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Universiteit Vrystaat
ECTOPARASITIES OIF FISHES !FROM
SOIETDOIRDNG INJATURE RESERVE
By
Jonathan VerruteJr
Dissertation submitted in fulfilment of the requirements for the degree
Magister Scientiae in the Faculty of Natural and Agricultural Sciences
Department of Zoology and Entomology
University of the Free State
Supervisor ProC.J. G. Van As
Co-supervisor Dr. L. L. Van As
AUGUST2002
UniversIte1t van dIe
OnmJe-Vrystoot
ILO~r O."Tf.IN
1 B AUG 2
fI uovs ~!)l UUOTEEK _
COIi1l~elT'Ofts
1. Introduction 1
2. Materials and Methods 4
0 Study area 4
Q Soetdoring Nature Reserve 5
0 Fieldwork 8
0 Collection of fish 9
0 Examination of hosts 9
0 Ciliophorans 11
0 Monogeneans 12
Cl) Crustaceans 14
(li Imaging 14
0 Type & reference material 15
0 Data analysis 15
3. Fishes of southern Africa 20
0 Distribution of fish fauna 20
0 Fish species of the Orange River 22
Cl) Cyprinidae 23
0 Austroglanididae 28
(il Clariidae 29
0 Cichlidae 30
0 Introduced fishes of the Orange River 32
(li The fish species of the Madder River 36
RESULTS 39
4. The phylum Ciliophora Doflein, 1901 40
0 Sessiline Ciliophorans 43
0 Sessiline Ciliophorans known from South Africa 43
(il The genus Apiosoma Blanchard, 1885 43
0 Species of Apiosoma known from South Africa 44
0 The genus Scopulafa Viljoen & Van As, 1985 44
0 Species of Scopulafa known from South Africa 45
0 Mobiline Ciliophorans 51
0 The genera Trichodina Ehrenberg, 1838, Tripartiella Lom, 1959 52
and Trichodinella Srámek-Husek, 1953
0 The genus Trichodina Ehrenberg, 1838 52
0 The genus Trichodinella Srámek-Husek, 1953 53
0 The genus Tripartiella Lom, 1959 53
0 Trichodinid species known from South Africa 53
0 Ciliophoran parasites from Soetdoring Nature Reserve 63
0 Apiosoma sp. A 63
0 Apiosoma sp B 64
0 Trichodina sp A 65
0 Trichodina sp. B 66
0 Trichodina sp. C 67
0 Tripartiella sp. A 69
0 Tripartiella sp. B 70
0 Trichodinella sp. A 71
5. The Class Monogenea (Van Beneden, 1858) 77
Q Branchial monogeneans from African fishes 81
0 Dactylogyridean monogeneans 81
0 Genus Dacfy/ogyrus Diesing, 1850 81
0 Dacfy/ogyrus Diesing, 1850 species of African cyprinids 82
0 Species recorded from Labeo Cuvier, 1817 hosts 82
0 Dacfy/ogyrus species known from South African hosts, other than 95
Labeo Cuvier, 1817 species
0 Species recorded from Cyprinus carpio Linnaeus, 1758 101
0 The genus Dogielius, Bychowsky, 1936 105
0 Species of Dogie/ius recorded from Labeo hosts 105
0 Dactylogyridean species from C/arias gariepinus (Burchell, 1822) 116
0 The genus Ouadriacanfhus Paperna, 1961 116
0 Species of Ouadriacanfhus Paperna, 1961 recorded from African 117
siluriform fishes
0 Diplozoid monogeneans 125
o The genus Paradiplozoon Achmerov, 1974 125
o Paradiplozoon Achmerov, 1974 species from African fishes 125
o Branchial monogeneans from Soetdoring Nature Reserve 127
o Dactylogyrus sp. A. 127
o Dactylogyrus freistatensis n. sp. 132
o Dogielius capensis n. sp. 137
o Quadriacanthus sp. A 142
o Paradiplozoon modderensis n. sp. 147
6. The parasitic Crustacea 153
e Subclass Branchiura Thoreli, 1864 153
o The genus Argulus MuilIer, 1785 155
o Species of Argulus known from South Africa 155
o Subclass Copepoda Milne Edwards 1940 156
o The genus Lamproglena Nordmann, 1832 162
o Species of Lamproglena Nordmann, 1832 known from Africa 163
o Parasitic Crustacea from Soetdoring Nature Reserve 175
o Argulus sp. A 175
o Lamproglena sp. A 180
7. Parasite Host Associations 185
8. General Discussion 195
o Remarks on the parasite and host populations 195
o Pathogenicity 201
e Alien species 204
o Endoparasites 206
9. References 208
Abstract 226
Opsomming 227
Acknowledgements 228
Chapter 1
Chapter 1 -Introduction 1
Fish have been of importance to man since the dawn of our ancestors. Man
has been utilising fish from the rivers of southern Africa for as long as they
have been present in the area. According to Skelton (1993) remains of fish
are frequently found at archaeological sites associated with the dwellings of
the Khoi and San peoples. Traditional fisheries have, however, only survived
in areas where sufficient fish communities were available, such as in the
tropics. Subsistence and commercial fisheries do still exist, for example the
"kapenta" sardine fisheries of Lake Kariba (Skelton 1993). Same of the many
threats to freshwater fishes, are introduced fishes and their parasites, as well
as the activities of man, which also indirectly threaten fish populations, by
creating environments in which parasites may thrive and adversely affect host
fishes. These threats also apply to fish populations from aquaculture
activities, which have become a rapidly growing sector of agriculture (Skelton
1993).
Fish parasitological research in Africa resulted in a steady flow of papers, but
dried up during the political instability during the post-colonial era. Presently a
number of parasitologists are still active in Africa, although the numbers are
much reduced.
Parasitological research in southern Africa has received much attention under
the guidance of Prof. Jo van As at RAU since 1980 and at the University of
the Free State since 1988. Research surveys conducted by the University of
the Free State's Aquatic Parasitology Research Group includes various
freshwater fish research projects (e.g. Basson & Van As 1987, Basson & Van
As 1989, Van As & Van As 1993, Van As & van As 1999) and marine projects
at the de Hoop Nature Reserve (Loubser 1994, Van As & Basson 1996, Smit
& Davis 1999).
The present study was initiated on request of the Department of
Environmental affairs and Tourism of the Free State, who were interested in
Chapter 1 - Introduction 2
the fish parasites of the Modder River System. The main objective of the
study was to determine infection patterns of parasites of the fishes from the
Soetdoring Nature Reserve. This would include determining whether any
introduced parasites are prevalent on the fishes and to investigate the various
host-parasite associations. Initially the project was intended to be a
comprehensive study on the endo-and ectoparasites associated with the
various fish hosts. It was soon realised that such a study would be to broad
for a Masters study, especially due to the extent of the systematics and
identification of endoparasitic helminths.
Up until this point in time, research projects of this study group, as well as the
research groups of other South African institutions have focused on a specific
group of parasites associated with fish hosts. Even in the whole of Africa
most of the research was focused either on a specific host, or on a specific
group of parasites. Very little research work on a spectrum of parasites or fish
hosts of a specific river system has been done in Africa. Such works include:
Paperna (1964a), Khalil (1968), Paperna (1968), Paperna & Thurston
(1968a), lombaard (1968), Thurston (1970), Khalil (1971), Paperna & lahav
(1971), Van As & Basson (1988), Douëllou (1992) and Hecht & Endemann
(1998).
Although some unpublished data of freshwater parasites of the Free State
exists, research is limited to that of Barkhuizen (1991), who researched the
life strategies and occurrence of the cestode Bothriocephalus acheilognathi
Yamaguti, 1934 in the Free State and the work of King & Van As 1996, King &
Van As 1997a, King & Van As 1997b and King & Van As 2001 on trematodes
associated with snail hosts in the Free State. Other research on freshwater
systems conducted by the University of the Free State includes that of
Seaman, Roos & Watson (2001 a, b), who researched the ecological state of
the Madder River. This dissertation would then be the first of its kind to study
the whole spectrum of fish ectoparasites present in a reservoir.
This study provides a unique opportunity to study the fish populations as well
as the parasites of the upper Madder River, as the study area is situated at
Chapter 1 - Introduction 3
the Soetdoring Nature Reserve. It will also be the first project to provide
information on a spectrum of fish parasites that occur in the Madder River.
During the first survey, the water level of the Krugersdrift Dam was estimated
at only 23%. This made the collection of fish an easy task. In the months to
follow, the Free State had exceptionally high rainfall, which continued for the
remainder of the study period. This high rainfall had an adverse effect on the
project, as the collection of fish was no longer simple, and the numbers of fish
collected dropped significantly.
The layout of this dissertation is as follows: The materials and methods used
during field and laboratory work is described in Chapter 2 as well a section
providing information on the study area. The fish species that occur in the
Orange River system are discussed in Chapter 3, followed by a discussion of
the ciliophoran parasites in Chapter 4. The monogeneans and parasitic
crustaceans are discussed in Chapter 5 and Chapter 6 respectively.
Results of the statistical analysis of data are presented in Chapter 7 and the
general discussion in Chapter 8. Chapter 9 contains the literature references,
which is followed by the Abstract and Acknowledgements. A copy of the
permit for collection of fish at the Soetdoring Nature Reserve is included in
Appendix A.
Chapter 2
Chapter 2 - Material and Methods 4
Study Area
The Madder River is one of the smaller rivers in South Africa. It forms part of
one of the most prominent river systems of southern Africa, the Orange-Vaal
River System. The main constituents of this system, the Orange- and Vaal
Rivers, have their origins in the Drakensberg in the eastern part of the
country. These two rivers flow in a western direction and the Vaal River joins
the Orange River east of Douglas, a small town in the Northern Cape
Province. From here the Orange River flows all the way to the West Coast,
where it has its mouth near Alexander Bay. Smaller rivers that form part of
the system include the Vet-, Riet-, and Caledon Rivers.
The Madder River has its origins in the hills of southeastern Free State, from
where it flows in a northwestern direction and then turns west (Anon 1966)
(Figure 2.1). Its origins are in the Moist Cool Highveld Grassland, which
changes as it flows to the west into Dry Sandy Highveld Grassland, Eastern
Mixed Nama-Karoo and then Kimberley Thorn Veld. The Madder River joins
the Riet River, which then flows on to join the Vaal River west of Douglas.
The largest part of the catchment area of the Madder River is situated in the
south central Free State Province and a smaller part in the Northern Cape
Province (Seaman, Roos & Watson 2001 a). This catchment comprises an
area of about 17 360 km2 (Midgley, Pitman & Middleton 1994). According to
Grobbelaar (1992) the Madder River has a mean annual runoff of 184 x 106
m3.
In the Free State, the Madder River is an important water source, as it
supplies water to Bloemfontein and some of the surrounding areas. Since
1896, several dams and weirs have been built in the Madder River, either to
provide water to Bloemfontein and surrounding towns (Botshabelo and Thaba
Nchu), or for irrigation purposes. The Sannaspos Weir was built in 1896 to
provide Bloemfontein with water, which was supplemented in 1904 with the
Chapter 2 - Material and Methods 5
Mazelspoort Weir and in 1913 with Mockes Dam. Rustfontein Dam was
completed in 1955, which currently supplies Thaba Nchu and Botshabelo with
water.
The Modder River flows through the Soetdoring Nature Reserve and into the
Krugersdrift Dam, which farms part of the nature reserve (Figure 2.2, Figure
2.4A). Krugersdrift Dam was built in 1970 and provides irrigation water for
farmers along the lower reaches of the river.
According to Seaman et al. (2001 a), most of the Madder River catchment
consists mainly of rocks of the Karoo Sequence, which are interspersed with
dolerite dykes in places. The origin of the Madder River is in Adelaide
formation and as it flows northwest through Ecca formation and Kalahari
Sands where it joins the Riet River. At this confluence, Dwyka tillite as well as
interbedded sedimentary and volcanic material are also found.
êoetcorlnq Nature Resell"Ve
The Soetdoring Nature Reserve is situated 45km north west of Bloemfontein
on the Madder River (Figure 2.2). It was established on 28 July 1978 and
comprises 7500ha, of which approximately 2000ha encloses the Krugersdrift
Dam.
The rainfall season is mainly between January and March and the average
annual rainfall is 560mm. During the period of the study, however, the rainfall
was substantially higher, causing the water levels of the Krugersdrift Dam to
rise considerably (Figure 2.3).
Main vegetation types of the reserve include False Upper Karoo and Dry
Cymbopogon - Themeda Veld. Four types of vegetation can be recognised;
grassveld, which is dominated by Themeda triandra and karroid veld, in which
Felicia muricata is dominant. In the riparian bush Acacia karroo is dominant,
and koppie scrub is dominated by Olea africana.
Theunissen
Boshof Soetdoring and rugersdrift Dam Winburg
Marquard
Soutpan
Dealesville
Verkeerdevlei
Excelsior
Petrusburg
Thaba Nchu
Rooipan
Luckhoff
Fauresm ith
•
Philippolis
LEGEND
~RM!rl'tbmes
~RMlrl
[ZJ RMlrl - Second"ry
_D8ms/pans
Figure 2.1. Map of the rivers of the Free State to indicate the position of the Modder River, Soetdoring
Nature Reserve and Krugersdrift Dam (adapted from Seaman et al. 2001a).
Figure 2.2. Map of the Krugersdrift Dam at the Soetdoring Nature Reserve showing sampling localities.
(adapted from tourist information map). 1 & 2-sampling localities that are permanently dammed, 3-riverine
sampling locality.
Chapter 2 - Material and Methods 8
1a:l
100 .74
G) 80
~>
-L~ 60(Il
~ 40
20
0
Figure 2.3. Line graph illustrating the water level of the Krugersdrift Dam
during the study period
A variety of mammals are found on the reserve, including a predator park,
which is home to a few lions. Some of the dominant mammals that roam the
reserve include black wildebeest, eland, blesbok, red hartebeest, springbok,
Burchull's zebra and gemsbok. A number of ostrich as well as white rhino
also occur on the reserve. The bush amongst the riverbanks gives sanctuary
to kudu, waterbuck, common reedbuck and impala.
Several facilities of the Soetdoring Nature Reserve are accessible to tourists,
including a Train Camp, which offers overnight accommodation. Various
picnic spots and barbecue facilities are also available. Recreational activities
at the reserve include game viewing, bird watching and a two-day canoe
route. Angling is a popular attraction at the Krugersdrift dam, as well as
windsurfing, camping and canoeing.
Fieldwork
All the fieldwork for this research project was conducted at the Soetdoring
Nature Reserve. Collections took place at three different localities (Figure
2.2, Figure 2.4D-F). During March 2001, an initial weeklong fieldtrip was
conducted at the reserve to aid as a pilot study. A fully equipped field
Chapter 2 - Material and Methods 9
laboratory was set up during this week in the vicinity of the Train Camp
(Figure 2.48, C). Subsequent fieldwork consisted of day trips to the reserve
on a monthly basis. Two of the collection sites (including the site at the Train
Camp) fell within the reserve itself, including the Krugersdrift Dam (Figure 2.2,
Figure 2.40, E). The other site was situated on the Madder River before it
flows into the dam (Figure 2.2, Figure 2.4E).
Sample localities in and around the Krugersdrift Dam were characterised by
slow flowing water, surrounded with grassy banks and Acacia trees. The
riverine locality had similar characteristics to the localities situated in the dam.
The riverine locality, however, had a rocky substrate. During the first survey
in March 2001, the water level of the dam was very low and the dam was
estimated to be only 23% full. The implication of the low water level was that
the riverine locality consisted of only rocky pools. In the following months,
after high rainfall to the region, this locality was transformed into fast flowing
rapids.
coneetton of fish
The methods for collecting fish consisted of cast nets as well as gill nets. Gill
nets consisted of a graded series of lengths, each 10 m long and each of a
different mesh size. The minimum mesh size was 40 mm and the maximum
140 mm (40 mm, 70 mm, 90 mm, 100 mm, 110 mm, 120 mm & 140 mm).
These nets were set early in the morning and lifted throughout the day to
prevent fish mortalities. Nets were removed again in the late afternoon. An
electra-fishing apparatus was also used, but with less success.
IExamill1lation of hosts
After collection, fishes were taken to a field laboratory during the first survey
where they were examined. During the succeeding field trips, fish were kept
alive in temporary holding tanks and transported to the laboratory in
Bloemfontein for examination. Fishes were anaesthetised and examined
mainly for ectoparasites but some endoparasites were also collected.
Figure 2.4. Various localities at the Soetdoring Nature Reserve. A - Modder River at Soetdoring Nature
Reserve, B, C - field laboratory in vicinity of the Train Camp, 0 - locality 1 at Krugersdrift Dam, E -
locality 2 at Krugersdrift Dam, F -locality 3 at Modder River before flowing into Krugersdrift Dam.
Chapter 2 - Material and Methods 11
The method for studying the different types of ectoparasites are unique, thus
each method will be described separately.
CiliophOll"éD I1IS
Smears of gills as well as skin were made of each fish. After collection, wet
smears were examined using a Zeiss Axiophot compound microscope.
Smears were allowed to dry for later processing or were fixed in Bouins'
fixative for further staining techniques.
o Light microscopy preparation
In preparation for compound microscopy sessiline ciliophorans were stained
with Harris' Hematoxylin according to Wellbarn (1967) to study the shape and
size of the macronucleus. Smears containing mobiline ciliophorans were
impregnated with silver nitrate in order to study the adhesive disc as
described by Basson, Van As & Paperna (1983).
e Morphological measurements
Measurements obtained from sessiline ciliophorans included length and width
of the body and the shape and size of the micronucleus and macronucleus.
Measurements of mobiline ciliophorans were made according to the method
of Van As & Basson (1989), in addition to the system proposed by Lam
(1958). Eleven measurements were obtained from the silver impregnated
structures (Figure 2.5), i.e. body diameter, diameter of adhesive disc, width of
border membrane, diameter of denticle ring, number of denticles, number of
radial pins per denticle, length of denticle, length of ray, width of central part
and length of blade. Measurements are presented in the following way:
minimum and maximum, followed in parentheses by the arithmic mean and
standard deviation (only in n>9) and number of specimens measured. In the
case of denticle number, and radial pins, the mode was used as suggested by
Van As & Basson (1989).
Chapter 2 - Material and Methods 12
Monogeneans
After gills were examined for monogeneans, infested gill arches were placed
in a 1: 4 000 formalin solution for about half an hour. When possible, live
specimens were first removed from the gills, before being placed in the
formalin solution. This solution is insufficient to fix the monogeneans, but will
kill them in a relatively short time. Host tissue was fixed in a 10% neutral
buffered formalin solution with monogeneans still attached. This method of
killing and fixing ensures that very few monogeneans contract on contact with
the formalin.
o light microscopy preparation
In preparation for compound microscopy, individual specimens were removed
from the gill tissue and mounted in a glycerine ammonium picrate solution
similar to that used by Malmberg (1957), to study the opisthaptoral structures.
Diplozoid specimens were stained using Mayer's paracarmine and mounted in
Eukitt.
o Morphological measurements
Measurements of the sclerotised parts of specimens from the genus
Oactylogyrus Diesing, 1850 were done according to the method of N'Douba,
Pariselle and Euzet (1997) (Figure 2.6A-K). Six basic measurements, i.e.
total length, base width, inner root, outer root, shaft and the tip were obtained
from the anchors. The dorsal and ventral bars were measured in terms of the
total length and width. The marginal hooklets were numbered according to
the system proposed by Malmberg (1990) and only the total length was
measured. The total length of the cirrus as well as the accessory piece were
measured and not only the length of the axis.
Sclerotised structures of specimens from the genus Oogielius Bychowsky,
1936 were measured according to Guegan, Lambert & Euzet (1988) (Figure
2.6L-S). Three basic measurements, i.e. total length, shaft + outer root, and
the tip were obtained from the anchors. Two basic measurements were
obtained from the transverse bar, i.e. total length and width. The marginal
Chapter 2 - Material and Methods 13
hooklets were numbered according to the system proposed by Malmberg
(1990). The total length of the cirrus as well as the accessory piece were
measured and not only the length of the axis.
Measurements of the sclerotised parts of all specimens from the genus
Quadriacanthus Paperna, 1961, were measured according to the method of
N'Douba, Lambert and Euzet (1999) (Figure 2.7A-M). Three basic
measurements were obtained from the anchors, i.e. total length, base width
and the tip length. Both the dorsal and ventral anchors possessed an
accessory sclerite, which was measured in length and width, respectively.
The half-length of the dorsal bar was measured as well as the centrum height
and the median process length. Half of the ventral bar was measured and the
width was measured at its widest point. The marginal hooklets were
numbered according to the system proposed by Malmberg (1990) and only
the total length was measured. The total length of the cirrus as well as the
accessory piece were measured and not only the length of their axis.
Specimens of the genus Paradiplozoon Achmerow, 1974 were measured in a
similar fashion to that proposed by Thomas (1957) and Fischthal & Kuntz
(1963). Two basic measurements, i.e. length and width were obtained from
the opisthaptoral clamps (Figure 2.7N-P). In addition to these measurements,
the length of the spur on the dorsal sclerite was also measured. Two
measurements were obtained from the prohaptoral region, namely diameter of
the oral suckers and the length of the pharynx. Measurements obtained from
the reproductive organs included length and width of the intra-uterine eggs,
ovary and testis.
Measurements of the monogeneans are presented in the following manner:
mean and standard deviation followed in parentheses by the minimum and
maximum values.
Chapter 2 - Material and Methods 14
CrlUlstaceans
After examination of the skin and gills, branchiurans were removed with the
aid of a scalpel and brush. Specimens were placed in a petri dish on a slide
with a drop of water. A cover slip was placed on the specimen and slight
pressure applied, while 70% ethanol was dripped in between the slide and
cover slip. This ensures that the organism is in a flattened position.
Thereafter the specimen was transferred to 70% ethanol. Copepods were
removed from the gills with two fine brushes and fixed in 70% ethanol.
e light microscopy preparation
The method proposed by Benz & Otting (1996) was used for the study of
branchiurans with the aid of light microscopy. Copepods were studied in a
similar fashion.
o Scanning electron microscopy (SEM) preparation
Specimens used for SEM studies were cleaned with two fine brushes to
remove mucus and debris, dehydrated in graded ethanol concentrations,
critical point dried, gold coated using an Emscape SC500 sputter coater and
viewed with a Jeol Winsem JSM 6400 SEM at 10 kV.
o Morphological measurements
Measurements of the branchiurans were made according to standard
methods. Seven basic morphological measurements were obtained from the
specimens, i.e. total length of the body, width of the body, carapace length,
length of carapace sinus, abdominal length, abdominal width and length of
abdominal sinus (Figure 2.8).
Imagol11lg
Digital images of the respective structures and parasites were taken using a
Zeiss Axiophot compound microscope and a Nikon Coolpix 990 digital
camera. These images were analysed and respective measurements made
using the Scion Image software package. Unless otherwise indicated, all
measurements are in micrometers.
Chapter 2 - Material and Methods 15
rype and!reference material
All type and reference material is in the collection of the Aquatic Parasitology
Research Group, Department of Zoology and Entomology, University of the
Free State.
Data analysis
Raw data was analysed to determine parasite prevalence of the fish
populations. Prevalence of parasites is presented as the percentage of hosts
infested with ectoparasites. The mean intensity was calculated as mean
number of parasites per infested host and abundance as the mean number of
parasites for all hosts collected (infested and uninfested).
B A
G
Figure 2.5. Illustrations of the measurements made from the silver impregnated structures of mobiline
ciliophorans. A - body diameter, B - adhesive disc diameter, C - border membrane width, ID- denticle
ring diameter, E - number of radial pins per denticle, F - denticle length, G - ray length, H - central part
width, I - blade length. a-apophysis of blade, alb-apex of blade, am-anterior margin of blade, ar-apophysis
of ray, ca-centre of adhesive disc, cp-central part, db-distal surface of blade, dc-deepest point of curve,
pm-posterior margin of blade, pr-point of ray, tp-tangent point
K
IR
Figure 2.6. Illustrations of the measurements of sclerotised structures of Dacty/ogyrus Diesing, 1850 and
Dogie/ius Bychowsky, 1937. A-K - Dacty/ogyrus. A - total length of anchor, B - base width, C - inner
root, 0 - outer root, E - shaft, F - tip, G - dorsal bar length, H - dorsal bar width, I - marginal hooklet
length, J - length of cirrus, IK- length of accessory piece. l-S - Dogie/ius. l - total length of anchor, M -
shaft+outer root, - N - tip, 0 - length of dorsal bar, P - width of dorsal bar, Q - marginal hooklet length, R
-length of cirrus, S -length of accessory piece.
l
N
Figure 2.7. Illustrations of the measurements of the sclerotised structures of Quadriacanthus Paperna,
1961 and Paradiplozoon Achmerav, 1974. A-N - Quadriacanthus. A - total length of anchor, B - base
width, C - tip, 0 - length of accessory sclerite, E - width of accessory sclerite, F - half length of dorsal bar,
G - width of dorsal bar, H - length of median process, I - half length of ventral bar, J - width of ventral bar,
K - marginal hooklet length, L -length of cirrus, M -length of accessory piece. N-P- Paradiplozoon. N-
length of clamp, 0 - width of clamp, P - length of spur.
A
Figure 2.8. Illustration of morphological measurements of Argulus Thiele, 1900. A - total body length, B
- width of body, C - carapace length, 0 - length of carapace sinus, E - length of abdomen, F - width of
abdomen, G - length of abdominal sinus.
Chapter 3
Chapter 3 - Fishes of southern Africa 20
Fnshes of southern Afroca
Southern Africa covers 16% of the continent, the fish fauna, however, contribute
less than 10% of the total African fish fauna. For example, in the Congo River
System, there are more than 700 species. The African Rift lakes each have a
large species composition, ranging from more than 300 to over 800 species.
Thus, compared to the rest of Africa, southern Africa's fish fauna is relatively
poor. The following account of the fish fauna of southern Africa is, except where
other authors are given, taken from Skelton (2001 ).
In southern Africa, 60% of the fish are primary freshwater fishes, meaning that
approximately 160 fish species occur in inland water, and have little or no
tolerance to salt water. The secondary freshwater fish species consists of 56
species. These occur mainly in freshwater systems, but may be tolerant of salt
water. The majority of the fishes are Afrotropical, which have affinities with taxa
in Northern Africa (Skelton 2000).
Dlstrlbution of fish fauna
According to Gabie (1965), there are several anomalies showed by the
distribution of fishes in southern Africa. It was believed that Central Africa is the
source of origin for most of the southern freshwater species and it has been
suggested that Africa was covered by large areas of internal drainage, which
could have offered a link between river systems (Gabie 1965). These
interconnected river basins, together with evolutionary as well as ecological
events in the history of the earth, might explain the distribution of fish in southern
Africa. According to Skelton (2000), the earlier model that the present day fauna
has arisen through a series of invasions from the tropies is rejected, and a new
model, which proposes two overlapping, but distinct faunas that have largely
evolved in situ, is suggested.
Chapter 3 - Fishes of southern Africa 21
The fish fauna of southern Africa can be grouped into a tropical Zambezian fauna
and a temperate fauna, with the latter then being further divided into a Cape
group and the Karoo group. The Zambezian fauna is not only the largest, but it
also includes some very diverse families. The temperate fauna is relatively small
and comprises about 36 species, but is completely endemic. Most of the
temperate species are cyprinids, although there are some interesting
austroglanidids and anabantids. On the other hand, the Cape fauna is relatively
poor, with only 15 species, which are restricted to the Cape Fold Mountains, the
Amatolas, and the Drakensberg. The Karoo fauna is centered on the Orange
River basin, and this includes the yellowfishes, labeos, barbs, and the southern
rock catfishes.
Proceeding from north to south, the numbers as well as diversity of fishes in
southern African rivers decreases (Figure 3.1), and according to Gabie (1965)
endemic tropical fish are few south of the Zambezi. For example, the Zambezi
River System fauna consists of 134 primary and secondary freshwater fish
species. Moving south, the Limpopo has only 50, the Phongolo 40, the Tugela
12, the Cunene 66, the Orange 16, the Olifants 10, and the Berg four (Figure
3.1 ). Of the 22 families that comprise these species, the Cyprinidae and the
Cichlidae dominate the fauna. The alien fish fauna of southern Africa consists of
24 species, which is approximately 9% of the total fish fauna (Skelton 2001 ).
Endemic fish of southern Africa comprises 61% of the total primary and
secondary freshwater species. A unique composition of fish species is found in
the different river systems, and each system has its own endemic fish fauna.
Eight species are endemic to the Clanwilliam-Olifants River System, six species
are endemic to the Orange River System, whilst two species are endemic to the
Limpopo River System, and the Zambezi River System has 23 endemic species.
Chapter 3 - Fishes of southern Africa 22
Figure 3.1. Map of southern Africa showing the major river systems (number of species in
parentheses). (Adapted from Microsoft Encarta Reference Ubrary 2002)
Fish species of the Orange River
The Free State fauna consists of fishes from the Cyprinidae, Cichlidae,
Austroglanididae and Clariidae. Cyprinids, austroglanidids and clariids are all
primary freshwater species, being unable to survive in saltwater (Jubb &
Farquharson 1965). The cichlids, however, have representatives that are
tolerant of salt water (Gabie 1965).
Jubb and Farquharson (1965) state that there are only 14 indigenous species in
the Orange River, but according to Skelton (2001) there are 16 indigenous fish
Chapter 3 - Fishes of southem Africa 23
species. Six of the species are endemic to the Orange River, or endemic to a
river or group of rivers within the Orange River drainage basin (Jubb 1964). The
distribution of fish in the Orange River is not homogenous. Jubb (1972) mentions
that in the part of the drainage system that flows into the Gariep Dam, only seven
indigenous species are found.
Cyprinidae
The cyprinids are an extremely large family of primary freshwater fishes. They
are distributed worldwide, with about 275 genera and more than 1600 species.
At least 24 of the genera and 475 of the species occur in Africa. Cyprinids are
highly variable regarding their biology as well as anatomy. They lack teeth on
the jaws, as well as a true stomach, but have strong pharyngeal bones in the
throat, and an extended and convoluted gut. Most of the cyprinids are adapted
for living in fast flowing water, which means that most of them are strong
swimmers.
Yellowfishes
Until recently all the yellowfishes belonged to the genus Barbus Cuvier &
Cloquet, 1916. For ichthyologists, this genus has long been a taxonomic
problem (Myers 1960). Taxonomists have recognized that the African species
are polyphyletic, and distinct at generic level from the European Barbus barb us
Linnaeus, 1758, which is the type species of the genus. According to Skelton
(2002), the yellowfishes have been moved to the genus Labeobarbus Ruppell,
1836 because of the genetic differences with other Barbus species. The
yellowfishes have a hexaploid karyotipe, while the European species are
tetraploid (Skelton 2002).
Yellowfishes are large barbine cyprinids, which can live for many years and are
characteristic to many African rivers and lakes, and according to Jubb (1964)
there are two species in the Orange River drainage basin, namely Labeobarbus
aneus (Burchell, 1822), and L. kimberleyensis (Gilchrist & Thompson, 1913).
Chapter 3 - Fishes of southem Africa 24
Within populations there can be a wide variation in the anatomical features of
these fish. Three forms are recognized based on the mouth and lips, which are
especially variable: the normal U-shaped mouth with normal lips; straight-edged
mouth with horny lower lips; and fleshy lips. The development of the lips is
determined by the feeding habits and can change from normal to thick depending
on the food resources. Each variation of mouth and lips appear to be an
adaptation for feeding from different substrates.
Species: Labeobarbus Icimberleyensis (Gilchrist & Thomson, 1913) (Figure
3.1A)
Common name: Largemouth yellowfish
This is the largest scale bearing fish in southern Africa, and can reach weights of
up to 22kg. They are absent from the southern tributaries in the Cape and higher
reaches of Lesotho and prefer the larger tributaries and dams. According to
Jubb (1964), the largemouth yellowfish is endemic to the Orange River drainage
basin. This fish is primarily a predator that prefers flowing water, but they also
survive well in dams. The young initially feed on insects, but become piscivorous
above 300mm. Breeding occurs in mid to late summer, in flowing water over
gravel beds. After two to three days the eggs hatch, and feeding begins three to
four days later. The males mature only after six years and the females after
eight. Because of its large size and piscivorous feeding habits, this species will
regularly take live bait and a variety of lures. This makes the largemouth
yellowfish a very popular angling species. Jubb (1972) noted that the largemouth
yellowfish used to be common in the Caledon River below 1500m. This species
is now becoming scarce and are being artificially cultured to restock their
numbers (Skelton 2001).
Species: Labeobarbus aneus (BurchelI, 1822) (Figure 3.1B)
Common name: Smallmouth yellowfish
This is a smaller species than L. kimberleyensis attaining weights of 7kg.
Smallmouth yellowfish occur naturally in the Orange River drainage system and
Chapter 3 - Fishes of southern Africa 25
this species is also endemic to the Orange River drainage basin (Jubb 1964), but
it has been translocated to larger Cape coastal rivers. According to Jubb (1972),
this species is more widely distributed in the system than the largemouth
yellowfish. These fish migrate upstream to spawn on gravel beds in spring to
midsummer after the first substantial rain of the season. Eggs hatch after 3-8
days and feeding begins after another 4-6 days. The large fish are omnivorous,
and feed on available food, which includes benthic invertebrates, plants, algae
and detritus. Smallmouth yellowfish is also an important angling species.
Labeos or Mudfishes
The genus Labeo Cuvier, 1817 comprises at least 80 species in Africa. The
labeos are specialised feeders and have well adapted mouthparts. Labeos also
have well adapted intestines, which is long and coiling, because of their feeding
habits. They often occur in flowing water, and most of them are strong
swimmers. Labeos migrate upstream to breed, and some have been observed
to cross exposed surfaces.
Species: Labeo umbratus (Smith, 1841) (Figure 3.1C)
Common name: Moggel
This species has commercial as well as subsistence uses and occurs in the
Orange-Vaal system, as well as several other systems of the south and
southeast Cape regions. The moggel is endemic to the region (Jubb 1964), but
has also been translocated to several systems in the eastern Cape as well as
Gauteng. They prefer standing and slow flowing water where they feed on soft
sediments and detritus. Labeo umbratus (Smith, 1841) has an extremely long
and coiling intestine (Jubb 1972). They are also capable of surviving conditions
in dwindling pools of mud. These fish can breed prolifically, and produce a high
number of offspring. The moggel is likely to constitute a large proportion of the
fish population in dams where it occurs (Jubb 1972). Flooded grassy riverbanks
are preferred spawning sites, and after the summer rains, breeding adults
Chapter 3 - Fishes of southern Africa 26
migrate upstream to these sites. Eggs hatch after only 40 hours, and the growth
rate is rapid.
Species: Labeo capensis (Smith, 1841) (Figure 3.1D)
Common name: Orange River mudfish
The mudfish is used in physiological as well as ecological research, and also has
potential commercial value. This species prefers running water and occurs in the
Orange-Vaal system, and according to Jubb & Farquharson (1965) it is endemic
to the system. The mudfish is also a detritus feeder (Jubb 1972). Spawning
migrations to shallow rocky rapids take place from November to January. The
growth rate of the mudfish is also fairly rapid.
Barbs or Minnows
The minnows have a tetraploid number of chromosomes, unlike the yellowfishes,
which are hexaploid. Minnows occur in shoals, and are well camouflaged, but
often have distinct markings. They form an important food for larger fish, and are
also used for live bait, and as fodder for bass and trout. Breeding takes place in
a variety of ways, and males usually develop bright colours.
Species: Barbus anoplus Weber, 1897 (Figure 3.1 E)
Common name: Chubbyhead barb
Chubbyhead barbs are widely distributed through the whole system (Jubb 1972),
but are absent from the lower Orange. This species is used as forage fish, is
omnivorous, feeding on zooplankton and a variety of phytoplankton. The
chubbyhead barb prefers habitats with vegetation that can provide shelter.
Females lay adhesive eggs amongst the vegetation during summer after rain.
Larvae hatch after three days and three or four days later begin to feed and
swim.
Chapter 3 - Fishes of southern Africa 27
Species: Barbus pallidus Smith, 1841
Common Name: Goldie barb
The goldie barbs distribution is divided between the coastal streams of eastern
Cape and tributaries of the Vaal. This species form pairs when breeding in the
summer and eggs are laid in the marginal vegetation of rocky clear water
streams.
Species: Barbus trimaculatus Peters, 1952
Common name: Threespot barb
The threespot barb is part of a group of barbs known as the spinefin barbs.
Spinefin barbs differ from the other barbs in that their primary dorsal fin ray is
spinous and not serrated. Threespot barb is a hardy species with a very wide
distribution, and prefers vegetated waters. After rain the breeding adults occur in
shoals that migrate upstream to spawn.
Species: Barbus paludinosus Peters, 1852 (Figure 3.1F)
Common name: Straightfin barb
The straightfin barb is placed in the sawfin barb group, which have a bony,
serrated primary dorsal fin ray. This group includes a third of the Barbus species
in southern Africa. The distribution is wide, occurring from the Orange to
tributaries of the Congo. These fish prefer larger rivers and slow flowing streams
and occurs in vegetated, marginal waters. They feed on a wide variety of small
animals as well as algae, diatoms and detritus. Spawning takes place during
summer, and females can lie up to 2500 eggs. The straightfin barb is prayed
upon by a variety of larger fish, as well as man, as it forms an important
component of the "matemba" fishery of Malawi.
Species: Barbus hospes Barnard, 1938
Common name: Namaqua barb
This species occurs only below the Augrabies Falls in the Orange River, and also
belongs to the sawfin barb group. According to Jubb (1964) the Namaqua barb
Chapter 3 - Fishes of southem Africa 28
is endemic to the Orange River. They occur in the open water and feeds on
zooplankton. The conservation status of B. hospes Barnard, 1938 is now
classified as near threatened, but has benefited from the regulated water flow
below the hydroelectric dams.
Barilins and Neobolins
These are related groups of large mouth predatory species. The anal fin of these
fishes is longer based than that of the other African cyprinids. The larger barilins
occur in the tropics of Africa and Asia, with the neobolins being smaller and
entirely African.
Species: Mesobola brevianalis (Boulenger, 1908)
Common name: River sardine
These small, sardine-like fishes occur in the Orange River, but only below the
Augrabies Falls. This species was formerly placed in the genus Engraulicypris
Gunther, 1893, but was later placed in the genus Mesobola Howes, 1984. It also
occurs in the Cunene, the Okavango, and the upper Zambezi as well as on the
east coast. The river sardine occurs in well-aerated water of flowing rivers where
they shoal together and feed on zooplankton. Breeding takes place during early
summer.
Austroglanididae
These small catfishes are endemic to southern Africa, and one of their
characteristics is the placement of barbels on the lower jaw. The austroglanidids
resembles fish from the Bagridae and until recently the three known species
were placed in the genus Gephyroglanis Boulenger, 1899 (Jubb 1964, Jubb
1972, Jubb & Farquharson 1965 and Gabie 1965), within the Bagridae.
However, the African rock catfishes are now classified within the genus
Austroglanis Skelton, Risch & De Vos, 1984.
Chapter 3 - Fishes of southem Africa 29
Species: Austrog/an;s seteten (Boulenger, 1901) (Figure 3.2A)
Common name: Rock catfish
This small silurid occurs in the major tributaries and mainstream of the Orange-
Vaal system. According to Jubb (1972), this species frequents rocky areas, and
it prefers the rapids of these rocky habitats. Rock catfish feed on small
invertebrates, with the larger specimens also feeding on small fish.
Unfortunately, no information is available on the breeding habits of A. sclaferi
(Boulenger, 1901). All three species of the genus Austroglanis are listed in the
Red Data Book. This species is threatened mainly due to changes to their
habitat, including building of weirs and dams, and other human activities.
Clariidae
Clariids are well known for their ability to breathe air, which is attributed to the
multi-branched accessory branchial air-breathing organ (Jubb & Farquharson
1965), and are also able to withstand desiccation. Most clariid species are
relatively small, although some species like the vundu and the sharptooth catfish
can attain very large sizes, up to 59kg.
Species: Clerie« gariep;nus (Burchell, 1822) (Figure 3.2B)
Common name: Sharptooth catfish
In Africa, the genus Clarias Scopoli, 1777 comprises eight species, with the
sharptooth catfish being the most widespread, occurring almost throughout the
whole continent. This is also a very large species, found in almost any habitat,
but prefer slow flowing rivers, dams and lakes, and can dig burrows when faced
with diminishing water. These fish have also been observed crossing patches of
land. The sharptooth catfish feeds on any organic matter, and scavenges for any
available food. It is also an important source of food for many predators, and is
also a source of food for man. This species is capable of feeding in packs,
where they herd together small fish. Breeding takes place in summer and eggs
are laid on vegetation in shallow grassy verges of rivers and dams. Eggs hatch
after 25-40 hours and the free swimming larvae feed within two to three days.
Chapter 3 - Fishes of southern Africa 30
Most individuals take two years to mature and are capable of living up to eight
years or more. This is a very dominant species where they occur and
translocation may threaten indigenous species. Clarias lazera Valenciennes,
1840, C. mossambicus Peters, 1852 and C. gariepinus (Burchell, 1822) were
once treated as separate species, but they have all been synonymised with C.
gariepinus (Skelton 2001). Therefore, in the following sections, only reference to
Clarias gariepinus will be made.
Cichlidae
Representatives of the Cichlidae have a worldwide distribution, occuring in
Africa, parts of south America, and parts of Asia. According to Gabie (1965),
some of the members of the Cichlidae are tolerant of salt water. Cichlids are
important as food, and are also used in scientific studies. They are characterised
by scales on the head and the body, the pelvic fins are in the thoracic position,
the lateral line is divided, and a single nostril is found on each side of the snout.
In many cases pairs are formed during breeding, and usually the adults guard the
eggs and the young. Nests are also often built. In many species the eggs are
incubated in the mouth of one of the parents, usually the female. Two main
lineages exist within the southern African area. One line is those who are
sedimentary and plant feeders, the tilapiines, and are characterised by a dark
eye-spot on the base of the dorsal fin when they are young, called the "tilapia-
spot". The other line is the haplochromines, which tend to be predators. Adult
haplochromines usually have clear spots or ocelli on the anal fin, often referred to
as "egg-spots". The function of these spots is to assist in the fertilisation of the
eggs. This is the largest African family with eight genera and 41 species
reported in southern Africa.
River Breams
This group consists of seven different genera. They are, however, not
necessarily closely related. Most of these species are small, or moderate in size.
Only one genus from this group, namely Hemichromis Peters 1858, is not a
Chapter 3 - Fishes of southern Africa 31
mouth brooder. The males are usually brightly coloured during the breeding
season and most have egg-spots.
Species: Pseudocrenilabrus philander (Weber, 1897) (Figure 3.1C)
Common name: Southern mouth brooder
This species was formerly placed in the genus Hemihap/ochromis Wickier, 1963,
but was later placed in the genus Pseudocreni/abrus Fowler, 1934. Southern
mouth brooders are distributed from the Orange River and southern Natal
northwards to the southern Zaire tributaries and Lake Malawi. These fish occur
in a variety of habitats and prefer vegetated zones, where they feed on small
arthropods as well as small fish. The males establish a territory, and build a
simple nest during the breeding season, which is from spring to summer. The
males defend their territory and also attract sexually mature females. The female
collects the eggs in the nest and then retreats to a quiet area where the eggs,
larvae and juveniles are brooded. This species is used as an aquarium species
and also in behavioural and evolutionary research. Threats to the southern
mouth brooder include introduced species, habitat change and pollution.
Tilapiines
This is a major branch of the African cichlids. Most of the species have a
vegetarian diet, with small teeth, fine pharyngeal teeth, and extended intestines.
Some of the genera are substrate brooders, while others are mouthbrooders.
These fishes are of importance to man as food, and some are popular angling
species.
Species: Tilapia sparrmanii Smith, 1840 (Figure 3.20)
Common name: Banded tilapia
The genus Ti/apia Smith, 1840 includes all the species that are substrate
brooders, and adults retain the "tilapia spot". Banded tilapia are tolerant of a
wide range of habitats, and Jubb (1972) states that it is tolerant of cold water, but
prefers temperatures above 15°C. Skelton (2001) notes that this species is more
Chapter 3 - Fishes of southern Africa 32
restricted by warmer than colder waters. It has a wide distribution, and has also
been translocated to the Cape. The banded tilapia is also an omnivore, feeding
on a wide range of available foods, even small fish. According to Jubb (1972),
the banded tilapia forms breeding pairs and both parents guard the nest. This
species is a common component of subsistence fishing and is an occasional
angling species.
Introduced fishes of the Orange River
At least 22 species of fish have been introduced to southern Africa (Skelton
2001). According to Bruton & Van As (1986), the first fishes were introduced into
southern Africa over 260 years ago. Reasons for introducing the fish range from
sport fishing, aquaculture, which includes food for introduced fishes, the stocking
of man-made dams and biological control. The most important impact of the
introduced fishes is the introduction of their parasites, which threaten natural
communities (Bruton & Van As 1986). Another impact is the predation of
introduced fish on the indigenous species. Alien fish species can also affect the
water quality, for example the carp that disturbs the bottom sediments during
feeding and increases turbidity (Bruton 1985; Schrader 1985). Another threat is
the hybridization with invasive fish (Bruton & Van As 1986), which could produce
viable offspring. In the Orange River there are seven introduced fish species,
which will be discussed below.
Cyprinidae
Species: Cyprinus carpio Linnaeus, 1758 (Figure 3.2E)
Common name: Carp
The carp was introduced into South Africa in the 1700s and several importations
are reported in the 1800s, while the Aischgrund strain was imported in 1955.
Introduced carp is now widespread throughout southern Africa, but are absent
from mountain areas and restricted to the warmer tropical areas. Carp has
invaded more catchments areas than any other species and its range has
recently been extended into the Phongolo and upper Mkuze systems (De Moor &
Chapter 3 - Fishes of southern Africa 33
Bruton 1996). The natural distribution includes Central Asia to the Black Sea and
the Danube in Europe, but carp is now widespread throughout the world. Being
an omnivorous species, carp feed by grubbing in sediments. Breeding takes
place in spring and summer, and they lay sticky eggs amongst the vegetation. It
is reported that large females can lie up to a million eggs. Carp is considered as
a valued angling and aquaculture species, although it is considered as a pest by
conservation authorities.
Poeclflldae
Species: Gambusia affinis (Baird & Girard, 1853) (Figure 3.2F)
Common name: Mosquitofish
These fish are unique in that fertilisation is internal and they bear live young. The
anal fin of the male is modified to form an intromittent organ. Naturally occurring
in Central and South America, mosquitofish was introduced in 1936 by aquarists,
and scattered populations now occur throughout southern Africa. Mosquitofish
was bred and distributed by Cape Inland Fisheries as a mosquito control agent,
but has proven to be an aggressive invader species capable of restricting other
fish populations. Mosquitofish are tolerant of a wide range of water
temperatures, as well as salinities ranging from fresh to higher than seawater.
Salmonidae
Species: Sa/mo trutta Linnaeus, 1752
Common name: Brown trout
Brown trout occurs naturally in Europe and North East Africa, but have been
introduced to streams of the South West Cape, Southern Cape, Eastern Cape,
the Drakensberg and Lesotho. These fish prefer mountain or upland streams
with well-oxygenated water, where it feeds on aquatic and terrestrial insects,
crabs, frogs and small fish. Breeding takes place in autumn or early winter when
males migrate to suitable gravel beds and establish territories. The female
excavates a nest by rapidly beating her body and tail. Eggs usually hatch after
Chapter 3 - Fishes of southern Africa 34
about three weeks and small trout gradually move downstream and begin
feeding.
Species: Oncorhynchus mykiss (Walbaum, 1792)
Common name: Rainbow trout
This species occur naturally in rivers of the Pacific Coast of North America from
northern Mexico to Alaska. Rainbow trout was introduced to dams and mountain
streams of southwestern, southern, eastern, northeastern Cape, Kwazulu -
Natal, eastern Gauteng, Swaziland and eastern Zimbabwe. Rainbow trout
occurs in clear well-aerated waters, feeding on a wide range of food sources
such as small invertebrates, crabs, frogs and even small fish. According to Jubb
(1972) in areas where the rainbow trout and the smallmouth yellowfish ranges
overlap, the number of small yellowfishes are becoming scarce due to the
predation of the trout on young immature yellowfish. Breeding takes place in
winter when breeding fish move to gravel beds where females dig a nest in which
spawning takes place. Eggs hatch after four to seven weeks and the larvae are
free swimming within a week.
Centrarchidae
Species: Lepomis macrochirus Rafinesque, 1819
Common name: Bluegill Sunfish
The natural distribution of the bluegill sunfish is eastern and central North
America. They are found in Cape coastal drainages, the middle reaches of rivers
in Kwazulu - Natal, southeastern and eastern Gauteng and northeastern Free
State. It was introduced into Lesotho as forage fish for the largemouth bass
(Jubb 1972). This species prefers well-vegetated water in rivers and dams.
They prey on invertebrates and small fish. Bluegill sunfish are considered a pest,
as they tend to overpopulate water and feed on the indigenous fish species.
Species: Micropterus salmoides (Lacepéde, 1802)
Common name: Largemouth Bass
Chapter 3 - Fishes of south em Africa 35
Largemouth bass occur naturally in central and eastern North America from the
Gulf of Mexico to southern Canada. It was introduced to the Cape in 1928 and a
subspecies known as Florida Bass (M. s. floridianus) was introduced to Kwazulu
- Natal in 1980. It occurs throughout Cape coastal drainages, Kwazulu - Natal
and Gauteng, although Jubb (1972) stated that there was no evidence that bass
have escaped and become established in any of the rivers. Largemouth bass
are also found in Malawi, Namibia and Zimbabwe. These fish prefer standing or
slow-flowing waters with submerged and floating vegetation. This is a primarily
piscivorous species, but will also feed on frogs, snakes and small mammals.
Males construct a nest and guard it, as well as the newly hatched larvae.
Largemouth bass is a very popular freshwater gamefish species.
Species: Micropterus dolomieu (Lacepéde, 1802)
Common name: Smallmouth bass
According to Jubb (1972), the small mouth bass was introduced into some dams
in Lesotho in 1937 to enhance the river fishing below the Trout zone. It now also
occurs in some rivers in southwest and eastern Cape, Kwazulu - Natal and
Gauteng and is found in the Caledon and Orange Rivers. Normally smallmouth
bass occur in flowing water and prefers rocky substrates. Males also construct a
nest and guard the eggs and larvae. The young fish feed on insects and small
fish, whilst the adults are mainly piscivorous, feeding on crabs occasionally. This
species is very successful in southwest Cape, and for this reason bass is no
longer stocked or produced by nature conservation authorities.
Chapter 3 - Fishes of southern Africa 36
The fish species of the Modder River
In Table 3.1 a list of fishes that occur in the Modder River, a tributary of the
Orange River, is compiled. The species in bold print indicate those that were
collected during the study period.
Cyprinidae
Introduced species
A B
c
E F
Figure.3.1. IIlustratoins of the fishes from the Modder River. A - Labeobarbus kimberleyensis (Gilchrist
& Thompson, 1913). B - L. aeneus (Burchell, 1822), C - Labeo umbratus (Smith, 1841),0 - L. capensis
(Smith, 1841), E - Barbus anoplus (Weber, 1897), F - B. paludinosus Peters, 1852. Taken from Skelton
(1993). (Not to scale).
A B
c
F
:1>"
Figure. 3.2. Illustrations of the fishes from the Modder River. A - Austroglanis sclateri (Boulenger, 1801),
B - Clarias gariepinus (Burchell, 1822), C - Pseudocrenilabrus philander (Weber, 1897), 0 - Tilapia
sparrmanii Smith, 1840, E - Cyprinus carpio Linnaeus, 1758, F - Gambusia affinis (Baird & Girard, 1853).
Taken from Skelton (1993). (Not to scale).
Results
The results of my study are presented in chapters 4-6. Each chapter is
concerned with a specific group of parasites, with the systematics and
literature of the respective group discussed first, followed by the results of
parasites collected from Soetdoring Nature Reserve. This includes diagrams
as well as light micrographs. For all groups where measurements are given,
these are presented as they appeared in original form. Where measurements
were not available, it was omitted or was measured from available drawings.
Diagrams have been redrawn from the original publication, or if not available,
redrawn from other authors. For the monogeneans, authors in the past did
not provide diagrams of all rnarqinal hooklets. In these cases only those
hooklets available are given. More recent cases, where all hooklets were
provided, it appears from number I-VII. This does not apply to diagrams of
Quadriacanthus, where the numbers of the marginal hooklets are given, since
the numbering of marginal hooklets from this genus differs from those of
Dacty/ogyrus and Dogie/ius.

Chapter 4 - The Ciliophora 40
1"lhe [p)lhy~tUlm Cn~~olP'lh(Q)lral Doflein, 1901
The ciliophorans are a group of acellular organisms, which include free-living,
commensalistic and parasitic forms. According to Lam & Dyková (1992) the
ciliophorans occurring in or on fish and may range from completely harmless
ectocommensals to very dangerous pathogens. Some ectoparasitic species
have no host preference, such as Ichthyopthirius Fouquet, 1876, which is
capable of infecting most teleast fishes. The endocommensal species, however,
may be restricted to a few host species. Ciliophorans generally possess one or
more diploid micronuclei, which are generative, as well as one or more polyploid
macronuclei, which are vegetative. Reproduction takes place either by binary
fusion, or sexually through the process of conjugation (Lam & Dyková 1992).
Since Van Leeuwenhoek observed the first acellular organism In 1676, the
taxonomy of the protozoans has undergone extensive revision. These will not be
discussed in detail, but will be summarised below.
Before the 1970's, all acellular organisms were placed under the phylum
Protozoa Goldfuss, 1820, according to the Butschli-Kahl classification system,
and the ciliophorans were all placed in the class Ciliata of the sub-phylum
Ciliophora (Corliss 1979). The system of Kahl (1932) was based on somatic
ciliation and the appearance of the adults (Lam & Dyková 1992).
The group shows many homogenous characters, which differs from the rest of
the Protozoa. At that stage the Ciliata was the only class in the sub-phylum, and
based on the diversity of forms and the extent of species which were included in
the class, Raabe (1964) suggested that the subphylum be elevated to the rank of
phylum. Corliss (1974) supported this suggestion and this led to the elevation
from sub-phylum to phylum.
Chapter 4 - The Ciliophora 41
Two major works appeared in 1994, concerning the higher systematics of the
Ciliophora. One of these works concerns the anatomy, systematics and biology
of the phylum Cilophora (Batisse, Bonhomme-Florentin, Deroux, Fleury,
Foissner, Grain, Laval-Peuto, Lom, Lynn, De Puytorac & Tuffrau 1994). The
other work is that of Corliss (1994) in which a user-friendly classification for all
the protists is proposed. These works differ from each other in that Corliss only
mentioned eight classes, with no subphylum division, whereas De Puyterac
begins the book with the classification of the Ciliophora with three subphyla, and
eleven classes.
The classification of Lom & Dyková (1992) is essentially that of Levine, Corliss,
Cox, Deroux, Grain, Honigberg, Leedale, Loeblich, Lom, Lynn, Merinfield, Page,
Polyanski, Sprague, Vavra and Wallace (1980). This system is based on the
structure of the buccal apparatus, as well as features of the cortex.
The work of Lom & Dyková (1992) is concerned with the protozoan parasites of
fishes, which includes three classes, i.e. the Kinetophragminophorea de Puytorac
et al., 1974, the Oligohymenophorea de Puytorac et al., 1974, and the
Polyhymenophora Jankowski, 1967.
This chapter will deal with two groups of ciliophorans, i.e. the sessiline
ciliophorans and the mobiline ciliophorans, both in the subclass Peritrichia. As
the aquatic parasitology research group of the University of the Free State has
done extensive research on the ciliophorans, this chapter will only be concerned
with research done in South Africa. The classification that will be used here is
that of Lom & Dyková (1992) (Table 4.1).
Chapter 4 - The Ciliophora 42
Vestibulifera de Pu et al., 1974 Trichostomatida
Hypostomata Schewiakoff, 1896 Cyrtophorida
Suctoria Claparéde & Lachmann, 1858 Suctorida
Hymenostomatida
Hymenostomata Delage & Hérouard, 1896
Scuticociliatida
Sessilina
Peritrichida Steyn, 1859
yhymenophora Spirotricha Botschli, 1889 Heterotrichida
ankovski, 1967
Chapter 4 - The Ciliophora 43
Sessiune clllophorans
Class: Oligohymenophorea de Puytorac et al, 1974
Subclass: Perttrlchlda Steyn, 1859
Order: Sessilina Kahl, 1933
These sessiline organisms occur on the gills as well as the skin of both
freshwater and marine fish. They attach to the host by means of a scopula,
which can either adhere directly to the substrate, or it can be cemented to the
substrate. In some cases a stalk is also secreted, which is in most cases non-
contractile. If the stalks are contractile, they posses a central spasmoneme,
which ensures the contractility of the stalk. According to Lom & de Puytorac
(1994), the body of these animals is bell-shaped to cylindrical, ovoid or conical.
The peristomal disc is generally well developed. A peristomal lip is situated on
the border of the peristome. The adoral spiral with two rows of cilia is situated on
the inside of this lip.
Sessolone Cilnophorans known from South Africa
The Gen us Apiosoma Blanchard, 1885
Generic diagll1losis
Species of this genus are solitary and occur mostly as ectoparasites on
freshwater fish. According to Viljoen & Van As (1985) the body is cylindrical to
elongate cup-shaped. The body tapers sharply and the scopula is small. Some
members of this genus posses a non-contractile stalk. The peristomallip covers
the peristomal disc, which is convex, and the adoral cilia, which consists of both
haplo- and polykinety. A single contractile vacuole is situated directly below the
peristome. The macronucleus is usually conical, and the apex is pointed towards
the scopula (Lom & Dyková 1992). In some cases the macronucleus is
ellipsoidal. One micronucleus is present, which is situated in the region of the
macronucleus (Viljoen & Van As 1985).
Chapter 4 - The Ciliophora 44
Species of Apiosoma known from South Africa
Viljoen & Van As (1985) described nine species of the genus Apiosoma from fish
collected from lakes, rivers, streams and ponds in South Africa. Seven of the
species were described as new species by these authors. The two known
species collected were Apiosoma nasalis (Timofeev, 1962) collected from
Pseudocrenilabrus philander (Weber, 1897) and A. piscicola Blanchard, 1885
collected from Barbus paludinosus (Peters, 1852), B. frimaculafus, Labeo
cylindricus Peters, 1852, Marcusenius macrolepidofus (Peters, 1852),
Micropferus dolomieu (Lacepêde, 1802), Oreochromis mossambicus (Peters,
1852), P. philander and Tilapia rendalli Dumeril, 1859.
The seven new species described by Viljoen & Van As (1985), included
Apiosoma eeutete Viljoen & Van As, 1985 collected from the skin and gills of
Mesobola brevianalis (Boulenger, 1908), A. curvinucleafa Viljoen & Van As, 1985
from the skin of O. mossambicus, A. micralesfi Viljoen & Van As, 1985 collected
from the skin of Micralesfes acufidens (Peters, 1852), A. mofhlapifsis Viljoen &
Van As, 1985 from the skin of Labeobarbus marequensis Smith 1841, A. obliqua
Viljoen & Van As, 1985 from the skin of L. cylindricus, A. phiala Viljoen & Van As,
1985 collected from the skin and gills of L. marequensis, B. paludinosus, B.
frimaculafus Peters, 1852, B. unifaeniafus Gunther, 1866, L. capensis (Smith,
1841), L. cylindricus, Mesobola brevianalis, O. mossambicus and P. philander as
well as A. viridis Viljoen & Van As, 1985 from the skin of O. mossambicus, P.
philander, T. rendalli and T. sparrmanii Smith, 1840.
The Genus Scopulata Viljoen & Van As, 1985
Generic diagnosis
According to Viljoen & Van As (1985) representatives of this genus are
ectoparasites of freshwater fish. The genus Scapula fa was created to
accommodate species that do not conform to characters of the genus Scyphidia
Dujardin, 1841. The body of these ciliophorans is cylindrical with a broad
scapula, and the body is not stalked. A prominent unciliated groove encircles the
Chapter 4 - The Ciliophora 45
body. The body is also encircled by pellicle striations. When the peristomallip is
expanded, adoral cilia consisting of haplo- and polykinety complete a spiral of
more than 360°, as well as a convex peristomal disc is revealed. A contractile
vacuole, as well as food vacuoles (in most species) is situated in the region
above the groove. The macronucleus is situated below the groove, with only one
micronucleus present, either below or alongside the lower part of the
macronucleus.
spectes of Scopulata known from South Africa
Van As & Viljoen (1985) described one new species in 1985, when they created
the genus. This species was Scopulata constrieta Viljoen & Van As, 1985 from
the skin of Oreochromis mossambicus. Two other species already described by
Viljoen & Van As (1983) as Scyphidia, were placed in the genus Scopulata in
1985. These species were S. dermata (Viljoen & Van As, 1983) from the skin of
Marcusenius macrolepidotus, Micralestes acutidens, B. trimaculatus, O.
mossambicus, P. philander, T. rendalli and T. sparrmanii, as well as S.
epibranchialis (Viljoen & Van As, 1983) collected from the gills and occasionally
the skin of M. dolomieu, O. mossambicus and P. philander.
Lom & Dyková (1992), however, provide the following key to the genera of
sessiline ciliophorans that are parasitic on fish.
1. a. Ciliophorans attached to the substrate directly by their scopula, mostly
circular, often a large diameter, sometimes lobed, occasionally split into
long projections... 2
b. Ciliophorans attached by semicircular outgrowths of the scopula joined
to form circle around secondary lamellae of gills ...
Caliperia Laird, 1953
c. Ciliophorans attached by means of secreted stalk... 4-
2. a. The locomotory fringe of cilia occurs only in telotrochs... 3
Chapter 4 - The Ciliophora 46
b. The locomotory fringe is permanent, occurring also in attached
ciliophorans... Ambiphrya Raabe 1952
3. a. Macronucleus is compact, conical or ellipsoidal, the cell shape usually
elongated conical... Apiosoma Blanchard 1885
b. Macronucleus is sausage-shaped, cell shape mostly cylindrical ...
Riboscyphidia Jankowski, 1980
4. a. A non-contractile stalk is branched, bearing a small colony of several
zooids... Epistylis Ehrenberg, 1830
b. The non-contractile stalk is short and bears a spoon-like shield
sheltering a single zooid... Propyxidium (Kent, 1881)
c. The stalk is contractile, unbranched, bearing a single zooid or
branched, bearing colonies of many zooids ...
opportunistic epibionts of the
genera Vorticella (Linnaeus, 1758), Zoothamnium (Modeer, 1790) and
Carchesium (Linnaeus, 1758).
According to this key, all species, which were formerly placed within the genus
Scopulata, are now placed within the genus Apiosoma. As the classification of
Lom & Dyková (1992) is used, for this dissertation the species of Scopulata will
be treated as species of Apiosoma.
A summary of the species of Apiosoma occurring in South Africa is given in
Table 4.2. The measurements of these species are summarised in Table 4.3.
Chapter 4 - The Ciliophora 47
Mesobola brevianalis Skin and Gills
Oreochromis mossambicus Skin
O. mossambicus Skin
Barbus trimaculatus Peters, 1852,
(Figure 4.2F) Pseudocrenilabrus philander (Weber, 1897) T. Skin
rendalJi Gilchrist & Thompson, 1917, T. sparrmanii
1840
Gills and occasionally
P. philander skin
Micralestes acutidens Skin
Skin
Skin and Gills
Skin
L. marequensis, Barbus paludinosus Peters, 1852,
B. frimaculatus, B. unitaeniatus Gunther, 1866, Skin and Gills
Labeo capensis (Smith, 1841), L. cylindricus, M.
brevianalis, Oreochromis mossambicus, P.
Skin
Skin
Chapter 4 - The Ciliophora 48
31.6-60.6 5.8-11.4 13.8-31.2 15.0-25.6 2.8-8.2 3.1-9.4
21.3-33.8 14.3-28.5 11.7-18.4 12.7-19.4 3.1-3.7 1.9-3.4
113.7-171.5 31.3-50.5 8.8-22.1 50.4-70.0 15.6-25.9
16.8-38.6 14.8-32.8 12.4-20.4 11.4-18.6 2.7-4.1 1.4-2.2
20.1-28.9 10.9-29.1 7.9-17.6 11.3-15.9 2.1-3.9 1.3-3.0
31.2-54.1 19.2-37.4 4.2-9.2 11.2-23.2 11.8-21.0 2.8-7.4 2.7-4.5
20.1-37.8 11.2-25.8 1.5-4.3 6.4-13.0 10.0-16.8 2.0-6.4 2.5-6.7
27.9-40.0 13.8-8.2 4.8-8.2 8.8-15.1 10.1-12.0 1.8-3.2 1.9-3.1
29.2-53.8 17.3-34.0 2.3-6.3 6.6-14.2 5.9-15.2 1.1-2.5 1.1-3.6
22.5-49.8 15.1-34.1 3.4-9.6 9.7-20.5 8.8-19.6 3.9-6.7 1.7-4.6
47.0-84.5 17.3-39.6 7.3-19.3 15.0-26.1 7.6-15.8 3.2-6.9 1.6-2.7
32.7-90.8 14.3-45.0 11.2-17.8 8.5-16.7
IB c
D E IF
Figure.4.1. Diagrammatic drawings of sessiline ciliophorans from South Africa. A - Apiosoma eau/ata
Viljoen & Van As, 1985 (redrawn from Viljoen & Van As 1985). B - A. piseieo/a Blanchard, 1885,
(redrawn from Viljoen & Van As 1985). C - A. miera/esti Viljoen & Van As, 1985 (redrawn from Viljoen &
Van As 1985). D - A. eurvinue/eata Viljoen & Van As, 1985 (redrawn from Viljoen & Van As 1985). E-
A. phia/a Viljoen & Van As, 1985 (redrawn from Viljoen & Van As 1985). F - A. viridis Viljoen & Van As,
1985 (redrawn from Viljoen & Van As 1985). Scale bar: 40IJm
A B c
D lE IF
Figure. 4.2. Diagrammatic drawings of sessiline ciliophorans from South Africa. A - Apiosoma obliqua
Viljoen & Van As, 1985 (redrawn from Viljoen & Van As 1985). B - A. nasalis (Timofeev, 1962) (redrawn
from Viljoen & Van As 1985). C - A. mothlapitsis Viljoen & Van As, 1985 (redrawn from Viljoen & Van As
1985). D - A. epibranchialis (Viljoen & Van As, 1983) (redrawn from Viljoen & Van As 1985). E - A.
constrieta Viljoen & Van As, 1985 (redrawn from Viljoen & Van As 1985). F - A. dermata (Viljoen & Van
As, 1983) (redrawn from Viljoen & Van As 1985). Scale bar: 40j.Jm
Chapter 4 - The Ciliophora 51
Mobiline Ciliophorans
Class: Oligohymenophorea de Puytorac et al, 1974
Subclass: Peritrichida Steyn, 1859
Order: Mobilina Kahl, 1933
The Mobilina Kahl, 1933 are constantly moving ciliophorans that can be
compared to the telotroch stage of sessiline ciliophorans. Body shape can vary
from flat discoid to hemispheric (Lam & Dyková, 1992). The most prominent part
of the body is the adhesive disc, which is situated on the aboral side of the
protist, and consists of skeletal structures that consist of three rings, which are
concentrically arranged. The most prominent is the innermost ring, the denticle
ring. The shape and structure of the denticles are very important in
distinguishing between the species. The denticle ring consists of a number of
denticles, which consists of a blade, a central part and a ray.
The adhesive disc is circular and is supported by the skeletal complex, which
consists of the denticle ring surrounded by the striped membrane. Directly
underneath the velum, which is formed by a fold in the pellicle, 50-100 marginal
cilia occur. Two rows of aboral cilia are present one consisting of short and soft
cilia and another row of long movable cilia. The macronucleus is horseshoe-
shaped. Mobiline ciliophorans occur on the skin as well as the gills of freshwater
and marine fish.
Lam & Dyková (1992) provide the following key to trichodinid genera occurring
on fish.
1. a. Adoral spiral makes two and a half to three turns ...
Vauchomia Mueller, 1938
b. Adoral spiral makes slightly more or slightly less than one turn ...
2
c. Adoral spiral makes one half to three-quarters of a turn... 3
.. V.. IBLlOT
Chapter 4 - The Ciliophora 52
2. a. Denticles with well-developed rays and blades ...
Trichodina Ehrenberg, 1838
b. Blades of denticles stunted ...
Hemitrichodina Basson & Van As, 1989
3. a. Denticles with well developed rays... 4
b. Rays stunted to form short crooks or platelets ...
Trichodinella Srámek-Husek, 1953
c. Rays absent, central part indistinct, blades triangular ...
Diparliella (Raabe, 1959)
3. a. Blades attached almost perpendicular to central part and denticles
interlocked only by conical central parts ...
Paratrichodina Lom, 1963
b. Blades extend obliquely backward from central part; denticles
interlocked by central parts and anterior projections of blades fitting into
corresponding notches in blades of preceding denticles ...
TriparlielIa Lom, 1959
The genera Trichodina Ehrenberg, 1838, Tripartiella Lom, 1959
and! Trichodinella Srámek-Husek, 1953
Lam (1958) provides a system of uniform specific characters for the description
of species, which is still being used, together with the characters suggested by
Van As & Basson (1989). These characters include the shape, the dimensions,
number, and diameter of the denticles. The number of radial pins of the striped
membrane has to be determined between the bordering denticles. For the
macronucleus, the diameter, width and the distance between the two
terminations are of importance. Shape and placement of the micronucleus is
also important.
Chapter 4 - The Ciliophora 53
The Genus Trichodina Ehrenberg, 1838
Generic Diagnosis
According to Basson & Van As (1989) the denticles of representatives of this
genus consist of blades, central parts and rays. The blades may be straight or
curved. The rays display various shapes, which may be rod-like, spine-shaped
or needle-shaped. They may also vary in length. There are no anteriorly
directed projections present in the central part. The adoral spiral can vary in
length, from 360° to 540°.
The genIUs Trichodinella Srámek-Husek, 1953
Generic diagnosis
The denticles of species from this genus have a delicate central part. Between
the central part and the blade, there is a notch into which a projection of the
anterior border of the central part from the following denticle fits well. This
causes the denticles to be wedged together by both the central parts and the
projections. The rays form a short delicate hook, which is curved along the
central part. The adoral spiral may vary from 180° to 2700 (Basson & Van As
1989).
The GenIUIsTriparlielia Lom, 1959
Generic diagnosis
According to Basson & Van As (1989) the denticle has a delicate central part,
with a ray that is in most cases directed backwards and a blade that is also
slanted obliquely backwards. The narrow bases of the blades by which they
connect to the central part, extends anteriorly and forms projections, which may
vary from short and thin, to wide and knee-like. These projections correspond
with a notch on the preceding denticle and thus the denticles are wedged
together by the central parts as well as the projections. The turn of the adoral
spiral may vary from 1800 to 2900.
Chapter 4 - The Ciliophora 54
Trichodinld species known from South Africa
The first description of trichodinids from the gills as well as the skin of freshwater
fish from South Africa was by Basson, Van As & Paperna (1983). They recorded
seven known species of trichodinids namely Trichodina acuta Lam, 1961 from
Pseudocrenilabrus philander, Tilapia rendalli, T. sparrmanii, Barbus trimaculatus,
and Cyprinus carpio Linnaeus, 1758; T. heterodenfata Duncan, 1977 from T.
rendalli, T. sparrmanii, B. paludinosus, B. trimaculatus and C. carpio; T. mutabilis
Kazubski & Migala, 1968 from B. paludinosus, B. trimaculatus and Carassius
auratus Linnaeus, 1758 (collected from a fish farm); T. nigra Lam, 1960 from
Oreochromis mossambicus, P. philander, Tilapia sparrmanii, and B. paludinosus;
T. pediculus Ehrenberg, 1838 from O. mossambicus, Tilapia rendalli, and T.
sparrmanii and Trichodinella epizootica (Raabe, 1950) from O. mossambicus, T.
rendalli and C. carpio.
Two new species were also described by Basson et al (1983). These included:
Trichodina centrostrigeata Basson, Van As & Paperna, 1983 from O.
mossambicus, P. philander, T. rendalli, T. sparrmanii and C. carpio and
Trichodina minuta Basson, Van As & Paperna, 1983 from O. mossambicus, P.
philander, T. sparrmanii and B. trimaculatus.
When a reappraisal of previously published material of Basson et al (1983) was
done, they came to the conclusion that the population of T. acuta reported from
South Africa in 1983 differed significantly from the original description by Lam
(1961). Van As & Basson (1989) then described Trichodina compacta Van As &
Basson, 1989, which was previously recorded as T. acuta.
In the same publication of 1989, Van As & Basson also described T. uniforma
Van As & Basson, 1989 and T. kazubski Van As & Basson, 1989 bath of which
were previously identified as T. mutabilis in 1983 from South Africa. New
surveys in southern Africa also revealed that the species that was recorded as T.
pediculus by Basson et al (1983) also differed significantly from populations
described from Europe by Kazubski & Migala (1968). As a result Van As &
Chapter 4 - The Ciliophora 55
Basson (1989) described T. magna Van As & Basson, 1989 from the populations
previously recorded as T. pediculus. Two years later, Trichodina marifinkae
Basson & Van As, 1991 was described from Clarias gariepinus (Burchell, 1822)
by Basson & Van As (1991).
According to Basson' (pers. comm.), however, T. mufabilis has indeed been
recorded since, from fish supplied to them by dealers in the ornamental fish
trade.
In 1993, Basson & Van As recorded the first confirmed European species of
Trichodina from South Africa. These species were T. acufa, and T. reticulete
Hirschmann & Partsch, 1955, which were collected from fish introduced into
South Africa, namely Carassius aurafus and Oncorhynchus mykiss.
In 1987, Basson & Van As did research in South Africa and described six new
species of TriparlielIa from the gills of freshwater fishes, namely T. clavodonfa
Basson & Van As, 1987 from O. mossambicus, P. philander and Mesobola
brevianalis; TriparlielIa lechridens Basson & Van As, 1987 from L. cylindricus, C.
carpio, O. mossambicus, M. brevianalis, B. paludinosus, B. frimaculafus and
Micralesfes acufidens; T. lepfospina Basson & Van As, 1987 from O.
mossambicus; T. macrosoma Basson & Van As, 1987 from Barbus eufaenia
Boulenger, 1904; T. nana Basson & Van As, 1987 from O. mossambicus and T.
orlhodens Basson & Van As, 1987 from T. rendalli swiersfrae Gilchrist &
Thompson, 1917.
One species of Trichodinella was also described by Basson & Van As (1987),
namely T. crennulafa Basson & Van As, 1987 from M. acufidens.
A summary of the trichodinid species occurring in South Africa is given in Table
4.4, and the measurements of these species are given in Table 4.5.
1 Prof. Linda Basson is a leader in the field of mobiline ciliophorans and is an associated
Professor at the University of the Free State, Bloemfontein, South Africa.
Chapter 4 - The Ciliophora 56
Skin
Skin
. compacta enger,
Van As & Basson, 1989 (Figure 4.3C) 1853, B. trimaculatus Peters, 1852, C. carpio, Skin
Labeobarbus marequensis Smith 1841, L
/cimberleyensis (Gilchrist & Thompson, 1913), Labeo
cylindricus Peters, 1852, P. philander, T. rendalli
rendalli (Boulenger, 1896), T. rendalli swierstrae
Gilchrist & 1917 T. c::n;.rr"n;or,;;
T.
Skin and Gills
Skin and Gills
Skin
P. philander, T. sparrmanii, B. trimaculatus Skin and Gills
Skin and Gills
Carassius auratus Linn 1758
Skin and Gills
Skin and Gills
Skin and Gills
Gills
Gills and occasionally
skin
Gills
L. cylindricus, C. carpio, B. paludinosus, B. Gills
trimaculatus
Oreochromis mossambicus Gills
Gills
O. mossambicus Gills
T rendalli swierstrae Gills
Chapter 4 - The Ciliophora 57
acuta 50.0-67.0 39.0-57.0 4.0-5.0 23.0-36.0 18-22 6.0-9.0 5.0-8.0 2.0-3.5 4.5-6.0
1961
37.4-54.4 31.2-45.8 2.0-4.4 18.7-33.3 26-30 2.0-6.2 3.2-6.0 1.1-3.0 2.8-6.4
40.9-58.9 31.7-49.1 3.8-5.5 18.3-29.7 18-21 3.8-7.3 2.5-4.6 1.8-4.2 2.9-4.7
heterodentata 47.5-69.1 39.5-59.8 3.2-6.2 23.2-37.8 22-29 5.1-8.6 4.6-8.1 1.6-3.3 3.4-5.5
Dunca 1977
T. kazubski
Van As & 34.3-54.6 26.7-39.5 3.2-5.9 16.4-26.3 22-26 3.6-5.7 3.6-6.4 1.5-3.2 3.5-5.7
1989
T. magna
Van As & 71.2-118.8 59.7-94.8 6.2-13.9 35.6-57.5 24-27 7.4-13.6 7.7-16.0 3.7-7.4 6.0-10.9
Basson 1989
T. minuta
Basson, Van As 28.2-38.0 22.4-33.7 2.6-4.1 12.2-18.2 19-22 3.2-5.7 2.6-4.4 1.7-2.7 3.1-4.6
&P rna 1983
T. nigra
Lom 1960 41.7-56.7 31.7-42.6 4.0-5.9 18.9-23.7 19-22 5.1-7.5 2.5-4.9 1.6-3.0 3.3-5.9
T. reticulata
Hirschmann & 40.0-55.0 31.0-46.0 3.0-5.0 20.5-29.0 22-27 4.0-6.0 3.5-6.0 1.0-2.0 4.5-6.5
Partsch 1955
T. uniforma
Van As & 47.9-74.8 37.6-62.5 3.9-7.4 24.5-40.6 24-29 5.2-8.7 5.8-9.5 2.0-3.5 5.5-8.3
Basson 1989
Chapter 4 - The Ciliophora 58
crennnulata 20.7-27.2 16.9-23.3 1.6-3.2 8.8-11.2 21-26 2.2-3.6 0.7-1.3 0.7-1.3 3.1-5.6
18.2-26.5 14.4-22.5 1.5-2.3 7.4-13.2 20-25 1.8-2.9 0.5-1.5 0.7-1.2 1.7-3.8
19.3-25.0 15.7-20.0 1.7-2.6 9.0-12.3 18-24 2.5-3.5 1.5-2.2 0.7-1.4 1.8-3.1
Basson & Van 19.1-24.7 15.4-20.4 1.6-2.8 7.1-11.0 20-26 1.8-4.3 0.6-1.7 0.8-1.6 3.0-4.7
As 1987
T. leptospina
Basson & Van 18.7-26.2 14.4-22.3 1.7-2.8 6.8-10.1 16-21 2.3-3.7 1.0-2.1 0.7-1.4 2.2-4.2
1987
T. macrosoma
Basson & Van 18.0-23.4 13.6-19.9 1.7-2.7 6.4-9.3 22-25 2.5-4.0 1.0-2.3 0.9-1.4 2.4-4.3
As 1987
T.nana
Basson & Van 16.8-26.1 13.3-21.6 1.0-2.5 6.7-10.8 16-19 2.2-3.6 0.6-1.6 0.8-1.5 1.7-3.3
1987
27.6-36.5 23.0-31.7 2.2-3.6 12.8-16.3 24-28 3.3-4.5 1.8-3.0 1.2-2.6 3.0-5.4
A B
c ID
lE IF
Figure. 4.3. Diagrammatic drawings of the denticles of trichodinids recorded from South Africa. A-
Trichodina acuta Lom, 1961 (redrawn from Basson & Van As 1993). B - T centrostrigeata Basson, Van
As & Paperna, 1983 (redrawn from Basson, Van As & Paperna 1983). C - T compacta Van As & Basson,
1989 (redrawn from Van As & Basson 1989). 0 - T heterodentata Duncan, 1977 (redrawn from Basson,
Van As & Paperna 1983). E - T. kazubski Van As & Basson, 1989 (redrawn from Basson & Van As,
1989). f - T. magna Van As & Basson, 1989 (redrawn from Van As & Basson 1989). Scale bar: 10IJm
A B
c ID
E
Figure. 4.4. Diagrammatic drawings of the denticles of trichodinids recorded from South Africa. A-
Trichodina minuta Basson, Van As & Paperna, 1983 (redrawn from Basson, Van As & Paperna 1983). B
- T. mutabilis Kazubski & Migala, 1968 (redrawn from Basson, Van As & Paperna 1983). C - T. nigra
Lom, 1960 (redrawn from Basson, Van As & Paperna 1983). D - T. uniforma Van As & Basson, 1989
(redrawn from Van As & Basson 1989). E - T. reticulafa Hirschmann & Partsch, 1955 (redrawn from
Basson& Van As 1993). Scale bar: 10f.Jm
A B
c D
Figure. 4.5. Diagrammatic drawings of the denticles of trichodinids recorded from South Africa. A-
Trichodinella crennulata Basson & Van As, 1987 (redrawn from Basson & Van As 1987). B - T.
epizootica (Raabe, 1950) (redrawn from Basson, Van As & Paperna 1983). C - Tripartiella clavodonta
Basson & Van As, 1987 (redrawn from Basson & Van As & 1987). 0 - T. lechridens Basson & Van As,
1987 (redrawn from Basson & Van As 1987). Scale bar: 1oum
A B
c o
Figure. 4.6. Diagrammatic drawings of the denticles of trichodinids recorded from South Africa. A-
Tripartiella leptospina Basson & Van As, 1987 (redrawn from Basson & Van As 1987). B - T. macrosoma
Basson & Van As, 1987 (redrawn from Basson & Van As 1987). C - T. nana Basson & Van As 1987
(redrawn from Basson & Van As 1987). D - T. orthodens Basson & Van As, 1987 (redrawn from Basson
& Van As 1987). Scale bar: 5IJm
Chapter 4 - The Ciliophora 63
Ciliophoran parasites from Soetdorlnq Nature Reserve
Two species of Apiosoma were collected from fishes of the Soetdoring Nature
Reserve. Apiosoma sp. A from the skin of P. philander and T. sparrmanii and
Apiosoma sp. B. from the gills of P. philander and C. carpio.
Six species of trichodinid parasites were collected. The species collected
represent three genera, i.e. Trichodina, Trichodinella and Tripartiella.
Trichodina sp. A was collected from the gills of Pseudocrenilabrus philander and
Trichodina sp. B from the gills of both Labeo capensis and Cyprinus carpio.
Trichodina sp, C was also collected from the gills of L. capensis and C. carpio.
One species of Trichodinella was collected, Trichodinella sp. A from the gills of
C. carpio, L. capensis and L. umbratus. Two species of Tripartiella were
collected, i.e. Tripartiella sp. A from the gills of L. capensis and L. umbratus, and
Tripartiella sp. B from L. capensis.
Apiosoma sp, A
Hosts and locality: Pseudocrenilabrus philander and Tilapia sparrmanii,
Soetdoring Nature Reserve, South Africa (280 52' S, 260 0' E).
Infection Site: Skin.
Specimens studied: Morphometric measurements and drawings were made
using light microscopy. Reference material (V2001/05/08-05, V2001/03/21-27) in
the collection of the Aquatic Parasitology Study group, University of the Free
State.
Description:
Stalkless. Body cylindrical (Figure 4.7A1& A2, Figure 4.10A), tapering towards
scopula. Length of body 54.7-80.7 (70.4, 9), diameter 19.5-27.5 (23.4, 9).
Groove situated at one-third of body length from peristome. Scapula small 10.7-
14.7 (12.1,9) in diameter. Food vacuoles distributed in region above groove.
Macronucleus elongated, triangular, situated below groove, length 20.3-33.5
Chapter 4 - The Ciliophora 64
(25.4, 9), diameter 12.4-19.1 (14.4, 9). Micronucleus oval-shaped, situated
alongside micronucleus, length 2.2-3.4 (3.1, 1), diameter 1.5-2 (1.7, 2).
Remarks:
Individuals were often observed in clusters on the fish host, which has a colonial
appearance. Apiosoma sp. A most closely resembles A. piscicola based on the
shape of the macronucleus, as well as morphometrical data from Viljoen & Van
As (1985). Due to the unavailability of observations from live specimens, specific
identification is not possible.
Apiosoma sp, B
Hosts and locality: Pseudocrenilabrus philander and Cyprinus carpio, Soetdoring
Nature Reserve, South Africa (280 52' S, 260 0' E).
Infection Site: Gills.
Specimens studied: Morphometric measurements and drawings were made
using light microscopy. Reference material (2001/03/21-27, V2001/11/22-08)
deposited in the collection of the Aquatic Parasitology Study group, University of
the Free State.
Description:
Body cylindricl (Figure 4.7B1 & B2, Figure 4.10B), length 32.9-49.7 (39.4, 9),
diameter 17.4-28.3 (23.6, 9). Groove centrally placed. Scapula broad, diameter
12.5-22.0 (17.7, 7). Food vacuoles distributed in region above groove.
Macronucleus round to oval, situated below groove, length 10.6-19.5 (13.8, 9),
diameter 11.5-19.8 (15.4, 9). Micronucleus not observed.
Remarks:
Specimens have a short and stout appearance, and most closely resemble A.
epibranchialis, on overall dimensions as reported by Viljoen & Van As (1985).
Specific identification is, however, not possible as observations from live
specimenswere not available.
Chapter 4 - The Ciliophora 65
Tttcnodtn« sp. A
Host and locality: Pseudocrenilabrus philander, Soetdoring Nature Reserve,
South Africa (280 52' S, 260 0' E).
Infection Site: Gills.
Specimens studied: Morphometric measurements and drawings were made
using light microscopy. Reference material (2001/03/22-13, 2001/03/22-45,
2001/03/22-46, 2001/03/22-50) deposited in the collection of the Aquatic
Parasitology Study group, University of the Free State.
Description:
Diameter of body 41.6-52.0 (49.5,7), adhesive disc cup-shaped, 33.9-43.5 (37.9,
7) in diameter, surrounded by finely striated border membrane, 3.7-5.2 (4.2, 7)
wide (Figure 4.1OC). Distinctive ridges present in the center of the adhesive disc.
Diameter of denticle ring 22.0-28.9 (24.2, 7). Number of denticles 23-26 (25).
Length of denticle 3.7-4.4 (4.0, 7): length of ray 3.4-6.3 (4.6, 7): width of central
part 1.8-3.3 (2.3, 7): length of blade 5.0-6.3 (5.7, 7). Distal surface of blade
slightly rounded, sloping in anterior direction, not parallel to border membrane
(Figure 4.8A). Tangent point slightly lower than distal surface. Anterior margin
varies, in some cases angular, in others curved. Anterior surface extends to y+1
line, extending past y line in some cases. Blade apophysis more prominent in
some cases than in others. Posterior margin forms L- shaped curve, which
corresponds to apex of anterior surface. Part connecting blade to central part
thinner than blade. Central part extends towards and in some cases beyond y-1
axis, but not more than halfway. Rays straight and extends anteriorly toward the
y-axes, tapering to rounded point. Centre ridges varies in thickness and length,
thicker than rays.
Remarks:
Based on the above description and morphometrical data, Trichodina sp. A can
be identified as Trichodina centrostrigeata.
Chapter 4 - The Ciliophora 66
The material collected from the Soetdoring Nature Reserve corresponds very
closely in morphometrical data to the type population described by Basson et al
(1983). It is also very similar to another population described by Van As &
Basson (1992) from the Zambesi River. Trichodina centrostrigeata can easily be
distinguished from other species based on the presence of centre ridges, as well
as denticle morphology and overall dimensions.
Trichodina SIP. B
Host and locality: Labeo umbratus and Cyprinus carpio, Soetdoring Nature
Reserve, South Africa (280 52' S, 2600' E)
Infection Site: Gills
Specimens studied: Morphometric measurements and drawings were made
using light microscopy. Reference material (2001/03/21-15, 2001/03/21-30)
deposited in the collection of the Aquatic Parasitology Study group, University of
the Free State.
Description:
Diameter of disc-shaped body 55.0-59.3 (57.1, 2), adhesive disc concave, 45.3-
47.3 (46.3, 2) in diameter, surrounded by finely striated border membrane, 4.9-
5.3 (5.1, 2) wide (Figure 4.100). Diameter of denticle ring 28.7-29.6 (29.1, 2).
Number of denticles 23-24. Length of denticle 7.18-7.20 (7.19, 2): length of ray
6.0- 6.5 (6.2, 2): width of central part 3.4-3.7 (3.5, 2): length of blade 3.8-4.2 (4.0,
2). Blade broad, with distal margin curved (Figure 4.8B). Tangent point higher
than distal surface. Posterior margin forms indentation, semi-lunar in shape.
Anterior margin rounded, with apex slightly protruding, reaching y+1 axis.
Connecting part between central part and blade broad, with central part
extending more than halfway past y-axis, in some cases completely. Point of
central part rounded, and closely associated with following denticle. Connecting
part between central part and ray similar in thickness to connecting part between
central part and blade, with apophysis of ray present, but not always prominent.
Chapter 4 - The Ciliophora 67
Ray thick and varies in length, tapering to blunt point. Ray directed to center
point, almost parallel to y+1 axis.
Remarks:
Based on the above description and overall body dimensions, Trichodina sp. B
can be identified as T. heterodentata.
Trichodina sp. B resembles T. magna, but the difference between these species
can be seen in the body size of T. magna, which is much larger, and the shape of
the denticle. The present population corresponds closely to the population
described by Basson et al (1983) in morphometrical data as well as denticle
shape and dimensions.
'ïrtcnoom« sp, C
Host and locality: Labeo capensis and Cyprinus carpio, Soetdoring Nature
Reserve, South Africa (280 52' S, 260 0' E)
Infection Site: Gills
Specimens studied: Morphometric measurements and drawings were made
using light microscopy. Reference material (2001/03/21-30, 2001/03/21, 42,
2001/03/22-44) deposited in the collection of the Aquatic Parasitology Study
group, University of the Free State.
Description:
Large trichodinid with disc-shaped body 51.2-72.3 (57.6,5) in diameter. Adhesive
disc concave, 38.7-59.3 (46.0, 5) in diameter, and surrounded by finely striated
border membrane 4.7-6.3 (5.8,5) wide (Figure 4.10E). Diameter of denticle ring
23.8-39.5 (28.9,5). Number of denticles 21-25 (21). Length of denticle 5.7-8.9
(7.1, 5): length of ray 5.6-9.9 (6.8, 5): width of central part 1.9-2.4 (2.1, 5): length
of blade 5.2-7.4 (6.2, 5). Blade broad, with distal margin parallel to border
membrane. Anterior side of distal surface rounded (Figure 4.9A). Tangent point
Chapter 4 - The Ciliophora 68
slightly lower than distal surface. Posterior margin almost straight up to two
thirds of blade length, forming curve into central part. Deepest point where curve
begins. Apex of anterior margin rounded. Anterior apophysis of blade not
present. Posterior projection of blade absent. Connection between central part
and blade thin. Central part delicate and extending more than halfway past y+1
axis. Central part above and below x-axis similar in shape. Rays almost parallel
to y-axes, in some cases directed anteriorly, sometimes reaching and extending
past y-axes. Rays of same thickness throughout, without apophysis.
Remarks:
Based on the above description and overall body dimensions, Trichodina sp. C
can be positively identified as T. mutabilis.
Trichodina sp. C resembles T. uniforma and T. kazubski, which were previously
mistaken for T. mutabilis by Basson et al (1983). The shape of the blade and
central part of T. uniforma, however, differs significantly. In T. mutabilis, the apex
of the anterior margin is not as prominent as in T. uniforma and the curve of the
posterior margin also differs. The overall body dimensions of T. kazubski is
smaller than that of T. mutabilis, and the rays are short and straight, as opposed
to the anteriorly directed rays of T. mutabilis. The population of T. mutabilis from
Soetdoring Nature Reserve is the first record of this species from a fish host in
the wild in South Africa. A population of T. mutabilis was found on ornamental
fish in South Africa that were originally introduced from the Far East (Basson,
pers. camm.). It is also the first record of this species from an indigenous host
species.
Chapter 4 - The Ciliophora 69
Tripartiella sp, A
Host and locality: Labeo capensis and L. umbratus, Soetdoring Nature Reserve,
South Africa (280 52' S, 2600' E)
Infection Site: Gills
Specimens studied: Morphometric measurements and drawings were made
using light microscopy. Reference material (2001/03/21-05, 2001/03/21-42)
deposited in the collection of the Aquatic Parasitology Study group, University of
the Free State.
Description:
Small trichodinid with bell-shaped body 19.3-24.4 (21.1, 3) in diameter, adhesive
disc concave, 14.4-19.8 (17.1, 3) in diameter, surrounded by finely striated
border membrane, 2.3-2.8 (2.5, 2) wide. Diameter of denticle ring 8.0-8.2 (8.1,
2). Number of denticles 24-25 (24). Length of denticle 2.0-3.0 (2.5, 2): length of
ray 1.0-1.1 (1.0, 2): width of central part 0.88-0.91 (0.9, 2): length of blade 3.8-4.1
(3.9,2). Blade slender, with distal margin parallel to border membrane. Anterior
side of distal surface rounded (Figure 4.9B). Tangent point slightly lower than
distal surface. Lateral sides of blade almost parallel. Anterior margin constricts,
forms pronounced apophysis, which extends more than halfway past y+1 axis.
Posterior projection of blade absent, with posterior margin constricting. Part of
blade connecting to anterior apophysis very thin. Connection between blade and
central part thin and delicate. Central part small with rounded point and part
above x axis similar to the part below x axis. Central part extends almost
completely past y-1 axis. Rays short and thin, tapering to sharp tip, almost
parallel to y axes, extending beyond line in some cases.
Remarks:
Based on the above description and morphometrical data, Tripartiella sp. A can
be identified as T. lechridens.
Chapter 4 - The Ciliophora 70
Tripartiella lechridens shows some similarity to three species of the genus
(Basson & Van As 1987), i.e. T. bulbosa (Davis, 1947), T. bursiformes (Davis,
1947) and T. lechridens. Tripartiella bulbosa and T. bursiformes, however, have
a larger diameter of the adhesive disc than T. lechridens. The constriction of the
blade in T. lechridens is a unique characteristic, which can be used to identify
Tripartiella sp. A as T. lechridens. Morphometrical data from the present
population is well within range with those given by Basson & Van As (1987) for T.
lechridens.
Tripartiella sp, B
Host and locality: Labeo capensis, Soetdoring Nature Reserve, South Africa (280
52' S, 260 0' E).
Infection Site: Gills.
Specimens studied: Morphometric measurements were made using light
microscopy. Reference material (2001/03/21-43) deposited in the collection of
the Aquatic Parasitology Study group, University of the Free State.
A single specimen was recorded, which was in the process of fission. This
specimen is provisionally identified as Tripartiella leptospina. A comparative
description could thus not be given, but some morphometrical data is given.
Diameter of body 16.2, diameter of adhesive disc 13.5, width of border
membrane 1.4, diameter of denticle ring, 7.4, number of denticles 20, length of
denticle 3.7, length of ray 1.0, width of central part 0.4 and length of blade 2.8.
Chapter 4 - The Ciliophora 71
Remarks:
The single specimen collected in this study, showed some remnants of an old
denticle ring, indicating that it was in the process of division. During binary
fission, the denticle shape of the newly formed ring on the outside are normally
slightly different from that of the adult individual. However, it was provisionally
identified as TriparlielIa leptospina (Basson, pers comm.).
Trtcnoainett« SIP. A
Hosts and locality: Cyprinus carpio, Labeo capensis and L. umbratus, Soetdoring
Nature Reserve, South Africa (280 52' S, 260 0' E).
Infection Site: Gills.
Specimens studied: Morphometric measurements and drawings were made
using light microscopy. Reference material (2001/03/21-01, 2001/03/21-02,
2001/03/21-03, 2001/03/21-29, 2001/03/21-41, 2001/03/21-42, 2001/03/21-43)
deposited in the collection of the Aquatic Parasitology Study group, University of
the Free State.
Description:
Diameter of body 19.0-22.5 (21.2, 7), adhesive disc cup-shaped, 15.4-20.0 (17.4,
7) in diameter, surrounded by finely striated border membrane, 1.7-2.4 (2.1, 7)
wide (Figure 4.10E). Diameter of denticle ring 7.4-9.5 (8.3, 5). Number of
denticles 19-21 (19). Length of denticle 1.1-2.0 (1.6, 7): width of central part 1.2-
1.8 (1.4, 6): length of blade 3.4-4.1 (3.7, 6). Blade short and slender, with lateral
margins almost parallel. Distal margin parallel to border membrane (Figure
4.9C). Tangent point at same level as distal surface. Anterior margin gently
curves into well-developed apophysis extending more than halfway past y+1
axis. Posterior margin forms indentation that corresponds with anterior
apophysis. Part connecting central part to blade varies, delicate in some cases,
broad in others. Central part well developed. Although ray is absent, a small
triangular protrusion is visible in some cases.
Chapter 4 - The Ciliophora 72
Remarks:
Based on the above description and morphometrical data, Trichodinella sp. A
can be identified as T. epizootica.
Trichodinella crennulata and T. epizootica are the only two species of the genus
known from South Africa. Trichodinella crennulata differs from T. epizootica in
the shape of the blade; the projections, as well as the central part complex.
Based on these characteristics, as well as morphometrical data, Trichodinella sp.
A is identified as T. epizootica The morphometrical data of the population from
Soetdoring Nature Reserve corresponds well with that reported by Basson & Van
As (1987).
A1 A2
82
Figure. 4.7. Microscope projection drawings of Apiosoma species from the fishes of the Soetdoring Nature
Reserve. A - Apiosoma sp. A. from the skin of Pseudocreni/abrus philander (Weber, 1897) and Ti/apia
spaffmanii Smith, 1840. B - Apiosoma sp. B from the gills of P. philander and Cyprinus carpio Linnaeus,
1758. Scale bar: 10jJm
A
Figure. 4.8. Microscope projection drawings of the denticles of trichodinids from fishes of the Soetdoring
Nature Reserve. A - Trichodina centrostrigeata Basson, Van As & Paperna, 1983 from the gills of
Pseudocrenilabrus philander (Weber, 1897). B - T. heterodentata Duncan, 1977 from the gills of Labeo
capensis (Smith, 1841) and Cyprinus carpio Linnaeus, 1758. Scale bar: 10j..lm
A
IB c
Figure. 4.9. Microscope projection drawings of the denticles of trichodinids from the fish of the Soetdoring
Nature Reserve. A - Trichodina mufabilis Kazubski & Migala, 1968 from the gills of Cyprinus carpio
Linnaeus, 1758 and Labeo capensis (Smith, 1841). B - Tripartiella lechridens Basson & Van As, 1987
from the gills of L. umbrafus (Smith, 1841). C - Trichodinella epizoofica (Raabe, 1950) from the gills of L.
capensis, L. umbrafus and C. carpio. Scale bar: 10IJm
Figure. 4.10. Light micrographs of ciliophorans collected from the fishes from the Soetdoring Nature
Reserve. A - Apiosoma sp. A, B - Apiosoma sp. B, C - Trichodina centrostrigeata Basson, Van As &
Paperna, 1983, 0 - T. heterodentata Duncan, 1977, E - T. mutabulis Kazubski & Migala, 1968, F -
Trichodinella epizootica (Raabe, 1950). Scale bar: 10IJm

Chapter 5 - The Monogenea 77
TIhl® (C~talS$ MOIJ1)Og]®ll1Heal (Van Beneden, 1858)
Monogeneans are a group of hermaphroditic flatworms parasitising mostly
aquatic vertebrates, and are most often associated with the gill chamber, skin or
other organs that are in direct contact with the external environment (Yamaguti
1963a; Euzet & Combes 1998). They occasionally also occur on aquatic
invertebrates. Monogeneans are very specific to the site of attachment, and in
some cases there is also specificity to certain microhabitats within an attachment
site (Euzet & Combes 1988).
The life-cycle of monogeneans is usually very simple, involving an egg,
oncomiracidium and the adult. Members of the Gyrodactylidae Cobbold, 1864
however, are viviparous. Generally, the life span of monogeneans can vary from
a few days to several years.
Several authors have contributed to the systematics of the Monogenea, which
has been emended in several publications since the separation of the
monogeneans from other trematodes. A summary of the landmarks in the
systematics is presented below.
o Van Beneden (1858) separated the Trematoda into two groups, namely the
monogénéses and digénéses.
o Carus (1863) changed the French suffix to a latinised one, referring to the
group as Monogenea. As this change is merely a minor orthographic change,
authorship should still be attributed to Van Beneden (1858).
c Odhner (1912) divided the monogeneans into two groups, namely the
Monopisthocotylea Odhner, 1912 and the Polyopisthocotylea Odhner, 1912,
based on the presence or absence of a genito-intestinal tract.
e Byehowsky (1937) elevated the Monogenea from the rank of order, to that of
class, based on the opisthaptor of the monogeneans, and the cercomer in the
Chapter 5 - The Monogenea 78
ontogeny of the cestodes, amphillinideans, and gyrocotylideans. With this
elevation, the name was changed to Monogenoidea, but Bychowsky still
credited authorship to Van Beneden. Other authors, including Price (1937)
objected to this, and accredited authorship to Caruso Some authors adopted
the use of Monogenoidea as proposed by Bychowsky, while others still
referred to it as the Monogenea.
~ The system of classification by Byckowsky (1937), led to the division of the
class into two subclasses, the Polyonchoinea (Bychowsky, 1937), and the
Oligonchoinea (Bychowsky, 1937).
e Lebedev (1988) put forward a classification system, which included a
subclass, the Polystomatoinea (Lebedev, 1986), which was previously either
placed amongst the higher Monogenea (Oligonchoinea) or the lower
Monogenea (Polyonchoinea). Orders were also introduced within the
monogenea for the first time.
~ Malmberg (1990) proposed a classification scheme based on the ontogeny of
the opisthaptor. This suggested a progressive evolution amongst the
monogeneans, resulting in an increase in the number of marginal hooks
during evolution. This is contrary to the theories of Bychowsky, Lebedevand
Euzet who support the theory of regressive evolution.
e Justine (1991) performed cladistic studies based on spermatozoan structure
and spermiogenesis of monogeneans, and found similarities in the
phylogenetic relationships with the classification of Lebedev (1988).
~ Boeger & Kritsky (1993) proposed a classification system based on the
phylogenies within the group, after subjecting the monogenean families to
cladistic analysis using a variety of anatomical and ultrastructural characters.
~ Lebedev (1995) proposed a classification system, which was similar to that of
Boeger & Kritsky (1993), and an emended version of the Lebedev (1988)
system.
c Due to molecular studies suggesting the Monogeneans to be non-
monophyletic, Justine (1998) concluded that a reappraisal of morphological
Chapter 5 - The Monogenea 79
synapomorphies should be undertaken, and that monophyly of the
Monogenea be tested on this basis.
~ Boeger & Kritsky (1997) put forward a revised hypothesis of monogenean
phylogeny based on new structural and anatomical data.
~ Mollaret, Jamieson & Justine (2000) concluded the Monogenea to be
paraphyletic, based on analyses of 28srDNA sequences. They also found
both the groups Monopisthocotylea, and Polyopisthocotylea to be
monophyletic.
c Boeger & Kritsky (2001) presented an emended version of the hypothesis of
Boeger & Kritsky (1997) for the relationships of family groups of the
monogeneans. In this classification, two subclasses were suggested, namely
the Polyonchoinea and the Heteronchoinea Boeger & Kritsky, 2001, with the
Polystomatoinea and the Oligonchoinea included as infrasubclasses of the
Heteronchoinea.
~ Olson & Littlewood (2002) perform further molecular analysis, and came to
the conclusion that the Monogenea is indeed monophyletic. This confirms the
classification of Boeger & Kritsky (2001 ).
Controversy still exists as to how the class should be referred to, i.e.
Monogenoidea or Monogenea, and many authors still debate which of the names
are most acceptable. For the remainder of this dissertation, the classification of
Boeger & Kritsky (2001) (Table 5.1) will be used, as it provides the most recent
classification based on the phylogeny of the group. In accordance with the
Round Table discussion of ICOPA IV, 1978 in Warsaw (Wheeler & Chisholm,
1995), this group will be referred to as the Monogenea (Van Beneden, 1858).
Chapter 5 - The Monogenea 80
SUPER
FAMILY
Gyrodactylidea
Dactylogyridea Tetraonchinea
Dactylogyrinea
Mazocraeinea
Protomicrocotyloidea
Gastrocoltylinea Gastrocotylina
Oligonchoinea
(Bychowsky, Gastrocotyloidea
1937)
Mazocraeidea
Discocotylinea
Microcotyloidea
Microcotylinea
Pyragraphoroidea
Chapter 5 - The Monogenea 81
Branchlat monoqeneans from Afrocan fishes
Monogeneans of the genera Dacfylogyrus Diesing, 1850 and Paradiplozoon
occur on the gills of a wide range of African fishes. In this chapter the
dactylogyridean and diplozoid species occurring on the fishes from Africa will be
discussed.
Dactyloqyrldean monogeneans
According to Yamaguti (1963a), the family Dactylogyridae belongs to the
superfamily Dactylogyroidea Yamaguti, 1963, and includes species in which
there are two or more head organs present. The lobes of the head mayor may
not be developed. Structures of the haptor include either one or two pairs of
anchors, and there are usually 14 marginal hooklets present. All of the species
discussed in this chapter are included either in the subfamily Dactylogyrinae
Bychowsky 1933, or the Ancyrocephalinae Bychowsky, 1935. The
Dactylogyrinae includes all those species with only one pair of anchors present,
while the Ancyrocephalinae includes those that possess two pairs of anchors and
in which the seminal receptacle is associated with the vagina (Yamaguti 1963a).
(Gell1HllIS Daciylogyrus Diesing, 1850
Generic Diagnosis
The genus Dacfylogyrus according to the amended description by Price (1967)
belongs to the subfamily Dactylogyrinae of the family Dactylogyridae. The haptor
is armed with a single pair of anchors, which are supported by a haptoral bar. A
ventral bar mayor may not be present. The marginal hooklets are usually of the
same shape, and subequal in size. Four eye-spots are present.
The copulatory complex is composed of a tubular cirrus, which is usually basally
articulated to the accessory piece. A vagina may be present or absent, and the
position of the vagina is variable. The vas deferens is usually looped around the
Chapter 5 - The Monogenea 82
intestinal limb, and the seminal vesicle is a simple dilation of the vas deferens.
One or two prostatie reservoirs may be present.
Dactylogyrus Diesing, 1850 species of African cyprlnlds
In Africa there are currently 92 known species belonging to the genus
Dactylogyrus, which are parasites of cyprinid fishes. According to Paperna
(1979a), the genus can be divided into three species groups. These groups
share some common morphological characters, but still differ morphologically
from each other to be ranked as different species (Paperna 1979a). Two of
these groups, namely the Dactylogyrus pseudoanchoratus Price & Géry, 1968
group, and the D. afrobarbae Paperna, 1968 group are known only from African
cyprinids fishes. The third species group, D. varicorhini Bychowsky, 1957, is
common to cyprinid fish from both Africa and Asia.
species recorded from Lalbeo Cuvier, 1817 hosts
In Africa, there are currently 24 species of Dactylogyrus that have been
described from Labeo species (Table 5.2), or recorded from species of Labeo by
other authors.
The first of these species was described in 1968, when Paperna described
Dactylogyrus afrobarbae Paperna, 1968 from Barbus sublineatus Daget, 1954
from Ghana. One year later however, Paperna recorded the same species from
Labeo coubie Ruppel, 1832, also in Ghana. Paperna (1969) described three
other species from Ghana, namely D. digitalis Paperna, 1969, D. labeous
Paperna, 1969 and D. senegalensis Paperna, 1969. All three species were
collected from L. coubie. Price, Korach & McPott (1969a) also, described D.
pienaari Price, Korach & McPott, 1969 from L. rosae Steindachner 1894, which is
to date the only species described from a Labeo species from South Africa.
Four years later, in 1973, Paperna described a number of new species from
research done in Africa. Of these species, four were described from Labeo
Chapter 5 - The Monogenea 83
species, namely D. braehydiseus Paperna, 1973, and D. /ongiphallus Paperna,
1973 from L. vietorianus Boulenger, 1901, both from Kenya. Daety/ogyrus
eye/acirrus Paperna, 1973 was found on L. eoubie, from Ghana and D.
he/ieophallus, from Labeo forska/ii Ruppel, 1836 collected from Uganda.
A fifth species was also collected from Kenya, namely D. brevieirrus Paperna,
1973 and was found on Barbus a/tiana/is Boulenger, 1900. Paperna also
recorded this species from Labeo vietorianus in 1973. Daety/ogyrus brevieirrus
was also recorded from other Labeo hosts, namely L. eylindrieus and L. forska/ii
by Paperna (1979a) from Tanzania and Uganda, respectively. Other authors
also reported it from Labeo species, namely L. parvus Boulenger, 1902,
(Guegan, Lambert & Euzet 1988) from Mali and again from L. parvus Boulenger,
1902 (Guegan & Lambert 1991), from West Africa.
Paperna (1979a) described a subspecies of D. pseudoanehoratus Price & Gery,
1968 from a Labeo host, namely D. p. miehronehus Paperna, 1979 from
Tanzania.
Guegan et al. (1988) described a number of species from Labeo hosts, all from
research done in Mali. These species included D. decaspirus Guegan, Lambert,
Euzet, 1988, D. fa/ei/oeus Guegan, Lambert & Euzet, 1988, D. jaeu/us Guegan,
Lambert, Euzet, 1988, D. titus Guegan, Lambert & Euzet 1988, and D.
retroversus Guegan, Lambert, Euzet 1988, all from L. eoubie. They also
described D. rastellus Guegan, Lambert & Euzet, 1988 and D. tubarius Guegan,
Lambert & Euzet, 1988 from L. senega/ensis Valenciennes, 1842, and D.
natha/iae Guegan, Lambert & Euzet, 1988 from a Labeo host.
Guegan & Lambert recorded D. fa/ei/oeus again from Mali in 1990 and in 1991
from Mali and West Africa respectively. These records were from Labeo eoubie,
L. parvus and L. wurtzi (not in CLOFFA)1.
1 Check-List of the Freshwater Fishes of Africa.
Chapter 5 - The Monogenea 84
Guegan & Lambert (1991) described four more species from Labeo hosts.
These were D. gucundus Guegan & Lambert, 1991, from L. parvus in West
Africa, D. longiphalloides Guegan & Lambert, 1991 from L. allauadi Pellegrin,
1933 from Sierra Leone, and two species from L. rouaneti Daget, 1962, namely
D. sematus Guegan & Lambert, 1991, and D. omega Guegan & Lambert, 1991,
collected in Guinea.
A comparison of the measurements of the species recorded from Labeo hosts is
given in Table 5.3. Where available the measurements were used from the
original descriptions or from redescriptions by other authors. In other cases
measurements were made from available drawings.
Chapter 5 - The Monogenea 85
L. victorian us Boule 1901
brevicirrus L. cylindricus Peters, 1968, L. forskalii Kenya, Uganda,
perna, 1973 (Figure 5.1 F-H) Ri.ippel 1836, L. parvus Boulenger, Tanzania, West Africa
1902 and L. victorianus and Mali
cyc/ocirrus L. coubie, L. cylindricus and Ghana, Tanzania,
aperna, 1973 (Figure 5.2A-C) L. senegalensis Valienciennes, 1842 West Africa, and
L. coubie Mali and Ghana
Ghana and Mali
Mali
L. forskalii anda
L. coubie Mali Ghana
West Africa and
1962 Guinea
Ghana
Sierra Leone
L. victorianus and L. anda
Labeo Mali
L. coubie Ghana
Guinea
L. rosae Steindachner 1894 South Africa
Labeo Tanzania
Mali
L. coubie Mali
L. rouaneti Guinea
Ghana
L. coubie Mali
Mali
Chapter 5 - The Monogenea 86
0 0 45 26 22 16 33 2 135 42
200-220 110-130 28-29 18 13 9 25 0 20-21 6-8
230-380 40-100 35-40 20-24 1-4 16-20 10-14 19-21 0 25-30 15-21
420-460 110-140 27-29 11-12 14 7-9 26-28 0 58-60 0
250-350 60-80 45-50 32-35 3-5 21-25 17-19 21-29 4-5 250-300 8-10
480-850 100-200 31-38 27-35 3-8 5? 12-18 28-34 4-6 70 40-47
280-470 40-80 30-40 23-27 1-2 12-19 11-16 24-28 3-5 17-23 17-25
180-200 40 33-35 20-22 2 15 14-19 16 0 72-82 20-25
240-350 40-70 25-35 21-24 1-2 12-16 8-12 14-17 3-4 15-20 24-28
250-630 40-120 47-55 26-33 3-6 22-29 17-18 22-26 0 40-47 26-30
230-400 40-80 38-43 29-31 3-4 16-21 12-17 20-23 4-5 33-39 30
250-360 40-80 40-45 24-28 1-3 19-21 12-14 17-20 3-5 40-46 40-46
190-240 50-80 34-41 20-24 1-4 16-22 11-17 15-24 45-63 32-40
400-700 80-130 26-30 24-28 5-7 10-13 10-13 22-26 3-5 60-70 22-30
220-480 50-80 33-40 24-27 2-4 14-20 11-17 18-22 3-4 60-65 0
360-830 70-120 32-36 26-30 3-6 10-14 13-15 24-28 4-6 0 35-42
197-244 79~129 26-32 24 2 9 12 17-22 4 70-80 12-16
60-100 31-34 22-25 2-4 12-13 9-12 25-26 0 28-38 14-17
Chapter 5 - The Monogenea 87
230-470 40-80 42-48 31-35 2-4 15-19 16-18 17-21 20-27
230-400 40-80 40-48 26-31 2-3 18-22 17-19 21-26 2-4 30-35 o
220-670 40-110 39-43 23-27 3-5 18-21 13-15 19-23 3-5 35-42 0
200-500 50-80 29-33 24-28 1-4 8-13 11-14 17-21 3-4 180 o
200-390 40-90 35-40 23-37 1-3 13-18 12-15 17-22 3-4 18-20 14-18
180-380 40-80 39-44 26-30 3-4 17-22 14-19 22-25 3-4 0 o
A B
=
o
c
lE
G
IF
Figure. 5.1. Diagrammatic drawings of Dactylogyrus Diesing, 1850 species. A, B - Dactylogyrus
afrobarbae Paperna, 1968 (redrawn from Paperna 1968). A - anchors and dorsal bar, B - cirrus. C-E-
D. brachydiscus Paperna, 1973 (redrawn from Paperna 1979). C - anchors and dorsal bar, ID- marginal
hooklets. E - cirrus. F-H - D. brevtclrrus Paperna, 1973 (redrawn from Guegan, Lambert & Euzet 1988).
F - anchors and dorsal bars, G - marginal hooklets, H - cirrus. Scale bar: 20j..lm
B
A
c
E
ID
F
G
Figure. 5.2. Diagrammatic drawings of Dactylogyrus Diesing, 1850 species. A-C - Dactylogyrus
cyclocirrus Paperna, 1973 (redrawn from Guegan, Lambert & Euzet 1988). A - anchors and dorsal bars,
B - marginal hooklets, C - cirrus. D-IF - D. decaspirus Guegan, Lambert & Euzet, 1988 (redrawn from
Guegan, Lambert & Euzet 1988). 0 - anchors and dorsal bars, E - marginal hooklets, F - cirrus. G-I- D.
digitalis Papema, 1969 (redrawn from Guegan, Lambert & Euzet 1988). G - anchors and dorsal bar, H -
marginal hooklets, I - cirrus. Scale bar: 20IJm
B 111 111)
A
c ~
D
= IF
G
J
Figure. 5.3. Diagrammatic drawings of Daety/ogyrus Diesing, 1850 species. A-C - Daety/ogyrus
fa/ei/oeus Guegan, Lambert & Euzet, 1988 (redrawn from Guegan, Lambert & Euzet 1988). A - anchors
and dorsal bar, B - marginal hooklets, C - cirrus. D-F - D. helieophallus Paperna, 1974 (redrawn from
Paperna 1979). D - anchors and dorsal bar, E - marginal hooklets, F - cirrus. G-I - D. jaeu/us Guegan,
Lambert & Euzet, 1988 (redrawn from Guegan, Lambert & Euzet 1988). G - anchors and dorsal bars, H-
marginal hooklets, I - cirrus. J-l - D. jueundus Guegan & Lambert, 1991 (redrawn from Guegan &
Lambert 1991). J - anchors and dorsal bars, K - marginal hooklets, L - cirrus. Scale bar: 20IJm
A
c
D
f
G
Figure. 5.4. Diagrammatic drawings of Dactylogyrus Diesing, 1850 species. A-C - Dactylogyrus labeous
Paperna, 1969 (redrawn from Guegan, Lambert & Euzet 1988). A - anchors and dorsal bars, B -
marginal hooklets, C - cirrus. D-F - D. longiphalloides Guegan & Lambert, 1991 (redrawn from Guegan &
Lambert 1991). 0 - anchors and dorsal bars, E - marginal hooklets, F - cirrus. G-I - D. longiphallus
Paperna, 1973 (redrawn from Papema 1979). G - anchors and dorsal bar, H - marginal hooklets. I -
cirrus. Scale bar: 20j.Jm
d B ltljil~
A
c
E
ID
F
G
IK
J
l
Figure. 5.5. Diagrammatic drawings of Dactylogyrus Diesing, 1850 species. A-C - Dactylogyrus
nathaliae Guegan, Lambert & Euzet, 1988 (redrawn from Guegan, Lambert & Euzet 1988). A - anchors
and dorsal bars, B - marginal hooklets, C - cirrus. D-F - D. oligospirophallus Papena, 1973 (redrawn
from Paperna 1979). D - anchors and dorsal bars, E - marginal hooklets, F - cirrus. G-I - D. omega
Guegan & Lambert, 1991 (redrawn from Guegan & Lambert 1991). G - anchors and transvers bars, H -
marginal hooklets, I - cirrus. J-L - D. pienaari Price, Korach & McPott, 1969 (redrawn from Price, Korach
& McPott 1969). J - anchors and dorsal bar, K - marginal hooklets, l- cirrus. Scale bar: 20j.lm
B )~!
A
C
~
E ill J ~ It
F
D
~
li)! tl ~
G 1(
J l
Figure. 5.6. Diagrammatic drawings of Dactylogyrus Diesing, 1850 species. A-C - Dactylogyrus
pseudoanchoratus micron chus Paperna, 1979 (redrawn from Paperna 1979). A - anchors and dorsal bar,
B - marginal hooklets, C - cirrus. D-F - D. rastel/us Guegan, Lambert & Euzet, 1988 (redrawn from
Guegan, Lambert & Euzet 1988). 0 - anhors and dorsal bar, E - marginal hooklets, F - cirrus. G-I - D.
retroversus Guegan, Lambert & Euzet, 1988 (redrawn from Guegan, Lambert & Euzet 1988). G - anchors
and dorsal bar, H - marginal hooklets, I - cirrus. J-L - D. sematus Guegan & Lambert, 1991 (redrawn
from Guegan & Lambert 1991). J - anchors and dorsal bars, K - marginal hooklets, L - cirrus. Scale bar:
20f.Jm
B
A
c
E
D
f
G
IJ
Figure. 5.7. Diagrammatic drawings of Dactylogyrus Diesing, 1850 species. A-C - Dactylogyrus
senegalensis Paperna, 1969 (redrawn from Guegan, Lambert & Euzet 1988). A - anchors and dorsal bar,
B - marginal hooklets. C - cirrus. D-F - D. titus Guegan, Lambert & Euzet, 1988 (redrawn from Guegan,
Lambert & Euzet 1988). [) - anchors and dorsal bar, lE - marginal hooklets, F - cirrus. G-I - D. tubarius
Guegan, Lambert & Euzet, 1988 (redrawn from Guegan, Lambert & Euzet 1988). G - anchors and
transvers bars, H - marginal hooklets, I - cirrus. Scale bar: 20jJm
Chapter 5 - The Monogenea 95
Dactylogyrus species known from South African hosts, other
than Lebeo Cuvier, 1817species
Twelve species of Dactylogyrus have been recorded from South Africa (see
Table 5.4). Of these species, D. pienaari (mentioned above) has been described
from a Labeo host. The remaining eleven species is known from other cyprinid
hosts.
Two of the species that were described from South Africa were described in
1969, namely D. jubbstrema Price, Korach & McPott 1969 from Glossogobius
giuris Hamilton, 1822, and D. myersi Price, McClellan, Druckenmiller & Jacobs
1969 from Barbus trimaculatus (Price et al, 1969a; Price et ai, 1969b). The other
three were described by Mashego in 1983, two from Barbus palidinosus, namely
D. teresae Mashego, 1983 and D. dominici Mashego, 1983, and one from
Barbus neefi Greenwood, 1962, namely D. enidae Mashego, 1983.
Price et al. (1969b) recorded D. varicorhini Bychowsky, 1957 from Labeobarbus
kimberleyensis. This species was originally described by Bychowsky (1957),
from Varicorhinus capoeta (Guldenstadt, 1772) from the Vazrob River, near
Stalinabad. Price et al. (1969b) did not give a description or measurements and
according to Paperna (1979a) this might well be another species because of the
morphological similarities in the specific species group.
The remaining species that were recorded from South Africa are all species that
were originally described from Uganda from Barbus and Labeobarbus hosts.
They were recorded again from South Africa in 1983 by Mashego. These
include, D. allolongionchus Paperna, 1973, D. afrosclerovaginus Paperna 1973,
D. afrolongicomis afrolongicomis Paperna, 1973, D. a. alberti Paperna 1973, all
from B. trimaculatus, as well as a species described by Paperna and Thurston
(1968b), namely D. spinicirrus Paperna & Thurston (1968b), from L. marequensis
(Smith, 1841).
Chapter 5 - The Monogenea 96
Barbus trimaculatus 1852
B. trimaculatus
B. 1852
B. trimaculatus
1962
Hamilton 1822
B. trimaculatus
Labeobarbus marequensis (Smith,
1841
B.
A comparison of the measurements of the species recorded from other cyprinid
hosts from South Africa is given in Table 5.5.
Chapter 5 - The Monogenea 97
280 100 35-36 20-22 5 17 12-17 51-63 2 42 32
230-310 50-100 38-43 22-28 1-5 17-23 12-17 51-63 5-10 25-30 20-26
130-400 45-100 36-41 27-32 2-4 13-16 7-12 38-40 2-4 22-30 16-32
200-310 80-160 0 42-54 3-6 11-19 16-20 36-51 3-7 22-25 17-22
218-419 31-75 58-80 40-54 2 23 40-54 43-58 4-5 25-45 15-19
171-281 31-38 68-81 50-56 3-9 21-31 19 31-43 4-6 21-25 19
190-226 50-60 32-38 18 3 18 15 15-18 4 21-25 14-17
363-463 56-110 150-158 100 6 100 50-56 38-44 0 25-38 16-25
400-450 o 70-80 o 5-8 16-18 o 31-35 o 78 25
238-413 38-69 100-1 06 69- 75 6-8 23-29 13-19 44-50 4-6 28-31 14-19
B ~l t ! l
A
c i
lE l ~ J ! ~
D
H ] ~ 1 t ~
G
&
J
l
fOQlullre. 5.8. Diagrammatic drawings of Dactylogyrus Diesing, 1850 species. A-C - Dactylogyrus
afrolongicomis afrolongicomis Paperna, 1973 (redrawn from Paperna 1979). A - anchors and dorsal bar,
B - marginal hooklets, C - cirrus. D-F - D. afrolongicomis alberli Papena, 1973 (redrawn from Paperna
1979). ID- anchors and dorsal bar, E - marginal hooklets, F - cirrus. G-I- D. afrosclerovaginus Paperna,
1973 (redrawn from Paperna 1979). G - anchors and transvers bar, H - marginal hooklets, 1- cirrus. J-L
- D. allolongionchus Paepma, 1973 (redrawn from Paperna 1979). J - anchors and dorsal bar, K -
marginal hooklets, l- cirrus. Scale bar: 20j.Jm
B
A
c Jr
~
lE
o
J
H r r
G
\\\_
~
Figure. 5.9. Diagrammatic drawings of Dactylogyrus Diesing, 1850 species. A-C - Dactylogyrus
domonici Mashego, 1983 (redrawn from Mashego 1983). A - anchors and dorsal bar, B - marginal
hooklets, C - cirrus. D-F - D. enidae Mashego, 1983 (redrawn from Mashego 1983). D - anchors and
dorsal bar, E - marginal hooklets, F - cirrus. G-I - D. jubbstrema Price, Korach & McPott, 1969 (redrawn
from Price, Korach & McPott 1969). G - anchors and transvers bars, li - marginal hooklets, I - cirrus.
Scale bar: 20J.jm
B
A
c
E
D
IF
H
G
Figure.5.10. Diagrammatic drawings of Dactylogyrus Diesing, 1850 species. A-C - Dactylogyrus myersi
Price, McClellan, Druckenmiller & Jacobs, 1969 (redrawn from Price, McClellan, Druckenmiller & Jacobs
1969). A - anchors and dorsal bar, B - marginal hooklets, C - cirrus. D-F - D. spiniciffus (paperna &
Thurston, 1968) (redrawn from Paperna & Thurston 1968). 0 - anchors and dorsal bars, E - marginal
hooklets, F - cirrus. G-I - D. teresae Mashego, 1983 (redrawn from Mashego 1983). G - anchors and
transvers bar, iii - marginal hooklets. I - cirrus. Scale bar: 20~m
Chapter 5 - The Monogenea 101
Species recorded from Cyprinus carpio Linnaeus, 1758
To date, no Dactylogyrus species collected from Cyprinus carpio have been
reported from Africa. The carp is an introduced species, thus the species of
Dactylogyrus that have been recorded from carp from other parts of the world will
be discussed.
According to Yamaguti (1963a) there are eight species of Dactylogyrus that have
been recorded from C. carpio. The first of these was D. auriculatus (Nordmann,
1832) from Europe, recorded from C. ca rpio, Phoxinus phoxinus Linnaeus, 1758
and Abramis brama Linnaeus, 1758. This is also the type species of the genus.
The species was redescribed by various authors, namely Roman (1953), Ergens
(1956), Prost (1957) and Lucky (1959). Diesing (1850) also described another
species, namely D. dujordinianus (Diesing, 1850) from Europe.
In 1924, Nybelin described D. vastator Nybelin 1924, which was recorded from
Europe, Japan and Siberia from C. carpio, Carassius auratus and C. carassius.
This species was, however, synonymised with D. intermedius Wegener, 1909 by
Nybelin (1937), which was described from Europe.
Yamaguti (1963a) lists the following species that have also been recorded from
C. carpio (references are, however, not provided): D. cyprini Buschkiel, 1930
from C. carpio from Java, D. extensus Mueller & Van Cleave 1932, from C.
carpio from North America and from Europe, D. solidus Achmerow, 1948.
Dactylogyrus extensus was redescribed by various other authors, i.e. Mueller
(1936), Fantham & Porter (1948), Mizelle & Klucka (1953), and Paperna (1959)
and was synonymised with D. solidus by Ergens (1956).
In 1952 Achmerov described another species, this time from C. c.
haematopterus, from Russia, namely D. falciformes Achmerow, 1952. Three
years later, Gussev described D. achmerowi, from carp in the Lake Khanka basin
(Gussev 1955).
Chapter 5 - The Monogenea 102
Comparative measurements of these species are given in Table 5.6.
68 55 5 11 5 38 5 45 61
51 52 8 17 22 34 11 474 161
72 66 9 16 19 44 12 77 69
38 42 3 17 31 33 5 213 60
49 43 8 14 7 39 5 46 57
A B
c n
=
E F
=
Figure. 5.11. Diagrammatic drawings of Dactylogyrus Diesing, 1850 species. A, B, - Dactylogyrus
achmerowi Nordmann, 1832 (redrawn fromYamaguti 1963a). A - anchors and dorsal bar, B - cirrus. C,
D,- D. auriculatus Gussev, 1955 (redrawn from Yamaguti 1963a). C - anchors and dorsal bar, D - cirrus.
le, F - D. extensus (Mueller & Van Cleave, 1932 (redrawn from Yamaguti 1963a). E - anchors and dorsal
bar, F - cirrus. Scale bar: 20IJm
A B
c D
=
Figure. 5.12. Diagrammatic drawings of Dactylogyrus Diesing, 1850 species. A, B, - Dactylogyrus
falciformes Achmerov, 1952 (redrawn from Yamaguti 1963a). A - anchors and dorsal bar, B - cirrus. C,
D - D. vastator Nybelin, 1924 (redrawn from Yamaguti 1963a). C - anchors and dorsal bar 0 - cirrus.
Scale bar: 20IJm
Chapter 5 - The Monogenea 105
The Genus Dagie/ius Byehowsky 1936
Generic Diagnosis
According to the amended generic diagnosis of Price & Yurkiewicz (1968),
Dogielius belongs to the subfamily Dactylogyrinae. One pair of anchors is
present on the haptor, and a simple dorsal bar supports the basis. Fourteen
marginal hooks are present, and all are similar in shape. Four eyespots are
present. The copulatory complex consists of a basally articulating accessory
piece and a tubular cirrus. A double prostatie reservoir is present. The seminal
vesicle is a simple dilation of the vas deferens, which is not looped around the
intestinal limb, as opposed to Dacfylogyrus. The testis is postovarian, but might
overlap the ovary in the dorsal view. The vagina opens ventrally, to the right of
the median line.
Specoes of Dogie/ius recorded from La/beo hosts
Twenty-two species of Dogielius are known from African freshwater fishes, and
of these, 15 have been described from Labeo hosts.
The first of these was D. junorsfrema Price & Yurkiewicz, 1969, which was
described by Price & Yurkiewicz in 1968 from Labeo ruddi Boulenger, 1907, from
Zimbabwe. Paperna (1969) described D. fropicus Paperna, 1969 from L. coubie
in Ghana. Paperna also recorded the same species from L. senegalensis
Valencienes, 1842 in the same year.
In 1973, Paperna described D. dublicornis Paperna, 1973 from L. cylindricus
from Tanzania. Paperna (1979a) described two subspecies of D. junorsfrema
from Labeo species, one from Tanzania, namely D. j. ruahae Paperna, 1979 and
one from Kenya, namely D. j. vicforianus Paperna 1979. The former was
collected from L. cylindricus and the latter from L. vicforianus.
Guegan, Lambert & Euzet described eight species from Labeo in 1989, all from
research done in Mali. Six of these species were described from L. coubie, i.e.
Chapter 5 - The Monogenea 106
D. anthocolpus Guegan, Lambert & Euzet, 1989, D. clavipenis Guegan, Lambert
& Euzet, 1989, D. complicatus Guegan, Lambert & Euzet, 1989, D. flagellatus
Guegan, Lambert & Euzet, 1989, D. grandijugus Guegan, Lambert & Euzet, 1989
and D. harpagatus Guegan, Lambert & Euzet, 1989. The remaining two species
were described from L. senegalensis, namely D. flosculus Guegan, Lambert &
Euzet, 1989, and from L. parvus, namely D. parvus Guegan, Lambert & Euzet,
1989.
Two years later, Guegan & Lambert (1991) described another two species, both
from West Africa. One species was described from L. allauadi namely D.
kabaensis Guegan & Lambert, 1991, and one from L. parvus, namely D.
rosumplicatus Guegan & Lambert, 1991.
A summary of the species of Dogielius occurring on Labeo hosts is given in
Table 5.7 and a comparison of the measurements are given in Table 5.8.
Chapter 5 - The Monogenea 107
Labeo coubie Ru ,1832 Mali
L. coubie Mali
D. complicatus
G Lambert & E L. coubie Mali
Peters 1868 Tanzania
Mali
Mali
L. coubie Mali
D. harpagatus
G Lambert & Euzet 1989 L. coubie Mali
L. ruddi Boulen 1907 Zimbabwe
Tanzania
nger,
Ken
L. alluaudi Peil 1933 West Africa
1902 Mali
West Africa and
L. Guinea
L. coubie Ghana
Chapter 5 - The Monogenea 108
300-450 60-100 38-41 45-50 26-29 63-70 50 50-60
250-350 60-100 33-36 34-37 28-30 57-60 30
350-550 110-150 47-52 45-51 25-27 62-67 310-410 80-90
150-200 80 22 29 16 50-54 39 33
300-430 80-100 36-40 34-38 30-33 61-70 150-200 46-56
250-350 60-100 40-46 42-49 23-29 45-50 50 37-47
260-450 60-110 33-37 36-41 39-43 80-100 32-40
220-350 60-80 28-32 31-37 21-25 44-51 25-30 31-38
178-243 46-72 32 32 19 47-55 19-24 17-22
150-210 70-10 19 24 14 42-48 22-30 16-25
140-230 50-80 19 28 14 44-49 36-42 33-43
330-420 60-80 30-36 41-45 14-17 50-56 22-30 19-22
250-350 60-90 29-33 33-38 18-22 38-47 25-30 31-34
330-450 70-90 32-36 41-45 15-18 50-57 25-30 30-36
250-400 70-100 35-40 39-45 21-26 55-65 35-40 32-36
A
c
D
Figure. 5.13. Diagrammatic· drawings of Dogielius Bychowsky, 1936 species. A-C - Dogie/ius
anthoco/pus Guegan, Lambert & Euzet, 1989 (redrawn from Guegan, Lambert & Euzet 1989). A-
anchors and dorsal bar, B - marginal hooklets, C - cirrus. D-F - D. c/avipenis Guegan, Lambert & Euzet,
1989 (redrawn from Guegan, Lambert & Euzet 1989). ID- anchors and dorsal bar, E - marginal hooklets.
F - cirrus. Scale bar: 20IJm
c
E
D
Figure. 5.14. Diagrammatic drawings of Dogielius Bychowsky, 1936 species. A-C - Dogielius
complicatus Guegan, Lambert & Euzet, 1989 (redrawn from Guegan, Lambert & Euzet 1989). A-
anchors and dorsal bar, B - marginal hooklets, C - cirrus. D-f' - D. dublicomis Paperna, 1973 (redrawn
from Paperna 1979). D - anchors and dorsal bar, E - marginal hooklets, F - cirrus. Scale bar: 20J,Jm
A
c
r ltll Jl
o
F
Figure.5.15. Diagrammatic drawings of Dogie/ius Bychowsky, 1936 species. A-C - Dogielius flagel/atus
Guegan, Lambert & Euzet, 1989 (redrawn from Guegan, Lambert & Euzet 1989). A - anchors and dorsal
bar, IB- marginal hooklets, C - cirrus. ID-F - D. f/oscu/us Guegan, Lambert & Euzet, 1989 (redrawn from
Guegan, Lambert & Euzet 1989). 0 - anchors and dorsal bar, E - marginal hooklets. F - cirrus. Scale
bar: 20jJm
B Il t \! 1 t
c
D
F
Figure. 5.16. Diagrammatic drawings of Dogielius Bychowsky, 1936 species. A-C - Dogie/ius
grandijugus Guegan, Lambert & Euzet, 1989 (redrawn from Guegan, Lambert & Euzet 1989). A-
anchors and dorsal bar, IB- marginal hooklets, C - cirrus. ID-F - D. harpagatus Guegan, Lambert & Euzet,
1989 (redrawn from Guegan, Lambert & Euzet 1989). 0 - anchors and dorsal bar, E - marginal hooklets,
f - cirrus. Scale bar: 20IJm
B \ \
A
c
ID E
IF
Figure. 5.17. Diagrammatic drawings of Dogie/ius Bychowsky, 1936 species. A-C - Dogielius
junorstrema Price & Yurkiewicz, 1968 (redrawn from Price & Yurkiewicz 1968). A - anchors and dorsal
bar, IB - marginal hooklets, C - cirrus. D-F - D. junorstrema ruahae Paperna, 1979 (redrawn from
Paperna 1979). D - anchors and dorsal bar, E - marginal hooklets, F - cirrus. Scale bar: 20j..lm
B
c
E 11!!! tl
IF
Figure. 5.18. Diagrammatic drawings of Dogielius Bychowsky, 1936 species. A-C - Dogielius
junorstrema vicforianus Paperna, 1979 (redrawn from Paperna 1979). A - anchors and dorsal bar, B -
marginal hooklets, C - cirrus. D-F - D. kabaensis Guegan & Lambert, 1991 (redrawn from Guegan &
Lambert 1991). D - anchors and dorsal bar, E - marginal hooklets, F - cirrus. Scale bar: 20fJm
A
c
lE !
f
HI
G
Figure. 5.19. Diagrammatic drawings of Dagje/jus Bychowsky, 1936 species. A-C - Dagje/jus parvus
Guegan, Lambert & Euzet, 1989 (redrawn from Guegan, Lambert & Euzet 1989). A - anchors and dorsal
bar, B - marginal hooklets, C - cirrus. D-F - D. rosumplicatus Guegan & Lambert 1991 (redrawn from
Guegan & Lambert 1991). 0 - anchors and dorsal bar, E - marginal hooklets, F - cirrus. G-I - D.
tropicus Paperna, 1969 (redrawn from Guegan & Lambert 1991). G - anchors and dorsal bar, H -
marginal hooklets, I - cirrus. Scale bar: 20IJm
Chapter 5 - The Monogenea 116
Dactylogyridean species from Clarias gariepinus (BurchelI, 1822)
In Africa, the genus Ouadriacanfhus Paperna, 1961, comprises 24 species which
parasitise the gills of siluriform fishes, except for one species described from a
representative of the Cichlidae (Paperna, 1979a). The latter, however,
(Ouadriacanfhus filapiae Paperna, 1973), is considered an accidental infestation
(Kritsky & Kulo 1988; Lim, Timofeeva & Gibson 2001). The remaining species of
Ouadriacanfhus have all been described from three host genera, namely Clarias,
Heferobranchus Geoffroy-Saint-Hillaire, 1809 and Bagrus Forsskál, 1775.
The Genus Quadriacanthus Paperna, 1961
Generic Diagnosis
The genus Ouadriacanfhus, as initially described by Paperna (1961) belongs to
the family Dactylogyridae Bychowsky, 1933 and the subfamily Ancyrocephalinae,
Bychowsky, 1937. Kritsky & Kulo (1988), however, emended this description.
They divided the body into four regions, namely a cephalic region, a trunk,
peduncle and haptor. The tegument is thin and smooth and there are four pairs
of cephalic lobes present, two lateral and two terminal. Four pairs of head
organs are present. The cephalic glands are unicellular and comprise two
bilateral groups, situated posterolateral to the pharynx. Eyes may be present or
absent, and the granules are scattered in the cephalic region.
The mouth is situated subterminally and midventrally. A muscular, glandular
pharynx is present, leading to a short oesophagus. Two intestinal caeca are
present, which confluent posterior to the gonads which are situated intercaecally
and overlap with the testis dorsal to the ovary. The seminal vesicle is a dilation
of the vas deferens, and is situated diagonally to the left of the midline in the
anterior trunk, with the vas deferens looping around the left intestinal caecum.
Two C-shaped prostatie reservoirs are present, the one wrapping around the
other. The copulatory complex consists of a basally articulated cirrus, and the
accessory piece. A short oviduct and delicate uterus is present. The vagina
opens on the sinistral side of the body, and the seminal receptacle is situated
Chapter 5 - The Monogenea 117
ventral to the anterior end of the ovary, and is intercaecal. Well-developed
vitellaria is dispersed in two bilateral bands, extending with intestinal caeca.
The haptor is armed with dorsal, as well as ventral anchors, each with a basal
accessory sclerite. A dorsal bar with expanded midregion and bilateral arms is
present. There is also a ventral bar consisting of two medially articulating
components. A posterior muscle pad is situated between the bars. Fourteen
marginal hooklets are present, with an ancyrocephaline distribution. Hook pair
six posses an elongated proximal dilation of the shank, while pairs one and
seven have a short proximal dilation of the shank. In pairs two, three, four and
five, the dilated shank is absent.
Specoes of Quadriacanthus Paperna, 1961 recorded from Afll"oCall11l
sllurlform fishes
Paperna (1961) created the genus Quadriacanthus to accommodate
Quadriacanthus clariadis, which he described from Clarias gariepinus, from Lake
of Galilee in Israel. Paperna (1965) then described another species of
Quadriacanthus from Clarias walkeri Gunther, 1896 namely Q. voltaensis, from
Ghana.
Eight years later, Paperna (1973) described Q. tilapiae Paperna, 1973, from a
single specimen, which was found on Oreochromis esculentus Graham, 1928
from Uganda. This species has not been recorded since the initial description,
and Kritsky & Kulo (1988) believe that this species is a synonym of Q. bagrae
Paperna, 1979.
In the late seventies, Paperna (1979a) subdivided Quadriacanthus clariadis into
three subspecies, namely Q. c. allobychowskiella Paperna, 1979 parasitising
Clarias gariepinus from Uganda, Q. c. bagrae Paperna, 1979 parasitising Bagrus
bajad (Forsskai, 1775), also from Uganda and Q. c. clariadis from Israel. In
Chapter 5 - The Monogenea 118
1986, EI-Naggar & Serag described another species from Egypt, namely Q.
aegypticus EI-Naggar & Serag, 1986, also from Clarias gariepinus.
In a comprehensive study on the African species, the three subspecies described
by Paperna were, however, raised to species level by Kritsky & Kulo (1988).
They also gave a redescription of the genus, and Q. clariadis, and described
three new species from Egypt, namely Q. ashuri Kritsky & Kulo, 1988, Q.
papernai Kritsky & Kulo, 1988, and Q. numidus Kritsky & Kulo, 1988, all from
work done on Clarias gariepinus. Two undescribed species were discovered
amongst the specimens that were labelled as paratype material of Q. clariadis.
Birgi (1988) described four new species, three from Clarias jaensis Boulenger,
1909 and one from Clarias pachynema Boulenger, 1903. All of these species
were described from Cameraan waters.
During 1995, Douëllou & Chishawa recorded three known species from research
done in Zimbabwe, namely Q. aegypticus, Q. bagrae Paperna, 1979, and Q.
numidus, collected from Clarias gariepinus.
In the late nineties, N' Douba, Lambert & Euzet (1999) did research in the Ivory
Coast on Heterobranchus isopterus Bleeker, 1863 and H. Iongifiiis Valenciennes,
1840 and described seven new species. Two new species were described by
N'Douba & Lambert also from the Ivory Coast in 2001, namely Q. eboreus
N'Douba & Lambert, 2001, and Q. ivoiriensis N'Douba & Lambert, 2001, both
parasitising Clarias ebriensis Pellegrin, 1920.
The African species of Quadriacanthus is summarised in Table 5.9. Comparative
measurements of the species recorded from C. gariepinus are given in Table
5.10.
Chapter 5 - The Monogenea 119
Uganda, Zimbabwe, Ghana
and
Clarias jaensis
Bi Boule 1909 Cameroon
Q. eboreus Clarias ebriensis Pellegrin,
N'Oouba & Lambert 2001 1920
Q. goureni
N'Oouba Lambert & E 1999
Clarias ebriensis
etenes pachynema
Boule 1903
Heterobranchus longifilis
Valencien 1840
and Zimbabwe
Q. thysi
N'Oouba Lambert & 1999
Q. tilapiae
Pa 1973
Ghana and
Ghana
Chapter 5 - The Monogenea 120
Q. aegypticus
EI-Naggar & Serag, 313-502 76-105 36-44 13-18 43-51 13-18 39-53 45-74 40-52 33-49
1986
Q. allobychowskiella
Pa 1979 380-499 88-105 26-31 8-15 44-51 15-18 44-56 51-74 41-48 30-43
340-431 101-165 35-38 12-14 37-42 12-14 33-45 56-75 38-43 28-29
287-481 80-126 30-34 9-12 33-42 12-16 42-64 51-78 23-27 17-21
343-444 71-134 29-34 9-11 47-72 12-15 42-65 52-72 22-31 17-26
1988 346-432 80-121 40-44 10-13 43-47 12-15 44-48 44-47 28-32 20-24
1988 329-461 78-108 33-41 8-13 34-37 9-13 24-33 40-49 35-43 29-37
0 0 30-34 9-12 33-42 12-16 42-64 51-78 23-27 17-21
A
c j J
(VI) (II-IV) (I,VII) (V)
o
B
f ( ) ;
le G I
(VI) (II-IV) (I) (VII) (V)
H
Figure. 5.20. Diagrammatic drawings of haptoral structures and cirrus of Quadriacanthus Paperna, 1961
species. A-D - Q. aegypticus EI-Naggar & Serag, 1986 (redrawn from Kritsky & Kulo 1988). A - ventral
bar and anchors, IB - dorsal bar and anchors, C - marginal hooklets, D - cirrus. IE-H - Q.
allobychowskiella Paperna, 1979 (redrawn from Kritsky & Kulo 1988). E - ventral bar and anchors, F -
dorsal bar and anchors, G - marginal hooklets. H - cirrus. Scale bar: 25IJm
A c rIl
(l1-IV,vI) (I,vll) (V)
B D
E
G
(II-IV,VI) (I,VII) (V)
f
Figure.5.21. Diagrammatic drawings of haptoral structures and cirrus of Quadriacanthus Paperna, 1961
species. A-D - Q. ashuri Kritsky & Kulo, 1988 (redrawn from Kritsky & Kulo 1988). A - ventral bar and
anchors, B - dorsal bar and anchors, C - marginal hooklets, ID- cirrus. E-IH - Q. bagrae Paperna, 1979
(redrawn from Kritsky & Kulo 1988). E - ventral bar and anchors, F - dorsal bar and anchors, G -
marginal hooklets, H - cirrus. Scale bar: 2SJ..Im
A c i t (
(II-IVVI) (VII) (I) (V)
IS ID
E G
(II-IV,VI) (lVII) (V)
f
Figure. 5.22. Diagrammatic drawings of haptoral structures and cirrus of Quadriacanthus Paperna, 1961
species. A-D - Q. clariadis Paperna, 1961 (redrawn from Kritsky & Kulo 1988). A - ventral bar and
anchors, B - dorsal bar and anchors, C - marginal hooklets, D - cirrus. E-H - Q. numidus Kritsky & Kulo,
1988 (redrawn from Kritsky & Kulo 1988). E - ventral bar and anchors, F - dorsal bar and anchors, G-
marginal hooklets, H - cirrus. Scale bar: 25~m
A c
(II-IV,VI) (I,VII) (V)
B D
E G
(I-IV,VI,VII) (V)
IF
Figure. 5.23. Diagrammatic drawings of haptoral structures and cirrus of Quadriacanthus Paperna, 1961
species. A-D - Q. papernai, Kritsky & Kulo, 1988 (redrawn from Kritsky & Kulo 1988). A - ventral bar and
anchors, B - dorsal bar and anchors, C - marginal hooklets, 0 - cirrus. E-H - Q. voltaensis Paperna,
1979 (redrawn from Kritsky & Kulo 1988). E - ventral bar and anchors, F - dorsal bar and anchors, G -
marginal hooklets, H - cirrus. Scale bar: 2SIJm
Chapter 5 - The Monogenea 125
Dlplozold monogeneaus
Diplozoid monogeneans are characterised by adult worms that are in permanent
fusion in the form of a cross (Yamaguti 1963a), and the absence of copulatory
organs. According to Khotenovsky (1985) the body of these worms can be
divided into two regions, an anterior part, ahead of the region of fusion, and a
posterior part, behind the region of fusion. There are usually four pairs of clamps
present on the haptor, and one pair of crooked anchors. Currently, there are two
species of Paradiplozoon Achmerov, 1974 known from Africa.
The Genus Paradiplozoon Achmerov, 1974
Generic Diagnosis
According to Khotenovsky (1985), Paradiplozoon Achmerov, 1974 species differ
from other diplozoids in that they have no enlargements in the posterior part of
the body. The posterior part can also be divided into two regions, and in the
anterior region folds may be present or absent, which vary in size between
species. Gonads are situated in the anterior region of the posterior part of the
body. The testes are single and protuberant. The uterus outlet is lateral, and
situated on the border between the two sections of the posterior part of the body.
Paradiplozoon Achmerov, 1974 species from African fishes
Thomas (1957) described the first diplozoid species from Africa. This species
was described from Ghana, namely Diplozoon ghanense Thomas, 1957 from
Alestes macrolepidotus. In 1963 Fischtkal & Kuntz described D. aegyptensis
Fischtkal & Kuntz, 1963 collected from Labeo forskalii from Egypt. Khotenovsky
(1985) later placed both these species in the genus Paradiplozoon, on the
grounds that there are no enlargements present in the posterior part of the body.
Measurements comparing the known species are given in Table 5.11.
Chapter 5 - The Monogenea 126
3210-3830 1860-2540 540-740 380-480 380-480 120-160 100-110 260- 1150
3620-5767 1879-3452 299-836 867-1871 130-245 65-79 92-102 81-132 254-313
Chapter 5 - The Monogenea 127
Bra1nchloal monoqeneans from Soetdoring Nature
Reserrve
Five species of monogeneans were collected from the fish of the Soetdoring
Nature reserve, which include two Dacty/ogyrus species, one Dogie/ius, one
Quadriacanthus and one Paradip/ozoon species. A new species of Dacty/ogyrus
was collected from Labeo capensis. Dacty/ogyrus sp. A was collected from carp
(C. carpio). A new species of Dogie/us was also collected from L. capensis.
Quadriacanthus sp. 8 was collected from C/arias gariepinus. A previously
recorded but undescribed species of Paradip/ozoon from the Orange River
system was also collected from L. capensis.
Dactylogyrus sp. A
Host and /ocality: Cyprinus carpio Soetdoring Nature Reserve, South Africa (280
52' S, 260 0' E)
Infection Site: Gills
Specimens studied: Morphometric measurements and drawings made using light
microscopy. Reference material (V2002/04/16-04, V2002/04/16-05,
V2002/04/16-06, V2002/04/16-07) deposited in the collection of the Aquatic
Parasitology Study group, University of the Free State.
Description
Large worms, measuring 1021.6±49.8 (1079.2-968.0) long and 306.7±30.8
(266.6-340.3) wide (Figure 5.26A). Anchors large (Figure 5.24A, Figure 5.268),
with total length of 72.2±2.2 (69.3-74.6); base width 27.8±1.0 (26.4-28.9); inner
and outer root relatively square, inner root 20.7±1.5 (19.0-22.4) long, outer root
11.1±1.9 (8.5-12.7) long; shaft length 70.3±1.1 (69.0-71.3); length of tip 18.3±1.5
(16.7-20.4); dorsal bar simple (Figure 5.248, Figure 5.26C); length 46.9±1.5
(45.2-48.9), width 8.8±1.8 (7.4-11.5); marginal hooklets (Figure 5.25A, Figure
5.260) equal in shape, pair I, 33.9±0.6 (33.5-34.9), pairs II, IV, VII 30.9±1.5 (27.7-
32.0), pair Ill, 31.8±2.5 (28.1-33.3), pair V, 28.4±0.8 (27.7-29.5), pair VI, 31.5±0.6
(30.6-32.0) long. Copulatory complex (Figure 5.258, Figure 5.26E) consisting of
curved penis 66.1 ±4.5 (62.0-71.8) long, and accessory piece 82.2±7.0 (71.8-
87.1) long, with distal part slightly enlarged and branched.
Chapter 5 - The Monogenea 128
Remarks:
Based on the above description and morphometrical data, Dactylogyrus sp A can
be identified as D. extensus (Figure 5.24, Figure 5.25, Figure 5.26 & Table 5.12).
In comparing the present material with the European populations of D. extensus
(Table 5.13) the only marked difference is the size of the cirrus and accessory
piece. Dactylogyrus auriculatus shows the closest resemblance to D. extensus,
but differs from it in the shape of the copulatory complex (Figure 5. 25B, Figure
5.26E).
A
B
Figure 5.24. Microscope projection drawings of Dactylogyrus extensus (Mueller & Van Cleave, 1932)
from Cyprinus carpio Linnaeus, 1758 collected from the Soetdoring Nature Reserve. A - anchors, B -
dorsal bar. Scale bar: 20IJm
II III IV V VI VII
A
B
Figure 5.25. Microscope projection drawings of Dactylogyrus extensus (Mueller & Van Cleave, 1932) from
the gills of Cyprinus carpio Linnaeus, 1758 collected from the Soetdoring Nature Reserve. A - marginal
hooklets, B - cirrus. Scale bar: 30IJm
Figure. 5.26. Light micrographs of Dactylogyrus extensus (Mueller & Van Cleave, 1932) collected from
the gills of Cyprinus carpio Linnaeus, 1758. A - whole mount, B - anchors, C - transverse bar, 0 -
marginal hooklets, E - cirrus. Scale bar A: 100lJm, B-E: 10IJm
Chapter 5 - The Monogenea 132
Dactylogyrus freistatensis n. sp.
Host and locality: Labeo capensis, Soetdoring Nature reserve, South Africa (280
52' S, 260 0' E)
Infection Site: Gills
Specimens studied: Morphometric measurements and drawings (Figure 5.27,
Figure 5.28, Figure 5.29 & Table 5.13) made using light microscopy. Reference
material (V2002/05/16-01, V2002/05/16-02, V2002/05/16-03, V2002/05/16-04
V2002/05/16-05, V2002/05/16-06, V2002/05/16-07) deposited in the collection of
the Aquatic Parasitology Study group, University of the Free State.
Description:
Small worms, measuring 326.4±21.8(294.9-356.8) long and 76.1±2.0 (73.3-77.5)
wide (Figure 5.29A). Anchors relatively large (Figure 5.27A, Figure 5.29B), with
total length of 45.0±1.7 (42.0-46.8); base width 8.6±0.9 (7.4-9.9); inner root
20.1±1.2 (18.2-21.7) long, outer root 1.8±0.8 (1.1-3.0) long; shaft length 28.4±1.0
(27.1-29.6); length of tip 10.5±1.0 (9.5-12.2); dorsal bar (Figure 5.27C, Figure
5.29B) length 21.1 ±1.5 (19.5-23.7), width 3.7±0.9 (3.3-4.6); vestigial ventral bar
10.0± 0.9 (9.0-11.1 )(Figure 5.27B); marginal hooklets (Figure 5.28A, Figure
5.29C) with proximal dilation of shank at 1/3 of length, pair I 17.3±1.2 (15.4-18.8)
pair 1115.1±0.9 (14.0-16.5) III 15.4±1.2 (14.1-16.8), pair IV 19.4±1.3 (17.3-21.1),
pair V 18.7±0.6 (17.9-19.3), pair VI 17.7±1.2 (16.2-19.2), pair VII 18.7±1.6 (16.1-
20.1) long. Copulatory complex (Figure 5.2B, C, Figure 5.29D) consisting of
penis 117.7±14.5 (98.13-132.7) long making varying spirals and forming bulb like
structure at proximal end, and accessory piece 13.8±0.8 (13.1-15.1) long with
enlarged basal part, ending in small fork (Figure 5.28B); vagina consists of long
twisted tube (Figure 5.28C).
Etymology: The specific name is derived from the Sotho name for the Free State
province (Freistata) in which the Soetdoring Nature Reserve is situated.
Remarks:
The specimens collected from Labeo capensis resemble D. senegalensis in the
shape of the penis and vagina, but differ from it in the shape of the accessory
Chapter 5 - The Monogenea 133
piece, and the absence of a vestigial ventral bar in D. senegalensis. It also
resembles D. labeous, D. jubbstrema and D. brevicirrus in the shape of the dorsal
bar, and the vestigial ventral bar, but differs from these species in the shape of
the cirrus and accessory piece. Dacfylogyrus freisfafensis n. sp. does not
resemble any of the Dacfylogyrus species previously recorded from South Africa.
295-357 73-78- 42-47 27-30 1-3 18-22 10-12 20-24 3-5 98-133 13-15
230-380 40-100 35-40 20-24 1-4 16-20 10-14 19-21 25-30 15-21
D. jubbstrema
Price, Korach & 190-226 50-60 32-38 18 3 18 15 15-18 4 21-25 14-17
M 1969
D./abeous
Pa 1969 230-400 40-80 38-43 29-31 3-4 16-21 12-17 20-23 4-5 33-39 30
D. senega/ensis
Pa rna 1969 200-500 50-80 29-33 24-28 1-4 8-13 11-14 17-21 3-4 180
A
Figure 5.27. Microscope projection drawing of Dactylogyrus freistatensis n. sp. From the gills of Labeo
capensis (Smith, 1841) collected from the Soetdoring Nature Reserve. A - anchors, B - vestigial ventral
bar, C - transverse bar. Scale bar: 20~m
II III IV V VI VII
A
B c
Figure 5.28. Microscope projection drawings of Dactylogyrus freistatensis n. sp. from the gills of Labeo
capensis (Smith, 1841) collected from the Soetdoring Nature Reserve. A - marginal hooklets, B - cirrus,
C - vagina. Scale bar: 20IJm
Figure. 5.29. Light micrographs of Oactylogyrus freistatensis n.sp. collected from the gills of Labeo
capensis (Smith, 1841). A - whole mount, B - anchors, transverse bar and marginal hooklets, C -
marginal hooklets, 0 - cirrus. Scale bar A: 100lJm, 8-0: 10IJm
Chapter 5 - The Monogenea 137
Dagie/ius capensis n. sp.
Host and locality: Labeo capensis, Soetdoring Nature reserve, South Africa (280
52' S, 260 0' E)
Infection Site: Gills
Specimens studied: Morphometric measurements and drawings (Figure 5.30,
Figure 5.31, Figure 5.32 & Table 5.14) made using light microscopy. Reference
material (V2002/05/16-08, V2002/05/16-09) deposited in the collection of the
Aquatic Parasitology Study group, University of the Free State.
Description:
Small worms (Figure 5.32A) measuring 345.6±13.0 (336.4-354.7) long and
101.2±19.6 (87.3-115.1) wide. Anchors small (Figure 5.30A, Figure 5.32B), with
total length of 28.3±1.9 (27.0-29.7) ending with sharp curve; length of shaft +
inner root 38.1±6.0 (33.4-42.3); length of tip 17.4±1.7 (16.2-18.6); dorsal bar
(Figure 5.30B, Figure 5.32C) 42.0±9.3 (35.4-48.6) long, 5.5±1.7 (4.3-6.7) wide;
marginal hooklets uniform in shape forming small bulb at proximal end of shank
(Figure 5.31A, Figure 5.320), pair I 13.4±1.4 (12.4-15.5), pair II 14.0±2.0 (12.6-
15.5), pair III 18.9±1.6 (17.8-20.1), pair IV 17.8±1.5 (16.7-18.9), pair V 19.2±0.1
(19.2-19.3), pair VI 20.7±2.3 (19.0-22.3), pair VII 21.1±2.8 (19.1-23.0) long.
Copulatory complex consisting of curved penis 25.2 long and accessory piece
34.5 long, which folds around penis at distal end (Figure 5.31 B, Figure 5.32E).
Etymology: The specific name is derived from the specific name of the host,
Labeo capensis.
Remarks:
This species closely resembles D. tropicus, D. flosculus, D. parvus and D.
kabaensis in the shape of the roots of the anchors, as well as the shape of the
dorsal bar. Dogielius capensis, however, differs from these species in the shape
of the penis and the accessory piece. Dogielius capensis is the first species of
Dogielius recorded from South Africa.
Chapter 5 - The Monogenea 138
250-350 60-100 40-46 42-49 23-29 45-50 50 37-47
1991 330-420 60-80 30-36 41-45 14-17 50-56 22-30 19-22
250-350 60-90 29-33 33-38 18-22 38-47 25-30 31-34
D. tropicus
Pa 1969 250-400 70-100 35-40 39-45 21-26 55-65 35-40 32-36
A
B
Figure 5.30. Microscope projection drawing of Dogielius capensis n. sp. from the gills of Labeo capensis
(Smith, 1841) collected from the Soetdoring Nature Reserve. A - anchors, B - transverse bar. Scale bar:
20IJm
II III IV V VI VII
A
IB
FigUlre 5.31. Microscope projection drawings of Dogielius capensis n. sp. from the gills of Labeo capensis
(Smith, 1841) collected from the Soetdoring Nature Reserve. A - marginal hooklets, B - cirrus. Scale bar:
20IJm
Figure. 5.32. Light micrographs of Dogielius capensis n.sp. collected from the gills of Labeo capensis
(Smith, 1841). A - whole mount, B - anchors, C - transverse bar, D - marginal hooklets, E - cirrus.
Scale bar A: 100IJm, B-E: 10IJm
Chapter 5 - The Monogenea 142
Quadriacanthus sp, A
Host and locality: Clarias gariepinus, Soetdoring Nature reserve, South Africa
(280 52' S, 2600' E)
Infection Site: Gills
Specimens studied: Morphometric measurements and drawings made using light
microscopy. Reference material (V2001/09/25-11, V2001/09/26-05,
V2002/04/16-02, V2002/04/16-08, V2002/04/16-10, V2002/04/16-12) deposited
in the collection of the Aquatic Parasitology Study group, University of the Free
State.
Description
Large worms (Figure 5.35A) 629.4±167.4 (434.7-881.3) long, and 156.2±37.4
(108.4-222.3) wide. Ventral anchor (Figure 5.33A, Figure 5.358) 41.2±2.2
(38.5-45.4) long with short superficial root; small base 11.8±1.7 (9.5-13.6) wide;
shaft curved with elongate tip 14.0±1.7 (12.3-16.6) long; accessory sclerite small
11.4±1.2 (9.7-13.2) long, with subequal winglike processes; dorsal anchor
(Figure 5.338, Figure 5.35C) 53.8±3.9 (48.1-59.4) long, with short roots, shaft
bent proximally, short tip 4.3±0.7 (3.4-5.5) long, accessory sclerite 19.0±1.3
(17.2-21.2) long, and 9.4±1.3 (7.7-11.9) wide with subequal wings, anchor base
16.5±1.9 (13.5-19.7) wide. Ventral bar component (Figure 5.33A, Figure 5.35D)
50.5±3.2 (46.3-56.3) long, and 9.6±1.0 (7.8-11.2) at greatest width; dorsal bar
(Figure 5.338, Figure 5.35E) 39.4±5.9 (33.8-49.4) long, and 16.6±1.6 (15.0-
20.2) at greatest width, median process 19.3±1.4 (17.3-21.8) long. Marginal
hooklets (Figure 5.34A) with delicate point and protruding thumb; pair I, 14.0±1.3
(12.2-15.7), pair II, Ill, IV, 15.2±1.5 (12.8-17.9), pair V, 34.4±2 (31.1-37.3), pair
VI, 21.1±1.7 (18.9-23.9), pair VII, 20.2±1.7 (17.9-22.8) long. Cirrus (Figure
5.348, Figure 5.35F) 55.1 ±10.0 (44.1-68.2) long, comprising long tapered tube
with narrow base; accessory piece 61.7±10.5 (48.9-73.7) long, forming two
bulbs, at 1/3 and 2/3's of length, ending in two distinct hooks.
Chapter 5 - The Monogenea 143
Remarks:
Based on the above description and morphometrical data, Quadriacanthus sp. A
can be identified as Q. aegypticus (Figure 5.33, Figure 5.34, Figure 5.35 & Table
5.15).
Two populations of Q. aegypticus could be distinguished based on the size of the
cirrus and accessory piece (Table 5.15). The length of the cirrus of one group
falls well within the range given for Q. aegypticus by Kritsky & Kulo (1988), while
the second group has a cirrus and accessory piece that is approximately 20j.Jm
longer. The material collected from Soetdoring Nature Reserve differs from the
material from Egypt only in the longer length of marginal hooklet pairs I and VII.
Quadriacanthus aegypticus can be distinguished from the other species of
Quadriacanthus by the shape of the accessory piece, which ends in two distinct
hooks. N'Douba, Lambert & Euzet (1999) described the accessory piece as
ending in two hooks, although in their drawing of the copulatory complex this
shape could not be distinguished. Kritsky & Kulo (1988) did not mention this
characteristic of the accessory piece, but from their drawing this characteristic
can clearly be seen. Quadriacanthus aegypticus also resembles Q. clariadis, but
differs from it in the shape and size of the cirrus and accessory piece. Q.
aegypticus is the first species of Quadriacanthus recorded from South Africa.
Table 5.15. Comparison of the Egyptian population of Quadriacanfhus aegypticus EI-Naggar & ~
Serag, 1986 with the population from Soetdoting Nature reserve. AP-Iength of accessory piece,
C-Iength of cirrus, DA-Iength of dorsal anchor, DAB-base width of dorsal bar, DB-length of dorsal
bar, TL-totallength, VA-Iength of entral anctior, VAS-base Width of ventral anchor, VB-length of
ventral bar, W-greatest width
POl?_ulation TL W VA VAB DA DAB VB DB C AP
Egypt
313-502 76-105 36-44 13-18 43-51 13-18 39-53 45-74 40-52 33-49
Soetdoring Nature
Reserve 434-881 108-222 39-45 10-15 48-59 14-20 46-56 34-49 44-68 49-74
B
Figure 5.33. Microscope projection drawings of Quadriacanthus aegypticus EI-Naggar & Serag, 1986
from the gills of Clarias gariepinus (Burchell, 1822) collected from the Soetdoring Nature Reserve. A-
ventral bar and anchors, B - dorsal bar and anchors. Scale bar: 20j.Jm
II III IV V VI VII
A
IB
Figure 5.34. Microscope projection drawings of Quadriacanthus aegypticus EI-Naggar & Serag, 1986
from the gills of Clarias gariepinus (Burchell, 1822) collected from the Soetdoring Nature Reserve. A-
marginal hooklets, B- cirrus. Scale bar: 20IJm
Figure. 5.35. Light micrographs of Quadriacanthus aegypticus El Naggar & Serag, 1986. A - whole
mount, B - ventral anchor, C - dorsal anchor, 0 - ventral bar component, E - dorsal bar, F - cirrus.
Scale bar A: tooprn, B-F: toprn
Chapter 5 - The Monogenea 147
Paradiplozoon modderensis n. sp.
Host and locality: Labeo capensis, Soetdoring Nature reserve, South Africa (280
52' S, 260 0' E)
Infection Site: Gills
Specimens studied: Morphometric measurements and drawings (Figure 5.36,
Figure 5.37, Figure 5.38, Figure 5.39 & Table 5.16) made using light microscopy.
Reference material (V2001/03/21-05, V2002/03/13-05, V2002/07/11-01,
V2001/11/26-05, V2001/11/27 -02) deposited in the collection of the Aquatic
Parasitology Study group, University of the Free State.
Description:
Adults united in pairs in permanent copula in the form of a cross (Figure 5.36A,
Figure 5.39A). Total body length 3734.4±395.6 (2880.0-4180.0), length of
anterior part 2312.2±319.1 (1750.0-2660.0), width 912.2±231.3 (550.0-1290.0),
length of posterior part 1308.5±151.0 (1110.0-1510.0), width 420.0±86.1 (310.0-
570.0). Prohaptor consists of a pair of cup-shaped buccal suckers (Figure
5.36B), 82.0±5.8 (72.3-93.9) in diameter. Four pairs of clamps present on the
haptor (Figure 5.37A, Figure 5.39B), all equal in size 99.7±4.3 (93.5-105.7) in
length and 48.3±3.3 (41.2-52.9) wide. Each clamp consists of dorsal and ventral
sclerites, which is strengthened by median U-shaped piece. Each dorsal sclerite
with well-developed spur 39.8±2.5 (35.8-44.5) long. Two small crooked anchors
(Figure 5. 37B) present between rows of clamps. Mouth opening subterminal,
between buccal suckers. Pharynx (Figure 5.36B) oval shaped, 71.9±5.6 (65.1-
79.5) long. Intestine not bifurcate, but with numerous diverticula. Testis single,
lobed, 219.3±74.4 (166.3-325.3) long and 84.9±2.3 (81.9-86.7) wide (Figure
5.38), situated posterior to, but in close contact with much folded ovary,
248.8±39.7 (204.8-301.2) long and 113.3±2.3 (84.3-127.7) wide (Figure 5.38).
Eggs large, 309.0±70.7 (250.3-387.5) long and 119.7±15.6 (103.7-134.9) wide
with very long and coiling filament (Figure 5.37C, Figure 5.39C).
Etymology: The specific name is derived from the Modder River from where the
fish hosts were collected.
Chapter 5 - The Monogenea 148
Remarks:
Paradiplozoon modderensis resembles both P. ghanense and P. aegyptensis,
but differs from them in the position of the testis and ovaries. In the case of P.
ghanense, the testis and ovary are located completely in the area of fusion and in
P. aegyptensis, the ovaries are also located in the area of fusion and the testis
are located only partially in the area of fusion. The testis and ovaries of P.
modderensis are located completely within the posterior part of the body.
Paradiplozoon modderensis also differs from the other two known species in the
size of the eggs and the haptoral clamps.
Species TL AL AW PL PW CL CW El EW
P. modderensis
n. 2880-4180 1750-2660 550-1290 1110-1510 310-570 94-106 41-53 250-388 104-135
P.ghanense
Thomas 1957 3210-3830 1860-2540 540-740 380-480 380-480 120-160 100-110 260 115
P. aegyptensis
Fischthal & Kuntz 3620-5767 1879-3452 299-836 867-1871 130-245 65-79 92-102 81-132 254-313
A
B
bs
Figure 5.36. Microscope projection drawings of Paradiplozoon modderensis n. sp. from the gills of Labeo
capensis (Smith, 1841) collected from the Soetdoring Nature Reserve. A - whole mount. Scale bar: 1mm.
B - buccal suckers, pharynx and esophagus. Scale bar: 20lJm. bs-buccal suckers, ph-pharynx
A
-
B
c
Figure 5.37. Microscope projection drawings of Paradiplozoon modderensis n. sp. from the gills of Labeo
capensis (Smith, 1841) collected from the Soetdoring Nature Reserve. A - clamp, B - crooked anchor, C
- egg. Scale bar: 10lJm. ds-dorsal sclerite, sds-spur of dorsal sclerite, vs-ventral sclerite
=
Figure 5.38. Microscope projection drawings of the reproductive system of Paradiplozoon modderensis n.
sp. from the gills of Labeo capensis (Smith, 1841) collected from the Soetdoring Nature Reserve. Scale
bar: 20lJm. ov-ovary, te-testis, vr-vitteline reservoir
Figure. 5.39. Light micrographs of Paradiplozoon modderensis n.sp. collected from the gills of Labeo
capensis (Smith 1841). A - whole mount, B - clamps, C - egg. Scale bar A: 1mm, B, C: 10IJm
Chapter 6
Chapter 6 - Parasitic Crustacea 153
SlUbc~ass Branchlura ThorelI, 1864
The branchiurans, or commonly known as fish lice, are all parasites of fish from
freshwater, marine, and brackish habitats (Van As & Van As 2001a). Fish lice
occur on the skin and fins, in the branchial chambers and mouth cavities of their
hosts. Both the males and females are parasitic, but some retain the ability to
leave the host and swim freely, which the female must do in order to lay her eggs
(Fryer 1982).
Up to 1854, the Branchiura ThorelI, 1864 was not recognised as a separate
group, but treated as part of the copepods. Since then the taxonomic position of
the group within the Copepoda Milne Edwards, 1840 has changed numerous
times. A brief summary of the milestones is presented below.
• Zenker (1854) questioned the placement of the branchiurans within the
copepods and placed the group within the Phyllopoda.
~ ThorelI (1864) suggested the name Branchiura for organisms which display
characteristics of the group. He also suggested that these characteristics
show similarities with the cladocerans.
e Claus (1875) again placed the Branchiura within the Copepoda, based on a
comprehensive study on the development of the larvae, as well as the
anatomy and morphology of the group.
~ Wilson (1902) accepted the classification of Claus (1875). The characters of
the appendages, proboscis and ovary are perceived as evidence for the
separation of the Argulidae from the class Branchiopoda, and are
subsequently placed within the Copepoda.
~ Grobben (1908) suggested that the ovary might have a paired origin, in
contrast with Wilson (1902), which suggested that the ovary is single.
Chapter 6 - Parasitic Crustacea 154
~ Martin (1932) confirmed the paired origin of the ovary and also showed that
the compound eye differs completely from that of the copepods. Martin also
showed significant differences with the Cladocera, and elevated the
Branchiura to the level of subclass under the Crustacea.
~ Yamaguti (1963b) reviewed the subclasses Branchiura and Copepoda, and
divided the Branchiura into two families, the Dipteropeltidae Yamaguti, 1963
and Argulidae Muller, 1785 and placed both in the order Argulidea. The
Argulidae is further divided into three subfamilies, namely Argulinae
Yamaguti, 1963, Chonopeltinae Yamaguti, 1963 and Dolopsinae Yamaguti,
1963.
~ Fryer (1969) rejected the classification of Yamaguti, mainly because major
similarities of the subfamilies are not recognised.
Presently, the Branchiura is classified as a subclass of the Maxillopoda Dahl,
1956, and comprise of a single family, the Argulidae (see Table 6.1). Some
authors still recognise the Dipteropeltidae, but this is not widely accepted.
SuIbC~a1ss: IBIT'a1nclhoura ThorelI, 1864
Order: ArglUioida Rafinesque, 1815
Family: ArguHdae Muller, 1785
The Argulidae comprise of four genera, namely Argulus Muller, 1785, Dolops
Audouin, 1837, Chonopeltis Thiele, 1900 and Dipteropeltis Calman, 1912.
According to Van As & Van As (2001a) the genera are distinguished from each
other on the form of the maxillules, which are either formed into hooks (in the
case of Dolops) or suckers (in the case of Argulus and Chonopeltis). The
presence or absence of a mouth tube and stylet as well as characteristics of the
antennule and antennae are used to differentiate between Argulus and
Chonopeltis. Only one species of Dipteropeltis is known, which was described
only from the female and has not been recorded since the original description
from South American waters (Van As & Van As 2001a). The genus Dolops is
Chapter 6 - Parasitic Crustacea 155
represented by 11 species of which only Dolops ranarum Stuhlman, 1891 has a
pan-African distribution. Fourteen species of Chonopeltis are known from African
freshwater habitats. The genus is also endemic to Africa. Nearly 150 species of
Argulus are known worldwide, most of them from freshwater habitats (Rushton-
Melior 1994). At least 35 species have been described from Africa.
The genIUs Argulus Muller, 1785
Generic diagnosis
Carapace trifoliate with distinct anterior lobe. In some cases carapace covers
whole cephalothorax, in others only the first two legs are covered. Respiratory
areas of two to three differentiated areas situated ventrally on lateral carapace
lobe. Paired antennules consist of two segments, with terminal segment ending
in a sclerotized hook. Maxillules present as hooks in larval form, which develops
into large suckers. Maxillae with four podomeres. Basal plate covered by scales
and spines with posterior and anterior projections. Stylet anterior to extended
mouth tube. Spermatophore absent (Van As & Van As, 2001a).
Species of Argulus known from South Africa
Extensive research has been done on the genus Argulus in South Africa by
authors such as: Kruger, Van As & Saayman (1983), Avenant-Oldewage &
Swanepoel (1993), Van As & Van As (1993), Avenant-Oldewage (1994),
Avenant-Oldewage & Oldewage (1995), Lutsch & Avenant-Oldewage (1995),
Van As & Van As (1999), Van As, Van Niekerk & Olivier (1999), Van As & Van
As (2001a), Van As & Van As (2001b), Van As, Van As, Christison & Cyprus
(2001).
Six species of Argulus have been recorded from South Africa, with four of these
from marine habitats. The remaining two species are freshwater species, namely
A. japonicus Thiele, 1900, which is an introduced species and A. capensis
Barnard, 1955 described from Sandelia capensis (Cuvier, 1829) by Barnard
(1955) from the western Cape rivers. This description, however, was based on a
Chapter 6 - Parasitic Crustacea 156
single female specimen, and has not been recorded since the original
description.
Subclass Copepoda Milne Edwards, 1940
Parasitic cope pods have a variety of body forms and hosts, including freshwater
and marine fishes, as well as invertebrates such as tunicates and polychaetes.
According to McLaughlin (1980) some species display great diversity in body
forms, and it is often difficult to recognise the adult parasite as a copepod.
In many species it is only the female that has undergone extensive morphological
change and is parasitic, while the male remains free-living and retains a
unmodified copepad appearance. The life cycle of copepods involves young that
hatch as nauplius larvae. There are usually five or six naupliar stages, which is
followed by four copepodite stages before adulthood is reached (McLaughlin
1980).
According to Huys & Boxshall (1991) the diversity of body form and biology of the
copepods lead to considerable confusion among early systematists. Due to this
confusion, parasitic forms and free-living forms were classified in separate higher
taxa. Thoreli (1859) recognised the affinity between free-living and parasitic
copepods and this marked the beginning of the search for a natural system of
phylogenetic relationships of the Copepoda (Huys & Boxshall 1991). Due to the
large number of classification schemes that have been proposed, (they will not all
be discussed here) a brief summary is presented below (adapted from Huys &
Boxshall 1991).
~ The classification systems of Latreille (1802), Lamarck (1818), Milne Edwards
(1840), Dana (1846, 1848), Baird (1850), Zenker (1854) and Claus (1857) all
placed the copepods in various orders and subclasses of the Crustacea, but
neither of them considered the free-living and parasitic forms in the same
group.
Chapter 6 - Parasitic Crustacea 157
~ ThorelI (1859) placed free-living and parasitic copepods in a single group for
the first time, and formed three groups based on the oral appendages,
namely the Gnathostoma ThorelI, 1859, Poecilostoma ThorelI, 1859, and
Siphonostoma Thoreli, 1859.
~ Claus (1863) adopted the name Copepoda for the Entomostraca and divided
the copepods into the Copepoda Carcinoidea which comprises the free-living
forms, as well as the temporary parasites, and the Copepoda Parasitica
which comprised the species with modified bodies, which are permanent
parasites.
~ Gerstaecker (1866-1879) recognised that semi-parasitic and parasitic families
do not belong in the same group and suggests lineages leading from free-
living forms to commensals and semi-parasites, to highly evolved parasites.
c Giesbrecht (1882) rejected the use of mouthpart structure and number of
genital apertures, but used tagmosis to divide the copepods into the
Gymnoplea Giesbert, 1882 and Podoplea Giesbert, 1882.
~ Sars (1901) rejected the classification of Giesbrecht, and divided the
Copepoda into seven suborders (Calanoida Sars, 1903, Harpacticoida Sars,
1903, Cyclopoida Burmeister, 1834, Notodelphyoida Sars, 1903,
Monstrilloida, Sars, 1903, Caligoida Sars, 1903 and Lemaeoida Sars, 1903)
based on seven genera, which Sars believed to be representing types of
copepods.
~ Calman (1909) classified the Copepoda as a subclass of the Crustacea, but
continued to include the Branchiura as an order.
~ Wilson (1910) supported the Sarsian system, but suggested the transfer of
the Lemaeidae Cobbold, 1879 to the Caligoida.
e Brehm (1927) combined the best characteristics of the systems of Giesbrecht,
Sars and Wilson.
~ Oakley (1930) pointed out flows in the Sarsian scheme regarding the
Lernaeoida, but suggests a few other alterations, including a new subdivision
of the Copepoda into the Cyclopiformes Oakley, 1930 and the Caligiformes
Oakley, 1930.
Chapter 6 - Parasitic Crustacea 158
e Gurney (1933) established a new order, the Misophrioida Gurney, 1933,
which contained the Misophriidae Brady, 1878.
~ Monod & Dolfuss (1932) adopted the system proposed by Oakley (1930),
were the Cyclopiformes contained the orders Monstrilloida, Calanoida,
Harpacticoida, Cyclopoida and Notodelphyoida, and the Caligiformes
contained the families Caligidae Burmeister, 1835, Dichelesthiidae Dana,
1853, Sphyriidae Wilson, 1919, Lernaeidae, Lernaeopodidae Olsson, 1869,
Choniostomatidae and the Herpyllobiidae Hansen, 1892.
e Wilson (1932) recognised seven suborders of true copepods, namely the
Calanoida, Harpacticoida, Cyclopoida, Notodelphyoida, Monstrilloida,
Caligoida, Lernaeopodoida and included the Branchiura as the suborder
Arguloidea.
~ Heegard (1947) suggested that evolutionary radiation in all directions had
taken place from the Cyclopoida, towards the other suborders, as well as the
parasitic copepods. He divided the parasitic copepods into the Pectinata and
Fisculata, based on the structure of the mandibles.
~ Lang (1948) challenged the Sarsian system with the rejection of the
Notodelphyoida, and suggested that the Copepods should be divided into four
suborders, the Progymnoplea Lang, 1948, Gymnoplea, Propodoplea Lang,
1948, and the Podoplea. The system of Lang contained most of the elements
of modern copepod classification, but did not consider parasitic copepods in
detail.
~ Yamaguti (1963b) placed parasitic copepods on vertebrate hosts in six
orders, i.e. the Cyclopidea Yamaguti, 1963, Lernaeopodidea Yamaguti, 1963,
Andreinidea Yamaguti, 1963 , Philichthyidea Yamaguti, 1963, Sarcotacidea
Yamaguti, 1963 and the Caligidea Stebbing, 1910.
~ Kabata (1979) recognised two lineages, namely Gymnoplea and Podoplea
and produced a comprehensive classification of the Copepoda, based on a
reassessment of parasitic copepods of fishes. He also placed the fish
parasite families in the appropriate orders.
Chapter 6 - Parasitic Crustacea 159
e Boxshall (1979) established a new order of Podoplea, the Mormonilloida
Boxshall, 1979.
ó Marcotte (1982) concluded that the ancestral copepod was benthic or
semibenthic. He considered the evolution of the Cyclopoida,
Poecilostomatoida ThorelI, 1859, and Siphonostomatoida ThorelI, 1859 into
planktonic and parasitic habitats to be the final great radiation.
~ Fosshagen & lliffe (1985) established a new order within the Gymnoplea,
namely the Platycopioida Fosshagen, 1985.
~ Starobogatov (1986) proposed a classification scheme of the Crustacea,
which differed entirely from the other schemes. The principle on which his
system is based was criticised by Boxshall & Huys (1989).
~ Boxshall (1986) proposed a phylogenetic system for copepod orders, based
on the work of Kabata (1979).
~ Huys (1988) introduced a separate order within the Podoplea, the Gelyelloida
Huys, 1988.
~ Ho (1990) considered ten orders in a phylogenetic analysis of the Copepoda,
using cladistic methods, and generated a consensus tree showing the
phylogenetic relationships of the orders.
~ Huys & Boxshall (1991) proposed a new classification system for the
Copepoda (Table 6.1). In this system, the phylogenetic relationships of the
orders are based on an analysis of 54 morphological characters.
Chapter 6 - Parasitic Crustacea 160
Cyclopoida Burmeister, 1834
Copepoda Neocopepoda Podoplea Giesbrecht, 1882 Poecilistomatoida ThorelI, 1859
MiJne Edwards, 1840 Huys & Boxshall, 1991
Chapter 6 - Parasitic Crustacea 161
Siphonostomatoida ThorelI, 1859
Chapter 6 - Parasitic Crustacea 162
SlLBlbc~ass:Copepoda Milne Edwards, 1840
mfraclass: Neocopepodla Boxshall & Huys, 1991
superorden Podoplea Giesbrecht, 1882
Order: Cyclopoidla Burmeister, 1834
Family: Lernaeldae Cobbold, 1879
Six genera of lernaeids are found parasitic on fish namely Lamproglena
Nordmann, 1832, Lernaea Linnaeus, 1758, Lernaeogiraffa Zimmermann, 1922,
Dysphorus Kurtz, 1924, Afrolernaea Fryer, 1956 and Opistholernaea Yin, 1960
(Paperna 1979b). The differentiation between lernaeid genera is based on the
morphology of the parasitic females. In all genera, except Lamprogiena, the
head of the adult female is embedded in the tissue of the host. The head is
armed with symmetrical protuberances, the head and "neck" is elongated and the
swimming legs are degenerated.
The genus Lamproglena is specialised for attachment to the host's gills by
means of spines on the maxillae and maxillipeds. Members of this genus retain
a recognisable copepad appearance, as well as partial segmentation. The
thoracic legs are rudimentary and the most posterior legs are absent (Paperna
1979b).
The Genus Lamproglena Nordmann, 1832
Generic Diagnosis
The body can be divided into three distinct regions, namely cephalothorax, leg-
bearing thoracic segments and abdomen. Cephalothorax is partially separated
from the first leg-bearing thoracic segment. First and second leg-bearing
thoracic segments form a distinct neck. Third and fourth thoracic segments form
an incipient trunk (Dippenaar, Luus-Powell & Roux 2001). Fifth thoracic segment
separates genital complex from anterior thoracic segments by a waist-like
constriction. Abdomen consists of three segments. Antennae with varying
Chapter 6 - Parasitic Crustacea 163
numbers of setae and maxillipeds are tipped with one to five claws. Thoracic
legs may be distinctly or indistinctly segmented (Dippenaar et al. 2001). Caudal
rami are longer than wide and each are tipped with spines (Yamaguti 1963b).
Species of Lamproglena Nordmann, 1832 known from Africa
Currently, there are 37 species of Lamproglena known worldwide, of which 13
have been reported from Africa. Two of these species were described from the
Red Sea, namely L. hemprechii Nordmann, 1832 from Myletes dentex (Linnaeus,
1758), and L. lichiae Nordmann, 1832 from Scomberoides Iysan (Forsskál, 1775)
by Nordmann (1832).
Almost a century later Zimmerman (1923) described L. werneri Zimmermann,
1923 from Bagrus bajad, from the Nile River. Wilson (1928) described another
species from the White Nile and the Red Sea, namely L. angusta Wilson, 1928
from the gills of the electric catfish, Malapterurus electricus (Gmelin, 1789).
Capart (1944) described L. monodi Capart, 1944 from hosts of the genera
Hemichromis Peters, 1858 and Haplochromis Hilgendorf, 1888. Fryer (1959),
however, synonymised this species with L. nyasea Fryer, 1956 which was
described from Lake Nyasa, Zimbabwe. Fryer (1956) described L. clariae Fryer,
1956 from Lake Nyasa, from the gills of Clarias gariepinus.
Capart also described two species in 1956 from Sudan i.e. L. elongata Capart,
1956 from Citharinus citharus (Geoffroy St. Hilaire, 1809), and L. wilsoni Capart,
1956 from Ciarotes laticeps (Ruppell, 1829). In the same year Capart reported L.
monodi also from Sudan, but from Ti/apia gali/aea (Linnaeus, 1758). In 1957,
Humes (1957) described L. cleopatra Humes, 1957 from Egypt, from the gills of
Labeo forskalii.
During 1960, Dollfus described L. aubentonii Dollfus, 1960 from Hydrocynus
brevis (Gunther, 1864), from Niger, but this species was synonymised with L.
hemprechii by Fryer (1968). In 1961 Fryer described a species from Barbus
Chapter 6 - Parasitic Crustacea 164
a/tiana/is radc/iffi Boulenger, 1903 from Lake Victoria, namely L. barbico/a Fryer,
1961 as well as two known species, namely L. monodi from species of
Hap/ochromis and Ti/apia and L. c/ariae from Heterobranchis /ongifi/is.
In a publication of parasitic crustaceans of cichlid fishes of Africa from the Musée
Royal de L'Afrique Centrale in Belgium, Fryer (1963) reported L. monodi from a
wide range of Ti/apia species.
The next year Fryer (1964) described L. intercedens Fryer, 1964 from the gills of
Citharines species from Ghana. Fryer (1965) described another species, namely
L. cornuta Fryer, 1964 from Heterobranchus bidorsa/is Geoffroy Saint-Hilaire,
1809 and also reported L. c/ariae collected from the gills of C/arias gariepinus,
both from the Nile River.
In 1967 Fryer published another report of parasitic copepods from cichlid fishes
from the Musée Royal de L'Afrique Centrale. This report, however, mainly
covered the genera Hap/ochromis, Hemichromis and Pseudocreni/abrus, which
were infested with L. monodi.
In the mid seventies, Shatter (1977) reported five known species of Lamprog/ena
from Nigeria, namely L. c/ariae from C/arias anguillaris (Linnaeus, 1758), L.
hemprechii from the gills of A/estes nurse (Ruppell, 1832), L. monodi from Ti/apia
ga/i/aea, L. werneri from Auchenog/anis occidentalis (Valenciennes, 1840) and L.
wilsoni from Chrysichthys nigrodigitatus (Lacepéde, 1803).
Douëllou & Erlanger (1994) reported two known species collected from Lake
Kariba, namely L. hemprechii from Hydrocynus vittatus (Casteinau, 1861) and L.
monodi, which were present on all the cichlid fishes examined.
Chapter 6 - Parasitic Crustacea 165
During 2001, Dippenaar et al. described a species from two Labeobarbus hosts
in South Africa, namely Lamproglena hoi Dippenaar, Luus-Powell & Roux, 2001
from Labeobarbus marequensis and Labeobarbus polylepis (Boulenger, 1907).
According to Dippenaar et al. (2001), four other species of Lamproglena have
been reported from southern Africa, namely L. monodi, L. clariae, L. barbicola
and L. cornuta.
Piasecki (1993) stated that L. hemprechii and L. lichiae propably were described
from fishes deposited the Berlin Museum. The hosts reported for L. hemprechii,
are all freshwater Hydrocynus species and were probably collected from the Nile
River. If the host reported for L. lichiae (Lichia aculeata = Scomberoides lysan) is
indeed correct, this would mean that L. lichiae is a marine species and would be
an exception amongst the other species of LamprogIena.
The African species of LamprogIena, the hosts and their distribution is
summarised in Table 6.2. In Table 6.3 the distinguishing characters of the
African species are summarised.
Chapter 6 - ParasiticCrustacea 166
Ma/apterurus e/ectricus (Gmelin, 1789) Nile River
Barbus a/tianalis radcliffi Boule 1903 Lake Victoria
Lake Nya ,Lake Victoria,
Ma and the White Nile
Heterobranchus bidorsalis Geoffroy Saint-Hilaire,
1809 Nile River southern Africa
Sudan
(Casteinau, 1861), H. forskalii (Cuvier, Zimbabwe, Ghana, Niger and Red
Hepsetus odoe (Bloch, 1794), My/etes dentex Sea
(Linnaeus, 1758)
Citharinus Ghana
Red Sea
Lake Moero, Congo, Zimbabwe,
and Central Africa
L. werner;
Zimmermann, 1923 Galma and Nile River
Chrysichthys
Sudan
Dippenaar, Luus- Labeobarbus marequensis (Smith, 1841), South Africa
Powell & 2001 Labeobarbus nnll,lt:>n,j",
Chapter 6 - Parasitic Crustacea 167
Total length: 6.5mm
Antennule: Fringe of spines on anterior margin near distal end. Terminal joint supplied
Lamproglena with setae
angusta Antennae: Four segmented with two setae on terminal segment
Wilson, 1928 Maxillae: Swollen basal segment and terminal spine
(Figure 6.1A-G) Maxilliped: Armed with three terminal claws and accessory spine on inner margin
Legs: Pairs 1-4 biramous, each ramus consisting of two segments and
terminati in two
Total length: 5mm
Antennule: Reduced to two distinct and one indistinct segment. Basal segment lacking
L. barbicola anterior fringe of setae
Fryer, 1961 Antennae: Four segmented, basal segment crowned with distal spinules
(Figure 6.1 H-M) Maxillae: Long with single spine
Maxilliped: Armed with three recurved distal claws
Pairs 1-4 similar allbiramous with reduced setation
Total length: 9mm
Antennule: Two segmented, basal segment with margin of reduced setae on preaxial
margin, terminal segment with four reduced setae and small preaxial seta
L. clariae Antennae: Two segmented, distal segment with two small papillae and three reduced
Fryer, 1956 setae
(Figure 6.2A-F) Maxillae: Two distal chitinized spines
Maxilliped: Armed with three recurved chitinized claws
s Pairs 1-4 biramous with no n of on and reduced setation
Total length: 2.6mm
Antennule: Swollen basal podomere and small distal podomere, both with naked setae
L. cleopatra Antennae: Indistinctly four segmented, with five small setae on terminal segment
Humes,1957 Maxillae: Terminal spine projecting through thin transparent covering layer
(Figure 6.2G-K) Maxilliped: Armed with three curved claws
Legs: Pairs 1-4 biramous with each ramus indistinctly two segmented.
E of all in blunt setae
otallength: 11mm
Antennule: Large and conspicuous, indistinct segmentation with few short setae on
L. cornuta anterior margin and distal seta
Fryer, 1965 (Figure Antennae: Two segmented, almost unarmed
6.3A-F) Maxillae: Stout with single spine
Maxilliped: Armed with single claw and rounded fleshy lobe
s: Pairs, 1-4 biramous with mentation almost absent
Total length: 4.5mm
L. e/ongata Antennule: Two segmented with numerous setae on terminal segment
Capart 1956 (Figure Maxilliped: Armed with five terminal claws
Chapter 6 - Parasitic Crustacea 168
Total length: 4.79mm
Antennule: Heavily sclerotized without setation
L. hemprechii Antennae: Four segmented, basal segment with short blunt outgrowth, distal segment
Nordmann,1832 with at least three setae
(Figure 6AA-D) Maxillae: Strongly inclined to basal part, with single sharp spine
MaxiIIi Armed with three terminal claws
Total length: 3mm
Antennule: Indistinctly two segmented, with 22 setae on basal segment and nine setae
on distal segment
L. hoi Antennae: Indistinctly four segmented, second segment with 8-10 setae, terminal
Dippenaar, Luus- segment with four setae on inner margin, five setae on distal margin
Powell & Roux, 2001 Maxillae: Two segmented ending in single spine
(Figure 6.6D-H) Maxilliped: Two segmented, armed with three claws, one with spine-like extension
Legs: Pairs 1-4 biramous with three segmented exopod and two segmented
end
Total length: 5mm
Antennule: Two segmented, reflexed dorsally with numerous setae
L. ;nfercedens Antennae: Same as antennule
Fryer,1964 Maxillae: Stout with single spine
(Figure 6.4E-J) Maxilliped: Armed with five recurved claws
Legs: Pairs 1 & 2 large and conspicuous, directed outward and backward. Pairs
3 & 4 small with reduced setation
Total length: 3.9mm
Antennule: Delicate with two small terminal setae
L.lichiae Antennae: Three segmented with round-tip process on anterior margin of basal
Nordmann, 1832 segment with five short spines
(Figure 6.5A-C) Maxillae: Single sharp spine
Maxil Armed with three terminal claws
Total length: 3.6mm
Antennule: Two segmented, basal segment with numerous setae on preaxial margin,
L. monad; distal segment with single preaxial seta and tuft of short terminal seta
eapart, 1944 Antennae: Two segmented
(Figure 6AD-H) Maxillae: Long with two distal spines
Maxilliped: Armed with three claws
Pairs 1-4 biramous with indistinct mentation reduced setation
No information available
Total length: 4.0mm
Antennule: Two segmented, terminal segment much reduced, external border with row
of setae
Maxill Armed with three claws
A B
c D
E
G ~
F "
H
J K
l M
FiQlure 6.1. Diagrammatic drawings of Lamproglena Nordmann, 1832 species. A-G - L. angusta Wilson,
1928 (redrawn from Wilson 1928). A - antennule, B - antenna, C - maxillae, D - maxilliped, E -leg I, F-
leg II, G -leg Ill. H-M - L. barbicola Fryer, 1961 (redrawn from Fryer 1961). H - antennule, 1-antenna, J
- maxillae, K - maxilliped, l-Ieg II, M - furcal rami. Scale bar: 300IJm
A B
c D
E IF
G H
J
••• r-
'. :.~.:.;.:.;::::~/~.,
. ":~
....
.' :.;:
IK
Figure 6.2. Diagrammatic drawings of Lamproglena Nordmann, 1832 species. A-F - L. etertee Fryer,
1956 (redrawn from Fryer 1956). A - antennule, B - antenna, C - maxillae, D - maxilliped, E -leg II, F-
furcal ramus. G-K - L. cleopatra Humes, 1957 (redrawn from Humes 1957). G - antennule, li- antenna,
I - maxillae, J - maxilliped, K - furcal ramus. Scale bar: 100(Jm
B
A
c D
E IF
G H
J VNJ. -
Figur~'I6.3. Diagrammatic drawings of Lamproglena Nordmann, 1832 species. A-F - L. cor~~t~"'Fryer,'I!
)965 (redrawn from Fryer 1965). A - antennule, B - maxillae, C - maxilliped, D - legl, le -leg II. F-
furcal rami. G-J - L. elongata Capart, 1956 (redrawn from Capart 1956). G - antenuie, H ..;m.. ,),(III~-r1! -
maxilliped, J - furcal rami. Scale bar: 100~m '.
A B
c D
E IF
G IHI
J (">:.~A·:;·~il
~
Figure 6.4. Diagrammatic drawings of Lamproglena Nordmann, 1832 species. A-I[) - L. hemprechii
Nordmann, 1832 (redrawn from Piasecki 1993). A - antennule, B - antenna, C - maxillae, D - maxilliped.
E-J - L. inter cedens Fryer, 1964 (redrawn from Fryer 1964). le - antennule, F - antenna, G - maxillae
and maxilliped, H - leg II, I - leg Ill, J - furcal rami. Scale bar A-D: 3001Jm, E,F: 3001Jm, G: 500lJm, H:
50lJm, I,J: 10IJm
A €...
c
n lE
IF G
=
1. .".1. .,.
=
Figure 6.5. Diagrammatic drawings of Lamproglena Nordmann, 1832 species. A-C - L. lichiae
Nordmann, 1832 (redrawn from Piasecki 1993). A - antennule and antenna, IB- maxillae, C - maxilliped.
D-H - L. monodi Capart, 1944 (redrawn from Fryer, 1956). 0 - antennule, E - maxillae, F - maxilliped, G
-leg I, H - furcal ramus. Scale bar A-C: 300lJm, D-H: 100IJm
A B AIV«·~~
c
D E
F G
HI
Figure 6.6. Diagrammatic drawings of Lamproglena Nordmann, 1832 species. A-C - L. wilsoni Capart,
1956 (redrawn from Capart 1956). A - antennule, B - maxillae, C - maxilliped. Scale bar: 100j..lm. D-H-
L. hoi Dippenaar, Luus-Powell & Roux 2001 (redrawn from Dippenaar, Luus-Powell & Roux 2001). 0-
antennule, E - antenna, F - maxillae, G - maxilliped, H - furcal rami. Scale bar: 50j..lm
Chapter 6 - Parasitic Crustacea 175
Parasitlc Crustacea from Soetdoring Nature Reserve
Two species of parasitic crustaceans were collected from fishes of the
Soetdoring Nature Reserve. These included representatives of the Branchiura
as well as the Copepoda.
An Argulus sp. was collected from the skin of Cyprinus carpio, Labeo capensis,
L. umbratus, and Labeobarbus kimberleyensis and a Lamproglena sp. was
collected from the gills of Clarias ga riepin us.
Argulus sp, A
Host and locality: Cyprinus carpio, Labeo capensis, L. umbratus and
Labeobarbus kimberleyensis Soetdoring Nature Reserve, South Africa (280 52'
S, 2600' E)
Infestation Site: Skin
Specimens studied: Morphometric measurements made using light microscopy.
Reference material (V2001/06/13-01, V2001/06/18-05, V2001/07/19-10,
V2001/11/23-01) deposited in the collection of the Aquatic Parasitology Study
group, University of the Free State.
Description:
Adult female: Body stout, 5.9mm long posterior margin of carapace extending
posteriorly to cover fourth leg (Figure 6.7A, Figure 6.9A). Carapace comprising
78% of total length. Lateral lobes of carapace rounded, separated by a U-
shaped sinus more than 1/3 length of carapace (36%). Paired respiratory area
on ventral side of lateral lobes; small rounded area directly anterior to larger
kidney shaped area. Thorax distinctly four segmented. Abdomen 1.3mm
comprising 22% of total length; width 70% of length; posterior lobes ovoid
separated by narrow sinus 1.6mm long, comprising 43% of total abdomen length.
Paired spermathecae rounded, situated in fused part of abdomen. First segment
of first antennae triangular with spinous medial projection. Second segment with
Chapter 6 - Parasitic Crustacea 176
anterior and posterior directed projections, terminates in robust ventrally directed
hook (Figure 6.7B, Figure 6.9B). Third and fourth segments slender with
numerous terminal setae (Figure 6.7 B). Second antennae five-segmented, coxa
heavily sclerotized with spinous process at posteromedial angle (Figure 6.7C,
Figure 6.9B). Distal four segments less sclerotized with small number of terminal
setae. First maxilla forms large suckers; rim with 40-48 supporting rods,
comprising 5-7 overlapping sclerites (Figure 6.9C). Second maxilla five
segmented (Figure 6.70). Basal plate armed with numerous scales on ventral
surface and three prominent pointed spines (Figure 6.90); terminal segment with
small claw and three short spines; ventral surface of all segments with patch of
scales. First to fourth pair of legs (Figure 6.9E) biramous and nearly equal in
size; flagellum present on legs one and two; pair of elongate projections on
posterior margin of second leg; long plumase setae present on all legs.
Adult male: Body stout 5.1mm long; carapace comprising 78% of total length;
carapace sinus comprising 31% of carapace length. Abdomen short 1.3mm,
comprising 25% of body length; width 69% of length; posterior lobes rounded,
separated by a narrow sinus 1.2mm long comprising 44% of abdomen length.
Paired elongate testis situated in fused part of abdomen and extending
posteriorly past sinus. Cephalic appendages and first two pairs of legs similar to
those of female (Figure 6.8A, B). Accessory copulatory structures on third leg
comprise a sac-like socket situated dorsally, with peg anteriorlyon leg four
(Figure 6.8C, D).
Remarks:
Based on the above description and morphometrical data as well as the key to
species of Argulus provided by Rushton-Mellor (1994), Argulus sp. A can be
identified as A. japonicus (Figure 6.7, Figure 6.8 & Figure 6.9).
This is an introduced species and does not seem to be host specific, as it was
found to infest all cyprinid hosts collected.
ID
Figure 6.7. Microscope projection drawings of Argulus japonicus Thiele, 1900 collected from cyprinid
fishes from the Soetdoring Nature Reserve. A - adult female (dorsal), scale bar: O,Smm, B - first antenna,
scale bar: 0.25mm, C - second antenna, scale bar: 0.5mm, 0 - second maxilla, scale bar: 0.5mm
A
B
c
IJ
Figure 6.8. Microscope projection drawings of AIgu/us japonicus Thiele, 1900 collected from cyprinid
fishes from the Soetdoring Nature Reserve. A, B, C, 0 - adult male (ventral). A -leg I, B - leg II, C - leg
Ill, D -leg IV. Scale bar: 0.5mm
Figure. 6.9. Scanning electron micrographs of Argulus japonicus Thiele, 1900 collected from cyprinid
fishes from the Soetdoring Nature Reserve. A - ventral view of female, B - first and second antennae, C
- sce rites of supporting rods of first maxilla, D - basal plate of second maxilla, E - legs of female (ventral).
Scale bar A, E: 0.5mm, B, D : 0.25mm, C: 0.1mm
Chapter 6 - Parasitic Crustacea 180
Lamproglena sp, A
Host and locality: Clarias gariepinus, Soetdoring Nature reserve, South Africa
(280 52' S, 260 0' E)
Infestation Site: Gills
Specimens studied: Morphometric measurements and drawings made using
SEM micrographs. Reference material (V2001/06/19-04, V2001/09/25-10,
V2001/05/01-01, V2001/11/28-05, V2001/09/20-08) deposited in the collection of
the Aquatic Parasitology Study group, University of the Free State.
Description:
Adult female: Body elongated, 5.3mm long, indistinctly segmented (Figure
6.12A). Abdomen with three segments. Antennule (Figure 6.1~C, Figure 6.12B)
two segmented bearing a row of reduced setae along preaxial margin; terminal
segment with four terminal setae and one preaxial. Antennae two segmented
(Figure 6.10C, Figure 6.12B), terminal segment with two reduced papillae and
three small setae. Maxillae short with wide base, bearing a single spine distally
(Figure 6.1OA, Figure 6.12C, 0). Maxilliped short and robust, terminating in three
,
chitinised claws (Figure 6.10B, Figure 6.120, E). Legs I-IV much reduced; all
biramous, indistinctly segmented. Exopod of leg I (Figure 6.11A) with single seta
at basis, three setae along external margin, two terminal seta; coxa rudimentary
with serrated edge. Exopod of leg II (Figure 6.11 B) with single seta at basis, one
seta on external margin, terminating in three setae; endopod with single seta at
basis. Leg III (Figure 6.11 C) with single seta at basis, two setae on external
margin, one at midlength of leg, one near terminal end. Leg IV (Figure 6.110)
with seta at basis of endopod, single seta on external margin .at midlength of leg,
two terminal setae. Leg V much reduced with three posterior setae (Figure
6.11 E). Caudal rami short, simple with four terminal papillae and one lateral
papilla (Figure 6.11 F, Figure 6.12F).
Chapter 6 - Parasitic Crustacea 181
Remarks:
Based on the above description and morphometrical data Lamproglena sp. A can
be identified as L. clariae (Figure 6.10, Figure 6.11 & Figure 6.12).
Lamproglena clariae is the only species known to infest C. gariepinus. There
are, however, morphological variations between different populations of L. clariae
(Fryer 1964). The population from the Soetdoring Nature Reserve show
similarities to the population described from Lake Nyasa in some characters,
such as the setae on the basis of the endopods. It also share similarities to the
population from Lake Victoria, particularly in the papillae of the furcal rami.
A
Figure 6.10. Microscope projection drawings of adult female Lamproglena clariae Fryer, 1956 from
Clarias gariepinus (Burchell, 1822) collected from the Soetdoring Nature Reserve. A - maxillae, B -
maxilliped, C - antennule and antennae. Scale bar: 100tJm.
A B
E F
Figure 6.11. Microscope projection drawings of aduH female Lamproglena clariae Fryer, 1956 from
Clarias gariepinus (BurchelI, 1822) collected from the Soetdoring Nature Reserve. A - leg I, B - leg II, C
- leg Ill, 0 -leg IV, E - leg V, F - furcal rami. Scale bar: 10IJm
Figure 6.12. Scanning electron micrographs of Lamproglena clariae Fryer, 1956 collected from Clarias
gariepinus (Burchell, 1822) from the Soetdoring Nature Reserve. A - anterior body part, B - antenna and
antennule, C - anterior view of cephalothorax, 0 - lateral view of cephalothorax, E - maxilliped, F - furcal
rami, G - female inbedded in gill filament. Scale bar A: 1mm, B, E, G: 100lJm, C, D, F: 10IJm
Chapter 7
Chapter 7 - Parasite Host Association 185
In this chapter, information on the occurrence of ectoparasites on the fish of the
Soetdoring Nature Reserve during the period of March 2001 to March 2002 is
given. Infestation statistics of different parasite groups is also provided.
Results of fish hosts that were collected and infested with ectoparasites is
presented in Table 7.1. Ciliophoran parasites collected included six trichodinid
species as well as species of the genus Apiosoma (see Chapter 4).
Monogenean parasites collected included gyrodactylid and dactylogyrid
parasites, as well as Paradiplozoon modderensis (see Chapter 5). Although
gyrodactylid representatives were collected, none of these could be described,
either because infestation levels were to low, or not enough individuals could be
successfully retrieved. Two species of parasitic crustaceans were collected, i.e.
Argulus japonicus and Lamproglena clariae (see Chapter 6).
Of the twelve fish species that occur in the Madder River, only eight species were
collected during the study period. This might be attributed to the high rainfall that
occurred during the summer of 2001/2002. During the first survey in March
2001, the water level of the Krugersdrift Dam was estimated at 23%. Due to high
rainfall in the following months and for the remainder of the study, the water level
never dropped below 80%.
Except for Gambusia affinis, all other species of fish examined was found to be
infested with one or more types of ectoparasite. Three specimens of
Labeobarbus kimberleyensis were collected, of which only one specimen was
infested with a single specimen of Argulus japonicus. The fish host most
frequently encountered was Labeo capensis, of which 47 specimens were
collected. Forty of these specimens were infested with ectoparasites. Eighteen
specimens of Labeo umbratus were collected, of which 14 were infested. A total
Chapter 7 - Parasite Host Association 186
of twenty specimens of the introduced carp were collected. Only one of these
specimens was not infested. A single specimen of Ti/apia sparrmanii was
collected. The skin of this specimen was infested with sessiline ciliophorans. A
total of 32 specimens of the other cichlid fish occurring in the Madder River,
namely Pseudocrenilabrus philander were collected. Thirty of these specimens
were infested. Of the 18 specimens of C/arias gariepinus that were collected, 16
were infested with ectoparasites.
The prevalence of the different groups of parasites infesting Labeo capensis is
given in Figure 7.1. The prevalence of trichodinid parasites infesting the gills and
skin of L. capensis was 12.8% and the prevalence of sessiline ciliophorans
infesting the host was 2.1%. Gyrodactylid monogeneans were also found
infesting the skin of L. capensis with a prevalence of 8.5%. The most prevalent
ectoparasites for L. capensis were dactylogyrid monogeneans, which had a
prevalence of 76.6%. These infestations were mainly Dacty/ogyrus freistatensis
and oogie/ius capensis. The diplozoid monogenean Paradip/ozoon modderensis
had a prevalence of 31.9%, with a mean intensity and abundance (Figure 7.2) of
3 and 0.89 respectively.
Chapter 7 - Parasite Host Association 187
100
90
80
ID
0 70c
ID 60
r>o 50
ID 40
I-
a... 30
20
10
0
I/) I/) I/) I/) I/) I/)
u Q) cco u u 'iii ::Jc C > 'CL- c uu 0 ........ >. ID cI/)
0 U
0> L-
I/) sa:. co 0 Cl... Q)£ u u a
O.
u Q)en .Q e ..>.... u .~'C u 0
I- 'u >. co
<9 0 E «
lFigure 7.1. Histogram illustrating prevalence of the different ectoparasites
infesting Labeo capensis (Smith, 1841). P-Paradiplozoon, A-Argulus
3.5
3
Cl)
2 2.5
"(ii
e 2
ctI
0..
......
0 1.5
zei 1
0.5
0
c~>. IDU
CU I/) C
~ID2C CU"C
C C::J
«.0
Figure 7.2. Histogram illustrating mean intensity and abundance for
Paradiplozoon modderensis n. sp.
Chapter 7 - Parasite Host Association 188
Mean intensity and abundance numbers refer to pairs of parasites and not
individual specimens. Figure 7.3 shows the distribution of P. modderensis within
the population of L. capensis. None of the fish were severely infested and the
highest infestation recorded was six parasites. The numbers of parasites were
not influenced by host size. The branchiuran Argulus japonicus had a
prevalence of 8.5% for L. capensis.
7
IJ) 6
.Q...).
(ii 5
,c_a
ca 4
0..._.. 3
0
0 2z 1 0<>
o
o 10 20 30 40
Host length (cm)
Figure 7.3. Scatter plot diagram illustrating the distribution of Paradiplozoon
modderensis n. sp. on specimens of Labeo capensis (Smith, 1841).
Figure 7.4 represents the prevalence of ectoparasites collected from Labeo
umbratus. The prevalence for infestations by both trichodinid and sessiline
ciliophorans was higher than for L. capensis, i.e. 33.3% and 5.6% respectively.
Infestations by gyrodactylid monogeneans had prevalence in the same range as
for L. capensis, i.e. 11.5%, but dactylogyrid prevalence was 55.6%, which is
lower by almost 20%. Argulus japonicus had a prevalence of 22.2% for L.
umbratus, which is almost three times higher than for L. capensis.
Chapter 7 - Parasite Host Association 189
60
50
Q) 40
u
c
Q)
(ij 30
>~
0... 20
10
0
UJ UJ
"0 C UJ UJ UJ
UJ
·ë Q) (Il,2 :!2
"0 ~ u::J
'6 (5 ~ .~ ::J ·ë
0 "(ii ..c: u Ol e"J 0s: UJ (Il 0 a.u Q)
Cf) g
a. <{
"0 ~ .~
ï:= 00 s, u(Il
(9 0
Figure 7.4. Histogram illustrating prevalence of the different ectoparasites
infestinq Labeo umbratus (Smith, 1841).
Figure 7.5 represents the prevalence of ectoparasites for Cyprinus csrpio. For
the cyprinids, the carp showed the highest infestation of trichodinid as well as
sessiline ciliophorans. The prevalence for trichodinids was 65.0%, which is
almost double the prevalence for L. umbratus and five times higher than for L.
capensis. Sessiline ciliophorans had a prevalence of 20.0%, which is almost four
times higher than for L. umbratus and ten times higher than for L. capensis.
Infestations by gyrodactylid monogeneans had a prevalence of 55.0% for C.
carpio, which is also higher than for both L. capensis and L. umbratus. The
prevalence for dactylogyrid monogeneans (55.0%), however, was similar to that
of L. umbratus, but lower than for L. capensis. In the case of C. carpio, however,
these infestations were dominated by Dactylogyrus extensus, which were not
collected from either L. capensis or L. umbratus. Argulus japonicus had a
prevalence of 20.0%, which is similar to that of L. umbratus, but almost double
that for L. capensis.
Chapter 7 - Parasite Host Association 190
70~~~~-------------------------------------.
60
50
Ool
~ 40
ro
~> 30
n, 20
10
o
Cf) Cf) Cf) Cf) Cf)
"C OCl C ".CL: -::J ::J·ë = (Il >- ::J .-(.)'0 Clco Cf).0J::. Co l ..0...
.Jo::.
Cf) c.. «c..
.L: wOl=0 z- .~o
I- ë3 (Ilo
Figure 7.5. Histogram illustrating prevalence of the different ectoparasites
infesting Cyprinus carpio Linnaeus, 1758.
The abundance and mean intensity of A. japonicus for the four cyprinid hosts
collected is compared in Figure 7.6. Abundance of this branchiuran is almost the
same for all four fish hosts. Highest mean intensity was 5.3 for L. capensis and
varied between one to two for the other three cyprinid hosts.
Three groups of ectoparasites were found associated with Clarias gariepinus
(Figure 7.7). The parasites with the highest prevalence were the dactylogyrid
Quadriacanthus aegypticus. This parasite had a prevalence of 77.8%.
Infestations by gyrodactylid monogeneans had a much lower prevalence of only
11.1%. The parasitic copepad Lamproglena clariae had a prevalence of 66.6%.
Mean intensity and abundance of L. clariae is represented in Figure 7.8 and the
distribution of the parasite within the host population in Figure 7.9. Lamproglena
clariae had a mean intensity of 7.6 parasites and an abundance of 5.1.
Distribution of this parasites do not seem to be affected by host length.
Chapter 7 - Parasite Host Association 191
OAbundance
oMean Intensity
2
Figure 7.6. Histogram illustrating the abundance and mean intensity of
Argulus japonicus Thiele, 1900 for the four cyprinid hosts collected. C-
Cvorinus. L-Labeo. Lb-Labeobarbus
90
80
w 70
CcJ 60w 50
Ctl
> 40
I..D_
a... 30
20
1 0
0
CJ) CJ) ID
32 u Ctl
> 'C 'C......- >- Ctl
CJ Cl
Ctl 0 CJ
U
.0._ ..>....-
_j
CJ
>- Ctl
(9 0
Figure 7.7. Histogram illustrating prevalence of the different ectoparasites
infesting Clarias gariepinus (Burchell, 1822). L-Lamproglena
Chapter 7 - Parasite Host Association 192
8
7
en
_ID. 6
"cin..u_ 5
-cu0.. 40 3
0 2
Z
0
M e a n Abundance
intensity
Figure 7.8. Mean intensity and abundance for Lamproglena clariae Fryer,
1956 collected from Clarias gariepinus (Burchell, 1822)
18
6)
16
Gl
14
IJ)
Q)
:!:: 12
IJ) Cl)
ctS Cl 0
'-
octS
10
.,_, 8
0
zei 64
a 0
2
€lO
0
o 50 100 150
Host length (cm)
Figure 7.9. Scatter plot diagram illustrating the distribution of Lamproglena
clariae Fryer, 1956 on specimens of Clarias gariepinus (Burchell, 1822)
The prevalence of ectoparasites for Pseudocrenilabrus philander is presented
in Figure 7.10. Trichodinid infestations by Trichodina centrostrigeata showed the
highest prevalence (84.4%) of all the parasites collected. The sessiline
ciliophorans had a prevalence of 53.1%. Infestation by both gyrodactylid and
Chapter 1 - Parasite Host Association 193
dactylogyrid monogeneans showed low prevalence, i.e. 9.4% and 6.3%
respectively.
100
Q)
u 80c
Q) 60
cu
> 40
Q)
L- 9.4
0... 20
0
CJ) CJ) CJ) CJ)
"C Q)
c ccu :'Q
"C
c
en L- >.....,
·e
"C 0 >.
0 CJ) s: u
0)
.r:. Q) Cl. cu 0
·ue CJ) .Q
"C >
0 ..u...
.
I- ·u L->. cu
CJ 0
Figure 7.10. Histogram illustrating the prevalence of different ectoparasites
infestinq Pseudocrenilabrus philander (Weber, 1897).
The cyprinid hosts collected during the study seem to be more prone to
monogenean infestations than to infestations by ciliophorans. This does not
apply to Cyprinus carpio, for which prevalence of infestation by trichodinids were
higher than monogenean prevalence. Prevalence of dactylogyrid monogeneans
for both Labeo capensis and L. umbratus were higher than gyrodactylid
prevalence. The prevalence of these two families of monogeneans was the
same for Cyprinus carpio. The diplozoid monogenean, Paradiplozoon
modderensis, was collected only from L. capensis and this monogenean appears
to be host specific. Argulus japonicus, which was introduced to South Africa
along with ornamental fish, does not seem to have preference for any of the
cyprinid fish from which it was collected. It did, however, have the highest
prevalence, mean intensity and abundance for L. capensis. The cichlid fishes,
Pseudocrenilabrus philander and Tilapia sparrmanii were more frequently
infested with ciliophorans than with monogeneans. Although only one specimen
of T. sparrmanii was collected, this individual was infested with sessiline
Chapter 7 - Parasite Host Association 194
ciliophorans, but not with any monogeneans. Less than 10% of the specimens of
P. philander were infested with dactylogyrid and gyrodactylid monogeneans.
Clarias gariepinus had the highest prevalence of gyrodactylid monogeneans and
no ciliophorans were collected from this fish host. Species of Quadriacanthus
are confined to siluriform hosts and Q. aegypticus was the only monogenean
species collected from the gills of C. gariepinus. Except for Heterobranchus
longifilis, Clarias gariepinus is the only other known host for the parasitic
copepod, Lamproglena ctariae, which was present on more than 66% of the
specimens collected.
Chapter 8
Chapter 8 - General Discussion 195
Remarks on the parasite and host populatlons
The diversity of fishes present in the Madder River is very low in comparison
to systems such as the Zambezi and even Limpopo and yet not even 70% of
the species were collected from the Soetdoring Nature Reserve. During the
pilot survey of March 2001, the water levels of the Krugersdrift Dam were very
low, and collecting high numbers of fish was done with ease. Seaman et al.
(2001 a) recorded six fish species from the reserve in March 1999, while in
March 2001, Seaman et al. (2001 b) recorded only two species, namely Labeo
capensis and Labeobarbus aeneus. The low numbers as well as the low
diversity of fish collected both by Seaman et al. (2001 b) and during the
present study can be attributed to the high water levels.
The slow flowing, or stagnant water conditions at the different sampling
localities could also have affected the low numbers of Labeobarbus
kimberleyensis, and the absence of L. aeneus and Austroglanis sclateri as
these species prefer fast flowing water. Two of the sampling localities (1 & 2)
(Fig 2.2, Figure 2.40 & Figure 2.4E) were permanently dammed, and there
was very little water flow. When the water level of the dam is low as it was
during the pilot survey there is very little water at locality 3 (Figure 2.4F). After
heavy rainfall, when the water level rises, locality 3 is turned into a fast flowing
rapid and thereby gradually filling the dam, resulting in water pushing back
into this site.
Considerable variation exists in the ectoparasitic fauna of the different fish
species. The ectoparasitic fauna collected from the fishes is summarised in
Figure 8.1-8.4. Cyprinid fishes were mainly parasitised by monogeneans, i.e.
dactylogyrids and gyrodactylids and to a lesser extent by ciliophorans. Carp
were the exception to this, being equally infested by monogeneans and
ciliophorans.
Chapter 8 - General Discussion 196
The dactylogyrid monogeneans collected from Labeo umbratus resemble
Dactylogyrus freistatensis and might well be the same species. Species of
Dactylogyrus known from Labeo are frequently collected from more than one
host species (see Table 5.2). However, in this study it could not be confirmed
that L. umbratus and L. capensis are host to the same dactylogyrid species
due to insufficient numbers of parasites collected from L. umbratus. The
dactylogyrid collected from the gills of C. carpio, i.e. D. extensus was
introduced along with carp, and not collected from the other cyprinids during
this study.
The cichlid species had a much higher prevalence of ciliophorans than
monogeneans, and it appears that ciliophorans are more abundant on smaller
fish specimens.
The parasitic fauna from the gills of Clarias gariepinus is very unique and
differs considerably from the parasites collected from the other fishes.
Quadriacanthus species are only known from siluriform fishes and although a
number of species of this genus are parasitic on Clarias gariepinus, it appears
that these species are host specific (see Table 5.10). During this study, C.
gariepinus was the only host from which parasitic copepods were collected.
The parasitic copepad, Lamproglena clariae also appears to be specific to
siluriform fishes, and has only been recorded from Heterobranchus Iongifiiis
and C. gariepinus (see Chapter 6).
Chapter 8 - General Discussion 197
Figure 8.1. Simplified illustration of the ectoparasites collected from the gills
and skin of cyprinid fishes from the Soetdoring Nature Reserve.
Chapter 8 - General Discussion 198
Cyprinus carpio
Figure 8.2. Simplified illustration of the ectoparasites collected from the gills
and skin of cyprinid fishes from the Soetdoring Nature Reserve.
Chapter 8 - General Discussion 199
Figure 8.3. Simplified illustration of the ectoparasites collected from the gills
and skin of cichlid fishes from the Soetdoring Nature Reserve.
Chapter 8 - General Discussion 200
Clarias gariepinus
Figure 8.4. Simplified illustration of the ectoparasites collected from the gills
of Clarias gariepinus (Burchell, 1822) from the Soetdoring Nature Reserve.
Chapter 8 - General Discussion 201
Pathoqenlclty
Clllophorans
Trichodinid populations often occur in high densities on wild fish populations,
but these infestations rarely cause mortalities (Lam & Dyková 1992). In
populations confined to ponds, tanks or aquaria, trichodiniasis is a frequent
problem. According to Schmidt & Roberts (1977), trichodinids may cause
some damage to the gills of fish, although most have little pathogenic effect.
Trichodinids are commonly accompanied by the presence of other parasites,
and it is usually hard to determine the pathogenic effect that they have on the
hosts (Davis 1947).
Several authors have reported on mortalities of fish as a cause of infestations
by ciliophorans (Paperna 1979b; Van As, Basson & Theron 1984). These
reports included mortalities of catfish, carp, and the Mozambique tilapia,
Oreochromis mossambicus, as a result of infestations by Trichodina species.
The pathogenic action of ciliophorans varies from irritation of surface cells, as
is the case with heavy infestations of ectocommensals, such as sessiline
ciliophorans, to destruction of surface cells and penetration into deep tissue
layers. Heavy infestations result in irritation of the skin integument and gill
epithelium resulting in hyperplasia and later degeneration and necrosis. Sarig
(1971) reported populations of trichodinids on the skin and gills so abundant
that the normal structure of epithelium is not evident.
Sessiline ciliophorans of freshwater fish can cause mortalities due to high
numbers of parasites on the gills of fish and hence cause the suffocation of
the host (Davis 1947; Lom & Corliss 1968; Rogers 1969; Rogers 1971).
Secondary infections by bacteria due to the attachment lesions of sessiline
ciliophorans have also been implicated as another possible cause of fish
mortalities.
Chapter 8 - General Discussion 202
Monogeneans
Unlike the oligonchoineans (which includes the family Diplozoidae), that have
a less destructive manner of attaching and feeding on the host, the
polyonchoineans (including the dactylogyrids) have a more disruptive manner
of feeding and attaching on exposed integument, and cause significant tissue
damage. Members of the Polyonchoinea have been known to cause
significant pathology to their hosts in contrast to the Oligonchoinea, which are
rarely associated with host mortalities (Cone 1995).
Most of the reported cases where dactylogyrids were implicated in mortalities
or severe infestations are from C. carpio cultures. Paperna (1964a) recorded
severe infections by Dactylogyrus vastator from carp stock. Another case of
carp mortalities was reported by Eller (1975) where mortalities of carp in
southern Russia were attributed to two species of Dactylogyrus, namely D.
vastator and D. extensus. According to Van As & Basson (1988) dactylogyrid
monogeneans (possibly of the genus Quadriacanthus) that occur on the gills
of catfish, have caused severe mortalities to catfish fry.
Infested gills have been described to be grey-white in colour, having lost the
natural red colour, were covered in mucous and had an irregular shape
(Paperna 1964b). Gills also showed strong hyperplasia of the gill respiratory
and lining epithelia, as well as the mucous goblets cells. This resulted in
deformations of the gills filaments, especially near the apices. Research
conducted by Buchmann, Slotved & Dana (1993) on the epidemiology of gill
parasite infections of carp, showed that D. extensus embeds itself in the gill
tissue and causes extensive cellular reaction.
Both D. vastator and D. extensus species cause epithelial hyperplasia and
have been responsible for severe losses of both fry and adults (Eller 1975).
Dactylogyrus extensus also causes epithelial cells to degenerate into
secretory cells, resulting in the production of copious amounts of mucous.
Excess excretion of mucous can also result from the method of attachment by
dactylogyrids, where the anchors are inserted into the tissue of the host, as
Chapter 8 - General Discussion 203
well as the movement of the monogeneans (Hwang & Yu 1987). The copious
amounts of mucous that are produced are enough to impair respiratory
functions of the gills (Sauer 1959).
The two species, D. vastator and D. extensus can occur on the same host
and are involved in a unique symbiotic interaction. Paperna (1964b) reported
that competitive exlusion exists between these two species. Gills infested
with D. vastator undergo hyperplasia of the epithelial lining as well as the
mucus goblet cells. These changes create conditions that are unsuitable for
attachment by D. extensus. Pronounced hyperplasia, however, renders the
gills unfavourable even for D. vastator and a decline, or even complete
disappearance of these parasites is seen. After healing of the gills, infestation
by Dactylogyrus species is again possible. An increase in the number of D.
vastator and decline of the other species again takes places. Eventually,
immunity against D. vastator is acquired and fish are again prone to
infestations by other Dactylogyrus species.
Feeding by the monogeneans is also a potential cause of damage. According
to Hwang & Yu (1987) feeding causes gills to bleed, which in turn cause
haemorrhaging and oedema, resulting in respiratory blockage. Cone (1995)
reported that monogeneans might well be mechanical vectors of viral and
bacterial pathogens.
Parasitic crustaceans
The feeding activities of parasitic crustaceans often involve feeding on
shredded host epidermis and branchial epithelium (Schmidt 1975). Parasites
also move around as they feed, stimulating mucus production, epidermal
proliferation and dilation of dermal capillaries. The feeding by species of
Argulus involves the use of the pre-oral sting and legs to abrade the host
epidermis. This causes an increase in the number of mucous cells, and the
production of mucus around the wound. Argulus japonicus however, feeds on
the blood of the host, and may also be responsible for the transmission of
dracunculid nematodes (Moravec, Vidal-Martinez & Aguirre-Macedo 1999).
Chapter 8 - General Discussion 204
The damage by individual branchiurans is seldom reason for alarm, although
heavy infestations by Dolops as well as Argulus have been implicated in fish
mortalities (Fryer 1968; Kruger, Van As & Saayman 1983).
Species of Lamproglena cause variable degrees of damage (Fryer 1968).
Lamproglena monodi causes little damage, with some proliferation of gill
tissue. In the case of Lamproglena clariae however, the proliferation of gill
tissue is immense and in some cases might well interfere with respiration.
This proliferation can be seen in Figure 6.12G, where the specimen seems to
be imbedded into the gills. According to Sproston, Yin & Hu (1950) this
appearance is due to growth of the gill around the parasite and not by
burrowing of the parasite into the gill.
Destruction of gill and skin tissue by ciliophorans, monogeneans and
crustaceans is reflected in the incapacitated condition of the fish, which may
lead to mortalities with an epizootic range. It is important to note however,
that the reported mortalities are a result of fish kept in unnatural conditions,
such as aquaria, fish ponds and other artificial impoundments. However,
extremely high intensity of infestations by ectoparasites was not recorded
from the fishes from Soetdoring Nature Reserve.
Allen Species
Part of the study was to determine if any introduced parasite species are
present in the system. Apart from the two alien fishes that were collected,
three introduced species of parasites were also collected. This includes two
ciliophorans, Trichodina mutabilis and Trichodinella epizootica and the
branchiuran, Argulus japonicus.
Common carp was introduced into southern Africa in the early 1700's. At
least seven alien parasite species, most of which have been responsible for
mortalities of indigenous species was introduced along with the carp (Bruton
& Van As 1987). Apart from the parasites that were introduced with carp, this
species also affects indigenous species by altering the habitat. The feeding
Chapter 8 - General Discussion 205
habits of carp disturb the sediment, decreasing the water quality. Turbidity of
the water is also increased, which may affect the success of predatory fish
species.
Introduced fish species may also compete with indigenous species for food
and space. They may also disrupt breeding patterns and parental care of
offspring (Bruton & Van As 1987). This has already been reported to be the
case for carp. Noble & Hemens (1978) reported that the population of carp in
the Vaal River has reduced the numbers of Labeo umbratus. It could also be
true of the mosquitofish, Gambusia affinis. Deacon, Hubbs & Zahuranec
(1964) studied the effects of introduced fishes on the native fishes of southern
Nevada, North America. They reported that in ponds where G. affinis were
introduced, there has been a marked decline in the number of indigenous fish.
The species of Apiosoma (Apiosoma sp. A) collected from carp during the
study resembles A. piscicola, which is one of the parasite species introduced
with fish. This species was also collected from Pseudocrenilabrus philander
and Tilapia sparrmanii. Although this species has not yet been implicated in
the mortalities of any indigenous fish species the possibility can not be ruled
out that this species could have a pathogenic effect on its hosts when
occuring in high numbers. This has been reported for species of Epistylis
Ehrenberg, 1930 that have been implicated in having extreme pathogenic
effects on the hosts, such as large haemorrahagic lesions (red sore disease)
with erosion of scales and sometimes bones (Rogers & Gaines 1975).
The dactylogyrid, D. extensus, which was collected from the gills of the carp is
a well-known parasite of this fish. It appears that this parasite species is host
specific. Many monogeneans, however, are known to display stenoxenic,
occurring on closely related hosts, or euryxenic specificity, occurring on
distantly related host species. The possibility therefore exists that under
certain conditions, D. extensus could infest the other cyprinids of the
Soetdoring Nature Reserve.
Chapter 8 - General Discussion 206
Two of the introduced parasite species collected were introduced with the
gold fish, Carassius auratus. Argulus japonicus is a serious pathogen of
indigenous fish when they occur in high numbers, which is often the case in
impoundments. This branchiuran is wide spread throughout South Africa and
has been responsible for mortalities of various indigenous fish (Kruger et al.
1983). Trichodina mutabilis is also a known pathogen of fishes introduced
with gold fish. Not only is this the first record of this species from a natural
fish population, but also the first record from an indigenous fish species
(Labeo capensis).
Endoparasites
The initial objective of this project was to include endoparasites as part of the
study. Due to the extent of the systematics and identification of the
endoparasitic helminths, these parasites were not included in the present
study. Fish collected during the study were however, examined for
endoparasites. The fish that were infected with endoparasites are
summarised in Table 8.1.
Table 8.1. Summary of the fish species collected from the Soetdoring Nature
Reserve infested with endoparasites. N-total number of fish collected, NHI-
number of hosts infested, P-number of hosts infested expressed as a
percentage of total number
Fish Host N NHI P Endoparasites
Clarias gariepinus (Burchell, 1822) 18 8 44.4 Nematodes and
Cestodes
Labeobarbus kimberleyensis 3 2 66.6 Cestodes
(Gilchrist & Thomson, 1913)
The cestodes collected from Labeobarbus kimberleyensis were preliminary
identified as Bothriocephalus acheilognathi Yamaguti, 1934. This species
was introduced into South Africa along with grass carp, Ctenopharyngodon
idellus Valenciennes, 1844, which occurs naturally in Japan and China.
Bothriocephalus acheilognathi has spread throughout the subcontinent
through intermediate host copepods (Bruton & Van As 1987). The cestode
infects a wide range of cyprinids and has been responsible for the mortalities
of C. carpio as well as L. kimberleyensis (Brandt, Van As, Schoonbee &
Chapter 8 - General Discussion 207
Hamilton-Attwell 1981; Van As, Schoonbee & Brandt 1981). The infected
specimens of L. kimberleyensis collected during this study were severely
parasitised with high numbers of cestodes removed from the intestine of the
fish host. This parasite could be considered as another threat to the already
vulnerable largemouth yellowfish. Positive identification of the nematodes
from the intestine of Clarias gariepinus was not made. According to Paperna
(1979b) there are two known species of adult nematodes from C. gariepinus,
i.e. Procamallanus laevionchus (Wedl, 1862) and Paracamallanus
cyathopharynx (Baylis, 1923). These nematodes firmly attach to the stomach
mucosa by means of the buccal capsule. Neither of these species, however,
have been reported to have a pathogenic effect.
• , I.
Chapter 9
Chapter 9 - References 208
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Abstract/Opsomming 226
The Soetdoring Nature Reserve is situated on the banks of the Modder River
northwest of Bloemfontein. The Krugersdrift Dam forms part of the reserve
and supplies water to farmers in the lower reaches of the Modder River.
Twelve fish species occur in the Modder River, of which two are introduced
species. Specific objectives of the study was to determine the fish parasite
diversity, and to establish if any introduced fish parasites are prevalent on the
fishes from the Soetdoring Nature Reserve.
During monthly surveys to the Soetdoring Nature Reserve from March
2001 to March 2002 fish were collected from three different localities in the
reserve. A total of eight fish species were collected, although in low numbers.
The parasites collected included ciliophorans, monogeneans and parasitic
crustaceans. Six known species of mobiline ciliophorans were collected from
fishes, i.e. Trichodina centrostrigeata Basson, Van As & Paperna, 1983, T.
heterodentata Duncan, 1977, T. mutabilis Kazubski & Migala, 1968,
Tripartiella /echridens Basson & Van As, 1987, T. /eptospina Basson & Van
As, 1987 and Trichodinella epizootica (Raabe, 1950). Two species of
sessiline ciliophorans were also collected, namely Apiosoma sp. A and
Apiosoma sp. B. Representatives of the Monogenea collected included three
new species, which were described as Dacty/ogyrus freistatensis n. sp.,
Dogie/ius capensis n. sp. and Paradip/ozoon modderensis n. sp. as well as
two known species, i.e. Dactylogyrus extensus (Mueller & Van Cleave, 1932)
and Quadriacanthus aegypticus EI-Naggar & Serag, 1986. The parasitic
crustaceans included one branchiuran species, Argulus japonicus Muller,
1785, and one parasitic copepod, Lamprog/ena c/ariae Fryer, 1956.
This study was first to examine the whole spectrum of ectoparasites
found associated with fish.
Keywords: Freshwater, fish parasites, Ciliophora, Monogenea, Branchiura,
Copepoda, Soetdoring Nature Reserve.
Abstract/Opsomming 227
Die Soetdoring Natuurreservaat is op die oewers van die Modderrivier noord-
wes van Bloemfontein geleë. Die Krugersdriftdam vorm deel van die
reservaat en voorsien water aan boere in die laer streke van die rivier. Twaalf
visspesies kom in die Modderrivier voor, waarvan twee ingevoerde spesies is.
Spesifieke doelstellings van die studie was om die diversiteit van visparasiete
vas te stel, asook om te bepaal of ingevoerde vis parasiete enigsins op die
visse van die Soetdoring Natuurreservaat voorkom.
Tydens maandelikse opnames is vis van drie verskillende lokaliteite by
die Soetdoring Natuurreservaat vanaf Maart 2001 tot Maart 2002 versamel.
Agt visspesies is versamel waarvan die getalle min was. Parasiete wat
versamel is, sluit die volgende in: verteenwoordigers van die Ciliophora,
Monogenea en parasietiese Crustacea. Ses bekende spesies van die
mobiele siliofore is versamel, nl. Trichodina centrostrigeata Basson, Van As &
Paperna, 1983, T. heterodentata Duncan, 1977, T. mutabilis Kazubski &
Migala, 1968, Tripartiella /echridens Basson & Van As, 1987, T. /eptospina
Basson & Van As, 1987 en Trichodinella epizootica (Raabe, 1950). Twee
spesies van sessiele siliofore is ook versamel, nl. Apiosoma sp. A en
Apiosoma sp. B. Verteenwoordigers van die Monogenea sluit drie nuwe
spesies in, nl. Dacty/ogyrus freistatensis n. sp., Dogie/ius capensis n. sp. en
Paradip/ozoon modderensis n. sp., asook twee bekende spesies, nl.
Oacty/ogyrus extensus (Mueller & Van Cleave, 1932) en Quadriacanthus
aegypticus EI-Naggar & Serag, 1986. Verteenwoordigers van die
parasietiese crustasieërs sluit die visluis, Argu/us japonicus Muller, 1775 en 'n
verteenwoordiger van die parasietiese Copepoda, Lamprog/ena clariae Fryer,
1956 in.
Die studie was die eerste om die voorkoms van die hele spektrum van
ektoparasiete wat met visse geassosieer is te bestudeer.
Acknowledgements 228
Acknowledgements
The author would like to express his sincere appreciation and thanks to
the following persons and institutions for their contributions to this
study.
Prof. Jo G. van As and Dr. Liesl L. van As: For their support and patience
throughout my research and write up and for providing me with the
opportunity to be part of the Aquatic Parasitology Research group.
Prof. Linda Basson: For her support and willingness to help whenever she
could.
Johann van As, Candice Jansen van Rensburg, Errol Visagie and the
students of the Aquatic Parasitology Research Group: For their friendship
and assistance with fieldwork and provide help whenever they could.
Kevin Christison: For his friendship and assistance in monogenean
research.
The Department of Zoology & Entomology, University of the Free State,
South Africa: For the use of facilities and support received during
undergraduate and postgraduate studies.
Pierre de Villiers and the Department of Environmental Affairs and
Tourism: For their permission to undertake the project and support during the
study.
The staff of the Soetdoring Nature Reserve: For their assistance during
fieldwork.
National Research Foundation: For the bursary received in support of my
studies.
Ansa Vermaak and my whole family: For their constant support and
assistance throughout my studies.