Applied Tropical Agriculture Volume 22, No. 2, 52-62, 2017. © A publication of the School of Agriculture and Agricultural Technology, The Federal University of Technology, Akure, Nigeria.

Parasites of Three Economically Important Fishes ( Ethmalosa fimbriata , Chrysichthys nigrodigitatus and Sarotherodon melanotheron ) from Lagos Lagoon, Southwestern Nigeria

Emmanuel, B.E.* and Aromodiu, H.A.W.

Department of Marine Sciences, Faculty of Science, University of Lagos, Akoka Yaba, Lagos, Nigeria *Corresponding author: [email protected]; [email protected]

ABSTRACT

Parasites in three economically important fishes (Ethmalosa fimbriata, Chrysichthys nigrodigitatus and Sarotherodon melanotheron) from Lagos Lagoon were studied between March and August, 2015. Out of 90 specimens analyzed, a total of 41 (45.6%) specimens were infected with parasites having a total parasite count of 735. Glochida accounted for the most abundant parasite in the gills and skin of C. nigrodigitatus having a prevalence of 43.81%, Ergasilus sp. had the least amount of prevalence with 0.41%, Gyrodactylus had a prevalence of 6.80%, Neobenedenia had a prevalence level of 0.95%. Larvae forms of Eustrongylides from S. melanotheron had a prevalence level of 4.08% while Piscinodinium which was identified from the gills of both S. melanotheron and E. fimbriata had a prevalence level of 41.36%, an unidentified worm had a prevalence of 2.59%. Human beings who consumed raw or under - cooked fish that are infected with larval stages of Eustrongylides have experienced gastritis or inflammation of the stomach and intestinal perforation requiring surgical removal of worms.

Key words : Parasite, fish, gill, skin, under - cooked, gastritis intestinal perforation

INTRODUCTION

Fishes are important to man as they serve as a good source fecundity reduction (Nmor et al.,2004) and mechanical of animal protein for both man and livestock. It also serves injuries depending on the parasite species and load (Echi et as a source of income in Nigeria and other countries in sub- al., 2009a, b). Fish is the most parasitized vertebrate and the Saharan Africa where some 35 million people depend presence of parasite is detrimental to fish population which wholly or partly on the fisheries sector for their livelihood may cause high mortality, weight loss and reduced (FAO, 1996). fecundity on both farmed and wild fish species especially Many diseases found in fish are closely linked to in waters contaminated with industrial and urban pollutants environmental degradation and stress; once the (Ramollo, 2008). In instances where host are overcrowded environment is disturbed the organisms too become such as in aquaria’s and fish ponds, parasitic disease can stressed (SEAFDEC, 1999). Parasitism, according to spread very rapidly causing large mortalities (Parpena, Marcogliese (2002) reflects a life style whereby one or 1996) while in natural systems they may threaten the more individual organisms (the parasites) live in close abundance and diversity of indigenous fish species obligate association in or on another (the host) and derives (Mashego, 2001). nutritional benefits at the host’s expense, usually without Parasites can be divided into micro-parasites and killing the host. Parasites are a major concern to freshwater macroparasites on the basis of size, the micro-parasites and marine fishes all over the world, and of particular include viruses, bacteria, fungi, protozoans, micro- importance in the tropics (Iyaji and Eyo, 2008; Bichi and sporidians and mixozoans. Surveys for microparasites in Dawaki, 2010; Ekanem et al., 2011). They constitute a fish hosts, most often consider only protozoans major limiting factor to the growth of farmed fish in Nigeria (Marcogliese, 2002). Macro-parasites are multicellular (Bichi and Yelwa, 2010). The effects of parasites on fish organisms mainly comprised of the helminthes and include nutrient devaluation (Hassan et al., 2010); arthropods. Furthermore, parasites can also be divided into alteration of biology and behaviour (Lafferty, 2008); ecto-parasites and endo-parasites on the basis of their lowering of immune capability, induction of blindness location in the fish’s body. Ecto-parasites are those found (Echi et al., 2009 a, b); morbidity, mortality, growth and on the external surfaces such as skin or gills while endo-

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Parasite in fishes from Lagos lagoon parasites are those housed within internal organs or cavities year with 64% prevalence. The pericardium inhabiting of a host (Marcogliese, 2002). Klinger and Floyd (2002) , Contracaecum sp, Amplicaecum sp and noted common parasites of fishes to include: Protozoans Eustrongylides sp were most prevalent in freshwater fish (Ciliates, Flagellates, Myxozoa, Microsporidia, Coccidia), hosts. Nematode parasite, Procamallanus laevionchus was monogenean trematodes, digenean trematodes, found with highest prevalence of 62.2% in S. schall at rivers or roundworms ( Camallanus, Capileria, Eustrongylides ), Niger and Benue confluence (Iyaji, 2011). Cestodes or tapeworms, acanthocephalans or thorny headed worms, parasitic crustaceans ( Ergasilus, Lernaea, Argulus ) Elsewhere, Raissy et al . (2008) reported the presence of and leeches . It is usually known that external parasite spiralis in the gills of Cyprinus carpio in Iran. constitutes the largest group of pathogenic parasites in The microsporidean Plistophora sp infections of warm water fishes. Parasite infection of the body cavity and Haplochromis angustifrons and H. elegans in Lake George the musculature of fishes have been reported as presenting had very low prevalence of less than 1% out of 302 fish marketing problems for commercially exploited species examined from both sexes (Paperna, 1973). Infections by (Petersen et al., 1993). For instance, heavy infestation of Nosemoides tilapia in Tilapia zilli, T. guinensis and the Alaska Pollack ( Theragra chalcogramme) with Sarotheradon melanotheron were common in Lake Nakoue pleroceroid of Nybelinia surmenicola has reduced the and Porto Novo lagoon with prevalence of 13-30% (Sakiti consumable part of the fish to the dorsal musculature and Bouix, 1987). The visceral myxobolus infections of (Grabda, 1970). Similarly, infestation with plerocerocoids Oreochromis sp in East African lakes were quite high of Gymnorlynchus thyrsitae has seriously affected the (prevalence 89-100%) while in Haplochromis sp they were exploitation of the highly valued Thyrsite atun in New only rarely above 25% (FAO, 1996). Prevalence of skin and Zealand (Mehl, 1970). gill infections of Myxobolus sp was very low (Paperna, 1973). Prevalence of Henneguya sp infecting Clarias The Piscinodinium pillulare recorded in this study causes a gariepinus of Okavanga River and the Delta in Botswana condition known as disease in which it coats the gills were also generally low, 14.3% in the cartilage of the of the infected fish and heavy infestation is known to cause accessory breathing organ and primary gill lamallea (Reed mass mortalities as reported by Kunz and Pung (2004) . et al ., 2003). Kostoingue et al ., (2001) reported primary gill Other effects of parasite on fish include muscle lamellae infections of Henneguya sp and their prevalence degeneration, liver dysfunction, interference with nutrition, in the following fish genera: Auchinoglanus occidentalis ; cardiac disruption, nervous system impairment, castration Citharinus citherus ; Mormyrus cashive ; Lates niloticus ; or mechanical interference with spawning, weight loss and Clarias auguilaris with prevalences of 36.8% (21/57) gross distortion of the body (Kunz and Pung, 2004). Other 25.8% (16/32) 13.3% (12/90) 4.4% (3/63) and 9.1% (4/44) severe pathological disorders reported by Bauer (1959); respectively from freshwater ecosystem of Chad, Central Sweeting (1977); Mitchell and Hoffman (1980) include Africa. Henneguya chrysichthyi gill infection in C. inflammation and atrophy of the viscera, resulting from nigrodigitatus had a prevalence of 37% (Obiekezie et al ., compression and displacement of organs by the parasites, 1988) with the highest intensity of infection in the 21-30 often together with accumulation of blood stained ascetic cm class, corresponding to fish in their second year fluid. (Ezenwa and Ikusemiju, 1981). Among the heminths, Obiekezie et al . (1988) found the A review from Nigeria indicated that freshwater fish monogenean Protancylodiscoides chysichthes occurred parasites belong to protozoans, trematode, nematode, throughout the year on the gills of the fish with monthly cestode, acanthocephalan, copepod and hirudinea groups prevalence of infection consistently above 70% (Except in (Iyaji and Eyo, 2008). Okaeme and Ibiwoye (1988) August) and low mean intensity during heavy rain months revealed that the protozoans constitute an important (July - Oct). Data on cestode infestations of fish are mostly economic disease of catfishes in Lake Kainji area in from wild fish species (FAO, 1996). Nigeria. Ibiwoye et al . (2006) reported the prevalence rate of 22.5, 76.25 and 1.25% for gastro-intestinal parasites, Despite all these reports, very little is known about the Procamallanus laevionchus and Sprironoura petriea parasitic infestation and prevalence in Ethmalosa fimbriata , (Nematodes), Polyonchobothrium clariae (Cestode) and Chrysicththys nigrodigitaus and Sarotherodon Clinostomum clarias (Trematode) in Clarias anguillaris in melanothron in Lagos lagoon . The aim of this study is Onitsha area along River Niger. Nyaku et al . (2007) also provide information on the types and relative abundance of reported the occurrence of platyhelminthes parasites as the several parasitic species found in three brackish water fish most common ectoparasites of three species of fish families of economic importance ( E. fimbriata, C. (Oreochromis niloticus, Auchenoglanis occidentalis and nigrodigitatus, S. melanotheron ) in Lagos lagoon and the Bagrus bayad ) in River Benue, Nigeria. Obiekezie et al . effects of these parasites on the survival of these species in (1988) recorded infections with larval stage of nematode the lagoon. Hysterothylacium sp of C nigrodigitatus throughout the -----53

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MATERIALS AND METHODS Laboratory analysis of fish samples Determination of Morphometric Characteristics Description of study site In the laboratory, the total length (TL) and standard length The Lagos lagoon shares its name with the city of Lagos, (SL) of each individual fish was measured in centimeters Nigeria . The Lagoon (Fig 1) lies between longitudes 30 20’ (cm) using a fish measuring board. The weight of each and 30 40’E and latitudes 60 15’ and 60 40’ the estimated individual fish was also taken in grams (g) using a weighing area of the main body is 150.56km 2 and has an area of 208 balance (Camry EK 5055). km 2 (FAO, 1969 cited by Nwankwo, 2004) and an average depth of less than two meter. The lagoon is the largest of Gill Examination for Parasites the of the four lagoon systems of the gulf of guinea (Webb, The gill of the individual fish specimen was extracted by 1958 cited by Nwankwo, 2004 ) and is one of the nine dissecting the fishes using a dissecting scissors. The coastal lagoons of South-western Nigeria (Webb, 1958; extracted gill sample was placed on a microscopic glass Nwankwo, 2004; Onyema, 2008a). It provides the only slide, a drop of water was added and the sample is covered opening to the sea for the nine lagoons of South Western using a cover slip then view under microscope for parasitic Nigeria. Owing to the dynamics of river inflow and prevalence using a magnification of 60X as described by seawater incursion, the Lagos lagoon experiences brackish omeji et al. (2010); Bichi and Ibrahim (2009) and Emere condition that is more discernable in the dry season and Egbe (2006). This procedure was repeated for all fish (Nwankwo, 2004). In the wet season, the increased river samples for consistency. inflow creates freshwater and low brackish conditions in various parts of the lagoon. The harmattan, a short season of dry, dusty North-East Trade winds are experienced Skin Mucus Examination for Parasites sometimes between November and January in the region The body mucus from the caudal part of fish was scrapped reducing visibility and lowering temperatures (Onyema et using a scrapper. Scraping was done carefully so as to avoid al. , 2003). Characteristically, Lagos Lagoon has a seasonal scales in the mucus which may impair the visibility of small fluctuation in salinity and high brackish water during the protozoan. Mucus was then placed on glass slide and a drop dry season (From December to May), while freshwater of water was added and then covered with a cover slip condition exists in the rainy season (June – November) before being viewed under microscope for ecto-parasites as (Kusemiju, 1975; Ugwumba and Kusemiju, 1992; Solarin, described by omeji et al. (2010); Bichi and Ibrahim (2009) 1998; Lawal-Are, 2006). The lagoon is fairly shallow and and Emere and Egbe (2006). The procedure was repeated is not plied by ocean going ships but by smaller barges and for all samples. boats. Lagos Lagoon receives freshwater from Lekki Ecto-parasites found were identified and their number Lagoon via Epe Lagoon in the North-east, and dis-charges counted. Examination of fish gill and mucus from skin were from Majidun, Agboyi and Ogudu creeks as well as Ogun done on the same day the fish were caught (live or fresh) as River in the North-west (Soyinka, 2008; Lawal-Are et al. , some ecto-parasites die after the host is dead. 2010). In the dry season, freshwater inflow is greatly reduced and Analysis of Parasitic Infestation seawater enters the lagoon through the harbour giving rise The analysis for parasitic infestation for finding the to marine conditions near the harbour and brackish water incidence and prevalence were carried out by following extending far inland (Hill and Webb, 1958; Nwankwo, equations (Poulin and Rhode, 1997) 1996; Onyema et al., 2003). Hence, areas located in close proximity to the harbour experience greater marine influence than places further inland. Prevalence of infection = x 100

Collection of fish specimens . Incidence of infection = Fish species were landed at the market by artisanal . fishermen using casts nets, drag nets and set gill nets. Samples of Ethmalosa fimbriata (30), Sarotherodon melanotheron (30) and Chrysichthys nigrodigitatus (30) Prevalence of individual parasites = were collected from the Better-life fish market in Makoko area of Lagos state between March-August 2015 (6 months). Five 5 specimens of each species was collected each month for analysis of parasitic prevalence throughout Analysis of Data the six months of the project. All data were analyzed using descriptive statistics. Prevalence (P) was represented in bar graphs and pie chart using Microsoft excels.

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Parasite in fishes from Lagos lagoon

RESULTS Piscinodinium (protozoa) and Eustrongylides (nematode) as shown in Table 4. Length - weight relationship of the fishes used for the study Out of the 90 specimen analyzed, a total of 41 (45.6%) The 90 specimens used consisted of different size groups, specimens were infected with parasites having a total the length of S. melanotheron mean ranged from parasite count of 735 from infected specimens. Glochida 17.42±0.77cm - 20.38±2.41cm with average range weight accounted for the most abundant parasite in the gills and from 103.4±12.26 g - 138.4±16.37g (Table 1), C. skin of C. nigrodigitatus having a prevalence of 43.81%, nigrodigitatus mean ranged from 26.92±1.20`cm - Ergasilus sp. had the least prevalence value with 0.41%, 35.76±2.61cm with average range weight from Gyrodactylus had a prevalence of 6.80%, Neobenedenia 165.2±28.07 - 412.4±114.14g (Table 2) and E. fimbriata had a prevalence level of 0.95, larvae forms of mean length ranged from 13.12±1.42cm- 17.76±1.88cm Eustrongylides from S. melanotheron had a prevalence with average range weight from 20.4±6.68 - 53.6±19.47g level of 4.08% while Piscinodinium which was identified (Table 3). from the gills of both S. melanotheron and E. fimbriata had a prevalence level of 41.36%, an unidentified specimen had Table 1: Mean monthly variation of length and weight for S. a prevalence of 2.59%. This is shown in Fig. 2. melanotheron Prevalence with respect to species Total length Standard Chrysichthys nigrodigitatus had a total prevalence 50.16% Month Weight (g) (cm) length (cm) of parasite consisting of Gyrodactylus (6.8%) and Glochida March 20.38±2.41 15.16±1.78 135.6±50.07 (43.36%) making it the species of fish having the highest April 18.31±1.31 13.96±1.02 125.6±24.14 amount of parasitic infestation. S. melanotheron had a total May 19.62±1.39 15.18±1.03 138.4±16.37 prevalence of 28.57% comprising of Ergasilus (0.41%), June 17.42±0.77 13.20±0.57 107.0±10.26 Piscinodinium (23.13%), Eustrogylides (4.08%) and July 19.42±1.20 14.64±1.34 132.4±12.26 Neobenedenia (0.95%). E. fimbriata had a total prevalence August 18.06±0.95 13.68±0.59 103.4±12.26 of 20.82% comprising of Piscinodinium (18.23%) and unidentified worm (2.59%). This relationship is shown in Table 2: Mean monthly variation of length and weight for C. Table 5 and Fig. 3. nigrodigitatus Prevalence of Parasites with respect to size of fish Total length Standard Month Weight (g) Glochida was discovered to be more prominent in larger (cm) length (cm) sized C. nigrodigitatus while Gyrodactylus was found to March 33.36±2.29 24.60±1.46 285.6±53.20 infest fish of different sizes but with an increased April 35.76±2.61 26.88±2.71 412.4±114.14 prevalence in larger species of C. nigrodigitatus, May 30.72±4.54 22.84±3.74 236.8±119.72 Eustrongylides and Neobenedenia was found in matured June 33.38±2.46 24.68±2.13 311.4±98.88 July 31.54±3.87 22.72±1.77 240.8±45.41 S.melanotheron, Piscinodinium was found to affect S. August 26.92±1.20 20.28±0.76 165.2±28.07 melanotheron and E. fimbriata irrespective of their size. This relationship is represented in Table 6 and Fig. 4. Table 3: Mean monthly variation of length and weight for E. fimbriata DISCUSSION

Total length Standard Month Weight (g) This study recorded a parasitic prevalence of 45.6% from (cm) length (cm) all infected specimens, C. nigrodigitatus recorded the March 14.68±1.62 12.10±1.36 28.2±8.97 highest prevalence of parasitic infection with 50.16%. This April 17.76±1.88 14.14±1.65 53.6±19.47 agrees with the finding of Olorin and Somorin (2006) which May 15.36±1.98 13.78±3.42 32.0±13.52 recorded the highest parasitic burden in C. nigrodogitatus June 15.46±0.66 12.62±0.49 33.4±5.08 which was found to be infected with the metacerceria of the July 13.12±1.42 10.44±1.36 20.4±6.68 trematode ( Clinostomum tilapiae ) and the adult of the August 14.28±1.02 11.34±0.96 25.4±6.15 acanthocephalan ( Neochinorynchus rutili ). S.

melanotheron had the highest number of parasite diversity Parasites of fishes in Lagos Lagoon with four different families of parasite, Ergasilidae Parasite species recorded in 90 specimens analyzed are (Ergasilus sp ), Capsilidae ( Neobenedenia mellari ), Glochida (parasitic larvae of mussels), Gyrodactylus, Oodinidae ( Piscinodinium pillulare ) and Neobenedenia, Ergasilus (parasitic copepod), Dioctophymatidae ( Eustrongylides sp ).

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Table 4: The species of parasites identified from specimens and the part of fish they were found

Fish Site of infection Family of parasite Specie of parasite S. melanotheron Gill Ergasillidae Ergasilus sp. S. melanotheron Gill Dioctophymatidae Eustrongylides sp. C. nigrodigitatus Gill and skin Unionidae Glochida (Anodonta grandis) C. nigrodigitatus Skin Gyrodactylidae Gyrodactylus arcuatus C. nigrodigitatus Skin Gyrodactylidae Gyrodactylus derjavini E. fimbriata Gill Oodinidae Piscinodinium pillulare S. melanotheron Skin Capsalidae Neobenedenia mellari S. melanotheron Gill Oodinidae Piscinodinium pillulare E. fimbriata Gill Unidentified worm

Figure 1: Map showing the sampling sites in Lagos lagoon

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Parasite in fishes from Lagos lagoon

Figure 2: Prevalence (%) of parasite from all infected specimens of S. melanotheron, C. nigrodigitatus and E. fimbriata

Figure 3: Prevalence of parasite with respect to species

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Figure 4: Prevalence of parasite with respect to size of fishes

PLATE 1a: (A) Slide of Eusrongylides sp. from gill infected of S. melanotheron. (Mg x60), (B) Slide of Neobenedenia mellari from skin of infected S. melanotheron (Mg x60) , (C) Slide of Piscinodinium pillulare from gill of infected E. fimbriata (Mg x60), (D) Slide of Ergasilus sp. from gill of infected S. melanotheron (Mg x60) ,

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Parasite in fishes from Lagos lagoon

PLATE 1b: (E) Slide of Gyrodactylus derjavini from skin of infected C. nigrodigitatus (Mg x60), (F) Slide of Glohida ( Anodota grandis ) from gill of infected C. nigrodigitatus (Mg x60).

Chen (1973) and Wang et al. (1997) reported the larvae of Vidya and Sukumar (2002) noted that potential factors Eustrongylides from the fish species of the families determining the transmission of parasites include Engraulidae, Cyprinidae, Siluridae, Bagridae, Channidae environmental conditions (affect the viability and behavior and Percichthyidae. The prevalence of parasitic infections of parasites) and feeding, movement and defecation corresponds with fish length which also in turn corresponds patterns of the host (determine the parasites encountered). to fish size and age as reported by Lagler et al. (1979), with In the wild it is difficult to isolate and quantify the effects exceptions from Piscinodinium sp. Poulin, (2000) stated of any single factor on parasitized fish population that larger fish have more internal and external space for dynamics. However, studies of fish in captivity or under parasite establishment and therefore tend to have heavier culture conditions have provided much information about infestations. This study recorded similar case of higher the effects of parasites on fish survival. From this study prevalence of parasitic infestation in agreement with the parasite infestation was known to cause swelling in the work of Omeji, et al., (2010) who reported higher rate of gills, rotting of fin and loss of scale. It was reported by Cruz protozoan parasites in bigger C. gariepinus and – Lacierda (2001) that Glochidia destroy the gills and Heterobranchus longifilis than the smaller ones. Emere and disrupt the respiratory function of the gill. Nematollahi et Egbe (2006) reported higher rate of protozoan parasites in al. (2013) also reported that parasites are among the bigger Synodontis clarias than the smaller ones an important factors responsible for weight loss, disruption of indication that parasites infest fish based on the size and the reproduction or impotency blindness, abnormal behavior, surface area. Gyrodactylus show an increase in prevalence epithelial lesions, deformities of gills and other symptoms with respect to size to a certain level then declines in this that ultimately lead to economic loss in fish industry. study, these results are in accordance with those of Ramollo Evidences suggest that parasites can act as severe et al (2006 ), who reported that the prevalence and intensity pathogens, causing direct mortality or rendering the fish of infestation generally increased with the host’s size, up to more vulnerable to predators (Kunz and Pung, 2004). a certain point and then declined. The prevalence of gyrodactylus in the fish species could be as a result of the Parasites are a natural component of the environment and fact that gyrodactylus are host specific (Marcogliese and may be viewed as an indicator of the relative health of an Price, 1997). Combination of factors, such as infection rate, ecosystem. The majority of species of parasites present on survival, reproduction, population growth and virulence, and within fish are not hazardous to human and those which determine host optimality (King and Cable, 2007). Parasite are hazardous tend to have complex life-cycles which infection rate from all specimen was generally low and this involve more than one type of host for development. could be attributed to several factors which include: Eustrongylides is known to affect birds that feed on infected temperature, salinity, season (raining or dry), this is in line fish and they cause a condition known as with Ramollo (2008), which reported that good biological (Franson and Custer, 1994). Humans who consumed raw or indicators are sensitive to environmental alterations so that under-cooked fish that carry the larval stages of changes in their numbers can be used as warning of Eustrongylides have experienced gastritis or inflammation deteriorating conditions before the majority of less of the stomach and intestinal perforation requiring surgical sensitive organisms are seriously affected. In the same vein, removal of worms (Measures, 1988).

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CONCLUSION Siluriformes, Mochokidae) at Rivers Niger- Benue Confluence, Lokoja, Nigeria . African Parasites are a natural component of the environment and Journal of Biotechnology. 12 (20): 3029-3039 may be viewed as an indicator of the relative health of an Ezenwa, B. I. O. and Ikusemiju, K. 1981. Age and growth ecosystem. The majority of species of parasites present on determination in the catfish Chrysichthys and within fish are not hazardous to human and those which nigrodigitatus (Lacépède) by use of dorsal spine. are hazardous tend to have complex life-cycles which Journal of Fish Biology , 19: 345-351 involve more than one type of host for development. F.A.O. 1969. Fisheries survey in the western and mid- Humans who consumed raw or under-cooked fish that carry western regions of Nigeria. FAO/Sf: 74/NIR 6. the larval stages of Eustrongylides have experienced 142pp. gastritis or inflammation of the stomach and intestinal F.A.O. 1996. Aquaculture potential in African perforation requiring surgical removal of worms. documentation issued on the occasion of the world food summit in Rome November 1996. Rome FAO. 20; REFERENCES Franson, J. C. and Custer, T. W. 1994. Prevalence of eustrongylidosis in wading birds from colonies in Bichi, A. H. and Dawaki, S. S. 2010. A survey of the California, Texas, and Rhode Island, United States ectoparasites on the gills, skin and fins of of America: Colonial Waterbirds, 17, p. 168–172. Oreochromis niloticus at Bagauda fish farm, Hill, M. B. and Webb, J. E. 1958. The ecology of Lagos Kano, Nigeria. Bayero Journal of Pure and lagoon II.The topography and physical features of Applied Sciences , 3(1): 83-86. the Lagos harbour and Lagos lagoon. Bichi, A. H. and Ibrahim, A.A. 2009. A survey of ecto and Philosophical Transaction of Royal Society, intestinal parasites of tilapia zillii (gervias) in tiga London, 241: 307-417. lake, kano, Northern Nigeria. Bayero Journal of Ibiwoye, T. I. I., Okaeme, A. N., Balogun, A. M. and Pure and Applied Sciences , 2(1): 79 – 82. Ogunsusi, R. A. 2000. Updating the helminth Bichi, A. H. and Yelwa, S. I. 2010. Incidence of piscine parasites fauna of freshwater fishes in Nigeria in parasites on the gill and gastrointestinal tract of the new millennium. First occurrence of Clarias gariepinus (Teugels) at Bagauda fish Eustrongyloides africanus ( Khalil and Thurston, farm, Kano. Bayero Journal of Pure and Applied (1973) larvae in Clarias species of Nigeria. 15th Sciences , 3(1): 104-107. Annual conference of the Fishes Society of Cruz – Lacierda, E.R. 2001. Parasitic diseases and pests. In Nigeria (FISON) Jos, Plateau State. Lio – Po, G. D., Lavilla, C. R. and Cruz – Ibiwoye, T. I. I., Nweke, S. U. and Sogbesan, A. O. 2006. Lacierda, E.R (Eds), Health management in Parasitic fauna of the gastrointestinal tract of aquaculture. Tigbaum, Iloilo, Philipines: Clarias anguillaris (Geoffrey, Pisces: Clariidae) Aquaculture Department, South east Asian in Onitsha Area of Nigeria. In: Proc. 20th Annual Fisheries Development Center 55 - 74 Conf. of FISON, Port Harcourt, Nigeria, Nov. 14- Echi, P. C., Eyo, J. E., Okafor, F. C. 2009a. Co-parasitism 18, 2005, 266-271Pp. and morphometrics of three clinostomatids Iyaji, F. O. and Eyo, J. E. 2008. Parasites and their Digenea: Clinostomatidae; in Sarotherodon freshwater fish host. Bio-Research, 6(1): 328-338. melanotheron from a tropical freshwater lake. Iyaji, F. O. 2011. Parasites of Siluriformes at Rivers Niger- Animal Research International , 6(2): 982-986. Benue Confluence. PhD Thesis University of Echi, P. C., Okafor, F. C. and Eyo, J. E. 2009 b. Co- Nigeria Nsukka. infection and morphometrics of three Klinger, R. E. and Floyd, R. F. 2002. Introduction to Fresh clinostomatids Digenea: Clinostomatidae; in water Fish Parasites. Florida Cooperative Tilapia guineensis Bleeker, 1862 from Opi lake, Extension Service. Institute of food and Agric Nigeria. Bio-Research , 7(1): 432-436. Sciences. University of Florida. Ekanem, A. P., Eyo, V. O. and Sampson, A. F. 2011. http://www.edis.Ifas-ufl.Edu. Accessed 20th June Parasites of landed fish from great Kwa River, 2006. Calabar, Cross River State, Nigeria. International Kostoingue B, Diebakate C.M., Faye, N. and Toguebaye, Journal of Fisheries and Aquaculture , 3(12): 225- B. S. 2001. Presence of Myxosporidea (Myxozoa: 230. Myxosporea) of the genus Henneguya Thelohan, Emere, M. C. and Egbe, N. E. L. 2006. Protozoan Parasites 1892 in freshwater fishes from Chad (Central of Synodontis Clarias (A freshwater fish). Best Africa). Acta Protozoologica 40 , 117-123. Journal, 3(3): 58-64. Kunz, A. K. and Pung, O. J. 2004. Effects of Microphallus Eyo, J. E., Iyaji, F. O. and Obiekezie A. I. 2013. Parasitic turgididus (: Microphallidae) on the infection of Synodontis batensoda (Ruppell, 1832, predation, behavior and swimming stamina of the 60-----

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