Comp. Parasitol. 76(1), 2009, pp.

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Monogenoids from the Gills of Acanthopagrus bifasciatus (Forsskal, 1775) (Perciformes: Sparidae) of the Red Sea, Egypt, with the Description of Lamellodiscus donatellae sp. n. (Diplectanidae)
GIOVANNI AQUARO,1 CHIARA RIVA,
AND

PAOLO GALLI

Department of Biotechnology and Biosciences, University of Milano-Bicocca, Piazza della Scienza 2, 20126 Milan, Italy A new species of monogenoid, Lamellodiscus donatellae n. sp., from twobar seabream, Acanthopagrus bifasciatus, of the Gulf of Sinai, Egypt, is described and compared with other congeneric species. Lamellodiscus donatellae n. sp. is included in the L. ergensi group, but it presents differences with each species of this group, including size and morphology of the sclerotized structures. Two known species were found and redescribed: Polylabris acanthopagri Mamaev and Parukhin, 1976, and Placodiscus acanthopagri Paperna, 1972. KEY WORDS: Monogenoidea, Diplectanidae, Lamellodiscus donatellae n. sp., Polylabris acanthopagri, Placodiscus acanthopagri, Acanthopagrus bifasciatus, twobar seabream, Egypt, Red Sea.
ABSTRACT:

Twobar seabream, Acanthopagrus bifasciatus (Forsskal, 1775) (Perciformes: Sparidae), is a reef associated marine sh living in tropical waters of the western Indian Ocean (Red Sea and Persian Gulf south to Natal, South Africa). This species is caught mainly with longlines, handlines, stakenets, and traps and marketed fresh or dried (Bauchot and Smith, 1984). Two species of monogenoids are known to infest twobar seabream: Placodiscus acanthopagri Paperna, 1972, from the Gulf of Suez (Paperna, 1972) and Polylabris acanthopagri Mamaev and Parukhin, 1976, from the Arabian Sea (Mamaev and Parukhin, 1976). The only information regarding Polylabris acanthopagri is the Russian description and an incomplete short list of the main features by Hayward (1996), who provided a revision of the genus. Moreover, Kritsky et al. (2000) reported Lamellodiscus sp. 2 from this host in the Persian Gulf. During the present study on reef shes from the South Sinai, Red Sea, Egypt, during October 2006, 8 specimens of A. bifasciatus were examined for monogenoids. In addition to the 2 previously known species, we found an undescribed species of Lamellodiscus Johnson and Tiegs, 1922. The aim of this work is to describe the new species and to redescribe Polylabris acanthopagri and Placodiscus acanthopagri. MATERIAL AND METHODS
Eight Acanthopagrus bifasciatus were collected by Bedouin shermen with nets from the Nabq Managed Resource Protected Area, which is part of the network of 5

parks and protected areas of the South Sinai Protectorates. Seven of these shes were deposited in the ichthyological collection of the Natural History Museum in Milan (MSNM Pi 3904-3860-3861), Italy. In the eld, gill arches were removed and placed in vials containing heated (658C) 5% formalin solution. Helminth specimens were described using different methods: some were mounted unstained with ammonium picrate glycerin (Malmberg, 1957) to study sclerotized parts. Other specimens were stained with Gomoris trichrome (Kritsky et al., 1978; Humason, 1979) and mounted in Euparal in order to observe internal anatomy. Drawings were made with the aid of a camera lucida and an Olympus BX50 microscope. Measurements, presented in micrometers, represent straight-line distances between extreme points and are expressed as the mean (6 standard deviation) followed by the range and number (n) of structures measured in parentheses; body length includes the haptor, and measurements taken for various structures are indicated by lines in Figures 25. Type and voucher specimens of Lamellodiscus donatellae n. sp., Polylabris acanthopagri, and Placodiscus acanthopagri collected during this study are deposited in the Natural History Museum of Milan, Italy (MSNM).

Lamellodiscus donatellae n. sp. (Figs. 18) Diagnosis Body fusiform. Haptor with 3 bars and 4 anchors. Two sclerotized lamellodiscs. Fourteen hooks. One testis; male copulatory organ a sigmoid tube with acute recurved tip and accessory piece. Ovary elongate and diagonal. Sinistral vaginal aperture sometimes with spermatophores. Trunk with vitellaria. Parasites of marine sparid shes. Description Body elongate 743 6 46 (680800, n 8), haptor 169 6 27 (135230, n 9) wide. Anterior region
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Corresponding author: e-mail: aquarogio@hotmail.com.

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Figures 18. Lamellodicus donatellae n. sp. 1. Habitus, dorsal view. 2. Ventral bar. 3. Ventral anchor. 4. Left dorsal bar. 5. Dorsal anchor. 6. Lamellodiscs. 7. Male copulatory complex. 8. Hook. Lines on Figures 25 indicate measurements taken on each of these structures.

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with 3 pairs of head organ and 4 eyespots; posterior pair of eyespots larger than anterior pair. Cephalic glands posterolateral to pharynx. Mouth subterminal, 2 intestinal caeca nonconuent. Haptor with 14 similar hooks, 3 bars, 2 pairs of anchors (dorsal and ventral), and ventral and dorsal lamellodiscs composed of incomplete and indented lamellae. Dorsal bars 66 6 5 (6076, n 9) long, 27 6 5 (1834, n 9) wide, divided in 2 parts with bid internal ends. Ventral bar 82 6 6 (7392, n 8) long, 21 6 5 (1126, n 8) wide, V-shaped, with midventral longitudinal groove. Ventral anchor 51 6 5 (4659, n 6) long, with elongate supercial and deep roots. Dorsal anchor 54 6 6 (4565, n 8) long, with less developed supercial root. Lamellodiscs 50 6 4 (4558, n 8) wide; rst lamella circular, remaining lamellae semicircular. Male copulatory complex comprised of a copulatory organ and accessory piece; copulatory organ 61 6 6 (5470, n 9) long, a sigmoid tube with acute recurved tip; accessory piece with submedial elongate branch. Ovary elongate, diagonal, looping right caecum. Testis spherical, with vas deferens connected to seminal vesicle; seminal vesicle ends in the male copulatory organ. Trunk with vitellaria except in the regions of other reproductive organs. Sinistral vaginal aperture; vagina short, usually with 1 or 2 subspherical spermatophores, connected with seminal receptacle. Taxonomic summary Monogenoidea Bychowsky, 1937; Polyonchoinea Bychowsky, 1937; Dactylogyrinea Bychowsky, 1937; Diplectanidae Monticelli, 1903; Lamellodiscus Johnson and Tiegs, 1922. Type host: Acanthopagrus bifasciatus (Forsskal, 1775). Type locality: Egypt, Sharm el Sheik in Nabq area (288029520N, 348269210E), October 2005, May 2006, May, 2007. Infection site: Gills. Deposited specimens: Holotype, MSNM Pi4851; 11 paratypes, MSNM Pi485262. Etymology: This species is named after Donatella Moretti, who patiently helped the rst author complete this work. Remarks Lamellodiscus donatellae n. sp. can be included in the ergensi group of Amine and Euzet (2005) (male

copulatory organ lyre type, lamellodiscs of ignoratus type (Oliver, 1987) and division of lateral bars). The ergensi group is composed of some parasites of Diplodus sargus living in the same geographical region: Lamellodiscus sanlippoi Amine, Nefair, and Euzet, 2006, Lamellodiscus ergersi Euzet and Oliver, 1966, Lamellodiscus kechemirae Amine and Euzet, 2005, Lamellodiscus tomentosus Amine and Euzet, 2005, and Lamellodiscus furcillatus Kritsky, 2000. The group also includes Lamellodiscus baeri Oliver, 1974, of Pagrus pagrus. Lamellodiscus donatellae n. sp. differs from L. sanlippoi by having a longer male copulatory organ (mean 61 lm compared to 50 lm of L. sanlippoi) and a shorter body (743 lm compared to 900 lm of L. sanlippoi). The ventral bar of L. sanlippoi does not show a longitudinal groove. It is not possible to carry out a comparison between internal soft structures (prostatic gland, seminal vesicle, etc.), because these are not described for L. sanlippoi. Moreover, the paratypes of L. sanlippoi were stained with picrate limiting information about the morphology of these structures. Lamellodiscus donatellae n. sp. differs from L. ergensi in body measurements with L. ergensi being shorter (470 lm compared to 743 lm), while the dorsal bars (84 lm compared to 66 lm) and ventral bar (93 lm compared to 82 lm) are longer in L. ergensi. Moreover, bar morphology, especially that of the dorsal bars, is more elongate and thin in L. ergensi. Size of the lamellodisc is larger in L. donatellae n. sp. (32 lm in L. ergensi compared to 50 lm in the new species). The prostatic gland in our specimens appears as a rigid bean-shaped structure with a minimal variation in morphology, while in L. ergensi the prostatic gland is subspherical to elongate. The male copulatory organs differ in length in the 2 species: 45 lm in L. ergensi; 61 lm in L. donatellae n. sp. There is no correspondence in the general anatomy between Lamellodiscus donatellae n. sp. and L. furcillatus, except that the male copulatory organs are comparable in morphology. The voucher specimens of Lamellodiscus sp. 2 of Kritsky et al. (2000), reported from A. bifasciatus in the Persian Gulf, present an undivided dorsal bar that excludes them from the ergensi group. Identication key for species of Lamellodiscus in the ergensi group (lateral bars divided into two parts): 1) Dorsal bars not completely divided: Lamellodiscus baeri Oliver, 1974 Dorsal bars completely divided: 2 2) Supercial and deep roots of ventral anchors of different lengths: 3

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3) 4)

5)

6)

Supercial and deep roots of ventral anchors similar in length: 4 Ventral bar long and thin: 5 Ventral bar short and wide: 6 Longitudinal groove in ventral bar: Lamellodiscus donatellae n. sp. Longitudinal bar without longitudinal cut: Lamellodiscus sanlippoi (Euzet, 2006) Dorsal bars with 3 bumps at external end: Lamellodiscus ergensi (Euzet, 1966) Dorsal bars with 1 bump at external end: Lamellodiscus tomentosus (Euzet, 1966) Dorsal bars with 3 bumps, of which 2 opposite, at external end: Lamellodiscus kechemirae (Euzet, 1966) Dorsal bars without the 2 opposite bumps at external end: L. furcillatus (Kritsky, 2000) Placodiscus acanthopagri Paperna, 1972 (Figs. 915)

Taxonomic summary Monogenoidea Bychowsky, 1937; Polyonchoinea Bychowsky, 1937; Dactylogyridea Bychowsky, 1937; Dactylogyrinea Bychowsky, 1937; Dactylogyridae Bychowsky, 1933, Placodiscus Paperna, 1972. Type host: Acanthopagrus bifasciatus (Forsskal, 1775). Type locality: Egypt, Sharm el Sheik in Nabq area (288029520N, 348269210E), October 2005, May 2006, May, 2007. Infection site: Gills. Deposited specimens: MSNM Pi487276 Remarks In addition to the structures described by Paperna (1972), we observed the vas deferens joining seminal vesicle and small vesicles associated with each anchor (Fig. 9), which probably contain a secretion involved in the anchoring process. Polylabris acanthopagri Mamaev and Parukhin, 1976 (Figs. 1619) Diagnosis Body lanceolate. Haptor elongate, composed of 2 parallel subequal rows of sclerotized microcotylid clamps. Small spherical pharynx. Two oval buccal organs. 3540 testis; S-shaped seminal vesicle ending in sclerotized male copulatory organ with a welldeveloped prostatic complex. Elongate doubleinverted U-shaped ovary with seminal receptacle. Medio-ventral vagina with 2 ducts. Vitellaria well developed. Egg with 2 laments. Parasites of marine sparid shes. Redescription Body lanceolate, haptor fused with body. Haptor long, arising from ventral surface of the body, armed with 2 parallel subequal rows of sclerotized microcotylid clamps (about 140 total clamps) of different sizes; clamps becoming smaller distally; clamps bilaterally symmetrical, anterior clamps 54 6 8 (4368, n 15) wide, posterior clamps 31 6 3 (2735, n 17) wide. Small mouth with 2 separate buccal organs 60 6 9 (4778, n 14). Small spherical pharynx, 30 6 4 (2335, n 8) in diameter; elongate straight esophagus ending in 2 intestinal branches that extend the entire length of body. About

Diagnosis Body elongate, widest in the testicular region. Haptor armed with 4 similar anchor, 2 bars, and 4 plaques. Fourteen hooks. Intestinal branches conuent posteriorly. One testis, male copulatory organ without an accessory piece. Vaginal aperture on the right. Parasites of marine shes. Redescription Body 528 6 53 (445637, n 9) long, widest in the testicular region. Haptor 71 6 53 (5887, n 6) wide, armed with 4 similar anchors, 2 transverse bars, and 4 plaques. Dorsal and ventral anchors of equal size: 22 6 4 (1527, n 14) long; bars 42 6 2 (3946, n 10) long, 5 6 1 (37, n 10) wide; plaques 17 6 4 (1428, n 9) long, 20 6 4 (1423, n 9) wide. Small vesicles associated with each anchor. Plaques located symmetrically around the center of the haptor. Twelve marginal hooks 12 6 2 (915, n 5) and 2 central hooks (shorter than 6 lm). Intestinal branches conuent posteriorly. Ovary anterior to the testis. Spherical to subovate testis joins vas deferens; vas deferens looping sinistral intestinal branch, ending in seminal vesicle. Male copulatory organ a clockwise coil of about 1 rings, thin, lacking an accessory piece. Well-developed prostatic gland anterior to male copulatory organ. Vaginal aperture on the right side of the body, posterior to male copulatory organ and prostatic gland. Seminal receptacle not observed. One pharynx, 6 head organ, and 4 eyespots are present in the cephalic region.

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Figures 915. Placodiscus acanthopagri. 9. Habitus, ventral view, arrow indicates vaginal aperture. 10. Dorsal anchor. 11. Ventral anchor. 12. Hook. 13. Dorsal bar. 14. Ventral bar. 15. Male copulatory organ.

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In the anterior portion of the body, anterior to the testes, an elongate double-inverted U-shaped ovary is present; seminal receptacle saccate. The short oviduct swells in the middle region; small Mehlis glands at the end of the oviductus. Medioventral vaginal pore of a small rounded vaginal vestibule with small openings on the dorsal side. Two thin vaginal ducts arising from the vaginal vestibule. Each with an enlargement next to the vaginal vestibule. The vaginal ducts extend laterally and posteriorly, uniting to form a ring. Vitellaria well developed and distributed along the entire body. One elongate egg observed, about 260 in total length, with 2 long terminal laments (egg about 150 long not including laments). Taxonomic summary Monogenoidea Bychowsky 1937, Oligonchoinea Bychowsky 1937, Mazocraeidea Bychowsky 1937, Microcotylidae Taschenberg, 1879, Prostatomicrocotylinae Yamaguti, 1968, Polylabris Euzet and Cauwet, 1967. The generic diagnosis was emended by Hayward C. J., 1996. Type host: Acanthopagrus bifasciatus (Forsskal, 1775). Type locality: Egypt, Sharm el Sheik in Nabq area (288029520N, 348269210E), October 2005, May 2006, May 2007. Infection site: Gills. Deposited specimens: MSNM Pi486771 Remarks
Figures 1619. Polylabris acanthopagri. 16. Habitus, ventral view. 17. Egg. 18. Male copulatory organ. 19. Clamp.

3540 testis located in posterior half of body. Vas deferens noticeably dilated forward of anterior testis, S-shaped seminal vesicle immediately posterior to male copulatory organ, a dilatation of vas deferens, with a developed muscular covering. Sclerotized conical male copulatory organ, located at level of the posterior end of the esophagus, with a large and discoidal base having 4 or 6 small teeth on the dorsal border (Fig. 18). Central ductus of male copulatory organ enlarged at the end, supplied with a sharp straight dagger recurved dorsally. Well-developed prostatic complex formed from a prostatic receptacle and 2 lateral large prostatic ducts uniting to form a central single prostatic duct.

Specimens described may be considered as a forma minor of Polylabris acanthopagri. All measurements of the specimens presently studied were approximately half of those presented in the original description of the species, although proportions were comparable. Moreover, internal anatomy is completely similar. The morphology of the egg is described for the rst time. ACKNOWLEDGMENTS We thank Prof. Delane C. Kritsky for his expert suggestions and for his great patience in reading the manuscript. We thank Dr. Marcus Vinicius Domingues for his availability to read the manuscript and his helpful corrections. We are also grateful to the Nabq Bedouin shermen Salhe and Fharagh for their help in collecting sh.

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LITERATURE CITED
Amine, F., and L. Euzet. 2005. Deux especes nouvelles du ` genre Lamellodiscus Johnston and Tiegs, 1922 (Monogenea: Diplectanidae) parasites de Sparidae (Teleostei) des cotes de lAlgerie. Systematic Parasitology 60:187196. Bauchot, M. L., and M. M. Smith. 1984. Sparidae. Var. pages in W. Fischer and G. Bianchi, eds. FAO Species Identication Sheets for Fishery Purposes. Western Indian Ocean (Fishing Area 51), vol. 4. FAO, Rome. Hayward, C. J. 1996. Revision of the Monogenean genus Polylabris (Microcotylidae). Invertebrate Taxonomy 10:9951039. Humason, G. L. 1979: Animal Tissue Techniques. W. H. Freeman Co., San Francisco, California. 661 pp. Kritsky, D. C., F. A. Jimenez-Ruiz, and O. Sey. 2000. Diplectanids (Monogenoidea: Dactylogyridea) from the gills of the Persian Gulf off Kuwait. Comparative Parasitology 67:145164. Kritsky, D. C., P. D. Leiby, and R. J. Kayton. 1978. A rapid stain technique for the haptoral bars of Gyro-

dactylus species (Monogenea). Journal of Parasitology 64:172174. Malmberg, G. 1957. Om forekomsten av Gyrodactylus pa svenska skar. Sartryck ur Skrifter utgivna av Sodra Sveriges Fiskeriforening, Arsskrift, 1976. Mamaev, Y. L., and A M. Parukhin. 1976. On the genus Polylabris Euzet et Cauwet, 1967 and some closely allied species of microcotylids (Monogenoidea: Microcotylidae). Parazitologiya (Leningrad) 10:245254. (In Russian.) Oliver, G. 1987. Les Diplectanidae Bychowsky, 1957 (Monogenea, Monopisthocotylea, Dactylogyridae). Systematique, biologie, ontogenie, ecologie. Essai de phylogenese. Universite des Sciences et Techniques du ` Languedoc, Montpellier. These de doctorat detat. ` 433 pp. Paperna, I. 1972. Monogenea of Red Sea Fishes. III. Dactylogyradae from littoral and reef shes. Journal of Helminthology 46:4762.