Checklist of acanthocephalan parasites of South Africa.

Twenty-one species of acanthocephalans, representative of thirteen genera from ten families of seven orders and three classes, are included in this updated checklist of acanthocephalans in South Africa. Although South Africa appears to have a less diverse acanthocephalan fauna compared to some other countries such as Iran in Asia, or Brazil in South America, this is probably an artefact of fewer parasitological surveys.

Introduction

South Africa’s landscape is the third most biologically diverse in the world with 6% of the world’s mammal species, 8% of bird species and 5% of reptile species of which many are endemic (da Silva and Willows-Munro 2016). In regard to invertebrates, only 36,803 species are listed for Africa, and 12,098 for South Africa (Hamer 2010). It is said that in South African habitats, there are many undiscovered and undescribed animal species, especially invertebrates. It is estimated that as many as 80,000 South African animal species remain to be discovered or described, and most of these animals are invertebrates (Hamer 2013).

The most comprehensive checklist of helminth parasites of Africa was compiled for freshwater fishes by Khalil (1971) and updated by Khalil and Polling (1997). It included very few records of acanthocephalans considering the total number of freshwater fish species present in the continent. The updated list (Khalil and Polling 1997) comprised 568 adult helminth parasites of which only 21 species are acanthocephalans. These records were compiled from 359 species of African freshwater fishes (assigned to 89 genera belonging to 32 families) of an estimated 3000 existing inland fish species (Khalil and Polling 1997). These examples illustrate the lack of knowledge of the helminth fauna of the wildlife of the African continent in general and in South Africa in particular.

This is the first checklist of acanthocephalans of South Africa and the aim is to provide a comprehensive record of all the previously reported species of occurring in South African hosts as well as new records from our on-going research on parasites of wildlife, while simultaneously demonstrating the need for more extensive parasitological surveys.

Materials and methods

Data were obtained from two sources, published records and our own ongoing studies on the of South African wildlife. These data are presented in two parts. In the first part parasites are listed systematically, with families, genera, and species in alphabetical order. The scientific name, including any synonyms, followed by the scientific and common name of the host, the locality in which the parasite was reported and museum (location) of type specimens where known. In the second part, the hosts are listed systematically by their scientific names and parasite records from each host are given together with locality and reference. The records without references are those of our ongoing study that are being reported here for the first time.

Classification of the follows Amin (2013). For the hosts, fish taxonomy is based on Skelton (2001, 2016) and Fishbase (Froese and Pauly 2016), bird taxonomy is based on Clements et al. (2016) and mammal taxonomy on Wilson and Reader (2005) and Apps (2012).

Abbreviations for museums are:

Natural History Museum London, London, UK;

Gothenburg Natural History Museum, Gothenburg, Sweden;

South African Museum at Cape Town, South Africa;

South Australian Museum, Adelaide, Australia;

United States National Museum Helminthological Collection

United States National Parasite Collection now held in the Invertebrate Zoology collection of the Smithsonian Museum, Washington, USA.

Acanthocephalan specimens from our ongoing wildlife parasitology projects were mostly collected from roadkill animals, museum collections, hunting/culling surveys and other research permits received for a limited number of specimens through the Limpopo Department of Economic Development, Environment and Tourism (LEDET) (permit number CPM004961 and ZA/LP/HO/3370 for freshwater fish research, 001-CPM403-00012 and ZA/LP/HO/3448 for frogs, ZA/LP/HO/3432 for rodents and ZA/LP/87586 for roadkills).

Acanthocephalans from freshly dead animals were placed in tap water and refrigerated for a few hours to one day until the proboscis was everted and then fixed and stored in 70% ethanol until studied. Acanthocephalans from frozen hosts were fixed and stored in 70% ethanol. Some specimens were prepared for examination by staining in Mayer’s acid carmine, destained in HCl in 70% ethanol, dehydrated through increasing concentrations of ethanol, cleared in xylene, and mounted as whole worms in Canada balsam. Other worms were examined as temporary mounts following clearing in lactophenol or beechwood creosote.

A total of 102 species of birds (151 individuals), 72 of mammals (420 individuals), 9 of reptiles (18 individuals) and 42 (1050 individuals) of fishes were examined for this study (details in Table 1).

Table 1.

Total number of host taxa examined and those infected with acanthocephalans (i.e. number of taxa that harboured acanthocephalans, in parenthesis) during our ongoing study on wildlife parasites in South Africa.

Taxon Group	Order	Family	Genus	Species
Amphibians	1 (0)	8 (0)	13 (0)	19 (0)
Birds	21 (5)	50 (5)	87 (5)	102 (5)
Fishes (freshwater)	8 (1)	13 (1)	24 (1)	42 (1)
Mammals	10 (4)	26 (4)	59 (6)	72 (6)
Reptiles	3 (1)	6 (1)	7 (1)	9 (1)
Totals	43 (11)	103 (11)	190 (13)	244 (13)

Parasite-Host List

Class: Meyer, 1931

Order: Southwell & Macfie, 1925

Family: Hamann, 1892

Genus: Van Cleave, 1916

Amin, Evans, Heckmann & El-Naggar, 2013

(de Marval, 1902) Southwell & Mac-Fie, 1925

Harris, 1973

(Bhalerao, 1937) Van Cleave, 1947

Notes.

is found only in Asia and the species in Africa is actually (Amin et al. 2013; Amin 2013) and not previously reported in South Africa (Junker and Boomker 2006).

Host.

(L. 1758) (Helmeted Guineafowl) () (type host).

Localities.

Kruger National Park, Mpumalanga Province, South Africa (type locality) (Junker and Boomker 2006); Vicinity of Petrus Steyn, Free State Province, South Africa (Davies et al. 2008); Musina, Limpopo Province, South Africa (Junker and Boomker 2007; Junker et al. 2008).

Smales & Halajian, 2018

Bonaparte, 1850 (Karoo Thrush) () (type host).

Locality.

Polokwane, Limpopo Province, South Africa (type locality) (Smales et al. 2018).

Type specimens.

Holotype male SAM AHC 48068, allotype female SAM AHC 48069, paratype SAM AHC 48070.

(Baer, 1925) Meyer, 1932

Baer, 1925;

(L. 1758) (Helmeted Guineafowl) ()

Pretoria, Gauteng Province, South Africa (Oosthuizen and Markus 1967).

(von Linstow, 1901) Dollfus, 1936

von Linstow, 1901;

(L. 1758) (Helmeted Guineafowl) ().

Rooipoort farm, Kimberley, Northern Cape Province, South Africa (Crowe 1977).

(Lichtenstein, 1842) (Southern Yellow-billed Hornbill) ()

Limpopo Province, South Africa.

Order: Schmidt, 1972

Family: Van Cleave, 1924

Genus: Travassos, 1915

Meyer, 1931

(Smith, 1831) (Southern African Hedgehog) ()

Mohlonong village and University of Limpopo, Limpopo Province, South Africa (Amin et al. 2014).

(Bremser, 1811) Travassos, 1915 (type species)

Bremser, 1811

Railliet, 1893

Porter, 1914

Railliet, 1919

Meyer in Petrochenko, 1958

Meyer, 1932

Meyer, 1932 (

(Smith, 1831) (Southern African Hedgehog) ().

Hammanskraal, Gauteng Province, South Africa (Le Roux 1930).

Host recorded as in Le Roux (1930).

Ward & Nelson, 1967

(Peters, 1852) (Bushveld Gerbil), (Smith, 1834) (Natal ), (Pygmy mouse) ().

Bloemhof, Free State Province; Vyeboom village, Limpopo Province; Hoopstad, Free State Province; South Africa.

sp.

(É. Geoffroy Saint-Hilaire, 1812) (Thick-tailed Bushbaby) ().

Venda, Limpopo Province, South Africa.

Remarks.

One male and one female worm were found in the small intestine of an adult bushbaby.

Order: Petrochenko, 1956

Family: Southwell & Macfie, 1925

Genus: Spencer Jones, 1990

Spencer Jones, 1990 (type species)

(Günther, 1875) (Giant Golden Mole) () (type host).

Nqadu Forest, Transkei, Eastern Cape Province, South Africa (type locality) (Spencer Jones 1990).

Holotype male BMNH 1988.2480; allotype female BMNH 1988.2481; paratypes BMNH 1988.2482-2491.

sp.

Daudin, 1802 (Rock Monitor) ().

Tzaneen; Tolwe, Limpopo Province, South Africa.

Class: Van Cleave, 1936

Order: Van Cleave, 1936

Family: Van Cleave, 1920

Genus: Thapar, 1927

Subgenus: Verma & Datta, 1929

(Mashego, 1988) Amin, 2005

Host.

(Greenwood, 1962) (syn. ) (Sidespot Barb) () (type host).

Locality.

Lingwe River, Venda, Limpopo Province, South Africa (type locality) (Mashego 1988).

Type specimens.

Holotype in Transvaal Museum no. TM14659; Paratypes TM5 at University of Limpopo, Zoology, 5.

sp.

(Peters, 1852) (Mozambique Tilapia) ().

Molepo Dam, Limpopo Province, South Africa (Kunutu et al. 2013).

Family: (Ward, 1917) Van Cleave, 1928

Genus: Stiles & Hassall, 1905

Subgenus: Hamann, 1892

Amin & Christison, 2005

(Temminck & Schlegel, 1843) (Japanese Meagre, Dusky Kob) ) (type host).

Breede River Estuary, Western Cape Province, South Africa (type locality) (Amin and Christison 2005).

No. SAMCTA29536 (holotype male and allotype female; same slide), nos SAMCTA29537-29545 (paratypes), USNPC no. 94918 (paratypes).

Family: Yamaguti, 1939

Genus: Yamaguti, 1935

Dollfus & Golvan, 1963

(Gilchrist, 1904) (syn. ) () (Sole).

False Bay, Western Cape Province, South Africa (Dollfus and Golvan 1963).

sp. innom.

(Pallas, 1814) (syn. ) (Blackhand Sole) ().

Klein River estuary, Hermanus, Western Cape Province, South Africa (Bray 1974).

Three contracted and immature specimens were found in one fish and one male in another fish. Thus it could not be identified to species level (Bray 1974).

Family: Lühe, 1912

Genus: Lühe, 1911

(Golvan & Houin, 1964) Golvan, 1969

Golvan & Houin, 1964

(Euphrasen, 1791) (Snoek) ().

South Africa’s West and South coasts (Nunkoo et al. 2016).

Bray, 1974

(Pallas, 1814) (syn. ) (Blackhand Sole) () (type host)

Heuninges River estuary, near Cape Agulhas, Western Cape Province, South Africa (type locality) (Bray 1974).

British Museum, Registration number 1974.521-550.

sp.

Cocco, 1833 (Oilfish) ().

South Africa’s West coast, Atlantic Ocean (Nunkoo et al. 2017).

Family: Van Cleave, 1916 (Golvan, 1960)

Smales & Halajian, 2017

(Temminck, 1824) (Lizard Buzzard) () (type host).

Makhado (Louis Trichardt), Limpopo Province, South Africa (type locality) (Smales et al. 2017).

Type Specimens.

Holotype male SAM AHC 47858; allotype female SAM AHC 47859; paratypes SAM AHC 47860.

(Meyer, 1931) Golvan, 1958

Meyer, 1931 (

(Temminck, 1821) (Spotted Eagle Owl) ().

Zandrivierspoort Farm, Polokwane, Limpopo Province, South Africa.

sp.

L., 1758 (Domestic Cat) ().

Pretoria, Gauteng Province, South Africa (Baker et al. 1989).

sp.

(Gmelin, 1788) (Banded Mongoose) ().

Polokwane, Limpopo Province, South Africa.

Family: Golvan, 1960

Subgenus: Kostylew, 1915

(Goeze, 1782) Schmidt & Kuntz, 1966

Goeze, 1782

Gmelin, 1791

Gmelin, 1791

(Rudolphi, 1819) Travassos 1926

Dujardin, 1845

(Goeze 1782) Kostylew, 1914

(Westrumb, 1821) Travassos, 1926

de Marval, 1902

(Porta, 1910) Meyer, 1932

(de Marval, 1902) Meyer, 1932

Van Cleave, 1918

Schmidt et Kuntz, 1966

(Pontoppidan, 1763) (Curlew Sandpiper); Temminck, 1823 (Kittlitz’s Plover); Vieillot, 1818 (Three-banded Plover) ().

Berg River, Western Cape Province, South Africa (Amin et al. 1999).

(Peters, 1854) (syn. ) (African Crake) ().

Blouberg, Limpopo Province, South Africa.

(Burchell, 1822) (Blacksmith Lapwing) ().

Berg River, Western Cape Province, South Africa (Amin et al. 1999).

Unidentified plagiorhynchid

Host. Vieillot, 1818 (White-fronted Plover), Strickland, 1852 (Chestnut-banded Plover); Temminck, 1823 (Kittlitz’s Plover); (L., 1758) (Black-winged Stilt); (Burchell, 1822) (Blacksmith Lapwing)

Locality. Berg River, Western Cape Province, South Africa (Amin et al. 1999).

Family: Meyer, 1931

Genus: Schmidt, 1975

(Weiss, 1914) Zdzitowiecki, 1989

Weiss, 1914

(Gmelin, 1789) (Long-tailed Cormorant) ().

Dyer Island, South Africa (Van Cleave 1937).

Van Cleave (1937) is mentioning that he looked at a large number of immature worms and he tentatively assigning them to .

Petrochenko, 1956

(Van Cleave, 1937) Golvan, 1994

Van Cleave, 1937

(Wahlberg, 1855) (Bank Cormorant) () (type host).

Dyer Island, South Africa (type locality) (Van Cleave 1937).

Holotype female (1737, 3) and one paratype female (1737, 1) in GNM. One paratype female (1737, 2) in the collection of H.J. Van Cleave, Urbana, Illinois, U.S.A.

Genus: Porta, 1908

(von Linstow, 1880) Porta, 1908

von Linstow, 1880

Gubanov, 1952 (

Cocco, 1833 (Oilfish) ().

South Africa’s West coast, Atlantic Ocean (Nunkoo et al. 2017).

(Rudolphi, 1819) Porta, 1908

Rudolphi, 1819

Molin, 1858

Risso, 1826

Leukart, 1828

Linton, 1888

Harada, 1935 (

(Euphrasen, 1791) (Snoek) ().

South Africa’s West and South coasts (Nunkoo et al. 2016).

Genus: Lühe, 1904 (fide Van Cleave, 1945)

Monticelli, 1905

Lühe, 1912

Railliet & Henry, 1907 (misprint)

Porta, 1907

Johnston, 1937

Morini & Boero, 1961

(Euphrasen, 1791) (Snoek) ().

South Africa’s West and South coasts (Nunkoo et al. 2016).

Results and discussion

A total of twenty-one species of acanthocephalans, from thirteen genera from ten families of seven orders, comprise this updated checklist of acanthocephalans in South Africa. Representatives of three of the four classes of acanthocephalans (Amin 2013) have been reported in South Africa, with only the Amin, 1987 not having been recorded yet. The composition of reported acanthocephalan fauna shows that the is the most represented family with five named species parasitic in marine fish and wild birds.

In South Africa, birds have the highest species richness of acanthocephalans to this date with nine named species (from five genera) and five records only identified to group level, followed by fish with eight named species (from six genera) and two species only identified to genus level, mammals with four named species (from two genera) and three species only identified to genus level and finally reptiles with a single species only identified to group level. No acanthocephalans have been reported in amphibians to date. During the current study 110 frog specimens belonging to 19 species were examined but none harboured any acanthocephalans. However, this forms a small part of the entire amphibian fauna of the country which includes 128 described frog species (Frost 2018).

Only a small fraction of the vertebrate fauna of South Africa has been surveyed for acanthocephalans and we expect that in future additional acanthocephalan species will be discovered and described. For example it is estimated that many of South Africa’s marine fish parasites have yet to be discovered (Smit and Hadfield 2015). South Africa has an extremely rich biodiversity (Huntley et al. 2005), with nearly 8% of the world’s known species of birds, 6% of mammal species and 5% of reptile species (Driver et al. 2012). Therefore we might expect a more diverse acanthocephalan fauna compared to that of Brazil which has 23 genera and 34 species (from only 119 fish species) (Santos et al. 2008) or Iran with 30 described species (Tavakol et al. 2015). The lower species richness reported for South Africa probably reflects sampling effort rather than the true diversity of the acanthocephalan fauna. Until more data are available it will not be possible to determine the true species richness of the South African acanthocephalan assemblage.

Host	Parasite	Locality Country/ Reference
Class Aves
Order Accipitriformes
Family Accipitridae
Kaupifalcomonogrammicus (type host)	Centrorhynchussarehae (Centrorhynchidae)	Makhado (Louis Trichardt), Limpopo Province, South Africa
Order Bucerotiformes
Family Bucerotidae
Tockus leucomelas	Mediorhynchustaeniatus (Gigantorhynchidae)	Limpopo Province, South Africa
Order Charadriiformes
Family Charadriidae
Calidris ferruginea	Plagiorhynchus (Prosthorhynchus) cylindraceus (Plagiorhynchidae)	Berg River, Western Cape Province, South Africa (Amin et al. 1999)
Charadrius marginatus	Unidentified plagiorhynchid acanthocephalan (Plagiorhynchidae)	Berg River, Western Cape Province, South Africa (Amin et al. 1999)
Charadrius pallidus	Unidentified plagiorhynchid acanthocephalan (Plagiorhynchidae)	Berg River, Western Cape Province, South Africa (Amin et al. 1999)
Charadrius pecuarius	Plagiorhynchus (Prosthorhynchus) cylindraceus (Plagiorhynchidae)	Berg River, Western Cape Province, South Africa (Amin et al. 1999)
	Unidentified plagiorhynchid acanthocephalan (Plagiorhynchidae)	Berg River, Western Cape Province, South Africa (Amin et al. 1999)
Charadrius tricollaris	Plagiorhynchus (Prosthorhynchus) cylindraceus (Plagiorhynchidae)	Berg River, Western Cape Province, South Africa (Amin et al. 1999)
Vanellus armatus	Plagiorhynchus (Prosthorhynchus) cylindraceus (Plagiorhynchidae)	Berg River, Western Cape Province, South Africa (Amin et al. 1999)
	Unidentified plagiorhynchid acanthocephalan (Plagiorhynchidae)	Berg River, Western Cape Province, South Africa (Amin et al. 1999)
Family Recurvirostridae
Himantopus himantopus	Unidentified plagiorhynchid Acanthocephalan (Plagiorhynchidae)	Berg River, Western Cape Province, South Africa (Amin et al. 1999)
Order Galliformes
Family Numididae
Numidameleagris (type host)	Mediorhynchusafricanus (previously identified as Mediorhynchusgallinarum) (Gigantorhynchidae)	Kruger National Park, Mpumalanga Province, South Africa (Junker and Boomker 2006); Vicinity of Petrus Steyn, Free State Province, South Africa (Davies et al. 2008); Musina, Limpopo Province, South Africa (Junker and Boomker 2007; Junker et al. 2008)
	Mediorhynchusnumidae (Gigantorhynchidae)	Pretoria, Gauteng Province, South Africa (Oosthuizen and Markus 1967)
	Mediorhynchustaeniatus (Gigantorhynchidae)	Rooipoort farm, Kimberley, Northern Cape Province, South Africa (Crowe 1977)
Order Gruiformes
Family Rallidae
Crecopsis egregia	Plagiorhynchus (Prosthorhynchus) cylindraceus (Plagiorhynchidae)	Blouberg, Limpopo Province, South Africa
Order Passeriformes
Family Turdidae
Turdussmithi (type host)	Mediorhynchusmokgalongi (Gigantorhynchidae)	Polokwane, Limpopo Province, South Africa (type locality) (Smales et al. 2018)
Order Strigiformes
Family Strigidae
Bubo africanus	Centrorhynchusclitorideus (Centrorhynchidae)	Zandrivierspoort Farm, Polokwane, Limpopo Province, South Africa
Order Suliformes
Family Phalacrocoracidae
Microcarbo africanus	Andracanthatunitae (Polymorphidae)	Dyer Island, South Africa (Van Cleave 1937)
Phalacrocoraxneglectus (type host)	Arhythmorhynchusturbidus (Polymorphidae)	Dyer Island, South Africa (type locality) (Van Cleave 1937)
Class Actinopterygii
Order Cypriniformes
Family Cyprinidae
Enteromius neefi	Acanthogyrus (Acanthosentis) phillipi (Quadrigyridae)	Lingwe River, Venda, Limpopo Province, South Africa (Mashego 1988)
Order Perciformes
Family Cichlidae
Oreochromis mossambicus	Acanthogyrus sp. (Quadrigyridae)	Molepo dam, Limpopo Province, South Africa (Kunutu et al. 2013)
Family Gempylidae
Ruvettus pretiosus	Bolbosomacapitatum (Polymorphidae)	South Africa’s West coast, Atlantic Ocean (Nunkoo et al. 2017)
	Rhadinorhynchus sp. (Rhadinorhynchidae)	South Africa’s West coast, Atlantic Ocean (Nunkoo et al. 2017)
Thyrsites atun	Bolbosomavasculosum (Polymorphidae)	South Africa’s West and South coasts (Nunkoo et al. 2016)
	Corynosomaaustrale (Polymorphidae)	South Africa’s West and South coasts (Nunkoo et al. 2016)
	Rhadinorhynchuscadenati (Rhadinorhynchidae)	South Africa’s West and South coasts (Nunkoo et al. 2016)
Family Sciaenidae
Argyrosomusjaponicus (type host)	Neoechinorhynchus (Neoechinorhynchus) dorsovaginatus (Neoechinorhynchidae)	Breede River Estuary, Western Cape Province, South Africa (type locality) (Amin and Christison 2005)
Order Pleuronectiformes
Family Soleidae
Pegusanasuta (Soleableekeri) (type host)	Rhadinorhynchuscapensis (Rhadinorhynchidae)	Heuninges River estuary (Bray 1974)
	Longicollum sp. innom. (Pomphorhynchidae)	Klein River estuary (Bray 1974)
Barnardichthysfulvomarginata (type host)	Longicollumchabanaudi (Pomphorhynchidae)	False Bay, Western Cape Province (Dollfus and Golvan 1963)
Class Mammalia
Order Afrosoricida
Family Chrysochloridae
Chrysospalaxtrevelyani (type host)	Heptamegacanthusniekerki (Oligacanthorhynchidae)		Nqadu Forest, Transkai, Eastern Cape Province, South Africa (Spencer Jones 1990)
Order Carnivora
Family Felidae
Felis catus	Centrorhynchus sp. (Centrorhynchidae)		Pretoria, Gauteng Province, South Africa (Baker et al. 1989)
Family Herpestidae
Mungos mungo	Centrorhynchus sp. (Centrorhynchidae)		Polokwane, Limpopo Province, South Africa.
Order Eulipotyphla
Family Erinaceidae
Atelerixfrontalis (Aethechinusfrontalis)	Moniliformiskalahariensis (Moniliformidae)		Mohlonong village and University of Limpopo, Limpopo Province, South Africa (Amin et al. 2014)
	Moniliformismoniliformis (Moniliformidae)		Hammanskraal, Gauteng Province, South Africa (Le Roux 1930)
Order Primates
Family Galagidae
Otolemur crassicaudatus	Moniliformis sp. (Moniliformidae)		Venda, Limpopo Province, South Africa
Order Rodentia
Family Muridae
Gerbilliscus leucogaster	Moniliformisacomysi (Moniliformidae)		Vyeboom village, Limpopo Province, South Africa
Mastomys natalensis	Moniliformisacomysi (Moniliformidae)		Bloemhof, Free State Province
Mus minutoides	Moniliformisacomysi (Moniliformidae)		Hoopstad, Free State Province, South Africa
Class Reptilia
Order Squamata
Family Varanidae
Varanus albigularis	Oligacanthorhynchidae sp. (Oligacanthorhynchidae)		Tzaneen; Tolwe, Limpopo Province, South Africa