survey on endoparasitic fauna of some commercially ... · fish interacts with the various levels of...

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EL-SHAHAWY (I. S.) AND COLLABORATORS126

Introduction

Fish remain important sources of food, nutrition, income and livelihoods for hundreds of millions of people around the world. Moreover, fish continues to be one of the most-traded food commodities worldwide with more than half of fish exports by value originating in developing countries [13]. Fish interacts with the various levels of food chain and influence the structures of lakes, streams and estuaries since; they are usually restricted to particular modes of life related to their food sources and reproductive requirements [2].

In Egypt, Clarias lazera, Oreochromis niloticus and Lates niloticus are the most principal sources for fish production and food fish for people in Upper Egypt in particular. It is

also used as a game fish where it is specially introduced into water reservoirs for the purpose of sport fishing, and is also used extensively in biological, physiological and behavioural research [42].

The majority of digenetic trematodes do not pose a serious of fish health. However, the presence of their metacercariae (MC) has taken a great interest in most countries especially for the human care against the transmissible diseases [17]. Metacercariae infections cause low weight gain, high mortality, immarketability of the infected fish and some of these parasites may have zoonotic importance [16].

On the other hand, Acanthocephalans are a group of endoparasitic helminths commonly found in both

SUMMARY

Knowledge of the local parasite fauna of fish and their morphology is of vital importance. Therefore, this study was aimed to estimate the prevalence and identify the most common endoparasites genera infecting some freshwater fishes in the River Nile, southern Egypt between April 2012 and March 2013. Two hundred and sixteen freshwater fish (72 of each following species: Oreochromis niloticus, Clarias lazera and Lates niloticus), were macroscopically examined, both externally and internally, for presence of helminths and encysted metacercariae. Microscopic examination was then conducted to identify the species. The parasite fauna of this geographical area is diverse; it consisted of 4 species; one trematode (Orientocreadium batrachoides), two cestodes (Tetracampos ciliotheca and Monobothrioides chalmersius) and one acanthocephala (Rhadinorhynchus niloticus) were recorded. Moreover, five species of encysted metacercariae viz., Clinostomum complanatum, Clinostomum tilapiae, Cyanodiplostomum sp., Opisthorchis sp., and Diplostomum tilapiae were detected in this survey. Among the 216 fish examined, 70 (32.4 %) were infected. The lowest rate of infestation was obtained in L. niloticus (18.1 %) and highest one in C. lazera (43.1 %). Furthermore, the prevalence was highest in spring season (44.4%) followed by summer (35.2%) and winter (29.6%), and was lowest in autumn (20.3%). Another interesting finding of the present investigation was the recovery of Clinostomum spp. which is considered to be one of the species could therefore represent potential health risks of eating uncooked or slightly cooked fish. This study underlined the idea that an analysis of fish-parasite fauna is very useful as pre-requisite for implementing preventative and control measures against parasitic disease.

Key words: Endoparasites, Freshwater fish, Seasonal dynamics, Egypt

RÉSUMÉ

Enquête sur la faune endoparasites de certains poissons commercialement importants de la rivière Nil, dans le sud de l’Egypte

Cette étude visait à estimer la prévalence et à identifier les genres endoparasites les plus fréquents qui infectent certains poissons d’eau douce dans le Nil, entre avril 2012 et mars 2013. Deux cent seize poissons d’eau douce (72 espèces Oreochromis niloticus, Clarias Lazera et Lates niloticus) ont été examinés macroscopiquement, à l’extérieur comme à l’intérieur, pour détecter la présence d’helminthes et de métacercaires cingés. Un examen microscopique a alors été effectué pour identifier l’espèce. La faune parasite de cette zone géographique est diverse; elle se composait de 4 espèces : un trematode (Orientocreadium batrachoides), deux cestodes (Tetracampos ciliotheca et Monobothrioides chalmersius) et un acanthocephale (Rhadinorhynchus niloticus). De plus, cinq espèces de métacercaires cingés, à savoir Clinostomum complanatum, Clinostomum tilapiae, Cyanodiplostomum sp., Opisthorchis sp., et Diplostomum tilapiae ont été détectées. Parmi les 216 poissons examinés, 70 (32,4%) étaient infectés. Le taux d’infestation le plus faible a été observé sur L. niloticus (18,1%) et le plus élevé chez C. lazera (43,1%). De plus, la prévalence était la plus élevée au printemps (44,4%), suivie par l’été (35,2%) et l’hiver (29,6%), et elle était la plus faible en automne (20,3%). Un autre résultat intéressant est la mise en évidence de Clinostomum spp. Qui est considéré comme l’une des espèces pouvant présenter des risques potentiels pour la santé humaine lors de consommation de poisson non cuit ou légèrement cuit.

Mots-clés : Endoparasites, poissons d’eau douce, Dynamique saisonnière, Egypte

Survey on endoparasitic fauna of some commercially important fishes of the River Nile, southern of Egypt (Egypt)

I. S. EL-SHAHAWY1*, M. O. El-SEIFY2, A. M. METWALLY1, M. M. FWAZ1

1Department of Parasitology, Faculty of Veterinary Medicine , South Valley University, Egypt2Department of Parasitology , Faculty of Veterinary Medicine, Kafrelsheikh University, Kafrelsheikh, Egypt

*Correspondence author: [email protected]

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ENDOPARASITES OF SOME COMMERCIALLY IMPORTANT FISHES 127

marine and freshwater fishes worldwide and are known to cause pathological conditions in many fin fishes [30]. The irreversible mechanical damage caused by the attachment of the armed proboscis affect the architecture of the intestinal tissues leading to pathological changes. In heavy infections they can cause occlusion of the gut and invasion/migration of the parasites into uncommon locations has also been reported [30].

With increasing the demand for freshwater fishes in Qena State for high quality protein consumption which constitutes a major component of diet, is a signal to screen for parasitic infections in these freshwater fish species. Therefore, the present study was developed to investigate the helminth parasite fauna of fish species in southern Egypt and the status of their parasite communities (prevalence, mean intensity, abundance and dominance).

Material and Methods

STUDY AREA

The present research was carried out in the southern region of Egypt where almost 80% of the population lives in rural areas, with an urbanization rate of only 19.7%. The city of Qena; wherein the study was conducted, is located between 26° 09’ 16” North and 032° 42’ 58” East. The study area is categorized as continental climate with four distinct seasons namely, winter season (January - March), spring (April-June), summer (July-September) and autumn season (October - December). The major rainy season is from January to March.

COLLECTION OF FISH SAMPLES

Between April, 2012 and March 2013, a total number of 216 randomly selected fish samples representing 3 fish species (72 Oreochromis niloticus, 72 Clarias lazera and 72 Lates niloticus) were collected fresh with the aid of traps and gillnets and local fish markets in and around the River Nile at Qena Governorate, southern Egypt. The collected samples (6 specimens from each fish/month) were submitted for parasitological investigation at the laboratory of Parasitology; Faculty of Veterinary Medicine; South Valley University in ice box after packed in plastic bags, labeled with different data about the investigated fish specimens. Length and weight of each fish individually were noted carefully, whereas the studied fishes were female.

EXAMINATION OF FISH FOR PARASITES

Fishes were killed by cervical dislocation prior to dissection (Research ethics committee of the University approval no. 15/40). A cut was made on the ventral side from the anal opening to the lower jaw. Then, two more cuts were made on the lateral side to expose the body cavity with alimentary canal and other internal organs. The surfaces of the visceral organs and body cavities and serous membranes were examined for parasites by using hand lens. Moreover, the alimentary canals were removed and cut into

parts (stomach and intestine) in 0.09% physiological saline for parasite recovery under a dissecting microscope. Each part was further carefully slit open to aid the emergence of parasites. Gastrointestinal parasites were further recognized by their wriggling movements on emergence in the normal saline under the microscope [25].

Fish were also macroscopically examined, both externally and internally, for presence of macroscopic encysted metacercariae (EMC) with the aid of a magnifying hand lens to detect any changes in the visceral organs and muscles, and microscopically by using direct compression between two glass slides [28]. Metacercariae identification was based on those dissected directly from tissues. They were separa-tely collected by the general feature and were tentatively identified to species level based on the morphological details, their dimensions and being either singly or in groups [12, 43], and directly photographed without staining.

PARASITOLOGICAL PROCESSING

The collected cestode and trematode were first relaxed in hot water, and then fixed in 5% formalin and transferred to 70% ethanol after one week [34]. For light microscopic studies, specimens were processed by the methods previously recorded as they stained with acetic acid alum carmine, destained in 70% acid ethanol (i.e. ethanol with several drops of HCl), dehydrated through a graded ethanol series, clarified in clove oil, and mounted in Canada balsam as permanent preparations. But for acanthocephala, specimen were pressed slightly between glass slides, fixed in AFA (alcohol–formol–acetic acid) overnight, stained with acetocarmine stain [22]. All recovered helminthes were identified by using the texts of [6, 27, 37, 46, 49].

DATA ANALYSIS

Prevalence, Density and Intensity of parasites were estimated through the following formula [26]

1. Prevalence = number of individuals of a host species infected with a particular parasite species ÷ number of hosts examined × 100.

2. Intensity = total number of individuals of a particular parasite species in a sample of a host species ÷ number of infected individuals of the host species in the sample.

3. Density or Abundance = total number of individuals of a particular parasite species in a sample of hosts ÷total number of individuals of the host species (infected + uninfected) in the sample.

Furthermore, the significance of differences was analyzed using chi-square (χ2) using the Statistical Package for Social Science version 15.0 (SPSS Inc., Chicago, IL), and p<0.05 was considered significant.

Results

ADULT HELMINTHS

Four helminths, distributed in 2 higher taxa viz., Platyhelminthes one trematode (Orientocreadium spp.),

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two cestodes (Tetracampos spp. and Monobothrioides spp.), and one acanthocephala (Rhadinorhynchus spp.) were encountered (Figure 1, Table I). The different species were morphologically identified as follow. Orientocreadium batrachoides (Tubangui, 1931) has the main morphological generic characters of the genus Orientocreadium by possessing a long narrow body with almost equally sized oral and ventral suckers which are found at one third of the body length, testes are symmetrical, while the vitelleriae are extend from the uterine level to the posterior end of the testes (Figure 1). Monobothrioides chalmersius was characterized by the presence of scolex devoid of bothria, but bearing numerous longitudinal furrows and possessing terminal introvert. Uterus never passes anterior to cirrus sac and is long, regularly wound tube. Post-ovarian vitelleriae were absent. Ovary is “H” shaped; coils of uterus extend anterior to wings of ovary. By contrast, the scolex of Tetracampos ciliotheca was nearly triangular with a flat to slightly raised rostellum armed with a crown of 26–30 hooks. No neck detected. The gravid segment was squarish; the uterus appeared as a round or oval sac occupying the whole segments and filled with eggs. Rhadinorhynchus niloticus was characterized by long proboscis with 14 curved hooks

in each of the 20-22 longitudinally arranged rows, short and spineless neck, slender Lemnisci and ellipsoidal testes in the middle third of the body. The infection rates of Orientocreadium batrachoides, Tetracampos ciliotheca and Monobothrioides chalmersius in C. lazera were 6.9%; 2.8% and 5.6% respectively, while Rhadinorhynchus niloticus were recovered only from the intestine of L. niloticus with overall infection rate of 12.5 %. Additionally, the infection rate of Orientocreadium batrachoides in O. niloticus was 2.8%.

Overall, of the 216 fish specimens examined, 70 samples proved to be infected (32.4%), out of which 43.1% (31/72) of the C. lazera, 36.1% (26/72) of the O. niloticus and 18.1% (13 /72 ) of L. niloticus were infected with at least one parasite, among the submitted specimens (χ2=10.94, P= 0.004). Moreover, Out of the 216 fish examined, 23.1% were infected with trematodes parasites. Most of these parasites were recovered from both O. niloticus and C. lazera (31.9%) than the other host species L. niloticus (5.5%). In this study, cestode species were the most prevalent parasite of C. lazera, with overall percentage of 11.1%; without record of infection among the other examined fish as depicted in Table IV. However, acanthocephala species was reported from L.

Helminth species Parasite group Fish species Location No. of examined fish No. of infected %Orientocreadium batrachoides Trematodes C. lazera

O. niloticus Intestine 72 52

6.92.8

Tetracampos ciliotheca Cestodes C. lazera Intestine 72 2 2.8Monobothrioides chalmersius Cestodes C. lazera Intestine 72 4 5.6

Rhadinorhynchus niloticus Acanthocephala L. niloticus Intestine 72 9 12.5

Table I: Prevalence of different species of helminth parasites among examined fish

Fish species

Length(mean±

SD)

Weight(mean±

SD)Season

No. of Examined

fish

Total no. of infected

fishTrematodes Cestodes Acanthocephala

n (%) Adult *EMC % n (%) n (%)

O. niloticus 14±0.43 50± 1.2

winter 18 6 (33.3) 1 4 27.8 0 (0) 1 (5.6)spring 18 11 (61.1) 1 10 61.1 0 (0) 0 (0)

summer 18 6 (33.3) 0 4 22.2 0 (0) 2 (11.1)autumn 18 3 (16.6) 0 3 16.6 0 (0) 0 (0)

Total 72 26 (36.1) 2 21 31.9 0 (0) 3 (4.2)

C. lazera 22±0.22 210±2.3

winter 18 10 (55.6) 1 5 33.3 4 (22.2) 0 (0)spring 18 7 (38.9) 2 5 38.9 0 (0) 0 (0)

summer 18 8 (44.4) 1 5 33.3 2 (11.1) 0 (0)autumn 18 6 (33.3) 1 3 22.2 2 (11.1) 0 (0)

Total 72 31 (43.1) 5 18 31.9 8 (11.1) 0 (0)

L. niloticus24±0.35 190±1.6

winter 18 0 (0) 0 0 0 0 (0) 0 (0)spring 18 6 (33.3) 0 1 5.6 0 (0) 5 (27.8)

summer 18 5 (27.8) 0 3 16.7 0 (0) 2 (11.1)autumn 18 2 (11.1) 0 0 0 0 (0) 2 (11.1)

Total 72 13 (18.1) 0 4 5.5 0 (0) 9 (12.5)Overall 216 70 (32.4) 7 43 23.1 8 (3.70) 12 (5.6)

Table IV: Prevalence and Seasonal dynamics of different helminth parasites among the examined fish

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niloticus and O. niloticus with an overall prevalence of 12.5% and 4.2%, respectively. This marked difference was found to be non-statistically significant (χ2= 3.41, P= 0 .18).

With regard to the seasonal dynamics, generally, the prevalence were higher in the dry than the rainy season among the examined fish specimens, as the infection rate was found in 24/54 fish (44.4%) in spring, 19/54 (35.2%) in summer, 16/54 fish (29.6%) in winter and 11/54 (20.3%) in autumn. This marked difference was found to be statistically significant (χ2=7.5, P= 0.05) (Table IV). The highest peak of adult trematode infection was recorded in spring (5.6%), while the lowest was in summer and autumn (1.9%). There was no significant difference detected between seasonal dynamics and the infection rate (χ2=5.17, P= 0.16); as well as it was clarified the seasonal dynamics of different helminth parasites among different fish species (Figure 3).

With respect to the mixed infection, the present data reported that 6.1% of examined fish had mixed infection; of which 0.0% in O. niloticus, 9.7% in C. lazera and 8.3% in L. niloticus, while the single one represented 26.4% of the examined samples (36.1% in O. niloticus; 33.3% in C. lazera and 9.7% in L. niloticus).

Figure 3: Seasonal prevalence of the recovered trematode species among examined fish (EMC= Encysted metacercariae)

Figure 1: Helminth parasites identified in freshwater fish (Scale bar= 0.5 mm). A) Orientocreadium batrachoides, B) Tetra-campos ciliotheca (Scolex), C) Tetracampos ciliotheca (Gravid segment), D) Monobo-thrioides chalmersius, E) Rhadinorhynchus niloticus (Proboscis), F) Rhadinorhynchus niloticus (Male)

A B C

D

E F

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ENCYSTED METACERCARIAE

Five species of encysted metacercariae were detected and identified as Clinostomum complanatum (6.9%), C. tilapiae (4.6%), Cyanodiplostomum spp. (5.1%), Opisthorchis spp. (1.9%), and Diplostomum tilapiae (1.4%) (Figure 2). Out of 216 examined fish, 43 were found to be infected with one or more species of encysted metacercariae with overall prevalence rate 19.4%, out of which 29.2% in O. niloticus, 25 % in C. lazera, while the lowest percent of infection was found in L. niloticus (5.6%). With respect to the fish species and the type of cyst, the present investigation found that the infection rate of microscopical cyst among O. niloticus and C. lazera was16.7% and 13.9% respectively, while the macroscopical cyst was 12.5% and 11% respectively as presented in Table II and Figure 2, f.

Regarding the seasonal prevalence of encysted metacercariae, the highest prevalence was recorded in spring (29.6%), while the lowest was in autumn (11.1%). There was no significant difference detected between seasonal dynamics and the infection rate (χ2=3.8, P= 0.28). On the other hand, among examined O. niloticus, the highest prevalence of encysted metacercariae was noticed during spring season (55.6%), while the lowest rate was reported in autumn (16.7%). By contrast, in C. lazera, the highest peak was noticed during winter spring and summer seasons (27.8%), while the lowest rate (16.7%) was reported in autumn season (Table IV).

Table III summarizes the density and distribution percent of cyst /g of muscle tissue in the different body parts of O. niloticus and C. lazera. It was observed that the highest

distribution percentage of the metacercariae was found in the tail region (31.5 and 100% respectively), and its mean density was 1.6 and 11.8cyst/cm

2

respectively. The distribution percentage of the metacercariae in the head region was 26.3% and 0% respectively, and its mean density was 4.7 and 0 cyst/cm

2

respectively. Additionally, the distribution percentage and density of the parasite in the trunk region, was 26.3% and 93.8%, and 0.7 and 8.1 cyst /cm

2

respectively. Furthermore, the mean intensity of infection of encysted metacercariae among O. niloticus, C. lazera and L. niloticus was 6, 16 and 3 respectively as shown in Table III.

Discussion

The overall prevalence rate of endoparasitic helminthes in this study was 32.4% (70 out of 216). These findings were nearly similar to the figures previously reported in the endoparasitic helminthes as the prevalence was 34.7%; all reports were from Uke River, Nigeria [1]. It was, however, higher when compared with records by other investigators in the rivers who reported overall parasite prevalence of 17.1% in the Osse River, 6.9% in the Okhuo River and 3.3% in the Great Kwa River [8,11]. These variations in the rate of parasitism could be attributed to abiotic and biotic conditions of the environments where the studies were carried out [11, 21].

The present results and earlier work of former studies [7] reported that worms have preference for region of attachment in the alimentary canal of fish. The distribution of parasite in the fishes showed a clear preference for the intestine and stomach where there is the highest concentration of the worms followed by the gut which had a very sparse population of the

Fish species Examined Fish Infected fish Microscopical EMC Macroscopical EMC

n n (%) n (%) n (%)O. niloticus 72 21 (29.2) 12 (16.7) 9 (12.5)

C. lazera 72 18 (25) 10 (13.9) 8 (11)

Table II: Prevalence of different species of encysted metacercariae (EMC) in the body of Oreochromis niloticus and Clarias lazera

Fish bodyO. niloticus (n=19) C. lazera (n=16) Lates niloticus (n=13)

Density Distribution Density Distribution Density DistributionMin/Max* n (%) Min/Max n (%) Min/Max n (%)

Head region 3/25 5 (26.3) - - - -Trunk region 1/3 5 (26.3) 2/25 15 (93.8) - -Tail region 2/4 6 (31.5) 2/26 16 (100) - -

Intensity of infectionParasite species

EMC/ g 2/10 (6)** - 2/30 (16) - 1/4(3) -Clinostomum sp. 3/25 (14) - 0/0 (0) - 0/0(0) -

Rhadinorhynchus niloticus 3/4 (3) - 0/0 (0) - 2/7(4) -

*Min/Max= Minimum/maximum, **numbers in parentheses are mean for intensity of infection

Table III: Density of cyst/g of muscle tissue, distribution in the different body parts and Intensity of infection of different helminths species among infected fish

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worms. The preference for intestine and stomach regions as sites of attachment could be attributed to the availability of food in this region. The extension of the worms to the fore gut occurred when there was heavy concentration of worms in the stomach and intestine region owing to lack of space.

The results showed that C. lazera was dominated by helminth parasites (43.1%). O. niloticus, in contrast, harbored moderate infection rate (36.1%), but L. niloticus exhibited the lowest infection percentage (18.1%). The variation in parasite prevalence among the three hosts may reflect different habitat use, behavior of fish, environmental conditions and also the type of diet and feeding habit [29, 32].

Trematodes had the highest peak of infection (23.1%), followed by acanthocephalan (5.6%) and then cestodes (3.7%) [40, 47], and the low cestode and acanthocephalan diversity in this inventory also fit previously described patterns for Egyptian freshwater fish. This might be attributed to the

type of intermediate host present and the prevailing physico- chemical factors [36].

The reason for high prevalence of trematode infection as compared to the other kind of parasitic infections might be due to the low host specificity of the adult stages of these parasites which makes them capable of infecting different fish genera and species. It may also be because of the availability of the different host required for the completion of the life cycle of these parasites [50].

Although all three host species were vulnerable to various parasitic infections, it was observed that O. niloticus was the most susceptible species to be infected by trematodes; whereas C. lazera was more disposed to trematodes and cestodes infections, and L. niloticus was demonstrated with acanthocephala. This may be attributed to the type of intermediate host present and type of stream inhabited [36].

Figure 2: Encysted metacercariae (EMC) identified in muscle of freshwater fish (Scale bar=50 µm). a) Clinosto-mum complanatum, b) Clinostomum tilapiae, c) Cyanodiplostomum sp., d) Opisthorchis sp., e) Diplostomum tilapiae, f) Macroscopic EMC in muscle of Clarias lazera (arrow). O.L= Outer layer, I.L= Inner layer, E.B= Excretory bladder, C.W= Cyst wall, H.B= Hind body, F.B= Fore body, S.P= Stalk like process

A

B

C

D

E F

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The parasitic infection is greatly influenced by the season, which basically interferes with ecology and physiology of the fish. The present study results appear that the percentage of total infection rate of helminth parasites were low during winter and higher in spring and summer. During winter season the prevalence of helminth parasites were low because of average temperature; and humidity which facilitates decreased the susceptibility of disease [31]. Additionally, it should be kept in mind that the seasonal dynamics of helminth parasites is influenced by various factors such as host hibernation, spawning of the host fish, changes in the immune response of fish at different temperatures, and the feeding habits of the host fish [15].

Co-infections by multiple parasites have a great influence on the host–parasite ecology and evolution through within-host interactions [20]. However, thirteen cases of mixed infections were observed in the present investigation, with two each occurring between trematode and cestode and trematode and acanthocephala. There was no significant difference in the degree of mixed infections (χ2=0.08, P= 0.77).

With respect to Orientocreadium batrachoides, the identified species in the current investigation is morphometrically close similar to other described comparable species of O. batrachoides [5]. Furthermore, the current species is morphologically distinguished from other Orientocreadium species by their longer and narrower body than O. pseudobagri, shorter and narrower than O. siluri and, O. chaenogobii, and four lobed pharynx in O. indicum that recovered from Rita buchanani Bleeker (Bagridae) from India.

Tetracampoos ciliotheca (Wedl, 1861), previously known as Polyonchobothrium clarias Woodland, 1925 has a widespread distribution in siluroid fishes of Africa. Previous records of this cestode include those from Egypt [9-10], Nigeria [14, 33] and from South Africa, [3, 23]. A detailed morphological description of this species from Clarias gariepinus [3], and the present specimens fit their description. Moreover, this study provides further evidence of the presence of T. ciliotheca in C. lazera.

Through this study, the prevalence of encysted metacercariae was 19.4 %. This finding was lower than those reported in different fresh water bodies in Egypt (100%) [38], (87%) [29], (67%) [44] and (70%) [39]. Such variation in prevalence may be related to the difference in the habitat, food supply, abundance of both aquatic snails (the intermediate host), and the aquatic piscivorous birds, which play the main role to complete the life cycle of some digenetic trematodes.

In terms of tissue distribution of recovered metacercariae in fish, our results show that the majority of metacercariae were found in the tail region followed by the muscles of the head and trunk region. But on contrary, in terms of tissue

density of recovered metacercariae in fish, our data show that the majority of metacercariae were found in the head region followed by the muscles of the tail region, and rarely in trunk region for O. niloticus, but in C. lazera in contrast, the majority of metacercariae were found in the tail region followed by the trunk region, and none at all in the head region. These findings reflect site prefe rence for each species, which in turn may be related to the difference in host species and location. Site preference of infection may be attributed to many factors, including host species and condition, geographical distribution and genetic varia tion of EMC [19]. Site preference of infection may be related to co-infec tion of EMC in single organ as represented in this study. A single host may harbour more than one type of metacercariae.

The effect of the seasonal variations on the parasitic infections in fish was a debate issue [45]. A consistent pattern of seasonal changes in prevalence of EMC was observed in Mugil cephalus, M. capito, T. nilotica and T. zilli with higher levels of EMC infection in late spring and the lowest level was recorded in winter [12]. Additionally, this figure was also supported by previous investigations who mentioned that the prevalence levels of Diplostomum sp. in the lenses of fish eyes were generally higher in the autumn and spring compared to the summer season [48].

The results of previous investigation claimed that an increase in the prevalence of parasitic infections is attributed to the stress of reproductive processes [4, 41]. Intensity of encysted metacercariae is thus a factor that could potentially contribute to the decline in infections observed in winter, suggesting an association between higher mortality and parasitism intensity [18]. The seasonal pattern, with variable amplitudes of fluctuation in different fish species in different seasons also suggests the presence of a seasonal infection-modifying factor [12]. Moreover, the difference in prevalence of EMC between seasons is believed to be due to a difference in the time of expo sure to parasites. Definitely, release of trematode cercariae from the snail host and successful transmission to the fish host is highly temperature-dependent [35]. On the other hand, the decreased level of EMC during the cold season may be explained by the death of the cercariae.

In conclusion, the occurrence and diversity of parasites in the studied fish species highlight the likelihood of disease outbreak in the aquatic ecosystems. This calls for raising awareness in fish health management and the application of appropriate control measures. Additionally, the finding of Clinostomum species represents the potential public health risks, therefore public awareness creation activities should be conducted on zoonotic nature of fish parasites and danger of consumption of raw or undercooked fish. Further studies are still required to carry out the genomic characterization of the gastrointestinal helminths and also to investigate the different intermediate hosts of the helminth parasites.

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Acknowledgements

This work was supported by the Deanship of scientific research, Najran University.

Conflict of interest

The authors declare that there is no conflict of interests regarding the publication of this paper.

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