JKAU: Mar. Sci., Vol. 22, No. 1, pp: 45-64 (2011 A.D. / 1432 A.H.) DOI : 10.4197/Mar. 22-1.4

Digenetic Trematodes (: Baer, 1827 and Rhipidocotyle Diesing, 1858) From Red Sea , Yemen Coast

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

Abstract. A total of 205 specimens of marine , belonging to four different species (60 Thunnus tanggol, 70 Sphyraena barracuda, 60 Lutjanus argentimaculatus,and15Carangiodes bajad) were examined for trematode parasites,especially Bucephalidae. Fishes were collected from local fish market in Hodeidah, during the period between September 2008 and July 2010. Three species of degenic trematodes were found, namely: 1- Bucephalus margaritae Ozaki and Ishibashi, 1934, belonging to Genus Bucephalus Baer, 1827.The digenetic trematode Bucephalus margaritae is described from the intestine and pyloric caecum of Sphyraena barracuda (English name: Barracudas) of family Sphyraenidae and from intestine of Carangoides bajad (English name: Jacks, Trevallies, and Scads) of family Carangidae. 2- Bucephalus varicus Manter, 1940. This parasite is described from the intestine of Carangoides bajad only. 3- Rhipidocotyle pentagonum (Ozaki, 1924) Eckmann, 1932 belonging to Genus Rhipidocotyle Diesing, 1858. The digenetic trematode Rhipidocotyle pentagonum is described from the stomach of fishes of family Scombridae (English name: Mackerels and tunas) Thunnus tanggol and Family of Lutjanidae (English name :Snappers/Jobfishes) Lutjanusargentimaculatus. 4- All species represent new records from the Red Sea,Yemen coastal water.

45 46 Ali B. Al-Zubaidy

Introduction Fish parasites are important sentinels of environmental health (Arkoosh et al., 2004) because they can only thrive in systems with the proper suite of invertebrates to serve as intermediate hosts, the correct physical and chemical conditions, and the proper physiology in the final host. Parasites also can act to regulate aquatic populations (McCallum and Dobson, 1995) and may be as important as competition and predation in structuring communities (Minchella and Scott, 1991). Parasites have proven quite useful as natural tags in delineating fish stocks (Urawa et al., 1998), and can provide valuable information on the diet, feeding behavior, migration patterns, and systematic of fish populations (Marcogliese and Cone, 1997). During a lifetime, a fish parasite may pass through one or more intermediate hosts, one or more fish species, and often a final avian or mammalian host, making the parasite both a trophic marker and the top predator in the food web (Moles, 2007). Marine parasites are of immense ecological and economic importance. Almost groups of marine including the various invertebrates, fish, marine birds and reptiles, are hosts to parasites (Rohde, 2006). The parasite fauna of marine fishes and invertebrates is extremely rich and diverse and has the largest total biomass. Many parasites are highly pathogenic to their hosts, and may affect their number, reduce the quality of raw fish and fish products, or be harmful to a human (Korotaeva, 1973). Digenetic trematodes represent a large group of internal metazoan . Trematodes have complex life cycles, in which a mollusc serves as the first intermediate host and a vertebrate is usually the definitive host (Taskinen, 1998). According to Cribb et al. (2002) have over 100 families, well over 1000 genera and many thousands of species, many of them are of great importance to marine ecosystems (Korotaeva, 1973). Digeneids are important fish parasites with fishes serving both as intermediate and final hosts(about 5000 species of digeneans of fishes from 1115 genera). Adults range in size from <0.2 mm to >10 cm. They are permanent parasites in most marine fishes, and in many freshwater fishes, , reptiles, mammals and birds(Bray, 1984). Larval stages occur in a variety of invertebrates and vertebrates. Its usually Digenetic Trematodes (Bucephalidae: Bucephalus Bear, … 47 occur in either the intestine, stomach or mouth, or occasionally lungs and other organs, (Larval forms occur in almost any tissue). The epipelagic zone is a peculiar and very interesting biotope parasitologically. The most abundant of them are digeneids (Pozdnyakov, 1981). Trematodes of the families Bucephalidae; Allocreadiidae; Opecoelidae; Lepocreadiidae; and Fellodistomidae are not common for the pelagic zone, but are found there occasionally. Buron and Morand (2002) reported that 57% of metazoan parasites in waters deeper than 1000 meter were digeneans, 25% crustaceans (80% copepods), 10% cestodes, 4% acanthocephalans, 2% nematodes and 2% monogeneans. Protistans (in which they included the myxozoans) make up less than 17% of parasite records. The Red Sea, an important offshoot from the Indian ocean, has a very rich and varied fish fauna (Saoud and Ramadan, 1983). The Literature on the parasites of Red Sea fishes, particularly helminths, is relatively limited, several papers on the trematodes of the Red Sea fishes were published by (Nagaty, 1954; Nagaty and Abdel-Aal, 1962; Saoud and Ramadan,1983; Hassanine and Gibson, 2005 a & b; Al- Zubaidy, 2010, and Al-Jahdali, 2010 ).

Materials and Methods A total of 205 specimens of marine fish, belonging to four different species (60 Thunnus tanggol, 70 Sphyraena barracuda, 60 Lutjanus argentimaculatus, and 15 Carangiodes bajad) were examined for trematode parasites, especially Bucephalidae. Fishes were collected from local fish market in Hodeidah, during the period between September 2008 and July 2010. Standard parasitological techniques were used to examine the alimentary canal of the fish. Trematodes were removed from their host fishes under a dissecting microscope and observed live under a compound microscope. Some worms were fixed in alcohol-formalin- acetic acid (AFA) under a slight cover slip pressure and preserved in 75% ethyl alcohol. Whole-mounts were stained in alum carmine, cleared in lactophenol and mounted in Canada balsam. Trematodes were identified to species level based on the keys of Skrjabin et al. (1964), Yamaguti (1971), Schell (1985), Gibson and Bray (2002), and With the help of Prof. Dr. Bray and Prof. Dr. Fabiana. 48 Ali B. Al-Zubaidy

Results and Discussion Parasitological investigation of 205 specimens of four species of marine fishes (Thunnus tanggol, Sphyraena barracuda, Lutjanus argenti- maculates, and Carangoides bajad ) revealed 3 species of parasites: Bucephalus margaritae Ozaki et Ishibashi, 1934; Bucephalus varicus Manter,1940 and Rhipidocotyle pentagonum (Ozaki, 1924) Eckmann, 1932. Rhipidocotyle pentagonum (Ozaki, 1924) Eckmann, 1932 Bucephalus margaritae Ozaki et Ishibashi, 1934 Bucephalus varicus Manter,1940 . Classification: Infrakingdom: Platyzoa Cavalier-Smith,1998 Phylum: Platy helminthes Gegenbaur,1859 Subphylum: Neodermata (Ehlers,1985)Cavalier-Smith,1998 Infraphylum: (Rudolphi,1808) Cavalier-Smith, 1998 Class: Trematoda Rudolphi 1808 Subclass: Digenea Carus 1863 Super order: Anepitheliocystidia La Rue, 1957 Order: Strigeatoidea La Rue, 1957 Suborder: Brachylaimata Super family: Bucephaloidea La Rue, 1926 Synonyms: Gasterostomatiformes Skrjabin et Schulz, 1937 Gasterostomata (Odhner, 1905) Skrajabin et Schulz, 1937 Alcicornata Skrjabin et Schulz, 1937 Family: Bucephalidae Poche, 1907 Subfamily: Bucephalinae Poche, 1907 Genus:Bucephalus Baer,1827 Synonyms: Gasterostomum Siebold, 1848 Eubucephalus Diesing, 1855 Labratrema Maillard, 1975 -Bucephalus margaritae Ozaki et Ishibashi, 1934 -Bucephalus varicus Manter,1940 . Genus: Rhipidocotyle Diesing, 1858 Synonyms: Nannoenteron Ozaki,1924 Nannoenterum Ozaki,1928 Pararhipidocotyle Kohn,1970 Digenetic Trematodes (Bucephalidae: Bucephalus Bear, … 49

Rhipidocotyle pentagonum (Ozaki, 1924) Eckmann, 1932 Bucephalus margaritae Ozaki et Ishibashi, 1934 Bucephalus varicus Manter,1940 .

1-Bucephalus margaritae Ozaki and Ishibashi, 1934 (Fig.1). 1.1. Description and Measurements (in µm) (base on 4specimens) Body: Its length varies from 343.0 to 834.5 (mean 533.7 ± 121.3) and 58.2 to 170.1(87.1 ± 18.1) width. Spined tegument, with small spines all over the body. Rhynchus: 112 in diameter, Funnel-like apical, with concave bottom and seven marginal tentacles, each one is divided in its basal part into two branches. Mouth: middle third of body. Oral sucker: post equatorial, circular, muscular, 349.5 ± 20.2 (229.3 – 556.1) from the anterior extremity. Pharynx: Small, rounded, 39-52(43± 2.1). Esophagus: Short, surrounded by glandular cells. Vitellaria: Numerous rounded, distributed in the median equatorial body region and laterally in two convergents camps, with 14 to 18 each side. Intestine: simple, sac shaped. Ovary: globular, rounded, 32.0± 9. 4 (24.5 – 46.1) long and 54.0 (36.0 – 117.3) wide. smooth edges, slightly right and located between the rear edge of the blind bowel and anterior testis. Glands: Mehlis gland and Laurer´s canal not evidenced. Uterus: Winding, which can reach the third front of the body and then reaches the region intertesticular. Uterine loops exceed the anterior limit of vitellaria and posteriorly reaches the body´s posterior extremity. Uterus final portion and partially involves the cirrus inside´s genital atrium. Testes: 2, rounded, smooth edges, posterior to oral sucker, one after the other or slightly oblique to each other, globular with 41.0 ± 9.7 (34.0 – 64.2) long and 26.7 ± 6.6 (20.2 – 44.1) wide (anterior) and 36.4 (22.3 – 82.2) long and 38.5 (28.0 – 76.0) wide (posterior). 50 Ali B. Al-Zubaidy

Eggs: Ovoids and operculated,19-20 (20±0.01) x 8-11(9 ±1.2), numerous small . Cirrus sac: Elongated, large with walls muscle, localized in the posterior third of the body beginning at the level of first testicule, 100.5 ± 17.9 (78.2 – 200.3) long. It contains a vesicle seminal, round, an elongated pars prostate. Excretory pore: Terminal. 1.2.Taxonomic Summary: Name: Bucephalus margaritae Ozaki et Ishibashi, 1934 , also in Bray (1984), Yamaguti (1958; 1971), Nahhas et al. (2006), Chinchilla et al. (2006) and Kohn et al. (2007). Synonyms: Prosorhynchus margaritae (Ozaki et Ishibashi, 1934) Ozaki, 1960; von Baer, 1827(in Caballero et al., 1953 and Baturo, 1977) ; Bucephalus varicus Manter, 1940(in Kohn ,1968; Madhavi, 1974; Amato, 1982; Takemoto et al., 1995, 1996; Pereira Junior et al., 1996; Chaves and Luque, 1998;Luque et al., 2000;Luque and Alves, 2001; and Alves et al., 2004); Bucephalus retractilis Yamaguti, 1952,1958,1971; Bucephalus pseudovaricus Velásquez, 1959, and Yamaguti (1971) ; Bucephalus carangoides Yamaguti, 1970; Bucephalus ulua Yamaguti, 1970,1971. Host: Sphyraena barracuda; Carangoides bajad. Locality: Red Sea, Hodeidah- Yemen coastal water. Site of infection: intestine and pyloric caecum. Prevalence: Sphyraena barracuda (7.14%); Carangoides bajad (13.3%). Intensity of infection: in Sphyraena barracuda,5 out of the 70 fish examined were parasitized by 2, 3, 7, 5 and 3 trematodes respectively. Range =2-7. Mean = 4.0 Parasite per infected fish. While the intensity of infection in Carangoides bajad : 2 out of the 15 fish examined were parasitized by 4, and 6 trematodes respectively. Range = 4- 6. Mean = 5.0 parasite per infected fish. 1.3. Species distribution: Worldwide and is found in tropical and subtropical waters being registered in the Caribbean sea, pacific coast of Panama,Mexico,Brazil, Venezuela, Guinea-Bissau, China, Mediterranean coast of Israel, Arabian Digenetic Trematodes (Bucephalidae: Bucephalus Bear, … 51

Gulf off the coast of Kuwait, Red Sea, Arabian Sea, Philippine, Hawaii, India and Japan (Amato, 1982; Chinchilla et al., 2006; Nahhas et al., 2006).

Discussion Genus Bucephalus requires a detailed review as many species are proposed on the basis of a single specimen have a fish as hosts migratory cosmopolitan and many are separated considering a few features that come in ranges of variability of some other species. Clearly, for statistical studies of Allometric growth, cytogenetic and elucidation of life cycles are required and possibly promote high synonymy. This genus has no less than 70 species, eleven of them (eight in the Caribbean and three in the Pacific) using a barracuda (Sphyraena) as definitive host (Chinchila et al., 2006). The specimens studied were identified as belonging to the species Bucephalus margaritae Ozaki et Ishibashi, 1934 on the basis of morphometric and body characteristics, the rhynchus standing out with seven retractile tentacles. According to Nahhas et al. (2006), the diagnostic character of greater relevance for B. margaritae is the presence of seven tentacles, each one with two projections: one big and basal and the other small and distal. According to Spakulová et al. (2002), 12 Bucephalus species has a rinchus surrounded by seven tentacles with two projections. Bucephalus priacanthi Manter, 1940 and Bucephalus scorpaenae Manter, 1940 are described from marine fishes of Florida and B. varicus in marine fishes from Brazil. Woodhead, 1930 is registered from freshwater fishes of United States; Bucephalus fragilis Velásquez, 1959 and Bucephalus uranoscopi Yamaguti, 1934 are described from marine fishes of the Philippines and Japan and Bucephalus anguillae Spakulová, Macko, Berrili et Dezfuli, 2002 in Anguilla anguilla (Linnaeus, 1758) of Adriatic Sea. Bucephalus minimus (Stossich, 1887), Bucephalus blanchardi (Stossich, 1898) and Bucephalus labracis Paggi et Orecchia, 1965 were described from D. labrax of Mediterranean Sea. Bucephalus minimus was transferred by Yamaguti (1971) to Bucephalopsis Yamaguti, 1971. Bartoli et al. (2005) reported Bucephalus gorgon (Linton, 1905) from carangids of West Mediterranean also containing seven tentacles in its rhynchus. However, besides their register of approximately 11 to 14 papillae at the basis of the seven tentacles, this 52 Ali B. Al-Zubaidy species does not present the small distal projection characteristic of B. margaritae. In addition, the only species from the cited above that clearly presents the ovary in a pre-pharynx position is B. margaritae (Spakulova et al., 2002).

Fig. 1. Bucephalus margaritae from fishes, Sphyraena barracuda & Carangoides bajad scale bar = 0.5mm.Te = tentacle. v = vitellaria. u = uterus. ov = ovary. T= testes. cs = cirrus sac. sv = seminal vesicle. pd = prostatic duct. ga = genital lobe. ed = ejaculatory duct. ep = excretory pore.

Another diagnostic character that varies in B. margaritae is the egg size. Nahhas et al. (2006) registered eggs of this species with 13-20 μm long and 10-18 μm wide. In Brazil, Kohn (1968), while studying B. margaritae collected from the esophagus of M. americanus, registered eggs with 21-27 by 11-12 μm. Nahhas et al. (2006) affirmed that the means of B. margaritae´s eggs measured found in the literature were 14- 27 by 10-13 μm. This parasite species is cosmopolitan, and fish used in preference to family Carangidae as definitive hosts. According to Costa et al. (2010), it a common parasite of many fish, which was found in the following fish families: Carangidae (19species); Sciaenidae (3species); Gadidae Digenetic Trematodes (Bucephalidae: Bucephalus Bear, … 53

(2species); Gerreidae (1species), and Sphyraenidae (2species). B. margaritae has been described by many authors as Sogandares and Hutton (1959), Nahhas and Cable (1964), Nahhas and Short (1965), and Rees (1970), Who identified it as B. varicus for the Gulf of Mexico, Florida, Caribbean Sea and the Pacific coast of America (Manter, 1940, and Caballero et al.,1953); on the Brazilian coast by Kohn (1968), Amato (1982), and Fernandes et al. (1985); for the Red Sea by Nagaty (1937); Fischthal (1980) in Mediterranean Sea, and Gupta and Puri (1981) in the Indian Ocean. Other authors point also in the Philippines, Hawaii, China Sea, Arabian Sea, and South African coasts(Chinchilla et al., 2006 ). An historical revision of B. margaritae and its relation with B. polymorphus was done by Bray (1984). Despite the morphological resemblance between the two species, leading some authors to indicate them as synonyms (Nahhas et al., 2006). 2-Bucephalus varicus Manter,1940 (Fig. 2). 2.1. Description (base on 7 specimens) and Measurements (in mm except the eggs in µm). Is a small trematode with a significant anterior end, it bears a sucker which is surrounded by seven contractile muscular digitate processes. Body elongate. The rhynchus is relatively large, with 7 tentacles on the anterior end. The tentacles are often not protruded, resulting in knob-like structures around the anterior sucker. Slight pressure on live specimens may cause the tentacles to protrude. The rhynchus should be examined in live flukes when possible. The definitive shape and structures may change in dead or improperly preserved samples. Body: 0.980-2.500 (1.90)long, 0.200-0.310(0.250) wide . Rhynchus: 0.169-0.225(0.200) x 0.147-260(0.210). Pharynx: 0,050 - 0,063 (0,056) x 0,036-0,049(0,042). Cirrus sac: 0. 210- 0.385(0.289) x 0.066-0.091(0.071). Testis: Anterior,0.115-0.135(0.123) x 0.100-0.165 (0.130). Posterior, 0.110-0.128(0.118) x 0.122-0.175(0.144). Ovary: 0,070-0,105 (0,089) x 0,057-0,082(0,072) Eggs:17-22 x11-13.

54 Ali B. Al-Zubaidy

Fig. 2. Bucephalus varicus from fish, Carangoides bajad. A-Whole worm,ventral view. Scale bar= 03 mm. Te = tentacle. v = vitellaria . ov = ovary. T= testes. cs = cirrus sac. B- Eggs.

2.2.Taxonomic Summary: Host: Carangoides bajad. Locality: Red Sea, Hodeidah- Yemen coastal water. Site of infection: Intestine Prevalence: 40.0%. Intensity of infection:6 out of the15 fish examined were parasitized by 2,2,1,2,4,and 4 trematodes respectively. Range =1-4 . Mean = 2.5 Parasite per infected fish. 2.3. Synonyms: Bucephalus polymorphus of Nagaty, 1937, and Caballero et al., 1953; B. pseudovaricus Velasquez; B. solitarius Kohn. The parasite name appears to be highly variable. This fluke needs to be redefined and refigured. 2.4. Species distribution: Bucephalus varicus is world wide parasite, has some interesting distributional gaps, this worm possibly occurs in greater amberjack and in jacks and other fishes from the Pacific coast of Panama; Baja California, Mexico; the Red Sea; Okinawa, Japan; and the Philippines(Williams and LucyBunkley-Willams,1996). Digenetic Trematodes (Bucephalidae: Bucephalus Bear, … 55

Discussion This species found on 6 fishes, maximally to 4 individuals per one fish, they have occurred in the intestine. It largely occurs in jacks, particularly those in the genus Caranx, but not exclusively enough to be family specific (Williams and LucyBunkley-Willams,1996). Its life cycle includes two intermediate hosts and one final host. As the second intermediate host a large variety of fish species has been described and metacercariae develop in epidermal cysts, not limited to a specific location on the fish body. The final hosts are various piscivorous fish species (Mühlegger et al.2009). Bucephalus varicus, investigated is similar in some morphometric characteristics with those described by different authors, Kohn (1968) in Brazil, Gupta and Puri(1981) in India and Pons (1993)in Venezuela (Table.1).Importantly,while all descriptions agree on the presence of seven tentacles, Pons(1993) also observed in each of the portions of the tentacle projection sharp as thorns. These projections were not observed in specimens investigated here, and also Gupta and Puri (1981) specimens, and according to Manter (1940), appear when you press the tip of the tentacle. From my own observation it is found that mostly, the specimens that were recovered already dead showed distinct differences when compared with the freshly-collected material. In spite of the world-wide for this species according to the various sources and references which referred to register it from the various fish hosts, world-wide geographical areas, it is important to refer to a clear fact that there has been an overlapping occurring from some others in the naming among this species Bucephalus varicus; B. margaritae, perhaps it may be the type-species B. polymorphus Baer, 1827. It seems this overlapping is a part of it, this may refer to the large variables in measuring the various organs for this species (Table 1) from the researchers, However these play a role relating to various factors represented by different ways of fixation and processing of material in the past, different developmental stages of the specimen studied, the influence of type fish hosts and ecology, moreover the difference may occur for some of parts of species after death and fixation. As a result, I draw the attention of researchers in the field to necessary avoidance of this overlapping through the study of elucidation of life cycles and carrying out some cytogenetic studies on this species. 56 Ali B. Al-Zubaidy

Table 1. Comparison of morphometric characteristics of B.varicus investigation with those reported by other authors. Measurements: (in mm except the eggs in µ m). organs B.varicus B.varicus B.varicus B.varicus 0,980-2,500(1,90) x 0,810-1,235(1,132) x Body 1,50-0,20 3,215 x 0,600 0,200-0,310 (0,250) 0,180-0,306(0,226)

With 7 tentacles With 7 tentacles With7tentacles With7 tentacles 0,169-0,225(0,200)x Rhynchus 0,167-0,252 (0,213) x 0,14 x 0,10 0,189 x 0,137 0,147-0,260(0,210) 0,157- 0,275(0,217)

0,050- 0,072(0,063) x 0,050 - 0,063(0,056) x Pharynx 0,054 x 0,051 0,103- x 0,111 0,047- 0,052(0,048) 0,036-0,049(0,042) 0,200- 0,441(0,305) x 0,210-0,385(0,289) x Cirrus sac 0,380 x 0,075 1,05 x 0,137 0,059-0,090(0,064) 0,066-0,091(0,071) A: 0,117-0,142 A:0,115-0,135(0,123)x Testis. (0,129) x 0,100-0,165(0,130) A-0,13 x 0,11 A: 0,231 x 0,222 A=Anterior 0,105-0,185(0,170) P:0,110-0,128(0,118)x P-0,13 x 0,10 P: 0,214 x 0,214 P=Posterior P:0,112-0,147(?)x 0,122-0,175(0,144) 0,132- 0,247 (0,260) 0,070-0,105 (0,089) x 0,080-0,115 (0,102) x Ovary 0,09 x 0,07 0,171 x 0,154 0,057-0,082(0,072) 0,067-0,092(0,082)

Eggs 21-27 x 11-12 12-17 x 8-12 15-16 x 7- 8 (7,5) 17-22 x 11-12

Menticirrhus Caranx Centropomus Carangoides bajad Host americanus malabaricus undecimalis (Carangidae) (Sciaenidae) (Carangidae) (Centropomidae) Site of esophageal Intestine intestine Intestine infected Locality Brazil India Venezuela Yemen Gupta & Puri, Reference Kohn (1968) Pons (1993) Present study 1981

3-Rhipidocotyle pentagonum (Ozaki, 1924) Eckmann, 1932 (Fig. 3). 3.1. Description (base on 5specimens), and Measurements (in µm except body length and width). Body: 1.97-2.87 mm (2.46 mm) in length by 0.41-0.86 mm (0.68 mm) in width Anterior sucker: 106-198 (134) x 122-254 (169). Cephalic hood: 168-279 (215) x207-348 (275). Pharynx: 79-149 (125) x 93-208 (133). Caecum: 326-457 (397) x 195-345 (291). Anterior testis: 150-265 (219) x 188-280 (203). Posterior testis: 117-279 (212) x 123-266 (194). Cirrus-sac: 559-988 (718) x149-253 (216). Digenetic Trematodes (Bucephalidae: Bucephalus Bear, … 57

Seminal vesicle: 87-186 (132) x 75-142 (106). Ovary: 129-185 (159) x 94-158 (124). Eggs: 18-22 (21) x 14-16 (15). 3.2. Taxonomic Summary: Host: Thunnus tanggol and Lutjanus argentimaculatus. Locality: Red Sea, Hodeidah- Yemen coastal water. Site of infection: stomach. Prevalence: Thunnus tanggol (8.3%) ; Lutjanus argentimaculatus (5%). Intensity of infection : in Thunnus tanggol: 5 out of the 60 fish examined were parasitized by 7, 3, 2, 5 and 1 trematodes respectively. Range =1-7. Mean =3.6 Parasite per infected fish. While the intensity of infection in Lutjanus argentimaculatus: 3out of the 60 fish examined were parasitized by 4,1,and 4 trematodes respectively. Range =1- 4. Mean=3.0 parasite per infected fish. Synonym: Nannoenterum pentagonum Ozaki,1924, Japan.

Discussion Family Bucephalidae Poche, 1907, are found in the intestine of marine, brackish water, and freshwater fish. They differ from all other digeneans by the configuration of their digestive system and terminal genitalia and by the presence of an anterior rhynchus, for attachment, that is dissociated from the digestive system (Overstreet and Curran, 2002; Bott and Cribb, 2005). Many nominal species have been described in some genera, particularly in the subfamily Bucephalinae Poche, 1907, Rhipidocotyle Diesing, 1858 being a case in point. Rhipidocotyle, includes more than 40 spp. of marine and freshwater fishes; larval stages known for some, not miracidium (Richardson, 1990). In this genus, the species are not always clearly characterized due to the great variability of the taxonomic characters, such as the number and arrangement of vitelline follicles, the position of the gonads relative to the vitelline fields and other organs, the extent of the digestive caecum and the characteristics of the cirrus-sac, uterine loops and excretory vesicle (Bartoli et al., 2006). The described material belongs to Rhipidocotyle because of its dorsally hooded rhynchus, curved pars prostatica, and pretesticular ovary (Overstreet and Curran, 2002; Jones et al., 2003). Rhipidocotyle, is previously recorded in the Red Sea fishes, and this represented in two species R. khalili and R. eckmanni (Nagaty, 1937). 58 Ali B. Al-Zubaidy

Fig. 3. Rhipidocotyle pentagonum from fishes, Thunnus tanggol & Lutjanus argentimaculatus.

Rhipidocotyle pentagonum was originally described from Scomberomorus nipponicus from Japan by Ozaki (1924), and has been reported in different hosts and localities: Thunnus thynnus from the Mediterranean (Eckmann, 1932) and from the Pacific Ocean (Yamaguti, 1938); Auxis thazard and Euthynnus affinis from the Gulf of Bengal (Madhavi,1974); E.lineatus from Mexico (Castillo-Sánches et al.,1997), and A. thazard and Katsuwonus pelamis from South America (Brazil) (Fernandes et al,. 2002). Rhipidocotyle pentagonum (Ozaki, 1924) is reported for the first time in Yemen parasitizing Thunnus tanggol and Lutjanus argentimaculatus hosts. The specimens are similar with those reported by Ozaki (1928), Eckmann (1932), Yamaguti (1938), and Fernandes et al. (2002). In the present study it is obvious that he specimens taken from Red Sea,Yemen coastal water presented larger measurements than those reported by Yamaguti, (1938) and Fernandes et al. (2002). Digenetic Trematodes (Bucephalidae: Bucephalus Bear, … 59

Parasites in general, and trematodes in particular, display a wide range of body sizes and shapes and substantial variation in the relative dimensions of anatomical structures (Gibson and Bray, 2002; Jones et al., 2005). This could clearly explain that the differences are not due to variations in technique only, but most likely to geographical variations, and may represent different strains of the same species. 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 digeneans. Thanks are also extended to Prof. Dr. B.D. Fabiana, in the Museo de plata Division Zoologia Invertebrates., Buenos Aires, Argentina, for his assistance in identification and additional information on the digeneans parasite.

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Digenetic Trematodes (Bucephalidae: Bucephalus Bear, … 63

المثقبات ثنائية التولد )عائمة بيوسيفاليدي جنسي بيوسيفاليس ورابيدوكوتايل( من أسماك البحر األحمر، الساحل اليمني

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

المستتتصم . تتتم جمتت 502 ستتمكة متتن أستتماك البحتتر ا حمتتر، الميتتا الستتاحمية اليمنيتتة، تعتتود إلتتأ أربعتتة أنتتوا ستتمكية مصتمفتتة )30 نمتتو من أسماك الدراك أو التونة، و40 نمو من أستماك البركتود ، و 30 نمتتتو متتتن أستتتماك الن ا تتتات أو أستتتماك الحمتتترة، و 52 نمتتتو متتتن أسماك البياض(، صالل الفترة من ستبتمبر 5005 إلتأ يوليتو 5050م. وقد تم فح تمك األستماك بحثتا عتن لفيميتات المثقبتات لائفتة ثنائيتة التولتتد، عائمتتة بيوستتيفاليدي وكانتتت نتيجتتة الفحتت تستتجيل ثالثتتة أنتتوا من تمك اللفيميات وهي:

5- بيوستتتتتتتتتتيفاليس مارجاريتتتتتتتتتتت أو اكتتتتتتتتتتي و ا با تتتتتتتتتتي، 5691 Bucephalus margaritae العائتتدة إلتتأ جتتنس بيوستتيفاليس بيتتر 5554 Bucephalus Baer, 1827 وقد سجل وجودها في أمعاء وأعتور أستماك البركتتتود متتتن عائمتتتة ستتتفيرينيدي Sphyraenidae، ومتتتن أمعتتتاء أستتتماك البياض من عائمة كرانكيدي Carangidae.

5- بيوسيفاليس فتاريكس متانتر، Bucephalus varicus 5610 وقد سجمت من أمعاء أسماك عائمة كرانكيدي Carangidae فقل.

9- ريبيدوكوتايل بينتاكونيوم )أو اكي، pentagonum )5651 Rhipidocotyle العائتتتتتتدة إلتتتتتتأ جتتتتتتنس ريبيتتتتتتدوكوتايل دايستتتتتتين ، 5525 64 Ali B. Al-Zubaidy

(Rhipidocotyle Diesing, 1858) وقد سجل وجودها فتي معتدة أستماك التونتتتتتتة متتتتتتن عائمتتتتتتة ستتتتتتكمبريدي Scombridae وأستتتتتتماك الن ا تتتتتتات أو أسماك الحمرة من عائمة ليوتجانيدي Lutjanidae

1- جمي األنوا أعال تعتد تستجيال جديتدا فتي أستماك البحتر ا حمر، الميا اليمنية.