JKAU: Mar. Sci., Vol. 24, No. 2, pp: 3-14 (2013 A.D. / 1434 A.H.) DOI : 10.4197/Mar. 24-2.1

The First Record of Two Polyopisthocotylean Monogeneans on Gills of the Great Barracuda, Sphyraena barracuda from the Red Sea, Yemeni Coastal Waters

A. B. Al-Zubaidy Department of Marine Biology and Fisheries, Faculty of Marine Science and Environment, Hodeidah University, Yemen e-mail: [email protected]

Abstract. A total of 85 specimens of the great barracuda, Sphyraena barracuda (Edwards, 1771) from the Red Sea, Yemeni coastal waters were examined for infection with the polyopisthocotylean monogeneans during the period from October 2009 till May 2010. The results showed the occurrence of two of these parasites; Vallisiopsis contorta Subhapradha, 1951 and Pentatres sphyraenae Euzet and Razarihelisoa, 1959. The occurrence of these monogeneans represents their first record from the Yemeni of the Red Sea.

Key words: , , Fishes, Red Sea, Yemen.

Introduction Fish have a great importance and significance in the life of mankind. These are most common and widely distributed almost in all parts of the world. Marine fish constitute about 90% of total world fish production (approximately 80 million tons) but the availability of fish supplies can be affected by parasites and diseases, which could ultimately affect nutrition and hence economics of populations (Rohde, 1993 and Hadfield, 2007).

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The total number of described fish helminthes exceeds far more than 30.000 species (Williams and Jones, 1994). The Neodermata or parasitic Platyhelminthes comprise an enormous diversity of species that occur in all seas, rivers and lakes and on all continental land masses. They include trematodes, cestodes and monogeneans (Richard and Justine, 2001). Monogeneans are ectoparasites of fishes exhibiting a relatively high degree of host specificity (Williams and Jones, 1994). Monogeneans included about 720 genera distributed among 53 families (Boeger and Kritsky, 2001). Monogenea comprise two very distinct groups, the and the Polyopisthocotylea, which differ considerably in respect of their morphology, pathogenicity, treatment and host response (Purivirojkul, 2008). There are relatively few studies concerning fish monogeneans of the Red Sea (Paperna, 1972 a, b, c; Paperna et al., 1984; Diamant and Paperna, 1986; Diamant, 1989; Tawfik et al., 2006; Bayoumy et al., 2007; Kritsky et al., 2007 and Al-Zubaidy, 2013). The present Study concerned with the record of two polyopisthocotylans from gills of the great barracuda, Sphyraena barracuda (Edwards, 1771) for the first time in the Red Sea, Yemeni coastal waters.

Material and Methods Investigated fishes used in this study were obtained from a local fish market (Al-Mehwat) at Hodeidah city, Yemen, during the period from October 2009 till May 2010. Specimens were placed in bags with ice and transported to the laboratory of the Department of Marine Biology and Fisheries, Hodeidah University. Scientific names of hosts are adopted from Froese and Pauly(2012). The gills from both sides of fishes were removed one by one by cutting them at their extremities and they were examined immediately in seawater. Monogeneans were removed alive with fine needles and immediately prepared for slides. Live specimens were fixed with AFA (alcohol-formalin-acetic acid) and mounted in glycerol gelatin (Malmberg, 1970). Phase contrast microscopy was used to study the hard parts of the and the copulatory organ of the reproductive system. For descriptions and measurements are calibrated using an optical microscope. The drawings were made using a camera Lucida and

The First Record of Two Polyopisthocotylean Monogeneans on Gill of the … 5 photographs were made with a Samsung digital camera, 10.1 mega pixels. Parasite measurements were given as range as well as the mean in parentheses. Parasitic identifications were done according to Yamaguti (1963, 1968). Parasite identifications were ascertained by Prof. Dr. Jean-Lou Justine, France, and Prof. Dr. Delane C. Kritsky, U.S.A.

Results and Discussion Two species of monogeneans belonging to the subclass Polyopisthocotylea were found on gills of Sphyraena barracuda collected from Red Sea, Yemen coast. These polyopisthocotylean monogeneans are arranged in the following systematic account of WoRMS (2013). Phylum Platyhelminthes Class Monogenea Subclass Polyopisthocotylea Order Family Protomicrocotylidae Subfamily Vallisiinae Vallisiopsis contorta Subhapradha, 1951 Family Chauhaneidae Subfamily Pentatrinae Pentatres sphyraenae Euzet and Razarihelisoa,1959. 1- Vallisiopsis contorta Subhapradha, 1951 (Fig. 1 and 2) Description: Body, 3.0-3.9 (3.6) mm in length, with a maximum width of 1.3-1.9 (1.5) mm, is bent on itself and also twisted, the anterior part lies at a right angle to the posterior part, and the dorsoventral axis of the anterior part is twisted. The entire surface of the body is transversely ringed; the posterior end of the body bears a pair of anchors, which are 0.025 mm long. Oral sucker 0.028-0.034 (0.032) long by 0.025-0.034 (0.030) mm wide. The haptor is asymmetrical. There are eight clamps, four on each side of the haptor. Those on one side lie close together and are nearer the anchors, while those on the opposite side are farther apart and are born on distinct lobes of the body.

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The clamp skeleton is typically discocotylid in pattern and bears a pair of accessory sclerites in connection with the middle piece, which are very similar to the' v-shape'. The width of the clamp is 0.057-0.062 (0.059) mm, hamuli 0.027-0.029 (0.028) mm long, shafts 0.016-0.018 (0.017) mm long; dorsal root 0.010- 0.012 (0.011) mm long, ventral root 0.008-0.010 (0.009) mm long; atrial spines 0.012-0.015 (0.013) mm long. The oesophagus is long and extends below the genital pore.

Fig. 1. Camera lucida drawings of Vallisiopsis contorta from Red Sea fish. A- Entire specimen; B- Clamp skeleton; C- Egg.

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The intestinal crura are branched. The two limbs of the intestine join together posterior to the gonads. The testes are follicular, overlap the anterior half of the ovary and extend beyond it. The ovary is in the form of a double loop extending posterior to the testes. The vitellaria are follicular and coextensive with the intestinal rami. The vitelline reservoir lies adjacent to the ovary. The eggs are spindle shaped and have polar filaments. Host and Locality: Great barracuda, Sphyraena barracuda (family Sphyraenidae) from the Red Sea, Yemeni coastal waters. Length and weight of infected fishes ranged between 20-65 cm and 0.410 -2.100 kg, respectively. Infection Parameters: Mean prevalence of the infection was 16.47%, while the intensity of infection was 1-2 (1.6) worms. Record of Specimens: Twenty-three specimens of this parasite were collected. Parasites were observed frequently on larger fishes (30- 65 cm, n=78) rather than on smaller fishes (20-29 cm, n= 7). The impact of the parasite burden is dependent not on the intensity (number of parasites per fish) but rather on the number of parasites in relation to the size of host. The gill surface of fish increases markedly with body length (Hughes, 1966) and the space available for parasite attachment therefore increases with host size (Buchmann, 1989). Previous Records: This parasite was previously reported in Lactarias lactarias Bloch and Schneider, 1801 (Lactariidae) from Madras coast by Subhapradha (1951) and in Sphyraena commersonii Cuvier, 1829 (synonym of S. barracuda) from Madagascar by Euzet and Razarihelisoa (1959). Habitat: The parasites were found on the second gill, between the two rows of gill filaments and were firmly attached to them with the aid of the clamps. According to Hanek and Fernando (1978), the differences in water current over the gill surface were considered to be important in determining the distribution of parasites on the gills. Most polyopisthocotyleans are not overtly pathogenic. As polyopisthocotyleans are blood feeders, the host does not show any pathological signs or host response compared to other parasites which browse widely on epithelium while feeding as do the mucus and epithelial feeders. These have attachment clamps which do not penetrate

8 A.B. Al-Zubaidy deeply into host tissues like the hamuli and marginal hooklets found in other monogeneans. Thoney (1986) reported that laboratory reared Sebastes melanops Girard, 1856, heavily infested with sebastis, did not show any signs of stress or pathology. Higher intensities of parasites may weaken the host, permitting capture by predatory fish or infection by other disease agents. When a certain number of polyopisthocotyleans occur on an individual host, they can become pathogenic and cause mortalities at the final stage. Documented examples of pathology caused by polyopisthocotyleans include: sagittata which cause serious gill damage to salmonids in Europe and Axine heterocerca which killed sea cage-cultured Siganus sp. in Japan (Roberts, 1978); Heteraxine heterocerca affecting Siganus quinqueradiata, damaging the rockfishes Sebastes melanops (Thoney and Hargis, 1991), S. schlegeli (Kim et al., 2001) and Zeuxapta seriolae killing amberjacks Seriola dumerili (Montero et al., 2004).

Fig. 2. Photographs of Vallisiopsis contorta from Red Sea fish. A-Whole mount; B- Anterior part of the body, eggs seen in the centre; C- Eggs; D- Posterior part of the body.

The First Record of Two Polyopisthocotylean Monogeneans on Gill of the … 9

Remarks: According to Jean-Lou Justine (Personal communication), this species resembles Vallisiopsis contorta Subhapradha, 1951 from S. commersonii from Madagascar, as redescribed by Euzet and Razarihelisoa (1959). S. commersonii is now considered a synonym of Sphyraena barracuda according to Froese and Pauly (2012). The characteristic description of the present specimens is conspecific with the type specimens of V. contorta from Madras coast except some morphometric differences. Among ectoparasitic monogenoideans, fluctuations of a biotic (e.g. salinity, temperature) and biotic (e.g. host size) conditions have been shown to influence morphometric variation observed in some haptoral structures (Mo, 1991; Rohde, 1991; Perera, 1992). This represents its first record and new geographic from the Yemeni waters of the Red Sea. 2- Pentatres sphyraenae Euzet and Razarihelisoa, 1959 (Fig. 3 and 4) Description: Body size 4.3 mm long x 1.3 mm wide. It is elongated with narrow anterior end and broad posterior end. Oral sucker rounded, muscular; Pharynx elongate, oval; Oesophagus 0.6 mm long. It is characterized by an asymmetrical posterior adhesive organ possessing five clamps on one side and three of a different shape on the other side. Testes numerous, ovary elongated in front of the testes. Vaginal pore in the mid-dorsal line. Genital pore transversely elongated.

Fig. 3. Camera Lucida drawing of Pentatres sphyraenae from Red Sea fish.

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Fig. 4. Photographs of Pentatres sphyraenae from Red Sea fish.

Record of Specimens: Two specimens (one damaged) of the parasite were collected. Most monogenean parasites in fishes live for less than one year (Smith et al., 2005). Host and Locality: Sphyraena barracuda (family Sphyraenidae), Red Sea, Yemen Coast, Hodeidah. The length and weight of the only one infected fish was 60 cm and 1.100 kg, respectively. Previous Records: This parasite was firstly recorded from S. commersonii from Madagascar by Euzet and Razarihelisoa (1959). Infection Parameters: Mean prevalence of the parasites was 1.17%, while the intensity was 2.0 worms. Habitat: The parasites were found on the filaments of the fourth gill arch. Remark: P. sphyraenae was orginally described from S. commersonii (which is now considered as a synonym of S. barracuda) from Madagascar. The subfamily Pentatrinae is erected for P. sphyraenae, since its gastrocotylid clamps are modified like those of the subfamily Priceinae (), but these are internally symmetrical and disposed in an asymmetrical fringing-arc around the hind body; the three

The First Record of Two Polyopisthocotylean Monogeneans on Gill of the … 11 larger clamps are pedunculated. The muscular penis and atrium are sub- lateral. The species is herein reported for the first time from the gill of P. sphyraenae from the Red Sea, Yemeni Coastal waters, and for the second time in the world (after a lapse of over 53 years). Acknowledgements Thanks are due to Prof. Dr. Jean-Lou Justine, Evolution Museum National d’Histoire Naturelle, Paris, France and Prof. Dr. Delane C. Kritsky, Idaho State University, U.S.A. for their assistance in parasites identification and for the additional information on the monogeneans. Thanks are also due to Prof. Dr. Furhan T. Mhaisen, Sweden, for reading the manuscript and for his valuable suggestions.

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14 A.B. Al-Zubaidy Sphyraena barracuda

. Sphyraena barracuda (Edwards, 1771) ! "#$ %& ' () ) 3445 ' ( /) * + ,+ -./ 0)$ ' , ",/ .3484 () 6 7 Vallisiopsis contorta Subhapradha, 1951 ")0 *. .Pentatres sphyraenae Euzet and Razarihelisoa, 1959 * */ "#$ ' , . ,