Skip to main content
NCBI home page
Saudi Journal of Biological Sciences logoLink to Saudi Journal of Biological Sciences
. 2022 Mar 4;29(5):3610–3616. doi: 10.1016/j.sjbs.2022.02.052

The survey of ectoparasites on two species of Triakids (Mustelus mustelus and M. punctulatus) sharks from Tunisian coasts

Bouchra Benmansour a,b, Feriel Youssef a, Manel Ben Ali c, Bander Albogami c, Fehmi Boufahja d,⁎
PMCID: PMC9280258  PMID: 35844364

Abstract

Between 2018 and 2020, 696 fish belonging to two species of sharks from the Family Triakidae (Mustelus mustelus and M. punctulatus) were collected from the coasts of Tunisia and inspected for parasites. Six copepod taxa (Perissopus dentatus Steenstrup & Lütken, 1861, Eudactylinella alba Wilson, 1932, Kroyeria lineata Van Beneden, 1853, Nesippus orientalis Heller, 1865 and Lernaeopoda galei Krøyer, 1837, Kroyeria sp.), four isopod species (Anilocra physodes (Linnaeus, 1758), Emetha audouini (H. Milne Edwards, 1840), Ceratothoa parallela (Otto, 1828) and Ceratothoa oestroides (Risso, 1816)) and two monogenean species (Erpocotyle sp1. And Erpocotyle sp2) were collected. A large number of global host records was reported, including the occurrence of E. audouini on M. mustelus and of Erpocotyle sp.2 on M. punctulatus. The study of the diversity of parasites per host species revealed that M. mustelus had a higher parasitic richness compared to M. punctulatus. In this study, it was provided for the first records on ectoparasites on Triakidae sharks from Tunisian coasts and their infection indices.

Keywords: Mustelus mustelus, Mustelus punctulatus, Copepods, Isopods, Monogeneans, Tunisian coast

1. Introduction

The Tunisian coast of the Mediterranean Sea is known to harbour a great richness of chondrichthyans fish, with at least 62 described species (Bradaï et al., 2012). The Family Triakidae comprises four species, namely Galeorhinus galeus (Linnaeus, 1758), Mustelus mustelus (Linnaeus, 1758) M. asterias Cloquet, 1819, and M. punctulatus Risso, 1827 (Saidi et al., 2009). However, the taxonomic identification of species appurtenant to the genus Mustelus sp. remains cumbersome, given the unclear and sometimes contradictory diagnosis traits. The species of this genus are normally sympatric, potentially explaining their strong morphologic similarities (Compagno, 1984, Ebert and Stehmann, 2013, Marino et al., 2018). According to Bradaï et al. (2012) the species Mustelus punctulatus and M. mustelus are common along the Tunisian coasts and have similar diet (e.g., crustaceans, cephalopods and bony fishes) (Compagno, 1984, Saidi et al., 2009). Both species are of great commercial and gastronomic value in Tunisia; as such, as a consequence of their extensive consumption, they became vulnerable and even threatened in some areas, according to the International Union for Conservation of Nature and Natural Resources (IUCN).

The body of a shark confers many attachment sites for other organisms (Dippenaar and Molele, 2015). However, the studies of their parasites are scarce and with a main focus on single taxonomic group, such as copepods (Essafi, 1975, Benmansour and Youssef, 2019, Youssef et al., 2019) and monogenea (Neifar, 2001), disregarding other phyla. The aim of the current work was to provide original data on the parasitic taxa found on Mustelus mustelus and M. punctulatus bodies within Tunisian waters in order to analyse their taxonomic richness on both host species and to better understand the associations with their hosts.

2. Material and methods

2.1. Prospected area and specimen examination

Between 2018 and 2020, a total of 480 individuals of Mustelus punctulatus and 216 of M. mustelus, respectively, were examined for ectoparasites (Table 1). The fish were collected weekly from local Tunisian fishermen in Bizerte Bay, Gulfs of Tunis, Hammamet, and from Gabes (Sfax and Zarzis) (Fig. 1). The fish were transported for further laboratory analysis and identified according to Compagno (1984), Fischer et al., 1987, Serena, 2005. The host nomenclature followed data in Froese and Pauly (2019).

Table 1.

Sampling details of Mustelus mustelus and M. punctulatus

Host Sampling location Season Number of examined fish
Mustelus mustelus Bay of Bizerte37°16′25″N-9°53′14″E20 to 100 m Autumn 22
Winter 32
Spring 30
Summer 36
Gulf of Tunis37°00′0.00″N-10°29′59.99′’E20 to 100 m Autumn 30
Winter 30
Spring 30
Summer 30
Gulf of Hammamet36°04′60.00″N-10°44′59.99″E20 to 100 m Autumn 30
Winter 15
Spring 47
Summer 28
Gulf of Gabes 34°00′0.00″N-10°30′0.00″E20 to 100 m Autumn 30
Winter 25
Spring 25
Summer 40



Mustelus punctulatus Bay of Bizerte37°16′25″N-9°53′14″E20 to 100 m Autumn 7
Winter 6
Spring 9
Summer 11
Gulf of Tunis37°00′0.00″N-10°29′59.99′’E20 to 100 m Autumn 8
Winter 7
Spring 10
Summer 12
Gulf of Hammamet36°04′60.00″N-10°44′59.99″E20 to 100 m Autumn 7
Winter 7
Spring 11
Summer 9
Gulf of Gabes34°00′0.00″N-10°30′0.00″E20 to 100 m Autumn 24
Winter 28
Spring 30
Summer 30
Open in a new tab

Fig. 1.

Fig. 1

Open in a new tab

Sampling sites, indicated by red circles.

2.2. Parasitological investigations

For every fish individual, all body traits (i.e. skin, mouth, gills, fins, cloaca, and nasal cavity) were thoroughly examined. Gills were placed afterwards in seawater in Petri dishes and arches of each gill carefully examined. Information about sampling date, prospected areas, taxonomic nomenclature and shape and corpulence of the host fishes and their parasite’s microhabitats were noted.

Copepods and isopods were extracted from hosts and fixed in ethanol (70%), afterwards cleared for 2 h in lactic acid before being examined observed undera 50× stereomicroscope (Model WildHeerbrugg M5A) and a Nikon DS-Fi2 camera coupled with a Nikon microscope (Image Software NIS Elements Analysis Version 4.0 Nikon 4.00.07–build 787–64 bit). The specimens were dissected and temporary mounted on slides in lactophenol (Yamaguti, 1963). The taxonomic identification of parasites was done based on taxonomic keys of Deets, 1994, Kabata, 2003, Ho and Kim, 2004, Boxshall and Halsey, 2004.

The examination of the collected isopods comprises the observation of their morphologic features and of different appendices in order to identify them to species level. Gender, life stage and fixing site of collected specimens were also identified. The taxonomic identification of isopods was performed according to the keys of Trilles, 1979, Bruce, 1986, Keable and Bruce, 1997, Horton, 2000, Charfi-Cheikhrouha et al., 2000.

Iron acetocarmine was necessary to stain monogeneans to be examined in permanent mounts, using Canada balsam (Bailenger and Neuzil, 1953). Monogeneans species identification was carried using the keys of Sproston, 1946, Neifar et al., 1998, Tazerouti et al., 2011, Chero et al., 2018.

2.3. Data analyses

The infestation rates were assessed through prevalence (P = N/H × 100) and mean intensity (MI = n/N) [N: number of infected hosts; H: total number of hosts examined; n: total number of collected individuals of one parasitic species] (see Margolis et al., 1982, Bush et al., 1997). The software Plymouth Routines In Multivariate Ecological Research ‘PRIMER’v.5.0 was used to quantify the parasites’ taxonomic diversity and evenness on their distribution on hosts, following the calculation of the indices Margalef’s species richness (SR), Shannon index (H′) and Pielou’s evenness (E).

3. Results

3.1. Taxonomic diversity

A total of twelve parasites, comprising copepods, isopods and monogeneans were identified (Table 2). Copepods comprised the most diverse group, namely:Eudactylinella alba Wilson, 1932, Kroyeria sp., Kroyeria lineata Van Beneden, 1853, Perissopus dentatus Steenstrup and Lütken, 1861, Nesippus orientalis Heller, 1865 and Lernaeopoda galei Krøyer, 1837 (Table 2, Fig. 2). Kroyeria sp. could comprise a new species that awaits further investigations. It was also observed that M. mustelus had a higher number of parasites, namely six species (Fig. 3) compared to M. punctulatus, which was the hosted of a single copepod species, Lernaeopoda galei.

Table 2.

List of ectoparasites species and their hosts. NEF: number of examined fish; P (%): prevalence; MI: mean intensity.

Host NEF Parasite taxonomic group Parasite family Parasite species Microhabitat P (%) MI
Mustelus mustelus 480 Copepods Eudactylinidae Eudactylinella alba Gills 1.4 1.1
Kroyeriidae Kroyeria lineata Gills 3.95 1
Kroyeria sp. Gills 1.04 1
Lernaeopodidae Lernaeopoda galei Cloacae cavity 2.50 1.2
Pandaridae Nesippus orientalis Mouth 0.41 1
Perissopus dentatus Dorsal fin 0.83 1
Isopods Cymothoidae Anilocra physodes Body side 0.41 1
Emetha audouini Body side 0.41 1
Ceratothoa parallela Cloacae cavity 1.8 1.16
Monogenea Hexabothriidae Erpocotyle sp. 1 Gills 6.04 2



Mustelus punctulatus 216 Copepods Lernaeopodidae Lernaeopoda galei Cloacae cavity 3.24 1
Isopods Cymothoidae Ceratothoa oestroides Gills 2.32 1
Ceratothoa parallela Cloacae cavity 1.5 1.5
Monogenea Hexabothriidae Erpocotyle s p. 2 Gills 5.55 1.5
Open in a new tab

Fig. 2.

Fig. 2

Open in a new tab

Mustelus mustelus and its parasites; a: Eudactylinella alba; b: Kroyeria lineata; c: Kroyeria sp.; d: Lernaeopoda galei; e Nesippus orientalis; f: Mustelus mustelus; g: Perissopus dentatus; h: Anilocra physodes; i: Emetha audouini; j: Ceratothoa parallela; k: Erpocotyle sp.

Fig. 3.

Fig. 3

Open in a new tab

Mustelus punctulatus and its parasites; a: Eudactylinella alba; b: Mustelus punctulatus; c: Erpocotyle sp.; d: Ceratothoa oestroides; e: Ceratothoa parallela.

Both hosts were infected by four isopod species (Table 2). M. mustelus was the host of three species (i.e. Anilocra physodes (Linnaeus, 1758), Emetha audouini (H. Milne Edwards, 1840) and Ceratothoa parallela (Otto, 1828)) whereas M. punctulatus of two (i.e. Ceratothoa parallela and Ceratothoa oestroides (Risso, 1816)).

Two monogenean species were also collected from both hosts: Erpocotyle sp. 1 and Erpocotyle sp. 2.

3.2. Parasitological indices of the studied parasite taxa

Data on the prevalence, mean intensity and infestation area are given in Table 2. Data analysis suggested that prevalence was low for most copepod and isopods but slightly higher for the monogeneans (Table 2). Among copepods, the species K. lineata found on M. mustelus presented the highest prevalence (P = 3.95%). Moreover, the species Lerneaopoda galei presented the second highest prevalence degree on M. punctulatus (P = 3.24%) and M. mustelus (P = 2.50%). This parasite had the highest mean intensity (MI = 1.2) among copepods (Table 2).

Nevertheless, the species N. orientalis, found on M. mustelus, presented the lowest prevalence (P = 0.41%) (Table 2).

The isopods had also low parasitological indices. C. oestroides on M. punctulatus had the highest prevalence (P = 2.32%), whereas C. parallela, found on both hosts, had a relatively higher prevalence on M. mustelus (P = 1.80%) and on M. punctulatus (P = 1.50%). Moreover, both parasites displayed a relatively high mean intensity, varying between 1 and 1.5 (Table 2).

The species A. physodes and E. audouini were found on M. mustelus and had the lowest parasitological indices (P = 0.41% and MI = 1) (Table 2).

The Monogeneans presented the highest parasitological indices recorded during this survey. The prevalence of Erpocotyle sp 1. on M. mustelus was P = 6.04% and of Erpocotyle sp.2 on M. punctulatus P = 5.55%. The mean intensity of both monogeneans was also high and varied between 1.5 and 2 (Table 2).

3.3. Parasitic richness per host taxa

The parasitic richness on both hosts revealed that M. mustelus was the richest (SR = 10), by hosting six copepods species, three species of isopods and one monogenean species (Table 3), whereas M. punctulatus had a lower parasitic richness (SR = 4), with one copepod, two isopods and one monogenean species (Table 3).

Table 3.

Parasites’ diversity indice for Mustelus mustelus and Mustelus punctulatus. SR: Species richness, H′: Shanon-Weaver index, E: Pielou index of evenness.

Host Index
SR H′ E
Mustelus mustelus 10 1,69 0,73
Mustelus punctulatus 4 0,89 0,64
Open in a new tab

The maximum value of Shannon index (H′ = 1.69) of the parasite assemblage was found on M. mustelus. A value of 0.89 for Shannon-Weaver index was found for M. punctulatus (Table 3), confirming that the former host possessed the highest parasitic richness.

The study of the Pielou index of evenness revealed that M. mustelus was the host of a highly diverse community of parasites (E = 0.73), followed by M. punctulatus (E = 0.64).

3.4. Parasites microhabitats

The parasites presence was intimately related to distinct microhabitats, as described in Table 2. Most parasites were collected from hosts’ gills. In turn, few other species were collected from cloaca (i.e.L. galei) or externally, from skin (i.e.,A. physodes and E. audouini). The species N. orientalis was the only parasite species collected from the mouth of M. mustelus.

4. Discussion

The current work revealed a high taxonomic diversity of ectoparasites on both species of sharks along the Tunisian coast, comprising a total of 12 species. The results obtained are in accordance with those of Raibaut et al. (1998), which confirmed the fact that the sharks appartenant to Families Carcharhinidae (i.e.Prionace glauca (Linnaeus, 1758)) and Triakidae (i.e. M. mustelus) were frequently associated with the maximum richness for copepods among elasmobranch taxa in the Mediterranean Sea.

The copepods collected from both host species were the dominant taxonomic group. Indeed, the copepods comprised the highest diversity, with six species, followed by isopods with four species and monogeneans with two species. According to Carrier et al. (2012), among the ectoparasites of elasmobranchs, the subclass of copepods presented the highest diversity.

Among the parasite copepods of M. mustelus, K. lineata had the highest prevalence (P = 3.95%), whereas N. orientalis had the lowest values (P = 0.41%).Is known that species from Kroyeria sp. genus are associated with a higher parasite load on their hosts compared to other copepods (Deets, 1994).

Among the six identified copepods, only the species L. galei was collected from both sharks (M. mustelus and M. punctulatus). This species is euryxenous (sensu Euzet and Combes, 1980) and is a common parasite among elasmobranchs. Moreover, this species was previously reported from various host taxa (Raibaut et al., 1998, Henderson et al., 2003, Dippenaar, 2004, Karaytug et al., 2004, Gaevskaya, 2012). Moreover, according to previous investigations, this species appears to have a preference for Triakids (see Raibaut et al., 1998, Dippenaar, 2004, Karaytug et al., 2004 for M. mustelus and Raibaut et al. (1998) for M. punctulatus). This parasite had a higher prevalence for M. punctulatus (P = 3.24%) compared to M. mustelus (P = 2.50%).

E. alba was found on the gills of M. mustelus. This copepod species is euryxenous, infesting numerous species of fish (Izawa, 2011). As previously described by Raibaut et al. (1998) from Mediterranean Sea and by Essafi (1975), it was also found on Dasyatis pastinaca from the Tunisian coasts. This is the first record of this parasite on M. mustelus in Tunisia as elsewhere.

K. lineata was another parasite found on the gills of M. mustelus. This species is cosmopolite and was previously reported from various locations worldwide, such as: Pacific Ocean (Izawa, 2008) and the Atlantic Ocean (Canadian coasts, see Deets, 1994, Benz, 1994). In Tunisia, K. lineata was found on M. asterias (Cloquet, 1918), and on M. mustelus (Essafi, 1975). This copepod species is stenoxenous, infesting mostly Triakidae species.

Kroyeria sp. was found on the gills of M. mustelus with low prevalence (P = 1.04%). The morphological study revealed that this species presented many differences compared to the other species known from the same genus from the Mediterranea Sea and the Atlantic Ocean. However, further studies are needed to support this hypothesis.

N. orientalis, found in the mouth of M. mustelus, is a well-known parasite of chondrichthyans (Cressey, 1967, Cressey, 1970). This euryxenous species has a large geographical distribution and was reported in the South African coasts by Dippenaar and Jordaan (2012) and from the Mediterranean Sea by Raibaut et al. (1998) on Alopias vulpinus (Bonnaterre, 1788), M. mustelus and M. punctulatus. In Tunisia, this species was found on M. mustelus and M. punctulatus by Essafi (1975).

P. dentatus is euryxenous and was found in South African coast (Dippenaar and Jordaan, 2007). This copepod presents a large Mediterranean geographical distribution. P. dentatus was inventoried by Raibaut et al. (1998) and by Essafi (1975) in Tunisia water from M. mustelus.

Among isopods, it wasobserved that M. mustelus had a slightly higher isopod richness (three species) than M. punctulatus (two species). The latter host was exclusive for Ceratothoa sp. species, whereas the former was the host of a more diverse parasitic fauna (A. physodes, E. audouini and C. parallela).

The genus Ceratothoa sp. had the highest parasitological indices are known from a large number of chondrichthyans sharks (Trilles, 1994).

C. parallela has euryxenous specificity and was reported from various Mediterranean areas (Trilles, 1994, Papapanagiotou and Trilles, 2001, Ramdane et al., 2007, Öktener and Trilles, 2004, Ferri et al., 2008). In Tunisia, this parasite was observed by Charfi-Cheikhrouha et al. (2000) on teleosteen fishes. According to Trilles (1994), this species was found on chondrichthyan fishes (i.e.Raja clavata Linnaeus, 1758 and R. asterias Delaroche, 1809) on both females and males. According to Pollerspöck and Straube (2018), this parasite has never been encountered before on M. mustelus and M. punctulatus in the world.

C. oestroides is a ubiquitous and euryxenic species. It was reported in the Mediterranea area (Trilles, 1994, Horton, 2000, Öktener and Trilles, 2004, Bariche and Trilles, 2005, Ramdane et al., 2007). In Tunisia, this isopod was found on various species of teleosteans (Bradaï, 2000); however, this is its first record on cartilaginious fish in the Mediterraneaarea, as elsewhere (Pollerspöck and Straube, 2018).

A. physodes and E. audouini are euryxenic species, with a wide host range and marked preference for teleosteans (Trilles, 1979). The former species has also a marked preference for Sparids and Maenids (Trilles, 1979) and was reported from various locations in the Mediterranean Sea, such as in Algeria (Trilles, 1994, Ramdane et al., 2007), Turkey (Öktener and Trilles, 2004, Koc et al., 2018) and Lebanon (Bariche and Trilles, 2005). In Tunisia, Charfi-Cheikhrouha et al. (2000) reported the occurrence of this parasite on several species of Teleosteans. The species E. audouini was found in several species of fish worldwide (Ramdane, 2007; Öktener and Trilles, 2004). The current record is the first for Tunisian coasts and on the shark M. mustelus.

The marked preference of both isopods for teleost fishes may explain their low prevalence (P = 0.41%) found in the current survey.

Chondrichthyans are known to host an extremely large number of monogeneans (Neifar, 2001, Boudaya and Neifar, 2016). However, it was only possible to collect two parasite species from the sharks M. mustelus and M. punctulatus. For M. punctulatus, a new species of Monogene, Triloculotrema euzeti n.sp. has been reported by Boudaya and Neifar (2016) in Tunisia. However, this parasite was found only in small host individuals in which the total length (TL) was less than 60 cm. In our study, all the fish examined had a length greater than 60 cm. For this reason, we did not find this monogene.

The two identified species belong to Erpocotyle genus. However, they appear to be different to E. catenulata (Guberlet, 1933) and E. laevis Van Beneden and Hesse, 1863, which are well-known parasites of M. mustelus (Lambert and Millard 1979; Llewellyn et al. 1984). Moreover, the current record of Erpocotyle species is the first for the shark M. punctulatus.

Host, microhabitat or site selections are displayed to various degrees throughout parasite taxa and groups (Kabata, 2003). Globally, all parasites exhibit high specificities in terms of attachment site and host (Kabata, 2003). Erpocotyle species are typically found on the gills of their host (Sproston, 1946).

The Family Cymothoidae is known for its binding site rather than host specificity. This family comprises species with unique morphologic features, adapted to specific attachment sites on hosts and some genera with precise location (Fogelman and Grutter, 2008). Only E. audouini is known to be found in the mouth of its host (Ramdane, 2010). The current survey presents a new binding site, whereas the rest of other isopod species were found in their typical binding sites.

The physiologic and morphologic mechanisms that determine the selection of a given site by a specific copepod are still unidentified for most species (Kabata, 2003). However, most of copepods were encountered on gills on both hosts. It was noted that L. galei was found in the same microhabitat (cloaca) on both hosts, suggesting that it may be the preferential binding site to this anatomic part on Triakidae sharks.

5. Conclusions

In the current study it was observed that the parasite richness of M. mustelus and M. punctulatus differs, even if both host species have similar ecologic and ethologic characteristics. This is probably the cause of intrinsic characters of each host species.

The results could be related to the lower population abundance of M. punctulatus compared to M. mustelus off the Tunisian coasts. In fact, the density of both sharks is considered as one of the universal key components in driving the interspecific parasite diversity.

This current survey completed the known data on parasitic infections for sharks M. mustelus and M. punctulatus in Tunisian coasts, supporting the further use of parasites for a better understanding of the biology and ecology of their hosts.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

Acknowledgments

The authors would like to thank Pr Geoff A. Boxshall (Natural History Museum, London) for his valuable advice and support during the taxonomic identification of parasite species. The authors extend their appreciation to the deanship of scientific research for funding this article by Taif University Research Supporting Project number (TURSP-2020/301), Taif University, Taif, Saudi Arabia.

Funding

The authors extend their appreciation to the deanship of scientific research for funding this article by Taif University Research Supporting Project number (TURSP-2020/301), Taif University, Taif, Saudi Arabia.

Footnotes

Peer review under responsibility of King Saud University.

References

  1. Bailenger J., Neuzil E. Nouvelles techniques d’examen des Helminthes: fixation; coloration; montage. Ann. Parasitol. 1953;28(5–6):392–398. [PubMed] [Google Scholar]
  2. Bariche M., Trilles J.P. Preliminary check-list of Cymothoids (Crustacea, Isopoda) from Lebanon, parasiting on marine fishes. Zool. Middle. East. 2005;34:5–12. doi: 10.1080/09397140.2005.10638082. [DOI] [Google Scholar]
  3. Benmansour B., Youssef F. Preliminary analysis of parasitic copepod species richness of Chondrichthyan fish off Tunisian coasts. Bull. Inst. Nat. Sci. Tech. Mer. 2019;46:95–106. [Google Scholar]
  4. Benz, G.W., 1994. Evolutionary biology of Siphonostomatoida (Copepoda) parasitic on vertebrates. Ph.D. thesis, University of British Columbia, Vancouver, Canada.
  5. Boudaya L., Neifar L. Triloculotrema euzeti n.sp (Monogenea, Monocotylidae) from the nasal tissues of the blackspotted smooth-hound Mustelus punctulatus (Carcharhiniformes, Triakidae) from off Tunisia. Parasite. 2016;23:62. doi: 10.1051/parasite/2016072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boxshall G.A., Halsey S.H. The Ray Society; London, UK: 2004. An Introduction to Copepod Diversity. [Google Scholar]
  7. Bradaï, M.N., 2000. Diversité du peuplement ichtyque et contribution à la connaissance des sparidés du Golfe de Gabès. PhD thesis, University of Sfax, Tunisia.
  8. Bradaï, M.N., Saïdi, B., Enajjar, S., 2012. Elasmobranchs of the Mediterranean and Black Sea: Status, Ecology and Biology. Bibliographic Analysis. In: FAO: Studies and Reviews. General Fisheries Commission for the Mediterranean., 91, Rome, Italy. p. 103.
  9. Bruce N.L. Cirolanidae (Crustacea: Isopoda) of Australia. Rec. Aust. Mus. 1986;6:1–239. [Google Scholar]
  10. Bush, A.O., Lafferty, K.D., Lotz, J.M., Shostak, A.W., 1997. Parasitology meets ecology on its own terms: Margolis et al. Revisited. J. Parasitol. 83, 575–583. doi: 10.2307/3284227. [PubMed]
  11. Carrier J.C., Musick J.A., Heithaus M.R. CRC Press, Taylor & Francis group; Boca Raton, USA: 2012. Biology of Sharks and Their Relatives. [Google Scholar]
  12. Charfi-Cheikhrouha F., Zghidi W., Ould Yarba L.M., Trilles J.P. Les Cymothoidae (Isopodes parasites de poissons) des côtes tunisiennes: écologie et indices parasitologiques. Syst. Parasitol. 2000;46:146–150. doi: 10.1023/A:1006336516776. [DOI] [PubMed] [Google Scholar]
  13. Chero J.D., Cruces C.L., Saez G., Camargo A.C.A., Santos C.P., Luque J.L. Hypanocotyle bullardi n. gen. n. sp. (Monogenea: Hexabothriidae) from gill of the diamond stingray Hypanus dipterurus (Jordan et Gilbert) (Myliobatiformes: Dasyatidae) in the Southeastern Pacific Ocean off Peru. Parasitol. Int. 2018;67:425–430. doi: 10.1016/j.parint.2018.03.010. [DOI] [PubMed] [Google Scholar]
  14. Compagno, L.J.V., 1984. FAO Species Catalogue. Vol. 4. Sharks of the World. An Annotated and Illustrated Catalogue of Shark Species Known to Date. Part 2-Carcharhiniformes. In: FAO 263 Fisheries Synopsis, Rome, Italy, vol. 125. pp. 251–655.
  15. Cressey R.F. Revision of the family Pandaridae (Copepoda, Caligoida) Proc. U.S. Nat. Mus. 1967;121:1–133. [Google Scholar]
  16. Cressey R.F. Copepods parasitic on sharks from the west coast of Florida. Smithson. Contr. Zool. 1970;38:1–30. [Google Scholar]
  17. Deets, G.B., 1994. Copepod-Chondrichthyan Coevolution: A Cladistic Consideration. PhD thesis, University of British Columbia, Vancouver, Canada.
  18. Dippenaar S.M. Reported siphonostomatoid copepods parasitic on marine fishes of southern Africa. Crustaceana. 2004;77:1281–1328. [Google Scholar]
  19. Dippenaar S.M., Jordaan B.P. New host and geographical records of siphonostomatoid copepods associates with elasmobranchs off the KwaZulu – Natal coast. South Africa. Onderstepoort J. Vet. Res. 2007;74:169–175. [PubMed] [Google Scholar]
  20. Dippenaar S.M., Jordaan B. Notes on the morphology and ecology of the adult females of Nesippus species (Siphonostomatoida: Pandaridae) with a key for identification. Zootaxa. 2012;3170:18–30. [Google Scholar]
  21. Dippenaar S.M., Molele R.A. Siphonostomatoid copepods infecting Squalus acutipinnis Regan, 1908 of South Africa. Afr. J. Mar. Sci. 2015;37:605–608. doi: 10.2989/1814232X.2015.1093024. [DOI] [Google Scholar]
  22. Ebert, D.A., Stehmann, M.F.W., 2013. Sharks, batoids and chimeras of the North Atlantic FAO Species Catalogue for Fishery Purposes. N° 7., Rome, FAO. 523 pp.
  23. Essafi, K. 1975. Contribution à l’étude des copépodes parasites des sélaciens de Tunisie. PhD thesis, Université Tunis El Manar, Tunis II, Tunisia.
  24. Euzet, L., Combes, C., 1980. Les problèmes de l’espèce chez les animaux parasites. In: Les problèmes de l’espèce dans le règne animal. Mém. Soc. Zool. Fr. 40, 239–285.
  25. Ferri J., Petric M., Matic-Skoko S., Dulcic J. New host record, black scorpionfish Scorpaena porcus (Pisces, Scorpaenidae) for Nerocila orbignyi and Ceratothoa parallela (Crustacea, Isopoda, Cymothoidae) Acta Adriat. 2008;49:255–258. [Google Scholar]
  26. Fischer W., Bauchot M.L., Schneider M. Fiche F.A.O d’identification des espèces pour les besoins de la pêche Méditerranéenne et Mer Noire. Zone. Pêche. 1987;37:761–1529. [Google Scholar]
  27. Fogelman R., Grutter A. Mancae of the parasitic cymothoid isopod, Anilocra apogonae, an early life history, host-specificity, and effect on growth and survival of preferred young cardinal fishes. Coral Reefs. 2008;27:685–693. [Google Scholar]
  28. Froese, R., Pauly, D., 2019. FishBase, <www.fishbase.org>.
  29. Gaevskaya, A.V., 2012. Parasites and Diseases of Fishes in the Black Sea and the Sea of Azov. I. Sevastopol: Ekosi-Gidrofizika.
  30. Henderson A.C., Flannery K., Dunne J. Biological observations on shark species taken in commercial fisheries to the west of Ireland. Biol. Environ.: Proc. R. Ir. Acad. 2003;103:1–7. [Google Scholar]
  31. Ho J.S., Kim I.H. Lernanthropid copepods (Siphonostomatoida) parasitic on fishes of the Gulf of Thailand. Syst. Parasitol. 2004;58:17–21. doi: 10.1023/B:SYPA.0000023828.12294.d1. [DOI] [PubMed] [Google Scholar]
  32. Horton T. Ceratothoa steindachneri (Isopoda: Cymothoida) new to British waters with a key to north-east Atlantic and Mediterranean Ceratothoa. J. Mar. Biol. Assoc. U.K. 2000;80:1041–1052. [Google Scholar]
  33. Izawa K. Redescription of four species of Kroyeria and Kroyerina (Copepoda, Siphonostomatoida, Kroyeriidae) infecting Japanese sharks. Crustaceana. 2008;81:695–724. doi: 10.1163/156854008784513465. [DOI] [Google Scholar]
  34. Izawa, K., 2011. Dangoka japonica nov. gen. sp. and Eudactylinella alba Wilson, 1932 (Copepoda, Siphonostomatoida, Eudactylinidae) infesting japanese Elasmobranchs. Crustaceana 84(10), 1269–1277.
  35. Kabata, Z., 2003. Copepods Parasitic on Fishes. 2nd, revised edition. Synopses of the British Fauna N° 47, 2nd, revised edition. Backhuys, pp. 1–274.
  36. Karaytug S., Sak S., Alper A. Parasitic copepod Lernaeopoda galei Kroyer, 1837 (Copepoda: Siphonostomatoida): A first record from Turkish seas. Turk. J. Zool. 2004;28(2):123–128. [Google Scholar]
  37. Keable S.J., Bruce N.L. Redescription of the North Atlantic and Mediterranean species of Natatolana (Crustacea:Isopoda: Cirolanidae) J. Mar. Biol. Assoc. U.K. 1997;77:655–705. [Google Scholar]
  38. Koc C., Aldemir O.S., Selamoglu Z. Helminth parasites of sea bass (Dicentrarchus labrax, Linnaeus, 1758), gray mullet (Chelon labrosus, Aisso, 1826) from Bafa Lake, Turkey. J. Surv. Fish. Sci. 2018;5(1):1–6. [Google Scholar]
  39. Margolis L., Esche G.W., Holmes J.C., Kuris A.M., Schrad G.A. The use of ecological terms in parasitology (Report of an ad hoc committee of the American Society of Parasitologists) J. Parasitol. 1982;68:131–133. doi: 10.2307/3281335. [DOI] [Google Scholar]
  40. Marino I.A.M., Finotto L., Colloca F., Di Lorenzo M., Gristina M., Farrell E.D., Zane L., Mazzoldi C. Resolving the ambiguities in the identification of two smooth-hound sharks (Mustelus mustelus and Mustelus punctulatus) using genetics and morphology. Mar. Biodiv. 2018;48(3):1551–1562. [Google Scholar]
  41. Neifar, L., 2001. Biodiversité et évolution des plathelminthes parasites des élasmobranches. PhD thesis, Faculty of Sciences of Tunis, University of Tunis ElManar, Tunisia.
  42. Neifar L., Euzet L., Ben Hassine O.K. Nouveaux Monocotylidae (Monogenea), parasites branchiaux de Dasyatis pastinaca (L.) (Euselachii, Dasyatidae). Compléments à la description de Heterocotyle pastinacae Scott, 1904. Syst. Parasitol. 1998;41:197–208. [Google Scholar]
  43. Öktener A., Trilles J.P. Report on Cymothoids (Crustacea, Isopoda) collected from marine fishes in Turkey. Acta Adriatica. 2004;45:145–154. [Google Scholar]
  44. Papapanagiotou E.P., Trilles J.P. Cymothoid parasite Ceratothoa paralella inflicts great losses on cultured gilthead sea bream Sparus aurata in Greece. Dis. Aquat. Org. 2001;45:237–239. doi: 10.3354/dao045237. [DOI] [PubMed] [Google Scholar]
  45. Pollerspöck, J., Straube, N., 2018. www.shark-references.com, accessed on November 6, 2018.
  46. Raibaut A., Combes C., Benoit F. Analysis of the parasitic copepod species richness among Mediterranean fish. J. Mar. Syst. 1998;15:185–206. [Google Scholar]
  47. Ramdane, Z., 2010. Identification et écologie des ectoparasites Crustacées des poisons Téléostéens de la côte Est algérienne. PhD thesis, Faculty of Sciences, University of Badji Makhtar, Annaba., Algeria.
  48. Ramdane Z., Bensoulah M.A., Trilles J.P. The Cymothoidae (Crustacea, Isopoda), parasites on marine fishes, from Algerian fauna. Belg. J. Zool. 2007;137:67–74. doi: 10.2478/s11686-008-0033-8. [DOI] [Google Scholar]
  49. Saidi B., Bradaï M.N., Bouaïn A. Reproductive biology and diet of Mustelus punctulatus (Risso, 1826) (Chondrichthyes: Triakidae) from the Gulf of Gabès, central Mediterranean Sea. Sci. Mar. 2009;73:249–258. [Google Scholar]
  50. Serena F. FAO Species Identification Guide for Fisheries Purpose; Rome: 2005. Field identification guide to sharksand rays of Mediterranean and Black Sea; p. p97. [Google Scholar]
  51. Sproston N.G. A synopsis of the monogenetic trematodes. Trans. Linn. Soc. Lond. 1946;25:185–600. [Google Scholar]
  52. Tazerouti F., Neifar L., Euzet L. Redescription of Monocotyle myliobatis (Monogenea, Monocotylidae) from the type host Myliobatis aquila (Elasmobranchii, Myliobatidae) off the Algerian coast. Acta Parasitol. 2011;56:274–279. [Google Scholar]
  53. Trilles J.P. Les Cymothoidae (Isopoda, Flabellifera: parasites de poissons) duRijksmuseum Van Natuurlijke Historie de Leiden. II. Afrique, Amérique et Régions Indo Ouest-Pacifiques. Zool. Meded. 1979;54:245–275. [Google Scholar]
  54. Trilles J.P. Les Cymothoidae (Crustacea, Isopoda) du monde (Prodrome pour une faune) Stud. Mar. 1994;21(22):1–288. [Google Scholar]
  55. Yamaguti, S., 1963. Parasitic Copepoda and Branchiura of fishes. In: Interscience (Ed.). New York, London and Sydney, pp. 1–1104.
  56. Youssef F., Tlig Zouari S., Benmansour B. New host-parasite records of siphonostomatoid copepods infesting elasmobranch fishes in Tunisian waters. J. Mar. Biol. Assoc. U.K. 2019;99:851–855. [Google Scholar]

Articles from Saudi Journal of Biological Sciences are provided here courtesy of Elsevier

RESOURCES