Prevalence, intensity and influence of water quality on parasites of farmed fish in Kirinyaga County, Kenya

R M Waruiru¹, P G Mbuthia¹, D W Wanja^1,2 and J M Mwadime³

¹ Department of Veterinary Pathology, Microbiology and Parasitology Faculty of Veterinary Medicine, University of Nairobi, P.O. Box 29053-00625, Kangemi, Nairobi, Kenya
rmwaruiru@yahoo.co.uk
² Animal Health and Industrial Training Institute (AHITI) Kabete, P.O. Box 29040-00625, Kangemi, Nairobi, Kenya
³ Institute of Primate Research P.O. Box 24481-00502 Karen, Nairobi, Kenya

Abstract

Parasitic infestation in fish can lead to severe retarded growth and may be accompanied by mortalities. Importantly, the quality of water in the holding facility may influence the parasitic biota. Therefore, a cross-sectional study was carried out from December 2017 to April 2018 in Kirinyaga County, Kenya, to determine the prevalence, intensity and the relationship between physico-chemical parameters of water and farmed fish parasites. A total of 294 live fish (Oreochromis niloticus, Clarias gariepinus, Carassius auratus and Cyprinus carpio carpio) were purchased from 22 randomly selected fish farms within the county. Physico-chemical parameters of water in 31 ponds were assessed in situ and ex situ, following standard procedures. Sampled fish were dissected immediately and subjected to parasitological examination by visual observation and light microscopy. The overall prevalence of parasitic infestation of the fish examined was 26.5% (78/294); with the highest infestation recorded in Nile tilapia (73.1%; 57/78). Eight parasite genera were recovered, with Diplostomum and Acanthocephalus species dominating each at 6.5% (19/294). The highest mean intensity was observed in Neascus spp. at 190 with an abundance range of 4-596 parasites. Mean physicochemical parameters of water were: pH (7.4), dissolved oxygen (5.9mgl^-1), water temperature (25.3°C), phosphates (1.1mgl^-1), nitrites (0.3mgl^-1), nitrates (29.3mgl ^-1) and ammonia free nitrogen (0.8mgl^-1). The water temperature and dissolved oxygen were below the optimal limit, while pH, ammonia, nitrites and phosphates levels in some ponds were above the desired limit for fish farming. Parasitic prevalence was positively correlated with ammonia free nitrogen, nitrates and phosphates, while there was a significant correlation between dissolved oxygen and abundance of the digenean trematode, Clinostomum cutaneum. These findings show that farmed fish harbour several parasite genera which may be influenced by physico-chemical characteristics of pond water. Fish farmers are advised to regularly monitor pond water quality in order to minimize fish stress and parasitic infestations; thus improving aquaculture productivity. Further long-term studies are recommended to determine the effect of water quality on parasitic fauna of farmed fish.

Key words: aquaculture productivity, Clinostomum cutaneum, Diplostomum, dissolved oxygen, Neascus

Introduction

Warm freshwater aquaculture in Kenya encompasses food fish (Oreochromis niloticus and Clarias gariepinus) and ornamental fish (Carassius auratus and Cyprinus carpio carpio) farming. In the recent times; there has been remarkable growth in aquaculture with marked intensification. Even though, Kenya like most tropic countries has long periods of warm weather that is ideal for proliferation of ecto- and endo-parasites; a major risk of diseases comes from intensification.

Fish parasitic diseases are a result of imbalance in interaction between fish and parasite factors and aquatic environment (culture) conditions. However, occurrence and magnitude of these diseases is closely related to sanitary conditions in water (Hossain et al 2007). Any characteristic of water quality is therefore the most important key to a successful fish production. Any characteristic of water that affects the survival, reproduction, growth, or management of fish is a water quality variable (Noga 2010). It is postulated that water pollution influences the pathogenicity potential of ecto- and endo-parasites (Khan and Thulin 1991); while in fish the same poor water quality increases disease susceptibility (Biswas and Pramanik 2016), by lowering the defense and immunogenic status of the fish (Noor El-Deen et al 2015).

Environmental factors such as water temperature, dissolved oxygen, salinity, hydrogen ion concentration and eutrophication have a positive influence on the occurrence of parasitic populations and communities (Ali et al 2004; Lagrue et al 2011; Zargar et al 2012; Ojwala et al 2018). Stress is related to lower water quality (lower values of dissolved oxygen, inadequate values of temperature, pH, and high levels of organic matter in the water), which provide a good environment for proliferation of protozoan parasites and occurrence of pathogenic agents, mainly the body surface parasites like ecto-protozoans of fish (Paulista et al 2009).

Parasites are recognized as an important limiting factor in the development of intensified fish culture; where they result in massive mortalities and reduced growth rates (Iwanowicz 2011). Legion studies on parasitic infestations in culture fish in Kenya have been carried out antecedently (Migiro et al 2012; Khamis et al 2017; Mavuti et al 2017; Maina et al 2017; Murugami et al 2018; Mukwabi et al 2019; Wanja et al 2020); however most of these studies have focused on the systematics with little attention in determining the association of water quality parameters in influencing the presence of fish parasites. Under pond culture conditions, a number of natural abiotic factors, particularly from water quality may influence the presence of parasites. Thus, this study was conducted with the intention to determine occurrence of parasites and to evaluate the effect of physico-chemical characteristics of water on parasitic infestation in farmed fish in Kirinyaga County, central Kenya.

Materials and methods

Ethical statement

Prior to commencement of this study, ethical clearance was approved by the Biosafety, Animal Use, Care, and Ethics Committee of the Faculty of Veterinary Medicine, University of Nairobi. Verbal consent was also sought from fish farmers enumerated in this study.

Study area and design

A cross-sectional study that involved fish sampling for parasitological examination and pond water quality assessment was carried out from December 2017 to April 2018 in Kirinyaga County. Kirinyaga County is situated in central Kenya between 0°39'S latitude and 37°12'E longitude, at an elevation of 1230m above sea level. The county has five sub-counties namely: Mwea West, Mwea East, Kirinyaga West, Kirinyaga Central and Kirinyaga East. The county was purposively selected owing to high number of active pisciculturists (Anonymous 2018). A total of 22 fish farms were engaged and most farmers cultured tilapia in liner fish ponds. Parasitological examination was done by visual observations and by light microscopy, while water quality features was assessed in situ and ex situ at the time of sampling, following American Public Health Association (2008) guidelines.

Water quality assessment

Pond water quality was assessed in 31 ponds (the same ponds in which fish sampling was done) in the morning (between 0800 and 1000 hours) on the day of fish sampling. Physico-chemical parameters of water including pH, temperature and dissolved oxygen were measured in situ using a portable waterproof HANNA Multiprobe meters (Hanna Instruments Inc., USA) at three different points of the pond. Water samples were collected for spectrophotometry chemical analysis for; phosphates, nitrites, nitrates and ammonia free nitrogen at Government Chemist, Kenyatta National Hospital, Kenya.

Fish collection

A total of 294 fish samples were harvested using a seine net from 22 smallholder fish farms distributed across all the five sub-counties of Kirinyaga County. Of these, 162 were Nile tilapia (Oreochromis niloticus), 80 were African catfish (Clarias gariepinus), and the rest were ornamental fish [goldfish (Carassius auratus) and koi carp (Cyprinus carpio carpio)]. Live sampled fish together with source pond water were immediately transferred to the County Veterinary Laboratory, Kerugoya town for parasitological assay.

Macroscopic and necropsy examination

An external examination of individual live fish was performed visually to check for any ectoparasites and gross lesions according to methods described by Woo (2006) and Noga (2010). The examined fish were euthanized and post-mortem examination was done using standard necropsy procedures (Noga 2010; Roberts 2012). Briefly, a midline incision was made with a sterile scalpel blade starting at the anterior end of the anal opening to the operculum. A lateral cut from the anal opening on the abdominal wall of the fish up to the upper corner of the operculum was made to expose the abdominal organs. The body wall was then deflected and the organs observed grossly in situ using methods described by Amlacher (1970); any pathological lesions present were noted and recorded. A third cut connecting the two previous incisions at the operculum was made to remove the skin and muscular flap.

Wet mount preparation, parasitological examination and identification of parasites

Wet mounts of skin scrapings and/or slime and gill filaments were obtained on slides on a drop of physiological saline and examined under light microscope for ectoparasites at X10 and X40 (Lucky 1977). The eyes contents were eviscerated on a clean slide and checked for ocular trematodes. The gastrointestinal tract was collected and preserved in 70% ethanol for parasitological examination. The contents were later emptied in a petri dish with normal saline (0.85% Sodium chloride) and examined for parasites using a dissecting microscope. Microscopic parasites were collected by a special needle; then washed for several times in warm saline solution and left in the refrigerator until the specimens had died and completely relaxed. The identification and characterization of parasites was performed using morphological features as described by others (Chubb et al 1987; Paperna 1996; Woo 2006; Noga 2010; Roberts 2012).

Data analysis

Collected data was validated, entered and stored in Microsoft Excel which was also used to calculate means and proportions. Parasitic infestations were evaluated using epidemiological parameters i.e., prevalence, mean abundance and mean intensity of infestation as described by Margolis et al (1982) and Bush et al (1997). Pearson’s correlation was used to establish the correlation co-efficient between different physico-chemical parameters and parasitic infestations.

Results

Composition and levels of parasitic infestation in sampled Fish

Out of 294 fish sampled and examined, 26.5% (78/294) were infested by one or more parasite species. Eight fish parasite species were isolated, identified and recorded as; Diplostomum spp., Neascus spp., Clinostomum cutaneum, Gyrodactylus spp., Dactylogyrus spp., Acanthocephalus spp., Piscicola spp. and Pseudophylledian cestodes. The most prevalent parasite genera were Diplostomum and Acanthocephalus each at 6.5%, with a mean intensity of 32.7 and 4.4, respectively (Table 1). The highest mean intensity was observed in Neascus spp. at 190.3 with a parasite density of 4-596 (Table 1). Majority of the parasites were recovered from the skin, while the rest were infesting the gills, intestines/gut, eyes, fins and muscle. Of the 78 infested fish, 73.1% (57/78) were Nile tilapia, 15.4 % (12/79) ornamental fish and the rest were African catfish.

Necropsy and microscopic findings

Digenean trematodes

Diplostomum spp. were identified by their cylindrical hind body containing the immature gonads (Figure 1) and were found actively swimming alive in the vitreous humor of examined Nile tilapia and African catfish.

Figure 1. Diplostomum spp. recovered from Nile tilapia and African catfish in Kirinyaga County, showing cylindrical hind body (black arrow)

Clinostomum cutaneum appeared as yellowish grubs/cysts on the skin of Nile tilapia. They were dorso-ventrally flattened, oval, with a sucker around the anterior mouth and an acetabulum. They had a digestive system consisting of a pharynx connected to the mouth opening and a short esophagus and two blind intestinal caeca (Figure 2).

Figure 2. Yellow grubs on the skin (red arrows) and metacercariae of Clinostomum cutaneum recovered from muscles of Nile tilapia (white stars shows intestinal ceca of metacercariae)

Metacercaria of the genus Neascus appeared as black grub/spots averaging 1-2mm in diameter on the fins, mouth, skin, gills and eyes in Nile tilapia (Figure 3); with no observable/significant post-mortem findings.

Figure 3. Multifocal black spots on the tail fin (red arrows) of Nile tilapia due to Neascus spp. metacercariae infestation

Monogenean worms

Adult worms of the genus Dactylogyrus were isolated from gills of Nile tilapia. They were recognized by the prohaptor bearing the four-lobed head with four eye spots and reproductive organs Gyrodactylus spp. were recovered from the skin of tilapia and identified by their anchor hooks at the posterior end.

Spiny headed worms

Acanthocephalus spp. were recovered from intestines of a tilapia and identified by their characteristic protruding proboscis (Figure 4).

Figure 4. Acanthocephalus spp. showing spiny proboscis (arrow) recovered from intestines of Oreochromis niloticus in Kirinyaga County

Leeches

Piscicola spp. are macro-ectoparasites which were found attached to the skin of Nile tilapia. The leeches were identified by anterior/oral and caudal suckers with a sub-cylin­drical elongate body. Piscicola spp. infested fish had excess mucus grossly with pale friable liver at necropsy (Figure 5). There were no significant findings seen in other visceral organs.

Figure 5. Detached Piscicola leeches (black arrows) recovered from Nile tilapia whose liver was pale and friable (inset)

Cestodes

Cestodes were identified by their segmented body (proglottids) and an anterior attachment organ (scolex) (Figure 6).

Figure 6. A cestode showing sucker (black arrow) recovered from intestines of Oreochromis niloticus in Kirinyaga County

Water quality

The mean and range values of some physico-chemical parameters of 31 pond water samples, against recommended limits for fish culture are tabulated in Table 2. Most ponds evaluated had water temperature below the recommended limit for fish rearing; while a few had pH levels above the recommended limit. Levels of nitrates were within the optimum range for pisciculture (Table 2).

Comparison of physicochemical parameters of water parameters and parasitic prevalence and abundance

Table 3 shows the water quality parameters against prevalence of parasites in that particular pond and their respective correlation coefficient and interpretation. Parasitic prevalence was positively correlated with ammonia free nitrogen, nitrates and phosphates in the study area (Table 3).

The correlation matrix between some independent variables (temperature, dissolved oxygen, pH and ammonia free nitrogen), and the dependent variable (parasitic abundance) is given in Table 4. There was a significant positive correlation (r = 0.5; p<0.05) between dissolved oxygen and Clinostomum cutaneum abundance (Table 4).

Discussion

In Kenya, more attention is being focused nowadays to the intensification and commercialization of aquaculture to mitigate the dearth of aquatic protein. There is little effort towards fish health especially diseases. This is despite the fact that, fish diseases including parasitic ones can inevitably exerts deleterious effects ranging from extremely damaging to insignificant change on the host.

Fish parasites were isolated in 26.5% of the fish collected from smallholder fish farms in Kirinyaga County. This finding was similar to a study by Maina et al (2017) that investigated occurrence of parasites in farmed Nile tilapia and African catfish in Kiambu County, Kenya. Parasitic infestations were found in all the four fish species examined with a higher prevalence recorded in Oreochromis niloticus compared to Clarias gariepinus, Carassius auratus and Cyprinus carpio carpio. A similar finding was reported by Mavuti et al (2017); in a study investigating ecto- and endo-parasitosis in farmed tilapia and catfish in Nyeri County. Higher infestation among tilapia may be due to high stocking density which is a common practice in tilapia culture and therefore may facilitate rapid propagation of parasites. In the present study; monogeneans, digenean trematodes, acanthocephalans, cestodes and leeches were recovered from examined farmed fish from Kirinyaga County.

Three digenean trematodes were recorded in this study; Diplostomum spp., metacercaria of Neascus spp. and Clinostomum cutaneum. Previous studies have reported occurrence of Diplostomum spp. and metacercariae of Clinostomum cutaneum (Gustinelli et al 2010; Mavuti et al 2017; Murugami et al 2018). Diplostomum spp. was found swimming in the vitreous humor of both catfish and tilapia without causing major pathological defects. However, higher number of Diplostomum worms in the eye of the host may result to blindness and are more prone to predation (Seppala et al 2005).

Metacercariae of Neascus spp. were observed in the skin, muscles, eyes, fins, gills of tilapia at a prevalence of 4.1% and a mean intensity of 190 cysts per infested fish. These findings are in disagreement with those of Thon et al (2019) who reported a prevalence of 1% and mean intensity of 1 in the skin of tilapia in Winam Gulf of Lake Victoria, Kenya. Skin metacercariae of C. cutaneum were isolated from tilapia only at a prevalence of 3.1%. This finding is partially in line with Gichohi (2010) and Mavuti et al. (2017); who reported this parasite in farmed tilapia, however at higher prevalence in both studies. Clinostomum cutaneum was isolated in both fish and piscivorous birds (grey heron) in recent studies undertaken in Sagana Aquaculture Center, Kirinyaga County (Gustinelli et al 2010; Murugami et al (2018). Metacercariae of Neascus spp. and C. cutaneum causes black spot and yellow grub diseases, respectively. The resulting diseases make the fish unsightly thereby causing economic losses due to rejection (Lane and Morris 2010). Human cases of C. complanatum infestation have been reported in Japan (Hara et al., 2014) and Korea (Chung et al 1995; Kim et al 2019) and hence a public health concern.

The monogeneans recovered in this study were; Dactylogyrus and Gyrodactylus species and these findings are similar to those of Mavuti et al (2017). However, Dactylogyrus spp., a gill parasite was dominating; being isolated in all the four fish species examined. Gyrodactylus spp. which is generally found on the skin and fins of fish was recovered from tilapia only. This is contrary to a study by Mavuti et al (2017) and Murugami et al (2018) in which Gyrodactylus species was found in catfish only. Gyrodactylus and Dactylogyrus species are the two most common genera of monogeneans that infest freshwater fish with cultured tilapia being more susceptible compared to wild ones (Lim et al 2016). Monogeneans are important pathogens in aquaculture systems where fish are in high stocking densities and in confined environments (Hecht et al 1998). They propagate rapidly and are readily transmitted among fish and, if left uncontrolled high morbidity and mortality can occur in farmed fish leading to serious economic loss to farmers (Shinn et al 2015).

Acanthocephalus species were isolated from intestinal wall of tilapia, catfish and goldfish with overall prevalence of 6.5%; contrary to the findings of Mavuti et al (2017) and Kamundia (2012) who observed the worms in tilapia only and at lower infestation rate. The findings also contradicts studies of Aloo (2002) and Akoll et al (2012) who all reported it encysting in the intestinal wall and in the liver of tilapia. Ingestion of isopods, amphipods, and/or copepods by the fish has been attributed with acanthocephalan infestations (Paperna 1996; Ngasepam et al 2015). In heavily infected fish acanthocephalans may perforate the gut wall with their proboscis and cause considerable damage with severe local inflammatory reaction (Jithendran and Kannappan 2010).

Cestodes of the family Pseudophyllidae were recovered from the intestines of tilapia and catfish with an overall prevalence of 1.7%. This is contrary to work by Murugami et al (2018); where Pseudophyllidean and Proteocephallid cestodes were isolated from catfish.

Water quality is an important factor when it comes to fish health management. Of the 31 fish pond water samples assessed in this study; 11 (36%), 10 (33%), 5 (16%) and 2 (6.5%) exceeded the recommended limits of < 0.03-2 mgl^-1, <0.2 mgl^-1, < 0.02 mgl ^-1 and <8.5 of phosphates, ammonia free nitrogen, nitrites and pH, respectively. High levels of phosphates and nitrates could be attributed to chemical fertilization of crops within the vicinity of the pond. The soluble chemicals may still end up into the pond through leaching from the soil into water. High ammonia levels may be due to overfeeding of fish especially with highly proteinous feeds or high pond stocking densities which may lead to build up of nitrogenous wastes (mainly ammonia) from fish. The slightly higher pond water pH (slightly alkaline) may be attributed to soil alkalinity and/or pond liming. Water temperature and dissolved oxygen levels in 58.1% and 22.5% of the pond water samples, respectively, were below the optimum limit for fish rearing. Kirinyaga County has a tropical climate which is influenced by its position on the equator and the Mount Kenya. Temperature ranges from 8.1 to 30.3°C (Anonymous 2018). Levels of dissolved oxygen are positively influenced by temperature (Bhatnagar and Devi 2013).

In the present study, occurrence of parasites was positively correlated with ammonia free nitrogen, nitrates and phosphates. The findings are partially in line with that of Ojwala et al (2018) who reported a positive correlation of various parasitic assemblage and some physicochemical characteristics of pond water including; nitrates and soluble reactive phosphates. However, the present findings are contrary with those of Puinyabati et al (2013), who reported a positive correlation of prevalence of trematode parasites in Channa punctata (spotted snakehead) with dissolved oxygen, pH, conductivity and water temperature. Abiotic factors particularly ones inclined to pond water characteristics have been recognized as an important bottleneck factors in the biological activity of the culture facility (Ngasepam et al 2015). For instance, water quality attributes have been associated with occurrence of digenean trematodes and other parasites (Chubb 1979). This study observed that dissolved oxygen and intensity of C. cutaneum were correlated positively (p<0.05) and this finding has not been reported in Kenya before. However, the findings are contrary to those of Zargar et al (2012).

Conclusions

• Digenean trematodes, monogeneans, acanthocephalans, cestodes and Piscicola leeches were recovered from farmed food and ornamental fish in Kirinyaga County
  
  
• Levels of ammonia free nitrogen, nitrates and phosphates were positively correlated with prevalence of parasitic infestation
  
  
• Dissolved oxygen demonstrated a significantly positive correlation to the occurrence and intensity of Clinostomum cutaneum
  
  
• Findings of this study will generate information necessary for understanding relationship between fish parasites and water quality features; this will help in designing non-therapeutic measures for preventing or managing fish diseases in aquaculture facilities in the future
  
  
• Farmers are advised to take better care of their fish ponds by frequently monitoring water quality of ponds, fish behavior, and water color for any abnormal changes

Conflicts of Interest

The authors have no conflict of interest, financial or otherwise, regarding this publication.

Acknowledgments

We wish to acknowledge the Norwegian Agency for Development Cooperation (NORAD) for financing this work under the capacity building for Training and Research in Aquatic and Environmental Health in Eastern and Southern Africa (TRAHESA) for financing this study. We thank the fisheries extension officers for assistance in locating farms; and fish farmers for their cooperation.

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