Prevalence of ecto- and endo-parasitic infections of farmed tilapia and catfish in Nyeri County, Kenya

S K Mavuti¹, R M Waruiru², P G Mbuthia², J G Maina³, J M Mbaria⁴ and R O Otieno²

¹ Directorate of Veterinary Services, Ministry of Agriculture, Livestock and Fisheries, Kenya
stekitong@yahoo.com
² Department of Veterinary Pathology, Microbiology and Parasitology, Faculty of Veterinary Medicine, University of Nairobi,
P.O. Box 29053-00625, Kangemi Nairobi, Kenya
³ Department of Animal Production, Faculty of Veterinary Medicine, University of Nairobi,
P.O. Box 29053-00625, Kangemi Nairobi, Kenya
⁴ Department of Public Health, Pharmacology and Toxicology, Faculty of Veterinary Medicine, University of Nairobi,
P.O. Box 29053-00625, Kangemi Nairobi, Kenya

Abstract

The objective of the present study was to determine the prevalence of fish parasites in farmed tilapia and catfish in Nyeri Central and Tetu sub-counties of Nyeri County, Kenya.  A total of 366 live fish comprising of 89 (24.3%) catfish and 277 (75.7%) tilapia were caught using a seine net and purchased from 15 fish farmers between August 2014 and November 2015. One hundred and fifty eight (158/366; 43.2%) fish were from liner ponds while, 108/366 (56.8%) were from earthen ponds. Eyes, skins, gills, muscles, stomachs and intestines of the farmed fish were examined for parasites using dissecting and compound microscopes.

The results showed that 115 of the fish were infected with one species of ecto- or endo-parasite in the gills, skin, muscle, eye or gastro-intestinal tract, giving an overall prevalence of 31.4%. Parasitic infection rate was significantly higher (p < 0.05) in tilapia (67.8%; 78/115) relative to catfish (32.2%; 37/115) and there was no significant difference (p > 0.05) in fish parasite infestation rates between earthen (52.2%; 60/115) and liner (48.8%; 55/155) ponds. The prevalence of liner pond parasitic infection was relatively similar between catfish (56.4%; 31/55) and tilapia (43.6%; 24/55). However, in earthen ponds, there were significant differences (p<0.05) between catfish (10%; 6/60) and tilapia (90%; 54/60).

Nearly 15% (57/366) of fish examined had gill monogenean flukes (Dactylogyrus spp.), 8.2% (30/366) had metacercariae nodules of Clinostomum spp. in the muscles, 2.7% had leeches on the gills and 1.9% had Diplostomum spp. in the eyes. Other parasites identified were Trichodina spp. (1.4%), Acanthocephala spp. (0.8%),Contracaecum spp. (0.5%), Gyrodactylus spp. 0.5% and Paracamallanus spp. (0.5%), respectively. The parasites reported may affect the health and quality of fish leading to condemnation at inspection. 

Key Words: fish parasites, flukes, infestation, nematodes, protozoa, sub-counties

Introduction

The explosive interest in fish farming stimulated by the Economic Stimulus Programme poses new challenges to the fish industry in Kenya ranging from poor knowledge of ideal management practices, nutritional requirements for optimum productivity, environmental pollution, biosecurity and spread of fish diseases (Munguti et al 2014). Fish diseases especially parasitic infections also constrain fish farming in Kenya (Fiovaranti et al 2007). Parasitic diseases, either alone or in conjunction with other environmental stresses, may influence weight or reproduction of the host, alter its population characteristics, or affect its economic importance (Rhode 1993).

Freshwater fish are considered important sources of parasitic infection to man and fish eating mammals (Mohamed 1996). The World Health Organization (1995) estimated that the number of people currently infected with fish borne trematodes exceeds 18 million.

Research by Aloo (2002) and Gichohi (2010) have documented the occurrence of endoparasites such as Polyacanthorhynchus, Amirthalingamia, Cyclustera, Proteocephalus, Contracaecum and Procamallanus in wild fish from fresh water lakes and rivers. Kamundia (2011) reported prevalence of Procamallanus, Contracaecum, Camallanus, Acanthocephala and Trypanosoma spp. in fish from Lake Victoria.

In Nyeri County, riverine waters are used to feed the fish ponds and there is therefore a possibility of parasites being introduced to farmed fish. Very little research has been undertaken to determine and document farmed fish parasites, their pathological effects and their effect on production in Kenya (Mbuthia 1993; Gichohi et al 2008). The present study aims to determine the prevalence and identity of fish endo and ecto parasites in farmed tilapia and catfish in Nyeri County. This information will help in developing preventive and control measures against disease-causing parasites of farm fish in Kenya.

Materials and Methods

Study area

The study was carried out in  Nyeri Central and Tetu sub-counties of Nyeri County situated between longitudes 36038 East and 37020 East; between the Equator and latitude 00 380 south. Temperature ranges between 12 and 27 ^oC while, annual rainfall ranges between 550mm in the lowland and 1500mm in the highlands. The two sub-counties have rivers/streams which are the source of water to the fish ponds where tilapia (Oreochromis niloticus) and catfish (Clarias gariepinus) are farmed.

Study design

A 15 month longitudinal study was undertaken in the two study areas where fish were purchased from farmers between August 2014 and November 2015.

Study fish

A total of 366 fish were obtained using a seine net mesh 1cm by 1cm and transferred to a container with water obtained from the pond where the fish came from and immediately transported to the Nyeri County veterinary laboratory for necropsy.

Postmortem examination

Live fish were stunned with a single blow to the back of the head and pithed to separate the central nervous system from the spinal cord. The skin was examined grossly for ectoparasites. Thereafter, skin scrapings were taken and examined under a dissecting microscope and parasites seen recorded. The gills, liver, peritoneal cavity, swim bladder, spleen, heart, and musculature were examined grossly and under a dissecting microscope for helminths. The abdominal, pericardial and peritoneal cavities and the eyes were also checked for parasites. Worms collected were preserved in 70% ethanol prior to identification.

Examination of gastrointestinal content for parasites

The gut was separated into stomach and intestines, preserved in 70% ethanol. The contents of each gastrointestinal segment were expressed out and examined in 0.64% physiological saline and thin transparent intestinal or stomach sections placed on slide and dissected with dissecting needles to expose contents which were examined at various magnifications for worms, worm eggs, flagellates and cysts according to Roberts (1989) and Untergasser (1989).

Processing and identification of helminths

On isolation, Platyhelminthes and acanthocephalans were fixed in hot formal saline (4%) solution for 24 hours, washed in distilled water for another 24 hours and then stored in 70% ethanol before identification. The whole mounts in 70% ethanol were downgraded to water, stained by Gower’s Carmine stain followed by a slow differentiation in 0.5% hydrochloric acid (HCL) in 70% ethanol for 1-12 hours depending on the size of the worms. Platyhelminthes sections were stained using Heidenhain´s azan stain (Roberts1989). Worms collected from the body cavity were preserved in 70% ethanol, manually counted and recorded. Trematodes were identified using morphological features as described by Cone (1995) and Paperna (1995). Nematodes and acanthocephalans were identified using morphological features as described by Anderson et al (1974) and Food and Agriculture Organization (1996).

Identification of ectoparasites

Ectoparasites were identified using morphological features as described by Untergasser (1989) and Woo (1995). Parasite distributions were described using prevalence as described by Margolis et al (1982) and Ford (1988).

Results

Prevalence of catfish and tilapia parasites in Nyeri County

Of the 366 fish sampled, 115 were infested with one species of either ecto- or endo-parasite in the gills, skin, muscle, eye or intestinal tract giving an overall prevalence rate of 31.4%.

Of the infected fish, 78/115 (67.8%) were tilapia while, 37/115 (32.2%) were catfish.

Sixty eight out of 115 (59.1%) of fish infested with parasites were from Tetu while, 47/115 (40.9 %) were from Nyeri Central (Table 1). Out of the 115 infested fish, 60 (52.2%) were from earthen ponds while, 55/115 (48.8%) were from liner ponds.

Prevalence of parasite species infesting catfish and tilapia

Two digenean trematodes [Clinostomum spp. (found in muscles) and Diplostomum spp. (found in the eye)], a gill Dactylogyrus spp. and a skin monogenean (Gyrodactylus spp.), two nematodes [Contracaecum spp. (found in abdominal cavity) and Paracamallanus spp. (found in intestines)], a protozoan, Trichodina spp. (found in gills and skin)], leeches (from the gills) and an Acanthocephalus spp. (from the intestines) (Table 2) were recovered from fish in this study.

Prevalence of monogenean trematodes

Dactylogyrus spp. was recovered from the gills of both tilapia and catfish. This parasite had a scalloped head (Figure 1) with eye spots anteriorly. Of the 366 fish sampled, 54 fish were infested by this parasite giving an overall prevalence of 14.8%. Over 51% (28/54) of fish infested were catfish while, 26/54 (48.1%) were tilapia (Table 3).  Nyeri Central had 30/54 (55.6%) fish infested by this parasite while, Tetu sub-county accounted for 24/54 (44.4%) (Table 3). Forty two out of 54 (77.8%) fish infested by this parasite were from liner ponds while, 12/54 (22.2%) were from earthen ponds.

Gyrodactylus spp. was recovered from the skin of catfish only with an overall prevalence of 0.5% (2/366). This parasite had a V-shaped head, did not have eye spots and had an opisthohaptor at the posterior end (Figure 2). All the 2 catfish infested by this parasite came from Nyeri Central Sub-county. One of the catfish infested was from an earthen pond while the other was from a liner pond (Table 3).

Figure 1: Anterior end of Dactylogyrus spp. anchored in the gills (B) of a tilapia fish showing a scalloped head (arrow)

Figure 2: Gyrodactylus spp. from the skin of a catfish showing a V-shaped head (V) and an opisthohaptor (O)

Prevalence of digenean trematodes

Clinostomum spp. was isolated from tilapia fish only with an overall prevalence of 8.2% (30/366). They appeared as white, yellowish or orange coloured spots on the skin and in the muscles as cysts (Figure 3).The metacercariae of Clinostomum spp. were oval, with a smooth body, dorsoventrally flattened, and with a sucker around the anteroventral mouth and an additional sucker or acetabulum.  Of the 30 tilapia fish infested, 22 (73.3%) were from Tetu while, 8/30 (26.7%) were from Nyeri Central (Table 4). Earthen ponds registered a 90.0% (27/30) infestation by Clinostomum spp. while, liner ponds had only 10.0% (3/30) infestation rate.

The metacercariae of Diplostomum spp. (“eye flukes”) had a cup-shaped fore body with the suckers, and a cylindrical hind body containing the immature gonads and were found free in the vitreous humour of the eyes (Figure 4). The digenean was only found infesting tilapia with an overall prevalence of 1.9% (7/366). All the 7 tilapia fish infested by this parasite were from Tetu Sub-county and they were all from earthen ponds.This parasite was neither recovered in catfish nor fish from Nyeri Central Sub-county (Table 4).

Figure 3: Cystic lesions on the skin of a tilapia fish infested with Clinostomum spp. (arrows)

Figure 4: A Diplostomum spp. metacercariae isolated from the vitreous humour of a tilapia fish (arrow)

Prevalence of nematodes

Contracaecum spp. larvae (L₃) were isolated from the abdominal cavity of catfish with a   prevalence of 0.5% (2/366).Of the 2 fish infested, 1 was from Tetu while, the other was from Nyeri Central. Liner and earthen ponds had each 1 catfish infested by Contracaecum spp.

Paracamallanus spp worms were recovered from the intestines of fish. It had a bilaterally symmetrical buccal capsule which was divided into two levels; a smaller anterior part with vertical chitinoid plates for attachment to gastrointestinal mucosa and a larger cavity behind the valves (Figure 5). Only male worms were isolated in this study and had a ventral caudal papillae and a spicule.This parasite was recovered in 2/366 fish (1 tilapia and 1 catfish) with a prevalence of 0.5%. The infested fish were fromTetu Sub-county. Liner pond had 1 catfish while, earthen ponds had 1 tilapia infested by Paracamallanus spp.

Figure 5: A Paracamallanus spp. from tilapia fish showing the vertical chitinoid plates (A) and the buccal cavity divided into two levels: - the upper smaller – (B) and lower larger parts (C) X 10

Prevalence of Acanthocephala spp.

These worms were tiny, bilaterally symmetrical, and they possessed a spined retractable proboscis (Figure 6a) which was sometimes invaginated in a saccular receptacle (Figure 6b). The worms were isolated from tilapia fish from earthen ponds in Tetu Sub-county and had a prevalence of 0.8% (3/366).

Figure 6: Anterior end of an Acanthocephalan spp from a tilapia fish showing a spined proboscis (arrow A) and an invaginated proboscis (arrow B)

Prevalence of Trichodina spp.

This parasite was observed from the skin of fish. Key characteristics were cilia for locomotion, round shape when seen from top of the parasite (dorsally) and a ring with hook - like denticles (Figure 7). Trichodina spp. was observed in both fish species with an overall prevalence of 1.4% (5/366). Four out of 5 (80.0%) of the fish were tilapia while, 1/5 (20.0%) were catfish. Sixty percent of the fish infested were from Tetu with the remaining 40% (2/5 being from Nyeri Central sub-county. All infested fish were from earthen ponds.

Figure 7: Round shaped Trichodina spp. from a catfish showing cilia (C) and denticle (D)

Prevalence of leeches

Leeches were observed in both catfish and tilapia in the gills. These parasites were larger than monogeneans and were differentiated from the latter by the presence of body segmentation. They differed from typical free living annelids since they possessed an anterior and a posterior sucker. These parasites infested fish with an overall prevalence of 2.7% (10/366). Out of 10 fish infested 70% were tilapia while, 30% were catfish. Fish from Tetu had higher infestation rate (70%) relative to 30% from Nyeri Central sub-county.

Discussion

This study has shown that farmed tilapia and catfish from Nyeri County in Kenya are infested with various ecto- and endo-parasites in the gills, skin, muscle, eyes or intestinal tract with an overall prevalence of 31.4%. Tilapia fish had a higher prevalence than catfish and this may be attributed to more tilapia fish being sampled compared to catfish as few farmers kept catfish.

The proportion of tilapia fish from earthen ponds infested by fish parasites was significantly (p<0.05) high (90%) compared to catfish (10%). Tilapia fish have scales and this predisposes them to trematode attachment and infestation while catfish have a slimy body which makes it difficult for monogeneans to attach. The existing weeds around the ponds offered a good condition for the propagation of the intermediate hosts of digenean trematodes, the snails.

Catfish from liner ponds had a significantly higher parasite infestation rate (56.4%) compared to tilapia (43.6%) and the difference between the two fish species could not be explained during this study. Poor fish pond management practices such as low fish pond water levels, lack of pond emptying after fish harvesting and pollution allows a conducive environment for propagation of fish parasites. Prolonged exposure to this condition predisposes both fish species to infestation by parasites.

The parasites recovered from this study were: two digenean trematodes;Clinostomum spp. and Diplostomum spp., two monogeneans; Dactylogyrus spp. and Gyrodactylus spp., two nematodes; Contracaecum spp. and Paracamallanus spp., a protozoan; Trichodina spp., a leech and an Acanthocephalus spp. Trematodes comprised a higher percentage (80.9%) followed by leeches (8.7%), protozoa; 4.3%, Nematodes; 3.4% and Acanthocephalus spp.; 2.7% of the parasites recorded. No cestodes were recovered in fish during this study. The study documents the occurrence of the monogenean fluke Gyrodactyus spp. and leeches for the first time in farmed catfish and tilapia in Kenya.

The higher prevalence of trematodes infestation observed is in line with reports of other workers (Falieva 1971; Onwuliri and Mgbemena 1987) which showed heavy infestation by trematodes in their studies. Gichohi (2010) reported in his study that nematodes comprised the larger percentage of parasites (30.3 %) in a field study followed by tapeworms (4.6 %) and trematodes (2.6 %) respectively. This is similar to other previous findings of helminth infections in Africa by other researchers (Barson and Avenant-Oldewage 2006).  Mathew et al (2014) in their study in Morogoro, Tanzania observed a higher prevalence of Trichodina spp. and monogeneans.

Dactylogyrus spp. was recovered from the gills of both tilapia and catfish with an overall prevalence of 14.8%. Ozturk and Ozer (2014) reported prevalence values of 74.1%, for Clarius carpio in wild fish in Turkey. Their data was higher than what was observed in the present study. These differences could be attributed to difference in fish species and environmental factors in different geographical areas where the studies were conducted.

Fish from liner ponds had a significantly higher infestation rate (77.8%) with Dactylogyrus spp. in relation to those from earthen ponds (22.2%). The life cycle of most monogeneans involves only one host and they mostly spread by way of egg releasing and free-swimming infective larvae. The earthen ponds in Nyeri were all constructed on a wetland with water going through the fish pond. The running water might have carried away with it any infective larvae while the liner pond water is stagnant and favours the multiplicity of infective larvae.

Catfish from liner ponds had a significantly high (61.9%) parasite infestation rate with  Dactylogyrus spp. compared to tilapia (38.1%). Catfish are generally larger in body size than tilapia of relatively the same age. Poulin (2000) stated that in fish population, parasitic infection tends to increase with increasing host age and size. Munoz and Cribb (2005) reported that larger hosts had higher parasites richness, abundance and intensity than smaller ones. Generally large hosts have more space and microhabitats for parasites than small hosts.

Acanthocephalus spp. was isolated from the intestines of tilapia fish only with a prevalence of 0.8%.  This was in agreement to Kamundia (2011) who observed a rate of infection with Acanthocephalus spp. of 1.8% in Oreochromis  niloticus from Homa Bay. Gichohi (2010) observed Acanthocephalus spp. in wild tilapia at a prevalence of 10.1 %. His observations were higher than in this study.

Skin monogenean fluke (Gyrodactylus spp.) was recovered from the skin of catfish only with an overall prevalence of 0.5%. Prikrylova et al (2012) described Gyrodactylus malalai sp. nov. from the fin surface of cichlid fishes, Oreochromis niloticus and Tilapia zillii caught in Lake Turkana, Kenya but not in farmed catfish. Otachi (2009) recovered monogenean dactylogyrids and gyrodactylids in caged Oreochromis niloticus in Machakos and   Sagana open fish ponds.

Clinostomum spp. was isolated from tilapia fish in the skin only with an overall prevalence of 8.2%. The infection in the farmed tilapia was probably due to the availability of the intermediate hosts, the common snails around the earthen ponds. Gichohi (2010) working in River Tana, Kenya found Clinostomum spp. only in farmed tilapia with a prevalence of 14.7 % in the skin. Aloo (2002) found Clinostomum spp. on the skin of tilapia fish in Lake Naivasha and Oloiden bay in Kenya. Zekarias and Yimer (2008) reported the occurrence of Clinostomum spp. in the brachial cavity of tilapia from Awassa dam in Ethiopia.

Tilapia fish from Tetu had a significantly higher Clinostomum spp. infestation (73.3%) relative to fish from Nyeri Central (26.7%). This was probably due to the higher number of earthen ponds with subsequent abundance of snail intermediate hosts. In liner ponds, enhanced management practices such as control of weeds and the piscivorous birds (definitive hosts), probably reduced the chances of the intermediate hosts transmitting Clinostomum parasites.

Trichodina spp. was observed in the skin of both fish species with an overall prevalence of 1.4%.The higher infestation in earthen ponds may be attributed to poor pond management practices (low water levels, lack of pond emptying after fish harvesting and pollution) which may predispose propagation of parasites.

Leeches were observed in both catfish and tilapia gills with an overall prevalence of 2.7%. Tilapia fish had a significantly higher prevalence (70%) than catfish (30%) in this study. Iyaji and Eyo (2008) reported in Nigeria that 19% of all studied silver catfish harboured leeches at the external perimeters of the mouth region. Gichohi (2010) and Kamundia (2011) in Kenya did not observe leeches in their studies.

Diplostomum spp.was only found infesting tilapia in the vitreous humour of the eyes but not catfish with a prevalence of 1.9%. Otachi (2009) in his work in Machakos and Sagana, Kenya isolated mainly free living diplomastid; Tylodelphis spp. in thevitreous humour at prevalences of 47.3 % and 41.6 % in farmed open and caged pond tilapia, respectively. Gichohi (2010) in upper Tana River basin, Kenya observed Diplostomum spp. with a prevalence of 54.3 % in tilapia relative to catfish (18%). His observations were in agreement with those of Violante-Gonzalez et al (2009) in Mexico in tilapia. In this study, all the fish infested by Diplostomum spp. were from earthen ponds due to availability of the intermediate hosts.

Contracaecum spp. larvae were isolated from the abdominal cavity of catfish. Gichohi (2010) reported an overall prevalence of 33.8 % infestation with Contracaecum spp. in catfish and tilapia in River Tana, Kenya. Aloo (2002) recorded the Contracaecum spp. in Oreochomis leucocystis and Tilapia zilli from Lake Naivasha and Oloiden bay in Kenya. Kamundia (2011) reported a prevalence of infestation with Contracaecum in O. niloticus from Dunga Beach in Lake Victoria was 41.4% and in L. niloticus 36%. In Homa Bay, 1.8% of the O. niloticus fish were found to be infected with Contracaecum spp. in the same study. This study did not record Contracaecum spp. in tilapia fish since this may be a parasite of wild fish more than farmed fish. It could as well be a parasite of catfish more than tilapia as was observed by Malvestuto and Ogambo-Ongoma (1978). Catfish are omnivorous and feed voraciously on all intermediate hosts including other smaller fish and their young ones, who may be infested, thus accumulating the worms (Malvestuto and Ogambo-Ongoma 1978). Gichohi (2010) noted that farmed tilapia and catfish had a lower prevalence (0.8 % and 18.5 %, respectively) of Contracaecum spp. compared to wild fish (tilapia 11.6% and catfish 40.7%). There was no significant difference in the infestation rate of Contracaecum spp.  among the sub counties and pond types.

Paracamallanus spp. was recovered from the intestines of both catfish and tilapia with an overall prevalence of 0.5%.  Gichohi (2010) isolated these helminths in catfish only and mainly from the intestines with a few from the stomach at a prevalence rate of 52.8%.  There was no significant difference in the infestation rate of Paracamallanus spp. among the fish species and the fish pond types in the present study.

Conclusions

• This study has shown that farmed tilapia and catfish from Nyeri County in Kenya are infested with both ecto- and endo-parasites.

Acknowledgements

The authors are grateful to the United States Agency for International Development (Peer Science Project) for financial support. We also thank the Nyeri fisheries officers and fish farmers for supporting this work.

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Received 15 February 2017; Accepted 9 May 2017; Published 1 June 2017

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