A Second Collection of Monogeneans and Trematodes (Phylum Platyhelminthes) Parasitic on Some Fishes from Tigris River at Baghdad Province, Iraq

study, data, anchored the field study, data, ABSTRACT Aims: This works aims to report on the monogeneans and trematodes that infect some species of fishes from Tigris infected with 13 species of monogeneans and four species of trematodes. The monogeneans included one species each of Paradiplozoon and Thaparocleidus , two species of Gyrodactylus and nine species of Dactylogyrus , while the trematodes included one species each of Ascocotyle and Clinostomum and two species of Diplostomum . Among all these parasites, A. coleostoma infected the highest number of hosts (five host species), while 13 parasite species infected only one host each. Among these fishes, Carassius carassius was infected with the highest number of parasite species (nine species), followed by Carasobarbus luteus (eight species) and Chondrostoma regium (four species) while no infection was detected from three fish species ( Alburnus caeruleus , Cyprinus carpio and Leuciscus vorax ). In addition, a total of seven new host records in Iraq were reported for seven species of these parasites. Conclusion: Host specificity is clear in monogeneans as 12 out of the 11 monogenean species infected one fish species each. All the trematodes were as metacercariae which later infect piscivorous aquatic birds.

infected with 13 species of monogeneans and four species of trematodes. The monogeneans included one species each of Paradiplozoon and Thaparocleidus, two species of Gyrodactylus and nine species of Dactylogyrus, while the trematodes included one species each of Ascocotyle and Clinostomum and two species of Diplostomum. Among all these parasites, A. coleostoma infected the highest number of hosts (five host species), while 13 parasite species infected only one host each. Among these fishes, Carassius carassius was infected with the highest number of parasite species (nine species), followed by Carasobarbus luteus (eight species) and Chondrostoma regium (four species) while no infection was detected from three fish species (Alburnus caeruleus, Cyprinus carpio and Leuciscus vorax). In addition, a total of seven new host records in Iraq were reported for seven species of these parasites. Conclusion: Host specificity is clear in monogeneans as 12 out of the 11 monogenean species infected one fish species each. All the trematodes were as metacercariae which later infect piscivorous aquatic birds.

INTRODUCTION
The study of fish parasites is necessary to increase the productivity of pond farms, to improve the stocks of valuable commercial fisheries in the natural waters and to the possibility of fish acclimatization in new sites or localities [1].
The class Monogenea, used to be known as monogenetic trematodes, includes skin and gill flat worms with direct life cycles [2]. These are important fish pathogens, especially for carp fingerlings under extensive fish culture practice. Their direct life cycles and fish crowding are good conditions for their easy spread among fishes [3].
According to their attachment organs, monogeneans are provided either with hooks and hooklets and hence they are known as monopisthocotyleans or with clamps and hence they are known as polyopisthocotyleans [4]. Monogeneans cause irritation and excessive mucus production and their infection creates an open window for bacterial invasion [5].
With very few exceptions, trematodes include endoparasitic flat worms with non-segmented body, closed digestive system, oral and ventral suckers and indirect life cycles. As adults, trematodes live inside various vertebrates and spend their larval stages in intermediate hosts, mainly snails but also in some fishes [6]. Adult trematodes of fishes usually live in the digestive systems of their hosts but few live in the circulatory system [7]. Some trematodes live as larvae (metacercariae) in fish eyes [8] or gills and skin [2]. They are responsible for important fish diseases such as worm cataract, yellow grub and black spot disease [2,9]. Some trematodes can infect humans that eat metacercaria-infected fishes if such fishes are inadequately cooked [10].
The first published work on fish parasites in Iraq was done by Herzog [11]. After that, extensive surveys were done which resulted in the record of 162 valid monogenean and 46 trematode species from freshwater fishes of Iraq [12]. The present work, which is a continuation of a previous one [13], aimed to investigate monogenean and trematode infections among eight species of fishes from three different sampling sites along Tigris River at Baghdad province.

MATERIALS AND METHODS
Fishes were sampled from three sites in Tigris River at Baghdad province: Al-Taji in the north of Baghdad city, Al-Shawaka in the center of Baghdad city and Al-Zaafaraniya in the south of Baghdad city, during the period from January to December 2011. These fishes were captured by gill and cast nets of different mesh sizes. Fishes were brought to the laboratory with containers filled with ice. These fishes (Table 1) were identified according to Coad [14] and their scientific names followed Froese and Pauly [15].
Total length and weight of each fish specimen were recorded. Smears from the skin, gills, buccal cavity and eye lenses were examined under a compound microscope. Parasite identification was done according to some major taxonomical books [4,16,17,18]. The prevalence of infection was calculated according to Margolis et al. [19]. The index-catalogue of parasites and disease agents of fishes of Iraq [12] was followed to indicate number of previous host records for each parasite in order to minimize list of references for each parasite species.

RESULTS AND DISCUSSION
A total of 98 fish specimens were captured from the three stations of collection ( Table 1). The result of fish inspection showed that five species of these fishes were infected with 13 species of the class Monogenea and four species of the class Trematoda ( Table 2).  Table (2). The following is brief account on the occurrence of these parasites.

Class Monogenea
A total of 13 monogenean species were reported from fishes of the present investigation. Nine of these monogeneans belong to the genus Dactylogyrus, two to the genus Gyrodactylus and one species each to the genera Paradipolzoon and Thaparocleidus. These monogeneans are alphabetically arranged in the following account.

Dactylogyrus achmerowi Gusev, 1955
This parasite was recorded from gills of C. luteus. The first record of this parasite in Iraq was from gills of C. carpio from Al-Wahda Fish Hatchery at Suwairah and Babylon (now Al-Furat) Fish Farm [20]. After that, it was reported from 10 other hosts in different inland waters and fish farms in Iraq [12] which included C. luteus.

Dactylogyrus anchoratus (Dujardin, 1845)
This parasite was recorded from gills of C. carassius and C. regium. The first report of this parasite in Iraq was from C. carpio from Tigris River at Al-Zaafaraniya, south of Baghdad [21]. Later on, it was reported from five other fish species which included C. carassius but not C. regium [12] which now represents the seventh host for D. anchoratus in Iraq.

Dactylogyrus arcuatus Yamaguti, 1942
This parasite was recorded from gills of C. carassius. Salih et al. [22] recorded this parasite for the first time in Iraq from skin, gills and buccal cavity of C. carpio from Al-Suwaira and Al-Latifiya fish farms. Later on, it was reported from five other hosts in Iraq which did not include C. carassius [12] and hence C. carassius represents a new host (the seventh) for D. arcuatus in Iraq.

Dactylogyrus dulkeiti Bychowsky, 1936
This parasite was recorded from gills of C. carassius. The first report of this parasite in Iraq was from gills of C. carpio from Al-Zaafaraniya Fish Farm, south Baghdad [23]. Later on, it was reported from four other fish species which included C. carassius [12].

Dactylogyrus formosus Kulwiec, 1927
This species was found from the gills of C. carassius. Asmar et al. [24] recorded it for the first time in Iraq on gills of Carassius auratus from a fish farm in south of Baghdad. Later on, it was recorded from another host which did not include C. carassius [12] and hence C. carassius represents a new host (the third) for D. formosus in Iraq.

Dactylogyrus minutus Kulwiec, 1927
This parasite was found on the gills of C. carassius. D. minutus was recorded for the first time in Iraq on the gills of C. carpio from Tigris River at Al-Zaafaraniya, south of Baghdad as well as from Al-Qadisia Dam Lake, west of Baghdad [21]. After that, it was reported from gills of 11 other fish hosts which included C. carassius [12].

Dactylogyrus skrjabini Achmerow, 1958
This parasite was reported from gills of C. luteus. Its first report in Iraq was from gills and buccal cavity of Hypophthalmichthys molitrix from Al-Suwaira and Al-Latifiya fish farms [22]. Later on, it was reported from five other hosts which included C. luteus [12].

Dactylogyrus varicorhini Bychowsky, 1957
This parasite was recorded from gills of C. luteus. The first report of this parasite in Iraq was from gills of both B. luteus (= C. luteus) and Varicorhinus trutta (= Capoeta trutta) from Tigris River at Baiji town of Salah Al-Deen province, Iraq [25]. Later on, it was reported from only one other host [12].

Dactylogyrus vastator Nybelin, 1924
This parasite was recorded from gills of C. luteus. Its first report from Iraq was from gills of Cyprinion macrostomum from Tigris River at Baghdad city and Al-Rashidiah town [26]. D. vastator is the commonest fish monogenean in Iraq as it has so far 33 fish hosts which included C. luteus [12].

Gyrodactylus elegans Nordmann, 1832
This parasite was recorded from gills of C. carassius. The first report on this parasite in Iraq was from gill arches of both C. carpio and Liza abu from Al-Zaafaraniya Fish Farm [27]. Later on, it was reported from 21 other fish hosts in north and mid Iraq which included C. carassius [12]. G. elegans is the commonest gyrodactylid species in fishes of Iraq [28].

Gyrodactylus medius Kathariner, 1895
This parasite was recorded from gills of C. carassius. The first report of this parasite in Iraq was from skin and gills of C. carpio from Babylon (now Al-Furat) Fish Farm near Hilla city [29]. Later on, it was reported from another host which was not C. carassius [12] and hence C. carassius represents a new host (the third) for this parasite in Iraq.

Paradiplozoon pavlovskii Bychowsky et Nagibina, 1959
This monogenean was found in the gills of Liza abu. It was reported for the first time in Iraq as Diplozoon pavlovskii from gills of Aspius vorax (= L. vorax) from Mehaijeran creek, Basrah [30]. Later on, it was recorded from nine other fish hosts from different locations in north, mid and south Iraq which did not include L. abu [12] and hence L. abu represents a new host for this parasite in Iraq.

Thaparocleidus vistulensis (Siwak, 1932)
This monogenean was found in the gills of Silurus triostegus. Its first report from Iraq, as Ancylodiscoides vistulensis, was from gills of S. triostegus from Tigris River at Baiji town of Salah Al-Dien province [25]. According to Lim et al. [31], A. vistulensis is a synonym of T. vistulensis. Later on, this parasite (as A. vistulensis) was reported from seven other hosts from north, mid and south Iraq [12].

Class Trematoda
The trematodes of the present study included one species each of genera Ascocotyle and Clinostomum and two species of Diplostomum (Table 2). These are alphabetically arranged in the following account.

Ascocotyle coleostoma (Looss, 1896)
Metacercariae of this trematode were recorded from gills and skin of C. luteus, C. carassius, C. regium, L. abu and S. triostegus. This metacercaria was reported for the first time in Iraq from gills of both Heteropneustes fossilis and L. abu from Diyala River, south of Baghdad [32]. This is the commonest trematode infecting freshwater fishes of Iraq as it has so far 34 host species [12] which included the five abovenamed hosts of the present study. Adults of A. coleostoma infect some piscivorous birds such as the grey heron Ardea cinerea in Babylon (now Al-Furat) Fish Farm, mid Iraq [33].

Clinostomum complanatum (Rud., 1814)
Metacercariae of this parasite were recorded from gills of C. luteus. This metacercaria was reported for the first time in Iraq from gills of C. luteus from Mehaijeran creek, Basrah [30]. Later on, it was reported from 21 different fish hosts [12]. Adults of this worm live in the mouth and pharynx of some fish-eating birds [9].

Diplostomum commutatum (Diesing, 1850)
Metacercariae of this parasite were recorded from eye lenses of C. luteus and C. regium. The first report of D. commutatum in Iraq was from eye lenses of A. vorax (= L. vorax) from Tigris River at Baghdad [34]. Later on, it was reported from three other hosts which included C. luteus but not C. regium [12] and hence C. regium now represents a new host (the fifth) for D. commutatum in Iraq.

Diplostomum spathaceum (Rud., 1819)
Metacercariae of this trematode were recorded from eye lenses of C. luteus, C. regium and C. carassius. This parasite was reported for the first time in Iraq from eye lenses of B. luteus (= C. luteus), C. macrostomum and C. carpio from  Dokan Dam Lake [35]. Later on, it was reported from 29 other hosts which did not include C. carassius [12]. So, C. carassius now represents a new host for D. spathaceum in Iraq. The adult worms live in the intestine of fish-eating birds such as some gulls like L. canus and L. ichthyaetus from Shatt Al-Arab River [36].

CONCLUSION
To conclude on the monogenean and trematode infections of fishes of the present study, A. coleostoma was the prevalent parasite among these fishes as it was recorded from five fish hosts, followed by D. spathaceum which was recorded from three fish species. On the other hand, all the monogeneans were detected from one host each, except D. anchoratus which was recorded from two host species.
In connection with fish hosts, C. carassius was infected with the highest number of parasite species (nine species), followed by C. luteus (eight species), C. regium (four species), L. abu and S. triostegus (two parasite species each) while no infection was reported from A. caeruleus, C. carpio and L. vorax. The absence of infection from these fish species might be attributed to the few samples of such fishes in comparison with those of other fish species (Table 1). In addition, seven new host records in Iraq were reported for seven species of these parasites.
Differences in the infection among fishes from the three sampling areas indicated that fishes of Al-Shawaka were infected with 15 species, those of Al-Taji with 11 species while those of Al-Zaafaraniya were infected with 10 species. These numbers are, to some extent, in accordance with number of fishes sampled ( Table 1).
All the four recorded trematodes of the present study were reported as metacercariae which develop to adults when the infected fishes are predated by piscivorous aquatic birds.