JKAU: Mar. Sci., Vol. 22, No. 1, pp: 3-13 (2011 A.D. / 1432 A.H.) DOI : 10.4197/Mar. 22-1.1

Hypocreadium cavum (Digenea: Lepocreadiidae: Hypocreadium) in Marine Fishes, stellaris (Balistidae) From the Red Sea, Coast of Yemen.

Ali B. Al-Zubaidy Department of Marine Biology and Fisheries, Faculty of Marine Science and Environment, Hodeidah University, Yemen

Abstract. Specimens of the marine fish, Abalistes stellaris (Balistidae) were collected from local fish market in Hodeidah during the period between September 2008 and July 2010 . Six out of 80 (7.5%) of these fish were found to harbour intestinal trematodes, Hypocreadium cavum Bray and Cribb, 1996 (Lepocreadiidae). Since there is no previous report on these digenetic trematode from any fish host in Yemen, the present recording may well be considered the first in this country.

Introduction Members of the Lepocreadiidae Odhner, 1905 have a cosmopolitan distribution as intestinal parasites of marine teleosts (Bartoli and Bray, 2004). They are recognizable as worms with widely distributed Vitelline folices, a spinous tegument, a cirrus-sac, usually with a distinct external seminal vesicle and a typically I-shaped excretory vesicle (Bray, 2005). Ozaki (1936) erected the genus Hypocreadium to include H.symmetrorchis in Monocanthus cirrhifer from Japan. Manter (1940), Arai (1962) and Nahhas and Cable (1964) concluded that Hypocreadium Ozaki,1936 should be considered as a synonym to Pseudocreadium Layman,1930. However, Yamaguti (1971) refused these conclusions and preferred to retain the genus Hypocreadium Ozaki, 1936 as a separate

3 4 Ali B. Al-Zubaidy genus which could be easily separated from other related genera according to the position of genital pore, ovary and prostate cells as well as the extension of the excretory vesicle. Bray and Cribb (1996) revised the genus, recognizing 13 species: Hypocreadium symmetrorchis (type- species); H. balistes; H. biminensis; H. cavum; H. galapagoensis; H. grandisquamis; H. indicum; H. lactophrysi ; H. lamelliforme; H. myohelicatum; H. patellare; H. scaphosomum and H. spinosum. Bray et al. (2009) recognized 15 species, including H. toombo Bray and Justine, 2006 and H. picasso Bray et al.2009. Balistid fish, Abalistes stellaris (Bloch and Schneider,1801) is a fish belonging to family Balistidae, with distribution in Indo-west Pacific, Red Sea and east Africa to southeast Asia, north to Japan and south to northern Australia, eastern Atlantic. It inhabits coastal areas, usually found over muddy and sandy bottoms, also around reefs together with the sponges and algae. It is feeding on benthic (Figueiredo and Menezes, 2000). The parasite fauna of this fish species from the Red Sea, Yemen coast, is poorly known. During investigations into helminths parasites of fish, A. stellaris, specimens of Hypocreadium Ozaki, 1936 were collected and identified as H. cavum Bray and Cribb, 1996 which represents the first record of this genus in Yemen Coastal water on the Red Sea.

Materials and Methods During September 2008 to July 2010, 80 specimens of the fish Abalistes stellaris (Balistidae) were collected from the local fish market in Hodeidah, Yemen. Standard parasitological techniques were used to examine the alimentary canal of the fish. Digenean collected from freshly killed fish were fixed by being pipetted into nearly boiling saline and immediately preserved in 5% formalin or 70% ethanol. Whole-mounts were stained in acetocarmine, cleared in Lacto phenol and mounted in Canada balsam. Measurements are quoted as the range with the mean in parentheses. The specimens are deposited in the laboratory of Marine Biology and Fisheries Department, Faculty of Marine Science and Environment, Hodeidah University, Hodeidah, Yemen. Trematode was identified to species level based on the keys of Bray and Cribb (1996); Bray et al.(2009) and with the help of Prof. Dr. R.A. Bray.

Hypocreadium cavum (Digenia: Lepocreadiidae: Hypocreadium)… 5

Results and Discussion Classification Class: Trematoda Rudolphi, 1808 Subclass: Digenea Carus, 1863 Family : Lepocreadiidae Odhner, 1905 Subfamily: Lepocreadiinae, Odhner, 1905 Synonym: Dermadenidae, Yamaguti, 1958 Genus: Hypocreadium Ozaki, 1936 Diagnosis: Body broadly oval, rounded or slightly wider than long; flattened. Tegumental spines sparse or apparently absent. Oral sucker sub terminal, sub globular. Ventral sucker rounded to oval and in the middle of body. Prepharynx present or apparently absent. Pharynx oval. Oesophagus usually distinct. Intestinal bifurcation in mid-forebody. Caeca undulating in arc around gonads, terminate blindly near median line posterior to ovary. Testes symmetrical in anterior hind body. External seminal vesicle saccular to elongate. Cirrus-sac large, claviform. Internal seminal vesicle sub globular. Pars prostatica vesicular; bipartite or elongate curved. Ejaculatory duct long and wide. Genital atrium distinct. Genital pore sinistral at various levels in forebody. Ovary inter- testicular; oval, weakly lobed or entire. Canalicular seminal receptacle and Lauer’s canal present. Uterus pre-ovarian, may also pass posteriorly to ovary. Eggs tanned, operculate. Vitelline follicular; fields around gonads with distinct wide border lacking follicles. Excretory pore dorsal just posterior to ovary or testes; vesicle wide, reaches to gonads, two arms reach into forebody. In marine teleost, mainly Tetraodontiforms. Type species H. symmetrorchis Ozaki,1936. H. symmetrorchis is unfortunately, atypical for the genus, in that it is broadly oval, rather than rounded as is the case for most species. Also, unfortunately, the excretory system was not described, but the similar species H. biminensis is described with the excretory pore dorsal at about the posterior margin of the testes (Bray and Cribb, 1996). Hypocreadium cavum Bray and Cribb, 1996 ( Fig. 1). Description (base on 3specimens) and Measurements (µm): Body: rounded,1.350-2.550 mm (2.08) in length,1.320-2.640 mm (2.100) wide at its middle. Pre oral lobe: 16- 40 ( 31). Spines: No tegumental spines seen. 6 Ali B. Al-Zubaidy

Oral sucker: sub terminal, round, 105-149×118-160(119-143). Ventral sucker: rounded, 145- 237×152-225 (131×159). Sucker ratio: 1:1.07-1.28 (1.15). Pharynx: Oval, 75-114×75-131(101×124). Oesophagus: distinct,79-160 (121) . Forebody: 620-1.080(851) in length, representing 37-39% of total body length. Intestinal bifurcation in mid-forebody. Testes: 2, entire, oval, symmetrical,135-320×156-288(254×210). External seminal vesicle: saccular, at level of ventral sucker, 120- 280×65-112(178×83). Internal seminal vesicle: oval. Cirrus-sac: large, claviform,337-510×156-230 (401×206). Ejaculatory duct: muscular, long, folded. Genital atrium distinct. Genital pore sinistral at level of anterior part of oesophagus. Ovary: more or less oval, 108-182×119-177(143×156).Oviduct passes anteriorly from ovary. Eggs: few, operculate. Lauer’s canal opens dorsally to ovary, sinistral testis or between. Uterus anteriorly to ovary. Excretory pore: dorsal, median.

Fig. 1. Hypocreadium cavum from Abalistes stellaris, ventral view. Scale bar = 0.5mm. os = oral sucker. Ph = pharynx. gp = genital pore. cs = cirrus sac. vs = ventral sucker. t = testes. ov = ovary. oe = oesophagus.

Hypocreadium cavum (Digenia: Lepocreadiidae: Hypocreadium)… 7

Taxonomic Summary: Synonyms: Pseudocreadium scaphosomum Menter,1940 of Parukhin and Chikunova (1964); Pseudocreadium patellarae (sic) (Yamaguti, 1938) of Oshmarin (1965); Hypocreadium indicum (Madhavis, 1972) of Hussain et al., (1986). Host: Abalistes stellaris, Balistidae, Starry . Locality: Red Sea, Hodeidah- Yemen coastal water. Site of infection: Intestine. Prevalence: 6/80 fishes examined; 7.5%. Intensity of infection: 1 parasite per each fish infected.

Discussion Prior to 2004, more than 30 subfamilies were described under the Lepocreadiidae Odhner, 1905. More recently, Bray (2005) has comprehensively reviewed this family, accepting the validity of only three subfamilies, the Lepocreadiinae Odhner, 1905; Lepidapedinae Yamaguti, 1958 and Aephnidiogeninae Yamaguti, 1934, based on essential differences in the structure of the male terminal genitalia. He accepted 60 genera as valid within the Lepocreadiinae. One of these is Hypocreadium Ozaki, 1936. It constitutes a group of poorly-known species, characterized by their flattened, broadly oval to circular outline and parasitism in tetradontid hosts. Another diagnostic character is the dorsally situated excretory pore, usually well anterior to the posterior extremity, between the caecal extremities. According to Bray and Cribb (1996) 13 species were recognized Hypocreadium cavum was one of them. Bray and Justine (2006) described H. toombo n. sp. from and Rhinecanthus sp. (Balistidae) in . Bray et al., (2009) redscribed 3 species of the genus Hypocreadium: Hypocreadium cavum; Hypocreadium patellare, and Hypocreadium picasso n. sp. from some species of triggerfish from different locality (Abalistes stellatus; Balistoides viridescens and Rhinecanthus aculeatus, R. verrucosus and fusc respectively). These species are found in the warmer waters of the western Atlantic Ocean and across the Indian and Pacific Ocean. The life cycle is unknown (Bray and Cribb, 1996). In this study, Hypocreadium cavum Bray and Cribb, 1996 was found in Abalistes stellaris, Balistidae, . According to Bray et al. (2009) the great preponderance of records of the genus is from 8 Ali B. Al-Zubaidy fishes of the tetraodontiforms families Monacanthidae, Balistidae, Ostraciidae and Triacanthidae. A few records from other host groups have been reported. Hypocreadium spinosum has been reported solely from the malacanthid Caulolatilus sp. (Manter, 1940) and Parukhin (1978) reported H. patellare from the haemulid Pomadasys hasta (Bloch). Recently, H. myohelicatum has been reported in the carangid Trachinotus rhodopus gill and the serranid Epinephelus itajara (Lichtenstein) (see Lamothe et al., 1997; and Pérez-Ponce de León et al., 1998, 2007). The balistids showing morphological specializations in order to feed echinoderms, coral polyps and other invertebrates with carapace (Vose and Nelson, 1994; and Kurz, 1995). Also, the species is opportunistic, benthic, carnivorous, with a wide spectrum diet [feeding on barnacles, polychaetes, decapod crabs, gastropods, sea stars, sea cucumbers, brittle stars, sea urchins and sand dollars], mainly bottom invertebrates (Costa et al., 1987; Vose and Nelson, 1994; Kurz, 1995; and Figueiredo and Menezes, 2000). Also, Lowe-Mcconnell (1999) observed that balistids fish are depredated by elasmobranches and carnivorous teleosts. This characteristic would give more possibilities of feeding intermediate hosts, as was mentioned in Alves and Luque (2001). According to George-Nascimento (1987), Marcogliese (2002), and Luque and Poulin (2004), the fish species at the intermediate level of the thropic web can showed a high number of parasite species, (18 endo and ectoparasite species recorded from this fish, unpublished data) because a possible accumulation of parasite species in addition with the other levels of the web, mainly larval stages. The presence of lepocreadiid digeneans were recorded for Balistes spp. in several studies (Bravo-Hollis and Manter,1957; Nahhas and Cable,1964; Lamothe,1965; Hussain et al.,1986; and Bray and Cribb,1996). The species studied now, agree well with those described by Bray and Cribb (1996) from the same host species in Heron Island, Australian water, and Bray et al.(2009) in the Indo-West Pacific region, Western Australia and off New Caledonia. Our specimens also similar to Hypocreadium indicum (Madhavis, 1972), differing in the oral sucker being at the base of an anterior notch, which is pronounced in all of the specimens we have of Hypocreadium cavum. In contrast, in Madhavis (1972) figure of Hypocreadium indicum the oral sucker is on as slight anterior protuberance. In addition, the gland-cell field around the

Hypocreadium cavum (Digenia: Lepocreadiidae: Hypocreadium)… 9 terminal genitalia appears distinctly more extensive in Hypocreadium cavum (Bray and Cribb,1996). Hypocreadium cavum was reported in 1999, by Machida and Kuramochi, but did not illustrate, this species from the Balistid, Pseudobalistes flavimarginatus from Palau in Micronesia. These authors point out that in their specimens the ventral sucker is larger and the eggs are smaller. In our specimens the ventral sucker is distinctly smaller and no eggs were seen. Bray and Cribb (2002) also reported this species from Sufflamen fraenatum. They found the measurements to agree with those of Bray and Cribb (1996). Lepocreadiidae, is previously recorded in the Red Sea fishes, and this is represented in five species belonging to three genera: Hypocreadium balistes (Nagaty, 1942) from Balistes aculeatus by Nagaty (1942), and From Abalistes stellaris and Rhinecanthus sp. by Parukhin (1970, 1971 and 1989); H. patellare (Yamaguti, 1938) Manter, 1940 from Abalistes stellaris by Parukhin (1989); P. sohali Nagaty, 1942 (Lepocreadium sohali) from Acanthurus sohal by Nagaty (1942); P. layman Saoud and Ramadan, 1985 from Diodon hystrix by Saoud and Ramadan (1985), and Gibsonius aegyptensis Hassanine, 2005 from Rhabdosargus haffara by Hassanine (2005). Besides, this study recoded H. cavum Bray and Cribb (1996). However, the variability of the species of Hypocreadium is poorly understood. In their key Bray and Cribb (1996) utilized the body-shape, the extension of the uterus into the post- ovarian region (or not), the presence of an anterior notch and the level of the genital pore as important key characters, along with more usual features such as sucker-ratio, egg-size and Vitelline distribution. According to Bray (2004), Lepocreadiidae is one of four families of Digean that have species reaching below 5,000 meters and it can be said their individual members inhabit the abyssal regions. Two subfamilies of Lepocreadiidae Odhner, 1905 are represented in deep- waters, the Lepocreadiinae Odhner, 1905 and the Lepidapedinae Yamaguti, 1958. Lepocreadiinae species, Prodistomum priedei Bray and Merrett, 1998, is, however, reported to 985 meters (Bray and Merrett 1998). This parasite appears to have migrated into deep waters in parallel with its perciform host. The Perciforms, an enormous shallow-water group, has relatively few deep-sea representatives (Weitzman 1997). Clearly a relatively few families contain species that have successfully radiated in the really deep sea. The best evidence we have is that only the Lepocreadiidae and Fellodistomidae have species-rich genera in the 10 Ali B. Al-Zubaidy deeper regions (Bray, 2004), thus the depth ranges of digeneids are clearly dictated to some extent by the distribution of their definitive hosts and are, presumably, also limited by the intermediate hosts. Generally, the members of the family Lepocreadiidae are common intestinal parasites of marine fishes (Marcogliese, 1995). Cercariae are usually trichocercous and occelated and produced by rediae in snails (Bray, 1988). On the other hand, metacercariae are reported to occur in a variety of planktonic and benthonic groups, including reports of infested ctenophores and hydromedusae (e.g. Marcogliese, 1995; Martorelli, 1991, 2001; and Gómez del Prado-Rosas et al., 2000).The members of Lepocreadiidae are known to live encysted in polychaetes; gastropods; bivalves; echinoids, and fish (Bray, 1988); and unencysted metacercariae have been reported for hydromedusae; ctenophores and mollusks (Bray, 1988). Also, one case of Lepocreadiidae metacercariae encysted in “coelenterates” has recently been reported (Martorelli, 1996). Lepocreadiidae cercariae might also actively penetrate the medusae, losing their tail, and persisting inside their host without the formation of cysts (Martorelli, 1991). The transference of the metacercaria from the gelatinous plankton to the paratenic or definitive hosts (fish) is possible because gelatinous organisms may be important food items in the fish diet. Although the complete life cycle of the present digenean is still unknown (Bray et al., 2009).

Acknowledgement I would like to express my deep gratitude to Prof. Dr. R. A. Bray, Department of Zoology, Natural History Museum, Cromwell Road, London, for identification of digenean and additional information on parasite.

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Hypocreadium cavum (Digenia: Lepocreadiidae: Hypocreadium)… 11

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Luque, J.L. and Poulin, R. (2004) Use of fish as intermediate hosts by helminth parasites. Acta Parasitologica., 49(4): 353-361. Machida, M. and Kuramochi, T. (1999) Digenean trematodes from tetraodontiform fishes from Japanese and adjacent waters. Bulletin of the National Science Museum, Tokyo. Series A. Zoology, 25: 1-25. Madhavis, R. (1972) Digenetic trematodes from marine fishes of Waltair Coast, Bay of Bengal. I. Family Lepocreadiidae. Journal of Parasitology, 58: 217-225. Manter, H.W. (1940) Digenetic trematodes of fishes from the Galapagos Islands and the neighboring Pacific. Allan Hancock Pacific Expeditions., 2: 325-497. Marcogliese, D.J. (1995) The role of zooplankton in the transmission of helminth parasites to fish. Rev. Fish. Biol. Fisher., 5: 336-371. Marcogiliese, D.J. (2002) Food webs and transmission of parasites to marine fish. Parasitology., 124(1): 83-99. Martorelli, S.R. (1991) Primera cita de una cercaria tricocerca parásita de Dorsanum moniliferum (Mollusca, Buccinidae) para el Atlántico sud-occidental. Aportes al conocimiento de su ciclo de vida. Geotropica, 37: 57-65. Martorelli, S.R. (1996) First record of encysted metacercaria in hydrozoan jellyfishes and ctenophores of the Southern Atlantic. J. Parasit., 82: 352-353. Martorelli, S.R. (2001) Digenean parasites of jellyfish and ctenophores of the Southern Atlantic. Hydrobiol., 451: 305-310. Nagaty, H.F. (1942) Trematodes of fishes from the Red Sea. Part 3. On seven new Allocreadiid species. Publications of the Marine Biological Station Ghardaqa (Red Sea), 4: 1-27. Nahhas, F.M. and Cable, R.M. (1964) Digenetic and aspidogastrid trematodes from marine fishes of Curaçao and Jamaica. Tulane Studies in Zoology., 11: 169-228. Oshmarin, P.G. (1965) On the trematode fauna and freshwater fishes of Vitnam. In: Leonov, A.A., Mamaev, Y.L. and Oshmarin, P.G. (Eds) Parasitic worms of domestic and wild animals. Vladivostok: Akademiya Nauk SSSR., 213-249 (In Russian). Ozaki, Y. (1936) Two new genera of the trematode family, Allocreadiidae. Zoological Magazine., 48: 513-518. Parukhin, A.M. (1970) On the study of trematode fauna in fish from the Red Sea and Aden Bay. Biologiya Morya, Kiev., 20: 187-213 (In Russian). Parukhin, A.M. (1971)A study on the trematode fauna of fishes of the Red Sea and Aden Bay. Biologiya Morya, Kiev., 25: 136-146 (In Russian). Parukhin, A.M. (1978) [On studies in trematodofauna of the Indian and Atlantic Ocean fishes]. Biologiya Morya, Kiev, 45: 90-99 (In Russian). Parukhin, A.M. (1989) [Parasitic worms of bottom fishes of the southern seas.] Naukova Dumka, Kiev, 155 p. (InRussian). Pérez-Ponce de León, G.; León-Règagnon, V. and Monks, S. (1998) Theletrum lamothei sp. nov. (Digenea), parasite of Echidna nocturna from Cuajiniquil, Guanacaste, and other digenes of marine fishes from Costa Rica. Revista de Biologia Tropical, 46: 345-354. Pérez-Ponce de León, G.; Garcia-Prieto, L. and Mendoza-Garfias, B. (2007) Trematode parasites (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa, 1534: 1-247. Saoud, M.F.A. and Ramadan, M.M. (1985)Studies on the trematodes of the genus Enenterum Linton, 1910 (Opecoelidae) and the genus Pseudocreadium Layman, 1930 (Lepocreadiidae) from some Red Sea fish. Qatar Univ. Sci. Bull., 5: 223-253. Vose, F.E. and Nelson, W.G. (1994) Gray triggerfish (Balistes capriscus Gmelin) feeding from artificial and natural substrate in shallow Atlantic water of Florida. Bulletin of Marine Science,. 55(4): 1316-1323. Weitzman, S.H. (1997) Systematics of deep-sea fishes. In: D.J. Randall and A.P. Farrell (Eds.), Deep-sea Fishes. Academic Press, San Diego., pp: 43-77. Yamaguti, S. (1971) Synopsis of the digenetic trematodes of vertebrates. Vols. 1 y 2. Keigaku Publishing Co., Tokyo. Japon. 1423 p.

Hypocreadium cavum (Digenia: Lepocreadiidae: Hypocreadium)… 13

هايبوكريديم كافيم )المثقبات ثنائية التولد: عائمة ليبوكريديدي: جنس هايبوكريديم( في األسماك البحرية، أباليستس ستيالريس )عائمة باليستيدي( من البحر األحمر، الساحل اليمني

علي بناوي الزبيدي قسم األحياء البحرية والمصائد، كمية عموم البحار والبيئة، جامعة الحديدة، اليمن

المستتتصم . تتتتم جمتتتج نمتتا ا أستتتماك الدراستتتة (Abalistes stellaris) العائتتدة ىلتتئ عائمتتة باليستتتيدي (Balistidae) متتن ستتوس الستتمك المركتت ي في مدينة الحديتدة، التيمن، صتالل التتترة متن ستبتمبر 8002 ىلتئ يوليتو 8000م. وجتتد أن ستتتة أستتماك )نستتبة 5.7٪( متتن مجمتتو 20 ستتمكة فحصتتتتتتتتتتت، كانتتتتتتتتتتت حاويتتتتتتتتتتة عمتتتتتتتتتتئ ال تيمتتتتتتتتتتي هايبوكريتتتتتتتتتتديم كتتتتتتتتتتافيوم Hypocreadium cavum. ونظرا لعدم وجود أي دراسة قي ه ا المجتال عمئ األسماك البحرية، الساحل اليمني لمبحر األحمر، لت ا فت ن ظرتور ه ا ال تيمي يعد التسجيل األول له في اليمن.