Prevalence and Intensity of Helminth Parasites of African Catfish Clarias gariepinus in Lake Manzala , Egypt

The African catfish, Clarias gariepinus, is generally considered to be one of the most important tropical catfish species for aquaculture purposes. Parasitological investigation was performed in two hundred naturally collected fish samples during the period of February to December 2014. The prevalence of gastrointestinal helminth parasites infecting C. gariepinus was investigated. A total of 249 helminth parasites belonging to four genera were recovered from 130 (65%) examined fish samples. They were digenea Orientocreadium batrachoides, cestode Polyonchobothrium clariae, and nematode Procamallanus laevionchus and Camallanus polypteri. Majority of the recorded parasites were found in the intestine. Female fish samples had higher prevalence rate 72 (90%) than males 58 (48.33%), and there was no significant difference (P > 0.05) in infestation rate between the two sexes. The relationship of host size (weight/length) and parasite infection showed that there was no significant difference in the parasitic infection among three classes, although fish of larger sizes had more infections. In addition, this study determines the effect of fish age on the prevalence and intensity of gastrointestinal parasites.


Introduction
Fish is regarded as the cheapest source of protein among the urban and rural populace [1] [2].The demand for fish as a source of protein increases as the human population grows [3].In an attempt to increase fish supply as protein source, there has been tremendous increase in the development of fish farming [4].Clarias gariepinus-Burchell 1822, the African catfish is generally considered to be one of the most important tropical catfish species for aquaculture in West Africa [5], with many names such as C. mossambicus Peters 1852 and C. lazera-Valenciennes 1840 being recognized as its junior synonyms [6].This African catfish is widely distributed throughout Africa, inhabiting tropical swamps, lakes and rivers, some of which are subjected to seasonal drying [1].However, farmers are constraint with massive fry and fingerling mortalities, especially in culture system due to the invasion of parasites [7] [8].
Akinsanya and Otubanjo [9] reported that fish from African freshwater were infected by a variety of adult helminth parasites ranging from monogenaen, digenean, cestodes, nematodes, acathocephalans and aspidogastrean.Paperna [10] reported different helminth parasite had varying degrees of been pathogenic.For example Spirocamalllanus spirallis, a common nematode parasite in the stomach of catfish which was reported to be non-pathogenic in spite of the form of attachment by their buccal capsule to the stomach mucosa of infected fish [11] [12], while species of Philometra and Acanthocephalans caused mild to severe pathology in fish.Parasites of fish could also constitute health hazards to humans when ingested with poorly cooked fish [13].Therefore, this study reports the occurrence and prevalence for some helminth parasites inhabiting the gastrointestinal tract of C. gariepinus in Lake Manzala, Egypt.

Study Area
Lake Manzala is the largest lake in the northern region of Egypt and the most productive for fisheries [14].It extends between longitudes 31˚45' -32˚22'E and latitudes 31˚00' -31˚30'N.It extends to 64.5 km in the maximum length and 49 km in the maximum width and 239 km in total length of the shore line [15].

Parasitological Examination
A total of 200 freshwater Clarias gariepinus (Family Clariidae) were collected alive from Lake Manzala at Kafr El-Sheikh governorate by the aid of fishermen and transported a live to laboratory of Parasitological Research in large plastic bags partially filled with water and supplied with a good aeration according to Langdon and Jones [16].The collection was made between February and December 2014.
The total length of each fish were measured in centimeters (cm) using measuring tape, while the weight of each fish was taken in grams (g) using a weighing balance.The sex of the fish was determined by examination of the papillae.Then, the collected fish samples were dissected and the mesenteric cavity examined for parasites.The gastrointestinal tract was then dissected from the rectum to the oesophagus and all parasitic helminth encountered were carefully detached from the stomach or intestinal mucosa.The internal organs of each fish were also examined for parasites or cysts.The helminth parasites from each fish were then fixed in 70% alcohol.The parasites were later stained and identified using identification keys of Yamaguti [17], Ukoli [18], Paperna [10].Prevalence and mean intensity for selected parasites were determined according to Margolis et al. [19].

Statistical Analysis
The prevalence (%), and mean intensity were analyzed according to Bush et al. [20].The relationships between factors such as host sex, weight, length, and parasitic infection were obtained from data using analysis of variance (ANOVA).All statistical analysis were done using SPSS version 15 for windows.

Ethical Considerations
Animal use followed a protocol approved and authorized by Institutional Animal Care and Use Committee (IACUC) in Faculty of science, Cairo University, Egypt.

Results
A total of two hundred fish were examined from Lake Manzala, 120 out of the 200 were males while the rest were female (Table 1, Figure 1(a)).The overall prevalence of helminth parasite in C. gariepinus was 65% (130/200).In addition, the prevalence of helminth infection in relation to host sex of C. gariepinus.Although, the prevalence in males (48.33%) was lower than in females (90%), and it was not statically significant (χ 2 = 0.85; P > 0.05) (Table 2).A total number of 249 parasitic helminths were recovered from 130 infected fish, while helminth intensity was higher in the intestine than in the stomach.Table 2 and Figure  In addition, nematodes have the highest occurrence (33.33%), while, cestodes showed maximum prevalence (25.0%) as tapeworms dominated in the examined fish species.
The examined fish were categorized into three groups according to their length, which were I, II, III (I larger size up to 29 cm, II medium size from 19 to less than 29, and III smaller size less than 19 cm).Table 3 and Figure (1(c)) showed that the smallest fish are relatively less infected than the other length groups of the examined C. gariepinus and the percentage of infection increases with increasing fish lengths.The prevalence observed between sizes in relation to intestinal helminth was not significant (χ 2 = 5.14; p > 0.05).
In addition, the weight of the normal and infected fish of C. gariepinus are grouped in three classes which were I, II, III (I larger weight up to 150 gm, II medium size from 132 gm to less than 150 gm, and III smaller size    from less than 132 gm).Parasitic helminthes were observed in all weight groups.Larger fish weights are heavily parasites than smaller ones (Table 4, Figure 1(d)).The prevalence observed between weight in relation to intestinal helminth was not significant (χ 2 = 8.91; P > 0.05).

Discussion
African catfish is one of the most important fish species in Africa and the Middle East [21] [22].However, parasitic infections are known to cause massive mortality in the fry and fingerling stages, especially in high-density aquaculture systems [23] [24].In the present study, the high infection rate (65%) of C. gariepinus from Lake Manzala could therefore, be attributed to the contamination of the Lake by various pollutants and numerous tributaries coming from the River Nile.Khan and Thulin [25] reported that urban effluents promote aquatic pollution, thus making aquatic organism vulnerable to increased incidence of parasites.Although female fish were infected with more parasites species, infections were not significant in both males and females of C. gariepinus, these data are similar to the findings of Ayanda [26], who reported higher parasitic infestation in female C. gariepinus than the male as a result of their quest for survival, Omeji et al. [27], Emere and Egbe [28] who reported that due to physiological state of the female, most gravid females could have reduced resistance to infestation by parasites.Of all helminth parasites recovered in the present study, they revealed that nematodes have the highest occurrence, while, cestodes showed maximum prevalence recovered from intestine, and these data are coincided by the results obtained by Paperna [10] and Eyo and Iyaji [29] who reported that the high infection of C. gariepinus by cestode parasites could be due to the ingestion of eggs, copepods and mollusks which serve as intermediate hosts of the larval stages of the cestodes.
Oniye et al. [30] reported that the increase in fish size is a reflection of increase in length and weight, which is hereby considered as a measure of age.In the present study, the high incidence of infestation obtained in bigger fish (>29 cm) is an indicator that size of the fish is important in determining the parasitic load compared to small fish, these data are similar to that obtained in previous reported by Mohammed [31] and Oniye and Aken'Ova [32] who stated that the prevalence was found to be increased as the fish grow, and that could be attributed to the longer time of exposure to the environment by body size.In addition, the higher percentage of parasitic infection observed in the weight class (˃150 g) indicated the increase in parasitism with increase in size.This could be due to the fact that bigger fish cover wider areas in search of food than the smaller ones and as a result, they take in more food than the smaller ones and this could expose them more to infestation by parasites.This agrees with the previous reports by Ayanda [26], Omeji et al. [27] [33] but disagrees with Tasawar et al. [34] who reported higher parasite load in smaller fish than the bigger counterparts.

Conclusion
It can be concluded that, there is a positive relationship between host age/size and increase in parasitism.In addition, the increased demand on fish as a source of protein should trigger further studies on fish species and their parasites to determine if there is a risk to humans by feeding more of a particular sex.

Figure 1 .
Figure 1.Different histograms for parasitic infection of C. gariepinus showing: (a) Percentage of infection in relation to sex fish host.(b) Distribution of parasitic infection on examined fish samples.((c), (d)) Prevalence of infection in categorized three classes of the examined fish samples in relation to: c Body length.d Body weight.

Table 1 .
Overall prevalence of the intestinal helminth in C. gariepinus.

Table 2 .
Prevalence, range and intensity for the recorded parasites of Clarias gariepinus.

Table 3 .
Relationship between body length and sex for C. gariepinus with the degree of parasitic infection.

Table 4 .
Relationship between body weight and sex for C. gariepinus with the degree of infection.