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African Journal of Aquatic Science 2003, 28(2): 14

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AFRICAN JOURNAL OF
AQUATIC SCIENCE
ISSN 16085914

The occurrence of the tapeworm, Ligula intestinalis (L.), in Barbus paludinosus from a small dam in Zimbabwe
Maxwell Barson1, 2* and BE Marshall1
1

Department of Biological Sciences, University of Zimbabwe, PO Box MP 167, Mount Pleasant, Harare, Zimbabwe
Present address: Department of Zoology, Rand Afrikaans University, PO Box 524, Auckland Park 2006, Johannesburg,
South Africa
* Corresponding author, e-mail: barson001@yahoo.co.uk
2

Received 9 May 2003, accepted in revised form 25 August 2003

Cestode parasites were collected from Barbus paludinosus from Munwahuku Dam near Harare, Zimbabwe over a period of 13
months. Plerocercoids of Ligula intestinalis were found in 7.2% of the fish. The majority of the infected fish carried one parasite,
with 3.1% having two and 1.6% with three. There was a positive correlation (r = 0.59, P < 0.05) between the weight of L. intestinalis
and that of their host, but there was no significant relationship between the condition factor of the fish and the weight of the parasite, and the parasite index was low (7.97 3.38) compared to previous studies in South Africa. The gonads of all infected fish were
atrophied. The prevalence of L. intestinalis in B. paludinosus was high between July and September 2000 and low thereafter. There
was no clear seasonal variation in the occurrence of the parasite, although the lengthy dry season might have had an effect on the
prevalence.
Keywords: Barbus paludinosus, Ligula intestinalis, parasite prevalence, parasite index, mean parasite intensity, Zimbabwe

Introduction
Together with nematodes and flukes, tapeworms (Class:
Cestoda) are among the most important helminth parasites
of fish (Roberts and Janovy 2000). Ligula intestinalis (L.)
(Diphyllobothriidae) is a cosmopolitan tapeworm that infects
cyprinid fishes and fish-eating birds, and is indigenous to
southern Africa (Prudhoe and Hussey 1977). Its eggs are
shed in the birds faeces and hatch in water to form infective
coracidia, which are ingested by copepods (Hoole 1994).
Cyprinid fish become the second intermediate hosts when
they eat parasitised copepods and are infected by the second-stage larva or plerocercoid (Hoole 1994).
Ligula is a significant fish parasite because heavy infestations induce host mortality, which is a threat to the commercial fisheries industry. It also causes pathological conditions such as the distension of the hosts body wall, muscle
and gonadal atrophy, lowered condition factors and a number of physiological and immunological disorders (Szalai et
al. 1989, Wyatt and Kennedy 1989, Hoole 1994). Adult
gravid ligulids in the final bird hosts disseminate their eggs
over large areas through the hosts droppings, making it difficult to control infection in wild fish populations (Kennedy
and Burrough 1981). There is concern over human health
risks associated with the eating of infected fish, especially
when raw or not properly cooked.
While cestode parasites of fish have been recorded from
many parts of Africa (Mashego 1982, Van As and Basson
1984, Paperna 1996, Khalil and Polling 1997), rather few

studieshave been done in Zimbabwe. In Lake Kariba, five

species of cestodes, including L. intestinalis, were found in
the intestines and body cavities of nine fish species including Clarias gariepinus (Burchell), and Barbus fasciolatus
Gnther (Chishawa 1991, Doullou 1992). The parasite has
also been found in B. paludinosus Peters and B. lineomaculatus Boulenger caught near Harare (Mettrick 1960), as well
as in Mesobola brevianalis (Boulenger) from the Runde
River in southeastern Zimbabwe and B. paludinosus from
Udu Dam, Nyanga (BE Marshall unpublished data).
This paper gives the results of an investigation into tapeworm infestation in B. paludinosus from Munwahuku Dam, a
small farm reservoir near Harare. This fish species was chosen because of its numerical dominance, relative abundance in the system and its tolerance to pollution. It was part
of a more detailed investigation of fish parasitism and was
the first attempt in Zimbabwe to determine the prevalence,
intensity, and seasonal pattern of parasites in this fish
species (Barson 2003).
Materials and methods
Specimens of B. paludinosus were collected monthly from
July 2000 to July 2001 using 8mm, 10mm and 12mm nylon
monofilament nets and fyke nets in the upper Munwahuku
Dam, a small farm dam about 20km west of Harare,
Zimbabwe. The fish were killed immediately after collection

Bason and Marshall

and examined macroscopically for ectoparasites. They were

then transported to the laboratory where their standard
length and weight were measured. The body cavity of each
fish was searched for plerocercoids of Ligula intestinalis and
the weight of each plerocercoid recorded. The worms were
killed in warm water (60C), fixed in 10% formalin for 24h
and transferred to 70% ethyl alcohol for permanent preservation.
The parasite index (PI) for each infected fish was calculated using the formula:
Wp X 100

where Wp= weight of parasite (g) and Wh = weight of host (g)

(Kennedy and Burrough 1981, Bean and Winfield 1989).
The condition of the fish was determined by Fultons condition factor (K), in which:
K=

45

Wh Wp

(W X 100)
L3

where W = weight (g), and L = standard length (cm)

(Bagenal and Tesch 1978). Keys in Yamaguti (1959) and
Schmidt (1986) were used to identify the parasites.

40
35
PREVALENCE (%)

PI =

The prevalence of L. intestinalis in B. paludinosus in the

Munwahuku Dam was within the range of that of other
Barbus and Labeobarbus species in some South African
reservoirs (Table 1), while the intensity was similar to that
recorded by Saayman et al. (1991) and Mashego (1982)
from South Africa, which rarely exceeds one parasite per
fish. However, high parasite intensities of up to 30 for Ligula

An unexpected consequence of dam-building in southern

Africa may have been to expose riverine fishes like B.
paludinosus to increased levels of parasitism by cestodes
like Ligula, caused by increasing the numbers of the first
intermediate host copepods, which are generally more
numerous in standing than in running waters (Wetzel 2001).
This suggestion is supported by the fact that fish from the
Munwahuku Dam were sometimes quite heavily parasitised,
whilst none of those collected in a previous survey from the
nearby Marimba River were infected (Barson 2003).

20

10
5
J

O N

D J F
2000-2001

Figure 1: The prevalence (%) of Ligula intestinalis in Barbus paludinosus from Munwahuku Dam between July 2000 and July 2001

0.8
LIGULA WEIGHT (g)

Discussion

25

15

Results
In the 885 B. paludinosus collected from the Munwahuku
Dam, the parasite prevalence was 7.2% and the intensity
ranged from 13 (mean = 1.1). Relatively large samples of
B. paludinosus (mean = 53.7 per month) were collected in
JulySeptember 2000, and the prevalence of parasites was
high, but fewer (22.3 per month) were collected during the
period OctoberDecember 2000 when the prevalence was
low. Only one (1.6%) of the 64 infected fish harboured three
tapeworms, two of them (3.1%) had two tapeworms and the
remainder had only one parasite in the body cavity.
The prevalence of L. intestinalis in the fish from the
Munwahuku Dam was high (2146%) between July and
September 2000 but low (<6%) at other times (Figure 1). A
prevalence of zero was recorded in October and December
2000 and in July 2001. There was a positive correlation
between the weight of Ligula and the weight of the host
(Figure 2), but there was no significant relationship between
the condition factor of the fish and the weight of the parasite
(Figure 3). The parasite index ranged from 0.7 to 16.3 with a
mean of 8.0. The gonads of all infected fish were atrophied.

30

y = 0.046 + 0.064x
r = 0.59, P > 0.05

0.6

0.4

0.2

BARBUS WEIGHT (g)

Figure 2: The weight of Ligula intestinalis parasites in relation to the
weight of their Barbus paludinosus hosts from Munwahuku Dam.
Broken lines indicate 95% confidence limits

African Journal of Aquatic Science 2003, 28: 14

Table 1: The prevalence and intensity of Ligula parasitism in some Barbus and Labeobarbus species from southern African impoundments.
N = sample size, P = prevalence (%), MI = mean intensity. Sources 1: Saayman et al. (1991), 2: Mashego (1982) and 3: this study

Locality
Munwahuku Dam
Middle Letaba Dam
Middle Letaba Dam
Luphephe and Seshego Dams
Luphephe and Seshego Dams, Nwanedzi River
Luphephe Dam
Middle Letaba Dam
Piet Gouws Dam

infection have been observed in European and North

American cyprinid fishes (Sweeting 1977, Kennedy and
Burrough 1981, Szalai et al. 1989, Loot et al. 2001). African
Barbus species are apparently able to survive infestations of
more than ten parasites per fish without this drastically
affecting the size of the parasite or killing the host (Mashego
1982). Large cyprinids such as Labeobarbus marequensis
(A. Smith) could perhaps carry a heavier parasite load,
although they seem not to be regular hosts (Mashego pers.
comm.).
The increase in the size of Ligula plerocercoids with that
of their host may explain why the intensity of infection tends
to be low. As the tapeworm grows in the body cavity of the
host it induces retardation of the hosts gonadal development (Paperna 1996), creates more space for itself and prevents other individuals from establishing themselves.
A high parasite index (PI) is generally associated with a
higher level of damage to the hosts body wall (Sweeting
1977), but the parasite index in B. paludinosus was relatively low, compared to other studies (Sweeting 1977, Saayman
et al. 1991) (Table 2). This explains why the condition of the
fish was not significantly altered, and why there was no evidence that their musculature had been affected. It is also
apparent that there was no significant difference between
the condition factor of parasitised and non-parasitised fish
(Figure 3).
Whilst Kennedy and Burrough (1981) found a seasonality in the prevalence of Ligula, neither the current study nor
those of Mashego (1982) or Saayman et al. (1991) did.
Because of an unusually long dry spell in the year 2000,
which extended to the end of December, the water level in
Munwahuku Dam dropped so low that it was easy for wading birds to prey on the fish in the shallow water. Parasitised
fish would be caught more easily than healthy ones because
ligulosis affects their buoyancy (Paperna 1996) and the
selective removal of parasitised individuals could account for
the zero prevalence recorded in October and December
(Figure 1).
Ligula infection can spread very quickly over a large area
via infected birds, drastically affecting fish populations
(Hoole 1994). In small dams where Barbus species have
successfully adapted, such as the Munwahuku Dam, this
parasite is a threat to natural fish populations. It is also very
difficult to control in wild populations.

N
885
98
33

72

FISH CONDITION FACTOR

Species
B. paludinosus
B. unitaeniatus
B. bifrenatus
B. unitaeniatus
B. paludinosus
B. radiatus
B. trimaculatus
L. marequensis

P
7.2
77.6
33.3
19.0
13.0
5.0
2.8
1.0

MI
1.1
2.0
1.4
1.0
1.0
1.0
1.0
1.0

Range
13
19
12
12
13

Source
3
1
1
2
2
2
1
2

mean
unparasitised
(K = 1.82)
mean
parasitised
(K = 1.69)

r = 0.17, P > 0.05, n = 48

0.2

0.4
0.6
LIGULA WEIGHT (g)

Figure 3: The relationship between the weight of Ligula intestinalis

and the condition factor (K) of Barbus paludinosus from
Munwahuku Dam.

Table 2: The mean parasite index (PI) in B. paludinosus from the

Munwahuku Dam infected by Ligula intestinalis, and in other
Barbus species from Middle Letaba Dam, South Africa (from
Saayman et al. 1991)
Species
B. paludinosus
B. unitaeniatus
B. bifrenatus
B. toppini

Locality
Munwahuku Dam
Middle Letaba Dam
Middle Letaba Dam
Middle Letaba Dam

N
64
54
4
128

PI
8.0
16.3
19.0
24.3

Range
0.716.3
5.634.4
11.333.5
8.249.3

Acknowledgements This study was funded by the Belgian

Government through the University of Zimbabwe-Flemish
Universities Link (Training of Fish Biologists project). We would also
like to thank T Nhiwatiwa, S Alferi, E Mpomba, C Mpamhanga, R
Nhavira, E Mamire and H Munemo for their assistance in the field.
Mr David Stewart of Ingwerati Farm gave us permission to sample
in his farm dam and Prof SN Mashego (University of the NorthWest, South Africa) assisted in identifying the parasites.

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