Napata Scientific Journal, Vol.1 (1) 2022 pp. 58-99

 

 

Review

 

A Review of Parasites of Freshwater Fishes of the Sudan from 1902 to 2020

 

1. N. Mahmoud^1*, R. M. Abdalla¹

¹ Department of Zoology, Faculty of Science, University of Khartoum

^∗Corresponding author: zuheirnm@hotmail.com.

 

Abstract

Background

This review was conducted from 1996 to 2020 aiming to compile the findings of parasites of freshwater fishes of Sudan in a single document.

Methods

The present review was based on 105 scientific paper, 3 conferences abstracts, 3 graduation dissertation, 7 master and 2 Ph.D. theses, one unpublished reports, 10 books, and one technical report. The work covered the period from 1902 to 2020.

Results

Some thousands of freshwater fish specimens were examined for their ecto-parasites and/or endo-parasites. Fifty-eight fish species were reported infected and 162 parasitic species including 32 new species were collected. The parasites found were three bacterial and three fungal species collected from Oreochromis niloticus. From 10 species of fish, 19 protozoans were described. From 10 species of fish, 22 Monogenean species were found including 7 new species. One new Aspidogastrean species was collected from Labeobarbus bynni. From 29 fish species 23 Digenean species were collected including five new ones. From 41 species of fish, 44 species of cestodes parasites were collected including 11 species new to science. Twenty parasitic Nematodes species including seven new ones were collected from 32 fish species. From 12 fish species 9 Crustacean were described. Nine Acanthocephalans including one new species from Ichthyborus besse were collected from 11 fish species. Co-infection was observed.

Conclusions:

The collected parasites included 31 new species to science. One new subfamily Sandonellinae from Heterotis niloticus was erected; and 10 new genera, Brevicaecum, Sandonia, Afromacroderoides (Digenea); Wenyonia, Sandonella, Amirthalingamia, Barsonella lafoni (Cestoda) and Dichelyne, Nilonema, (Nematoda) were described. Revision of parasitic species designated as CithariniellaTrypanosoma type 1, 2, 3; Dactylogyrus species type 1, 2, 3, 4, 5; Dogielius sp. 1;Amplicaecum type 1 and Amplicaecum type 2; Contracaecum sp. Third stage-larvae Type 2; Procamallanustype 1, 2, 3 and those parasites identified to the genus level should be given due attention. Some recommendations for further research were offered.

Keywords: Freshwater fishes, Parasites, Sudan, Sandonellinae, Heterotis niloticus.

 

 

 

Introduction

 

Parasitism is a biological phenomenon caused by parasites at various levels in the food chain in any ecosystem. It is a life strategy for several forms of biota. Parasites range in size from microscopic forms to macroscopic ones. Examples are Trypanosoma mukasaiin the blood of O. niloticus [1] and the ectoparasitic sea lampreys Petromyzon marinus on the minke whales Balaenoptera acutorostrata [2, 3], beside fishes, whales, dugong and sea turtles. This ecto-parasite is large enough to be seen by the naked eyes from several meters.

A fundamental feature associated with parasitism in fishes is the negative impact cost by some parasite on its host affecting behavioral response in some cases. This cost included but not limited to loss of blood, intestinal fluid and of energy in defensive mechanisms against the parasites. Irritability, attracting secondary infection to establish, skin necrosis and anemia are also associated with parasitism. Some parasites act as a blood sucking ecto-parasites (Mothocya belonae an isopod parasite of the marine garfish Belone [4]. Parasites can deprive the host from sizable quantities of intestinal fluids as reported by [5, 6] in Clarias gariepinus infected bythe intestinecestodes Polyunchobothrium polypteri Leydig, 1853. According to [7] anemia in goldfish Carassius auratus is the resultant of infection with Trypanosoma danilewskyi. Parasitism was reported by [8] to affect courtship dance in the three spine sticklebacks (Gasterosteus aculeatus).

Fishes (Class: Pisces)are indeed superior in number of individuals and species to other vertebrates. Probably more than 25,000 different species of fish are extant and many new forms are discovered every year [9]. Parasites wise, new fish species are usually followed by new species or new fish hosts or new parasite localities records.  In the River Nile and its tributaries in Sudan there are about 123 fish species belong to 22 families [10], but only about 50 of these fish species are of economic importance and are recognized as a source of animal protein [11]. In the aquatic environment the fish is subjected to viruses, fungi, bacteria, protozoa, helminthes, crustacean, and acanthocephalan some of which are potentially infectious. Fish diseases and parasites are detrimental for proper utilization of some of these valuable food resources. Studies of captive freshwater fishes have provided much information about fish parasites [5] and diseases [6]. Fish parasites and hence diseases are being understood as longtime factors, and various methods are being probed to control them especially when fish are kept in confinements such as fish ponds or aquaria. The first step is always the proper isolation, identification and description of existing parasites [12]. In Sudan studies on freshwater fish parasites probably dates back to the pioneer work of Jagerskiold and his collaborators in 1902). According to [5] helminthes are very common in freshwater fishes of Sudan and cause few lesions by the intestinal ones.

Although the history of parasitological studies on freshwater fishes’ dates back to 1902, the fauna of these parasites in Sudan is still little known. Khalil from 1960 to 1997 published 18 papers on helminthes parasites from freshwater fishes and described seven species new to science and made 30 new records to the Sudan. Khalil [13] reported 15 species of adult digenetic trematodes, three species of larval trematodes, 16 species of adult cestodes, 13 species of adult nematodes, two species of larval nematodes and three species of acanthocephalans. Four species of adults and four species of larval worms are recorded for the first time in the Sudan and 30 new hosts were listed by [13].

In his update of parasites, infections and diseases of fishes in Africa [14] repeatedly referred to Khalil’s work. The checklists on fish parasites in Africa produced by [15, 16] were criticized by [17] on basis of being out of date and do not provide reliable information on the current state of species diversity of these fish parasites. A monogenean Macrogyrodactylus polypteri was described by [5, 18, 19, 20, 21] from Polypterus sp. To the parasites of freshwater fish of Sudan, [22, 23, 24] added 19 monogenean species including six new to science and six under evaluation for their taxonomic status.

It is unfortunate that the theses of [1, 5, 25, 26, 27] were not published and are looked upon as grey research, despite the useful information therein about parasites of freshwater fishes of Sudan.

 

Objectives

This article used the existing literature to create a new knowledge. The objective of this literature review is to compile the available information about parasites of freshwater fishes of Sudan embodied in dissertations, thesis, books, conferences abstracts and scientific articles in a single document. Fish parasites, the fish species infected the infected organs or tissues and the references were given in appropriate tables. This review which is by no means complete covered the period from 1902 to 2020. It is hoped that

 

Table 1. New parasitic species recorded from freshwater fishes of Sudan (* new genus)
Taxon		Fish (type) host	Author(s)_
Monogenia
Afrogyrodactylus girgifae		Brycinus [Alestes] nurse	[30]#
Quadriacanthus fornicates		Clarias gariepinus[lazera]	[22]#
Quadriacanthus pravus		Clarias gariepinus	[22]#
Quadriacanthus zuheiri		Clarias gariepinus	[22]#
Quadriacanthus mandibulatus		Heterobranchus bidorsalis	[22]#
Dogielius sennarensis		Labeo niloticus	[23]#
Characidotrema pollex		Brycinus nurse	[24]#
Aspidogastrea
Allocreadium sudanensis		Labeobarbus [Barbus] bynni	[31]
Digenea
Aspidogaster africanus		Labeobarbus bynni	[32]
Brevicaecum niloticum*		Citharinus citharus	[33]
Sandonia sudanensis*		Synodontis schall	[33]
Orientocreadium lazeri		Clarias gariepinus	[34]
Afromacroderoides lazerae*		Clarias gariepinus	[35]
Cestoda
Wenyonia virilis*		Synodontis schall	[37]
Wenyonia minuta		Chrysichthys auratus	[37]
Wenyonia accuminuta		Synodontis membranaceaus	[38]
Proteocephalus synodontis		Synodontis schall	[37]
Proteocephalus sandoni		Heterotis niloticus	[39]
Lytocestus alesstesi		Alestes sp.	[40]
Sandonella sandoni*		Heterotis niloticus	[41]
Bothriocephalus prudhoei		Clarias anguillaris	[42]
Ichthybothrium ichthybori		Ichthyborus besse	[15]
Amirthalingamia macracantha		Oreochromis niloticus	[43]
Barsonella lafoni*		Clarias gariepinus	[44]#
Nematoda
Dichelyne fossor*		Lates niloticus	[29]
Nilonema gymnarchi*		Gymnarchus niloticus	[45]
Raphidascaroides bishaii		Gymnarchus niloticus	[46]
Falcaustra  hexapapillata		Distichodus nefasch	[47]
Cithariniella citharini*		Citharinus citharus	[48]
Cucullanus mormyri		Mormyrus caschive	[17]#
Procamallanus pseudospiralis.		Synodontis schall	[17]#
Acanthocephala
Neochinorhynchus ichthyobori		Ichthyborus besse	[49]

 

researchers in fish parasites and their related pathology find this article of relevance and useful in formulating future research projects.

 

Desk Work

The present review was based on 105 scientific papers, 3 conferences abstracts, 3 graduation dissertations, 7 masters and 2 Ph.D. thesis, one unpublished reports, 10 books, and one technical report. The systematic of these parasites is based on some electronic sites and some taxonomic papers. The names of fish hosts recorded were those provided in FishBase as valid names [28]. Generic/species names used in the original description are retained in square brackets as synonyms when first mentioned

 

A Quick Glimpse

Perhaps the first authenticated work on parasites fr.om freshwater fishes in the Sudan was that of the Swedish Zoological Expedition to Egypt and the White Nile from1901 to 1910, which was led by Prof. Jagerskiold. The parasites collected, some of which were prototypes, were deposited at the Department of Zoology, Uppsala University. A new genus was erected and a new nematode species (Dichelyne fossor Jagerskiold, 1902) was described from the intestine of lates niloticus from the White Nile by [29]. Since then one new subfamily Sandonellinae and several new genera and species were recorded form freshwater fishes of the Sudan. Significant contribution was made by Lotfi Fakhori Kahlil (1960-1979). Tomas Scholz (Institute of Parasitology CAS CR, Czech Republic) and Alain de Chambrier (Natural History Museum, Geneva, Switzerland) in (2006-2008) in collaboration with Zuheir N. Mahmoud made an extensive field surveys. The survey is part of a project aimed at revising the morphology and verifying the taxonomic status of poorly known African Cestodes of the orders Proteocephalidea, Caryophyllidea and Pseudophyllidea, and other helminthes parasites of freshwater fish, as a prerequisite for phylogenetic studies on the evolution of these parasites and their fish hosts. The interesting findings encouraged the collaboration of the Institute of Parasitology, Biology Centre of the CAS, the Department of Botany and Zoology, Faculty of Science, Masaryk University, Czech Republic and Sudan Institute of Natural Sciences to carry out more field work in Sudan. This fruitful collaboration led to description of one new genus and 10 new parasitic species to Science. These were indicated by^# after the author(s) in Table 1.

 

Findings and Discussion

Parasitic bacteria

Bacterial infection may cause heavy losses of fish from natural water bodies or species reared in ponds. The first to study bacteria of freshwater fishes of the Sudan was [25] who revealed the presence of Bacillus sp. and Diplococcus sp. from the blood of O. niloticus. It was not made clear by [25] whether these are due to secondary infection or not? In many cases fish injuries act as a pathway facilitating viral and/or bacterial infections.Bacterial infection usually induces morphological and physiological changes in fish. Aeromonas hydrophile infecting the mouth of O. niloticus and causing fin deformity were reported from several specimens collected from Al Azozab White Nile by [50].

 

Parasitic fungi

Fungi are associated with injuries causing diseases of freshwater fishes [51]. Infection of fish skin by fungi is manifested by appearance of cotton wool cover over the epidermis damaging it as it spreads causing extensive necrosis [52]. Body injuries in fish facilitates invasion by integument parasitic fungal species. Soprolegnia sp., Achlya sp. and Aureobasidium sp., were collected from the skin and mouth of O. niloticusby [25]. The fungus Aureobasidium sp., was reported for the first time as a fish pathogen in Sudan by [25].  According to [25] whenever fungal infections were found in O. niloticus, myxosporeans were also detected. The relationship between the natural seasonal occurrence of Saprolegnia sp.in the freshwater and the periodicity of the fungal infections recorded on O. niloticus was demonstrated by [25]. 

 

Parasitic protozoa

According to [12] the internal protozoan parasites, like Myxosporidions a serious internal fish pathogen, stuck in the fish tissue and either kill the host or persist for long periods of time deteriorating fish health and quality. Protozoan parasites have attracted the attention of various researchers. Paperna [14] wrote “in 1841 what was either a Trypanosome or probably a Trypanopolasm species was recorded by Valentin from the blood of the trout Salmo fario”. He added in the following year “1842” Remok found what seemed definitely to have been a Trypanosome in the blood of the pike (Esox sp.). Since then a long list of findings in various parts of the world were published in periodicals or incorporated in theses and/or technical reports. Some of these were new to science. According to [53] a total of 153 species of trypanosomes have been described from freshwater and marine fishes. In addition, 33 unnamed records from various fish hosts exist. According to [14] about ten forms of trypanosomes were reported from fish in Africa, out of which five or six were accepted as valid species. In Sudan only two species were found (T. mukasai from O. niloticus and Trypanosoma alhusaini from Clarias gariepinus) and the rest were designated cautiously by investigators as Trypanosoma Type 1, Trypanosoma Type 2, or Trypanosoma sp.

Protozoan fish relationship may be of no relation, commensalism or parasitism. In fish hatcheries and field situations some infections of the fish by protozoan are recognized as normal and pose no health and/or economic problem. Protozoan ecto-parasites such as Costia spp. and Trichodina spp. are among the genera which may infect fish causing suffering, death in fish populations and consequently serious economic losses if it happened in fish ponds.  According to [12] epidermal tissue destruction caused by protozoan usually attracts viral, bacterial and fungal infections. Very little work on protozoa of Sudanese freshwater fishes had been done compared with the work done in the region. Three categories of protozoan’s: trypanosomes, myxosporeans and ciliates were reported.  According to [26] impression smears of liver and spleen revealed the presence of Myxobolus sp. Bütschli, 1882 and M. heterospora Baker, 1963; in 2% of the studied fishes. Investigations of body cavity and viscera revealed that 72% of fishes were infected with one or both parasites [26].

Fish trypanosomes are more than 190 species [54]. The first report of fish trypanosomes from Sudan was due to [55] who noted the presence of a Trypanosoma sp. in the blood of S. [Lynodontis] schall, Bagrus bajad [bayad] and Mugil species but gave no description of the parasite. Trypanosoma spp. in the blood of Mugil sp., B. bayad, S. schall, Chrysichthys auratus [auratii], Coptodon [Tilapia] zillii, Clarias anguillarias and Polypterus sp. from the Nile in Sudan was found by [56]. It is likely that Mugil sp. is a misidentified cyprinid species, as Mugil sp. has never been recorded among freshwater fishes of Sudan [57, 58]. Four protozoan species were reported from O. niloticus and Sartherodon galilaeus [Tilapia galilaea] fishes in the Sudan (Table 4) by [1]. Those were Trypanosoma mukasi Hoare, 1932, Myxosoma heterospora Baker, 1963, Myxosoma brachyspora Baker, 1963 and a Myxosoma identified to the genus level. The host-parasites relationship for O. niloticus and S. galilaeus was investigated by [1]. This trait was improved by rigorous statistical analysis carried by [5, 26]. Trypanosoma alhusaini Mohamed, 1978 from C. gariepinus and a Trypanosoma sp. from Polypterus senegalus and S. schall were reported by [5]. The occurrence of T. alhusaini was reported only by [5]. Unfortunately, the extensive measurements on trypanosomes from P. senegalus and S. schall were not compared to find out whether there is specific variation? Or whether there are one or more forms of the Trypanosom sp?  The presence of T. mukasi in O. niloticus was confirmed by [25, 51]. Based on multiple regressions analysis of six measured characters against total body length excluding the free flagellum, three distinct length groups of trypanosomes were found by [25]. These were T. mukasi (27.21±4.09), Trypanosoma Type 1 (46.55±3.59) and Trypanosoma Type 2 (59.71±2.64). The clear cut differences in length made this grouping valid and of relevance in any comparative study of blood trypanosomes of fishes. The advancement in molecular biology and sequencing can determine the validity of this designation as Type 1 or Type 2 and even defining the species. According to [59] isoenzymes and molecular sequencing are useful in resolving the confusion regarding the synonymy of species and naming the valid species.

A total of seven Myxosporean parasites (Myxosoma heterospora, Myxosoma brachyspora, Myxosoma equatoriali, Myxosoma sarigi, Myxobolus agolus, Myxobolus galilaeus and Myxobolus sp.) were recorded by [1, 5, 25, 26] from O. niloticus, S. galilaeus and C. gariepinus (Table 2). All these were reported as first record to Sudan. Shamat [25] produced transmission and scanning electron photomicrographs for the studies Myxosporean species and based the identification on similarities and differences in spore size, 11 morphological measurements and site of infection.

The ecto-parasitic ciliate Trichodina sp. from O. niloticus was reported by [1, 51]. Trichodina heterodentata Duncan, 1977 were collected from the skin and gill lamellae of O. niloticus by [25].

Most of the fish specimens examined for their protozoa were collected from the White Nile and fish ponds in Khartoum. No attempts were made to quantify the prevalence rates in infected fish species. Trypanosoma species are transmitted to fish through a blood-sucking vector, usually a species of leech, but isopod crustaceans can also be potential vectors of Trypanosomiasis in fish. This needs further investigation. The Apicomplexa,  Cyrilia nili [syn. Haemogregarina nili, Wenyon, 1909] infect fresh water fish and are transmitted by the African fish leech Batracobdelloides tricarinata Blanchard, 1897, [14] it was found in blood smear of Parachanna obscura.

The detection of these vectors attacking freshwater fish in Sudan should be given due attention as trypanosomes were found in a number of fish species including O. niloticus, S. galilaeus, C. zillii, C. gariepinus, B. bajad, C. auratus and Polypterus sp., see Table 2.

 

Table 2.Protozoa parasites of freshwater  fishes from Sudan
Parasites	Infected organ / tissue	References
Parachanna obscura
Cyrilia nili Wenyon, 1909	Blood	[60]
Oreochromis niloticus
Trypanosoma mukasai Hoare, 1932	Blood	[1, 25, 51, 61, 62]
Trypanosoma type 1	Blood	[25]
Trypanosoma type 2	Blood	[25]
Myxosoma heterospora Baker, 1963	Hepatopancreas, brain, heart	[1, 25, 51, 61]
Myxosoma brachyspora Baker, 1963	Hepatopancreas, brain, heart, spleen	[1, 25, 26]
Myxosoma sarigi Landsberg, 1985	Hepatopancreas, brain, heart	[1, 25]
Myxosoma equatorialis Landsberg, 1985	Hepatopancreas, brain, heart	[1, 25]
Myxobolus agolus Landsberg,1985	Hepatopancreas, brain, heart	[25]
Myxobolus galilaeus Landsberg, 1985	Hepatopancreas, brain, heart	[25]
Myxobolus sp. Bütschli, 1882	Hepatopancreas, brain, heart, liver,  kidney, ovaries	[1, 25, 54]
Cryptobia sp.  Leidy, 1856	Liver	[61, 62]
Trichodina heterodentata Duncan, 1977	Skin and gill lamellae	[25, 61]
Myxospora sp. Butschli, 1882	Gill lamellae	[50]
Trichodina sp. Ehrenberg, 1831	Skin and gill lamellae	[1]
Sartherodon galilaeus
Trypanosoma sp. Gruby‎, 1843‎	Blood	[55]
Trypanosoma mukasai Hoare, 1932	Blood	[1]
Myxosoma heterospora Baker, 1963	Hepatopancreas	[36]
Myxosoma brachyspora Baker, 1963.	Hepatopancreas	[36]
Myxosoma sp. Thélohan, 1892	Hepatopancreas	[36]
Coptodon zillii
Trypanosoma sp.  Gruby‎, 1843‎	Blood	[55]
Clarias gariepinus
Trypanosoma alhusaini Mohamed, 1978	Blood	[5]
Myxosoma sp. Bykhovskaya-Pavlouskaya, 1964	Hepatopancreas	[5]
Trypanosoma sp. Gruby‎, 1843‎	Blood, Liver	[62]
Haemogregarine  sp. Danilewsky, 1885	Blood	[62]
Myxobolus sp. Bütschli, 1882.	Liver, kidney, ovaries	[26, 54]
Synodontis schall
Trypanosoma sp. Gruby‎, 1843‎	Blood	[5, 55, 56]
	Liver	[26]
Labeobrabus bynni
Myxosoma heterospora Baker, 1963	Spleen	[26]
Bagrus bajad
Trypanosoma sp. Gruby‎, 1843‎	Blood	[55]
Chrysichthys auratus
Trypanosoma sp. Gruby‎, 1843‎	Blood	[55]
Polypterus sp.
Trypanosoma sp. Gruby‎, 1843‎	Blood	[55]

 

Parasitic Trematoda

The knowledge of trematode fauna remains highly incomplete [63, 64]. Current estimates of trematode species in African freshwater fishes revealed the presence of 66 species (based on adults) allocated in 33 genera of 20 families reported from 59 freshwater fish species [64].

The earliest study on trematodes of freshwater fishes of the Sudan was probably the historic work of the Swedish Zoological Expedition to Egypt and the White Nile from 1901 to 1910. Odhner, a member of the expedition, in 1902 described two digeneans (Callodistomum diaphanmun)from Polypterns senegalus and Cheloptes ovofractas from S. schal.  His work was published nine years later by [65] Table 3. The majority of African Monogenea species are ecto-parasites found on gill lamellae, skin and fins, and rarely in mouth cavity and nostrils; a few species are endo-parasitic in foregut, stomach and urinary bladder [24, 60].

Macrogyrodactylus polypteri Malmberg, 1957 is a viviparous monogenetic described from the skin of C. citharinus and from gill lamellae of P. senegalus by [18, 19] and from the skin and fins of P. senegalus by [5, 20,21]. Macrogyrodactylus polypteri was also described from Polypterus bichir by [21]. According to [19] M. polypteri, which is likely confined to African fishes, feeds on epidermal cells and mucous when young and upon the blood of its host, at least in part, when adult. A detailed description of its life cycle was given by [19]. To the physiology, biology and morphology of M. polypteri [5] made very useful contribution and reported that heavy parasitaemia by M. polypteri causes anemia in P. senegalus as well as significant drop in the level of Hb, PCV, RBC, WBC, total protein, albumen, globulin and glucose levels.  The chemical investigation of the gut contents of M. polypteri carried out by [5] established a blood feeding habit for this parasite. According to [5] warm water is the best medium for induction of birth of M. polypteri. The ultra-structure of M. polypteri was revealed by using scanning electron microscopy by [5]. Allocreadium sudanensis sp. nov., was described and compared with five African species of the genus Allocreadium and produced a key for their identification by [31]. Allocreadium sudanensis is the first member of Subclass Aspidogastrea to be collected from freshwater fishes of Sudan.

A systematic survey of the monogeneans parasitizing freshwater fishes in Africa was carried by ichthyo-parasiologist of the Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic [66]. Their taxonomic evaluation of the monogeneans found was based on macro and ultra-structural, molecular and phylogeny studies. Their collection resulted in a catalogue of 482 monogenean species parasitizing African freshwater fishes [66]. Afrogyrodactylus girgifae sp. n. was described from the fins of Brycinus nurse (type host) from Sinnar (type locality), Blue Nile, Sudan by [30].The specific name is derived from ‘girgifa’, common name for B.nurse in Nubian, old Sudanese. Significant addition to the monogenean of Sudan was made by [22, 23, 24] who described six new monogeneans species to science from Sudan and several locality records of monogenea to Sudan.

Seven Quadriacanthus species from the gill lamellae of three catfishes for the first time in Sudan. These were Q. aegypticus, Q. clariadis, Quadriacanthus fornicatus n. sp., Quadriacanthus pravus n. sp., and Quadriacanthus zuheiri n. sp. from Clarias gariepinus (type host); Quadriacanthus mandibulatus n. sp. from Heterobranchus bidorsalis (type host); and Q. bagrae from Bagrus docmak (type host) were described by [22]. In addition, they made taxonomic evaluation of the monogeneans found on basis of morphometric mesurements and molecular biology methods usingtwo nuclear ribosomal DNA fragments. The interspecific relationships among Quadriacanthus spp., were investigated for the first time [22]. According to [22] for both 18S-ITS1 and 28S, Q. clariadis was found to be most closely related to Q. bagrae. Quadriacanthus mandibulatus was observed to be the most distant species from others [22]. The separation of Q. mandibulatus from the other species corresponds with the different morphology of its copulatory tube [22]. The copulatory tube is terminally enlarged and with sub terminal flange in Q. mandibulatus, while the tube in all other congeners studied is comparatively small and with oblique tapering termination [22]. Quadriacanthus clariadis from a clariid fish is sister species to Q. bagrae from a bagrid host indicating a possible host-switching event in the evolutionary history of the genus [22]. TheDactylogyrids (Platyhelminthes: Monogenea) from Sudanese Labeo spp was studied by [23]. Based on a morphometric evaluation of the sclerotised structures [23] reported the presence of ten Dactylogyrus spp., and three Dogielius spp. These were Dactylogyrus nathaliae from L. niloticus, D. rastellus and D. retroversus from Labeo horie; D. senegalensis and D. yassensis from L. horie and L. niloticus from Kosti, White Nile [23]. Five Dactylogyrus sp., and designated them as Dactylogyrus sp. 1 from L. horie, Dactylogyrus sp. 2, Dactylogyrus sp. 3, Dactylogyrus sp. 4 and Dactylogyrus sp. 5 the last 4 ones were from L.niloticus and were rigorously investigated by [23]. Dogielius fl osculus from L horie, a new species to science Dogielius sennarensis n. sp., from L. niloticus from Sinnar were described by [23], who also reported Dogielius sp. 1 from L. horie from Sinnar, Blue Nile and L niloticus from Kosti, White Nile. Completion of characterization of Dactylogyrus sp1- 5 and Dogielius sp. 1 spp., will add to science and the parasites of freshwater fishes of Sudan.

Characidotrema (Monogenea: Dactylogyridae) from B. nursefishes from Kosti and Sinnar, Sudan was studied by [24]. They described Characidotrema pollex as a new species to science, they also recorded C. brevipenis, C.nurse, C.spinivaginus and C. zelotes. All collections were made from B. nurse from Kosti and Sinnar [24]. According to [24, 66]species identification was based on morphological analysis of the sclerotized structures supported by the genetic relationships among these species using nuclear ribosomal DNA (partial 18S rDNA, ITS1, and 28S rDNA) sequence data. Morphological analysis confirmed that the most apparent character distinguishing species in the genus is the morphology of the male copulatory organ and vagina [24, 66].

The digenetic parasites recorded so far from the freshwater fish of Sudan are 24 out of 57 trematodes species (Table 3). The presence of the digenetic Clinostomum complanatum larva, from H. niloticus from Khartoum were listed by Scholz and de Chambrier in an unpublished report on their 2006 and 2008 freshwater fish parasitological expedition to Sudan.

Sandonia sudanensis gen. et sp. nov., was described from the intestine of Synodontis schall (type host) and Distichodus niloticus collected from the Nile near Khartoum by [33]. Its affinities with members of the subfamily Schizamphistomainae was discussed by [33]. Its presence in the type host and the type locality was confirmed by [5]. Additional hosts were B. docmak, Distichodus nefasch, D. rostratus, Synodontis batensoda, S. clarias, S. membranaceus, S. nigrita, S. sorex and Synodontis sp., added by [64].

A detailed description of Diplostomulum tregenna Nazi Gohor, 1932 a trematode of the fat tissue in the cranial cavity of C. gariepinus was given by [36] who in addition demonstrated experimentally part of its life cycle. The presence of D. tregenna in the type host was confirmed by [5]. A new species of TrematodesOrientocreadium lazeri from the intestine of C. gariepinus (Table 1) was described by [33]. Brevicaecum niloticum gen. et sp. nov., was described from the intestine of Citharinus citharus (type host) collected from the Nile near Khartoum by [33]. It was placed by McClelland (1957) in the subfamily Kalitrematinae. Brevicaecum niloticum (Trematoda, Paramphistomidae) was redscribed from the intestine of C. citharus by [33] who amended the characters of the genus and erected a new subfamily Brevicaecinae to accommodate the genus. Aspidogaster africanus was redscribed as a new species from Labeobarbus bynni by [31]. The description was based on detailed morphological features such as the position of the ovary in relation to testis. Glossidium lazerae [Afromacroderoides lazerae] gen. et. sp. nov. (Allocreadiidae; Walliniinae) was collected, described and figuredfrom specimens found in the intestine of the African freshwater fish C. gariepinus from the White Nile near Khartoum, Sudan, by [35]. The new genus is distinguished by the shape of its cirrus sac, the presence of a bipartite seminal vesicle and a spiny cirrus from the related genera Paramacroderoides and Pseudoparamacroderoides [35]. According to [67] Glossidiumpedatum Loss, 1899 was first reported from B. bajad and Bagrus docmak from the lower reaches of the River Nile. Glossidiumpedatum was collected and described from the intestine of Clarias mossambicusfrom Lake Haik in Ethiopia by [68] and from C. gariepinus from South Africa by [69]. Both authors noted similarities between G. pedatum and A. lazerae [35] and synonymized it with G. pedatum [67]. However, [70] based on his diagnoses of genus Glossidium, did not considered the synonyms between G. pedatum and A. lazerae thus he made the new combination Glossidium lazerae.

The trematodes described by [1] were Euclinostomum heterostomum, Clinostomum tilapiae and Clinostomum phalacrocorcis in different tissues in O. niloticus. Clinostomum tilapiae Ukoli, 1966 was found in the bucco-pharynged cavity of O.niloticus by [26]. The occurrence of a parasite in different tissues of a host is probably a strategy to avoid competition.

One monogenean (M. polypteri) and seven digeneans (Basidiodiscus ectorchis, S. sudanensis, Callodistomum diaphanum, C. ovofractas, and Diplostomulum tregenna (Metacercaria); and two unidentified adult digeneans were reported by [5] Table 3. The hemorrhage in C. gariepinus infected by D. tregenna was noticed by [5, 34] who related the extent of hemorrhage to the intensity of infection. Callodistomum diaphanum Odhner 1902 was reported from S. schall by [5], and from S. schall, P. bichir and P. endlichheri by [64]. The parasites of O. niloticus and H.  forskalii collected from Khartoum fish market were studied by [71]. From the investigated fish specimens three metacercaria, Euclinostomum heterostomum, Clinostomum tilapiae and C. phalacrocoracis with the parasitic incidence of 78% in O. niloticus and 61% with females exhibiting higher percentage of infection than males [71]. Ahmed [6] worked on two freshwater fish, O. niloticus and C. gariepinus collected from Jebel Aulia reservoir and the sewage ponds South of Khartoum. He reported C. tilapiae and Clinostomum sp. from O. niloticus from the reservoir. Metacercaria of C. tilapiae and of C. phalacrocoracis from O. niloticus were reported by [26].

Nemathobothrium labeonis McClelland, 1955 was collected from a Labeo sp by [13].  Later, [72] collected N. labeonis from Labeo coubie, L. forskalii, L. horie and L. niloticus. From some freshwater fishes of Sudan [64] recorded Sanguinicola chalmersi Odhner, 1924 from Auchenoglanis occidentalis and S. schall; Cholepotes ovofarctus (Odhner, 1902) from S. schall and Synodontis sp., Thaparotrema piscicola (Odhner, 1902) from G. niloticus. Description of Sanguinicola sp. Plehn, 1905 as an exraintestinal parasite from S. schall and A. occidentalis was made by [13]. For Nematobothrium sp., [64] listed two hosts Labeo coubie and, L. senegalensis

A summary of trematodes of freshwater fish of Sudan collected from organs/tissues by different investigators were given in Table 3.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Table 3. Trematodes of freshwater fishes from Sudan.
Parasites	Infected organ /tissue	References
Class Monogenea
Polypterns senegalus
Macrogyrodactylus polypteri Malmberg,1957	Skin, fins	[5, 18, 19, 20, 21]
Polypterus bichir
Macrogyrodactylus polypteri Malmberg,1957	Skin, fins	[21]
Clarias gariepinus
Quadriacanthus aegypticus El-Naggar and Serag, 1986.	Gill lamellae	[22]
Quadriacanthus clariadis Paperna, 1961.	Gill lamellae	[22]
Quadriacanthus fornicatus Francová and Řehulková, 2017	Gill lamellae	[22]
Quadriacanthus pravus Francová and Řehulková, 2017	Gill lamellae	[22]
Quadriacanthus zuheiri Francová and Řehulková, 2017	Gill lamellae	[22]
Heterobranchus bidorsalis
Quadriacanthus mandibulatus Francová and Řehulková, 2017	Gill lamellae	[22]
Bagrus docmak
Quadriacanthus bagrae Paperna, 1979	Gill lamellae	[22]
Labeo niloticus
Dactylogyrus nathaliae Guégan, Lambert & Euzet, 1988	Gill lamellae	[23]
Dactylogyrus spp.	Gill lamellae	[23]
Dogielius sennarensis Pardova et al.,2018	Gill lamellae	[23]
Labeo horie
Dactylogyrus rastellus Guégan, Lambert & Euzet, 1988	Gill lamellae	[23]
Dactylogyrus retroversus Guégan, Lambert & Euzet, 1988	Gill lamellae	[23]
Dactylogyrus senegalensis Paperna, 1969	Gill lamellae	[23]
Dactylogyrus yassensis Musilová, Řehulková and Gelnar, 2009	Gill lamellae	[23]
Dogielius osculus Guégan, Lambert and Euzet, 1989	Gill lamellae	[23]
Dogielius sp.	Gill lamellae	[23]
Brycinus nurse
Characidotrema pollex Kičinjaová and Řehulková, 20109	Gill lamellae	[24]
Characidotrema brevipenis Paperna, 1969	Gill lamellae	[24]
Characidotrema nursei Ergens, 1973	Gill lamellae	[24]
Characidotrema spinivaginus Paperna, 1973	Gill lamellae	[24]
Characidotrema zelotes Kritsky, Kulo & Boeger, 1987	Gill lamellae	[24]
Subclass Aspidogastrea Faust et Tang, 1936
Labeobarbus bynni
Allocreadium sudanensis Saoud, Abdel-Hamid and Ibrahim, 1974	Intestine	[31]
Subclass Digenea Carus, 1863
Oreochromis niloticus
Euclinostomum heterostomum Rudolphi, 1809	Kidney	[1, 71]
Clinostomum tilapiae Ukoli, 1966	Operculum muscle, buccal cavity	[1, 6, 26, 71]
Clinostomum phalacoracis Dubois, 1931	Buccopharyngeal	[1, 26]
Clinostomum sp.  Leidy, 1856	Buccal cavity	[6]
Sartherodon galilaeus
Euclinostomum heterostomum Rudolphi, 1809	Kidney	[1]
Clinostomum tilapiae Ukoli (1966)	Operculum muscle	[1]
Clinostomum phalacoracis Dubois, 1931	Buccopharyngeal cavity	[1]
Clarias gariepinus
Orientocreadium lazeri  Khalil, 1961		[33]
Diplostomum tregenna Nazmi Gohor, 1932	Fat tissue in the cranial cavity	[5, 34]
Diplostomum spathaceum Rudolphi, 1819	Intestine	[36]
Diplostomum mashonense Dubois, 1961	Intestine	[36]
Glossidium lazerae Khalil, 1972	Intestine	[35]
Labeobarbus bynni
Aspidogaster africanus Saoud, Mohamed et Abdel-Hamid, 1974	Intestine	[31]
Polypterns senegalus
Callodistomum diaphanmun Odhner, 1902	Gall bladder	[5]
Callodistomum diaphanmun Odhner 1902	Intestine	[5]
Synodontis schall
Sanguinicola sp. Plehn, 1905	Exraintestinal	[13]
Basidiodiscus ectorchis Fischthal & Kuntz 1959	Stomach, upper intestine	[5]
Sandonia sudanensis McClelland,1957	Stomach, upper intestine	[5]
Cheloptes ovofractas Odhner, 1902	Gall bladder	[5, 58]
Callodistomum diaphanum Odhner 1902	Intestine	[5, 58]
Bagrus docmak
Phyllodistomum sp. Braum, 1899	Intestine	[26]
Hydrocynus forskalii
Euchinostomum heterostomum Rudolphi, 1809	Buccal cavity	[71]
Clinostomum tilapiae Ukoli, 1966	Buccal cavity	[71]
Clinostomum phalacoracis Dubois, 1931	Buccal cavity	[71]
Phyllodistomum sp. Braum, 1899		[26]
Citharinus citharus
Brevicaecum niloticum McClelland, 1957	Intestine	[73]
Auchenoglaris occidentalis
Sanguinicola sp. Plehn, 1905	Exraintestinal	[13]
Heterotis niloticus
Clinostomum complanatum Rudolphi, 1814	Intestine	*
Allocreadium sudanensisSaoud, Abdel-Hamid and Ibrahim, 1974	Intestine	[31]
Labeo spp.
Nemathobothrium labeonis McClelland, 1955	Eye orbit	[13, 68]
Gymnarchus niloticus
Acanthostomum gymnarchi Dollfus, 1950	Intestine	[58, 69]
Thaparotrema piscicola Odhner, 1902	Intestine	[64]

*Scholz, T. and de Chambrier, A.  two unpublished reports on their 2006 and 2008 freshwater fish parasitological expedition to Sudan.

 

 

 

It is apparent from Table 3 that:

Trematodes species were found parasitizing 16 fish species.

1. The following 11 trematodes were new species to science: Brevicaecum niloticum; Sandonia sudanensis; Orientocreadium lazeri; Aspidogaster africanus; Allocreadium sudanensis; Afrogyrodactylus girgifae; Quadriacanthus fornicatus; Quadriacanthus pravus; Quadriacanthus zuheiri; Quadriacanthus mandibulatus and Dogielius sennarensis.
2. Three Diplostomum were collected from Clarias gariepinus
3. Euclinostomum heterostomum, tilapiae, C. phalacoracis and Clinostomum spp. are of common occurrence in O. niloticus, S. galilaeus, S. schall and H. forskalii.
4. Clinostomum , Anguinicola sp. and Phyllodistomum sp. needs redescription to the species level.
5. Macrogyrodactylus polypteri was extensively studied compared with other trematodes.

 

Parasitic Cestodes

Some cestodes, collected by Dr. Franz Werner from freshwater fishes in the Sudan and North Uganda in 1905 were described by [74]. The collection made by C. M. Wenyon and A. J. Chalmers from the Sudan, was examined by [35, 36]. In 1925, Woodland reported on some new Monticellia like ‘Proteocephalus synodontis‘ and other cestodes from Sudanese Siluroids and also Marsypocephalus heterobranchus from H. bidorsalis. The fish cestodes collected by the Swedish Zoological Expedition to Egypt and the White Nile were examined by [75], who described Proteocephalus glanduligerus of Clarias anguilaris. The parasitological collection made by H. Sandon and S. El Marash and deposited at London School of Hygiene and Tropical Medicine, United Kingdom, was cautiously revised by [40]; who described from the intestine of H. niloticus, B. bajad and B. docmak a proteocephalidean tapeworm Proteocephalus sandoni n. sp. Lynadale, 1956. Some Proteocephalid cestodes from freshwater fishes mostly from around Khartoum were described by [77]. These were Proteocephalus sulcatus Klaptocz, 1906 from the intestine of Clarotes laticeps; Proteocephalus beauchampi Fuhrmann and Bare, 1925) from Chrysichthys sp. Synodontis schall was added as a new host for P. beauchampi by [5]. Other Proteocephalids collected by [77] included Corallobothrium solidum Fritsch, 1886 and Electrotaenia malopteruri Frisch, 1886 from Malapterurus electricus in addition [77] reported on a ProteocephaIid worm, M. heterobranchus Woodland, 1925 collected from the intestine of H. bidorsalis. A redescription of Proteocephalus glanduligerus from Clarias catfishes including material from Sudan and some African countries was made by [78]. According to [78] P. glanduligerus was described as Ichthyotaenia glanduligera by [75] from C. anguillaris from the Nile River in Cairo, Egypt. Proteocephalus sulcatus a poorly known parasite of C. laticeps was redescriped by [79] who added the following fish hosts Clarias anguillaris, C. gariepinus, C. laticeps, Polypterus endlicheri. A redescription of Proteocephalus synodontis Woodland, 1925 was made by [79]. The investigtors included taxonomically and phylogenetically important features for P. synodontis from S. schall (type species) from the Nile River in Khartoum (Type host) and added S. caudovittatus, S. eupterus, S. frontosus, S. nigrita, S. serratus, S. batensoda as a new host records from the Nile near Khartoum, Kosti Sinnar and Khashm el Girba was made by [79]

The genus Wenyonia was established by [37] to accommodate three new species from the River Nile at Khartoum, Sudan. These were Wenyonia virilis Woodland, 1923 (type-species) n. gen.; n. sp., from S. schall; Wenyonia acuminata Woodland, 1923 n.sp., from S. membranaceaus and Wenyonia minuta Woodland, 1923 n.sp., from C. auratus. Subsequent studies by [37] added Wenyonia species, new fish host and locality records. To the Wenyonia of Sudan, a Wenyonia sp. Woodland, 1923 was collected from the stomach and intestine of C. gariepinusand C. anguilaris from Khartoum by [5]. Wenyoniayoudeoweii Ukoli, 1972 were collected from S. frontosus and S. serratus by [27, 77]. Wenyonia synodontis Ukoli, 1972 was added by [27] and Wenyonia kainjii Ukoli, 1972 was added by [84]. Wenyonia virilis Woodland, 1923, were collected from S. schall by [5, 26] from Khartoum. Wenyonia virilis from Synodontis eupterus, S. frontosus, S. nigrita and S. schall from Khashm El Girba (Atbara River); from S. caudovittatus, S. nigrita and S. schall from Kostı (White Nile) and from S. schall from Sinnar (Blue Nile) were collected and described by [82].  Wenyonia virilis collection made by [27] was from Jebel Aulia, Um Shaba, Alkawa and Kosti on the White Nile and from Lake Roseries, Blue Nile. Wenyonia acuminata Woodland, 1923, were collected from C. gariepinus and S. schall (new fish hosts from Khartoum) by [5]. The prevalence and intensity of W.minuta Woodland, 1923 in S. frontosus from Khashm El Girba (Atbara River), in S. nigrita and S.schall from Kostı (White Nile) and in S. caudovittatus, S. serratus and S. schall Sinnar (Blue Nile) was studied by [82]. Wenyonia youdeoweii Ukoli, 1972 prevalence and intensity was studied from S. caudovittatus, S. schall and S. serrata from the White Nile (Kosti, Sudan) by [82].Wenyonia youdeoweii was also collected fromS. serrataand S. nigrita by [27] form same localities as W. virilis. Wenyonia synodontis Ukoli, 1972 was described from Synodontis nigrita and Synodontis serratus by [27] form the same localities of W. virilis. The contribution of [27, 77] to new fish host and locality records of Wenyonia of Sudan is clearly apparent. Wenyonia kainjii Ukoli, 1972 from Synodontis batensoda, S. caudovittatus, S. clarias, S. eupterus, S. frontosus, S. nigrita, S. schall was reported by [82] in their guide to the parasites of African freshwater fish.

From the collection made by Sandon and El Marash two cestodes: Lytocestus alestesi n. sp. Lynadale, 1956 from and Lytocestus filiformis Woodland, 1923 from Alestes sp., were described by [38].   On the basis of other Sudanese specimens (Table 4), [85] re-examined the original material of L. alestesi Lynsdale, 1956 and concluded that it should be considered as synonym of Lytocestus filiformis Woodland, 1923. The presence of L. filiformis in the type host was confirmed by [84]. Lytocestus longicollis Devi, 1973 an intestinal of C. gariepinus, S. schall, A. occidentalis and Auchenoglanisbiscutatus was recorded by [27].

A new genus, Sandonella Khalil, 1960 was described by [41]. On basis of additional morphological data, revision of the taxonomy of the genus and diagnostic character [41] erected a new subfamily Sandonellinae. Hemodified the key to the subfamilies of Proteocephalidae and erected a new genus, Sandonella, to accommodate sandoni species. The improved description of S. sandoni (an enigmatic and morphologically unique Cestode parasitic in the Osteoglossiform fish H. niloticus in Africa) by adding detailed rediscription of morphological characters based on scanning electron microscopy was made by [83]. The validity of the monotypic subfamily Sandonellinae and its placement in the Proteocephalidea by [83] has since been widely accepted.

Amirthalingamia Bray, 1974 a ng., was erected as new genus to replace Paradilepis by [43]. Amirthalingamia (=Paradilepis) macracantha, was redescribed, as a larval form from the liver and intestinal wall of O. niloticus and as an adult form fromPhalacrocorax carboa fish-eating bird, from the Green Belt, Sudan by [43]. According to [43], A. macracantha differs from other Dilepididae in having 20 large rostellar hooks of three sizes, in two rows, arranged in a bilaterally symmetrical pattern. Two other dilepidid larvae, believed to belong to the genera Paradilepis and Parvitaenia were also found in O. niloticus [43]. The Green Belt was demolished after construction on the new sewage treatment plant south of Khartoum.

From the parasites of tilapiasaround Khartoum Contracaecum larvae from the intestinal wall, Paraspidodera speciesfrom the rectum and Acanthosentis tilapia Baylis, 1948 were reported as first record for Sudan by [1], who found a proportional relation between the intensity of infection and the total length of the fish.

Twelve cestodes species from C. gariepinus, P. senegalus, S. schall and S. serratus were reported by [5]. These were Garyophyllaeus sp., Stocksia sp.(reported for the first time from the Sudan, W. virillis, W. acuminata, Wenyonia sp. Polyonchobothrium clarias, P. polypteri, Marsypocephalus recangulus, Proteocephalus beuchampi, P. pentantoma, P. synodontis, unidentified larval cestodes and a Proteocephalid cestode larva.  According to [5] Stocksia sp. is highly host specific as it has so far been found only in C. gariepinus.

Ahmed [6] examined O. niloticus and C. gariepinus collected from Jebel Aulia reservoir and the sewage treated water ponds South of Khartoum and reported Polyonchobithrium polypteri and Polyonchobithrium clarias in C. gariepinus from Lake Jebel Aulia.

A Cyclophyllidean cestode larva from the intestine of O. niloticus and W. virilis from the intestine of S. schall were added by [26] fom fish specimens collected from Al Kalakla Alqubba, 12km south of Khartoum White Nile.Since the publication of the checklist by [16], a number of new genera, new species, new fish hosts and new locality records from African freshwater fish including Sudan have been published (Tables 1 and 4).

Scholz and de Chambrier in 2006 and 2008 examined freshwater fishes from Khartoum (Nile), Kosti (White Nile), Sinnar (Blue Nile) and Khashm el Girbar (Atbara River) for their cestodes and nematodes. All parasites collected from outside Khartoum were new locality records. To the Sudan cestodes detailed redescription including electron microscopic studies were made for some species. Barsonella lafoni was added as a new genus and few species of Proteocephalidean from Clarias catfishes based on material from Wadi Halfa, Lake Nubia, Sudan and Tarkana Lake Kenya by [44].

Bothriocephalidean tapeworms (Cestoda) of freshwater fish in Africa including four species from Sudan were redescribed by [72]. Detailed description of I. ichthybori from I. besse based on 3 mature and 6 immature specimens from Kosti was made by [72]. A redescribtion of Kirstenella gordoni from H. biodorsalis from Kosti and Polyunchobothrium polypteri from A. occidentalis, P. senegalus and P. endlichheri from Kosti and P. bichir from Sinnar was due to [72]. Their description of Tetracampos ciliotheca was based on material collected from C. anguilaris from Khartoum, Al Kawa, Kosti and Sinnar as well as material collected from Clarias sp. from Khartoum, Lake Nubia and Sinnar. They added C. gariepinus and C. auratus as additional hosts. Based on material from Sudan and other African countries a key to the freshwater Bothriocephalideans larvae from Africa was set by [72]. As the type material of T. ciliotheca was not found, the specimen from Clarias sp. from Sinnar was designated as neotype and was deposited in IPCAS (No. C-466) by [72]. The presence of the cestode Monobothrioides tchadensis, from Auchenoglanis sp. from Kosti was listed by Scholz and de Chambrier in an unpublished report on their 2006 and 2008 freshwater fish parasitological expedition to Sudan. The findings of C. solidum Fritsch, 1886 and E. malapterui Fritsch, 1886 from the intestine of M. electricus and P. sulcatus Klaptocz, 1906 from C. laticeps were confirmed by [27, 67].

Several redescription of cestodes from freshwater fiishes of Sudan were made. Parasites rediscribed included Brevicaecum niloticumby by [73]; Acanthostomum gymnarchi, with notes on the genera. Acanthostomum,Atrophacaecum and Gymnajotrema and Haplocaecum Simha, [76], Protocephalid cestodes [77]; Proteocephalus glanduligerus from Clarias catfishes [78]; Proteocephalus sulcatus from Clarotes laticeps [79]; Tapeworms (Cestoda: Proteocephalidea) of Synodontis spp. [80]; Proteocephalus pentastoma and Polyonchobothrium polypteri from species of Polypterus [81] Wenyonia from catfishes [82]; the enigmatic and morphologically unique Sandonella sandoni from Heterotis niloticus [83]. The work of [74] and [75] is pioneer for parasites of freshwater fishes of Sudan.  The chapter on cestodes in the guide to the parasites of African freshwater fish by [84] and the systematic position of Caryophyllaeus fuhrmani and Lytocestus alestesi by [85] are of significance.

Scholz and de Chambrier in 2006 and 2008 confirmed from collection in Kosti area the presence of six cestodes from fish species. These were Wenyonia chalmersius and M. rectangulus in Clarias gariepinus which was reported by [5]; Polyonchobothrium polypteri in Polypterus sp.by [81] and in C. gariepinus by [6]; Corallobothrium solidum and Electrotaenia malopteruri in Malapterurus electricus and Marsypocephalus heterobranchu in Heterobranchus sp. which was reported by [77].

A detailed description of Cyclophyllidean sp.parasitizing the intestine of O. niloticus collected from the White Nile near Khartoum was made by [26]. A new genus, Ichthyologist (Cyclophyllidea: Dilepididae) was erected by [86] to accommodate Ichthyolepis africana n. sp., from Marcusenius macrolepidotus (type host) from South Africa. The new species parasitizes several freshwater Mormyridae including Mormyrus caschive, M. niloticus and Pollimyrus isodori in the Sudan [79]. According to [86] I. Africana represent a unique example of host switching of a tapeworm from birds to teleost fish in Africa and is the first cyclophyllidean tapeworm that sexually matures in teleost fishes.

Scholz and de Chambrier in 2006 and 2008 stuies showed that there is a need to carry out exhaustive morphological and taxonomic revision, DNA sequencing and re-descriptions of Proteocephalus sp. juv. (?P. synodontis) from Synodontis; Acanthostomum sp. from Bagrus spp.; Amphistomidae gen. sp. from Synodontis and Digenea gen. sp. from Synodontis; to verify their taxonomic status.

All cestodes of freshwater fish of Sudan were found in the intestine, except Amirthalingamiamacracantha, Paradilepis larva and Dilepidid larva which were found in liver and intestine of O. niloticus [43]; Cysticercus larva from the hepatopancreas of O. niloticus and S. galiliaeus by [1] and Wenyonia sp. which was found in the intestine and stomach of C. gariepinus by [5]. A summary of cestodes collected from freshwater fish of Sudan by different investigators were given in Table 4.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Table 4. Cestodes of freshwater fishes from Sudan
Parasites	References
Oreochromis niloticus
Amirthalingamia macracanthaBray, 1974	[43]
Paradilepis larva Hsü, 1935	[43]
Parvitaenia larva Burt,1940	[43]
Dilepidid larva Railliet and Henry, 1909	[1]
Polyonchobothrium clariai, Woodland, 1925	[6]
Polyunchobothrium polypteri Leydig, 1853	[6]
Cysticercus Larva  Gmelin, 1800	[1]
Cyclophyllidean sp. van Beneden in Braun, 1900	[26]
Sarotherodon galiliaeus
Polyonchobothrium clariai, Woodland, 1925	[6]
Polyunchobothrium polypteri  Leydig, 1853	[6]
Dilepidid larva Railliet and Henry, 1909	[1]
Cysticercus LarvaGmelin, 1800	[1]
Clarias gariepinus
Proteocephalus beauchampi  Fuhrmann and Baer, 1925	[13]
Proteocephalus glanduligerus Janicki, 1928	[77]
Polyonchobothrium polypteriLeydig, 1853	[6]
Bothriocephalus cuspidatus Cooper, 1917	[27]
Tetracampos ciliotheca Wedl. 1861	[72]
Polyunchobothrium clariai Woodland, 1925	[5, 6]
Polyunchobothrium polypteri Leydig, 1853	[5, 6, 83]
Marsypocphalus rectangulus Wedl, 1861	[5, 27, *]
Wenyonia  sp. Woodland, 1923	[5]
Wenyonia acuminate Woodland, 1923	[5]
Stocksia sp. Woodland, 1937	[5]
Lytocestus longicollis Devi, 1973	[27]
Clarias anguilaris
Proteocephalus glanduligerus Janicki, 1928	[72]
Polyonchobothrium clarias, Woodland, 1925	[5, 84]
Wenyonia  sp. Woodland, 1923	[5]
Monobothrioides chalmersius  Woodland, 1924	[84]
Clarias sp.
Barsonella lafoni de Chambrier, Scholz,  Beletew and Mariaux, 2009	[44]
Tetracampos ciliotheca Wedl. 1861	[72]
Polypterus senegalus
Proteocephalus pentastoma Klaptoaz, 1906	[5]
Polyunchobothrium polypteri Leydig, 1853	[5, 68, 83]
Polypterus bichir
Polyunchobothrium polypteri Leydig, 1853	[68, 83]
Proteocephalus pentastomus Klaptocz, 1906	[84]
Polypterus endlicheri
Polyunchobothrium polypteri Leydig, 1853	[68, 83]
Polypterus sp.
Proteocephalus pentastoma Klaptoaz, 1906	[81]
Polyonchobothrium polypteri Leydig, 1853	[81]
Synodontis schall
Wenyonia virilis Woodland, 1923	[5, 26, 35, 77]
Wenyonia acuminata Woodland, 1923	[5]
Proteocephalus synodontis Woodland, 1925	[5, 36, 76]
Proteocephalus beuchampi Fuhrmann and Baer, 1925	[5]
Lytocestus longicollis Devi, 1973	[27]
Synodontis caudovittatus
Proteocephalus synodontis  Woodland, 1925	[79]
Synodontis eupterus
Proteocephalus synodontis Woodland, 1925	[79]
Synodontis frontosus
Proteocephalus synodontis Woodland, 1925	[79]
Wenyonia virilis Woodland, 1923	[27]
Synodontis nigrita
Proteocephalus synodontis Woodland, 1925	[79]
Wenyonia synodontis Ukoli, 1972	[27]
Synodontis serratus
Proteocephalus synodontis Woodland, 1925	[79]
Wenyonia virilis Woodland, 1923	[27]
Wenyonia youdeoweii Ukoli, 1972	[27]
Spironoura sp. Leidy, 1856	[5, 45]
Synodontis membranaceus
Wenyonia acuminata Woodland, 1923	[35,  77]
Synodontis batensoda
Wenyonia kainjii Ukoli, 1972	[84]
Hydrocynus forskalii
Proteocephalus sp.  Weinland, 1858	[71]
Brycinusnurse
Lytocestus alestesi Lynadale, 1956	[40]
Lytocestus filotormis Woodland, 1923	[40]
Malapterurus electricus
Corallobothrium solidum Fritsch, 1886	[27, 73]
Electrotaenia malapteruri Fritsch, 1886	[27, 73]
Heterobranchus biodorsalis
Marsypocephalus heterobranchus Woodland, 1925	[27, 73]
Kirstenella gordoni Woodland, 1937	[72]
Heterotis niloticus
Proteocephalus sandoni  Lynsdale, 1960	[41]
Sandonella sandoni  Khalil, 1960	[39, *]
Clarotes laticeps
Proteocephalus sulcatus Klaptocz, 1906	[27, 73]
Chrysichthys auratus
Proteocephalus beauchampi Fuhrmann and Baer, 1925	[*]
Ichthyborus besse
Ichthybothrium ichthybori Khalil, 1971	[15, 68]
Auchenoglanis cf. acuticeps
Monobothrioides tchadensis Troncy, 1978	[*]
Proteocephalus synodontis Woodland, 1925	[79]
Auchenoglanis occidentalis
Lytocestus longicollis Devi, 1973	[27]
Polyunchobothrium polypteri Leydig, 1853	[72]
Auchenoglanisbiscutatus
Lytocestus longicollis Devi, 1973	[27]
Mormyrus caschive
Lytocestus filiformis Woodland, 1923	[72]
Ichthyolepis africana Scholz, Tavakol, Luus-Powell, 2020	[86]
Chrysichthys auratus
Wenyonia minuta Woodland, 1923	[35,  77]

*Scholz, T. and de Chambrier, A.  two unpublished reports on their 2006 and 2008 freshwater fish parasitological expedition to Sudan.

 

 

It is apparent from Table 4 that:

1. Forty-four Cestode species were found in 26 fish species.
2. Three Clarid catfish species were infected by 10 genera of cestodes 8 of which were identified to the species level.
3. Eight Mochidae harbour 12 species and one cestode identified at the genus level.
4. Proteocephalus synodontis were recorded from eight fish species.
5. Eight Proteocephalus sp were collected from 15 fish species.
6. 6. Lytocestus alestesi and Lytocestus filotormis were collected from Brycinusnurse.
7. Corallobothrium solidumand Electrotaenia malapterui from M. electricus seems to be host specific.
8. 8. Clarias harboured at least six parasitic species. Proteocephalidea is represented by nine species of parasites, with the genus Proteocephalus being represented by four species.
9. Barsonella lafoni a new genus and a new species was described from material collected from Africa including Wadi Halfa, Lake Nubia.

 

Parasitic Nematoda

Probably the first freshwater fish parasite recorded from Sudan was Dichelyne fossor described by [29] as a new genus (n. gen.); and new species) n. sp., nematode from Lates niloticus (type host) and from Bagrus bajad. More details on the nematodes collected from Egypt and the White Nile by the Swedish Zoological Expedition was given by [87]. From 1902 to 2020, 12 nematodes species were described from Sudan including n. gen. and/or n. sp in addition to seven nematodes identified to the genus level.

Cucullanus clarotis Baylis, 1923 was recorded from S. schall by [13] and from C. laticepsby [93]from Khartoum. A recent study on nematodes of Sudan and Ethiopia by [17] recorded and redescribed in detail Cucullanus baylisiCampana-Rouget, 1961. The material was collected from intestine ofSynodontis schall (Kosti White Nile) and Synodontis sp. (Sinnar, Blue Nile). Based on light and scanning electron microscope investigations, they revealed that Cucullanus baylisi was erroneously reported by [13, 71] as C.clarotis.Cucullanus baylisi was re-named ‘Cucullanus dubius nom. n.’ by [17] due to its poor and questionable description. It was designated as a species inquirenda by [17].

A new nematode species Nilonema gymnarchi n. sp [45] was described from the freshwater fish G. niloticus. The described species was a female collected from the lung-like air bladder.

Raphidascaroides bishaii Khalil, 1961 was described as a n. sp. from G. niloticus, by [46].

Falcaustra sudanensis from Distichodus brevipinnis(from Khartoum, White Nile) and Spironoura hexapapillata fromDistichodus nefasch(from Kosti, White Nile) were described in 1962 by [47] as two new nematode species to science from Sudan. Falcaustrasudanensis was collected from the intestine of D. brevipnnis by [47]. Its presence in D. brevipnnis and from D. niloticus was confirmed by [26]. A redescription of F. sudanensis in 2017 by [17] led to modification of its valid name to read Spironoura sudanensis.Spironoura hexapapillata Khalil, 1962 was restudied from its type host and type locality by [17]. The authors concluded thatFalcaustra hexapapillata Khalil, 1962 is a senior to [syns. Spironoura hexapapillata Khalil, 1962]. Spironura sp. Leidy, 1856was collected from the intestine of Synodontis batensoda,D. brevipennis and Distichodus sp [13] andfromthe intestine of S. schall by [5, 13].

Diplostomulum tregenna Nazmi Gohor, 1932 from the Nile fish C. gariepinus was described from the fat tissue in the cranial cavity by [36] who experimentally demonstrated part of its life cycle. Cithariniella citharini Khalil, 1963 was described as n. gen. and n. sp., of oxyurid from a freshwater fish, C. citharus in the Sudan [48]. The material was collected from the rectum of several specimens of C. citharus. Cithariniella citharini was the only Pharyngodonidae from Sudan freshwater fishes [48].Distichodus brevipinnis, S. schall and S. serratus were added by [91] as additional hosts for Citharinus from Sudan. Philometra bagrin. sp. Khalil, 1969 was collected from the subcutaneous tissue of B. bajad by [13].

Procamallanus laeviconchus Wedl, 1861 [Syn. Cucullanuslaeviconchus Wedl, 1861] was collected from the esophagus, stomach, intestine and gill lamellae of C. gariepinus by [13]; from S. schall by [5, 26, 17]; from S. serratus Sy [5] and from B. bajad, B. docmak, D. niloticus, D. brevipennis, from H.forskalii by [26] and from Schilbe intermedius by [17]. All these fish hosts were collected from the White Nile near Khartoum, Sudan. Procamallanus icyathopharynx Wedl, 1862 was found in the esophagus, stomach, intestine and gill lamellae of C. gariepinus by [13]. A new species to science, Procamallanus (=Spirocamallanus) pseudospiralisMoravec and Scholz, 2017 was collected from the intestine of S. schall (type host) from River Nile in Khartoum (type locality) by [17]. An additional locality was Khashm el Girba, Dam Lake. Other hosts were S. frontosus and S. nigrita. A Key to Procamallanus spp. parasitic in freshwater fishes in Africa was included. From the intestine and stomach of S. schall [92] described three Procamallanus Olsen, 1952 and designated them asProcamallanus type 1, 2 and 3.

Procamallanus spiralis Baylis, 1923 was collected from the intestine of Clarias anguillaris, Auchincglanis occidentalis, S. schall and S. batensoda by [13]; from the stomach and intestine of S. schall by [5, 13, 26]; from S. serratus by [5] and from B. docmak by [26].

Cucullanus barbi n. sp. Baylis, 1923 was redescribed from Labeobarbus binnyi from Khartoum by[93]. It was rediscribed from the types host collected from White Nile in Kostí and Blue Nile in Sinnar, Sudan by [17].

An adult nematode Gendrid tilapiae Baylis, 1930 was reported for the first time in Sudan from the rectum of a single specimen of O. niloticus by [1] who also described Acanthosentis tilapiae Bolyis, 1948 from the intestine of O. niloticus and S. galilaeus. Amphicaecum sp. Baylis, 1920 was collected from mesenteries surface of stomach and intestine, and from sinus venosus of O. niloticus by [13, 26]; from C. gariepinus by [6]; from L. niloticus by [92]; and from B. bajad, H. forskalii, L. niloticus and S. mystus by [26].

Contracaecum sp. Reilliet and Henary, 1912 was collected from the intestine and sinus venosus of O. niloticus by [1, 26, 87, 88]; from S. galilaeus by [1, 89]; from C. zillii by [90]; from the visceral cavity and stomach wall of C. gariepinus by [5, 6] from P. senegalus by [5] and from B. bajad, H. forskalii, L. niloticus,and Schilbe mystus by [26].An in vitro experiments made by [89] demonstrated part of the life cycle of Contracaecum sp., and revealed that molting in small larval nematodes takes 2 to 3 days.

Rhabdochona sp.  Raillet, 1916 was collected from the intestine of G. niloticus by [89] and from H. forskalii by [26]. Metaquimperia sp, Karve, 1941 was collected from the stomach of P. senegalus by [5]. Porrocaecum sp. Railliet and Henry, 1912 was collected from the intestine of O. niloticus and L. niloticus by [92].

A new species of nematode, Cucullanus mormyri sp. n. Moravec et Scholz, 2017 was collected from the intestine of M. caschive (Type host) from Kosti on the White Nile (type locality); other hosts were a Mormyrus sp. and Marcusenius cyprinoides (both belong to Mormyridae) [17].

From the sinus venosus of O. niloticus, S. galilaeus and C. zillii larvae of Amplicaecum Baylis, 1920 were collected by [13] who designated them as Amplicaecum type 1 and Amplicaecum type 2.

Cucullanus sp. Muller, 1877 was collected from the intestine, occasionally gill lamellae of S. schall by [5, 26], from L. bynni by [26] and from the intestine of S.serratus by [5]. Dujardinascaris malapteruri Baylis, 1923 was collected from Malapterurus electricus by [91].

Other nematodes collected and described by [17]were:

1. Falcaustra similisMoravec et Van As, 2004 was collected from frontosus, S. serratus (Sinnar, Blue Nile), S. frontosus, S. nigrita, S. schall (Khashm el Girba).
2. Falcaustra guiersiVassiliadès, 1973 (considered a junior synonym of hexapapillata Khalil, 1962) was collected from D. brevipinnis and D. nefasch.
3. Cithariniella khalili Petter, Vassiliades et Troncy, 1972 was collected from the intestine of membranaceus andS. serratus from White Nile River in Kostí and Blue Nile in Sinnar.
4. Multicaecum heterotisPetter, Vassiliades and Marchand, 1979 was collected and rediscribed from the intestine of niloticus (type host) from Khartoum and Kosti.
5. Camallanus longicaudatus Moravec, 1973 was collected and rediscribed from the intestine of Labeo niloticus from Nile River niloticus from Khartoum.
6. Paracamallanus cyathopharynx Baylis, 1923 from gariepinus (type host) was collected from the intestine of Clarias sp. from Sinnar (Blue Nile).
7. To the larval nematodes [17] added: Records of Contracaecum Third stage-larvae Type 2 of Moravec et al. 1993 from the body cavity of B. nurse, C. gariepinus, Clarias sp. and O. niloticus (River Nile in Khartoum) and B. nurse in Khashm el Girba Dam Lake. Both B. nurseand C. gariepinus are new host and ranges for Contracaecum sp. Third stage-larvae Type 2. The body length of third stage-larvae Type 2 was about 10 mm from B. nurse and about 30–50 mm from O. niloticus.
8. Capillariidae sp Raillet, 1815 was collected from the intestine of Auchenoglanis sp. from Kosti. The collection was a single gravid female nematode.
9. Spinitectus polli Campana-Rouget, 1961 was collected from the intestine of schall from Khartoum.

The nematodes of freshwater fishes encountered so far from Sudan, were given in Table 5.

 

 

 

Table 5. Nematode of freshwater fishes from Sudan
Parasites	Infected organ / tissue	References
Oreochromis niloticus
Gendrid tilapiae Baylis, 1930	Rectum	[1]
Acanthosentis tilapiae Bolyis, 1948	Intestine	[1]
Contracaecum sp. Reilliet and Henary, 1912	Mesenteries of stomach and intestine, sinus venosus	[1, 26, 87, 88]
Amphicaecum sp. Baylis, 1920	Mesenteries of stomach and intestine, sinus venosus	[13, 26]
Porrocaecum sp. Railliet and Henry, 1912	Intestine	[92]
Sarotherodon galilaeus
Acanthosentis tilapiae Bolyis, 1948	Intestine	[1]
Contracaecum sp.  Reilliet and Henary, 1912	Intestine, sinus venosus	[1, 89]
Coptodon  zillii
Contracaecum sp.Reilliet and Henary, 1912	Sinus venosus	[90]
Clarias gariepinus
Procamallanus laeviconchus Wedl,1861	Esophagus, stomach, intestine and gill lamellae	[13]
Procamallanus icyathopharynx Wedl, 1861	Esophagus, stomach, intestine and gill lamellae	[13]
Amphicaecum sp. Baylis, 1920	Intestine	[6]
Contracaecum sp. Reilliet and Henary, 1912	Visceral cavity, stomach wall	[5 , 6]
Clarias anguillaris
Procamallanus  spiralis Baylis, 1923	Intestine	[13]
Clarias sp.
Procamallanus  spiralis Baylis, 1923		[13]
Synodontis schall
Procamallanus  spiralis Baylis, 1923	Stomach, intestine	[5, 13, 26]
Cucullanus sp. Mueller, 1877	Intestine, Gill lamellae	[5, 26]
Procamallanus laeviconchus Wedl, 1861	Esophagus,  stomach,  gill lamellae	[5, 26]
Procamallanus type 1	Intestine and stomach	[92]
Procamallanus type 2	Intestine and stomach	[92]
Procamallanus type 3	Intestine and stomach	[92]
Spironoura sp. Leidy, 1856	Intestine	[5, 13]
Cucullanus clarotis Baylis, 1923	Intestine	[13**, 71]
Synodontis batensoda
Procamallanus  spiralis Baylis, 1923	Intestine	[13]
Spironoura sp. Leidy, 1856	Intestine	[13]
Synodontis serratus
Procamallanus laeviconchus Wedl, 1861	Stomach	[5]
Procamallanus  spiralis Baylis, 1923	Intestine	[5]
Cucullanus sp. Muller, 1877	Intestine	[5]
Synodontis frontosus
Falcaustra similisMoravec et Van As, 2004		[17]
Synodontis membranaceus
Cithariniella khalili Petter, Vassiliadès et Troncy, 1972		[17]
Labeobarbus bjnni
Cucullanus brati Baylis, 1923		[93]
Cucullanus sp. Muller, 1877	Intestine occasionally Gill lamellae	[26]
Distichodus brevipinnis
Spironoura sudanensis Khalil, 1962	Intestine	[26, 45]
Falcaustra guiersiVassiliadès, 1973		[17]
Spironoura sp. Leidy, 1856	Intestine.	[13]
Distichodus niloticus
Spironoura sudanensis Khalil, 1962	Intestine	[26]
Procamallanus laveiconchus Wedl (1862)	Esophagus, stomach, intestine	[26]
Spironoura sp. Leidy, 1856	Intestine.	[13]
Citharinus citharus
Cithariniella citharini Khalil, 1963	Intestine	[48]
Polypterus senegalus
Metaquimperia sp. Karve, 1941	Stomach	[5]
Contracaecum sp. Reilliet and Henary, 1912	Visceral cavity, stomach wall	[5]
Bagrus docmak
Procamallanus  spiralis Baylis, 1923	Stomach and intestine	[26]
Procamallanus laeviconchus Wedl (1862)	Stomach	[26]
Bagrus bajad
Amphicaecum sp. Baylis, 1920	Mesenteries, surfaces of stomach and intestine, sinus venosus	[26]
Procamallanus laeviconchus Wedl,1862	only larvae in the  esophagus, stomach, and intestine	[26]
Philometra bagriKhalil, 1969	Subcutaneous tissue	[13]
Thwaite Bagri Khalil, 1965		[95]
Hydrocynus forskalii
Procamallanus laeviconchus Wedl, 1861	Gill lamellae	[26]
Amphicaecum sp. Baylis, 1920	Mesenteries of stomach and intestine, sinus venosus	[26]
Contracaecum sp. Reilliet and Henary, 1912	Mesenteries of stomach and intestine, sinus venosus	[26]
Rhabdochona sp.	Intestine	[26]
Lates niloticus
Contracaecum sp. Reilliet and Henary, 1912	Mesenteries of stomach and intestine, sinus venosus	[26]
Amphicaecum sp. Baylis, 1920	Mesenteries of stomach and intestine, sinus venosus	[26]
Schilbe mystus
Amphicaecum sp. Baylis, 1920	Mesenteries of stomach and intestine, sinus venosus	[26]
Gymnarchus niloticus
Nilonema gymnarchi Khalil, 1960	Swim bladder	[45]
Rhabdochona sp,		[89]
Labeo niloticus
Amphicaecum sp.Baylis, 1920	Intestine	[92]
Porrocaecum sp.	Intestine	[92]
Auchincglanis occidentalis
Procamallanus  spiralis Baylis, 1923	Intestine	[13]
Malapterurus electricus
Dujardinascaris malapteruri Baylis, 1923		[91]

 

** According to [17]Cucullanus clarotis was erroneously named by [13, 93]. Its correct name is Cucullanus baylisi.

 

 

From Table 5 it is apparent that:

1. The nematode laeviconchus seems to have no preference to a specific host.
2. Omer (1999) studied the parasites of niloticus from Khartoum, recorded their prevalence rate and concluded that no histological evidence of ill-effect.
3. To the nematodes of Sudan 12 adult and two larval belonging to the Ascaridoidea, Camallanoidea, Cosmocercoidea, Habronematoidea, Oxyuroidea, Seuratoidea and TT
4. The findings of [17] represented several new host and geographical records for example sudanensisfromD. brevipennis and D. niloticus was collected from Khartoum and C. barbi from Kosti (White Nile) and Sinnar (Blue Nile).
5. Scholz and de Chambrier in 2006 and 2008 confirmed from Clarias collected from Kosti the presence of Procamallanus spiralis previously reported from Khartoum from Clarias gariepinus by [13]; from S. schallS. schall and Synodontis sirratus by [5] and by [26] from B. docmak.

 

Parasitic Crustacea

Parasitic Copepodsof freshwater fishes of Sudan received very little attention. Lemaea laphiara Harding, 1950, Opistholemaea laterobrachialis nilotica Fryer, 1965 and Lamprogiena mondi Caport, 1944 were recorded by [1] from gill lamellae, fins and scales of O. niloticus and S. galilaeus as first record to Sudan. In 1986 [5] added Lemaea haphocephala (Cunnuhngton, 1914) from the skin around anal finof P. senegalus. The ecto-parasites Lamproglena mondi, Capart, 1944 from O. niloticus; Lamproglena sp. von Nordmann, 1832 from H. forskalii and Ergasilus sp. von Nordmann, 1832 from the gill lamellae of B. bayad and B. docmak were collected by [26] who found an overall prevalence rate of 18.6%. A recent study by [96] reported the occurrence of five crustaceans from freshwaterfishes of Sudan. These were Dysphorus torquatus Kurtz, 1924 from H. niloticus; Lamproglena elongata Capart, 1956 from C. citharus, Lernaeocera werneri Kurtz, 1922 from C. gariepinus, D. nefasch, M. electricus; Lernaeocera senegali Zimmermann, 1922 from P. senegalus and Ergasilus nodosus Wilson, 1924 from B. bajad.

 

Acanthocephala parasites

According to [13] Acanthocephala found in the Sudan were Tenuisentis niloticus Meyer, 1932 from H. niloticus, Neoechinorhynchus sp. (Günther, 1864) in C. citharus and 2–5 unidentified acanthocephala in S. batensoda. In a subsequent study [76] addedAcanthostomum abscoditumLooss, 1901andAcanthostomum spinicepsLooss, 1901 from B. bajad and B. docmak and Acanthostomum gymnarchiDollfus, 1950 from G. niloticus. The first record of Polyacanthorhynchus kenyensis Schmidit and Canaris, 1967 in Sudan from the kidney of O. niloticus was made by [97]. According to [97] this spiny-headed worm added to the list of faunal similarities between Africa and South America. Neochinorhynchus ichthyoboriSaoud, El-Naffar and Abu-Sinna, 1974 was described as a new species by [49] from the intestine of I. besse. They stated that it is the first species of the genus Neochinorhynchus to be recorded from Africa. Neochinorhynchus ichthyoboridiffers from the 6 other species of the genus in trunk length, in the measurements of the proboscis, its hooks, the lemnisci, and in lacking sexual dimorphism [49].Three species of Polyacanthorhynchus are parasitic of caiman in South America and their occurrence in Crocodylus niloticus, Varanus niloticus and/or Trionyx spp., as definite host in Sudan should not be excluded [97]. Acanthogyrus (=Acanthosentis) tilapiae Baylis, 1948 was found in the intestine of O. niloticus and S. galilaeus by [1, 26].  Their occurrence in both species probably represent a case of co-evolution and multiple infections at the same time.From O. niloticus [94] identified an Acanthogyrus sp., while from Labeo niloticus,[92] found an Acanthocephala sp.

 

Conclusions

A couple thousand of freshwater fish specimens were examined for their ecto-parasites and/or end-parasites. Fifty-eight fish species were reported infected and 162 parasitic species including 32 new species were collected. These were three bacterial and three fungal species collected from O. niloticus. From 10 species of fish, 19 protozoans were described. From 10 species of fish, 22 Monogenean species were found including 7 new species. One new Aspidogastrean species was collected from Labeobarbus bynni. From 29 fish species 23 Digeneans species were collected including five new ones. From 41 species of fish, 44 species of cestods parasites were collected including 11 species new to science. Twenty parasitic Nematodes species including seven new ones were collected from 32 fish species. From 12 fish species 9 Crustacean were described. Nine Acanthocephalans including one new species from Ichthyborus besse were collected from 11 fish species (Appendix 1).

One new subfamily Sandonellinae from Heterotis niloticus was erected; and 10 new genera, Brevicaecum, Sandonia, Afromacroderoides (Digenia); Wenyonia, Sandonella, Amirthalingamia, Barsonella lafoni (Cestoda) and Dichelyne, Nilonema, (Nematoda) were described. Revision of Trypanosoma species type 1, 2, 3 [25]; Dactylogyrus species type 1, 2, 3, 4, 5; Dogielius sp. 1 [23]; Amplicaecum type 1 and Amplicaecum type 2 [13]; Contracaecum sp. Third stage-larvae Type 2 [17],Procamallanus type 1, 2, 3 [92] and those parasites identified to the genus level shouds be given due attention.

Scholz and de Chambrier in 2006 and 2008 study showed that there is a need to carry out exhaustive morphological and taxonomic revision, DNA sequencing and re-descriptions of Nematoda gen. sp. 1 from Distichodus; Nematoda gen. sp. 2 from H. niloticus to verify their taxonomic status.This notion carried out forward the subsequent studies made by the Institute of Parasitology, Biology Centre of the CAS, the Department of Botany and Zoology, Faculty of Science, Masaryk University, Czech Republic and Sudan Institute of Natural Sciences which led to description of one new genus and 10 new parasitic species and more material are yet in the verification tube.

Many parasites of freshwater fish described in Ethiopia and Egypt [100, 101, 102, 103, 104, 105] are likely to be found in Sudan. An example is Bothriocephalus acheilognathi Yamaguti, 1934 (a Bothriocephalidean tapeworms, Cestoda) reported by [72] from both countries.

Despite the extensive surveys made by [27] at Jebel Aulia, Um Shaba, Alkawa and Kosti on the White Nile and from Lake Roseries no digenias, cestodes, nematodes, crustaceans and acanthocepha parasites were found in B. bayad, B. docmak and C. auratus (see appendix 1). The negative findings by [27] might be a matter of chance but probing the presence of an antibody complement system secreted into the intestine to prevent the establishment of parasites should be investigated.

Several parasites species were recorded from same fish genus probably indicating a co-evolution of the fish genus and the parasites genus. Examples included Acanthostomum abscoditum and Acanthostomum spiniceps reported from Bagrus bayad and Bagrus docmak by [76]. Spironoura sudanensis from D. niloticus and D. brevipennis [26]. Proteocephalus synodontis from Synodontis eupterus, S. frontosus, S. nigrita and S. serratus [27, 76]. The trematode Macrogyrodactylus polypteri from Polypterns senegalus [5, 18, 19, 20] and P. bichir [21].

A guide to the parasites of African freshwater fish [98]; a systematic survey of the Monogenea parasites of freshwater fishes in Africa [66] and Parasitic crustaceans of African freshwater fishes from the Nile and Niger systems [99] beside this review are milestone for future research in freshwater fish parasitology.

The review showed that there is a need to launch a genuine international project with multi-nations team to study in details the parasites of fishes of Sudan from the Nile and non-Nilotic inland water bodies. Such project is expected to cover:

1. The fish parasites of freshwater fishes of Sudan, their description and systematics.
2. Establishment of life cycles of each parasite especially those infecting commercial fishes.
3. Host-parasite relationship, correlation between parasites and the health status of fish and their histopathological consequences.
4. The impact of single or multiple infections by parasitic species on fish species reared in earthen ponds, floating cages and/or pen culture.
5. The fish parasites of Dinder River and Rahad River is an area of interest because both rivers belong to Nilo- Sudanic and highland East African fish regions.
6. The role of piscvorous birds in diversity of fish parasites.
7. Capacity development by enhancing research facilities, promoting technician skills, and avail scholarships for postgraduate students.

 

Acknowledgement

The senior author is grateful for Prof. Dia el Din Ahmed Elnaiem who introduced him to Prof. Tomas Scholz of the Institute of Parasitology CAS CR, Czech Republic and to Dr. Alain de Chambrier of the Natural History Museum, Geneva, Switzerland.

 

References

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Annex 1.  Parasites infecting different freshwater fish species in Sudan.

Fish  species	Bacteria	fungi	Protozoa	Monogenea	Aspido- Gastrea	Digenea	Cestoda	Nematoda	Crustacea	Acantho- cephala
Polypterns senegalus				√		√	√	√	√
Polypterus bichir				√		√	√
Polypterus endlicheri						√	√
Polypterus sp.			√				√
Heterotis niloticus						√	√		√	√
Gymnarchus niloticus						√		√
Mormyrus caschive							√	√
Mormyrus niloticus							√
Mormyrus sp.								√
Marcusenius macrolepidotus							√
Marcusenius cyprinoides								√
Pollimyrus isodori							√
Labeobarbus bynni			√		√	√	√	√
Labeo niloticus				√		√	√	√		√
Labeo horie				√		√
Labeo coubie						√
Labeo senegalensis						√
Labeo sp.						√
Distichodus nefasch						√		√	√
Distichodus brevipinnis								√
Distichodus niloticus							√	√
Distichodus rostratus						√
Ichthyborus besse							√			√
Citharinus citharus				√		√		√	√	√
Brycinus nurse				√			√
Hydrocynus forskalii						√	√	√	√
Bagrus bajad			√			√	√	√	√	√
Bagrus docmak				√		√	√	√	√	√
Auchenoglaris occidentalis						√	√	√	√
Auchenoglanis acuticeps							√
Auchenoglanis biscutatus							√
Auchenoglanis sp.							√
Chrysichthys auratus			√				√
Chrysichthys sp.							√
Clarotes laticeps							√	√
Schilbe mystus							√	√
Schilbe intermedius								√
Clarias gariepinus			√	√		√	√	√	√	√
Clarias anguilaris							√	√
Clarias sp.							√	√
Heterobranchus bidorsalis				√			√
Synodontis schall			√			√	√	√
Synodontis batensoda						√	√	√		√
Synodontis clarias						√
Synodontis caudovittata							√
Synodontis frontosus							√	√
Synodontis membranaceus						√	√	√
Synodontis nigrita						√	√	√
Synodontis serratus							√	√
Synodontis sorex						√
Synodontis eupterus							√
Synodontis sp.						√	√
Malapterurus electricus							√	√	√
Lates niloticus								√
Parachanna obscura			√			√				√
Oreochromis niloticus	√	√	√			√	√	√	√	√
Sartherodon galilaeus			√			√	√	√	√	√
Coptodon zillii			√					√
No. of  infected fish species= 58	1	1	10	9	1	29	41	32	12	11
No. of parasite species=162	3	3	10	22	1	23	44	20	9	9
No. of new parasite species=32	0	0	0	7	1	5	11	7	0	1

6 Freshwater Fishes

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