DOI: 10.2478/s11686-008-0048-1 © 2008 W. Stefañski Institute of Parasitology, PAS Acta Parasitologica, 2008, 53(3), 258–262; ISSN 1230-2821 crampus sp. nov. (, ), a parasite of Dentex maroccanus (Teleostei, ) from off Tunisia

Lassâd Neifar Laboratoire de Biodiversité et EcosystPmes Aquatiques, Faculté des Sciences de Sfax, BP 1171, 3000 Sfax Tunisia

Abstract Lamellodiscus crampus sp. nov. (Monogenea, Diplectanidae) is described from the gills of Dentex maroccanus (Valenciennes) collected from the Gulf of GabPs (Tunisia) in the oriental part of Mediterranean Sea. The new species belongs to the “ignora- tus” group (sensu Oliver 1987) characterized by a lamellodisc with complete lamellae and a “lyre” shaped male copulatory organ, and the “ignoratus” sensu stricto subgroup, characterized by a with simple lateral dorsal bars, as proposed by Amine and Euzet (2005). Lamellodiscus crampus can be easily distinguished from all the congeneric species of the subgroup “ignoratus” by the presence, in the “lyre” male copulatory organ, of five spines in the distal portion on the axial side of the paired piece.

Keywords Monogenea, Diplectanidae, Lamellodiscus crampus sp. nov., Sparidae, Dentex maroccanus, Gulf of GabPs

Introduction During our investigations on monogenean parasites from Sparidae off the Tunisian coast, we collected from the gills of Diplectanids from the genus Lamellodiscus Johnston et Tiegs, Dentex maroccanus Valenciennes, 1830 a new Lamellodiscus 1922, are gill parasites of Teleostei. Thirty-one species are belonging to the “ignoratus” s. str. subgroup. This parasite is currently known in the Mediterranean Sea (Oliver 1987; herein described. Neifar et al. 2004; Amine and Euzet 2005; Amine et al. 2006a, b; Amine et al. 2007a, b). According to the structure of lamellodisc, two morphological groups were recognised by Materials and methods Oliver (1987): the “ignoratus” group, with 10 complete lamel- lae, and the “elegans” group, with lamellae equally subdivid- Fifteen specimens of Dentex maroccanus were collected by ed in two parts excepting for first and last lamellae. This trawler from the south eastern area of the Gulf of GabPs grouping is compatible with the molecular phylogenetic (33°45´N, 11°38´E) during 2007 and 2008. The host species analysis obtained for the Lamellodiscus species (Desdevises was identified using Fisher et al. (1987) and Bauchot and et al. 2002). Within the “ignoratus” group, Amine and Euzet Hureau (1986). Sparid nomenclature follows Eschmeyer (2005) distinguished two subgroups: the “ignoratus” s. str. (1998). Fish were dissected shortly after death. Gills were subgroup, with lateral dorsal bars in one part and enlarged at removed and placed in separate Petri dishes containing fil- the axial end, and the “ergensi” subgroup, with lateral dorsal tered seawater and examined for parasites under incident light bars in two parts, more or less united (Fig. 1). using a stereomicroscope. Monogeneans were detached from Many attempts have been made to resolve phylogenetic the gills with a strong water current and transferred to a dish relationships among Lamellodiscus species (Desdevises et al. containing filtered seawater. Living parasites were partially 2002, Domingues and Boeger 2008). Several species of La- compressed beneath a coverslip and examined using a light mellodiscus must be redescribed tacking into account mor- microscope. Several specimens were mounted directly in phological characters previously underestimated. Malmberg’s ammonium picrate-glycerol (Malmberg 1957).

Corresponding address: [email protected]

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Œl¹ski

The slides were sealed with Canada balsam. In order to describe the morphology of the haptoral sclerites and copula- tory organ, some specimens were also mounted in Berlese’s fluid. Drawings were made under a light microscope with the aid of a drawing tube, then scanned and redrawn with Corel Draw Software. Measurements were made either on fixed or living specimens. Measurements, made on drawings, are given (in micrometres) as range, followed by mean, and number of observations in parentheses (n). The measurements of sclero- tized structures are indicated in Figure 2.

Results

Class: Monogenea (Carus, 1863) Bychowsky, 1937 Subclass: Odhner, 1912 Order: Bychowsky, 1937 Family: Diplectanidae Bychowsky, 1957 Subfamily: Lamellodiscinae Oliver, 1969

Lamellodiscus crampus sp. nov. (Figs 3–5)

Description (based on 28 flattened specimens): Adults 310– 570 (427, n = 12) long including haptor; maximum width 50– Fig. 1. Haptor of Lamellodiscus from the “ignoratus” group: 130 (84, n = 12) at the level of ovary. Haptor posterior, differ- A – subgroup “ignoratus” s. str., B – subgroup “ergensi”. Scale bar entiated from body proper, 105–140 (126, n = 12) width. Dor- = 100 µm sal and ventral lamellodiscs of the “ignoratus” group, 35–55

Fig. 2. Lamellodiscus Johnston et Tiegs, 1922. Methods of measurements of various sclerotized organs: A – dorsal bar; B – ventral bar (Mp: constricted median part); C – dorsal anchor (a – total length, b – length shaft-point, c – length guard-point); D – ventral anchor (a – total length, b – length shaft-point, c – length guard-point, d – length shaft-guard, f – shaft length, g – guard length); E – male copula- tory organ (U – unpaired piece length, Pa – axial branch of paired piece length, Pl – lateral branch of paired piece)

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Stanis³a (48, n = 28) in diameter, with 10 concentric rows of lamellae; anterior forming circular complete ring 15–18 (16, n = 11) in diameter. Dorsal anchor with incipient guard; a: 26–38 (31, n = 26), b: 26–31 (29, n = 25), c: 15–19 (16, n = 25). Two lateral dor- sal bars with spatulate medial end and curved lateral end, 47–65 (54, n = 28) long. Ventral anchor with developed han- dle, wide guard, bent shaft and short point; a: 30–39 (36, n = 28), b: 29–38 (35, n = 28), c: 17–25 (22, n = 22), d: 11–17 (14, n = 28), f: 11–15 (14, n = 28), g: 3–5 (4, n = 28). Ventral medi- an bar 49–65 (57, n = 27) long with constricted median part Mp: 8–16 (11, n = 22) long and tapered ends. Fourteen simi- lar uncinuli (seven pairs), with diplectanid disposition (Fig. 3). Cephalic glands on each lateral side of the pharynx, both with ducts leading to three lateral head organs. Larval ocellar granules dispersed in prepharyngial part. Mouth anterior, sub- terminal, opening ventrally. Pharynx spherical, 27–35 (30, n = 11) in diameter. Oesoph- agus very short. Lateral oesophageal glands present. Simple lateral intestinal caeca not united posteriorly. Subspherical testis, intercaecal in posterior half of the body. Vas deferens emerging from antero-sinistral side of testis, not encircling left intestinal caecum, enlarging to form one large seminal vesicle. Vas deferens passing on right side, anterior to male copulato- ry organ. Prostatic reservoir pyriform, anterior to male copu- latory organ. Male copulatory organ, formed by two sclero- tized, articulated pieces (Fig. 5). Unpaired piece U: 37–55 (43, n = 28) long, with curved tip and base covered by a thin scler- otized skirt-like envelope. Paired piece with lateral branch Pl: 13–19 (16, n = 21) shorter than axial branch Pa: 22–29 (25, n = 21). Distal part of axial branch armed with 5–6 minute spines (Fig. 5, arrow). Ovary median, subequatorial, anterior to testis, looping dorso-ventrally around right intestinal caecum. Mehlis’s glands and ootype not observed. Vaginal aperture sinistral

Fig. 4. Lamellodiscus crampus sp. nov. Haptoral sclerotized pieces: Fig. 3. Lamellodiscus crampus sp. nov.: Composite drawing of five A – dorsal bar, B – ventral bar, C – dorsal anchor, D – ventral anchor, live specimens, dorsal view. Scale bar = 100 µm E – ventral lamellodisc. Scale bar = 25 µm

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Oliver, 1967; L. knoepffleri Oliver, 1969; L. acanthopagri Rou- bal, 1981; L. falcus Amine, Euzet et Kechemir-Issad, 2006; L. neifari Amine, Euzet et Kechemir-Issad, 2006 and L. con- fusus Amine, Euzet et Kechemir-Issad, 2007. Lamellodiscus crampus sp. nov., can be easily distinguished from all these species by the morphology of the male copulatory organ, which is armed with 5–6 minute spines on the distal part of the axial branch.

Discussion

Four Sparidae species from the genus Dentex Cuvier, 1814 are reported from the Mediterranean Sea. Dentex macrophthal- mus (Bloch, 1791) and D. maroccanus are only present on the southern coasts of the Mediterranean Sea and have an average total length of 20 cm. Dentex dentex Linnaeus, 1752 and D. gibbosus (Rafinesque, 1810) are present throughout the Mediterranean Sea and have an average total length of 40 cm (Bauchot and Hureau 1986). On these last two species only one Capsalidae species (Encotyllabe vallei Monticelli, 1907) and two Polyopisthocotylea (Microcotyle sp. and Gotocoty- la acanthura (Parona et Perugia ,1891)) have been reported Fig. 5. Lamellodiscus crampus sp. nov. Male copulatory organ: U – (Euzet et al. 1993). Aleshkina (1984) described Lamellodiscus unpaired piece length, Pa – axial branch of paired piece, Pl – lateral dentexi from the gills of D. macrophthalmus from the south- branch of paired piece, S – spines. Scale bar = 25 µm west coast of Africa. This species, belonging to the “elegans” group, has not been reported from the Mediterranean Sea. It can be distinguished from L. crampus sp. nov. by the mor- with funnel-shaped opening, enlarged on vaginal chamber phology of the and the structure of the male cop- often filled with slightly sclerotized mass. Vaginal chamber ulatory organ. connected with narrow duct to globular seminal receptacle, Therefore, there seems to be a difference in the parasitism anterior to ovary. Vitelline follicles lateral, coextensive with by monogeneans between Dentex species found in the south- intestinal caeca, contiguous anterior to prostatic reservoir and ern part, and those reported across the Mediterranean. What posterior to testis. Eggs not seen. are the reasons for this difference? Is it linked to biogeography Type host: Dentex maroccanus (Valenciennes, 1830) (Spa- or host size or phylogeny? This should be investigated in fur- ridae). ther studies. Infection site: Between secondary gill lamellae. The description of this new species suggests that diple- Type locality: Gulf of GabPs (33°45´N, 11°38´E), Medi- ctanid parasites from Dentex spp., as for most Sparidae, have terranean Sea. an oioxenic specificity. Holotype: Muséum National d’Histoire Naturelle, Paris, No. HEL 57 Th 147. Paratypes: Muséum National d’Histoire Naturelle, Paris, References No. HEL 58 Th 147bis; British Museum (Natural History), London, No. 2008.7.25.1. Aleshkina L.D.1984. New species of the family Diplectanidae (Mo- nogenea) in the South-East Atlantic. Zoologicheskiy Zhurnal, Infection indices: Prevalence of L. crampus was 65%, the 63, 1253–1256 (In Russian, with summary in English). intensity 2–3. Amine F., Euzet L. 2005. Deux nouvelles espPces du genre Lamel- Etymology: Neologism from French “crampon” (cramp) lodiscus Johnston & Tiegs, 1922 (Monogenea: Diplectanidae) refers to the morphology of axial branch of paired piece of parasites de Sparidae (Teleostei) des côtes de l’Algérie. Sys- male copulatory organ. tematic Parasitology, 60, 187–196. DOI: 10.1007/s11230- 004-6346-6. Remarks: From the morphology of the squamodisc and Amine F., Euzet L., Kechemir-Issad N. 2006a. Description de deux male copulatory organ, this species belongs to the “ignoratus” nouvelles espPces de Lamellodiscus Johnston & Tiegs, 1922 group (Oliver 1987). The presence of simple dorsal lateral (Monogenea, Diplectanidae) du groupe morphologique ‘igno- bars enlarged at the axial end places this species in the “igno- ratus’, parasites de Diplodus sargus et D. vulgaris (Teleostei: ratus” s. str. subgroup (Euzet and Amine 2005). This subgroup Sparidae). Systematic Parasitology, 64, 37–45. DOI: 10.10 07/s11230-005-9016-4. includes L. pagrosomi Murray, 1931; L. ignoratus Palombi, Amine F., Euzet L., Kechemir-Issad N. 2007a. Lamellodiscus thero- 1949; L. fraternus Bychowsky, 1957; L. erythrini Euzet et ni sp. nov. (Monogenea, Diplectanidae), a gill parasite from

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Diplodus puntazzo (Teleostei, Sparidae) from the Mediter- Eschmeyer W.N. 1998. Catalogue of . California Academy of ranean Sea. Acta Parasitologica, 52, 305–309. DOI: 10.2478/ Sciences, 2905 pp. s11686-007-0052-x. Euzet L., Combes C., Caro A. 1993. A checklist of Monogenea of Amine F., Euzet L., Kechemir-Issad N. 2007b. Description de La- Mediterranean fish. Proceedings of the Second International mellodiscus confusus n. sp. (Monogenea: Diplectanidae) par- Symposium on Monogenea, Montpellier, France, 1–11. asite de Sarpa salpa (Teleostei: Sparidae). Parasite, 14, 281– Fischer W., Bauchot M.L., Schneider M. 1987. Fiches FAO d’iden- 285. tification des espPces pour les besoins de la pLche. Méditer- Amine F., Neifar L., Euzet L. 2006b. Lamellodiscus sanfilippoi n. sp. ranée et Mer noire. Zone de pLche 37. Vertébrés. Vol. 2. FAO (Monogenea, Diplectanidae) parasite branchial de Diplodus Publishing, Rome, 761–1530. sargus (Teleostei, Sparidae) en Méditerranée. Parasite, 13, Malmberg G.V. 1957. Skrifter Utgivna av Sodra Sveriges Fiskeri- 45–49. forening, 19–76. Bauchot M.L., Hureau J.C. 1986. Sparidae. In: (Eds. P.J.P. White- Neifar L., Euzet L., Oliver G. 2004. Lamellodiscus (Plathelminthes, head, M.L. Bauchot, J.C. Hureau, J. Nielson and E. Tortone- Monogenea, Diplectanidae) nouveaux parasites branchiaux se) Fishes of the North-eastern Atlantic and the Mediterra- des poissons marins du genre Pagrus (Teleostei, Sparidae). nean. Vol. 2. Unesco Publishing, Paris, 883–907. Zoosystema, 26, 365–376. Desdevises Y., Morand S., Legendre P. 2002. Evolution and deter- Oliver G. 1987. Les Diplectanidae Bychowsky, 1957 (Monogenea, minants of specificity in the genus Lamellodiscus (Monoge- Monopisthocotylea, Dactylogyridea). Systématique, Biolo- nea). Biological Journal of the Linnean Society, 77, 431–443. gie, Ontogénie, Ecologie, Essai de phylogenPse. ThPse d’état, Domingues M.V., Boeger W.A. 2008. Phylogeny and revision of the Université des Sciences Techniques du Languedoc, Mont- Diplectanidae Monticelli, 1903 (Platyhelminthes: Monoge- pellier, France. noidea). Zootaxa, 1698, 1–40.

(Accepted July 14, 2008)

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