Tanzania Journal of Science 46(1): 42-52, 2020 ISSN 0856-1761, e-ISSN 2507-7961 © College of Natural and Applied Sciences, University of Dar es Salaam, 2020

A Survey of Parasites from Pangani Catchment and Lake Kitangiri in Singida, Tanzania

Fred D Chibwana1*, Johnson G Mshana2 and Jestina V Katandukila1 1Department of Zoology and Wildlife Conservation, University of Dar es Salaam, P. O. Box 35064, Dar es Salaam, Tanzania 2Department of Science and Production, Sokoine University of Agriculture, P. O. Box 3004, Morogoro, Tanzania * Corresponding author: [email protected]; [email protected] E-mail co-authors: [email protected]; [email protected]

Received 22 Sep 2019, Revised 27 Dec 2019, Accepted 1 Jan 2020, Published 31 Mar 2020

Abstract Inland water fisheries are a significant source of dietary protein to human populations, and consequently they are essential economic activities worldwide. However, both natural waters and aquaculture systems, which form the freshwater fisheries are faced with a problem of fish parasitic diseases which may result in reduced productivity and market value. The present study, therefore, carried out a survey on fish parasites from the Pangani catchment (Nyumba ya Mungu dam and Lake Jipe) and Lake Kitangiri in Singida Region in Tanzania to seal the gap of occurrence, diversity and abundance of helminths. Three species of fish viz. 111 African sharptooth (Clarias gariepinus), 36 African butter catfish ( mystus) and 9 cichlid tilapia (Oreochromis amphimelas) were examined for parasites. Most were co-infected with two helminth genera, Contracaecum in the abdominal cavities and Tylodelphys in the cranial cavities with prevalences higher than 70%, while a few fish were infected with Diplostomum in the eyes’ vitreous humour and unidentified trematodes in the intestines. Pangani catchment and Lake Kitangiri were recorded as new localities for Tylodelphys species, and O. amphimelas as a new host species.

Keywords: Fish, Helminths, Nyumba ya Mungu Dam, Lakes Kitangiri and Jipe

Introduction increase in the human population, improved Freshwater fisheries industry has a livelihood incomes and the rise in significant contribution to development as a urbanisation coupled with stagnation or vital source of proteins. Besides providing decline of extra proteins further exacerbate food to millions of people, the freshwater the need for fish products. As a result, most fisheries contribute significantly to the overall communities globally have responded by economic incomes through export commodity venturing into aquaculture to enhance wild trade, tourism and recreation (Worldfish fisheries capture. Accordingly, as African Center 2002). As a consequence, the aquaculture advances, societies need to freshwater fisheries industry has become an address cross-cutting challenges including essential economic activity for both rural and lack of national policies to guide aquaculture urban populations in Africa and the globe. development, unfavourable investment The increasing gap between supply and policies, the absence of linkage between demand for fish products has further made farmers and conservation organs, limited fisheries capture the most substantial research/technology and extension, extractive use of wildlife worldwide. An inadequate quality seed and feed, and above 42 http://journals.udsm.ac.tz/index.php/tjs www.ajol.info/index.php/tjs/

Tanz. J. Sci. Vol. 46(1), 2020 all infectious and parasitic diseases (Hecht which is mostly incriminated in reduced fish and Endemann 1998, Brummett and Williams production. As such, a parasitological survey 2000). The occurrence of parasites and becomes obligatory to provide all parasitic diseases in natural and aquaculture stakeholders in the fisheries industry with a systems impairs fish productivity. better understanding of the potential parasites Helminthiasis is a common parasitic affecting small lakes fisheries in Tanzania. disease resulting from an infection with Therefore, the present study was initiated to monogeneans, trematodes, cestodes, determine the occurrence, diversity and nematodes and acanthocephalans. Some of abundance of helminths harboured by these helminths have a three host life cycle selected fish types from Nyumba ya Mungu involving snails/crustaceans as primary hosts, dam and Lakes Jipe and Kitangiri in fish as secondary hosts and piscivorous Tanzania. birds/mammals as definitive hosts. These helminths have attracted much attention Materials and Methods because of their pathogenicity in fishes in The study area aquaculture or natural systems. For instance, The present study was carried out in metacercarial stages of some trematodes like three water bodies, namely Nyumba ya Diplostomum may lodge in the eyes and brain Mungu Dam and Lakes Jipe and Kitangiri. cavities of fishes (Chappell et al. 1994, Nyumba ya Mungu is a human-made water Chibwana 2018). When at high densities, they reservoir that was constructed in 1965 for can cause haemorrhage, eye cataracts or hydro-electric power generation and irrigation cranial distortion that could ultimately result and fisheries activities. The dam is located in in reduced host survival and massive fish Pangani River Valley in the Masai Steppe, deaths in farms (Sandland and Goater 2001). approximately 10 km south of Mwanga town On the other hand, intestinal helminths in in Kilimanjaro, Tanzania (Figure 1). The dam fishes may lead to stunted growth. is maintained by two significant inflows: the Consequently, parasites can severely reduce rivers Kikuletwa and Ruvu. The dam is fish yields from the natural and/or connected to Lake Jipe through the River aquacultural systems and, therefore, become Ruvu, about natural 35 km to the east, but among the limiting factors for the 2030 geographically separated by the North Pare Agenda of the United Nations in achieving its mountain range. second Sustainable Development Goal (SDG) Lake Jipe is located along the border of zero hunger. between Tanzania and Kenya (Figure 1). The In Tanzania, so far fishes that have been lake is shared between two countries: 12 km2 examined for helminths are the clariids on the Tanzanian side and 14 km2 to Kenya as (Clarias gariepinus) from various freshwater part of Tsavo West National Park, which systems (Mwita and Nkwengulila 2008, covers the southern portion of the lake. It is a Chibwana and Nkwengulila 2010, Mwita small and shallow lake with an area of about 2014), the cichlids (Oreochromis urolepis) of 28 km2 and an average depth of less than 3 m. Mindu dam (Chibwana 2018) and cyprinids It is found in Mwanga district, in Kilimanjaro of Lakes Victoria and Malawi (Wanink 1992, Region. The lake has a length of Msafiri et al. 2014). Besides, fishes of some approximately 12 km, and a width of 2.5 km lakes such as Lake Jipe, Nyumba ya Mungu wide (Maltby 2009). Lake Jipe has the main Dam and other small water bodies have been inflow from Mount Kilimanjaro in Tanzania reported to experience stunted growth. through River Lumi with a meander in Kenya. Overfishing is, however, the only factor River Muvulani forms another main inflow

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Chibwana et al. - A survey of fish parasites from Pangani catchment and Lake Kitangiri together with other several temporary streams to Tulia River, has an area of length of 105 from the Pare Mountains. Ruvu River is the square kilometres (Reuben et al. 2017). only outflow which connects the lake to Various activities are conducted around the Nyumba ya Mungu. area such as aquaculture activities, fishing Lake Kitangiri is located in Singida and irrigation. region in Tanzania at latitude 4°4ʹ South and 34°17ʹ East (Figure 1). Lake Kitangiri, is next

Figure 1: Map showing the study sites, i.e., Nyumba ya Mungu Dam, Lakes.

Fish collection and parasites recovery and procedures (Moravec et al. 1991, The African sharptooth catfish (Clarias Anderson 1992, Eccles 1992, Khalil et al. gariepinus), the African butter catfish 1994, Gibson et al. 2002). The parasitological (Schilbe mystus) and the cichlid tilapia terms: prevalence and mean intensity of (Oreochromis amphimelas) were bought from infection were attributed according to Bush et artisanal fishers at Lakes Kitangiri and Jipe, al. (1997). The trematode metacercariae were and Nyumba ya Mungu Dam between recovered from the cranial cavity of Clarias January and February 2019. Fish gariepinus and eye’s vitreous humour of identification, examination for parasites and Oreochromis amphimelas, while nematodes their subsequent identification as well as were removed from abdominal cavity and parasites counting followed standard guides intestines (Plate 1).

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Plate 1: Infection sites (IS) of some parasites: diplostomids in the cranial cavity and anisakids in the abdominal cavity.

Data analysis prevalence, while bigger fish of between 31 Both descriptive and inferential statistics cm and 40.9 cm lengths had a prevalence of were used. Data did not fit the Gaussian 34.2%. The fishes measuring between 41 cm assumptions, so Spearman correlation and 50.9 cm long had the lowest prevalence coefficient was used to test if the lengths and of 18.5%. Similarly, 74.3% of Tylodelphys weights of C. gariepinus correlated with metacercariae were isolated from fish Contracaecum sp and Tylodelphys sp measuring 21 to 30.9 cm long, while 25.7% infections. Data for prevalence and mean of the parasites were recovered from 31 to 50 intensity with respect to sex and size of fish cm long fishes. were analysed by Chi-square. Tables and The overall prevalences of infection were charts for descriptive statistics were plotted in not significantly different in male and female Excel. fishes (Figure 2B) (x2 = 0.8637, P = 0.352708). Although the mean intensity of Results Tylodelphys sp was higher than that of Parasites in fish samples from Nyumba ya Contracaecum sp (Table 1), the variations Mungu were not significantly different (t = 1.508, P = Among the examined specimens of fish, 0.142). The correlations between fish 12 out of 15 (80%) were infected. The most condition parameters (body weight and host abundant parasites were Tylodelphys sp and length) and the two parasite families were not Contracaecum sp (Figure 2A) at a prevalence significant (Figure 2 C & D). However, of 33% and 67%, respectively. They were Contracaecum sp had a positive significant correspondingly recovered from the cranial correlation with host length (r = 0.622, P = and abdominal cavities. The fishes measuring 0.0132). The prevalences of parasites between between 21 cm and 30.9 cm long were sexes of fish were not significantly different infected with Contracaecum at 47.3% (x2 = 0.864, P = 0.3527).

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Chibwana et al. - A survey of fish parasites from Pangani catchment and Lake Kitangiri

Table 1: Prevalence, mean intensity and intensity range of Contracaecum sp and Tylodelphys sp for both sexes in Nyumba ya Mungu Dam Parasite Host sex Prevalence Mean intensity ± Intensity Site of Infection (%) std range Contracaecum sp Female 33.3 41 ± 32.81 9-88 Abdominal cavity Male 46.7 35 ± 54.30 2-154 Abdominal cavity Tylodelphys sp Female 13.3 764 ± 282.84 564-964 Cranial cavity Male 26.7 143.25 ± 139.61 20-304 Cranial cavity

Figure 2: The relationship between parasite intensity (number of parasites per host) and body conditions (length and weight) of fish from Nyumba ya Mungu Dam.

Parasites in fish samples from Lake of the eyes, and Contracaecum species in the Kitangiri abdominal cavity. The overall prevalence of In Lake Kitangiri, 80 fish, 35 catfish C. parasites in O. amphimelas was 66.67%. gariepinus, 36 African butter catfish S. Prevalence and intensities for parasites mystus, and 9 tilapia O. amphimelas, were recovered from S. mystus and O. amphimelas examined for parasites. A total of 1479 are also shown in Table 2. In Clarias parasites were isolated from the three host gariepinus, the most vulnerable fish were species. In C. gariepinus, 27 individuals were those with large body sizes, particularly those infected with helminths at an overall ranging from 27 to 48 cm, which confirmed prevalence of 77.14%. Two groups of the variation between infection and host sizes parasites were found, i.e., nematodes (x2 = 8.624, P < 0.025). Similarly, in S. (Contracaecum spp and unknown nematodes) mystus, 18–26 cm long fish were more and trematoda (Tylodelphys spp) and their infected than 9–17 cm long fish (x2 = 2.5, P < respective prevalences and intensities are 0.25). shown in Table 2. African butter catfish S. The prevalence and mean intensity mystus, were also infected with undescribed concerning sex were not analysed to avoid nematodes and Contracaecum, with an bias as in all species unequal numbers of overall prevalence of 61.11%. On the other males and female fish were examined due to hand, O. amphimelas were infected with availability. Diplostomum species in the vitreous humour

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Table 2: Prevalence, mean intensity (number of parasites per host) and intensity range of helminths recovered from fish species in Lake Kitangiri Host species Parasite No. fish No. fish Prevalence Mean Intensity Site of species examined infected (%) intensity range infection Clarias gariepinus Undescribed 35 7 20 2 1-8 Intestines nematodes Tylodelphys 35 21 60 125 1-5000 C. cavity Contracaecum 35 9 25.71 2.8 1 - 50 A. cavity Schilbe mystus Undescribed 36 22 61.11 4.64 1-10 Intestines Nematodes Contracaecum 36 29 80.56 6.662 1-23 A. cavity Oreochromis amphimelas Diplostomum 9 2 22.22 2 1-3 Eye Contracaecum 9 5 55.56 7 6-12 A. cavity Note: A = Abdominal; C = Cranial

Parasites in fish samples from Lake Jipe between sexes of hosts; male fish had a The catfish C. gariepinus from Lake Jipe heavier infection than females (x2 = 49.1853, were also infected with two major groups of P < 0.05). endo-helminths; nematodes (roundworms) Figures 3A and 3B show a relationship and the platyhelminths (flatworms). pattern of coinfection of anisakids and Roundworms Contracaecum (Family: diplostomid species in an individual catfish of Anisakidae) were abundant in the abdominal Lake Jipe. Although the sites of infection of cavity and Tylodelphys species (Family: Contracaecum and Tylodelphys species are Diplostomidae) were occupying the cranial far apart in the fish body, the intensities of cavity. The overall prevalence of diplostomid species in the cranial cavity were Contracaecum and Tylodelphys infection negatively correlated with those of were 86.89% and 85.14%, respectively (Table Contracaecum in the abdominal cavity. For 3). The prevalences of infection between the instance, fishes that were infected with more parasite families were not significantly than 5000 individuals of diplostomid species, different (x2 = 0.017, P > 0.9). There was no they had no Contracaecum species. Similarly, significant infection variation between male fishes that were infected with 181 individuals and female fish with either diplostomids or of Contacaecum species (the highest intensity anisakids (x2 = 0.019, P = 0.8902). Also, the value) harboured zero diplostomid species chi-square statistic of 0.04 at a p-value of (Figures 3A and B). Numerically, diplostomid 0.841 showed no significant variation in species were more than Contracaecum (t = infection between young and adult catfish. 6.157, P =1.06  10–8) as depicted by Figures There was, on the other hand, a significant 3A and B. difference in the intensities of infection

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Chibwana et al. - A survey of fish parasites from Pangani catchment and Lake Kitangiri

Table 3: Prevalence, mean intensity (number of parasites per host) and intensity range of helminths recovered from Clarias gariepinus species in Lake Jipe No. fish Prevalence Intensity of infection (No. parasite Host Parasite species examined (%) per fish host) Mean Range Std Error Total Tylodelphys spp 61 86.89 679.98 3-5880 166.78 Contracaecum sp 61 85.25 32.35 1-181 4.55 Male Tylodelphys spp 40 87.5 475.44 3-5500 155.73 Contracaecum sp 40 87.5 56.33 1-181 22.73 Female Tylodelphys spp 21 85.71 874.85 4-5880 328.87 Contracaecum sp 21 80.95 18.45 2-54 3.73

Figure 3: The relationship between intensities of anisakid and diplostomid species (number of parasites per host) in coinfected Clarias gariepinus from Lake Jipe.

Discussion family, the Clariidae. This study, on the other This study provides baseline information hand, has dealt with three families of fish: on fish parasites in small lake systems, i.e., Clariidae, and Cichlidae. Lakes Jipe and Kitangiri and Nyumba ya However, its scope was similar to Mwita Mungu Dam. Similar studies in Tanzania (2014), i.e., to examine all helminths in a have been mostly conducted in Lake Victoria particular host, unlike Chibwana and and Mindu Dam Tanzanian (Musiba and Nkwengulila (2010) that intended to study Nkwengulila 2006, Mwita and Nkwengulila diplostomids occurring in the cranial cavities 2008, Chibwana and Nkwengulila 2010, of C. gariepinus. Mwita 2014). However, this study differs The findings of the current study have from the previously mentioned reports by its revealed the presence of roundworms and inclusion of more fish species from different flatworms infecting a wide range of fishes families. For instance, Musiba and irrespective of waterbody under study. Nkwengulila (2006) and Chibwana and Among these parasites, the trematodes, Nkwengulila (2010) explored the parasites of Tylodelpys (Family: Diplostomidae) and only one fish species, Clarias gariepinus, nematode Contracaecum, of the (Family: while Mwita and Nkwengulila (2008) and Anisakidae) were the most common. Sites of Mwita (2014) examined parasites of only one infection (i.e., eyes and the cranial cavities)

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Tanz. J. Sci. Vol. 46(1), 2020 for Tylodelphys and their closely related diverse parasites at varying intensities. genus Diplostomum, have been frequently Furthermore, C. gariepinus is omnivorous reported (Musiba and Nkwengulila 2006, (Awachie and Ezenwaji 1981), which makes Mwita and Nkwengulila 2008, Chibwana and it prone to infection by many parasites. The Nkwengulila 2010, Madanire-Moyo and fewer parasite species found in the present Barson 2010, Chibwana et al. 2013, Mwita study corroborate Woolnough et al. (2009) 2014, Tavakol et al. 2015, Chibwana 2018). view that water body size and shape influence Similarly, the occurrence of Contracaecum both species interactions (i.e., host-parasite species in the abdominal cavities of fish is interactions), genetic changes, resource use common (Mwita and Nkwengulila 2008, and mate choices. Mwita 2014). Moreover, both diplostomids Generally, the parasitological status for and anisakids are common parasites of catfish majority of fishes in Tanzania is incomplete, in natural and human-made freshwater and S. mystus and O. amphimelas are not systems in Tanzania (Musiba and exceptional. S. mystus have been studied, Nkwengulila 2006, Mwita and Nkwengulila though not extensively in Sudan (Khalil 1969) 2008, Chibwana and Nkwengulila 2010, and Egypt (El-Naggar 1985). Both studies Mwita 2014) and elsewhere in Africa reported the occurrence of a monogenean, (Madanire-Moyo and Barson 2010, Tavakol Schilbetrema aegyptica in gills. The present et al. 2015). study, on the other hand, has recorded two The prevalence of parasites in the present nematode species in S. mystus in the small study was higher than previously reported. intestine and abdominal cavity with a Out of 156 fish examined, 102 were infected prevalence of more than 80%. Parasitic with parasites. Three known and one infections in S. mystus were also significantly unknown species of helminths were isolated correlated with sex and body size in which from 102 infected fish collected from the case, large-sized fish and males were more three freshwater bodies Nyumba ya Mungu preferred by parasites than small-sized and Dam, and Lakes Jipe and Kitangiri. The females. It could be attributed to more endoparasites comprised of Contracaecum internal spaces for parasite occupancy in larvae from all the fish species studied; two larger-sized than smaller-sized fish. The digenean metacercariae (Tylodelphys species elevated levels of oestrogen are suggested to complex in C. gariepinus and Diplostomum protect female hosts from parasitic infections sp from O. amphimelas); and unidentified (Mwita 2014). nematodes from C. gariepinus and S. mystus. Furthermore, O. amphimelas, which is This number of species was supprisingly endemic to Lakes Kitangiri, Singida, Manyara much smaller than reported for catfish alone and Eyasi in Tanzania, is one of the in other freshwater bodies. Mwita and endangered fish species in the world. As such, Nkwengulila (2008) and Mwita (2014) a parasitological study in this species had not recorded 13 species from C. gariepinus from been carried out. The findings of the present Lake Victoria. Nkwengulila and Mwita survey have shown O. amphimelas being (2008) argued that the intensity and diversity infected with Diplostomum metacercariae in of the parasites could be influenced by diet the vitreous humour of the eye and and vagility of the host intensities (see Contracaecum larvae in the abdominal cavity. Balbuena and Raga 1993, Holmes and Bartoli The presence of Diplostomum metacercariae 1993), and highly vagile fish such as catfish trematodes in the eyes of O. amphimelas can transverse a wide range of habitats and might further reduce their populations thus increasing chances of being infected by because fish heavily infected with the

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Chibwana et al. - A survey of fish parasites from Pangani catchment and Lake Kitangiri metacercariae may lose vision, experience although fishes from inland water bodies are a reduced growth and subsequently cause death good source of protein (an alternative to red of the fish (Chappell et al. 1994, Chappell meat), if not well prepared they can be 1995, Niewiadomska 1996). detrimental to our health. Thorough The present study also reported the preparation or cooking of fish is highly superabundance of nematode larvae of the recommended to avoid consumption of genus Contracaecum under the family metacercariae of harmful parasites. Since Anisakiidae from all the fish species and aquaculture settings rely upon the natural water bodies studied. Nematode species systems (rivers and lakes) for belonging to this family include parasites of seedling/fingerlings, we recommend the use significant economic and medical importance of fingerlings of the second or third because of their capability to infect humans generation to avoid keeping infected fish from (Oshima 1987). This ability is facilitated by the wild. their three host life cycles, which involve invertebrates and fish as first and second Acknowledgements intermediate hosts, respectively; and We thank the University of Dar es Salaam piscivorous fish, sea mammals, mammals and for funding this research through a provision fish-eating birds as definitive hosts (Levsen et of a research grant (UDSM Research Grants, al. 2008). Humans succumb to anisakids CoNAS-ZLW18059), without which the infection upon consumption of uncooked or study would not have been possible. Besides, undercooked fish, resulting in we appreciate the continual support offered to hypersensitivity and allergic reactions us by the University of Dar es Salaam induced by proteins produced by dead particularly the Department of Zoology and parasites or epigastric pain related to the Wildlife Conservation, for frequently presence of living parasites (Buchmann and allowing us to be away from the station of our Mehrdana 2016). Nematodes of the family duty for fieldwork. We also recognise the Anisakidae are ubiquitous and occur in Asia, services of Mr Richard Massinde of the Europe, Africa, and America (Dadar et al. Department of Zoology and Wildlife 2016). Accordingly, the occurrence of Conservation for his technical assistance in anisakids (Contracaecum larvae) in the three the field and laboratory. water bodies studied and all fish species studied is a warning sign to potential risks of References consuming raw or underprepared fish. Anderson RC 1992 Nematode parasites of vertebrates: their development and Conclusion transmission. CAB International, The present study has explicitly shown Wallingford, UK. that fishes from Pangani catchment (Lake Jipe Awachie JE and Ezenwaji GMH 1981 The and Nyumba ya Mungu Reservoir) and Lake importance of Clarias spp. in the fisheries Kitangiri in Singida, are susceptible to development of the Anambra River basin, parasites and parasitic diseases. The fishes Nigeria. CIFA Technical Papers (FAO). harbour parasites of medical, veterinary and Balbuena JA and Raga JA 1993 Intestinal economic importance, i.e., Diplostomids helminth communities of the long-finned (Diplostomum and Tylodelphys) in the cranial pilot whale (Globicephala melas) off the cavities of Clarias gariepinus and eyes of Faroe Islands. Parasitol. 106: 327-333. Oreochromis species, respectively. Anisakids Brummett RE and Williams MJ 2000 The (Contracaecum), on the other hand, inhabit in evolution of aquaculture in African rural the abdominal cavities of almost every fish and economic development. Ecol. Econ. species in the studied areas. It implies that 33: 193-203.

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