Branchial Chamber and Gastrointestinal Tracts Parasites of Fish Species in Benue and Niger Rivers, North Central, Nigeria

Department of Biology, Kogi State College of Technical, Kabba, Kogi State, Nigeria Department of Animal and Environmental Biology, Kogi State University, Anyigba, Kogi State, Nigeria Biology Department, Faculty of Applied Sciences, Umm Al-Qura University, Makkah 21955, Saudi Arabia Department of Animal and Environmental Biology, University of Uyo, Uyo, Akwa Ibom State, Nigeria Department of Pharmacology and /erapeutics, Faculty of Veterinary Medicine, Damanhour University, Damanhour 22511, AlBeheira, Egypt


Background
Freshwater environments are exceedingly biodiverse. Freshwater constitutes only 0.8% of the earth' surface area with approximately 0.02% of the habitable volume of the Earth and contains about 30% of vertebrate species [1][2][3]. e freshwater is essential to human life, leading to humans traditionally dwelling along rivers and wetlands. is proximity of people to these water bodies constitutes declines in freshwater species and quality [4,5]. e IUCN [6] reported that 24.6% of freshwater species are threatened, while 27.0% fish species is threatened. Series of factors such as habitat loss, pollution, invasive species, over exploitation, and climate change are responsible for this loss in the freshwater biodiversity and quality [7,8]. ese factors affect the fish species biodiversity and parasite fauna of freshwater environments. Also, the spatial and temporal variability of intermittent rivers is likely to have a major influence on parasite diversity and abundance and on the dynamics of parasitic diseases because of their direct effects on parasite free-living stages and indirect effects on freshwater fishes [3].
Fish are rich source of protein to man and other animals. ey contain lipids, mineral oils, and vitamins which have a remarkable impact on the lives of many individual and communities [9,10]. Fish oils are known to contain omega-3 essential fatty acid which helps for the proper functioning of the brain, heart, and immune system [11]. Fishes interact at the various levels of food chain, thereby influencing the habitat structure [9]. Despite their significance to man, freshwater fish species are known for harbouring parasitic organisms by either serving as intermediate or definitive host of parasites which are harmful to man and animals [12].
ese parasitic protozoans and helminths are known to affect the health, growth, and survival of the fish while causing nutrient devaluation, alteration in biology and behaviour, lowering of the immune system, blindness, morbidity, mortality, fecundity reduction, and mechanical injuries [13].
Nigeria is blessed with many freshwater bodies of which rivers Niger and Benue are the two major freshwater bodies cutting across the country from north to south. Series of studies have been conducted on parasites of freshwater fish species in different parts of the Nigeria [14][15][16][17][18][19][20]. Little or no study was conducted on the parasites of the branchial chamber of freshwater fish.
is study was conducted to investigate the parasitic profile of the branchial and gastrointestinal tracts (GIT) of freshwater fish species from Niger and Benue rivers at Lokoja.

Study Area.
e study was carried out in Lokoja, Kogi State, Nigeria. It lies between latitude 7°40′N-8°10′N and longitude 6°40′E-7°10′E. Lokoja is a city situated at the confluence of Niger and Benue rivers having extensive flood plains with numerous perennial ponds and marshes on both banks of the rivers before and within the confluence. e vegetation along the rivers comprises mainly of wooded savannah grassland with shrubs and trees. e climate of the area consists of two seasons, the dry season and wet season. e wet season begins toward the end of March and ends towards the end of October or early December, while the dry season begins in November and lasts until late march. e annual rainfall ranges between 1016 mm and 1700 mm and mean daily temperature ranges between 25°C and 29°C [21]. ree (3) sampling sites were selected along the rivers: Irenedu village-along Lokoja-Koton-Karfe road (Niger River), Mozum village-located on the eastern bank (Benue River), and Chintaco village-downstream of the confluence (Figure 1).

Ethical Approval and Consent to Participate.
is study follows guidelines for the care and use of experimental animals established by the Animal Care and Use Committee of the Kogi State University, Anyigba, Nigeria, for the purpose of control and supervision of experiments on animals.

Collection of Fish
Samples. Fish samples were collected within a period of 12 months (May 2019-April 2020), with the aid of artisanal fishers using cast and gill nets of various mesh sizes. e fish were collected on ice and transported to the laboratory for subsequent analysis. e fish samples were identified using texts standard keys [22,23].

Sex Determination.
e sex of each fish was determined by physical observation of the urogenital papillae. It is long or distended in male, while in female, it is round and reddish in the matured ones. e sex was confirmed by internal examination after dissection to expose the paired testes in the males and paired ovaries in the females [24].

Examination of Fish for Parasites.
e two opercula of each fish were removed, and their inner sides were examined under the dissecting microscope. Recovered parasites were placed in 0.7% physiological saline; thereafter, the gills were dissected out, placed in Petri dish containing physiological saline, and examined with the aid of a dissecting microscope. Parasites found were noted, removed, and preserved in 4% formalin for further identification and classification. e GIT was removed from each fish and placed in a Petri dish containing physiological saline for examination as stated above.

Identification of Parasites.
e detected parasites were identified according to their morphology using a stereomicroscope. Standard keys for identification of fish parasites were used [25,26]. (1) e chi-square test was used to determine if any significant difference exists in prevalence between sexes, body parts, fish species, and parasites species, while the t-test was used to determine if any significant difference exists in prevalence between the gills and intestines of fish species examined. Analysis was performed using the Statistical Package for Social Science version 21.0 (SPSS Inc., Chicago, IL) at p ≤ 0.05.
Comparison of parasites harboured by the fishes revealed a significant difference (p ≤ 0.05) in their occurrence.  Table 3). Comparison of the prevalence of parasites in individual fish species revealed a significant difference (p ≤ 0.05) in Clarias sp., T. zillii, O. niloticus, and S. schall, while there was no significant difference (p > 0.05) in M. atlanticus (Table 3).

Sex-Specific Prevalence of Parasites in Fish Species.
e occurrence of parasites in sexes of fish species examined is presented in Table 4. Overall sex-specific prevalence of the parasites in the fish species examined revealed no significant difference (p > 0.05). Females had a prevalence of 80.3% (191 fish) higher than males with prevalence of 73.3% (148 fish) (    (Table 6).
In terms of the fish species, T. zillii harboured the highest number of parasites in the three locations, Mozum (96.8%), Chintaco (96.4%), and Irenedu (92.3%), while M. atlanticus harboured the least number of parasites in the three locations with prevalence of 37.0% (Chintaco), 78.2% (Irenedu), and 79.3% (Mozum). Significant variation (p ≤ 0.05) exists in the prevalence of the parasites in the fish species examined from the three locations (Table 7).

Discussion
is study showed a high parasitic infection in fish species from rivers Niger and Benue at Lokoja. is prevalence was higher than the prevalence of 59.2% observed in a study at Niger River at Illushi, Edo State [27], 17.1% in Osse River, Benin, Nigeria [28], 6.9% in Okhuo River, Benin, Nigeria [29], and 3.3% in Great Kwa River, Calabar [16]. e high prevalence of infection in this study could be due the high level of pollutants accumulation as a result of long distance travelled by both rivers as well as the influx of pollutants from their several tributaries [30,31]. Heavy parasitic infection in fish has been linked to environmental contamination by different pollutants including heavy metals and hydrocarbons [32] and organic enrichment of sediments by domestic sewage [33]. Other studies reported that urban effluents promote aquatic pollution, therefore making aquatic organisms vulnerable to increased incidence to parasites [34,35]. e high parasitic infection in this study might be due to the large influx of pollutants from the environment into the water bodies. Rohlenova et al. [36] reported that unfavourable temperature may alter fish physiology including immune function favouring parasite invasion. Other factors such as the behaviour and life history of the parasites and host fish might contribute to high parasitic infection [37].
A total of seven parasites species were found in fish samples from rivers Niger and Benue at Lokoja. Similar fish species were reported in a study carried out in Lake Gerio, Yola, Adamawa [15]; two of the parasites (Capillaria sp. and Contracaecum sp.) observed in this study were found in the Lake Gerio. Capillaria sp. was the second most prevalent parasite observed in their study with a prevalence of 16.7% higher than the prevalence of 10.5% observed in this study. Another study [38] on Clarias gariepinus in Owerri, Nigeria, reported the presence of Camallanus sp. (48.33%) and Contracaecum sp. (11.67%). In a study carried out on Clarotes laticeps, a fish species found in rivers Niger and Benue at Lokoja [18], they reported the presence of the Proteocephalus largoproglotis, Rhabdochona congolensis, and Contracaecum microcephalum alongside other parasites. e presence of the metacercariae of Clinostomum in the fish samples observed is an indicator of the presence of snails in the study sites which are the first intermediate hosts of parasites (Clinostomum). e metacercariae of Clinostomum is known to damage the muscles of fish, making it degusting and unsalable [39]. e high nematode parasites in fish host is an indication that the fish hosts feed on mud, debris, or detritus as found in most Clarias sp. and Synodontis sp. [40]. Hussen et al. [41] reported that helminths are mostly found in fresh water fishes where factors such as parasite species and its biology, host, and its feeding habitats, physical factors, hygiene of the water body, and presence of intermediate hosts contribute to their prevalence and intensity.
is study observed that female fish were more parasitized than male fish. Similar observation was reported in the studies by Mhaisen et al. [42], Ibiwoye et al. [43], and Amos et al. [15] that female fish are more infested than their male counterpart, while Biu et al. [44] disagree when they reported that variations in parasitic infection among the sexes of fish were by chance. Emere [45] reported differences      International Journal of Zoology 7

International Journal of Zoology
in the incidence of infestation between male and female fish, which may be due to differential feeding either by quantity or quality of feed or as a result of different degrees of resistance to infection. Also, the increased rate of food intake by the female fish to meet their food requirements for the development of their eggs might have exposed them to more contact with the parasites [17,46]. Studies by Paperna [47], Onwuliri and Mgbamena [48], and Oniye [49] have reported parasites of gills from different fish species.
e prevalence observed in this study is lower than what was observed in River Kaduna [17] and 17.7% in Kano [50]. No study in Nigeria has reported parasites from the gills of freshwater fish examined in this study. Majority of the parasites observed in this study were from the gastrointestinal tracts (GIT). e prevalence of these GIT parasites was higher than what was observed in the studies of Anosike et al. [51], Oniye et al. [52], and Dankishiya and Zakari [53] who reported prevalence of 34.70%, 19.17%, and 40.85%, respectively.  11.8%)). is study did not observe the influence of physicochemical parameters on parasites assemblage in fish species in Benue and Niger rivers. Future studies to establish the relationship between the physicochemical parameters and parasites assemblage are highly encouraged.

Data Availability
e datasets used to support the findings of this study are available from the corresponding author upon request.

Ethical Approval
is study follows guidelines for the care and use of experimental animals established by the Animal Care and Use Committee of the Kogi State University, Anyigba, Nigeria, for the purpose of control and supervision of experiments on animals.

Conflicts of Interest
e authors declare that they have no conflicts of interest.