 1817
Heterocotyle forcifera Neifar, Euzet and Ben Hassine, 1999; Heterocotyle mokhtarae Neifar, Euzet and Ben Hassine, 1999; Heterocotyle striata Neifar, Euzet and Ben Hassine, 1999; Neoentobdella apiocolpos (Euzet and Maillard, 1967) Kearn and Whittington, 2005
Diclidophora sp. Nudaciraxine imperium Châari, Derbel and Neifar, 2010; Pseudoaspinatrium gallieni (Euzet and Ktari, 1971) Mamaev, 1986
Umbrina cirrosa Linnaeus, 1758
Calceostomella inermis (Parona and Perugia, 1889) Palombi, 1943; Diplectanum grassei Oliver, 1974; Diplectanum melvillei Oliver and Paperna, 1984; Sciaenacotyle pancerii (Sonsino, 1891) Mamaev, 1989
Uranoscopus scaber Linnaeus, 1758
Tetraonchoides paradoxus Bychowsky, 1951
Monogenean species diversity in the Gulf of Gabes.
Monogenean family
Monogenean species
Fish species
Number of fishes examined
P (%)
MA
Ml
Ancyrocephalidae
Haliotrema balisticus
Batistes capriscus
2
100
6
6
Ligophorus vanbenedenii
Chelon auratus
21
80
6.4
8
Ligophorus szidati
80
4.8
6
Ligophorus angustus
Chelon labrosus
4
100
3
3
Ligophorus macrocolpos
Chelon saliens
12
50
0.75
1
Ligophorus minimus
75
2
2
Ligophorus heteronchus
100
8.33
8
Ligophorus acuminatus
100
10.3
10
Capsalidae
Benedenia monticellii
Mugil cephalus
22
13.6
0.22
1
Capsala maccallumi
Euthynnus alletteratus
4
50
3
6
Diplectanidae
Diplectanum aeguans
Dicentrarchus labrax
2
100
10
10
Pseudodiplectanum syrticum
Synapturichthys kleinii
30
90
15.3
17
Lamellodiscus knoepffleri
Spicara smaris
9
88
4.4
5
Lamellodiscus elegans
Diplodus annularis
82
22
0.5
2
Lamellodiscus fraternus
71.4
4.7
6
Lamellodiscus ignoratus
Diplodus puntazzo
6
83.3
18
21
Diplodus vulgaris
5
100
28
28
Lamellodiscus theroni
Diplodus puntazzo
6
66
13
20.5
Lamellodiscus hilii
50
1
2
Lamellodisscus bidens
66
2.2
4
Lamellodiscus impervius
33
1.6
4
Lamellodiscus ergensi
Diplodus vulgaris
5
100
3.6
3
Lamellodiscus verberis
Lithognatus mormyrus
4
100
38
38
Lamellodiscus erythrini
Pagellus erythrinus
7
85.7
15.28
20
Lamellodiscus rastellus
Pagrus auriga
2
100
24
24
Lamellodiscus confusus
Sarpa salpa
14
100
12
12
Lamellodiscus parisi
28
0.5
2
Lamellodiscus echeneis
Sparus aurata
4
75
1.5
2
Hexostomatidae
Neohexostoma euthynni
Euthynnus alletteratus
4
75
6
8
Microcotylidae
Metamicrocotyla cephalus
Mugil cephalus
22
13
0.6
7
Polylabris tubicirrus
Diplodus annularis
82
2.5
1
1
Microcotyle erythrini
Pagellus erythrinus
7
42
0.85
2
Mazocraeidae
Grubea cochlear
Scomber japonicus
21
19
0.1
1
Pseudokuhnia minor
55
2.35
4
Kuhnia scombri
18
0.36
2
Pseudanthocotyloides heterocotyle
Engraulis encrasicolus
31
54
2.4
4
Mazocraes sp.
Sardinella aurita
46
8.6
0.08
1
Mazocraes pilchardi
Sardina pilchardus
63
15
0.19
1
List of Monogenea parasites of Tunisian aquatic organisms. Records are listed by monogenoidean families and ordered per: parasite species (alphabetically), host species (alphabetically), reference (chronologically). NR, New record. Areas: 1, North; 2, East ; 3, South; 4. hydrographic network in the north.
Monogenoides species
Host species
Microhabitat
Reference
Family Amphibdellatidae Carus, 1885
Amphibdella paronaperugiae Llewellyn, 1960
Torpedo torpedo (Linnaeus, 1758) (1, 3)
gills
Neifar, 1995, 2001
Amphibdelloides benhassinae Tazerouti, Euzet and Neifar, 2006
Torpedo torpedo (Linnaeus, 1758) (1, 3)
gills
Neifar, 1995, 2001 ; Tazerouti et al., 2006
Amphibdelloides kechemirae Tazerouti, Euzet and Neifar, 2006
Torpedo marmorata Risso, 1810 (1, 3)
gills
Neifar, 1995, 2001 ; Tazerouti et al., 2006
Amphibdelloides vallei Llewellyn, 1960
Torpedo marmorata Risso, 1810 (1, 3)
gills
Neifar, 2001
Family Ancyrocephalidae Bychowsky, 1937
Glyphidohaptor plectocirra (Paperna, 1972) Kritsky, Galli and Yang, 2007
Siganus luridus (Rüppell, 1829), S. rivulatus Forsskål and Niebuhr, 1775(3)
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