Luus-Powell_323-329.indd


INTRODUCTION

The Pentastomida represent an ancient taxon, com-
prising some 131 species in seven families (Almeida 
& Christoffersen 1999). Adults of most species in-
habit the nasal passageways and lungs of snakes, 
lizards and crocodilians, while others are found in 
the air sacs of gulls and terns, and in the nasophar-
ynx and sinuses of canids and felids (Bakke 1972; 
Banaja, James & Riley 1975; Riley 1986). Two spe-

cies, Raillietiella bufonis and Raillietiella indica, use 
amphibians as final hosts (Ali, Riley & Self 1982). 
The pentastomid life cycle usually includes a verte-
brate intermediate host in which larvae undergo 
several moults to reach the infective stage (Riley 
1986; Winch & Riley 1986a; Riley & Huchzermeyer 
2000), but insects have been reported as intermedi-
ate hosts of some raillietiellid parasites, while Rei-
ghardia sternae, a parasite of gulls, has a direct life-
cycle (Banaja et al. 1975; Riley 1986).

Two families of pentastomids, Sebekidae and Sub-
triquetridae, use various freshwater fish species as 
intermediate hosts (Fain 1961; Overstreet, Self & 
Vliet 1985; Winch & Riley 1986a, b; Junker, Boomker 
& Booyse 1998). The sebekiid genera, Agema, Alo-
fia, Leiperia and Selfia, have to date only been re-
corded from crocodilian final hosts, but a single 
Sebekia species is also thought to mature in a che-

323

Onderstepoort Journal of Veterinary Research, 75:323–329 (2008)

Pentastomid parasites in fish in the Olifants and 
Incomati River systems, South Africa

WILMIEN J. LUUS-POWELL1*, ANTOINETTE JOOSTE1 and KERSTIN JUNKER2

ABSTRACT

LUUS-POWELL, WILMIEN J., JOOSTE, ANTOINETTE & JUNKER, KERSTIN. 2008.  Pentastomid 
parasites in fish in the Olifants and Incomati River systems, South Africa. Onderstepoort Journal of 
Veterinary Research, 75:323–329

During parasitological field surveys of freshwater fish, sebekiid and subtriquetrid pentastome larvae 
were recovered from the body cavity or swim bladder of several fish species from various localities in 
Limpopo and Mpumalanga Provinces, South Africa. Sebekia wedli was recovered from the body cav-
ity of Marcusenius macrolepidotus (Mormyridae) from Flag Boshielo Dam, Limpopo Province, and 
Alofia sp. and Subtriquetra rileyi were found in the swim bladder of Oreochromis mossambicus 
(Cichlidae) from the Phalaborwa Barrage, Limpopo Province. The latter species was also collected 
from the swim bladder of O. mossambicus in dams in the Phalaborwa region and the Ga-Selati River, 
Limpopo Province. A single specimen of Sebekia okavangoensis was present in the body cavity of 
Clarias gariepinus (Clariidae) in a dam on a sugarcane farm in the Komatipoort region, Mpumalanga 
Province. Pentastomid infections in the Mormyridae and Clariidae represent new host records.

Keywords: Alofia sp., Clarias gariepinus, Marcusenius macrolepidotus, Oreochromis mossambicus, 
Pentastomida, Sebekia okavangoensis, Sebekia wedli, South Africa, Subtriquetra rileyi

* Author to whom correspondence is to be directed. E-mail: 
powellw@ul.ac.za

1 Department of Biodiversity, University of Limpopo (Turfloop 
Cam pus), Private Bag X1106, Sovenga, 0727 South Africa 

2 Department of Veterinary Tropical Diseases, University of 
Pre toria, Private Bag X04, Onderstepoort, 0110 South Africa

Accepted for publication 22 August 2008—Editor



324

Pentastomid parasites in fi sh in Olifants and Incomati River systems, South Africa

lonian host (Dukes, Shealy & Rogers 1971; Riley, 
Spratt & Winch 1990). The sebekiids Diesingia and 
Pelonia, on the other hand, have hitherto been re-
ported exclusively from chelonian final hosts (Sam-
bon 1922; Overstreet et al. 1985; Junker & Boomker 
2002). Adults of the Subtriquetridae are known from 
crocodilians only (Riley et al. 1990).

In South Africa infective larvae of Sebekia wedli, Lei-
peria cincinnalis and Subtriquetra rileyi have been 
reported from the cichlids Tilapia rendalli (redbreast 
tilapia) and Oreochromis mossambicus (Mozam-
bique tilapia) from the Phabeni Dam in the Kruger 
National Park (KNP) (Junker et al. 1998). Junker, 
Boomker & Bolton (1999) recorded the Nile croco-
dile, Croco dylus niloticus, as the definitive host of S. 
wedli and L. cincinnalis, as well as of Alofia nilotici, 
Alofia sim psoni, Sebekia cesarisi and Sebekia oka-
vango ensis in South Africa. The final host of S. rileyi 
is as yet unknown. The pentastomid parasites in-
cluded in this publication are products of a number 
of parasitological studies on freshwater fish from 
sev eral local ities in two provinces of South Africa.

MATERIALS AND METHODS

During fish health surveys, a total of 1 047 fish, be-
longing to 14 species were collected at nine locali-
ties in South Africa and examined for parasites 
(Tables 1 and 2).

Fish were captured using gill nets of stretched mesh 
sizes, ranging from 30–120 mm, and transported 
live to the field laboratory where they were kept in 
con tainers with well aerated water. Immediately be-
fore dissection, fish were killed by decapitation. En-
cysted larvae were removed from their cysts and 
placed in water to unfold. In order to prevent them 
from contracting, they were fixed by adding small 
quantities of 70 % ethanol to the water over a period 
of approximately 1 h, after which they were trans-
ferred to 70 % ethanol.

Pentastomids were mounted and cleared in Hoyer’s 
medium for identification. Measurements were tak-
en from whole mounted specimens according to the 
schematic layout proposed by Riley et al. (1990). 
Hook and oral cadre morphology, combined with 
the number of annuli, were used as identification 
criteria.

The ecological terms prevalence, mean intensity 
and abundance are used in accordance with Bush, 
Lafferty, Lotz & Shostak (1997). Standard deviation 
was not calculated, since too few specimens were 

collected which renders standard deviation values 
meaningless (Rózsa, Reiczigel & Majoros 2000).

RESULTS 

Pentastomid larvae were encountered at four locali-
ties in the Olifants River drainage system in Limpopo 
Province (Table 2). Eight encysted infective S. wed-
li larvae were collected from the body cavity of five 
of 29 Marcusenius macrolepidotus (Mormyridae) 
(bulldog) in Flag Boshielo Dam, constituting a new 
intermediate host record for this parasite. While a 
single cyst was located on the swim bladder, the 
remainder were found between fat deposits on the 
mesenteries. Cysts had a yellowish colour and close-
ly resembled those of Clinostomum metacercariae, 
although slightly smaller in size. No free-living lar-
vae were detected in the swim bladder. The preva-
lence of infection was 17.2 %, with a mean intensity 
of 1.6 (range 1–3) and an abundance of 0.3.

Subtriquetra rileyi was free-living in the swim blad-
der of O. mossambicus from dams in the PIC region. 
The prevalence of infection was 6.3 %, the mean in-
tensity 1.9 (range 1–6) and the abundance 0.1. No 
pentastomid larvae were recovered from sharptooth 
catfish, Clarias gariepinus (Clariidae), the only other 
host examined at these sites at the time (Table 2).

At the Phalaborwa Barrage, S. rileyi, and a total of 
three infective larvae of an Alofia sp. were recov-
ered from O. mossambicus. Concurrent infections 
of S. rileyi and Alofia sp. occurred in two hosts, with 
the former moving freely in the swim bladder while 
the Alofia sp. was encapsulated. Combined, the two 
species had a prevalence of 30 %, a mean intensity 
of 2.4 (range 1–5) and an abundance of 0.7. Clarias 
gariepinus and Labeo rosae (Cyprinidae) examined 
at this site harboured no pentastomid larvae (Table 
2). This is the first published record of an Alofia spe-
cies from fish intermediate hosts in South Africa.

In the Ga-Selati River, three S. rileyi larvae were re-
covered from one O. mossambicus of 36 examined, 
resulting in a prevalence of 2.7 %, and an abundance 
of 0.08. Larvae were moving freely in the swim blad-
der. No pentastomid larvae were found in C. garie-
pinus at this site (Table 2).

With respect to the Incomati River drainage system, 
Mpumalanga Province, a single infective larva of S. 
okavangoensis was encysted on the mesenteries of 
C. gariepinus, from a dam on a sugarcane farm in 
the Komatipoort region. This is the first report of C. 
gariepinus as intermediate host of a pentastomid.



325

W.J. LUUS-POWELL, A. JOOSTE & K. JUNKER

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326

Pentastomid parasites in fi sh in Olifants and Incomati River systems, South Africa
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327

W.J. LUUS-POWELL, A. JOOSTE & K. JUNKER

DISCUSSION

The fact that S. wedli, S. okavangoensis and the 
Alofia sp. had reached the final larval stage, as evi-
denced by double hooks and rows of annular spines 
typical for infective sebekiid larvae (Winch & Riley 
1986a), confirms that M. macrolepidotus, C. gariepi-
nus and O. mossambicus are indeed the respective 
true intermediate hosts for these pentastomids. Sim-
ilarly, Winch & Riley (1986a) found only the infective 
stage of Sebekia to be encysted.

Morphological characteristics of infective larvae of 
S. wedli from M. macrolepidotus correspond well 
with those recorded from O. mossambicus and T. 
rendalli (Junker et al. 1998). Ranging from 73–77, 
the number of annuli in infective larvae from M. 
macrolepidotus was similar to that observed in the 
latter hosts, namely 71–76 (Junker et al. 1998). 
Other characteristics that support the identification 
of S. wedli were the single row of chloride cell pore 
caps on the anterior border of the annuli and the 
overall appearance of the oral cadre. The latter is 
readily distinguished from congeneric African spe-
cies by appearing open anteriorly and having a less 
pronounced ovoid profile (Riley & Huchzermeyer 
1995).

The arrangement of the chloride cell pore caps in an 
irregular field at the anterior border of the annuli, 
about 2–3 cells deep, and the mitre-shaped appear-
ance of the oral cadre, observed in the specimen 
from C. gariepinus confirm its identification as S. 
oka vangoensis as described by Riley & Huch zer-
meyer (1995).

All infective Sebekia and Alofia larvae found during 
this study were encysted, the cysts being attached 
to either the swim bladder or the mesenteries. Con-
versely, Junker et al. (1998) recorded encysted as 
well as free-living infective S. wedli larvae from T. 
rendalli and O. mossambicus. The majority were, 
however, encysted and the authors speculated that 
free-living infective larvae had only recently moulted 
into this developmental stage. Junker et al. (1998) 
recovered S. wedli from the swim bladder only, and 
not from the mesenteries. They did, however, col-
lect encysted infective larvae of another sebekiid, L. 
cincinnalis from this site in T. rendalli and O. mos-
sambicus.

The literature suggests that sebekiids may occupy a 
number of sites in their intermediate hosts, and 
Overstreet et al. (1985) reported infective larvae of 
Sebekia mississippiensis under the connective tis-
sues lining muscle, kidney, liver and swim bladder 
of a variety of fish intermediate hosts.

Sebekia wedli larvae appear to be host specific in 
Flag Boshielo Dam, as none of the other seven fish 
species examined at the time, including 12 O. mos-
sambicus and three T. rendalli, harboured pentasto-
mid larvae (Table 2). Sebekia wedli had a relatively 
high prevalence of 40.5 % in T. rendalli in the KNP, 
but only three of 119 O. mossambicus harboured 
this pentastome (Junker et al. 1998). Hence, it is pos-
sible that the sample size with respect to the other 
hosts in Flag Boshielo Dam was too small to detect 
infection.

Although mormyrids were studied intensively at 
Nwanedi-Luphephe and Tzaneen Dams, Limpopo 
Prov ince, and Loskop and Blyde Canyon Dams, 
Mpu malanga Province (Table 2), pentastomid lar-
vae were only recovered from M. macrolepidotus 
from Flag Boshielo Dam. 

Flag Boshielo Dam has a large population of Nile 
crocodiles. These crocodilians have long been es-
tablished as a final host of S. wedli (Sambon 1922), 
and Junker et al. (1999) reported this pentastomid 
from Nile crocodiles in South Africa. Mormyrids are 
bottom feeders, favouring the muddy bottomed mar-
gins of rivers and floodplains (Skelton 2001), and 
are thus likely to ingest pentastome eggs, which are 
shed in crocodile faeces, and settle onto the bottom 
substrate. It remains a matter of speculation as to 
why S. wedli was not observed in intermediate hosts 
at any of the other dams, since both Loskop and 
Bly de Canyon Dams, as well as Tzaneen Dam also 
support crocodile populations. Possibly sample siz-
es at all these Dams were too small to detect pen-
tastome infections. Prevalence data on pentasto-
mids in Nile corocodiles in any of the above dams, 
including Flag Boshielo, are lacking.

Clarias gariepinus constitutes an important compo-
nent of the diet of Nile crocodiles (Guggisberg 1972; 
Whitfield & Blaber 1979), and its own feeding habits 
would readily expose it to ingesting pentastome 
eggs. Riley & Huchzermeyer (2000) noted that Cla-
ri as spp. were common in swamp forest pools in the 
northern Congo Republic and postulated that it might 
serve as intermediate host for the pentastomids, 
Agema silvaepalustris, Alofia parva and S. oka vango-
ensis, that were recovered from swamp forest dwarf 
crocodiles, Osteolaemus tetraspis, in that region. 
However, no proof of the role of Clarias in the trans-
mission of pentastomids has so far been presented. 
The prevalence of infection in C. gariepinus is low 
and only one of four hosts at the Komatipoort local-
ity was infected, while a total of 112 collected at 
eight additional localities did not habour the parasite 
(Table 2). Ten C. gariepinus from the KNP also har-



328

Pentastomid parasites in fi sh in Olifants and Incomati River systems, South Africa

boured no pentastomids (Junker, unpublished data 
1996). Winch & Riley (1986b) concluded that the 
absence of Subtriquetra subtriquetra in bottom-
feed ing Tilapia spp. in Trinidad, despite its presence 
in Aequidens pulcher, another bottom-feeder in the 
same reservoir, was probably due to an immune re-
sponse. This could also be an explanation for the 
low prevalence of pentastomids in C. gariepinus.

To date, several fish species belonging to a number 
of families world-wide have been recorded as inter-
mediate hosts of sebekiids, namely Sebekia oxy-
cephala in A. pulcher (Cichlidae) (blue acra) and 
Tilapia sp. (Cichlidae) in Trinidad and Gambusia 
affi nis (Poeciliidae) (mosquitofish) in Florida (Boyce, 
Cardeilhac, Lane, Buergelt & King 1984; Winch & 
Riley 1986a). Fundulus grandis (Fundulidae) (gulf 
killifish), Lepomis macrochirus (Centrarchidae) (blue-
gill), Micropogonias undulatus (Sciaenidae) (Atlantic 
croaker), Micropterus salmoides (Centrarchidae) 
(largemouth bass) and Xiphophorus helleri (Poecili-
idae) (swordtail) are confirmed intermediate hosts 
for Sebekia mississippiensis (Overstreet et al. 1985). 
Fain (1961) lists Alestes macrophthalmus (Alestidae) 
(torpedo robber), Bathybates ferox (Cichlidae), 
Chry sichthys brachynema (Claroteidae) (salmontail 
catfish), Chrysichthys mabusi (Claroteidae), Lates 
mi crolepis (Latidae) (forktail lates), Lates niloticus 
(Latidae) (Nile perch), Mastacembelus sp. (Mas ta-
cembelidae) and Oreochromis niloticus (= Tilapia 
nilotica) (Cichlidae) (Nile tilapia) as intermediate 
hosts of L. cincinnalis in Central Africa. The latter 
was also present in Serranochromis meridianus 
(Cichlidae) (Lowveld largemouth) in South Africa 
(Junker 2002). Few data exist on the intermediate 
hosts of Subtriquetra, which has sofar been recov-
ered from A. pulcher, O. mossambicus and T. ren-
dalli (Winch & Riley 1986b; Junker et al. 1998). Fain 
(1961) reports S. subtriquetra from Brazilian fish in 
general.

While S. rileyi has now been reported from interme-
diate fish hosts from several localities in South 
Africa, its final host has not been identified. According 
to Riley et al. (1990) adult subtriquetrids are exclu-
sive to crocodilians, but adult S. rileyi were absent 
in crocodiles harbouring other pentastome infec-
tions in the KNP, suggesting the involvement of a 
different final host, perhaps piscivorous terrapins or 
birds (Junker 2002).

ACKNOWLEDGEMENTS

The Division for Research Development and Admin-
istration, University of Limpopo, is thanked for finan-

cial assistance. The research at Phalaborwa was 
supported by a grant from the National Research 
Foundation of South Africa (Thuthuka Programme; 
TTK2004081000029). We are grateful to the De-
partment of Biodiversity, University of Limpopo, for 
infrastructure and Messrs H.E. Hattingh and J. 
Theron for technical assistance during some of the 
field surveys.

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    /HRV (Za stvaranje Adobe PDF dokumenata najpogodnijih za visokokvalitetni ispis prije tiskanja koristite ove postavke.  Stvoreni PDF dokumenti mogu se otvoriti Acrobat i Adobe Reader 5.0 i kasnijim verzijama.)
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    /NLD (Gebruik deze instellingen om Adobe PDF-documenten te maken die zijn geoptimaliseerd voor prepress-afdrukken van hoge kwaliteit. De gemaakte PDF-documenten kunnen worden geopend met Acrobat en Adobe Reader 5.0 en hoger.)
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    /UKR <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>
    /ENU (Use these settings to create Adobe PDF documents best suited for high-quality prepress printing.  Created PDF documents can be opened with Acrobat and Adobe Reader 5.0 and later.)
  >>
  /Namespace [
    (Adobe)
    (Common)
    (1.0)
  ]
  /OtherNamespaces [
    <<
      /AsReaderSpreads false
      /CropImagesToFrames true
      /ErrorControl /WarnAndContinue
      /FlattenerIgnoreSpreadOverrides false
      /IncludeGuidesGrids false
      /IncludeNonPrinting false
      /IncludeSlug false
      /Namespace [
        (Adobe)
        (InDesign)
        (4.0)
      ]
      /OmitPlacedBitmaps false
      /OmitPlacedEPS false
      /OmitPlacedPDF false
      /SimulateOverprint /Legacy
    >>
    <<
      /AddBleedMarks false
      /AddColorBars false
      /AddCropMarks false
      /AddPageInfo false
      /AddRegMarks false
      /ConvertColors /ConvertToCMYK
      /DestinationProfileName ()
      /DestinationProfileSelector /DocumentCMYK
      /Downsample16BitImages true
      /FlattenerPreset <<
        /PresetSelector /MediumResolution
      >>
      /FormElements false
      /GenerateStructure false
      /IncludeBookmarks false
      /IncludeHyperlinks false
      /IncludeInteractive false
      /IncludeLayers false
      /IncludeProfiles false
      /MultimediaHandling /UseObjectSettings
      /Namespace [
        (Adobe)
        (CreativeSuite)
        (2.0)
      ]
      /PDFXOutputIntentProfileSelector /DocumentCMYK
      /PreserveEditing true
      /UntaggedCMYKHandling /LeaveUntagged
      /UntaggedRGBHandling /UseDocumentProfile
      /UseDocumentBleed false
    >>
  ]
>> setdistillerparams
<<
  /HWResolution [2400 2400]
  /PageSize [595.276 841.890]
>> setpagedevice