Alien freshwater fish parasites from South Africa: Diversity, distribution, status and the way forward.

The global translocation and introduction of freshwater fish into non-native regions has created the perfect opportunity for the co-introduction of their parasites. In a recent review on non-native freshwater fish introductions in South Africa, 55 fishes were reported as introduced into novel environments in South Africa, with 27 alien and 28 extralimital. However, the parasites potentially co-introduced by these non-native fishes have received much less attention from researchers than the hosts themselves. Thus far, the only attempts at summarising our knowledge on the diversity of introduced freshwater fish parasites in this region dates back to the 1980s when only four parasite species were considered to be alien, with a further eight species as doubtful. Over the last thirty years, more records have been added and this paper aims to provide an up-to-date review of our knowledge on the diversity, distribution, status (co-invasive or co-introduced) and the direction for future studies on introduced freshwater fish parasites in South Africa. Here we consider seven species (four ciliates, and one cestode, copepod and branchiuran respectively) as confirmed co-invaders, and 16 species (one flagelate, four ciliates, one cestode and ten monogeneans) as co-introduced. In addition, six species (three ciliates, two monogeneans and one copepod) previously recorded as invasive are deemed to be of uncertain status, and one ciliate is removed from the list of known invasive parasites from this region. It is further proposed that future research should focus on extralimital co-introductions, especially in the Eastern and Western Cape regions of South Africa where more than half of the fishes present are introduced species. It is also recommended that all new records of introduced parasites and new distribution records of known invasive parasites should include the deposition of voucher specimens in museums and, as far as possible, include molecular confirmation of its identification.

Introduction

Worldwide, the translocation and subsequent introduction of freshwater fish into non-native regions is known to cause an effect on the native biota. However, a secondary ecological and economical risk is also created but often disregarded. This risk is the co-introduction of the alien invasive fish parasites. Potential impacts of parasites due to host switching from introduced to a native host have been well documented (Adlard et al., 2015). Probably the best studied example is the introduction of the swim bladder nematode, Anguillicoloides crassus (Kuwahara, Niimi and Itagaki, 1974), into Europe and subsequent impact on wild European eels, Anguilla anguilla (Linnaeus, 1758). In a recent review on non-native freshwater fish introductions in South Africa, Ellender and Weyl (2014) listed a total of 55 fishes that have been introduced into novel environments in South Africa, with 27 alien and 28 extralimital (native to South Africa that have been translocated into areas where they did not naturally occur) introductions. These authors also emphasised that the introduction of associated parasites is a serious threat to native fish communities in South Africa.

To date, the only available checklist for freshwater fish parasites from southern Africa is the work done in the 1980s by Van As and Basson (1984). Ninety-five species of parasites were listed from 52 hosts and included 13 presumed alien parasites, although the authors did not specifically identify them as alien. Most of these (10) were protozoans with the remaining three being a cestode, a copepod, and a branchiuran respectively (see Table 1). Of the 52 hosts listed, only four were invasive fishes infected with nine of the alien parasites recorded from southern African fishes at that stage. The common carp, Cyprinus carpio Linnaeus, 1758, was clearly responsible for most of the co-introductions and co-invasions into South Africa with seven of the thirteen parasites recorded from this host (Table 2). The first attempt to summarise the extent of aquatic introductions into southern Africa was by Bruton and Merron (1985), who compiled a checklist of alien and translocated aquatic animals from this region. In their report, Bruton and Merron (1985) listed 12 fish parasites, including 11 reported by Van As and Basson (1984) with the addition of the copepod Achtheres pimelodi Kroyer, 1863 (syn. Achtheres micropteri Wright, 1882). However, they only regarded four as alien with the status of the remaining eight species considered doubtful; suggesting that further taxonomic research might reveal that they are indigenous. In a book chapter on biological invasions in southern Africa, Bruton and Van As (1986) confirmed the assessment made by Bruton and Merron (1985) without adding additional information. Two years later, De Moor and Bruton (1988) published the first atlas of alien and translocated aquatic animals from southern Africa and only included the four fish parasites considered by Bruton and Merron (1985) as alien. These were the European trichodinid, Trichodina acuta Lom 1961 (ciliate); whitespot, Ichthyophthirius multifiliis Fouquet, 1876 (ciliate); Asian fish tape worm, Schyzocotyle (Bothriocephalus) acheilognathi Yamaguti, 1934 (cestode); and the Japanese fish louse, Argulus japonicus Thiele, 1900 (branchiuran). The most recent checklist of alien animals of southern Africa is a photo guide book by Picker and Griffiths (2011) that included all freshwater, marine and terrestrial species. These authors included two of the four species reported by De Moor and Bruton (1988) (A. japonicus and S. acheilognathi) and added the gill flukes Gyrodactylus kherulensis Ergens, 1974 and Pseudodactylogyrus anguillae (Yin and Sproston, 1948).

Table 1

Alien fish parasites found within South Africa indicating their invasion status, as well as recorded hosts, locality records and primary reference.

Classification	Genus Species	Status	Host fish	Location - River system	Reference
Phylum: Euglenozoa
Class: Kinetoplastea
Order: Prokinetoplastida
Family: Ichthyobodonidae	Ichthyobodo necator	Co-invader	Cyprinus carpio	Not specified	Todal et al. (2004)
Phylum Ciliophora
Class: Oligohymenophorea
Order: Mobilida
Family: Trichodinidae	Trichodina acuta	Co-introduced	Oncorhynchus mykiss	Metsimatsho River	Basson and Van As (1993)
	Trichodinella epizootica	Uncertain	Carassius auratus	Modder River	Basson et al. (1983)
			Cyprinus carpio	Modder River	Basson et al. (1983)
	Trichodina mutabilis	Co-introduced	Carassius auratus	Commercial supplier (Cape Town)	Mouton et al. (2001)
	Trichodina nigra	Uncertain	Carassius auratus	Modder River	Basson et al. (1983)
			Cyprinus carpio	Modder River	Basson et al. (1983)
	Trichodina reticulata	Co-introduced	Carassius auratus	Local distributor (Bloemfontein)	Basson and Van As (1993)
	Trichodina uniforma	Co-introduced	Carassius auratus	Komatipoort River (Fish farm)	Van As and Basson (1989)
Order: Hymenostomatida
Family: Ichthyophthiriidae	Ichthyophthirius multifiliis	Co-invasive	Anguilla mossambica	Keiskamma	Jackson (1978)
			Cyprinus carpio	Lowveld Fisheries Research Station; Tompi Seleka; Olifants River	Van As et al., 1984, Basson, 1982
			Carassius auratus	Commercial suppliers	Mouton et al. (2001)
			Enteromius (Barbus) paludinosus	Turfloop Dam	Basson (1982)
			Poecilia reticulata	Commercial suppliers	Mouton et al. (2001)
			Oncorhynchus mykiss	Bushmans River Trout Farm; Ingwagwana River; Polela River	Bragg (1991)
			Oreochromis mossambicus	Lowveld Fisheries Research Station; Sheshego Dam	Van As et al., 1984, Basson, 1982
			Salmo trutta	Bushmans River	Bragg (1991)
Order: Sessilida
Family: Epistylididae	Apiosoma nasalis	Uncertain	Pseudocrenilabrus philander	Westdene Dam	Viljoen and Van As (1983)
	Apiosoma piscicola	Co-invasive	Coptodon rendallii	Groot-Letaba River	Viljoen and Van As (1985)
			Enteromius (Barbus) paludinosus	Vaal River	Viljoen and Van As (1985)
			Enteromius (Barbus) trimaculatus	Nwanedzi River; Olifants River	Viljoen and Van As (1985)
			Labeo cylindricus	Mothlapitse River; Nwanedzi River; Olifants River	Viljoen and Van As (1985)
			Marcusenius macrolepidotus	Olifants River	Viljoen and Van As (1985)
			Micropterus dolomieu	Sabie River	Viljoen and Van As (1985)
			Oreochromis mossambicus	Nwanedzi River; Olifants River; Klein Letaba River; Mogalakwena River; Tompi Seleka and Lowveld Fisheries Stations; Sabie River; Groot-Letaba River; Lepellane River	Viljoen and Van As (1985)
			Pseudocrenilabrus philander	Mooi River; Vaal River; Nwanedzi River; Olifants River; Westdene Dam; Lydenburg Fisheries	Viljoen and Van As, 1983, Viljoen and Van As, 1985
Class: Phyllopharyngea
Order: Chlamydodontida
Family: Chilodonellidae	Chilodonella hexasticha	Co-invasive	Coptodon rendalli	Lebowa Fisheries Station	Basson, 1982, Van As and Basson, 1984
			Enteromius (Barbus) paludinosus	Turfloop Dam	Basson, 1982, Van As and Basson, 1984
			Pseudocrenilabrus philander	Nwanedzi River; Pietersburg Dam	Van As and Basson (1984)
			Oreochromis mossambicus	Olifants River; Pietersburg Dam; Kouga River; Nyl River; Lebowa Fisheries Station; Nwanedzi River	Paperna and Van As, 1983, Basson, 1982, Van As and Basson, 1984
			Tilapia sparrmanii	Olifants River; Lebowa Fisheries Station	Paperna and Van As (1983)
	Chilodonella piscicola (syn. C. cyprini)	Co-invasive	Coptodon rendalli	University of Johannesburg aquarium; Olifants River	Basson, 1982, Van As and Basson, 1984
			Oreochromis mossambicus	Lowveld Fisheries Research Station	Van As and Basson (1984)
			Pseudocrenilabrus philander	Vaal River (Christiana); Orlando Dam (Klip River in Vaal River)	Basson, 1982, Van As and Basson, 1984
			Tilapia sparrmanii	Lowveld Fisheries Research Station	Van As and Basson (1984)
Phylum: Platyhelminthes
Class: Cestoda
Order: Bothriocephalidea
Family: Bothriocephalidae	Schyzocotyle acheilognathi (syn. B. acheilognathi)	Co-invasive	Cyprinus carpio	Komatipoort - commercial ponds; Olifants River; Vaal River; Mtata River	Boomker et al. (1980); Brandt et al., 1981, Van As et al., 1981, Schramm, 1992, Brandt et al., 1980
			Enteromius annectens	Phongolo River	Current study
			Enteromius argenteus	Olifants River	Mashego (1982)
			Enteromius bifrenatus	Phongolo River	Current study
			Enteromius brevipinnis	Marite River (Sabie River)	Schult and Schoonbee (1999)
			Enteromius mattozi	Olifants River	Mashego (1982)
			Enteromius paludinosus	Olifants River	Mashego (1982)
			Enteromius trimaculatus	Mooi River; Olifants River	Van As et al., 1981, Mashego, 1982
			Labeobarbus maraquensis	Olifants River	Mashego (1982)
			Labeobarbus aeneus	Vaal River; Great Fish River	Bertasso and Avenant-Oldewage, 2005, Stadlander et al., 2011
			Labeobarbus kimberleyensis	Vaal River	Brandt et al., 1981, Bertasso and Avenant-Oldewage, 2005
Order: Caryophyllidea
Family: Lytocestidae	Atractolytocestus huronensis	Co-introduced	Cyprinus carpio	Olifants River; Letaba River; Vaal River; Riet River	Scholz et al. (2015); Current study
Class: Monogenea
Order: Dactylogyridea
Family: Ancyrocephalidae	Clavunculus bursatus	Co-introduced	Micropterus salmoides	Friedrichskrön Dam; Thomas Baine Nature Reserve	Truter et al. (2017)
	Onchocleidus dispar	Co-introduced	Micropterus salmoides	Thomas Baines Nature Reserve	Truter et al. (2017)
	Onchocleidus furcatus	Co-introduced	Micropterus salmoides	Mooi River and Potchefstroom Dam; Friedrichskrön Dam	Truter et al. (2017)
	Onchocleidus principalis	Co-introduced	Micropterus salmoides	Thomas Baines Nature Reserve	Truter et al. (2017)
	Syncleithrium fusiformis	Co-introduced	Micropterus salmoides	Friedrichskrön Dam	Truter et al. (2017)
Family: Dactylogyridae	Acolpenteron ureteroecetes	Co-introduced	Micropterus salmoides	Jonkershoek inland fish hatchery; Groot-Letaba River (Tzaneen Dam)	Du Plessis, 1948, Matla, 2012
			Micropterus punctulatus	Jonkershoek inland fish hatchery	Du Plessis (1948)
			Micropterus dolomieu	Jonkershoek inland fish hatchery	Du Plessis (1948)
	Dactylogyrus extensus	Co-introduced	Cyprinus carpio	Vaal River (Vaal Dam)	Crafford et al., 2014a, Crafford et al., 2014b)
	Dactylogyrus lamellatus	Co-introduced	Cyprinus carpio	Vaal River (Vaal Dam)	Crafford et al., 2014a, Crafford et al., 2014b)
	Dactylogyrus minutus	Co-introduced	Cyprinus carpio	Vaal River (Vaal Dam)	Crafford et al., 2014a, Crafford et al., 2014b)
Family: Pseudodactylogyridae	Pseudodactylogyrus anguillae	Uncertain	Anguilla mossambica	Between Fish and Buffalo Rivers (Eastern Cape); Great Fish River; Koonap River; Kei River; Keiskamma River	Christison and Baker, 2007, Parker et al., 2011, McHugh et al., in press
Order: Gyrodactylidea
Family: Gyrodactylidae	Gyrodactylus kherulensis	Co-introduced	Cyprinus carpio koi	Kuilsrivier; Durban	Maseng (2010)
			Cyprinus carpio	Vaal River (Vaal Dam)	Crafford et al. (2014a)
	Gyrodactylus kobayashii	Uncertain	Carassius auratus	Kuilsrivier	Maseng (2010)
Phylum: Arthropoda
Subphylum: Crustacea
Class: Maxillopoda
Subclass: Copepoda
Order: Cyclopoida
Family: Lernaeidae	Lernaea cyprinacea	Co-invader	Coptodon rendalli	Phongolo River	Smit et al. (2016)
			Labeo capensis	Orange River	Robinson and Avenant-Oldewage (1996)
			Labeo congoro (syn L. rubropunctatus)	Mogalakwena River; Olifants River;	Van As and Viljoen, 1984, Robinson and Avenant-Oldewage, 1996
			Labeo cylindricus	Limpopo River	Van As and Basson (1984)
			Labeo rosae	Olifants River; Selati River;	Robinson and Avenant-Oldewage (1996)
			Labeo ruddi	Olifants River	Robinson and Avenant-Oldewage (1996)
			Labeo umbratus	Olifants River	Robinson and Avenant-Oldewage (1996)
			Labeobarbus marequensis	Crocodile (West) River; Olifants River; Lowveld Fisheries Station	Van As and Basson, 1984, Robinson and Avenant-Oldewage, 1996
			Labeobarbus kimberleyensis	Vaal River	Robinson and Avenant-Oldewage (1996)
			Oreochromis mossambicus	Olifants River; Selati River; Crocodile River (West); Lowveld Fisheries Station; Phongolo River (Nyamiti pan)	Robinson and Avenant-Oldewage, 1996, Van As and Viljoen, 1984, Van As and Basson, 1984, Viljoen, 1986, Smit et al., 2016, Welicky et al., 2017
			Pseudocrenilabrus philander	Harts River (Barberspan)	Truter et al. (2016)
Order: Cyclopoida
Family: Siphonostomatoida	Achtheres pimelodi	Uncertain	Micropterus dolomieu	Not specified	Barnard, 1955, Fryer, 1968
Class: Ichthyostraca
Subclass: Branchiura
Order: Arguloida
Family: Argulidae	Argulus japonicus	Co-invasive	Clarias gariepinus	Vaal River; Olifants River; Pienaars River	Kruger et al., 1983, Van As and Basson, 1984, Avenant-Oldewage, 1994, Avenant-Oldewage, 2001
			Cyprinus carpio	Vaal River; Harts River; Pienaars River; Komati River; Olifants River	Kruger et al., 1983, Van As and Basson, 1984, Avenant-Oldewage, 1994, Avenant-Oldewage, 2001
			Enteromius mattozi	Pienaars River	Van As and Basson (1984)
			Labeo capensis	Vaal River; Harts River; Mooi River; Pienaars River	Kruger et al., 1983, Van As and Basson, 1984, Avenant-Oldewage, 1994
			Labeo rosae	Olifants River	Avenant-Oldewage (1994)
			Labeo umbratus	Vaal River; Harts River; Mooi River; Olifants River	Kruger et al., 1983, Van As and Basson, 1984, Avenant-Oldewage, 1994, Avenant-Oldewage, 2001
			Labeobarbus aeneus	Vaal River; Harts River; Mooi River	Kruger et al., 1983, Van As and Basson, 1984, Avenant-Oldewage, 1994
			Labeobarbus kimberleyensis	Vaal River; Harts River	Kruger et al., 1983, Van As and Basson, 1984
			Labeobarbus marequensis	Crocodile River (West) (Hartebeespoort Dam); Pienaars River; Bronkhorstspruit River	Van As and Basson, 1984, Avenant-Oldewage, 2001
			Oncorhynchus mykiss	Lydenburg Fish Hatchery	Van As and Basson (1984)
			Oreochromis mossambicus	Crocodile River (West); Pienaars River; Olifants River	Avenant-Oldewage, 1994, Van As and Basson, 1984, Avenant-Oldewage, 2001

Table 2

Fish hosts with known alien parasites from South Africa.

Classification	Genus species	Parasite species
Family: Mormyridae	Marcusenius macrolepidotus	Apiosoma piscicola
Family: Anguillidae	Anguilla mossambica	Ichthyophthirius multifiliis
Family: Cyprinidae	Carassius auratus	Ichthyophthirius multifiliis
		Trichodina mutabilis
		Trichodina reticulata
		Trichodina uniforma
	Cyprinus carpio	Argulus japonicus
		Atractolytocestus huronensis
		Dactylogyrus minutus
		Dactylogyrus lamellatus
		Gyrodactylus kherulensis
		Ichthyophthirius multifiliis
		Ichthyobodo necator
		Schyzocotyle acheilognathi
	Enteromius annectens	Schyzocotyle acheilognathi
	Enteromius brevipinnis	Schyzocotyle acheilognathi
	Enteromius bifrenatus	Schyzocotyle acheilognathi
	Enteromius trimaculatus	Apiosoma piscicola
		Schyzocotyle acheilognathi
	Enteromius argenteus	Schyzocotyle acheilognathi
	Enteromius paludinosus	Apiosoma piscicola
		Chilodonella hexasticha
		Ichthyophthirius multifiliis
		Schyzocotyle acheilognathi
	Enteromius mattozi	Argulus japonicus
		Schyzocotyle acheilognathi
	Labeobarbus kimberleyensis	Argulus japonicus
		Lernaea cyprinacea
		Schyzocotyle acheilognathi
	Labeobarbus aeneus	Argulus japonicus
		Schyzocotyle acheilognathi
	Labeobarbus marequensis	Argulus japonicus
		Lernaea cyprinacea
		Lernaea cyprinacea
		Schyzocotyle acheilognathi
	Labeo umbratus	Argulus japonicus
		Lernaea cyprinacea
	Labeo capensis	Argulus japonicus
		Lernaea cyprinacea
	Labeo rosae	Argulus japonicus
		Lernaea cyprinacea
	Labeo ruddi	Lernaea cyprinacea
	Labeo congoro	Lernaea cyprinacea
	Labeo cylindricus	Lernaea cyprinacea
Family: Clariidae	Clarias gariepinus	Argulus japonicus
		Dactylogyrus extensus
Family: Salmonidae	Salmo trutta	Ichthyophthirius multifiliis
	Oncorhynchus mykiss	Argulus japonicus
		Ichthyophthirius multifiliis
		Trichodina acuta
Family: Centrarchidae	Micropterus salmoides	Acolpenteron ureteroecetes
		Clavunculus bursatus
		Onchocleidus dispar
		Onchocleidus furcatus
		Onchocleidus principalis
		Syncleithrium fusiformis
	Micropterus dolomieu	Apiosoma piscicola
		Acolpenteron ureteroecetes
	Micropterus punctulatus	Acolpenteron ureteroecetes
Family: Cichlidae	Pseudocrenilabrus philander	Apiosoma piscicola
		Chilodonella piscicola (syn C. cyprini)
		Chilodonella hexasticha
		Ichthyobodo necator
		Lernaea cyprinacea
	Tilapia sparrmanii	Ichthyobodo necator
		Chilodonella piscicola (syn C. cyprini)
		Chilodonella hexasticha
	Coptodon rendallii	Apiosoma piscicola
		Chilodonella piscicola (syn C. cyprini)
		Chilodonella hexasticha
		Lernaea cyprinacea
	Oreochromis mossambicus	Apiosoma piscicola
		Argulus japonicus
		Chilodonella piscicola (syn C. cyprini)
		Chilodonella hexasticha
		Ichthyobodo necator
		Ichthyophthirius multifiliis
		Lernaea cyprinacea
Family: Poeciliidae	Poecilia reticulata	Ichthyophthirius multifiliis

In addition to the checklist, atlas, and guides mentioned above, many independent studies on specific aspects of alien freshwater parasites were undertaken during the past four decades, however, not a single publication attempted to provide a concise summary of our knowledge on this important subject. The aim of this review is thus to provide an up-to-date review of our knowledge on alien invasive freshwater fish parasites from South Africa with the specific focus on their status (co-introduced or co-invasive), known distribution, and hosts. Based on our current knowledge and international trends, this paper also aims to provide direction for future studies.

Confirmed co-invasive freshwater fish parasites

Phylum Ciliophora

Ichthyophthirius multifiliis

The ciliate I. multifiliis, the causative agent of the disease ichthyophthiriosis, is an important pathogen of freshwater teleosts globally, and accounts for significant economic losses to the aquaculture industry (Matthews, 2005). Similar to many other invasive parasites, I. multifiliis was most likely co-introduced into freshwater ecosystems throughout the world with the introduction of its native cyprinid hosts from Asia (Nigrelli et al., 1976). It was first reported from Africa (Uganda) by Paperna (1972), followed by Jackson (1978) reporting I. multifiliis from the longfin eel, Anguilla mossambica Peters, 1852, collected in the Keiskamma, South Africa (Table 1, Fig. 1A). Other records of I. multifiliis from South Africa include infestations on the introduced C. carpio, Salmo trutta Linnaeus, 1758 and Oncorhynchus mykiss (Walbaum, 1792), with spillover to the native Oreochromis mossambicus (Peters, 1852) and straightfin barb, Enteromius (Barbus) paludinosus (Peters, 1852) also recorded (Basson, 1982, Van As et al., 1984, Bragg, 1991). During a pilot study on the health status of ornamental freshwater fishes imported to South Africa, Mouton et al. (2001) recorded I. multifiliis from guppies, Poecilia reticulata Peters, 1859 and goldfish, Carassius auratus (Linnaeus, 1758). This study clearly demonstrated the potential for continual introductions of this pathogenic parasite through the ornamental fish trade and further emphasised the need for proper health screening of all imported fishes into South Africa.

Fig. 1

Maps indicating the South African distribution records for (A)Ichthyophthirius multifiliis Fouquet, 1876; (B)Apiosoma piscicola (Blanchard, 1885); (C)Chilodonella hexasticha (Kiernik, 1909) and Chilodonella piscicola (Zacharias, 1894); (D)Schyzocotyle (Bothriocephalus) acheilognathi (Yamaguti, 1934).

Apiosoma piscicola

Apiosoma piscicola, first described more than 120 years ago from C. carpio collected in France, is a sessile peritrich from the Epistylididae that lives on the gills and body surface of its host (Li et al., 2008). With its native host being C. carpio, it is no surprise that this species has a similar global distribution and status as an invasive species, and has been reported as such from, amongst others, Canada (Cone and Odense, 1987), Egypt (El-Tantawy et al., 2013), and Mexico (Aguilar-Aguilar and Islas-Ortega, 2015). The first report of A. piscicola from South Africa was by Viljoen and Van As (1983) from the skin of the southern mouthbrooder, Pseudocrenilabrus philander (Weber, 1897), collected from the Westdene Dam in the Jukskei River (Table 1). In a follow-up study on sessile peritrichs from freshwater fishes in South Africa, Viljoen and Van As (1985) reported A. piscicola from an additional seven hosts collected in more than ten rivers as well as three fisheries stations (Table 1, Fig. 1B). This wide distribution and host range clearly indicated that this species has been a well-established co-invader long before its first report in the 1980s. As the focus of the Viljoen and Van As (1985) study was the northern regions of South Africa (Gauteng, Limpopo, North West and Mpumalanga provinces), it would be important to determine the presence, distribution and hosts of this alien in the rest of South Africa's rivers.

Chilodonella hexasticha

Members of the chilodonelid genus Chilodonella Strand, 1928 that parasitise fishes are known to cause the disease chilodonellosis, which can lead to extreme high host mortalities, especially under aquaculture conditions (Mitra and Haldar, 2004, Pádua et al., 2013, Bastos Gomes et al., 2017). Two species, C. hexasticha and C. piscicola (Zacharias, 1894) are considered to be the main agents of chilodonellosis and occur globally on the body surface, gills, and fins of freshwater fish hosts. Although the majority of records of pathology caused by Chilodonella spp. are from aquaculture facilities, such as those in Finland (Rintamäki et al., 1994), these parasites have also been reported as the main cause of deaths of native fish in natural habitats, such as the Finke River near Alice Springs, Australia (Langdon et al., 1985). In the latter case, Langdon et al. (1985) reported that C. hexasticha induced severe generalised epithelial hyperplasia in the gills, which possibly compromised respiratory exchange and killed the fish through hypoxaemia.

The first record of C. hexasticha in South Africa, according to Paperna and Van As (1983), was most probably a conference contribution by Du Plessis (1952). This publication reported mass mortalities of the native Mozambique tilapia, Oreochromis mossambicus, due to heavy infections of a Chilodonella sp., from various fish ponds in South Africa. Its presence in South Africa, and the pathology it caused on native wild caught and farmed fishes, was confirmed by Paperna and Van As (1983) and Van As et al. (1984). Thus far, C. hexasticha has been reported from four cichlids and one cyprinid collected in more than five river systems and two aquaculture facilities (Table 1, Fig. 1C). No research in South Africa has been conducted on this important pathogen since the 1980s and specifically not regarding the control thereof. Therefore, in the light of the current global and South African drive towards increasing fresh water aquaculture, it is imperative that research into this and other disease causing invasive parasites are prioritised (Bastos Gomes et al., 2017).

Chilodonella piscicola (syn. C. cyprini)

The taxonomic status of this Chilodonella species was only resolved in the 1970s when C. cyprini was synonymised with C. piscicola and clear evidence was provided that C. hexasticha and C. piscicola are distinct species (Mitra and Haldar, 2004, Bastos Gomes et al., 2017). It is therefore no surprise that the first records of C. piscicola in South Africa, noted by Basson (1982) and Van As and Basson (1984), initially referred to this species as C. cyprini. These records from South Africa were not included in the recent review of the Chilodonella by Bastos Gomes et al. (2017), most probably due to the original identification as C. cyprini; however, it can now be included with the other seven countries listed as confirmed records of C. piscicola. In addition, its presence on two wild caught cichlids, Coptodon rendalli (Boulenger, 1896) and Pseudocrenilabrus philander, is together with the record from Tibet (see Bastos Gomes et al., 2017), the only records of this parasite on native wild caught fishes (Table 1, Fig. 1C). Similar to C. hexasticha, C. piscicola has also been found to cause mortalities in fish aquaculture, however, the former is associated with warmer climates (between 26 and 31 °C), while the latter exhibits a wide thermal tolerance in the lower range (between 4 and 20 °C) (reviewed by Bastos Gomes et al., 2017). With the majority of South Africa's river and impoundment temperatures dropping down to below 20 °C in winter, the potential for C. piscicola to proliferate under these conditions in the wild needs to be investigated.

Phylum Platyhelminthes

Schyzocotyle (Bothriocephalus) acheilognathi

It has been well documented that the Asian tapeworm, S. acheilognathi, was most likely first introduced during 1975 into South Africa with its native host, the grass carp Ctenopharyngodon idella Valenciennes, 1844 (Boomker et al., 1980, Bertasso and Avenant-Oldewage, 2005, Stadlander et al., 2011). Following its introduction, it successfully established itself in the common carp, Cyprinus carpio (introduced for commercial carp farming). The first published report of this invasive parasite was thus in C. carpio by Boomker et al. (1980), from a commercial fish farm in the Komatipoort area, Mpumalanga Province of South Africa (Table 1, Fig. 1D). As S. acheilognathi appears to not be host specific both on an intermediate or definitive host level, this parasite quickly spilled over to native hosts across South Africa when C. carpio was introduced for aquaculture and recreational angling purposes and C. idella for controlling aquatic weeds (Stadlander et al., 2011, Ellender and Weyl, 2014). The first record of this species as a co-invader following spillover was that of Brandt et al. (1981) reporting it parasitising the Vaal-Orange largemouth yellowfish, Labeobarbus kimberleyensis Gilchrist and Thompson, 1913, collected from the Vaal Dam in the Vaal River (Fig. 1D). In the same year, Van As et al. (1981) reported another spillover event, this time in Boskop Dam, Mooi River, with the three-spot barb, Enteromius (Barbus) trimaculatus, as the infected host (Fig. 1D). Since these first reports, S. acheilognathi has been reported from at least 10 native hosts (Table 1) from six rivers (Fig. 1D) in South Africa (Mashego, 1982, Barkhuizen, 1991, Schramm, 1992, Retief et al., 2007, Stadlander et al., 2011, Kuchta et al., 2012, Swanepoel, 2015), making it one of the most widespread co-invasive parasites reported in South Africa.

The pathological effects of S. acheilognathi on native hosts in aquaculture conditions, as well as its threat to wild populations, have been well documented globally (Dove et al., 1997, Salgado-Maldonado and Pineda-López, 2003, Pullen et al., 2009). However, research in South Africa has mainly focussed on its distribution, ecology, and potential use as bioindicators of metal pollution (Bertasso and Avenant-Oldewage, 2005, Retief et al., 2007, Degger and Avenant-Oldewage, 2009), with a paucity of data on its population and community level impact on threatened native species. Future studies should specifically focus on these impacts and on regions of high endemicity, such as the Cape Floristic Region of the southern and southwestern Cape Province where the largest percentage of South Africa's threatened freshwater fishes occur.

Phylum Arthropoda

Lernaea cyprinacea

The global distribution of the copepod Lernaea cyprinacea as an invasive ectoparasite, and the severe effects of it on native freshwater fish hosts, has been well documented (see Welicky et al., 2017). Despite the first record of the introduction of this ectoparasite into Africa dating back to the 1960s (Robinson and Avenant-Oldewage, 1996), it was only recorded for the first time from South Africa twenty years later. Van As and Basson (1984) recognise the unpublished Masters dissertation of Viljoen (1982) as the first document to report L. cyprinacea from South Africa. In addition to Viljoen (1982) records of O. mossambicus and Labeobarbus marequensis (Smith, 1841) from Hartebeespoort Dam in the Crocodile River (West) and Labeo cylindricus Peters, 1852 from the Limpopo River as hosts, Van As and Basson (1984) recorded an infestation of L. cyprinacea on O. mossambicus from the Lowveld Fisheries Station (Table 1, Fig. 2A). Further confirmation of the presence of L. cyprinacea on South African native fishes was by Van As and Viljoen (1984) and Viljoen (1986) who also reported the presence of L. cyprinacea on O. mossambicus in Hartebeespoort Dam as well as from Labeo congoro Peters, 1852 (syn. Labeo rubropunctatus) in the Glen Alpine Dam, Mogalakwena River (Table 1, Fig. 2A).

Fig. 2

Maps indicating the South African distribution records for (A)Lernaea cyprinacea Linnaeus, 1758; (B)Argulus japonicus Thiele, 1900; (C)Ichthyobodo necator Henneguy, 1883 (needs molecular confirmation); (D)Trichodina acuta Lom, 1961, Trichodina mutabilis Kazubski and Migala, 1968, Trichodina reticulata Hirschmann and Partsch, 1955, and Trichodina uniformaVan As and Basson, 1989.

Interestingly, Bruton and Merron (1985) included L. cyprinacea in their list of what they considered to be doubtful alien species and therefore De Moor and Bruton (1988) did not include this species in their atlas to alien aquatic animals in southern Africa. More than ten years later Robinson and Avenant-Oldewage (1996) increased our knowledge on the distribution and hosts of L. cyprinacea and added another six cyprinid hosts collected from three different rivers (Table 1, Fig. 2A). These authors also provided a detailed morphological study of L. cyprinacea as well as an updated geographical distribution in Africa. Recently the identity of L. cyprinacea in South Africa was genetically confirmed and two more hosts and three localities where added (Smit et al., 2016, Truter et al., 2016, Welicky et al., 2017). The most surprising fact regarding the host records of L. cyprinacea in South Africa is that it does not include any of the invasive cyprinids which were potentially responsible for the co-introduction and subsequent co-invasion of this parasite. Globally, the severe effects on native freshwater fish hosts by L. cyprinacea have been well documented; however, the first study on the impact of this co-invader on native fish health in South Africa is the recent work by Welicky et al. (2017). In their paper, the authors reported on the change in host health following a natural drought induced treatment for L. cyprinacea, leaving hosts without this parasite in a much better overall health state than those infected. Future work should include host immune response to infection as well as laboratory based studies on the effect of L. cyprinacea on host fitness.

Argulus japonicus

With a very low host specificity, and one of its hosts from its native range (C. carpio) being considered among 100 of the world's worst invasive alien species (Lowe et al., 2000), it is no surprise that the Japanese fish louse, A. japonicus, is one of the most prevalent and widespread co-invaders in South African freshwater systems. Although reports exist that C. carpio, and its other native host, the goldfish Carassius auratus, were already introduced into South Africa in 1859 and 1726 respectively (De Moor and Bruton, 1988), the first official record of the co-invading A. japonicus was only in 1983. Kruger et al. (1983) reported it from 11 hosts, including C. carpio, from two sites (Lake Baberspan and Bloemhof Dam) in the Orange-Vaal River system (Table 1, Fig. 2B). However, it was clear that the introduction of A. japonicus happened much earlier, with Van As and Basson (1984) adding another five hosts and four more localities, including sites from the Crocodile River (West) (Hartbeespoort Dam and Roodeplaat Dam), showing a wide spread occurrence not typically associated with a recent introduction. Van As (1987) supported this and went further by proposing that the records of Argulus spp. by Du Plessis (1952) and Lombard (1968) from the South African Mpumalanga Province were in fact A. japonicus, indicating a much earlier introduction. Following the above reports, additional records of its co-invasion have been published, clearly indicating its wide distribution throughout South Africa (Fig. 2B) and successful spillover onto at least nine native hosts (Avenant-Oldewage, 1994, Avenant-Oldewage, 2001). Although more recent work on A. japonicus in South Africa focussed on its anatomy, ultrastructure, and reproduction (Tam and Avenant-Oldewage, 2006, Avenant-Oldewage and Everts, 2010), there are still gaps in our knowledge on the full extent of its distribution throughout South Africa and its impact on native fishes at population and community levels.

Confirmed co-introduced freshwater fish parasites

Phylum Euglenozoa

Ichthyobodo necator

The ectoparasitic flagellate I. necator has been implicated in disease and mortality of cultured fish globally and is, amongst other things, probably the major cause of death of cultured salmonid fry in Scottish fish farms (Robertson, 1985). In South Africa, specimens identified as I. necator have been reported in the early 1980s from three native cyprinids and the alien C. carpio. These specimens were collected from impoundments in two rivers in the Limpopo Province (Paperna and Van As, 1983, Van As and Basson, 1984), and an aquaculture facility and a river (Kouga River) in the Eastern Cape Province of South Africa (Van As and Basson, 1984) (Fig. 2C). More recently, Ichthyobodo Pinto, 1928 isolates collected from pond-reared koi-carp C. carpio fry from South Africa (specific locality not known) were included in a molecular study by Todal et al. (2004) that aimed to test previous suggestions that I. necator comprises a complex of species. Todal et al. (2004) concluded that there were at least eight strains or species from the 14 isolates tested. The South African isolate showed the highest sequence similarity with the isolate from C. auratus collected in Singapore and grouped together with isolates from an Apistogramma sp. (Brazil) and a Morone Mitchill, 1814 hybrid (USA) (Todal et al., 2004). This molecular evidence suggests that the Ichthyobodo isolate from C. carpio in South Africa can be considered as co-introduced. However, the I. necator identified from native fishes needs to be molecular characterised in order to determine whether they are co-invaders spilled over from C. carpio or are a native South African sibling species.

Trichodina acuta

The mobilid peritrich, T. acuta, is a known invasive parasite and has, since its original description, been reported from at least seven different non-native regions (Basson and Van As, 1993). In South Africa, Basson et al. (1983) reported T. acuta from four cichlids and two cyprinid species collected at more than six different localities in the northern provinces of South Africa. These hosts included T. acuta's type host, C. carpio, and thus further strengthened their conclusion that this parasite is a co-introduced species that spilled over to South African native fishes. However, in their remarks on the species, Basson et al. (1983) commented on the distinct variability in size and denticle dimensions between the South African population and those reported from Israel and the Philippines. Van As et al. (1984) also reported what they identified as T. acuta from a Fisheries Research Station where it was implicated in the mortalities of two different fish species. Bruton and Merron (1985) and De Moor and Bruton (1988) further included this species in their respective lists of confirmed invasive aquatic invertebrates. In their review on the taxonomic status of fish ectoparasitic trichodinids, Van As and Basson (1989), with new information available to them, re-evaluated their original records of T. acuta from South Africa. By using additional characteristics which enabled them to provide a better understanding of differences in denticle shape, Van As and Basson (1989) described what was previously identified as a South African population of T. acuta, as all belonging to a new species, Trichodina compacta Van As and Basson, 1989, thereby removing T. acuta from the list of invasive parasites from South Africa. However, a few years later, Basson and Van As (1993) accurately identified T. acuta in South Africa and this time on rainbow trout, Oncorhynchus mykiss (Walbaum, 1792). This species was collected from a cage culture on a trout farm in the Free State province of South Africa (Table 1, Fig. 2D) confirming its status as a co-introduced parasite in South Africa. Basson and Van As (1993) also provided a detailed discussion on possible routes of introduction into South Africa, especially since its native hosts are European and Asian cyprinids and not salmonids, and concluded that it must have been a recent introduction and future research should focus on the potential spillover to South African native hosts.

Trichodina mutabilis

The history of discovery of T. mutabilis from South Africa is similar to that of T. acuta (see above) and thus not repeated here in detail. In short, Basson et al. (1983) reported this species from various invasive and native hosts in South Africa and then later Van As and Basson (1989) redescribed those specimens thought to be T. mutabilis as two species new to science, Trichodina kazubskii Van As and Basson, 1989 parasitising native fishes and Trichodina uniforma Van As and Basson, 1989 from the introduced C. auratus (see section 3.2.4). More than ten years later, Mouton et al. (2001) reported T. mutabilis again from South Africa, describing this parasite from C. carassius during a health survey of ornamental fishes imported to South Africa (Table 1, Fig. 2D). The fact that spillover of T. mutabilis to native non-cyprinid hosts in India (Mitra and Bandyopadhyay, 2005), and its heavy infection on moribund C. carpio in an aquaculture facility in the USA (Kritsky and Heckmann, 2002) has been reported, shows the potential threat of this co-introduced parasite to both native species and aquaculture in South Africa.

Trichodina reticulata

As one of the most prevalent ectoparasites of the goldfish, C. auratus, it is not surprising that T. reticulata has a similar global distribution to that of its popular ornamental fish host. Basson and Van As (1993) found this to be true when they recorded T. reticulata from C. auratus obtained from a local ornamental fish distributor in Bloemfontein, South Africa (Table 1, Fig. 2D). Notwithstanding being reported from more than 12 countries (Martins et al., 2012), it has never been implicated in spillover to native hosts. This is confirmed by the study of Dove and O'Donoghue (2005) who examined 2003 fishes belonging to 33 species from 58 sites in Queensland, Australia, and only found T. reticulata on wild caught C. auratus and another introduced species, the Eastern mosquitofish Gambusia holbrooki Girard, 1859. Based on current available information, it is most likely that if T. reticulata does get into South Africa's natural waterways it will remain a co-introduced parasite with a low possibility of spillover, however this needs to be further investigated.

Trichodina uniforma

As mentioned above (section 3.2.2), T. uniforma described by Van As and Basson (1989) from C. auratus was originally identified as the invasive T. mutabilis. The same authors further concluded that despite extensive surveys throughout southern Africa, they did not find this species in any other locality other than the original fish farm in the Komatipoort River, which they described it from, nor on any other hosts other than the introduced C. auratus (Table 1, Fig. 2D). This raised the question as to whether T. uniforma was co-introduced with C. auratus or if it was spillback from its native hosts. Since its description in 1989, various authors have reported this species from (amongst other hosts) C. auratus and C. carpio from their native range in China (see Tang et al., 2007, Qi et al., 2011, Li et al., 2014), thus confirming its status as a co-introduced parasite in South Africa. Recently, Tang and Zhao (2016), using 18S rDNA, supported Van As and Basson (1989) morphological identification of T. uniforma as a separate species to T. mutabilis.

Atractolytocestus huronensis

One of the most recent reports of a co-introduced parasite from South Africa is that of the cestode A. huronensi. Scholz et al. (2015) reported this tapeworm from the intestine of C. carpio from four localities in the Limpopo Province of South Africa (Table 1, Fig. 3B). Their paper was also the first to include morphological and molecular confirmation of the identity of the introduced parasite. Although Scholz et al.'s (2015) report on this co-introduction is recent, the co-introduction of A. huronensi into South Africa might not be. During parasitological surveys conducted between 2013 and 2016 by the authors of this review in the Vaal River (North West Province), as well as in the Riet River (Northern Cape Province), A. huronensi specimens were collected from C. carpio at both sites (Smit unpublished records). These records are now included here (Table 1, Fig. 3A) and demonstrate a much wider distribution in different river systems than originally thought, and thus an unlikely pattern usually seen in a recent introduction. We concur with Scholz et al. (2015) that future work on this tapeworm should include phylogeographic studies employing molecular markers to reveal the source of introduction of this co-introduced parasite.

Fig. 3

Maps indicating the South African distribution records for (A)Atractolytocestus huronensis Anthony, 1958; (B)Acolpenteron ureteroecetes Fischthal and Allison, 1940; (C)Dactylogyrus extensus Mueller and Van Cleave, 1932, Dactylogyrus minutus Kulwiec, 1927 and Dactylogyrus lamellatus Achmerow, 1952; (D)Gyrodactylus kherulensis Ergens, 1974.

Acolpenteron ureteroecetes

The first record of a co-introduced parasite into South Africa is, according to our records, that of Du Plessis (1948), who reported the presence of the monogenean A. ureteroecetes in the urethras of three bass species, Micropterus dolomieu (Lacepède, 1802), Micropterus punctulatus (Rafinesque, 1819), and Micropterus salmoides (Lacepède, 1802), bred in the Jonkershoek Fish Hatchery, Western Cape Province. Although all three species were infected, only M. salmoides had high parasite loads that directly lead to the mortality of large numbers of fingerlings (Du Plessis, 1948). Mortality of cultured M. salmoides due to A. ureteroecetes infections were more recently reported by Petrie-Hanson (2001) from pond reared fish in Mississippi, USA, confirming Du Plessis' (1948) original observation of A. ureteroecetes' pathogenicity. The only record of A. ureteroecetes in wild M. salmoides from South Africa is a non-peer reviewed published conference abstract by Matla et al. (2010) reporting a very low infection of this species from the ureter-urinary bladder of M. salmoides collected in the Tzaneen Dam, Limpopo Province (Table 1, Fig. 3B). As the stocking of most of the M. salmoides populations in South Africa was via the Jonkershoek Fish Hatchery (De Moor and Bruton, 1988), the co-introduction of A. ureteroecetes into the Limpopo Province was most likely from the original Jonkershoek Fish Hatchery stock. Research into the parasites of other populations of M. salmoides will most probably reveal a much wider distribution of A. ureteroecetes in South Africa and warrants further research.

Dactylogyrus extensus, Dactylogyrus minutus and Dactylogyrus lamellatus

The three dactylogyrids, D. extensus, D. minutus, and D. lamellatus are well documented known co-invaders, with their widely introduced host, C. carpio, for the former two and the grass carp, Ctenopharyngodon idella for the latter (Dove and Ernst, 1998, Yang et al., 2016). Crafford et al. (2014a) recorded all three of these species from their respective wild caught introduced hosts from the Vaal Dam in the Vaal River, South Africa (Table 1, Fig. 3C), with Dactylogyrus extensus and D. minutus collected from C. carpio, and D lamellatus from C. idella. With representatives of Dactylogyrus Diesing, 1850 considered to be very host specific, the chances of host switching to native fish by these co-invaders are limited (Dove and Ernst, 1998, Simková et al., 2001). This is further supported by the work of Crafford et al., 2012, Crafford et al., 2014a, Crafford et al., 2014b on the monegeneans of fishes from the Vaal Dam, who did not report any spillover of these introduced Dactylogyrus species onto any of the native hosts studied.

Gyrodactylus kherulensis

The gyrodactylid G. kherulensis is a parasite of the common as well as the koi carp, C. carpio koi. Similar to the dactylogyrids reported above, G. kherulensis has also been co-introduced worldwide due to the popularity of its natural host as an aquaculture and ornamental species. The first report of G. kherulensis in South Africa was in a non-peer reviewed published conference abstract by Maseng et al. (2010). These authors collected G. kherulensis from commercially bought, as well as wild caught, C. carpio in the Western Cape Province of South Africa (Table 1, Fig. 3D). Recently Crafford et al. (2014a) found a total of three G. kherulensis specimens on the body surface of a single C. carpio, collected from the Vaal Dam in the Vaal River (Table 1, Fig. 3D), confirming its status as a co-introduced parasite in South Africa.

Ancyrocephalid monogeneans of largemouth bass, Micropterus salmoides

As part of this special issue on invasive parasites, Truter et al. (2017) provided the first peer reviewed published record of five ancyrocephalid monogeneans form largemouth bass, Micropterus salmoides, collected at three localities in South Africa. In that paper the authors provide full descriptions as well as distribution records and maps (see Truter et al., 2017), for these species. For completeness of the current review these species, Clavunculus bursatus (Mueller, 1963), Onchocleidus dispar (Mueller, 1936), O. furcatus (Mueller, 1937), O. principalis (Mizelle, 1936) and Syncleithrium fusiformis (Mueller, 1934) are only listed here and not further discussed.

Parasites of uncertain invasive status

Apiosoma nasalis

This sessile peritrich was originally described from the nasal cavities of cyprinids from the Amur River Basin, Russia; however, in his taxonomic revision of this genus, Lom (1966) suggested that re-examination of live specimens of this species is needed to confirm its identity. Its possible presence in South Africa was first recorded by Viljoen and Van As (1983) from Pseudocrenilabrus philander collected in the Westdene Dam, Johannesburg (Table 1). The authors acknowledged the uncertainty regarding its identity, especially as they collected it from the skin and gills and not the nasal cavities, and therefore proposed that their identification be provisional until more material from other localities and fish species are collected. However, in Viljoen and Van As (1985) the same authors recorded A. nasalis from P. philander, again from the Westdene Dam, but this time without stating any uncertainties. It is thus not clear if the 1985 record was from new material or just a repeat of the 1983 record. As the 1985 record did not include more fish hosts from different localities as proposed by Viljoen and Van As (1983), the invasive status of this species is considered as uncertain.

Trichodinella epizootica and Trichodina nigra

Both T. epizootica and T. nigra were included in the report by Basson et al. (1983) on trichodinids from selected fishes of South Africa (also see section 3.2.1.). Basson and Van As (1993), however, suspected that their original identification was incorrect and that re-evaluation of these species will most likely show that they are not representatives of either T. epizootica or T. nigra. Until proper re-evaluation, we place both these species here in the uncertain invasion status category.

Gyrodactylus kobayashii

The gyrodactylid, G. kobayashii, is a parasite of the goldfish, C. auratus, and has a world-wide distribution due to it being co-introduced with its ornamental fish hosts. In a non-peer reviewed published conference abstract by Maseng et al. (2010), the authors reported G. kobayashii present on both commercially bought, as well as wild caught, C. auratus in the Western Cape Province of South Africa (Table 1). Maseng et al. (2010) did not list the specific locality of the wild caught fish in the conference abstract but indicated the locality as the Kuils River in her unpublished Masters dissertation (Maseng, 2010). As this record of the co-introduction of G. kobayashii into South Africa is in non-peer reviewed publications, these records are classified as uncertain until formal publication thereof.

Pseudodactylogyrus anguillae

The monogenean, P. anguillae, is an ectoparasite originally described from the gills of the Japanese eel, Anguilla japonica Temminck and Schlegel, 1846. Following its original description, it was discovered to have invaded Europe where it was first found in 1977 on the gills of the European eel, Anguilla anguilla from an eel farm in the western Soviet Union (Buchmann et al., 1987). Pseudodactylogyrus anguillae has subsequently been recorded from wild populations of the American eel, Anguilla rostrata (Lesueur, 1817) in Canada (Cone and Marcogliese, 1995) and the USA (Hayward et al., 2001). The first report from South Africa was by Christison and Baker (2007) who reported P. anguillae from the gills of the longfin eel, Anguilla mossambica collected from four rivers in the Eastern Cape (Table 1). Parker et al. (2011) and McHugh et al. (2017) subsequently extended the distribution range by including additional sites from the Eastern Cape (Table 1). However, Ogawa et al. (2015) and McHugh et al. (2017) raised concerns about the identity of what was thought to be P. anguillae from South Africa as its origin in this region is uncertain since no record of the introduction of A. japonica, or any other non-native eels into South Africa, can be found (Ellender and Weyl, 2014). Until further molecular analysis on the South African population of P. anguillae, using a combination of different genetic markers, has been completed and its identity confirmed, we provisionally assign this species to the uncertain invasive status category.

Achtheres pimelodi (syn. Achtheres micropteri)

The lernaeopodid copepod, A. pimelodi, is an ectoparasite found on the gills of various fish host in the USA, including the smallmouth bass, M. dolomieu (Muzzall and Whelan, 2011). Barnard (1955) presumed that A. pimelodi (using the synonym A. micropteri) might have been introduced into South Africa with the smallmouth bass, M. dolomieu, but it is not clear whether he actually collected any from South Africa. Later, Fryer (1968) listed this species (also using the synonym A. micropteri) in his paper on the distribution of parasitic Crustacea from African freshwater fish, but once again there was no indication on whether he collected any himself or if he was just referencing Barnard (1955). No other record of this parasite from South Africa exists and thus its current status as alien in South African waters is doubtful and needs further study.

Species previously reported as invasive but hereby removed from the list

Trichodina pediculus

Basson et al. (1983) originally reported Trichodina pediculus Ehrenberg, 1838 from two cichlids in South Africa, but later Van As and Basson (1989) corrected the original identification and described the original specimens as Trichodina magna Van As and Basson, 1989. This correction was confirmed by Basson and Van As (1993), and as no further reports of T. pediculus from South Africa exists, it is hereby removed from the list of invasive freshwater fish parasites of South Africa.

Conclusions and future direction

All previously reported alien freshwater fish parasites were reviewed and categorised according to their invasive status. Based on available information, seven species were classified as co-invasive, 16 as co-introduced, six as uncertain invasive status, and a single species previously reported as invasive was removed from the list. The total confirmed number of alien parasites (23) in South Africa is low when considering that at least 17 species of alien freshwater fishes are established in South African waters, with the majority of the first introductions dating back to the mid twentieth century (Ellender and Weyl, 2014). Possible reasons for the low numbers of alien parasites might include that the original introductions where from stock already low in parasite diversity, for example, largemouth bass were introduced into South Africa from breeding facilities in Europe (De Moor and Bruton, 1988); or that the South African environment, although suitable to the host, is not suitable for its parasites. However, the most likely reason is probably the lack of extensive parasitological surveys in all the different regions of South Africa, as the current distribution records of alien parasites in South Africa is more related to the distribution of fish parasitologists than that of the parasites themself [see Van As (2015) and Smit and Hadfield (2015) for reviews on the history of fish parasitology in South Africa]. A more targeted approached focussing specifically on South Africa's coastal provinces should provide more accurate information on the current distribution and diversity of invasive freshwater fish parasites.

The role of invasive parasites in mass fish-kill events in natural systems has already been established, for example, in Australia Langdon et al. (1985) identified invasive Chilodonella spp. as the main cause of death of native fish in the Finke River near Alice Springs (also see section 2.1.3.). In South Africa, mass fish-kill events are often reported and usually attributed to sudden change in water temperature, oxygen levels, and stressors such as pollution, and potentially even invasive fishes (Wepener et al., 2011), however, thus far invasive parasites have not been considered as a contributing factor or even the cause of these incidents. Future research on invasive parasites in South Africa should therefore include their potential role in mass fish-kill events.

To date, no research in South Africa (and very limited internationally) has focussed on the co-introduction of parasites by translocated species, especially those that were introduced through inter-basin water transfer schemes. Ellender and Weyl (2014) listed 21 extralimited fish species that were already established in their new environments. Future research should therefore also focus on the parasites of these species in both their native and introduced range, as well as the possible spillover to native fishes.

One of the biggest challenges when working with invasive parasites is the confirmation of the identity of the species, especially if representatives of the same family or even genus occur naturally in that region. We therefore propose that all future work on invasive parasites should include both morphological and molecular approaches when determining the species. It is also of utmost importance to deposit voucher specimens into recognised collection facilities for future verification, comparison, and research in general.

Although this review specifically deals with freshwater fish parasites introduced into South Africa, the information presented on the majority of the different parasites is also applicable to the rest of Africa and other countries worldwide. Similarly, the need for future research on the role of invasive parasites in fish-kills, parasites introduced by extralimited fishes, as well as the molecular identification and deposition of voucher specimens, should be prioritised globally.

Conflict of interest

The authors declare there is no conflict of interest.