Research Article

The Parasites Monascus sp. (Fellodistomidae) and Helicometrina nimia (Linton, 1910) (Opecoelidae) Digenea of Pampus argenteus and Greasy Grouper Epinephelus tauvina (Forsskål, 1775) (Teleostei: Serranidae) Fishes, Arabian Gulf, New Host and New Geographical Records  

Majid A.A. Bannai
Marine Vertebrate, Marine Science Center, Basra University, Iraq
Author    Correspondence author
International Journal of Marine Science, 2017, Vol. 7, No. 10   doi: 10.5376/ijms.2017.07.0010
Received: 21 Mar., 2017    Accepted: 18 Apr., 2017    Published: 21 Apr., 2017
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Bannai M.A.A., 2017, The parasites Monascus sp. (Fellodistomidae) and Helicometrina nimia (Linton, 1910) (Opecoelidae) digenea of Pampus argenteus and greasy grouper Epinephelus tauvina (Forsskål, 1775) (Teleostei: Serranidae) fishes, Arabian Gulf, new host and geographic records, International Journal of Marine Science, 7(10): 88-95 (doi: 10.5376/ijms.2017.07.0010)


On the new investigation of some Trematode fauna of Arabian Gulf fishes, Monascus sp. a digenea parasite of pampus argenteus and Helicometrina nimia of greasy grouper, Epinephelus tauvina are register. Fish specimens were collected during the year 2016. A description of the studied specimens, besides comments concerning its taxonomic status, the morphological characters and measurements of the present material of Monascus sp. The Monascus sp. parasite are described on the present study compared with some measurements of Nine nominal species have been reported in the genus Monascus up to 1993 and showing that similarity with M. filiformis and differ in the size of parasite. The results indicated that the parasites are considered as having new hosts viz, p. argenteus and as new records in the Iraqi marine fishes. In the present study, a new host and a new host locality are presented for the two species. The taxonomic status of members of Helicometrina has been questionable, the validity of diagnostic features, especially in regard to the number of testes. In the present study, specimens presented a permanent and steady number of testes (n=9) and therefore its use as a diagnostic character and is very similar with Linton (1910). Epinephelus tauvina is considered a new host for Helicometrina nimia, and Northwest Arabian Gulf a new locality for the species.

Trematode Monascus sp.; Helicometrina nimia; Digenea: Opecoelidae; Marine fish; Arabian Gulf


The Digenetic trematode represents the largest group of parasites as they comprise about 18,000 (Crib et al., 2001). Family Fellodistomidae comprises to two subfamilies, Fellodistominae Nicoll 1909 and Haplocladinae Odhner 1911, which are composed of a large number of genera of small flukes. The type genus of the family was described by Stafford in 1904 from the gall bladder of a Canadian wolf-fish, Anarrhichas lupus (Srivastava, 1935).


The fish fauna of the Arabian Gulf is highly enriched and nearly 500 species of bony as well as cartilaginous fish were recorded from different coasts (Krupp and Muller, 1994). M. filiformis is reported for the first time in the gut of Stromateus brasiliensis of the south-western Atlantic Ocean (Luciana et al., 2015). M. filiformis had been reported in Pampus (Stromateidae) from India (Sey et al., 2003), on Cepola rubescens (Cepolidae) from Italy, on Selaroides leptolepis (Carangidae) from Kuwait, on Mugil ophuyseni (Mugilidae) from China (Sey et al., 2003), on Trachurus trachurus (Carangidae) from Denmark, Iberian Peninsula, Norway and Turkey (Køie, 1979; Lozano et al., 2001; MacKenzie et al., 2004; Oguz and Bray, 2006) and, on Trachurus lathami (Carangidae) from Venezuela (Nasir and Go´mez, 1977).


In the Atlantic Ocean, M. filiformis has been found only in five species of fish ,Brazil: Chloroscombrus chrysurus (Carangidae) and Trachurus lathami (Carangidae) (Amato, 1982), Oligoplites saurus (Carangidae) (Travassos et al., 1965; 1967), Peprilus paru (Stromateidae) (Wallet and Khon, 1987), Micropogonias furnieri (Sciaenidae) (Pereira et al., 2000); and from cold temperate waters of Argentina it was reported infesting only Trachurus lathami (Girola et al., 1992).


The Opecoelidae Helicometrina nimia (Linton, 1910) has been reported from marine fishes of the Pacific, California, Chile, and Atlantic to Espiritu and coasts of Americas (Linton, 1910; Manter, 1940; Manter and Van Cleave, 1951; Travassos et al., 1967; Inzunza et al., 1989). Helicometrina nimia (Opecoelidae) is a digenean with wide distribution. More than 50 fish species belonging to 21 families in 6 orders have been registered as hosts of H. nimia along the coasts of the Americas.


Groupers, Epinephelus spp. represent one of the most important resources targeted by coastal fisheries and aquaculture in Arabian Gulf (Smith, 1971).


Epinephelus tauvina is a highly valued and widely distributed in the Arabian Gulf (El-Sayed et al., 2007). Saoud et al. (1988) described H. qatarensis. According to Mittal and Pande (2007), the valid species of Helicometrina are H. nimia; H. parva Manter; H. septorchis Srivastava; H. mirzai Siddiqi and Cable; H. quadrorchis Manter and Pritchard; H. hexorchis Gupta and Sehgal; H. scomberi Gupta and Jahan; H. unicum Gupta and Puri and H. chauhani Mittal and Pande. The authors also presented a key to the species of genus based on the number of testes. Hafeezullah (1971) register twenty eight specimens of the genus of Helicometrina from marine fish are in India with different number of testes.


In addition to that Arabian Gulf revealed that described from different coasts, from Kuwaiti coasts a wide variety of species were described (Al-Yamani and Nahhas, 1981; Nahhas et al., 1998; 2006). El-Naffar et al. (1992), Kardoush (2003) also reported more than 20 species of digenetic trematode from the Emirati coasts. Some scattered studies were also recorded from other coasts, including Saudi Arabia (Bayoumy et al., 2012) and Oman (Machkevskyi et al., 2014) and Iraq (Bannai, 2002; Bannai and Essa, 2015; Bannai et al., 2005a; 2005b).


Where little attention was carried out about fish parasite in general and especially that of Arabian Gulf, Iraqi marine water fishes. Therefore, the present study aims to investigate the species’ parasites infecting.


1 Materials and Methods

Monthly fish samples were collected from Khor Abdullah, north west of the Arabian Gulf, during the years 2016, a total of 20 fish specimens were collected from P. argenteus and a Total of 30 fish specimens were collected from Greasy Grouper E. tauvina. Fishes kept in ice box and brought to the laboratory. Methods of relaxation, fixation, staining and mounting of helminthes are basically those described by Roberts (2001). Each fish was opened and the intestine was separated from the other visceral organs and placed in a Petri-dish containing physiological saline and examined for parasites. The parasites were washed in a 0.6% saline solution and fixed in 70% ethanol. They were stained with alum carmine, dehydrated and then cleaned in xylene and mounted in Canada balsam. Drawings were prepared by camera Lucida. The specimens were deposited in the Department of Marine vertebrate, Marine Science Center, University of Basra, Iraq. Parasites identification was done with the aid of Yamaguti (1971) and Dr.Thomas Gribb Department of Microbiology and Parasitology, University of Queensland, Brisbane 4072, Australia and aid of Dr. David Ian Gibson, Natural History Museum London.


2 Results

Trematode fauna currently occurs in Arabian Gulf fishes, Monascus sp. of pampus argenteus and Helicometrina nimia from Epinephelus tauvina fishes.


1- Class: Digenea

    Order: Bucephalata

    Family: Fellodistomidae

    Genus: Monascus

    Monascus sp. (Figure 1)

    Prevalence: 1

    Mean intensity: 15%

    Host: pampus argenteus

    Site of infection: intestine



Figure 1 Photograph of Monascus sp. ventral view


Description based on one specimen. Body elongates 20 mm×0.57 mm; Tegument smooth. Oral sucker terminal, 0.4 mm with an oval aperture; oval ventral sucker 0.34×0.26. Prepharynx 0.37; pharynx 0.13×0.10; intestine extend to posterior end of body; anus absent. Testes two, anterior testis 0.47×0.39 mm; posterior testis 0.52×0.39; cirrus sac anteriorly, Ovary, 0.26×0.26. Vitelline follicles lateral, extending from near posterior level of acetabulum to mid-level between testes. Eggs 0.026×0.06. The parasite are described on the present study compared with some measurements of Nine nominal species have been reported in the genus Monascus up to 1993 (Table 1) and showing that similarity with M. filiformis that described by Koie (1979) and differ in the size of parasite. The results indicated that the parasites are considered as having new hosts viz, p. argenteus and as new records in the Iraqi marine fishes.



Table 1 Some measurement of some Monascus spp according Koiem 1079 and present study


2- Class: Trematoda

    Order: Plagiorchiida

    Family: Opecoelidae

    Genus: Helicometrina

    Helicometrina nimia (Linton, 1910) (Figure 2)

    Prevalence: 8.25

    Mean intensity: 22.6%

    Host: Epinephelus tauvina Forsskål, 1775

    Site of infection: intestine



Figure 2 1 and 2: Helicometrina nimia (Linton, 1910) photograph and camera Lucida drawing scale bare mm 0.5mm; 4: Epinephelus tauvina (Forsskål, 1775) host 


Description: the average measurements obtained from 6 specimens are: 4.0-8.1 (5.6 mm) in total length by 1.12-1.71 (1.4 mm) maximum width; a short esophagus and a muscular pharynx that was longer than wide (0.15 mm by 0.12 mm); a post-bifurcal genital pore with a long cirrus sac running from the level of the acetabulum close to the genital pore; acetabulum 0.41 mm in diameter 0.37–0.44 mm; a pre-testicular ovary (0.55 width by 0.30 length), typically with 4 primary lobes and a variable number of secondary lobes; a coiled uterus with 5 to 6 loops between the ovary and the posterior end of the acetabulum; 9 rounded testes (0.35 mm wide); irregularly shaped vitelline follicles extending from the intestinal bifurcation to the end of the body running continuously along both sides of the body.


3 Discussion

Monascus sp. especially known from fishes caught in subtropical and tropical seas, with most records from the Mediterranean. Most records are from fishes of the family Carangidae. The Original name of the genus Monascus are Haplocladus filiformis (Rudolphi, 1819), and synonym are Haplocladus minor (Odhner, 1911); synonym Haplocladus orientalis (Srivastava, 1941); synonym according to Bray and Gibson (1980), Haplocladus typicus (Odhner, 1911), Monascus elongatus (Karyakarte and Yadav, 1976), Monascus monenteron (Looss, 1907), Monascus ovilobatus (Kumari, 1975), Monascus typicus (Odhner, 1911; Looss, 1912); synonym Monascus netoi (Travassos et al., 1967); synonym Monascus orientalis (Srivastava, 1941; Yamaguti, 1958); in addition to that Monascus trilobatus (Bilqees, 1973).


According to Koie (1979), Nine species have been reported of the genus Monascus that are: M. filiformis (Rudolphi, 1819) from Cepola rubescens Linnaeus in Italia; M. typicus (Odhner, 1911) from Caranx trachurus Linnaeus at Palermo and Trieste; M. minor (Odhner, 1911) from Pleuronectes limanda (Linnaeus) in the Sweden; M. monenteron (Looss, 1907) from an unknown host; M. orientalis (Srivastava, 1941) from Synaptura orientalis from Bay of Bengal; M. netoi from Oligoplites saurus from Brazil; M. chauhani Vasntha (Kumari, 1975) from 2 unnamed species of Pampus from India; M. americanus (Amato, 1982) from Trachurus lathami from Brazil; and M. mediolongiusculus (Ding, 1993) from Mugil ophuyseni Bleeker from Guangdong Province, China. In addition to that the other species, in the Arabian Sea also belongs to this group. Monascus filiformis, a parasite described by Rudolphi in 1819 as Distoma filiformis, was transferred to the genus Monascus by Looss (1907) without a generic diagnosis.


Hafeezullah (1984) referred to a number of several taxonomy advantage, one of them the presence of one or two caeca, ovary round or trilobed. Also Hafeezullah (1984) referred to the work of Koie (1979), who worked out the life cycle of M. filiformis. Amato (1982) considered a trilobed ovary an important species characteristic that led him to synonymize M. typicus of Lamothe-Argumedo (1969) and M.filiformis of Nasir and Gomez (1977).


The Monascus sp. from present study are compared with total preparations of Monascus spp. of Koie (1979) study, and see deferent if the body length and results indicated that the parasites are considered as having new hosts in p. argenteus and as new records in the Iraqi marine fishes.


Helicometrina nimia (Linton, 1910) has been reported from marine fishes along the Pacific, California, to Valdivia, southern Chile, and Atlantic to Espiritu Santo, Brazil, coasts of the Americas (Linton, 1910; Manter, 1940; Manter and Van Cleave, 1951; Travassos et al., 1967; Inzunza et al., 1989). Helicometrina nimia is a digenean with wide distribution. As well as, More than 50 fish species of fishes have been registered as hosts of H. nimia along the coasts of the Americas. A few additional reports of H. nimia come from the Indo Pacific. However, as stated by Cribb et al. (2002), these records should be reconsidered. Helicometrina nimia is a wide distribution (Oliva and Munoz, 1985). Fish families most commonly used as hosts for H. nimia are Serranidae, Pomodasydae, Scorpaenidae and Clinidae (Inzunza et al., 1989).


In total, 15 species have been described in the genus Helicometrina of those, 11 were characterized by the presence of 9 testes (Jupta and Jahan, 1975; Perez-Ponce de Leon, 1992). Deelman (1960) considered Helicometrina orientalis (Srivastava, 1936) and Helicometrina elongata (Noble and Park, 1937) synonymous with H. nimia. Oliva and Munoz (1985) stated that Helicometrina trachinoti (Siddiqi and Cable, 1960) must be considered synonymous with H. nimia.


According to Siddiqi and Cable (1960), Helicometrina mirzai differs from H. nimia in body size (less than 2.0 mmin H. mirzai; more than 2.0 mm in H. nimia) and from H. trachinoti (¼H.nimia) by interrupted vitellaria at the level of the ventral sucker. H. mirzai mustbe considered as a new synonym of H. nimia. Cribb et al. (2002) stated that some additional reports from the Indo Pacific should be reconsidered, because they are indistinguishable from H. nimia as noted early by Hafeezullah (1971).


Accordingly, only H. nimia can be reliably considered a valid species in the genus. Helicometrina labrisomi is easy to distinguish from the type species by a combination of characters that includes an oval, entire, and smooth ovary, never lobed in H. labrisomi, instead of the lobed ovary that is characteristic of H. nimia, a uterus with 2 to 3 loops in the new species and 5 to 6 in H. nimia, and a pharynx that is wider than it is long in the new species instead of longer than wide in H. nimia, as well the position of the genital pore, which is pre-bifurcal or at the intestinal bifurcation in H. labrisomi but never post-bifurcal.


Cribb et al. (2002) suggested that Opecoelids (including Helicometrina) are common parasites of Epinephelinae (Serranidae). A review of hosts of H. nimia from the coast of the Americasalso suggested that serranids, as well as the related lutjanids, arecommon hosts for this parasite; however, some fish host records,such as those from Bothidae, Blennidae, Gobiesocidae, and Labrisomidae (Inzunza et al., 1989; Perez-Ponce de Leon, 1992; Munoz and Randhawa, 2011; Munoz and Zamora, 2011; Munoz and Castro, 2012), must be carefully evaluated, because,unfortunately, none of the cited references includes a descriptionand/or figures, and voucher specimens (if available) must be reexamined.


Our results show that H. nimia specimens recorded from the greasy grouper E. tauvina from Northwest Arabian Gulf are very similar with Linton (1910) and in the present study consider the register as a new host and a new host locality are presented for the species.



I am grateful to Dr. Thomas Gribb Department of Microbiology and Parasitology, The University of Queensland, Brisbane 4072, Australia for identification of species of parasite. Also I am grateful to Dr. David Ian Gibson, Natural History Museum, London, Jacopo Culurgioni Agenzia della Regione Sardegna per la ricerca scientifica, and Salvatore Mele, Università degli Studi di Sassari for their support conservation in research gate.



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. Digenea: Opecoelidae
. Marine fish
. Arabian Gulf
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