Investigation of a parasitic outbreak of Lernaea cyprinacea

Linnaeus (Crustacea: Copepoda) in fish from Zimbabwe

Author(s): Maxwell Barson, Atridah Mulonga, Tamuka Nhiwatiwa
Source: African Zoology, 43(2):175-183. 2008.
Published By: Zoological Society of Southern Africa
DOI: http://dx.doi.org/10.3377/1562-7020-43.2.175
URL: http://www.bioone.org/doi/full/10.3377/1562-7020-43.2.175

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Investigation of a parasitic outbreak of Lernaea

cyprinacea Linnaeus (Crustacea: Copepoda) in
fish from Zimbabwe
Maxwell Barson*, Atridah Mulonga & Tamuka Nhiwatiwa
Department of Biological Sciences, University of Zimbabwe, P.O. Box MP 167, Mt Pleasant, Harare, Zimbabwe, and
Laboratory of Aquatic Ecology and Evolutionary Biology, Catholic University of Leuven, Belgium
Received 15 January 2008. Accepted 17 June 2008

Infestation of fish by the crustacean ectoparasite Lernaea cyprinacea Linnaeus, 1758 was
investigated to establish the extent of infestation, potential effects of the parasite and its
ecological adaptations. Fish samples were collected from impoundments in the Malilangwe
Wildlife Reserve in the southeastern lowveld of Zimbabwe and these included the cichlids
Oreochromis mossambicus, Oreochromis placidus and Tilapia rendalli, the cyprinids Labeo
altivelis and Barbus paludinosus, the clariid Clarias gariepinus, the centrarchid Micropterus
salmoides and the characid Hydrocynus vittatus. All the cichlids and one cyprinid (L. altivelis)
were infested with L. cyprinacea. The two Oreochromis species exhibited prevalence as high
as= 100% and mean intensity up to 149 parasites per fish. Lernaea cyprinacea exhibited an
aggregated distribution in host populations and were attached mostly to the ventral and
caudal regions of hosts, while the head was the least preferred attachment site. With a few
exceptions, there was no significant correlation between parasite prevalence and intensity
with host size, sex, condition factor, gonadosomatic index or fecundity.
Key words: ectoparasite, fish, prevalence, intensity, Malilangwe, Zimbabwe.

INTRODUCTION
Parasites are common among fishes, affecting them
in a variety of ways (Khan et al. 1993), and they are
among the key threats to the sustainability of
fisheries that support 90 million people the world
over as a source of protein and income. Fish parasites have been intensively studied in many parts
of the world, including Africa (Paperna 1996; Khalil
& Polling 1997). Although considerable work has
been done on the morphology, systematics and
life histories of crustacean parasites of fish (Kabata
1979; Paperna 1996; Robinson & Avenant-Oldewage
1996; Boxshall et al. 1997), there are limited studies
on the ecology of crustacean parasites (Dogiel
1961; Kabata 1981) In Zimbabwe, there is limited
information available on fish parasites due to a
lack of personnel experienced in fish parasitology.
Recently published work has focused mainly
on helminth endoparasites (Chishawa 1991;
Doullou 1991; Barson & Marshall 2003; Barson
2004), with only three reports on crustacean parasites (Erlwanger 1991; Doullou 1992; Doullou &
Erlwanger 1994).
Members of the copepod genera Lernaea,
Ergasilus and the branchiuran Argulus, are known
to be serious pests of fish in culture (Heckmann
2003) and sometimes cause severe pathological
*Author for correspondence.
E-mail: barson@science.uz.ac.zw / barson001@yahoo.co.uk

effects and mortalities of host fish populations

(Kabata 1981; Paperna 1996). One parasite that has
been of great concern among fish culturists is
Lernaea cyprinacea (Bulow et al. 1979; Robinson &
Avenant-Oldewage 1996). A number of studies
have also reported the impact of L. cyprinacea on
wild fish populations (Amin et al. 1973; Whitaker &
Schlueter 1975; Adams 1984; Robinson & AvenantOldewage 1996).
Lernaea cyprinacea is an opportunistic ectoparasite of many freshwater fish species and non-fish
hosts like amphibians (Bauer 1961; Paperna 1996;
Piasecki et al. 2004). Adult females of L. cyprinacea
attach to exposed body surfaces of host fish including the head, dorsal, ventral, and caudal regions,
but most frequently to the bases of fins (Adams
1984). Their aggregation on body sites induces
severe local damage with adverse consequences to
host function and survival (Bauer 1961; Paperna
1996). However, there are no official reports of
L. cyprinacea-induced fish mortalities from Africa.
The distribution of L. cyprinacea is cosmopolitan
(Marcogliese 1991). In Africa it was first recorded
in the early 1960s in Lake Victoria and Lake Edward
(Fryer 1968). It was introduced into southern
Africa in the early 1980s and has been recorded in
the Limpopo, Olifants, Orange, Selati and Vaal
Rivers and in the Hartbeespoort Dam (Van As &
Basson 1984; Robinson & Avenant-Oldewage 1996).

African Zoology 43(2): 175183 (October 2008)

176

African Zoology Vol. 43, No. 2, October 2008

Its spread has been attributed to international

translocations of edible and ornamental fish,
particularly cyprinids (Paperna 1996; Robinson &
Avenant-Oldewage 1996). Lernaea cyprinacea is not
host-specific, having a wide range of host species
including members of the family Cichlidae,
Cyprinidae, Salmonidae and Siluroidae (Uzmann
& Rayner 1958; Uehara et al. 1984; Berry et al. 1991;
Robinson & Avenant-Oldewage 1996).
A severe L. cyprinacea infestation on fish populations in some impoundments within the Malilangwe Conservancy, Chiredzi District, southeastern lowveld of Zimbabwe, was first observed
in 2003 and fish mortalities suspected to have been
caused by the infestation were later reported in
2004/2005 (B. Clegg, pers. comm.). As the presence
of this parasite in Zimbabwe has not previously
been reported, the objective of the current study
was to report the first occurrence of L. cyprinacea
in Zimbabwe, and to assess the prevalence and
intensity of the parasite on various potential host
species in southeastern Zimbabwe.
MATERIALS & METHODS
Study area
The Malilangwe Conservancy is a wildlife reserve
located in the Chiredzi District, southeastern
lowveld of Zimbabwe (20582115S, 3147
3201E; altitude <600 m a.s.l.). It supports a large
wildlife population and its water bodies have a
large and diverse aquatic fauna and flora. Of
major importance is the presence of the Mozambique tilapia, Oreochromis mossambicus, an indigenous fish species that is a red-listed as Critically
Endangered by the International Union for the
Conservation of Nature (Cambray & Swartz 2007).
The area receives low and erratic rainfall (mean
annual precipitation varies between 450 and
650 mm and mean annual runoff is approximately
60 mm) and is, therefore, prone to seasonal
droughts and severe dry spells (Mugabe et al.
2003). River flows are annually and inter-annually
variable (Traill & Bigalke 2006) and artificial impoundments and pans supplement surface water
resources from rivers and natural springs. The
study was undertaken in three impoundments on
the reserve, namely Malilangwe (210208S,
315243E), Nduna (210108S, E31 5670E) and
Hlambamlonga (210337S, 315308E).
General methods
Fish specimens were collected between October
and December 2006 using a 30 m long (18 mm

mesh) seine net and monofilament gill net

fleets (mesh size 672 mm). Largemouth bass
(Micropterus salmoides) were collected by angling
as they avoided the nets. The fish were identified
to species level according to Skelton (1993) and the
number of individuals of each species counted.
The standard length (mm) and weight (g) of each
individual fish was measured. The external body
surfaces as well as the gill chamber and mouth
cavity of each fish were examined for the presence
of adult females of L. cyprinacea. The number of
parasites on each fish (intensity) was counted for
each region of attachment (head, dorsal, ventral
and caudal) separately. Cutaneous lesions <4 mm
in diameter were assumed to be sites of L. cyprinacea attachment and were included in the count,
because parasites are sometimes dislodged when
handling the fish (Grabda 1963).
The sex of each individual fish was assessed
visually. The gonads were removed and weighed
(to the nearest g). Ova from mature breeding
females were fixed in 10% formalin, preserved in
70% ethanol and subsequently counted to obtain a
measure of fecundity. Parasite prevalence per fish
species was determined by calculating the number
of fish infested with adult female L. cyprinacea
and/or characteristic L. cyprinacea lesions as a percentage of the total number of fish examined per
species (Margolis et al. 1982). Mean parasite intensity (MI) for each host species in each impoundment was obtained by dividing the total number
of L. cyprinacea in a sample of a host species by the
number of infested individuals of the host species
in the sample (Margolis et al. 1982).
The influence of host sex on parasite intensity
was determined for each host species by: (1)
comparing the parasite intensity between the two
sexes (Mann-Whitney U test) and (2) correlating
parasite intensity with host body size, Fultons
condition factor and gonadosomatic index
(Spearmans Rank correlation test). Fultons condition factor (K) was assessed by:
K=

100 W
,
L3

where W = total body weight (g), and L = standard length (cm). The gonadosomatic index (GSI)
for each individual fish was calculated as:
GSI =

Gonad weight (g)

.
Total body weight (g)

RESULTS
From the three impoundments, the following fish
species were examined: Oreochromis mossambicus,

0
0
0

0
0
0
0

0
0
0
340360

0
0
0

0
0
0
0

0
0
0
160450

0
0
0
175390
5
0
0
0
190500
14
0
0
470860

0
0
0
0
0
0
899

14
0
0
1
0
1
0
100
0
140
0
1
0
24
0
100
0
190300

0
1143

17
12
0
2
1
0
15.4
14.3
0
95190
90215

205
59
0
1223
160
0
52
15
0
96.3
98.6
0
84245
70245

283
65
0
14419
26225
127
100
149
100
97
88.9
7
190285
185265
180230

Cichlidae
O. mossambicus 130
O. placidus
45
T. rendalli
63
Cyprinidae
B. paludinosus
0
L. altivelis
9
Clariidae
C. gariepinus
8
Characidae
H. vittatus
19
Centrarchidae
M. salmoides
4

RI
Hlambamlonga
SL
P
MI
(minmax)

n
RI
MI
Nduna
P
SL
(minmax)

n
RI
Malilangwe
SL
P
MI
(minmax)

n
Species

Table 1. Prevalence and intensity of Lernaea cyprinacea on fish species present in Malilangwe, Nduna and Hlambamlonga impoundments in Zimbabwe. n = sample size,
SL = standard length (in mm), P = prevalence (%), MI = mean intensity, RI = range of intensity.

Barson et al.: Parasitic outbreak of Lernaea cyprinacea in fish in Zimbabwe

177

Oreochromis placidus, Tilapia rendalli (all Cichlidae),

Labeo altivelis, Barbus paludinosus (both Cyprinidae),
Clarias gariepinus (Clariidae), Hydrocynus vittatus
( C h a r a c i d a e) a n d M i c r o p t e r u s s a l m o i d e s
(Centrarchidae) (Table 1). Lernaea cyprinacea was
prevalent in all three cichlid species and in
L. altivelis (Table 1), but B. paludinosus, C.
gariepinus, H. vitatus and M. salmoides were not infested.
There were marked differences in the intensity
of L. cyprinacea among the three impoundments,
with fish from the Malilangwe impoundment
being more intensely infested than those from
Nduna and Hlambamlonga (Table 1). Fish from
Hlambamlonga only had characteristic L. cyprinacea
lesions and no adult parasites were encountered.
Parasite intensity also differed between host
species, with Oreochromis species being the most
heavily infested (Table 1). Parasite intensity on
O. mossambicus averaged 149, 52 and 2 parasites per
fish in Malilangwe, Nduna and Hlambamlonga
impoundments, respectively. Oreochromis placidus
was the second highest parasitized with mean
intensity of 97, 15 and 1 in the three impoundments, respectively (Table 1).
The parasites generally showed an aggregated
frequency distribution where few individuals
within a host population had high parasite intensity, while the majority had low to moderate intensity (Fig. 1). Lernaea cyprinacea was found attached
all over the host body surface but with greater
intensity towards the ventral and caudal regions
in all the infested fish species (One-way ANOVA,
P < 0.05) (Fig 2). The head region had the least
number of parasites (Fig. 2). This trend was
observed in all the impoundments.
Lernaea cyprinacea infested fish of all size groups
in all host species. There was no significant correlation between parasite intensity and size of host
fish (SL) for host populations from Malilangwe
impoundment (r < 0.5, P > 0.05) (Table 2), except
in L. altivelis, where there was a significant negative relationship where parasite intensity decreased with increasing size of host (r = 0.85, P =
0.004) (Table 2). In host species from Nduna and
Hlambamlonga impoundments, increased size of
host corresponded to increase in parasite intensity
(r > 0.5, P < 0.05) (Table 2). Lernaea cyprinacea
infested fish of both sexes, with similar rates of
infestation in all impoundments (Mann-Whitney
U test, P > 0.05).
Condition factor was similar among individuals
of the same fish species. Mean condition factor of

178

African Zoology Vol. 43, No. 2, October 2008

Fig. 1. Frequency distribution of Lernaea cyprinacea in host fish populations in the three impoundments in Malilangwe
Conservancy, Zimbabwe. a, Oreochromis mossambicus; b, Oreochromis placidus; c, Tilapia rendalli ; d, Labeo
altivelis (Malilangwe); e, O. mossambicus; f, O. placidus (Nduna); g, O. mossambicus; h, O. placidus (Hlambamlonga).

Barson et al.: Parasitic outbreak of Lernaea cyprinacea in fish in Zimbabwe

179

Fig. 2. Proportion of adult females (and/or characteristic lesions) of Lernaea cyprinacea attached
to each body region of fish in two dominant host
species in the three impoundments in Malilangwe
Conservancy, Zimbabwe. a, Malilangwe; b, Nduna;
c, Hlambamlonga.

O. mossambicus in Malilangwe, Nduna and Hlambamlonga impoundments was 4.0, 3.0 and 4.0,
respectively, and that of O. placidus was 4.0 in all
three impoundments. Oreochromis mossambicus
from Nduna showed a significant negative correlation between condition factor and parasite
intensity (r = 0.44, P = 0.000). No other host
species from any impoundment showed significant correlation (r < 0.5, P > 0.05).
There was a significant positive correlation
between fish fecundity and parasite intensity in
O. mossambicus from Nduna impoundment
(r = 0.48, P = 0.006). In the rest of the host species,
fecundity did not correlate significantly with
parasite intensity (r < 0.5, P > 0.05). In all

impoundments, gonadosomatic index was similar

among fish of the same sex within a species. Only
O. mossambicus males from Hlambamlonga
showed a significant correlation between gonadosomatic index and parasite intensity (r = 0.18, P =
0.018) (Table 3).
DISCUSSION
In this survey, it was found that L. cyprinacea was
not host specific. The prevalence of the parasite
differed among host species, being highest among
cichlids, particularly Oreochromis mossambicus and
O. placidus in which it was 100% in the Malilangwe
impoundment (Table 1). Labeo altivelis also had
100% prevalence. Its absence from M. salmoides is

Table 2. Spearmans rank correlations (r ) between parasite intensity of Lernaea cyprinacea and size of host fish in the
three impoundments in Zimbabwe. Correlations significant at P < 0.05 are indicated in boldface.
Species

Impoundment
Nduna

Malilangwe

r
O. mossambicus
O. placidus
T. rendalli
L. altivelis

0.03
0.23
0.01
0.85

P
0.707
0.132
0.936
0.004

Hlambamlonga
P

0.68
0.62

0.000
0.000

0.19
0.14

0.006
0.260

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African Zoology Vol. 43, No. 2, October 2008

Table 3. Spearmans Rank correlations (r ) between host fish gonadosomatic index and parasite intensity of Lernaea
cyprinacea in the three impoundments, in Zimbabwe. Correlations significant at P < 0.05 are indicated in boldface.
Species

Impoundment
Nduna

Malilangwe

Hlambamlonga
P

O. mossambicus
Male
Female

0.25
0.08

0.211
0.423

0.12
0.16

0.183
0.145

0.18
0.07

0.018
0.545

O. placidus
Male
Female

0.18
0.14

0.493
0.472

0.24
0.13

0.121
0.590

0.16
0.00

0.361
0.997

T. rendalli
Male
Female

0.26
0.11

0.254
0.496

.
.

.
.

L. altivelis
Male
Female

0.40
0.40

0.600
0.505

.
.

.
.

in contrast to the findings of Uehara et al. (1984).

This may be due to behavioural mechanisms such
as avoiding or repelling the parasite by remaining
in habitats that are not favourable to infective
copepodites (Whitaker & Schlueter 1975). The
structure and arrangement of scales in some fish
species might not allow for easy penetration of the
parasites anchor (Kabata 1981), while some fish
species have developed natural immunity to the
parasite (Putz & Bowen 1964; Whitaker &
Schlueter 1975; Uehara et al. 1984).
The high parasite prevalence on O. mossambicus,
O. placidus, T. rendalli and L. altivelis is rarely
encountered in wild populations (Bulow et al.
1979; Medeiros & Maltchik 1999) and suggests a
possible epidemic outbreak of the parasite in the
impoundments. The infested host fish species had
variable parasite prevalence and intensities that
might be attributed to differences in ecological
and behavioural adaptations (Damaree 1967).
Oreochromis mossambicus and O. placidus, the most
infested cichlids, are not fast swimmers, and
during breeding (which coincided with the time of
sampling), they are concentrated more in the littoral zones (Lowe-McConnell 1987). As such, it
would have been more likely for infective copepodites of L. cyprinacea, which prefer warm waters
(Paperna 1996) in the littoral zone, to encounter
these species more frequently than the other
fishes. Damaree (1967) reported that fish collected
from muddy water and muddy bottoms were
more frequently infested with L. cyprinacea, but it
was not the case in this survey; parasite intensity

was low in L. altivelis, and nil in Clarias gariepinus,

both of which are benthic feeders (LoweMcConnell 1987; Skelton 1993).
Individuals within a host species were not uniformly infested with L. cyprinacea; few individuals
were heavily infested, while the majority had low
to moderate parasite intensity. This finding
supports the hypothesis that parasitic copepods,
including L. cyprinacea may exhibit gregarious
behaviour (Fryer 1966) and is consistent with the
results obtained by other authors (Eisen 1983;
Poulin et al. 1991). Aggregated distribution is a
strategy of parasitism that prevents collapse of a
host population due to the deleterious effects of
the parasite (Poulin 2007) and can be influenced by
the tendency for a fish that has acquired one parasite to acquire others, as was noted in East African
lakes by Fryer (1966).
The presence of L. cyprinacea on all size groups of
hosts indicates that the prevalence of the parasite
was not influenced by host size. The observed
increase in parasite intensity with increased host
size in O. mossambicus and O. placidus from the
Nduna impoundment is consistent with findings
of Dogiel (1961) and Adams (1984) and can be
attributed to the larger surface area available for
the parasites in large hosts and to the longer
period of contact with the parasite in older larger
hosts (Dogiel 1961; Adams 1984). There are conflicting reports on size-related differences in
L. cyprinacea infestations; while some authors have
reported an increase in parasitism with increased
host size, Amin et al. (1973) found smaller host fish

Barson et al.: Parasitic outbreak of Lernaea cyprinacea in fish in Zimbabwe

to be more heavily infested, as was the case with

L. altivelis in this survey. High parasite intensity in
younger fish could indicate that these fish are
relatively easy to infest, or that their defence
mechanisms are less well developed.
Lernaea cyprinacea may retard (Kabata 1985) or
increase (Khan et al. 1993; Lysne et al. 2006) the
growth rate of its host. A large host would tolerate
the stress of infestation better than a small one and
would be a better competitor for resources (Khan
et al. 1993), thus individuals probably allocate
more resources to growing larger when infested.
The result from the Malilangwe impoundment
that parasite intensity was not significantly correlated to host size may be unreliable because of the
limited size range (180250 mm SL) of sampled
fish. Absence of juvenile fish of host species in the
Malilangwe impoundment may be a result of high
parasite intensities and juveniles might have been
victims of L. cyprinacea copepodid infestation of
gills that causes early mortality (Paperna 1996). In
small fish, adult parasites easily penetrate vital
organs and cause death (Marcogliese 1991; Piasecki
et al. 2004) or make them more susceptible to
secondary infections and vulnerable to predators
in the impoundment.
The attachment of L. cyprinacea on the body
surfaces of host fish was not random; ventral and
caudal areas had greater numbers of parasites
than expected if the parasites had attached randomly. This result agrees with the postulation that
certain parasitic copepods are not only hostspecific, but are also site-specific, a phenomenon
determined by morphological and physiological
factors of the host (Kabata 1981). In this study,
highest parasite density was observed on the
ventral and caudal regions of host fish, while other
studies reported L. cyprinaceas preferential attachment to bases of fins, especially the dorsal fin
(Whitaker & Schlueter 1975; Adams 1984). Localization at the base of fins must confer some advantage to the parasite, such as protection from
current and abrasion and that tissues at the base of
fins are easier to penetrate (Adams 1984). Some
studies have reported more frequent attachment
to the ventral than to the dorsal aspects of host fish
(Amin et al. 1973; Durham et al. 2002). In this study,
the head region of the hosts was the least frequent
attachment site for adult females, probably
because ectosteal bones beneath the skin of the
head limit attachment to the head (Berry et al.
1991).
Evaluating the effect of L. cyprinacea on host

181

condition and reproduction was difficult because

most individual hosts were infested and there
were limited numbers of non-parasitized individuals to use for comparison. It was, however,
assessed on the basis of different parasite intensities among hosts since the severity of the effects of
the parasite depends on the intensity of infestation (Kabata 1981). At the existing infestation
levels, there was no significant correlation between
parasite intensity and host gonadosomatic index
or fecundity.
Fish introductions are responsible for the spread
of L. cyprinacea in Africa (Robinson & AvenantOldewage 1996), but no introductions were made
in the study area in the last 10 years (B. Clegg, pers.
comm.). A probable source could be the Runde
River where L. cyprinacea was observed in 2005
(M. Barson, unpubl. data) and the parasite might
have reached these impoundments via connecting to the Runde River, most likely during floods
resulting from the 2000 tropical Cyclone Eline. To
confirm this assumption, it would be necessary to
investigate the occurrence of L. cyprinacea in whole
catchments connecting the impoundments to the
Runde River system.
Further investigations and long-term sampling
would help determine seasonal variations in
L. cyprinacea infestation. Experimental work could
be done to ascertain the influence of host size and
sex on L. cyprinacea infestation, as well as the
assumed effect of L. cyprinacea on juvenile fish. The
lack of observable effect of the parasite on host
condition could be further investigated at
histopathological and immunological levels. The
influence of physical and chemical variables like
temperature, pH, salinity and nutrient concentrations on L. cyprinacea infestation needs further
investigation, and multivariate studies are recommended to investigate interactions between environmental and ecological factors in L. cyprinacea
infestations.
ACKNOWLEDGEMENTS
We are grateful to the owners and managers of
the Malilangwe Wildlife Reserve for authorizing
this study and for their hospitality, particularly
Bruce Clegg (Research Manager) and his staff. The
study was funded by a grant from the VLIR-UOS
(Flemish Interuniversity Council, Belgium)
through the UZ-VLIR Aquatic Ecology Project. We
also acknowledge Brian Marshalls (Lake Victoria
Fisheries Organisation, Jinja, Uganda) contribution towards the conception of this study, Univer-

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African Zoology Vol. 43, No. 2, October 2008

sity of Zimbabwe staff and students for their field

and laboratory support, and Annemarie AvenantOldewage (University of Johannesburg) for reading an early draft of this paper.
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Responsible Editor: O.L.F. Weyl