Abstract
African Zoology 2015, 50(2): 79–92 Copyright © The Authors Printed in South Africa AFRICAN ZOOLOGY ISSN 1562-7020 EISSN 2224-073X Open Access article distributed under the terms of the http://dx.doi.org/10.1080/15627020.2015.1043644 Creative Commons Attribution License [CC BY 4.0] (http://creative.commons.org/licenses/by/4.0) Review Paper Marine fish parasitology in South Africa: history of disco very and future direction Nico J Smit* and Kerry A Hadfield Water Research Group (Parasitology), Unit for Environmental Sciences and Management, Potchefstroom Campus, North-West University, Potchefstroom, South Africa * Corresponding author, email: nico.smit@nwu.ac.za Almost 200 years have passed since the first description of a marine fish parasite from South Africa. It is therefore an opportune time to look back, take stock of and reflect on the history of discovery within this field and, based on what we know, propose the future direction for research. The aim of this paper is hence to provide some background information on the growth in our knowledge and understanding of the major groups of marine fish parasites and to give an account of how pioneers, such as Barnard, Stebbing, Fantham and Kensley, led the age of discovery and exploration in marine fish parasitology in South Africa. The paper also presents a brief overview of the contributions made by internationally acclaimed parasitologists, such as Rodney Bray and Angela Davies, to our knowledge of marine fish parasites from this region and also to acknowledge the role played by the South African parasitologists, especially over the past 30 years. A rich base of fundamental knowledge is available in South Africa and this research field continues to grow. The prognosis for the future of marine parasitology in South Africa is good; however, as we continue to acquire and record new information about species, it is proposed that future research should be more focused on the lesser studied groups, such as monogeneans, protists and Myxozoa, as these have received uneven attention to date. In addition, it is proposed that the scope of research on marine fish parasitology be broadened to include ecological and applied aspects, using modern techniques. Keywords: biodiversity, fish parasites, marine, South Africa Introduction According to FishBase (Froese and Pauly 2015), South main role-players in this field and, finally, based on what Africa is host to more than 1 900 fishes including many we already know, to provide suggestions for future research endemic species (approximately 47), specifically on the following international trends and local needs. This paper unique south coast, where the Atlantic and Indian Oceans is not intended to serve as a checklist for the marine fish meet. This mix of the cold, nutrient-rich Benguela Current parasites in South Africa but highlights some of the informa- flowing northwards from Antarctica, with the warm Agulhas tion available on the parasitic groups as well as the growth Current flowing southwards from the tropics, creates an or lack of knowledge in certain fields. Due to the intercon- area with one of the highest levels of marine biodiver- nectivity of the marine environment and global distribution sity. South Africa has been identified as one of the 17 of many fish species, when discussing specific groups of ‘megadiverse’ countries in the world (Mittermeier et al. parasites the focus will remain on those species with South 1997), but the species richness of South African marine Africa as its type locality. Authorities are provided for the systems has rarely been investigated (Griffiths et al. 2010). parasite species only and not for the fish hosts. Even if calculated quite conservatively, using the assump- tion that each fish species harbours at least one unique Crustacean parasites species of parasite (Adlard et al. 2015), it is estimated that many of South Africa’s marine fish parasites are The first marine parasite, to the authors’ knowledge, to be still awaiting discovery. It should, therefore, come as no recorded from a South African fish host was in 1818 when surprise that much work still remains to be done by parasi- William Elford Leach described an externally attaching tologists in this region, even though almost 200 years have crustacean, the isopod, Anilocra capensis Leach, 1818, passed since the first description of a marine fish parasite found in the waters around the Cape of Good Hope, Cape from South Africa. Town (Leach 1818). The three syntypes Leach described The aim of this review is thus to provide an account of the are still housed in the Natural History Museum, UK (BMNH history of discovery of marine fish parasites in South Africa, 1979.329) without additional information. As these cymothoid as well as to give background information on some of the isopods are, in parasitological terms, very large (50 mm) African Zoology is co-published by NISC (Pty) Ltd and Taylor & Francis 80 Smit and Hadfield and easily observed and collected by fish biologists (Smit et African Crustacea, including a guide to the marine isopods al. 2014), it is to be expected that they were the first marine from this region (Kensley 1978). The guide reports parasites to be collected from this region. 275 isopod species of which only 12 were cymothoids Throughout the 1800s, this trend continued with the and four were gnathiids. He later compiled an updated majority of new species added to the South African fish checklist of the marine Isopoda from the Indian Ocean, parasite fauna being large conspicuous species. In addition increasing the number of cymothoids to 16 but did not add to the isopods, the Copepoda also started to receive any new information on the gnathiids from South Africa attention. Copepods are, by far, the largest group of parasitic (Kensley 2001). Crustacea with the highest number of species, and they No more research was done on parasitic Isopoda until often parasitise both freshwater and marine fishes. Although the late 1900s, when researchers under the leadership smaller than parasitic isopods, these crustaceans are still of Prof. Jo van As and Prof. Linda Basson of the Aquatic easily observed with the naked eye and can have many Parasitology Research Group (APRG), Department of detrimental effects on their fish hosts (Johnson et al. 2004). Zoology and Entomology, University of the Free State During the 1800s many marine parasitic Crustacea (UFS), started publishing results on gnathiid isopods. The were described from various localities around the world; first two papers were extensions of Barnard’s work as however, many years passed before they were reported Smit et al. (1999) had redescribed Gnathia africana and from South Africa. Interestingly, the start of marine provided notes on the infective praniza larvae stages. parasitology in South Africa in the 1900s was characterised Smit et al. (2000) went on to describe the adult female of by a group of scientists with a wide range of interests and G. africana and after further studies the authors were able an incredible ability to publish their discoveries. Only a few, to construct the lifecycle of G. africana (Smit et al. 2003a). if any, would have described themselves as parasitologists; While conducting experiments on these gnathiid isopods, however, through their research on the biodiversity of Smit and Davies (1999) were also working on the blood South Africa they played a major role in the discovery and parasites transmitted during their feeding phases (see the documentation of marine fish parasites. These researchers section on Apicomplexa (sporozoans) given below). include Reverend Thomas Roscoe Rede Stebbing, Revision of another Barnard species (G. cryptopais) Dr Keppel Harcourt Barnard and later Dr Brian Kensley, yielded the first Caecognathia Dollfus, 1901 species in all contributing hugely to our current understanding of the South Africa. The distinguishing characteristics of the crustacean fish parasites of South Africa. gnathiid frontal border allowed for this relocation and thus, G. cryptopais became Caecognathia cryptopais and Isopoda is currently the only species of this genus in South Africa A series of papers published by Stebbing in the early (Smit et al. 2000). Furthermore, two new species, G. nkulu 1900s catalogued the South African crustaceans with notes Smit & Van As, 2000, and G. pantherina Smit & Basson, on both the parasitic isopods and copepods (Stebbing 2000, were also described from the Cape south coast 1902, 1910). These papers mostly listed known species of South Africa shortly thereafter (Smit and van As 2000; (described from elsewhere in the world) from South Africa Smit and Basson 2002). Gnathia pantherina was the first as well as giving a brief account of the species synonymy. gnathiid to be collected on elasmobranch fishes and was Shortly thereafter, Barnard described the first gnathiid described from a leopard catshark, Poroderma pantherinum; isopod from South Africa, Gnathia africana Barnard, 1914 a puffadder shyshark, Haploblepharus edwardsii; and a from False Bay, as well as G. spongicola Barnard, 1920; blackspotted electric ray, Torpedo fuscomaculata. After G. disjuncta Barnard, 1920; and G. cryptopais Barnard, pathology studies on these sharks, it was also noted that 1925 from the south coast of South Africa (Barnard 1914a, G. pantherina juveniles cause significant focal damage 1920, 1925a). These gnathiid isopods are temporary to the gill septum indicating a possible negative impact ectoparasites with three parasitic juvenile stages and on these hosts if infected with high numbers of gnathiids free-living adults (Smit and Davies 2004) and although (Hayes et al. 2007). At this point all the gnathiid isopods Barnard did record the parasitic juveniles, he was never from South Africa were collected from the colder south able to identify their hosts. Only 85 years after the descrip- coast waters, but based on the knowledge that these tion of G. africana was the world introduced to its hosts, a parasites thrive in warmer waters, it was assumed that more variety of intertidal fish, including the super klipfish, Clinus species would occur in the warmer east coast waters. This superciliosus (see Smit and Davies 1999). was confirmed when G. pilosus Hadfield, Smit & Avenant- Barnard worked on many different groups of organisms in Oldewage, 2008, along with its lifecycle, was described from South African waters, including molluscs, insects and fish; Sheffield Beach, South Africa (Hadfield et al. 2008, 2009). however, his main interest was undeniably crustaceans with In 2008, Hadfield and Smit (2008) described a new a series of publications published from 1914 to 1955 on the genus and species of the gnathiid isopod, Afrignathia various orders within the Crustacea. Many new recordings multicavea Hadfield & Smit, 2008. This monotypic genus of known species were made in these papers, adding has only been found in South Africa. It is distinctive based species numbers to the South African fauna and knowledge on a number of features not seen in any of the other on these lesser studied organisms, including some parasitic genera, such as a pylopod consisting of only one article, cymothoid species (Barnard 1914b, 1925b, 1940, 1955b). a mandible with two rows of unequal teeth on the blade The South African zoologist, Brian Frederick Kensley, and apex, and unknown cephalon appendages (possibly followed in the footsteps of Barnard, focusing on crustacean maxillae 1), which are usually absent in all known male research. He published numerous papers on the South gnathiids (Hadfield and Smit 2008). Five specimens of African Zoology 2015, 50(2): 79–92 81 this species were originally collected from the south coast Currently, the gill-attaching genus, Mothocya, is also between 1961 and 1972, but no further collections have being revised for the region, with another new species since been made. from Sodwana Bay (Hadfield et al. 2015). This genus is After years of no new information on the cymothoids, one of the more widespread gill parasitic genera, often Wright et al. (2001) published ecological information on the with a laterally twisted body caused by the shape of the external parasite, Anilocra capensis, and its influence on the gill arches and operculum. Only one species, Mothocya host fish Pachymetopon blochii. Since 2010, the research melanosticta Schioedte & Meinert, 1884, was thought to group of the authors of the present review paper (NJS and occur in South Africa; however, upon closer examination KAH) and collaborator Dr Niel Bruce, Museum of Tropical of the specimens, this proved to be a misidentification. The Queensland, Australia, have focused on the taxonomic other specimens studied added two known species to the revision of these cymothoid isopods. This work was long South African fauna as well as a new species, bringing the overdue as many of the known South African isopods total number of Mothocya species in South Africa to three have been incorrectly identified. These revisions have led (Hadfield et al. 2015). This work on the parasitic isopods, to the publication of a revision of four of the mouth- and and especially on the Cymothoidae, is necessary in order gill-inhabiting genera from South Africa, and included the to gain an understanding of specific species and numbers description of several new species (see below). present and the effects these parasites have on their fish One of the most unique cymothoid isopods in South hosts. There are significant variations in the morphological Africa is Cinusa tetrodontis Schioedte and Meinert, 1884. differences between species; however, with the current This monotypic genus has only been found in South Africa molecular drive in science, this setback should be resolved and only in the mouth of one host, the evil-eye pufferfish, and hopefully these lesser understood parasites will be Amblyrhynchotes honckenii. Unlike most South African given more attention. cymothoids, this species seems to be extremely host specific and is found on the palate and not over the tongue Copepoda like other buccal cavity cymothoids (Hadfield et al. 2010). Copepods, although generally smaller than cymothoid Almost 200 years after the first cymothoid isopod from isopods, are common on wild and captive fish and South Africa had been described, Hadfield et al. (2013) frequently observed and studied by taxonomists, ecologists described the tongue-replacement isopod, Cymothoa and pathologists. The first two copepod species from South sodwana Hadfield, Bruce & Smit, 2013 from the host, Africa were Medesicaste penetrans Heller, 1865, and Trachinotus botla, or wave garrick, from Sodwana Bay. Pandarus armatus Heller, 1865 (now Pandarus cranchii This poorly understood genus and its species from the Leach, 1819), described from the Cape of Good Hope on south-western Indian Ocean were also revised (Hadfield et the Cape gurnard Trigla capensis (now Chelidonichthys al. 2013). During the same year Parker and Booth (2013) capensis) and on Scyllium africanum (now Poroderma published details regarding the detrimental effects this africanum), respectively (Barnard 1955a). Thirty years on, parasite has on its fish host, together with comprehen- Achtheinus pinguis Wilson, 1912 was also described from sive ecological data; however, in their paper the authors the Cape of Good Hope on the sawshark, Pliotrema warreni, identified the parasite as Cymothoa borbonica, Schioedte after being collected in 1898 by Gilchrist (Barnard 1955a). and Meinert, 1884 but in fact it was the same species, Due to the large number of species in the Copepoda, C. sodwana, that had been described a month earlier. many early researchers produced extensive monographs Another noteworthy cymothoid species from South and checklists. Barnard (1948) added new records and Africa was a member of the tongue-replacement isopod of species of parasitic copepods from South Africa, followed the genus Ceratothoa Dana, 1852. For many years, three by a thorough account of the material that was in the South Ceratothoa species were recognised from South African African Museum (SAM) and had been donated to him at marine waters, namely Ceratothoa imbricata (Fabricius, that time (Barnard 1955a). In these papers he described 1775); C. retusa (Schioedte & Meinert, 1883); and Caligus lalandei Barnard, 1948; C. engraulidis Barnard, C. trigonocephala (Leach, 1818). A recent study by Hadfield 1948; C. tetrodontis Barnard, 1948; Lepeophtheirus et al. (2014a) indicated that the latter two species were in brachyurus Barnard, 1948; L. plotosi Barnard, 1948; fact misidentifications of another species that was described Hatschekia acuta Barnard, 1948 (now Hatschekia conifera in their paper as Ceratothoa famosa Hadfield, Bruce & Smit, Yamaguti, 1939); Chondracanthus congiopodi Barnard, 2014. This species was aptly named for being famous as 1955 (now Chondracanthus tuberculatus Nordmann, the photograph of it inside the mouth of Diplodus sargus 1832); Acanthochondria lepidionis Barnard, 1955; capensis from Tsitsikamma National Park went viral on the and Eubrachiella sublobulata Barnard, 1955. Caligus internet and has since been used in many media reports hottentotus Barnard, 1957 was described shortly thereafter worldwide, including daily news reports, documentaries, on the Hottentot fish (Pachymetopon blochii) from Table nature programmes, magazines, children’s books, and even Bay together with Gloiopotes auriculatus Barnard, 1957 in a Hollywood motion picture called The Bay (see Hadfield (now Gloiopotes watsoni Kirtisinghe, 1934) on a striped et al. 2014a). Along with this species, Ceratothoa africanae marlin (Makaira) caught at Mossel Bay. Hadfield, Bruce & Smit, 2014 was also described, and After Barnard’s extensive reviews, a large number of C. retusa was redescribed (with notes on its variability) in species were deposited in the SAM and thus Kensley Hadfield et al. (2014b). Thus, two species were removed and Grindley (1973) compiled a catalogue of the South and another two were added, leaving the total at three African Copepoda in the museum, including full details of Ceratothoa species in South Africa. all the species where possible. In addition, Kensley and 82 Smit and Hadfield Grindley (1973) added a number of new records for South Oldewage & Van As, 1988 and Ergasilus ilani Oldewage & Africa (and a few other countries too) for numerous known Van As, 1988, both from Mugil cephalus. copepods as well as new species to science. The following In 1994, Oldewage also described the first species were described from South Africa: Lepeophtheirus Holobomolochus Vervoort, 1969 species in South Africa. natalensis Kensley & Grindley, 1973; Lernanthropodes Not only was this a new species and genus record for the natalensis Kensley & Grindley, 1973; Lernanthropus ecclesi country, but it was also the first time this genus had been Kensley & Grindley, 1973; Lernanthropus sarbae Kensley found in the Southern Hemisphere (Oldewage 1994). It & Grindley, 1973; Pseudocycnoides rugosa Kensley & was located off the west coast of South Africa, attached to Grindley, 1973 (now Cybicola armata (Bassett-Smith, the gills and inner opercula of Malacocephalus laevis and 1898); Brachiella lithognathae Kensley & Grindley, 1973 named Holobomolochus maleus Oldewage, 1994 (now (now Sparidicola lithognathi); Lophoura elongata Kensley Hamaticolax maleus). & Grindley, 1973; and Naobranchia pritchardae Kensley & Oldewage and collaborators also compiled and published Grindley, 1973. The latter species was named by Kensley a number of checklists and surveys for specific groups of and Grindley (1973) for the parasitologist Prof. Mary copepods. These include Oldewage and van As (1989) who Hanson Pritchard, University of Nebraska-Lincoln, who compiled a list of the Caligus Müller, 1785 species in African collected many of the species they described in their 1973 coastal waters along with their hosts, location and reference paper. Interestingly, Pritchard was on a six-month visit to for the record. Oldewage and Smale (1993) reported on South Africa in 1961 to collect fish trematodes (digeneans) the parasite fauna of eight shark species from Cape Recife and only collected the copepods on the side. on the south coast of South Africa. Lastly, one of the most After these inclusive and detailed reviews, there seemed comprehensive checklists of parasitic Copepoda of African to be a decline in the number of studies on marine parasitic fishes (freshwater and marine) was assembled by the copepods; however, many noteworthy records were still husband and wife team, Oldewage and Avenant-Oldewage being published but in shorter, more concentrated papers. (1993). This thorough and extensive checklist included all of Most of the research in the mid to late 1900s focused on the valid host diversity and geographical distribution records updating museum records with new biodiversity information published up to that point, and provided a platform for all (Ho 1970, 1972) or on reporting isolated species descrip- future research on these parasites. tions (Dojiri 1989; Oldewage 1989). Although many of Most recently, members of the research group of Prof. these short manuscripts provided only isolated descrip- Susan Dippenaar, Department of Biodiversity, University tions of a single species, such as Caligus saucius Dojiri, of Limpopo (UL) have added contributions to the marine 1989 a parasite of the blenny Cirripectes castaneus from parasitic copepods. In 2000, Dippenaar et al. (2000) the KwaZulu Reef (north of Island Rock), these papers described a new species, Kroyeria deetsi Dippenaar, Benz continued to provide valuable information on the South & Olivier, 2000 from the gills of spinner sharks, Carcharhinus African copepods. The first Lernaeenicus Le Sueur, 1824 brevipinna, collected off the east coast of South Africa. Two species in South Africa was recorded by Oldewage (1989) new species, Pupulina cliffi Dippenaar & Lebepe, 2013 and from the coast off the Kowie River mouth in the viscera P. merira Dippenaar & Lebepe, 2013 were collected from of the whitefin trevally, Carangoides equula. This species the mobulid rays, Mobula kuhlii and M. eregoodootenkee, was named Lernaeenicus kabatai Oldewage, 1989; it was from the east coast of South Africa (Dippenaar and Lebepe in very close proximity to the other known species from 2013). Schistobrachia jordaanae Dippenaar, Olivier & Benz, southern Africa, Lernaeenicus gonostomae Kensley & 2004 was collected from the gill filaments of a diamond ray, Grindley, 1973, located just off the coast of Mozambique. Gymnura natalensis (Dippenaar et al. 2004). Most of the Researchers at the Department of Zoology at the then material used by these authors was collected in collabora- Rand Afrikaans University (RAU; now University of tion with the KwaZulu-Natal Sharks Board, emphasising the Johannesburg [UJ]), in particular Dr Willie Oldewage, role played by the KwaZulu-Natal Sharks Board in shark published a number of papers on marine parasitic research in South Africa. copepods with novel information on new host or locality In addition to the description of new species, the UL and records (Oldewage 1993a, 1993b), redescriptions UFS research groups published descriptions of the unknown (Oldewage 1995), and morphological or life-stage studies adults of known fish parasitic copepods (Dippenaar et al. (Oldewage 1992b, 1993c). During research voyages on 2001; Grobler et al. 2002; Dippenaar and Jordaan 2006), the FRS Africana as part of the hake biomass surveys morphological studies (Dippenaar and Olivier 1999; conducted by the Research Institute for Sea Fisheries, Grobler et al. 2003b, 2004), new host and locality records Oldewage examined 25 species of fish infected with 10 (Dippenaar and Jordaan 2007), and even the rare observa- parasite species (Oldewage 1992a). These included tions of a hypersymbiont found on a copepod parasitising two parasites, Achtheinus oblongus Wilson, 1908 and a marine fish (Olivier et al. 2000). This hypersymbiont on Charopinus dalmanni (Retzius, 1829), located in South the monogenean Udonella Johnston, 1835 had to date been Africa and being recorded for the first time. The trip took found exclusively on caligid copepods, but in this particular place on the south coast of South Africa from Cape case, Udonella myliobati Guberlet, 1936 was found on Agulhas to Port Alfred and 43% of the hake specimens Lepeophtheirus natalensis, an ectoparasite of the spotted collected were heavily infected with Medesicaste penetrans ragged-tooth shark, Carcharias taurus. This fascinating (Oldewage 1992a). The first record of ergasilids from the interaction appeared to show the monogeneans feeding southern half of Africa was reported by Oldewage and on the epithelial cells of the shark skin rather than the fish van As (1988) when describing Dermoergasilus mugilis mucus and gill epithelium ‘kicked’ back by the copepod African Zoology 2015, 50(2): 79–92 83 (Olivier et al. 2000). Subsequently, Grobler et al. (2003a) In a presentation to the South African Association for found another species, Udonella caligorum Johnston, 1835, the Advancement of Science (S2A3), Fantham reported on a Caligus sp. parasitising mullet in Lake St Lucia, also on (amongst other things) on a motile amoeba from the the east coast of South Arica. digestive tract, trypanosomes and haemogregarines from In 2005, Dippenaar performed a detailed literature the blood, coccidia in the intestine, ciliates from the skin search, focusing on South Africa only, and compiled an and gills, and myxosporeans from the gall bladder of mainly updated list of the marine parasitic copepods, including the intertidal fishes (Fantham 1918a, 1918b). Fantham’s tenure hosts known as well as the localities within South Africa at the University of the Witwatersrand in South Africa ended (Dippenaar 2005). At that stage, only 9% of the world’s in 1932 and with it the general interest in fish parasitic siphonostomatoids were reported from southern African protists and Myxozoa for many years to come. However, 50 waters indicating the necessity for increased investi- years later, primarily through the work of the APRG at the gations into this parasitic group. With current research UFS, the enthusiasm to gain knowledge and understanding addressing spatial distribution (Dippenaar et al. 2009), of this group of marine fish parasites was rekindled. cryptic molecular diversity (Dippenaar et al. 2010), and host–parasite associations (Mokumo et al. 2015) in certain Mastigophora (flagellates) species, it will be exciting to observe what the South African Fantham (1918a, 1918b) reported on two trypanosomes copepodologists will produce in the future. in his abstract of the S2A3 presentation mentioned above. These trypanosomes, from a garrick, Lichia amia, and Branchiura a skate, Raja capensis (now Raja clavata), were never Barnard was once again the pioneer for another crusta- named, but still constitute the first records of marine fish cean group, the Branchiura. In his 1955 paper on parasitic trypanosomes from this region. Similarly, Fantham (1919) copepods, Barnard (1955a) described two new species noted, but did not name, trypanosomes from the bamboo of Argulus Müller, 1785 and recorded a third known fish, Box salpa (now Sarpa salpa) and the carpenter sea species to the South African fauna. The two new species, bream Dentex argyrozona (now Argyrozona argyrozona). A. multipocula Barnard, 1955 and A. capensis Barnard, In the same paper, Fantham (1919) also described and 1955 were described from Richards Bay (on the north coast named two trypanosomes from intertidal fishes, namely of KwaZulu-Natal) and Zoetendals Vlei (a coastal indenta- Trypanosoma nudigobii Fantham, 1919 and T. capigobii tion in the Cape Agulhas region of the Western Cape), Fantham, 1919, and a few years later named a third, respectively, and A. belones Van Kampen, 1909 was identi- T. blenniclinii Fantham, 1930, also from intertidal fish fied from Lake St Lucia, KwaZulu-Natal (Barnard 1955a). (Fantham 1930). More than 70 years later, in a study on Following this initial publication, 39 years passed before the blood parasites of intertidal fishes on the west and another Argulus species was described from South Africa. south coast of South Africa, Hayes et al. (2006) detected Argulus kosus Avenant-Oldewage, 1994 was described trypanosomes in the fish blood films that resembled all from a strepie, Sarpa salpa in Kosi Bay (on the north coast three species previously described by Fantham (1919, of KwaZulu-Natal), and a year later A. smalei Avenant- 1930). Due to their similarity to Fantham’s species, Hayes Oldewage & Oldewage, 1995 was described from a unicorn et al. (2006) suggested that these three species may all leatherjacket, Aluterus monoceros from Algoa Bay, Port be polymorphic forms of T. nudigobii, the first species that Elizabeth (Avenant-Oldewage 1994; Avenant-Oldewage had been described by Fantham in 1919. In a follow-up and Oldewage 1995). This latter species was, however, later study, using both morphology and molecular characterisa- synonymised with A. kosus by van As et al. (1999). tion, Hayes et al. (2014) confirmed that these three species The most recent marine argulid to be described from were indeed a single pleomorphic species and based on South Africa was in 2001, bringing the total known number their results these authors proposed that T. blenniclinii of Argulus species in the region to seven (five of which are and T. capigobii are junior synonyms of T. nudigobii. The marine or estuarine). Argulus izintwala van As & van As, genetic results of Hayes et al. (2014) also showed that the 2001 was removed from the skin of the kelee shad, Hilsa South African trypanosome has a phylogenetic affinity with kelee, during surveys of Lake St Lucia on the north coast of marine fish trypanosomes of Norway. KwaZulu-Natal (van As and van As 2001). No subsequent In their first paper, Hayes et al. (2006) already proposed taxonomic studies have been done on this group, but new that T. nudigobii might be transmitted between intertidal host records and redescriptions of older Argulus species fishes at the De Hoop Nature Reserve by the leech (A. multipocula) have been completed (van As et al. 2001; Zeylanicobdella arugamensis De Silva, 1963. Their recent Smit et al. 2005), adding greatly to our knowledge of these paper (Hayes et al. 2014) provided further molecular parasitic crustaceans. evidence that the trypanosomes examined in the fish blood and in the leeches had identical 18S rDNA sequences, Protistan parasites and Myxozoa demonstrating that only a single pleomorphic species was present, thus providing conclusive evidence that The first major contribution to the parasitic protists and Z. arugamensis is indeed the vector of T. nudigobii. The Myxozoa of South Africa was made by British-born Harold Hayes et al. (2014) study was the first in the world to link Benjamin Fantham. In contrast to Stebbing, Barnard the vertebrate hosts and vector of a marine fish trypano- and Kensley, Fantham was a true parasitologist with the some by morphological and molecular means. majority of his research focusing on parasitic protists Despite Fantham (1918b) already reporting a trypano- from a variety of animals inhabiting different ecosystems. some from a skate back in the early 1900s, the first, and 84 Smit and Hadfield to date only, trypanosome described and named from for further proof of this led her to South Africa where she South African elasmobranchs is T. haploblephari Yeld & started a very productive collaboration of research and Smit, 2006, infecting two endemic catshark species (Yeld student training with the APRG at UFS and the research and Smit 2006). The T. haploblephari infection reported by group of the first author (NJS), first at UJ and then at Yeld and Smit (2006) was unique as sharks from all size North-West University (NWU), where she was appointed as and age categories were infected and the parasitaemia Extraordinary Professor in Parasitology until her untimely was relatively high with infections of up to 72 parasites per death in December 2013. In their first paper reporting on blood smear. With South Africa’s high diversity of elasmo- the presence of H. bigemina in South Africa, Smit and branchs it can be expected that many more trypanosomes Davies (1999) mentioned the potential of the larvae of the are in need of discovery. gnathiid isopod Gnathia africana to transmit this haemo- gregarine in South Africa. Professor Davies’s almost Apicomplexa (sporozoans) 30-year search for proof of gnathiid transmission Similar to trypanosomes, Fantham had only mentioned culminated in 2001, on the 100-year anniversary of the the presence of haemogregarines from various marine fish description of the species, with the paper on the life cycle hosts in his 1918 and 1919 publications; however, in his of H. bigemina in its South African host (Davies and Smit 1930 publication, Fantham (1930) described and named 2001). In this breakthrough research paper Davies and a species infecting the intertidal blenny, Parablennius Smit (2001) presented the complete development of cornutus, as Haemogregarina fragilis Fantham, 1930. H. bigemina, in not only the fish host, but also in the larvae Subsequently, this first haemogregarine species from of G. africana that had fed on infected fish. Based on the South African marine fishes got caught up in a taxonomic evidence they provided, it is now generally accepted that roller-coaster ride. First, in 1995, as part of a revision of the gnathiid isopods can also transmit fish blood parasites and Haemogregarinidae, Siddal (1995) moved H. fragilis to the this mode of transmission has been included in general fish genus Desseria, renaming it D. fragilis. Almost 10 years later parasitology textbooks, such as Woo (2006). Smit et al. (2003b) conducted a taxonomic re-evaluation The point that gnathiid isopods are an additional vector of D. fragilis and, based on material from the type host, of fish blood parasites and not the only vector was further synonymised it with the cosmopolitan fish haemogregarine, emphasised when Prof. Davies and colleagues showed Haemogregarina bigemina Laveran & Mesnil, 1901. The that not only can the leech Z. arugamensis transmit a Smit et al. (2003b) paper was, however, not the first report trypanosome, as previously mentioned, but also the of H. bigemina from South Africa. This species’ presence in haemogregarine H. curvata, a double event previously South Africa was already noted by Smit and Davies (1999) unreported from the marine environment (Hayes et al. who found it infecting a variety of intertidal fish of the families 2006). In recognition of her contribution to the advance- Blenniidae, Clinidae and Gobiesocidae. ment of parasitology in Africa, Prof. Davies was awarded With Fantham’s H. fragilis no longer a valid species, the the prestigious Elsdon-Dew Medal of the Parasitological label of first Apicomplexa to be named from South African Society of Southern Africa in September 2013, three marine fishes now belongs to Haemogregarina koppiensis months before she passed away. Smit & Davies, 2001 infecting the evil-eye pufferfish (Amblyrhynchotes honckenii) caught in the De Hoop Nature Ciliophora (ciliates) Reserve (Smit and Davies 2001). This is quite an unusual The first ciliate Fantham (1918a) reported on in his fish haemogregarine in it being an encapsulated gamont presentation to the S2A3, was an organism he proposed with a recurved tail and also displays a unique pattern of to be closely allied to Ichthyophthirius (commonly known intraerythrocytic merogony (Smit and Davies 2005). as freshwater white spot disease), which most likely was Following the description of H. koppiensis, the same Cryptocaryon irritans Brown, 1951, the marine white spot authors (Smit and Davies 2006) described Desseria zei disease. His report also constituted the first documentation Smit & Davies, 2006 from Zeus capensis. A year later, of a disease-causing marine parasite from South Africa, H. curvata Hayes, Smit, Seddon, Wertheim & Davies, 2006 as Fantham (1918a) indicated that ‘much mortality was described from a variety of intertidal fish (see Hayes et occurred’ among fishes with this infection which were kept al. 2006). Up until the description of the latter species, all in an aquarium at St James, Cape Town. More recently, known South African haemogregarines had been reported Vaughan and Christison (2007) reported that since opening from the cold-temperate west coast or the warm-temperate to the public in 1995, the Two Oceans Aquarium in Cape south coast of South Africa. Ferreira et al. (2012) described Town has encountered sporadic outbreaks of C. irritans in the first haemogregarine from teleost fish from the subtrop- a wide diversity of fishes. It is thus of utmost importance ical east coast of South Africa. This species, H. kunegemina to undertake further research on this major pathogen, Ferreira, Smit & Davies, 2012, was detected in the blood of particularly in light of the drive towards marine aquaculture three intertidal blenny species. in South Africa. One of the most intriguing questions when studying fish The second ciliate mentioned by Fantham (1918a) blood parasites is their mode of transmission. This was was a peritrich in the family Trichodinidae and found on one of the main focus areas of the research of the late the gills of a variety of intertidal fish. This parasite was Prof. Angela Josephine Davies from Kingston University, never described and, to the authors’ knowledge, only two UK. In the 1970s she proposed that, in addition to marine tricho-dinids have been described and named leeches, larvae of gnathiid isopods can also transmit fish from South Africa. In contrast to Fantham’s species, both blood parasites (Davies and Johnston 1976). Her search these described trichodinids are endosymbiotic and found African Zoology 2015, 50(2): 79–92 85 in the intestinal and urogenital tracts, respectively. The to be a parasite with a worldwide distribution, infecting a first species, Trichodina luba Basson, Van As & Fishelson, wide range of host species and is responsible for significant 1990, was found in surgeonfish, Acanthurus xanthopterus, economic losses to the fishery sector (Henning et al. 2013). and the second is Trichodina rhinobatae Van As & Basson, 1996 from the lesser guitarfish, Rhinobatos annulatus Helminth parasites (see van As and Basson 1996). The techniques involved in the description of trichodinids from the gills and external The most significant contribution, to our knowledge, of surfaces of marine fish seem to be problematic; however, helminths infecting marine fishes of South Africa was by once these issues have been resolved, many new species Dr Rodney A Bray and colleagues at the Natural History should be described from the South African coast. Museum (NHM), London, UK, who published a series of 10 papers on the helminth parasites of South African marine Myxozoa fishes based on specimens held in the collection of the Early myxozoan research in southern Africa dates back to NHM, SAM, Cape Town or collected by various well-known 1918 when Fantham became the first researcher to report South African biologists. In recognition of their contributions myxosporeans from South Africa, as was the case when Bray (1978, 1985, 1987) and Bray et al. (1988) named he was the first to report the marine fish parasitic protist. new species in honour of some of these researchers; for During the period 1918 to 1930 he reported various types of example, Enenterum elsti Bray, 1978 from the stone-bream myxosporeans from gall bladders of several South African Neoscorpis lithophilus was named for Dr Rudy van fishes, mainly intertidal (Fantham 1918a, 1918b, 1919, der Elst, Oceanographic Research Institute, Durban; 1930). None of his descriptions contained sufficient descrip- Cephaloporus bakeri Bray, 1985 parasitising the red-tail tive information and illustrations, making it impossible to filefish off Sodwana in KwaZulu-Natal was named in honour distinguish them from other similar species and, according of Dr Michael Baker, Rhodes University, Grahamstown; to Reed et al. (2007), are considered to be nomina nuda. Pseudaephnidiogenes rossi Bray, 1985, from the intestine of However, his work was not in vain as it drew the attention the barehead goby, Caffrogobius nudiceps, for Dr Graham of researchers to the possibility of myxozoans inhabiting Ross, Port Elizabeth Museum; Dactylostomum griffithsi the gall and urinary bladders of South African intertidal fish Bray, 1987 for Prof. Charles Griffiths, University of Cape and indirectly led to the description of Ortholinea basma Town; and Acanthocephaloides cyrusi Bray, Jones & Ali, 2000 from the urinary bladder of the agile klipfish, Lewis, 1988 for Prof. Digby Cyrus, University of Zululand. Clinus agilis; subsequently, the descriptions of three more The series was initiated with a paper by Stephen Prudhoe myxozoans followed, namely Ceratomyxa dehoopi Reed, (1956) describing a new trematode and completed 32 years Basson, Van As & Dyková, 2007; C. cottoidii Reed, Basson, later by the tenth and final paper in the series by Bray et al. Van As & Dyková, 2007; and C. honckenii Reed, Basson, (1988), recording a new species of Acanthocephala. As the Van As & Dyková, 2007, collected from the gall bladders major part of our knowledge on South African fish helminths of Clinus superciliosus, C. cottoides and Amblyrhynchotes is acquired from museum collections and donations from honckenii, respectively (Ali 2000; Reed et al. 2007). More fish researchers, it again highlights the importance of recently, Reed et al. (2009) described, but did not name, these types of collections to our understanding of fish a fifth urinary and gall bladder infecting myxosporean parasitology, especially in South Africa. from intertidal fish. They identified the parasite from the gall bladder of Pavoclinis graminis as a Sphaeromyxa Acanthocephala (thorny or spiny-headed worms) species and reported that it constituted the first record of a Two of the papers in the series on South African helminths representative of this genus from South Africa. In addition to by researchers from the NHM mentioned above were on the the urinary and gall bladder infecting species from intertidal Acanthocephala. In the first of these, Bray (1974) described fish, Reed et al. (2007) also described Henneguya clini two new species but only named one, Rhadinorhynchus Reed, Basson, Van As & Dyková, 2007 from the gills and gill capensis Bray, 1974. The second species was consid- arches of C. superciliosus. ered to be a member of the genus Longicollum Yamaguti, The most infamous of all myxosporeans from South 1935 and closely related to a species previously described Africa was described in 1924 by the ichthyologist John from South Africa, L. chabanaudi Dollfus and Golvan, Dow Fisher Gilchrist from the muscles of the Cape sea 1963. Both these species described by Bray were fish, or ‘snoek’, Thyrsites atun. Interestingly, Fantham also collected from the blackhand sole, Solea bleekeri (now played a role in this discovery. In Fantham’s (1919) paper Pegusa nasuta), whereas L. chabanaudi is a parasite he actually proposed that the snoek parasite that Gilchrist of the lemon sole, Barnardichthys fulvomarginata (see originally thought might have been a microsporidian is in Bray 1974). The second paper (number 10 in the NHM fact a myxozoan. Gilchrist (1924) followed Fantham’s series) by Bray et al. (1988) described a new species, advice and correctly described the species as a myxozoan A. cyrusi, already mentioned above (new species named parasite, Chloromyxum thyrsites Gilchrist, 1924 (later in honour of researchers, as described in the section on to be renamed to its currently accepted name of Kudoa Helminth parasites). The type host of A. cyrusi was also the thyrsites). The host of this myxozoan is a large pike-like blackhand sole, but an additional host, the spotted grunter, fish (snoek) that is of great economic importance in South Pomadasys commersoni, was also recorded. Africa. Once infected, the flesh of the fish becomes soft More recently, Amin and Christison (2005) described and liquefies (myoliquefaction) causing a condition termed another new Acanthocephala species from South ‘pap snoek’ by the locals. Today K. thyrsites is considered Africa. This species was collected from the dusky kob, 86 Smit and Hadfield Argyrosomus japonicus from the Breede River Estuary and and added another new species from South Africa. This described as Neoechinorhynchus dorsovaginatus Amin & parasite, collected from a skate in South African waters, Christison, 2005. This species is only the fourth species of was named E. yiae Caira, Rodriguez & Pickering, 2013 and this genus, consisting of almost 90 recognised species, to described from R. cf. miraletus off South Africa. be recorded from Africa and the first from South Africa. Currently, no resident South African parasitologist is working on marine fish parasitic cestodes, even though it is Cestoda (tapeworms) clear from the above discussion that much research on this It comes as no surprise that studies on marine fish group is still required. cestodes from South Africa are scanty as very few marine teleosts are definitive hosts of tapeworms. More often Digenea (endoparasitic flukes or trematodes) the teleosts serve as intermediate hosts of the large Although the parasitic protozoa were the main focus of trypanorhynch order of cestodes that have elasmobranchs Fantham’s research, he is also credited with the first as final hosts (Schramm 1991) as well as members of the description of a marine fish parasitic digenean (trematode) orders (some newly erected) Onchoproteocephalidea from South Africa. In Fantham (1938) the author described Caira, Jensen, Waeschenbach, Olson & Littlewood, a new species, Lecithostaphylus spondyliosomae Fantham, 2014, Phyllobothriidea Caira, Jensen, Waeschenbach, 1938 that he collected in 1920 from a Hottentot fish, Olson & Littlewood, 2014, Rhinebothriidea Healy, Caira, Spondyliosoma blochii, while examining various fishes at Jensen, Webster & Littlewood, 2009, Lecanicephalidea the Marine Aquarium in St James, Cape Town. Although he and Tetraphyllidea sensu lato (see Caira et al. 2014). examined many other Hottentot fish, he found this parasite However, our knowledge of cestodes from this region in only a single specimen. was kick-started by an extensive monograph on South Twenty years passed before the second species, African cestodes of fishes by Dr Edwin Linton, University of Aephnidiogenes rhabdosargi, now Pseudaephnidiogenes Georgia. Linton (1924) was sent a collection of cestodes by rhabdosargi (Prudhoe, 1956) was collected and described Prof. Gilchrist, UCT, to study. In the resulting monograph from the stomach of two specimens of yellow-fin bream Linton (1924) recorded nine different species, four as adults (Rhabdosargus sarba) caught in Durban Bay, South Africa. from elasmobranchs, of which he described two as new to Bray (1984) considered this 1956 paper by Prudhoe as the science, with one Echeneibothrium austrinum Linton, 1924 first of a series of papers on the South African helminths from an unidentified large skate, still valid (now considered accumulated in the Natural History Museum, London. As a rhinebothriidean – see Ruhnke et al. 2015). The remaining mentioned earlier, the second paper in the series dealt five species were larval forms from various teleosts, with the Acanthocephala, whereas the third dealt with including the economically important, shallow-water Cape digeneans, in which Bray described two new species hake, Merluccius capensis and the snoek Thyrsites atun. Of of Enenterum Linton, 1910 (see new species named in the five larvae he was able to identify four to species level honour of researchers in the section on Helminth parasites). and one to genus only. Years later in a study of the major In 1981, while visiting the SAM in Cape Town, Bray endoparasites of the Cape hakes, Botha (1986) found large found in the collection a vial with trematodes collected post-larval stages of Hepatoxylon trichiuri (Holten, 1802) in from the stomach of a luvar, Luvarus imperialis caught off the coelomic cavity of both M. capensis and M. paradoxus; Cape Town. He immediately recognised the significance however, no mention was made of the cestode reported by of the material and presented it to his colleague Dr David Linton (1924) from the same host. In the same year, Payne Gibson also from the Natural History Museum, London. (1986) also studied the parasites of another economically On close examination of these specimens Gibson (1983) important species, the kingklip, Genypterus capensis, and realised that it was the same species as that known as found that these parasites belonged to the same cestode, Distoma gigas Nardo, 1827, a species last collected in H. trichiuri. Payne (1986) concluded that despite high levels the nineteenth century with only seven known specimens. of infestation in large fish this cestode does not pose any With the new morphological information available provided health risks to kingklip. by the South African material he was able to describe a Recently, a group of researchers from the University new subfamily, Kenmackenziinae Gibson, 1983 and within of Connecticut, USA, published three papers on new it a new genus Kenmackenzia Gibson, 1983 with the type species of the diphyllidean cestodes from South African species Kenmackenzia gigas Nardo, 1827. He named elasmobranchs. In the first paper Echinobothrium joshuai both the subfamily and genus for Dr Ken MacKenzie of the Rodriguez, Pickering & Caira, 2011 was described from Marine Laboratory, Aberdeen, in recognition of his contri- the skate, Cruriraja hulleyi, a recently described species of butions to the study of parasites as biological indicators of skate collected off the coast of South Africa (Rodriguez et fish stocks. Years later, the same Ken MacKenzie would al. 2011). This is a unique record as E. joshuai is only one initiate together with Dr Cecilé Reed (UCT) the use of fish of a few diphyllideans known to parasitise deeper-water parasites as biological tags in stock assessments of the elasmobranchs. In the second paper Caira et al. (2013a) economically important sardine, Sardinops sagax, in South described a further two species from the same genus, Africa (Reed et al. 2012). E. dorothyae Caira, Pickering, Schulman & Hanessian, 2013 In papers five to nine of this series Bray (1984, 1985, from the spotted skate, Raja straeleni and E. dougbermani 1986a, 1986b, 1987) laid the foundation of our knowledge Caira, Pickering, Schulman & Hanessian, 2013 from the on South African digeneans through recording a total of 43 lesser guitarfish, Rhinobatos annulatus. In the final paper species of which 18 were new to science, including four Caira et al. (2013b), described a new species from Senegal, new genera. African Zoology 2015, 50(2): 79–92 87 In addition to the series of papers dedicated to the Cape Town, and various international collaborators. Since South African digeneans, Bray (1990, 1991) compiled 2008 these researchers have published a number of reviews on the Hemiuridae (Digenea) from marine fishes papers documenting the biodiversity of teleost and elasmo- of the southern Indian Ocean. In these reviews Bray also branch monogeneans from South Africa. In the first paper recorded species from South Africa. In the first (Bray 1990) the authors reviewed the genus Dendromonocotyle Hargis, he recorded three known species from South Africa for the 1955 from South Africa with a description of two new first time and described Elytrophalloides humerus Bray, species from stingrays (Vaughan et al. 2008; Vaughan 1990 from the large-spot pompano, Trachinotus botla from and Chisholm 2009). A year later Vaughan and Chisholm Sodwana, KwaZulu-Natal. In the second paper (Bray 1991), (2010a) described Heterocotyle tokoloshei Vaughan focusing on the genus Lecithochirium Lühe, 1901, he and Chisholm, 2010 from the gills of a single short-tail recorded six species from South Africa, of which three had stingray, Dasyatis brevicaudata, kept in captivity at the been known previously, but not from this region, and three Two Oceans Aquarium in Cape Town, South Africa. In the new species, of which he only named one, Lecithochirium same year Vaughan and Chisholm (2010b) also described parafusiforme Bray, 1991 from the stomach of the yellow- Neoheterocotyle robii Vaughan and Chisholm, 2010 from edged moray, Gymnothorax flavimarginatus collected at the gills of the lesser guitarfish Rhinobatos annulatus, La Mercy, KwaZulu-Natal. This latter species brought the followed by the description of Myxinidocotyle eptatreti number of known digenean species from South African Vaughan and Christison, 2010 from the skin of the sixgill fishes to around 60 and to the authors’ knowledge not a hagfish, Eptatretus hexatrema (Vaughan and Christison, single new species has been added in the past 24 years. 2010), and that of Gyrodactylus eyipayipi Vaughan, Christison, Hanson and Shinn, 2010 from the skin, gills, flute Monogenea (ectoparasitic flukes) and male brood pouch of captive specimens of the greater In contrast to other parasitic groups, the history of pipefish Syngnathus acus. The latter species was the first discovery of South Africa’s marine Monogenea only began marine Gyrodactylus species reported from the African much later. In the middle of the twentieth century Manter continent (Vaughan et al. 2010). The most recent descrip- (1955) described two new species of monogeneans, tion was that of Pseudoleptobothrium christisoni Vaughan as Squalonchocotyle callorhynchi Manter, 1955 (now and Chisholm, 2011 from the dermal denticles of the dorsal Callorhynchocotyle callorhynchi) and Callorhynchicola skin surface of a single female lesser guitarfish collected off multitesticulatus Manter, 1955 from the gills of the Cape Cape Agulhas (Vaughan and Chisholm 2011). The majority elephant fish, Callorhinchus capensis. This group of of these papers formed part of a study on the monogenean monogeneans is unique in that they only parasitise fauna of elasmobranchs and teleosts for the development chondrichthyan host fishes. Recently, Vaughan and and the improvement of captive husbandry of these fishes in Christison (2012) collected C. callorhynchi again and public aquaria and clearly illustrated the potential of applied used it as a basis for addressing the taxonomic confusion parasitology in the South African marine environment. within this group of parasites. In this paper the authors redescribed C. callorhynchi, providing additional informa- Nematoda (roundworms) tion on its distribution and also proposing novel parame- Compared to the freshwater fish parasitic nematodes, to ters for measuring the haptoral armature of hexabothriids which a comprehensive series of papers was dedicated (Vaughan and Christison 2012). (see the freshwater parasitology review in this issue by As part of their study on the parasitic Copepoda of van As 2015), information on marine nematodes is limited. elasmobranchs, Dippenaar (UL) and colleagues also As was seen in the review of the Cestoda, it would appear reported on new monogeneans from sharks caught by the that the expertise on this group of parasites lay outside the KwaZulu-Natal Sharks Board (see section on Copepoda). borders of South Africa. Nematode species described from In their first paper Bullard and Dippenaar (2003) described South African marine fish mainly comprise the parasitic a new species belonging to a new genus, Branchotenthes species infecting eels, but described from the eels when robinoverstreeti Bullard and Dippenaar, 2003 from the in their freshwater phase, and thus not further consid- bowmouth guitarfish, Rhina ancylostoma. Interestingly, ered here. Although many records exist of Anisakis larvae this was the second time that a South African marine fish from different teleost hosts (see review by Reed 2015), parasite shared a name with Prof. Robin Miles Overstreet, one of the few records of a named marine fish parasitic Gulf Coast Research Laboratory, USA. The first was species from this region is Proleptus obtusus Dujardin, when Bray (1985) named a new genus of digenean 1845 collected from the intestine of the puffadder shyshark for Prof. Overstreet, Overstreetia sodwanaensis Bray, Haploblepharus edwardsii off the De Hoop Nature Reserve, 1985, a parasite of the wide-banded hardyhead silver- South Africa (Moravec et al. 2002). side, Pranesus pinguis (now Atherinomorus lacunosus) Although the species identification of the Anisakis from Sodwana on the South African east coast. In their nematode larvae found in the teleost will always be second paper Bullard et al. (2004) reported the presence of problematic, Mattiucci et al. (2009) recently described a Dermophthirius carcharhini MacCallum, 1926 on the dusky new species, Anisakis nascettii Mattiucci, Paoletti and shark, Carcharhinus obscurus. Webb, 2009 from beaked whales off the New Zealand and To date the largest body of work on South African fish South African coasts using molecular and morphological monogeneans has been done by Dr Kevin Christison, techniques. This allowed them also to identify the potential Department of Agriculture, Forestry and Fisheries, Cape intermediate host, in the case of A. nascettii most probably Town, and by David Vaughan, Two Oceans Aquarium, a cephalopod rather than a fish. However, this shows that 88 Smit and Hadfield the techniques now exist to link the Anisakis larvae found in discovery. On the one hand, this bears testament to our the teleost to the adult parasite in the definitive host. very high diversity, but on the other hand it also leaves us with more challenging and applied research questions. It Minor groups is thus imperative that while we continue to acquire new information and document new species and records, we Hirudinea (leeches) also have to provide answers to more ecological questions, These blood-feeding marine parasites are rarely studied such as life-cycle assessments, the role of parasites in the in South Africa. In 1958, Moore reported on all the food web and trophic transfers, the impact of parasites leeches in the collection of the Natal Museum, adding 18 on the health of fish hosts, and the implications of global new species from four families (Moore 1998). However, climate change for fish populations. The latter is specifically only one of these, Malmiana stellata Moore, 1958 (now of international relevance as global warming could shift the Ottoniobdella stellata), had been recorded from the coastal balance between parasites and hosts (Adlard et al. 2015). waters in South Africa. This species was collected from Answers to these questions will allow us to apply our a toby fish (Tetraodontidae) at Richards Bay. In 2004, knowledge to stock assessments of commercially important Austrobdella oosthuizeni Utevsky, 2004 was described from fishes, health assessments of aquaculture species and Bloubergstrand on the west coast of South Africa, where assessment of ecological changes due to global climate it was found on Jasus lalandii (the Cape rock lobster). shifts. Fortunately, in South Africa there is growing interest Although it was not found on a fish host, Utevsky (2004) in marine parasitology and at least four universities suggested that the leech used the crustacean as a substrate (North-West University, University of the Free State, for cocoon deposition but would still feed on the blood of University of Limpopo and University of Cape Town) and fishes as many other marine leeches do (Meyer and Barden one government department (Department of Agriculture, 1955). Other species of Austrobdella parasitising fish hosts Forestry and Fisheries) have parasitology research groups in other parts of the world provided evidence to support his actively plying their trade in marine fish parasitology. With a notion. Utevsky (2007) then proceeded to describe a new solid foundation built by many internationally and nationally genus and species from South Africa, Lizabdella africana renowned scientists the future of marine parasitology in Utevsky, 2007. This unique species has a paired male South Africa looks bright. gonopore, which separates it from all other known species and genera. It was collected on mullets of the genera References Liza and Mugil (Utevsky 2007). Leeches are also known vectors for blood parasites and in South Africa the leech Adlard RD, Miller TL, Smit NJ. 2015. The butterfly effect: parasite Zeylanicobdella arugamensis was implicated as a vector diversity, environment, and emerging disease in aquatic wildlife. Trends in Parasitology 4: 160–166. of both a haemogregarine and a trypanosome (see earlier Ali MA. 2000. Ortholinea basma n. sp. (Myxozoa: Myxosporea) section on Protistan parasites and Myxozoa). from the Agile Klipfish Clinus agilis (Teleostei: Clinidae), Although these parasites are easily observed on their fish light and scanning electron microscopy. European Journal of hosts, few taxonomists are able to identify them and there Protistology 36: 100–102. are undoubtedly many more marine leeches still unknown Amin OM, Christison KW. 2005. Neoechinorhynchus (Neoechino- from South Africa and awaiting discovery. rhynchus) dorsovaginatus n. sp. (Acanthocephala: Neoechino- rhynchidae) from the dusky kob Argyrosomus japonicas Future direction (Sciaenidae) on the southern coast of South Africa. Systematic Parasitology 61: 173–179. From the history of discovery presented above, it is clear Avenant-Oldewage A. 1994. A new species of Argulus from Kosi Bay, South Africa and distribution records of the genus. Koedoe that over the past 100 years or more of marine fish parasite 37: 89–95. research in South Africa, researchers have always been Avenant-Oldewage A, Oldewage WH. 1995. A new species of actively engaged in increasing our understanding of the Argulus (Crustacea: Branchiura) from a bony fish in Algoa Bay, biodiversity of these parasites from this region. However, it South Africa. South African Journal of Zoology 30: 197–199. is also clear that there was a bias towards certain groups of Barnard KH. 1914a. Contributions to the crustacean fauna of South parasites, especially towards the larger more conspicuous Africa. 1. Additions to the marine Isopoda. Annals of the South species. The known biodiversity of the marine fish parasites African Museum 10: 197–230. thus rather reflects the interests of the specific groups of Barnard KH. 1914b. Contributions to the crustacean fauna of South researchers involved rather than a concerted, systematic Africa. 3. Additions to the marine Isopoda, with notes on some effort to map species distributions of the various parasitic previously incompletely known species. Annals of the South African Museum 10: 325a–358a, 359–442. groups. Groups that are globally very well represented, Barnard KH. 1920. Contributions to the crustacean fauna of South but not to the same extent in the South African fauna, Africa. No. 6. Further additions to the list of marine Isopoda. are the helminths (in general), but more specifically the Annals of the South African Museum 17: 319–438, pls. XV–XVII. monogeneans and digeneans, and also the protists and Barnard KH. 1925a. Description of a new species of Gnathia Myxozoa. These groups are of ecological, veterinary and (Crustacea, Isopoda) from South Africa. Annals and Magazine of economic importance and thus warrant more research from Natural History, series 9 15: 417–418. a South African perspective. Barnard KH. 1925b. Contributions to the crustacean fauna of South The preceding sections also show that throughout Africa. No. 9. Further additions to the list of Isopoda. Annals of the years marine parasitology research in South Africa the South African Museum 20: 381–410. has remained in the comfort zone of exploration and Barnard KH. 1940. Contributions to the crustacean fauna of African Zoology 2015, 50(2): 79–92 89 South Africa. 12. Further additions to the Tanaidacea, Isopoda, new species of Echinobothrium (Cestoda: Diphyllidea) from and Amphipoda, together with keys for the identification of the batoids off South Africa. Comparative Parasitology 80: 22–32. hitherto recorded marine and freshwater species. Annals of the Caira JN, Rodriguez N, Pickering M. 2013b. New African species South African Museum 32: 381–543. of Echinobothrium (Cestoda: Diphyllidea) and implications for Barnard KH. 1948. New records and descriptions of new species of the identities of their skate hosts. Journal of Parasitology 99: parasitic Copepoda from South Africa. Annals and Magazine of 781–788. Natural History 12: 242–254. Davies AJ, Johnston MRL. 1976. The biology of Haemogregarina Barnard KH. 1955a. South African parasitic Copepoda. Annals of bigemina Laveran and Mesnil, a parasite of the marine fish the South African Museum 41: 223–312. Blennius pholis Linnaeus. Journal of Protozoology 23: 315–320. Barnard KH. 1955b. Additions to the fauna list of South African Davies AJ, Smit NJ. 2001. The life cycle of Haemogregarina Crustacea and Pycnogonidae. Annals of the South African bigemina (Adeleina: Haemogregarinidae) in South African hosts. Museum 43: 1–107. Folia Parasitologica 48: 169–177. Barnard KH. 1957. Additions to the fauna list of South African Dippenaar SM. 2005. Reported siphonostomatoid copepods Crustacea. Annals and Magazine of Natural History 12: 1–12. parasitic on marine fishes of Southern Africa. Crustaceana 77: Botha L. 1986. Major endoparasites of the Cape hakes Merluccius 1281–1328. capensis and M. paradoxus, with brief notes on some Dippenaar SM, Benz GW, Olivier PAS. 2000. Kroyeria deetsi n. sp conspicuous ectoparasites. South African Journal of Marine (Kroyeriidae: Siphonostomatoida), a parasitic copepod infecting Science 4: 45–49. gills of spinner sharks, Carcharhinus brevipinna (Müller & Henle, Bray RA. 1974. Acanthocephala in the flatfish Solea bleekeri 1839), in the Indian Ocean. African Zoology 35: 185–192. (Soleidae) from Cape Province, South Africa. Journal of Dippenaar SM, Jordaan BP. 2006. Nesippus orientalis Heller, Helminthology 48: 179–185. 1868 (Pandaridae: Siphonostomatoida): description of the adult, Bray RA. 1978. Two new species of Enenterum Linton, 1910 young and immature females, a first description of the male and (Digenea) in the marine fish Neoscorpis lithophilus (Kyphosidae) aspects of their functional morphology. Systematic Parasitology from the south-western Indian Ocean. Journal of Helminthology 65: 27–41. 52: 131–139. Dippenaar SM, Jordaan BP. 2007. New host and geographical Bray RA. 1984. Some helminth parasites of marine fishes and records of siphonostomatoid copepods associated with cephalopods of South Africa: Aspidogastrea and the digenean elasmobranchs off the KwaZulu-Natal coast, South Africa. families Bucephalidae, Haplosplanchnidae, Mesometridae and Onderstepoort Journal of Veterinary Research 74: 169–175. Fellodistomidae. Journal of Natural History 18: 271–292. Dippenaar SM, Lebepe MC. 2013. Two new species of Pupulina Bray RA. 1985. Some helminth parasites of marine fishes of South van Beneden, 1892 (Copepoda: Siphonostomatoida: Caligidae) Africa: families Gorgoderidae, Zoogonidae, Cephaloporidae, from mobulid rays off South Africa. Systematic Parasitology 85: Acanthocolpidae and Lepocreadiidae (Digenea). Journal of 27–35. Natural History 19: 377–405. Dippenaar SM, Mathibela RB, Bloomer P. 2010. Cytochrome Bray RA. 1986a. Some helminth parasites of marine fishes of oxidase I sequences reveal possible cryptic diversity in the South Africa: families Enenteridae, Opistholebetidae and cosmopolitan symbiotic copepod Nesippus orientalis Heller, Pleorchiidae (Digenea). Journal of Natural History 20: 471–488. 1868 (Pandaridae: Siphostomatoida) on elasmobranch hosts Bray RA. 1986b. Some helminth parasites of marine fishes from the KwaZulu-Natal coast of South Africa. Experimental of South Africa: Santeria rubalo gen. et sp. nov. (Digenea, Parasitology 125: 42–50. Cryptogonimidae). Journal of Natural History 20: 817–823. Dippenaar SM, Olivier PAS. 1999. New morphological information Bray RA. 1987. Some helminth parasites of marine fishes of South of the parasitic copepod Kroyeria dispar Wilson, 1935 Africa: family Opecoelidae (Digenea). Journal of Natural History (Copepoda: Kroyeriidae) from the east coast of South Africa. 21: 1049–1075. South African Journal of Zoology 34: 125–129. Bray RA. 1990. Hemiuridae (Digenea) from marine fishes Dippenaar SM, Olivier PAS, Benz GW. 2001. Kroyeria sphynae of the southern Indian Ocean: Dinurinae, Elytrophallinae, Rangnekar, 1957 (Copepoda, Siphonostomatoida, Kroyeriidae): Glomericirrinae and Plerurinae. Systematic Parasitology 17: first description of the male, supplementary remarks on the 183–217. female, a new geographic record for the species, and a key to Bray RA. 1991. Hemiuridae (Digenea) from marine fishes of the geographic record for the species, and a key to Kroyeria males. southern Indian Ocean: Genus Lecithochirium Lühe, 1901 Crustaceana 74: 883–894. (Lecithochiriinae). Systematic Parasitology 18: 193–219. Dippenaar SM, Olivier PAS, Benz GW. 2004. Schistobrachia Bray RA, Spencer Jones ME, Lewis JW. 1988. Acanthocephaloides jordaanae n. sp. (Copepoda: Siphonostomatoida: Lernaeo- cyrusi n. sp. (Acanthocephala: Arhythmacanthidae) from south- podidae) from gill filaments of a diamond ray (Gymnura east African teleost fishes. Systematic Parasitology 12: 109–116. natalensis) captured in the Indian Ocean and a key to species Bullard SA, Dippenaar SM. 2003. Branchotenthes robinoverstreeti of Schistobrachia, Dendrapta, and Brianella. Journal of n. gen. and n. sp. (Monogenea: Hexabothriidae) from gill Parasitology 90: 481–484. filaments of the Bowmouth guitarfish, Rhina ancylostoma Dippenaar SM, van Tonder RC, Wintner SP. 2009. Is there (Rhynchobatidae), in the Indian Ocean. Journal of Parasitology evidence of niche restriction in the spatial distribution of Kroyeria 89: 595–601. dispar Wilson, 1935, K. papillipes Wilson, 1932 and Eudactylina Bullard SA, Dippenaar SM, Hoffmayer ER, Benz GW. 2004. New pusilla Cressey, 1967 (Copepoda: Siphonostomatoida) on the locality records for Dermophthirius carcharhini (Monogenea: gill filaments of tiger sharks Galeocerdo cuvier off KwaZulu- Microbothriidae) and Dermophthirius maccallumi and a list of Natal, South Africa? Hydrobiologia 619: 89–101. hosts and localities for species of Dermophthirius. Comparative Dojiri M. 1989. Two species of Caligus (Copepoda: Siphono- Parasitology 71: 78–80. stomatoida) parasitic on fishes from Southern Africa. Journal of Caira JN, Jensen K, Waeschenbach A, Olson PD, Littlewood DTJ. Natural History 23: 363–374. 2014. Orders out of chaos – molecular phylogenetics reveals Fantham HB. 1918a. Some parasitic Protozoa found in South the complexity of shark and stingray tapeworm relationships. African fishes and amphibians. South African Journal of Science International Journal for Parasitology 44: 55–73. 15: 337–338. Caira JN, Pickering M, Schulman AD, Hanessian NJ. 2013a. Two Fantham HB. 1918b. Parasitic Protozoa in South African marine 90 Smit and Hadfield fishes. Marine Biological Report, Cape Town 4: 73–74. Hadfield KA, Smit NJ, Avenant-Oldewage A. 2008. Gnathia pilosus Fantham HB. 1919. Some parasitic Protozoa found in South Africa sp. nov. (Crustacea, Isopoda, Gnathiidae) from the east coast of II. South African Journal of Science 16: 185–191. South Africa. Zootaxa 1894: 23–41. Fantham HB. 1930. Some parasitic Protozoa found in South Africa Hadfield KA, Smit NJ, Avenant-Oldewage A. 2009. Life cycle of the XIII. South African Journal of Science 27: 376–390. temporary fish parasite, Gnathia pilosus (Crustacea: Isopoda: Fantham HB. 1938. Lecithostaphylus spondyliosoma n. sp., a Gnathiidae) from the east coast of South Africa. Journal of trematode parasite of the hottentot fish, Spondyliosoma blochii, the Marine Biological Association of the United Kingdom 89: found in South African waters. Transactions of the Royal Society 1331–1339. of South Africa 26: 387–393. Hayes PM, Lawton SP, Smit NJ, Gibson WC, Davies AJ. 2014. Ferreira ML, Smit NJ, Davies AJ. 2012. Unusual haemogregarines Morphological and molecular characterization of a marine fish parasitizing intertidal teleosts from the subtropical east coast of trypanosome from South Africa, including its development in a South Africa, with the description of Haemogregarina kunegemina leech vector. Parasites and Vectors 7: 50. sp. nov. Journal of the Marine Biological Association of the United Hayes PM, Smit NJ, Davies AJ. 2007. Pathology associated with Kingdom 92: 1209–1215. parasitic juvenile gnathiids feeding on the puffadder shyshark, Froese R, Pauly D (eds). 2015. FishBase. World Wide Web Haploblepharus edwardsii (Voigt). Journal of Fish Diseases 3: electronic publication, version (01/2015). Available at http://www. 55–58. fishbase.org [accessed 25 January 2015]. Hayes PM, Smit NJ, Seddon AM, Wertheim DF, Davies AJ. 2006. Gibson DI. 1983. Kenmackenzia gen. nov. and Kenmackenziinae A new fish haemogregarine from South Africa and its suspected subfam. nov. (Digenea, Sclerodistomidae): new taxa to dual transmission with trypanosomes by a marine leech. Folia accommodate the giant trematode Distoma gigas Nardo. Journal Parasitologica 53: 241–248. of Natural History 172: 189–202. Henning SS, Hoffman LC, Manley M. 2013. A review of Kudoa- Gilchrist JDF. 1924. A protozoal parasite (Chloromyxum thyrsites induced myoliquefaction of marine fish species in South Africa sp. n.) of the Cape sea-fish, the “snoek” (Thyrsites atun, Euplin). and other countries. South African Journal of Science 109: 1–5. Transactions of the Royal Society of South Africa 11: 263–273. Ho JS. 1970. Revision of the genera of the Chondracanthidae, Griffiths CL, Robinson TB, Lange L, Mead A. 2010. Marine a copepod family parasitic on marine fishes. Beaufortia 17: biodiversity in South Africa: an evaluation of current states of 105–218. knowledge. PLoS ONE 5: e12008. Ho JS. 1972. Copepods of the family Chondracanthidae Grobler NJ, Christison, KW, van As JG, Olivier PAS. 2003a. (Cyclopoida) parasitic on South African marine fishes. Observations on the development of Udonella caligorum Parasitology 65: 147–158. Johnston, 1835 (Monogenea: Polyonchoinea) on a parasitic Johnson SC, Treasurer JW, Bravo S, Nagasawa K, Kabata Z. copepod species of Caligus (Copepoda: Caligidae), collected 2004. A review of the impact of parasitic copepods on marine from Lake St Lucia, South Africa. African Zoology 38: 393–396. aquaculture. Zoological Studies 43: 229–243. Grobler NJ, van As JG, Olivier PAS. 2002. Description of the Kensley B. 1978. Guide to the marine isopods of southern Africa. previous unknown male of Caligus mortis Kensley, 1970, Cape Town: South African Museum and The Rustica Press. parasite of intertidal fish species from South Africa. Folia Kensley B. 2001. Biogeography of the marine Isopoda of the Indian Parasitologica 49: 131–136. Ocean, with a check-list of species and records. In: Kensley B, Grobler NJ, van As JG, Olivier PAS. 2003b. Additional Brusca RC (eds), Isopod systematics and evolution. Crustacean morphological information on two species of Caligus (Copepoda: Issues 13. Rotterdam: AA Balkema. pp 205–264. Caligidae) parasitic on South African marine and estuarine fish. Kensley B, Grindley JR. 1973. South African parasitic copepods. African Zoology 38: 139–143. Annals of the South African Museum 62: 69–130. Grobler NJ, van As JG, Olivier PAS. 2004. New morphological Leach WE. 1818. Cymothoadées. In: Cuvier F (ed.), Dictionnaire information on the parasitic copepods Caligus epinepheli des Sciences Naturelles, vol. 12. Paris: Strasbourg et Levrault. Yamaguti, 1936 and Caligus rotundigenitalis Yu, 1933 (Copepoda: pp 338–354. Caligidae) from South Africa. Crustaceana 77: 187–196. Linton E. 1924. Gyrocotyle plana sp. nov. with notes on South Hadfield KA, Bruce NL, Smit NJ. 2010. Redescription of the African cestodes of fishes. Fisheries and Marine Biological monotypic genus Cinusa Schioedte and Meinert, 1884 (Isopoda, Survey Report no. 3 for the year 1922. Special report VIII. Cape Cymothoidae), a buccal-cavity isopod from South Africa. Town: Cape Times Ltd. Zootaxa 2437: 51–68. Manter HW. 1955 Two new monogenetic trematodes from Hadfield KA, Bruce NL, Smit NJ. 2013. Review of the fish-parasitic elephant fishes (Callorhynchus) from South Africa and New genus Cymothoa Fabricius, 1783 (Isopoda, Cymothoidae, Zealand. In: Essays in the Natural Sciences in Honor of Captain Crustacea) from the south-western Indian Ocean, including a Allan Hancock, on Occasion of his Birthday, July 26, 1955. Los new species from South Africa. Zootaxa 3640: 152–176. Angeles: University of Southern California Press. pp 211–220. Hadfield KA, Bruce NL, Smit NJ. 2014a. Review of the fish Mattiucci S, Paoletti M, Webb SC. 2011 Anisakis nascettii n. sp. parasitic genus Ceratothoa Dana, 1852 (Crustacea, Isopoda, (Nematoda: Anisakidae) from beaked whales of the southern Cymothoidae) from South Africa, including the description of two hemisphere: morphological description, genetic relationships new species. Zookeys 400: 1–42. between congeners and ecological data. Systematic Parasitology Hadfield KA, Bruce NL, Smit NJ. 2015. Review of Mothocya Costa, 74: 199–217. in Hope, 1851 (Crustacea: Isopoda: Cymothoidae) from southern Meyer MC, Barden AA Jr. 1955. Leeches symbiotic on Arthropoda, Africa, with the description of a new species. African Zoology 50: especially decapod Crustacea. Wasmann Journal of Biology 13: 147–163. 297–311. Hadfield K, Bruce N, Szinetár C, Smit N. 2014b. Ceratothoa retusa Mittermeier RA, Gil PR, Mittermeier CG. 1997. Megadiversity: (Schiœdte & Meinert, 1883) (Isopoda, Cymothoidae), a variable Earth’s biologically wealthiest nations. Monterrey, Mexico: species of fish parasitic marine isopod from the Indian Ocean. Conservation International, CEMEX. Crustaceana 87: 448–462. Mokumo PJ, Dippenaar SM. 2015. Reports of Kroyeria species Hadfield KA, Smit NJ. 2008. Description of a new gnathiid, collected from South African waters with notes on the host– Afrignathia multicavea gen. et sp. n. (Crustacea: Isopoda: parasite associations. African Zoology 50: 127–132. Gnathiidae), from South Africa. African Zoology 43: 81–89. Moore JP. 1958. The leeches (Hirudinea) in the collection of the African Zoology 2015, 50(2): 79–92 91 Natal Museum. Annals of the Natal Museum 14: 303–340. Reed CC, Mackenzie K, Van der Lingen CD. 2012. Parasites of Moravec F, van As JG, Dyková I. 2002. Proleptus obtusus South African sardines, Sardinops sagax, and an assessment Dujardin, 1845 (Nematoda: Physalopteridae) from the puffadder of their potential as biological tags. Bulletin of the European shyshark Haploblepharus edwardsii (Scyliorhinidae) from off Association of Fish Pathologists 32: 41–48. South Africa. Systematic Parasitology 53: 169–173. Rodriguez N, Pickering M, Caira, JN. 2011. Echinobothrium Oldewage WH. 1989. A new species of Lernaeenicus (Copepoda: joshuai n. sp. (Cestoda: Diphyllidea) from the roughnose Siphonostomatoida) from southern Africa. South African Journal legskate, Cruriraja hulleyi (Rajiformes: Rajidae), off South Africa. of Zoology 24: 319–321. Comparative Parasitology 78: 306–311. Oldewage WH. 1992a. Occurrence and distribution of parasitic Ruhnke TR, Caira JN, Cox A. 2015. The cestode order Copepoda (Crustacea) off the southern coast of South Africa. Rhinebothriidea no longer family-less: a molecular phylogenetic South African Journal of Wildlife Research 22: 33–35. investigation with erection of two new families and description of Oldewage WH. 1992b. Description of Perissopus oblongus eight new species of Anthocephalum. Zootaxa 3904: 51–81. (Wilson, 1908) (Copepoda, Pandaridae) from southern African Schramm M. 1991. Grillotia perelica (Cestoda: Trypanorhyncha) sharks with a first description of the male. Crustaceana 63: plerocercoids in mullet (Pisces: Mugilidae) from estuaries in 44–50. Transkei, southern Africa. South African Journal of Marine Oldewage WH. 1993a. Occurrence and distribution of copepod Science 11: 169–178. parasites on the west coast of South Africa. Journal of African Siddal ME. 1995. Phylogeny of adeleid blood parasites with a Zoology 107: 413–418. partial systematic revision of the haemofrefarine complex. Oldewage WH. 1993b. Three species of piscine parasitic copepods Journal of Eukaryotic Microbiology 43: 116–1125. from southern African coastal waters. South African Journal of Smit NJ, Basson L. 2002. Gnathia pantherina sp. n. (Crustacea: Zoology 28: 113–121. Isopoda: Gnathiidae), a temporary ectoparasite of some Oldewage WH. 1993c. Morphological variation in Hatschekia elasmobranch species from southern Africa. Folia Parasitologica conifera Yamaguti, 1939 (Copepoda, Siphonostomatoida) from 49: 137–151. the Southern Atlantic Ocean. Crustaceana 65: 41–45. Smit NJ, Basson L, van As JG. 2000. A redescription of the adult Oldewage WH. 1994. A new species of Holobomolochus Vervoort, male of Caecognathia cryptopais (Barnard, 1925) (Crustacea: 1969 (Copepoda, Poecilostomatoida) from the west coast of Isopoda: Gnathiidae) from southern Africa. Folia Parasitologica South Africa. Crustaceana 67: 324–328. 47: 61–66. Oldewage WH. 1995. Redescription of Alebion carchariae Kroeyer, Smit NJ, Basson L, van As JG. 2003a. Life cycle of the temporary 1863 (Copepoda, Siphonostomatoida) from Isurus oxyrinchus in fish parasite, Gnathia africana (Crustacea, Isopoda, Gnathiidae). South Africa. Crustaceana 68: 38–42. Folia Parasitologica 50: 135–142. Oldewage WH, Avenant-Oldewage A. 1993. Checklist of the Smit NJ, Bruce NL, Hadfield KA. 2014. Global diversity of fish parasitic Copepoda (Crustacea) of African fishes. Zoologische parasitic isopod crustaceans of the family Cymothoidae. Dokumentatie 23: 1–28. International Journal for Parasitology: Parasites and Wildlife 3: Oldewage WH, Smale MJ. 1993. Occurrence of piscine parasitic 188–197. copepods (Crustacea) on sharks taken mainly off Cape Recife, Smit NJ, Davies AJ. 1999. New host records for Haemogregarina South Africa. South African Journal of Marine Science 13: bigemina from the coast of southern Africa. Journal of the 309–312. Marine Biological Association of the United Kingdom 79: Oldewage WH, van As JG. 1988. Two new species of Ergasilidae 933–935. (Copepoda: Poecilostomatoida) parasitic on Mugil cephalus L. Smit NJ, Davies AJ. 2001. An encapsulated haemogregarine from from southern Africa. Hydrobiologia 162: 135–139. the evileye pufferfish in South Africa. Journal of the Marine Oldewage WH, van As JG. 1989. Occurrence and distribution of Biological Association of the United Kingdom 81: 751–754. Caligus (Copepoda: Siphonostomatoida) in African coastal Smit NJ, Davies AJ. 2004. The curious life-style of the parasitic waters. Revue de Zoologie Africaine 103: 91–98. stages of gnathiid isopods. Advances in Parasitology 58: Olivier PAS, Dippenaar SM, Khalil LF, Mokgalong NM. 2000. 289–391. Observations on a lesser-known monogenean, Udonella Smit NJ, Davies AJ. 2005. Intraerythrocytic merogony in the myliobati, from a copepod parasite, Lepeophtheirus natalensis, development of Haemogregarina koppiensis (Apicomplexa: parasitizing the spotted ragged-tooth shark, Carcharias taurus, Adeleorina: Haemogregarinidae). Folia Parasitologica 52: from South African waters. Onderstepoort Journal of Veterinary 277–278. Research 67: 135–140. Smit NJ, Davies AJ. 2006. Desseria zei sp. nov. (Adeleorina: Parker D, Booth AJ. 2013. The tongue-replacing isopod Cymothoa Haemogregarinidae) infecting Zeus capensis from deep waters borbonica reduces the growth of largespot pompano Trachinotus off the south and west coast of South Africa. Journal of the Marine botla. Marine Biology 160: 2943–2950. Biological Association of the United Kingdom 86: 1477–1480. Payne AIL. 1986. Observations on some conspicuous parasites Smit NJ, van As JG. 2000. A new species, Gnathia nkulu sp. n. of the southern African kingklip Genypterus capensis. South (Crustacea: Isopoda: Gnathiidae) from southern Africa. Folia African Journal of Marine Science 4: 163–168. Parasitologica 47: 235–240. Prudhoe S. 1956. On a new trematode from South African fishes. Smit NJ, van As JG, Basson L. 1999. A redescription of the adult Annals and Magazine of Natural History 9: 72–75. male and praniza of Gnathia africana Barnard, 1914 (Crustacea, Reed CC. 2015. A review of parasite studies of commercially Isopoda, Gnathiidae) from southern Africa. Folia Parasitologica important marine fishes in sub-Saharan Africa. Parasitology 142: 46: 229–240. 109–124. Smit NJ, van As JG, Basson L. 2002. Redescription of the female Reed CC, Basson L, van As LL, Dyková I. 2007. Four new of Gnathia africana (Crustacea, Isopoda, Gnathiidae) from myxozoans (Myxosporea: Bivalvulida) from intertidal fishes along southern Africa. Folia Parasitologica 49: 67–72. the south coast of Africa. Folia Parasitologica 54: 283–292. Smit NJ, van As JG, Davies AJ. 2003b. Taxonomic re-evaluation of Reed CC, Basson L, van As LL, Dyková I. 2009. First record of a the South African fish haemogregarine, Desseria fragilis. Journal myxozoan of the genus Sphaeromyxa Thelohan, 1892 (Myxozoa: of Parasitology 89: 151–153. Bivalvulida) from the tip of Africa. Bulletin of the European Smit NJ, van As LL, van As JG. 2005. Redescription of Argulus Association of Fish Pathologists 29: 73–76. multipocula Barnard, 1955 (Crustacea: Branchiura) collected 92 Smit and Hadfield on the west coast of South Africa. Systematic Parasitology 60: Vaughan DB, Chisholm LA. 2010b. Heterocotyle tokoloshei sp. 75–80. nov. (Monogenea: Monocotylidae) from the gills of Dasyatis Stebbing TRR. 1902. South African Crustacea. Part 2. In: Marine brevicaudata (Dasyatidae) kept in captivity at Two Oceans investigations in South Africa, vol. 2. Cape Town: Cape of Good Aquarium, Cape Town, South Africa: description and notes on Hope Department of Agriculture. pp 1–92. treatment. Acta Parasitologica 55: 108–114. Stebbing TRR. 1910. General catalogue of South African Vaughan DB, Chisholm LA. 2011. Amendment of Pseudolepto- Crustacea. Part V of S.A. Crustacea, for the marine investiga- bothrium Young, 1967 (Monogenea, Microbothriidae) with the tions in South Africa. Annals of the South African Museum 6: description of Pseudoleptobothrium christisoni sp. nov. from the 281–594, Pls 216–222. dermal denticles of Rhinobatos annulatus (Rhinobatidae) off the Utevsky AY. 2004. A new species of marine leeches (Hirudinea; southern tip of Africa. Acta Parasitologica 56: 280–289. Piscicolidae) from the coastal waters of South Africa. Vestnik Vaughan D, Chisholm L, Christison K. 2008. Overview of South Zoologii 38: 79–83. African Dendromonocotyle (Monogenea: Monocotylidae), with Utevsky AY. 2007. A new genus and species of marine fish leech descriptions of two new species from stingrays (Dasyatidae) (Annelida: Hirudinea: Piscicolidae) from South Africa. African kept in public aquaria. Zootaxa 1826: 26–44. Invertebrates 48: 41–46. Vaughan D, Christison K. 2007. Cryptocaryon irritans: food-fish for van As JG. 2015. A brief history of freshwater fish parasitology in thought. Parassitologia 49(Suppl. 2): 131. southern Africa. African Zoology 50: 93–107. Vaughan DB, Christison KW. 2010. A new species of Myxinidocotyle van As JG, Basson L. 1996. An endosymbiotic trichodinid, (Monogenea: Acanthocotylidae: Myxinidocotylinae) from captive Trichodina rhinobatae sp.n. (Ciliophora: Peritrichia) found in the sixgill hagfish, Eptatretus hexatrema (Chordata: Myxinidae), with lesser guitarfish, Rhinobatos annulatus Smith, 1814 (Rajiformes: amendment of the subfamily diagnosis. Zootaxa 2650: 47–56. Rhinobatidae) from the South African Coast. Acta Protozoologica Vaughan DB, Christison KW. 2012. Towards addressing the 35: 61–67. current state of confusion within the Hexabothriidae Price, van As JG, van As LL. 2001. Argulus izintwala n. sp. (Crustacea: 1942 (1908): Callorhynchocotyle Suriano & Incorvaia, 1982 Branchiura) from Lake St Lucia, South Africa. Systematic (Monogenea: Hexabothriidae) re-visited, with the preliminary Parasitology 48: 75–79. evaluation of novel parameters for measuring haptoral armature van As LL, van As JG, Christison KW, Cyrus DP. 2001. Argulus of hexabothriids. Zootaxa 3229: 1–34. belones Van Kampen, 1909 (Crustacea: Branchiura) found on Vaughan DB, Christison KW, Hanson H, Shinn AP. 2010. the needlefish, South Africa. Proceedings of the Microscopy Gyrodactylus eyipayipi sp. n. (Monogenea: Gyrodactylidae) from Society of Southern Africa 31: 63. Syngnathus acus L. (Syngnathidae) from South Africa. Folia van As JG, van Niekerk JP, Olivier PAS. 1999. Description of the Parasitologica 57: 11–15. previously unknown male of Argulus kosus Avenant-Oldewage, Wright RV, Lechanteur YARG, Prochazka K, Griffiths L. 2001. 1994 (Crustacea: Branchiura). Systematic Parasitology 43: Infection of hottentot Pachymetopon blochii by the fish louse 75–80. Anilocra capensis (Crustacea: Isopoda) in False Bay, South Vaughan DB, Chisholm LA. 2009. Three Dendromonocotyle species Africa. African Zoology 36: 177–183. (Monogenea: Monocotylidae) reported from captive rays, includ- Woo PTK (ed.). 2006. Fish diseases and disorders, vol. 1: ing D. lotteri sp. n. from Himantura gerrardi (Elasmobranchii: Protozoan and metazoan infections (2nd edn). Wallingford: CABI Dasyatidae) in the public aquarium at the Atlantis resort, Dubai. Publishing. Folia Parasitologica 56: 99–106. Yeld EM, Smit NJ. 2006. A new species of Trypanosoma Vaughan DB, Chisholm LA. 2010a. A new species of Neohetero- (Kinetoplastida: Trypanosomatidae) infecting catsharks from cotyle Hargis, 1955 (Monogenea: Monocotylidae) from the gills South Africa. Journal of the Marine Biological Association of the of Rhinobatos annulatus Müller & Henle (Rhinobatidae) off the United Kingdom 86: 829–833. southern tip of Africa. Systematic Parasitology 77: 205–213. Received 7 February 2015, accepted 19 April 2015 Associate Editor: Carol Simon
Journal
African Zoology
– Taylor & Francis
Published: Apr 3, 2015
Keywords: biodiversity; fish parasites; marine; South Africa
