Engraulicypris sardella (Günter, 1868) is a cyprinid fish exploited in the waters of Lake Nyasa that has been found to be infested by Ligula intestinalis (Linnaeus, 1758). Although L. intestinalis has been the subject of a number of studies, there is no information on the effects of this parasite on E. sardella. This study was therefore aimed at assessing the prevalence and intensity of the parasite L. intestinalis, condition of the fish and impact on fecundity of E. sardella. Data recorded for each individual fish included: total length, weight, sex and maturity stage, number of parasites, gonad assessment and egg count. Number, length and total weight of  L. intestinalis found per fish host were recorded.

The average infestation rate from the two landing sites (Matema and Kafyofyo) was 32.5%. Kafyofyo had the highest infestation rate (50%) and Matema (15%); on average, each infested fish had 1.7 parasites. The majority of infested fish carried one parasite (57%) with 23.1% having two parasites, 13.8% three parasites, 1.5% four parasites and 4.6% five parasites. There was significant difference between the weight of fish with parasites and those without parasites (P < 0.05). Mean length and weight of parasites was 73.6 mm and 0.25 g, respectively. There was also a significant difference between the weight of gonads of infested and non-infested fish (P < 0.05). The average weight of gonads from infested fish was 0.28 g, while that of non-infected fish was 0.32 g. Gonads of all infected fish were atrophied. Number of eggs (fecundity) decreased significantly with parasite infestation. Condition factors of both infected and uninfected fish did not show any significant difference (Mann-Whitney U-test P > 0.01). Therefore, it was concluded that L. intestinalis parasites affect fecundity and consequently inhibit the reproductive capacity of this cyprinid fish population.

Introduction

Lake Nyasa, situated in the western rift valley, is home to over 1000 fish species and reputedly has the largest number of endemic fish species of all lakes in the world. In Lake Nyasa, the pelagic waters support mainly cyprinid, cichlid, mochokid and clarid fish species (Allison et al., 1995). The lake plays a vital role in livelihoods and food security to people living near the lake and its basin. Engraulicypris sardella (Gutter, 1868) a small endemic cyprinid fish in Lake Nyasa locally called “Usipa”, is an important human food resource for the riparian countries of Malawi, Mozambique and Tanzania (Tweddle and Lewis, 1990). E. sardella forms an important part of the foodweb of Lake Nyasa. It is an important prey species for cichlids such as Copadichromis, Rhamphochromis, and Diplotaxoton (Allison et al., 1995). Its main food is zooplankton, particularly crustaceans. Copepods form about 50% of the food; it also feeds inshore on phytoplankton (green algae), other crustaceans (Cladocera), Rotifers (Trichocela), while offshore it feeds on Chaoborus edulis (Lake Fly) (Allison et al., 1995).

Ligula intestinalis, a whitish worm, dorso-ventrally flattened, is a cestode parasite that infects E. sardella in Lake Nyasa by filling the body cavity. Ligulids are important cestode parasites of cyprinid fish in lakes and reservoirs throughout the world (Kennedy, 1974; Dick and Choudhury, 1995; Bush et al., 2001; Loot et al., 2002). In Africa, infection by cestode larvae has been reported from fish of the Nile in Egypt and the Sudan and from the East African lakes (Paperna, 1980; Okedi, 1981).

Ligulids have a complex life cycle (Figure 1) involving copepods as the first intermediate host; fish act as the second intermediate host and piscivorous birds are the final host. Parasite eggs are deposited via bird faeces into water where hatching eggs release free-swimming coracidium larvae.

A parasitic relationship between L. intestinalis, a pseudophyllidean cestode in its plerocercoid stage and E. sardella (Figure 2) in Lake Nyasa has been observed since the year 1996. Thereafter in 2006, during J.K. Kihedu's MSc thesis data collection, the parasite was also seen (Kihedu, Sokoine University of Agriculture, Morogoro, Tanzania, 2006, unpublished). Although L. intestinalis has been the subject of a number of studies elsewhere in the world and despite the importance presently attached to E. sardella in Lake Nyasa, there is limited information on the effects of this cestode on E. sardella.

This research project therefore assessed the occurrences and effects of the parasite, L. intestinalis on the fish host, E. sardella at selected landing sites of Matema and Kafyofyo, situated on the extreme north of Lake Nyasa.

Method of study

Study site

Sampling was done in two fish landing sites, Kafyofyo and Matema (Figure 3), situated in the northern part of Lake Nyasa where it is accessible to artisanal fishers using dugout canoes. Each site was sampled weekly. Sample collection from artisanal fishers was the only option available at the study landing beaches; there are no large scale fishing operations at these sites.

Sampling

Samples of E. sardella were randomly purchased from local fishers who usually use light attraction for fishing. Sampling was carried out once per week from each site of Matema and Kafyofyo for a period of ten months (February–November 2007). Easy access to the two selected study sites was among the factors which determined the selection of the two landing beaches. A sample of 2000 gm was randomly taken and was then sub-sampled to 500 gm for assessment in the laboratory. Fish were visually inspected for the presence of larval cestode infection in their body cavity and were identified according to Van Dobben (1952) as Ligula intestinalis. Total Length (TL) to the nearest cm and weight of E. sardella were recorded. Individual weight was recorded using a sensitive electronic balance accurate to the nearest 0.01 gm. Fish were gutted for sexual maturity determination according to Nikolsky (1963) followed by removal of gonads and parasites. Length, weight, and number of parasites were also recorded. Females of E. sardella belonging to stages 4 and 5 (ripe and running, respectively) had their gonads taken for egg count and weight to establish fecundity. The states of gonad maturity and sex were assigned by viewing the gonads at tenfold magnification through a microscope. Condition factor (K) of the fish was assessed based on Fulton Condition Factor (1902). Data were analysed with respect to parasitic prevalence. Software Graphpad Instat Version 3 was used for statistical analysis of data, applying t-tests for some parametric independent samples, U-tests (Mann-Whitney test) for non-parametric independent samples and correlation to test the significance of variation between treatments.

Results

Infestation of the Plerocercoids of L. intestinalis in E. sardella from the two fishing grounds was on average found to be 32.5%. Kafyofyo had the highest infestation rate of 50% over Matema 15%. On average infested fish carried 1.7 parasites. The majority of fish analysed were found not to be infected, for those infected the majority carried one parasite (57%) with 23.1% having two parasites, 13.8% three parasites, 1.5% four parasites and 4.6% five parasites.

There was significant difference between the weight of fish with parasites and without parasites (P < 0.05, r = 0.15, n = 1061). Mean length and weight of parasites was 73.6 mm and 0.25 gm, respectively. The overall prevalence and parasite weight increased with total length of fish (Figure 4). Above 50 mm threshold value, a positive correlation between TL and infection rate becomes evident. Large fish of size class greater than 115 mm had higher chance of infestation than small fish. Intensity of the parasite did not show any correlation with the size of its host fish. Average number (intensity) was 1.5 parasites per fish of all size classes.

Length weight relationship of E. sardella

Length weight relationship of E. sardella shows that fish which were infected by L intestinalis had the value of b = 3.187 (allometric growth) compared to the fish which were not infected by the parasite which had a value of b = 3.0247 (isometric growth).

It was also established in this study that the length of E.sardella was positively correlated with that of the parasite L. intestinalis (Figure 5).

There was a significant difference between the weight of gonads of infested and non-infested fish (P < 0.05). The average weight of gonads from infested fish was 0.28 gm, while that of non-infected fish was 0.32 gm. Gonads of all infected fish were atrophied.

The present study results also showed that the number of eggs (fecundity) decreased significantly with parasite infestation. The average number of eggs of affected fish was 228 eggs while for unaffected fish it was 1628 eggs.

Condition factor (K) of both infected and none infected fish did not show any significant difference (Mann-Whitney U-test P > 0.01, n = 1057). The condition factors of uninfected fish were slightly higher compared to infected fish (Table 1).

Discussion

The rate of infection of fish caught in the two landing sites of Matema and Kafyofyo were found to be different; this might have been caused by higher rate of fish processing at the beach of Kafyofyo which attracted more infected birds than the beach of Matema. It was observed during data collection that due to poor infrastructure of Kafyofyo, fishers have the tendency of processing their fish at the beach. For Matema beach this was minimal.

Large fish of size classes greater than 105 mm have shown to be more infected by the parasites than small fish larger than 50 mm. Prevalence increases with the increase in body size of its host. The increase in prevalence reflects both accumulation of parasites over time as fish gets older and also a change in feeding habits of fish.

The higher infection rate in larger fish than in small ones can also be explained by the concept of diet shift whereby larger fish specialize in feeding on zooplankton (Allison et al., 1995), ingesting more copepods infected with tapeworms than small fish. Below a threshold of 50 mm length the infection rate was zero, probably due to poor preying capacity of such small fish on evasive copepods. Small fish of E. sardella feed mainly on algae, especially chlorophytes (Allison et al., 1995).

Results showed that fish which were not infected by the parasite L intestinalis had isometric growth while infected fish showed allometric growth. This clearly indicates that the growth of non-infected fish was isometric, which means the increase of length of the fish was proportional to the increase of its weight, no change of body shape as the fish grow. However, the growth of infected fish was allometric, which may have been the result of the smaller weight values of infected fish. Therefore, the increase of length of fish is not proportional with the increase of its weight; length is increasing more than the increase of its weight. As the fish grows the shape changed to become leaner (b < 3) or plump (b > 3). The present study's findings agree with other studies conducted elsewhere: Ergonul et al. (2005) in their study of the effects of L. intestinalis plerocercoids on the growth features of Tench, Tinca tinca in Lake Mogan, Ankara, Turkey who found that the growth of infected fish was allometric (b = 2.745), whereby for uninfected fish the growth was isometric (b = 3.014).

Results of condition factor (CF) showed that the conditions of both infected and non-infected fish were not significantly altered. The explanation for parasitized fish being in as good a condition as their non-parasitized counterpart can be attributed to the fact that some parasites become specialized for exploiting the reproductive organs of the hosts. This can be achieved directly by feeding on the gonads of the host or usurping the space normally allocated to gonads and eggs, or indirectly by diverting energy away from the gonad developments to somatic usage (Sorensen and Minchella, 1998). Usually, a castrated host diverts energy toward somatic growth instead of allocating it to reproduction (gigantism). Thus the conditions of parasitized fish were not altered because they spend very little energy for reproduction since their reproductive capacity has been significantly lowered by parasitism, and most of their energy is used for somatic growth. Condition factors give information when comparing two populations living under certain feeding, density and climate conditions: when determining the period of gonadal maturation and when following up the degree of feeding activity of a species to verify whether it is making good use of its feeding resources (Bagenal and Tesch, 1978). Braga (1986) and others showed that values of the condition factor vary according to seasons and are influenced by environmental conditions.

In the present study, it was found that all infected female fish had atrophied eggs (shrunken and compressed eggs) due to the number of eggs of the affected fish being smaller than that of the unaffected fish. It is therefore concluded that L. intestinalis reduces the fecundity of the host fish E. sardella. Findings from this present study agree with other studies conducted elsewhere. Paperna (1996), Van Dobben (1952) and Okedi (1981) reported that the tapeworm hamper the gonadal development and retarding maturation of the ovary of the host fish. Recently it has been reported by Nsinda et al. (2013) that the tapeworm reduces fecundity of Dagaa fish Rastrineobola argentea in Lake Victoria.

Conclusions

In conclusion, this study revealed that L. intestinalis plerocercoids caused the fish host to become infertile through inhibition of gonad development and decreased the fecundity of the fish host. In addition, the parasites caused rejection of parasitized fish at the market due to the ugly appearance of the parasite and therefore reduced the marketability of the fish.

Acknowledgements

The authors would like to thank the Netherland Fellowship Programme (NFP) who financed this study and Tanzania Fisheries Research Institute for provision of laboratory services.

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