Ciliophora

Smit, Nico J., Malherbe, Wynand & Hadfield, Kerry A., 2017, Alien freshwater fish parasites from South Africa: Diversity, distribution, status and the way forward, International Journal for Parasitology: Parasites and Wildlife 6 (3), pp. 386-401 : 391-392

2.1. Phylum Ciliophora

2.1.1. Ichthyophthirius multi fi liis

The ciliate I. multi fi liis, 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. multi fi liis 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. multi fi liis from the longfin eel, Anguilla mossambica Peters, 1852 , collected in the Keiskamma, South Africa (Table 1, Fig. 1A ). Other records of I. multi fi liis 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. multi fi liis 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.

2.1.2. 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.

2.1.3. 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; Ṕadua 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 (Rintam¨aki 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).

2.1.4. 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 ǪC), while the latter exhibits a wide thermal tolerance in the lower range (between 4 and 20 ǪC) (reviewed by Bastos Gomes et al., 2017). With the majority of South Africa's river and impoundment temperatures dropping down to below 20 ǪC in winter, the potential for C. piscicola to proliferate under these conditions in the wild needs to be investigated.

Figures

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).