Checklists of nematodes of freshwater and marine fishes of Basrah Province , Iraq

Reviewing the literature on all the nematodes parasitizing 45 species of freshwater and marine fishes of Basrah province (eight elasmobranchs and 37 teleosts) indicated the presence of 48 nematode taxa. Thirty-five of such nematodes were recorded from marine localities against eight taxa from freshwater localities and two taxa from both marine and freshwater localities. These nematodes belong to two classes, three orders and eight families. All such nematodes belong to the class Secernentea except two taxa which belong to the class Adenophorea. Orders Ascaridida and Spirurida are represented with 22 and 24 taxa, respectively, while order Enoplida has only two taxa. The total number of nematode species recorded for each fish host species fluctuated from a minimum of one nematode species in 17 fish hosts to a maximum of eight nematode taxa in Cynoglossus arel only. Number of fish hosts reported for these nematodes fluctuated from one host in case of 31 taxa to a maximum of 20 hosts in case of Contracaecum sp. 1 larva.


Introduction
The nematodes show a very wide range of ecological adaptations.Most of them live in waters (fresh, brackish and sea waters) and in the soil, while others are semiparasitic or parasitic species attacking both animals and plants.Out of about 16,000 described species of nematodes, nearly 40% are animal parasites and some 8% of the known parasitic nematodes occur in invertebrates (Anderson, 1988).
Nematodes (Nematoda) represent the most frequent and the most important parasites of fishes in freshwater, brackishwater or marine environments throughout the world.They attack most body organs, parasitizing them as adults and/or as larvae.Some nematode species are known as the agents of serious fish diseases causing considerable losses in fish cultures and in some regions and some of them cause important public health problems such as anisakiosis, gnathostomosis or paracapillariosis (Moravec, 2007a).The significance of recognizing these parasites increases with development of aquaculture in many countries and with transcontinental transfers of fishes.A prerequisite for developing effective control measures in fish culture is the exact identification of these parasites as well as the knowledge of their frequently complicated host-parasite-environment relationships (Moravec, 1994).
The province of Basrah is the only province in Iraq which has an overlooking on the Arab Gulf.In this province, different varieties of aquatic environments are met.These included the shallow marshy area in the north, Shatt Al-Arab River, its tributaries and estuary, Shatt Al-Basrah canal as well as the marine habitats of the northwest part of the Arab Gulf (Mhaisen et al., 2013a).Information concerning nematodes of fishes of Basrah province are scattered in different local scientific references.Some of them are really out dated.Some nematodes as well as some fishes have been misidentified, misspelled or quoted with wrong authorities.For these reasons, it was decided to review these data in accordance with up-to-date nematode classification using major taxonomic accounts and also to revise fish names and provide an updated host-nematodes checklist in addition to the nematodes list.This review is a continuation of series of literature reviews on major groups of parasites of fishes of Basrah province (Mhaisen et al., 1993;2013 a, b, c;2014).Finally, it was also planned to compare the richness of infected fishes of this province with nematodes with those of the whole country of Iraq based on data extracted from the index-catalogue of parasites and disease agents of fishes of Iraq (Mhaisen, 2014).

Sources and Methods
A total of 42 references (research papers, M. Sc. and Ph.D. theses and one conference abstract) dealing with nematodes of fishes of Basrah province were used to prepare the present review.Data from such references were gathered to provide nematodes list and host-nematodes list.The systematic account of different classes and orders of these nematodes is based on some textbooks and related revisions (Moravec, 2006;Anderson et al., 2009;Gibbons, 2010).For fishes, the scientific names were reported as they appeared in their original references but they were then checked with a recent account on freshwater fishes of Iraq (Coad, 2010).However, the valid names used here were based on Iwatsuki (2013) and with minor modifications, on relevant electronic sites (Eschmeyer, 2014;Froese and Pauly, 2014).
The index-catalogue of parasites and disease agents of fishes of Iraq (Mhaisen, 2014) was used to show number of nematodes reported for each infected fish species in Basrah in comparison with that of the whole country of Iraq as well as the richness of fishes of Basrah with nematodes in comparison with such richness in fishes of the whole Iraq.

Surveys Achieved on Fish Nematodes in Basrah:
Digging for literature showed the presence of 42 references on nematodes of fishes of Basrah.From these references, five major categories of fish habitats can be grouped.These are: 1-The marshy area (Al-Hammar marsh and Al-Mdaina marshes) north of Basrah.2-Shatt Al-Arab River and its creeks and canals.3-Brackish waters of Shatt Al-Arab estuary near Al-Fao town, south of Basrah.4-Fish farms in Basrah province.5-Marine waters of the northwest of the Arab Gulf.
Only one report is known on fish nematodes from the brackish waters of Shatt Al-Arab estuary near Al-Fao town (Ali, 2001).
Only one report on nematodes from fish farms of Basrah province (Jassim, 2007) was done on fishes of Basrah University Experimental Fish Culture Station.

Nematodes Recorded from Fishes of Basrah:
The literature review indicated the existing of 48 nematode taxa belonging to two classes, three orders, eight superfamilies and eight families as indicated in Table (1).These nematodes are alphabetically presented under their orders, families and genera.Notes on misspelling in names of some nematodes and their hosts, authorities and synonyms are corrected in accordance with information from some systematic books (Moravec, 2006;Anderson et al., 2009;Gibbons, 2010) as well as some correspondence with some experts.Names of fish hosts are quoted as they appeared in the reviewed literature but the valid names have been updated according to Eschmeyer (2014) and Froese and Pauly (2014).The full authority of each valid fish host is shown in Table (2).

Class Adenophorea:
This class is represented in fishes of Basrah with one order, the Enoplida.

Order Enoplida:
This order is represented in fishes of Basrah with one superfamily, the Trichinelloidea.
Anisakis sp.larva was reported from the body cavity of Ablennes hians from Shatt Al-Arab estuary near Al-Fao town (Ali, 2001).The first Anisakis sp.larva was reported from the freshwater fish Cyprinion macrostomum from Dokan Lake (Abdullah, 1990).So far, five hosts are reported for Anisakis sp. in Iraq (Mhaisen, 2014).The final hosts of the members of Anisakis are marine mammals except sirenians (Anderson et al., 2009).Larvae of this parasite have serious economical and medical importance as raw fishes infected with Anisakis or Pseudoterranova are rejected through the industrial processing of the products.Anisakis larvae in human cause intestinal inflammation "anisakiasis" which shows something like the intestine cancer symptoms (Möller, 1989;Berland, 1996).
Unidentified larval specimen of the family Anisakidae was reported from the intestine of Carangoides malabricus from Iraqi marine waters (Al-Ataby, 2012), erroneously as Skrjabillanus sp. of the family Skrjabinallidae, order Dracunculoidea.One of us (A.H.A.) examined the single larva of this specimen.It was possible to see a muscular esophagus, ventriculus (glandular portion), appendage and a conical tail with sharp tip.No buccal capsule is present and hence it was erroneously identified as Skrjabillanus.Skrjabillanus species have a simple esophagus and a long esophagus gland (Anderson et al., 2009).They infect the gas bladder, urinary bladder, kidneys, subsquamal part of scales and humour of eyes of freshwater fishes in Palearectic region (Moravec, 2006;Anderson et al., 2009;Gibbons, 2010).Skrjabillanus has four nominal species infecting tissues of freshwater fishes mainly cyprinids (Moravec, 2006).
Third larval stages of Contracaecum spp.were recorded from body cavity, internal organs and mesenteries of 20 fish species in Basrah.In Iraq, such larvae were recorded for the first time in Iraq from ten fish species from different inland waters of Iraq, excluding Basrah (Herzog, 1969).So far a total of 40 fish hosts are known for Contracaecum spp.larvae in Iraq (Mhaisen, 2014).Based on the differences in lengths of caecum to appendage, caecum to esophagus and appendage to esophagus (Moravec, 1994), two types of Contracaecum species are found in fishes of Basrah.These are Contracaecum sp. 1 which is found in all fishes of Basrah infected with Contracaecum sp.larvae, except Heteropneustes fossilis by Ali (2001) and Contracaecum sp. 2 in H. fossilis only (Ali, 2001).Contracaecum sp. 1, which is conspecific with that of Shamsuddin et al. (1971), has a long caecum while Contracaecum sp. 2 has very small caecum.
Contracaecum sp. 2 larvae recorded from Basrah included only those from the body cavity and mesentries of H. fossilis from Shatt Al-Arab River near Nahr Khooz village (Ali, 2001).
Al-Daraji (1995) reported females of Contracaecum sp. from J. (J.) belangerii from Khor Al-Zubair estuary and Bannai (2002) recorded such females from three species of marine fishes (A.hians, Saurida undosquamis and Sillago sihama) from Khor Abdullah.It is well known that adult Contracaecum species are parasites of birds and mammals, so they cannot mature in fishes.Therefore, Ali (2008) and Al-Salim and Ali (2010) transferred the above female Contracaecum records of both Al-Daraji (1995) and Bannai (2002) to the genus Hysterothylacium Ward et Magath, 1917 and as only females were available, it is impossible to identify them to the species level.
Some adult Contracaecum species were recorded from some piscivorous birds in Basrah.C. microcephalum was reported from the purple heron Ardea purpurea (Al-Hadithi and Habish, 1977;Habish, 1977;Awad et al., 1994), from the pygmy cormorant Phalocrocorax pygmeus and the little egret Egretta grazetta from Basrah marshes (Awad et al., 1994) and from E. grazetta, the bittern Ardeola ralloides and the little bittern Ixobrychus Ali (2008) described unidentified adult and fourth larval stages of species of Mawsonascaris from the intestine of Himantura gerrardi from Khor Al-Ummaia.Then, the same parasite was described as a new species which is Mawsonascaris parva by Ali et al. (2012) from the intestine of Himantura randalli as the type host was already described as a new species in the same year of parasite description from the Arab Gulf by Last et al. (2012).The genus Mawsonascaris includes six nominal species which infect the digestive tract of elasmobranchs (Ali et al., 2012;Li et al., 2012).
Two unidentified larval species of Terranova types BA and BB were recorded from three carcharhinid sharks from Khor Al-Ummaia.Terranova sp.type BA larvae were reported from the stomach and intestine of Carcharhinus dussumieri (Ali, 2008;Ali and Al-Salim, 2013), gills, liver, stomach and intestine of C. sorrah (Ali, 2008;Ali and Al-Salim, 2013) and from stomach and intestine of R. acutus (Ali, 2008;Ali and Al-Salim, 2013).According to Ali (2013), C. sorrah was reported as C. macloti by Ali (2008).Terranova sp.type BB larvae were reported from the stomach of C. dussumieri (Ali, 2008;Ali and Al-Salim, 2013), intestine of C. sorrah (Ali, 2008;Ali and Al-Salim, 2013) and from stomach of R. acutus (Ali, 2008;Ali and Al-Salim, 2013).All specimens of Terranova spp.from Basrah belonging to the third larval stages and a single specimen to early fourth larval stage inside the cuticle of the previous stage (larva with lips but lacks tooth) of Terranova sp.type BB were reported from carcharhinid sharks due either to newly infection which might took place with these parasites or to unsuitable final hosts.

Superfamily Seuratoidea:
This superfamily is represented in fishes of Basrah with one family, the Cucullanidae.

Family Cucullanidae:
This family is represented in fishes of Basrah with three species of the genus Cucullanus in addition to some specimens of unidentified species of this genus.
Females of Cucullanus sp. were recorded only from the intestine of L.

Order Spirurida:
This order comprises approximately half number of all nematode taxa so far recorded from fishes of Basrah.It is represented in fishes of Basrah with five superfamilies: Camallanoidea, Dracunculoidea, Gnathostomatoidea, Thelazioidea and Spiruroidea.

Superfamily Camallanoidea:
This superfamily is represented in fishes of Basrah with one family, the Camallanidae.

Family Camallanidae:
This family is represented in fishes of Basrah with unidentified species belonging to the genus Camallanus.
Camallanus ancylodirus Ward & Magath, 1916 was recorded only from the intestine of C. carpio in Al-Mdaina marshes (Jori, 2005).Personal communication between one of us (A.H.A.) and Dr. František Moravec concerning C. ancylodirus reported by Jori (2005) revealed that this species is not C. ancylodirus.So, it is designated as Cucullanus sp. 1 in the present checklist.
Camallanus kirandensis Baylis, 1928 was reported only from the intestine of S. triostegus in Al-Hammar marsh (Jori, 2006).Again, the personal communication between with Dr. František Moravec concerning C. kirandensis reported by Jori (2006) revealed that it is not C. kirandensis.So, it is designated as Cucullanus sp. 2 in the present checklist.
Specimens of the fourth larval stage of Camallanus sp. were recorded only from the mesenteries of C. arel from Khor Al-Ummiah (Ali, 2008;Al-Salim and Ali, 2011).

Superfamily Dracunculoidea:
This superfamily is represented in fishes of Basrah with one family, the Philometridae.

Family Philometridae:
This family is represented in fishes of Basrah with seven species of the genus Philometra and two species of the genus Philometroides in addition to four unidentified species of the genus Philometra.All the 13 taxa recorded in this family, except one species (Philometroides cyprini), were reported from marine waters.
Philometra tylosuri Moravec & Ali, 2005 was described only from the musculature and subcutaneous tissues of the hound needlefish T. crocodilus from Al-Fao coast (Moravec and Ali, 2005).
Four unidentified species of Philometra were also reported from the ovaries of S. leiura and T. crocodilus from Shatt Al-Arab estuary at Al-Fao town (Ali, 2001) and from the body cavity of both Sphyreana jello and N. thalassina from Khor Al-Ummaia (Ali, 2008).Due to the rather high degree of host specificity in philometrids (Moravec, 2006) and their speciescharacteristic tissue sites (Moravec and Ali, 2005;Moravec, 2006), it can be assumed that the above-named four unidentified Philometra spp.belong to different species and account separately in the present study as Philometra spp.1-4.The genus Philometra includes parasites of body cavity and tissues of marine, brackish and freshwater fishes.A total of 105 nominal species of Philometra are encountered up to the end of 2013 (Personal communication with Dr. F. Moravec).
Philometroides acanthopagri Moravec, Jassim & Al-Salim, 2012 was described only from the musculature near the pectoral fin and nasal cavity of Acanthopagrus latus from the coastal marine waters of the Arab Gulf (Moravec et al., 2012;Jassim, 2013).According to the personal communication between one of us (A.H.A.) and Prof. Dr. Y. Iwatsuki on 8 th Dec. 2013, A. latus is not distributed in the Arab Gulf and hence A. latus, reported here, is actually representing A. arabicus.This fact comes in agreement with Iwatsuki (2013), Adday (2013), Eschmeyer (2014) and Froese and Pauly (2014).

Superfamily Gnathostomatoidea:
This superfamily is represented in fishes of Basrah with two families: Gnathostomidae and Physalopteridae.

Family Gnathostomatidae:
This family is represented in fishes of Basrah with adults and larval forms of unidentified Echinocephalus.
Echinocephalus sp. 1 larvae were reported from the intestinal wall of both J. belangerii and S. sihama from Khor Abdullah (Bannai, 2002;Awad et al., 2003) and from the intestine of S. triostegus from Al-Hammar marsh (Jori, 2006).The generic name Sillago was misspelled as Silago by Awad et al. (2003).Bannai (2002), Awad et al. (2003) and Jori (2006) stated that Echinocephalus sp.larvae were provided with four transverse rows of spines on the cephalic bulb.As Echinocephalus spp.larvae are known to have 6-8 rows of spines (Millemann, 1963;Moravec and Justine, 2006), we conclude that the report of four rows of spines as indicated by the above three references from Basrah is erroneous and it is possible to indicate that with deformed specimens or improperly preserved ones loss of spines is quite possible.
Echinocephalus sp. 2 larvae were recorded from the mesenteries of both C. arabicum and C. arel from Khor Al-Ummaia (Ali, 2008;Ali and Al-Salim, 2013).Echinocephalus sp. 2 larvae have six transverse rows of spines on the cephalic bulb in comparison with larvae of Echinocephalus sp. 1 which were claimed by Bannai (2002), Awad et al. (2003) and Jori (2006) to have four rows.In addition, in Echinocephalus sp. 2 larvae, Ali (2008) and Ali and Al-Salim (2013) showed the presence of two groups of ventro-dorsally minute spines between the pseudolips and the first row of the large spines, each group consists of three transverse rows, the first and second rows have two minute spines and the last row has three minute spines, while such minute spines were never mentioned by Bannai (2002), Awad et al. (2003) and Jori (2006) in Echinocephalus sp. 1 larvae.The genus Echinocephalus has ten nominal species as parasites of the alimentary canal of elasmobranchs (Moravec, 2007b).It is difficult to separate different larval stages of Echinocephalus by morphological criteria.Also, it is difficult to associate the morphologically dissimilar larvae with their respective adults other than by observing specimens actually undergoing the final moult (Andrews et al., 1988;Beveridge, 1991;Moravec and Justine, 2006).There is a concern that at least some species of Echinocephalus may have public health significance as potential invaders of the human digestive tract (Bower, 2006).

Family Physalopteridae:
This family is represented in fishes of Basrah with three taxa, one belongs to the genus Paraleptus and two taxa belong to the subfamily Proleptinae.
Unidentified species of Paraleptus was reported from the stomach of C. arabicum in Khor Al-Ummaia (Ali, 2008).This is the only report on Paraleptus in Iraq (Mhaisen, 2014).The genus Paraleptus is one of the four genera of the subfamily Proleptinae which includes parasites of elasmobranchs (Moravec, 2007b).Paraleptus has eight valid species (Personal  communication between A.H.A. and Dr. Liang Li on 17 th Feb. 2014).
Unidentified larval species type BA of the subfamily Proleptinae was isolated from the mesenteries of Cynoglosus arel (Ali, 2008;Ali and Al-Salim, 2013).Another larval species type BB of this subfamily was recorded from the intestine of C. carpio from Univesrsity of Basrah fish farm (Jassim, 2007).

Superfamily Thelazioidea:
This superfamily is represented in fishes of Basrah with the family Rhabdochonidae.

Family Rhabdochonidae:
This family is represented in fishes of Basrah with one species of the genus Rhabdochona.
Rhabdochona garuai Agrawal, 1965 was recorded from the intestine of S. triostegus in Al-Hammar marsh (Jori, 2006).Dr. F. Moravec examined the illustration and description of R. garuai of Jori (2006) and believed that it was a misidentification of R. garuai by Jori (2006).So, we regretfully consider R. garuai, reported by Jori (2006) as Rhabdochona sp.The genus Rhabdochona comprises a large number of species parasitizing freshwater fishes in all the zoogeographical regions (Moravec, 2010).This genus includes four subgenera: the monotypical subgenus Rhabdochona, Globochona, Globochonoides and Sinonema which differ from each others mainly by numbers of anterior prostomal teeth, presence/ absence of lateral alae and some other features (Moravec, 2010).R. garuai belongs to the subgenus Globochona.The genus Rhabdochona has 97 valid species at the present (Moravec et al., 2013).

Addendum:
With this article, checklists of all the groups of parasitic worms infecting fishes of Basrah province were achieved.However, only one group remains untreated.This is the group of leeches (phylum Annelida, class Clitellata, subclass Hirudinea).Only one report on this group from fishes of Basrah is available.This is the record of the leech Hemiclepsis marginata (O.F. Müller, 1774) from gills of L. abu at the junction of Al-Khora canal with Shatt Al-Arab River (Mhaisen et al., 1993).This leech was reported for the first time in Iraq from the skin of three fish species in fish ponds near Baghdad (Khalifa, 1985).In Iraq, six taxa of leeches are so far documented (Mhaisen, 2014).
To sum up, it is worthwhile to show here that the 48 nematode taxa so far recorded from fishes of Basrah province represent 60% of the total number of nematode taxa from freshwater and marine fishes of whole Iraq (Mhaisen, 2014).Such high percentage is due to the presence of marine nematodes from fishes of Basrah province in addition to the freshwater nematodes.Moravec (2006), Anderson et al. (2009) and Gibbons (2010).* Numbers in curly brackets occurring after the authority of each parasite refer to number of host species recorded for that parasite in Basrah province/ number of hosts recorded for the same parasite from the whole inland waters of Iraq based on data obtained from the index-catalogue of parasites and disease agents of fishes of Iraq (Mhaisen, 2014).
Thanks are due to Dr. František Moravec of the Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic for his comments and advice on some nematode taxanomy.Thanks are also due to Dr. Li Liang of the College of Life Science, Hebei Normal University, China for providing us with information on Paraleptus and Acanthocheilus.Thanks are due to Prof. Dr. Yukio Iwatsuki of the Department of Marine Biology and Environmental Sciences, Faculty of Agriculture, University of Miyazaki, Japan for confirming the idendity of images of Acanthopagrus arabicus from Shatt Al-Arab River.

Table 2 .
List of fishes of Basrah province and their richness § with the nematodes._____________________________________________________