Bothriocephalus acheilognathi Yamaguti, 1934

Kuchta, Roman, Burianová, Alena, Jirkú, Miloslav, Chambrier, Alain, Oros, Mikuláš, Brabec, Jan & Scholz, Tomáš, 2012, Bothriocephalidean tapeworms (Cestoda) of freshwater fish in Africa, including erection of Kirstenella n. gen. and description of Tetracampos martinae n. sp., Zootaxa 3309, pp. 1-35 : 4-6

Bothriocephalus acheilognathi Yamaguti, 1934

( Figs. 1, 2, 4 , 12 )

Syns. (only taxa reported from Africa; for other synonyms – see Pool & Chubb 1985; Pool 1987; Kuchta & Scholz 2007): Bothriocephalus (Clestobothrium) kivuensis Baer & Fain, 1958 ; Bothriocephalus aegyptiacus Ryšavý & Moravec, 1975 ; Bothriocephalus barbus Fahmy, Mandour & El-Naffar, 1978 ; Bothriocephalus sp. of Yimer (2000), Al-Bassel (2003), and Zekarias & Yimer (2007).

Type host: Acheilognathus rhombeus (Temminck & Schlegel) ( Cypriniformes : Cyprinidae ).

Other definitive hosts in Africa (for extensive list of hosts from other continents, see Dove & Fletcher 2000): Barbus altianalis Boulenger , Barbus argenteus Günther , Barbus brevipinnis Jubb , Barbus bynni (Forsskål) , Barbus mattozi Guimarães , Barbus paludinosus Peters , Barbus trimaculatus Peters , Cyprinus carpio Linnaeus , Labeobarbus aeneus (Burchell) , Labeobarbus kimberleyensis (Gilchrist & Thompson) , Labeobarbus marequensis (Smith) , Labeobarbus nedgia Rüppell ( Cypriniformes : Cyprinidae ).

Type locality: Lake Ogura , Kyoto Prefecture, Honshu, Japan (35°2'N, 135°53'E).

Distribution in Africa: Congo basin – Democratic Republic of the Congo; Incomati basin – South Africa; Limpopo basin – South Africa; Maputo basin – South Africa; Nile basin – Egypt, Ethiopia; Orange basin – South Africa.

Prevalence and intensity of infection: Precise data are not available, but this cestode seems to be rather infrequent. Despite extensive sampling, the present authors found only a single barbel infected with B. acheilognathi in Ethiopia (out of 56 barbels examined; see Appendix 1). However, Bertasso & Avenant-Oldewage (2005) found prevalence up to 90% in L. kimberleyensis from South Africa.

Type material: MPM 23780 (holotype).

Material studied: Type material: holotype (one slide of whole mount and one slide of histological sections) of B. acheilognathi ; holotype (one worm on 20 slides) of B. aegyptiacus ex B. bynni from Cairo, Egypt ( IPCAS C– 14); three syntypes (3 mounted scoleces and histological sections) of B. kivuensis ex B. altianalis from Lake Kivu , Democratic Republic of the Congo ( MHNG 40332 ) ( Fig. 12 ) ; vouchers: one specimen ex L. kimberleyensis from Vall Dam , South Africa, collected by M. Barson ( MHNG 36429 ) ; one specimen of Bothriocephalus sp. ex Hydrocynus sp. (Craciformes: Alestidae ) from Bagata, Kwilu, Democratic Republic of the Congo ( MHNG 55308 ) ; new material: three specimens ex L. nedgia from Beshelo River , near Old Bridge, Ethiopia, collected by Moges Beletew ( MHNG 55310 ) ( Figs. 1, 2, 4 ).

Published records from Africa: Baer & Fain (1958, 1960); Ryšavý & Moravec (1975); Amin (1978); Fahmy et al. (1978); Boomker et al. (1980); Brandt et al. (1981); van As et al. (1981); El-Naffar et al. (1984); Basson & van As (1993); Paperna (1996); Schulz & Schoonbee (1999); Al-Bassel (2003); Bertasso & Avenant-Oldewage (2005); Retief et al. (2006, 2007, 2009); Zekarias & Yimer (2007); Degger & Avenant-Oldewage (2009); Degger et al. (2009); Stadtlander et al. (2011).

Remarks: Up to date, six species of Bothriocephalus Rudolphi, 1808 have been reported to occur in freshwater fish in Africa, especially in barbels ( Cyprinidae : Barbinae ) ( Baer & Fain 1958; Tadros 1967; Ryšavý & Moravec 1975; Fahmy et al. 1978; Bertasso & Avenant-Oldewage 2005; Stadtlander et al. 2011). However, the present study has shown that apart from marginal occurrence of B. claviceps (see below), only one species, the Asian fish tapeworm, Bothriocephalus acheilognathi , actually parasitizes African fish. Bothriocephalus prudhoei Tadros, 1967 is invalidated (synonym of Kirstenella gordoni – see below) and three remaining species of Bothriocephalus , namely B. (Clestobothrium) kivuensis Baer & Fain, 1958 ; B. aegyptiacus Ryšavý & Moravec, 1975 ; and B. barbus Fahmy, Manour & El-Naffar, 1978 , are synonyms of B. acheilognathi (see Pool 1987; Kuchta & Scholz 2007).

Bothriocephalus acheilognathi has been introduced from its original distribution area in East Asia throughout the world ( Scholz et al. 2011b). It is a pathogen of fry of cultured fish, especially carp and other cyprinids, and has been reported to cause mortalities ( Williams & Jones 1994). Numerous bothriocephalidean tapeworms have been synonymized with B. acheilognathi , including African taxa (see Kuchta & Scholz 2007 for list of synonyms). Pool (1987) synonymized B. aegyptiacus and B. kivuensis with B. acheilognathi , whereas B. barbus was considered to be a synonym of B. acheilognathi by Kuchta & Scholz (2007). Molecular data confirm these synonymies ( Fig. 62 ).

The host spectrum of B. acheilognathi is extraordinarily wide and includes more than 200 species of unrelated fish ( Scholz et al. 2011b), with cyprinids representing the most suitable definitive hosts. In Africa, it has been recorded in 12 cyprinid species of two native genera, Barbus (7 spp.) and Labeobarbus (4 spp.), as well as in introduced Cyprinus caprio ( Stadtlander et al. 2011) . Records from the Nile basin, South Africa, as well as the Congo basin suggest that B. acheilognathi is present throughout the continent wherever suitable cyprinid hosts are available. Surprisingly, there are no records from Labeo spp., suggesting that members of this speciose pan-African cyprinid genus constituting a significant component of ichthyofauna of many African basins are not suitable hosts. Such presumed unsuitability of Labeo spp. as hosts for B. acheilognathi might be the reason of its apparent absence in basins in which cyprinids are dominated by Labeo spp. This assumption is supported by the absence of B. acheilognathi in Lake Turkana (this study, Appendix 1), where none of the examined cyprinids, i.e. 42 Labeo spp. and 11 Barbus bynni , was infected (ratio of examined fish does not reflect real ratio in the lake in which two Barbus spp. in very low densities share the lake with huge populations of two Labeo spp.).

Findings of B. acheilognathi in clariid catfish in Ethiopia, Nigeria and Zimbabwe ( Anosike et al. 1992; Yimer 2000; Moyo et al. 2009; Bichi & Yelwa 2010) may represent accidental findings due to predation, but extraordinarily high values of prevalence (up to 60%; Moyo et al. 2009) indicate that Clarias Scopoli catfish may harbour this parasite more frequently. Unfortunately, no voucher specimens of these remarkable, but suspicious findings have been preserved, which casts doubts upon correct identification of the worms found. It thus cannot be excluded that the authors misidentified Tetracampos ciliotheca Wedl, 1861 , which is a very frequent and abundant intestinal parasite of Clarias catfish in Africa (see below) and the scolex of which somewhat resembles that of B. acheilognathi , especially when hooklets on the apical disc are detached after death of worms.

Tapeworms from Tilapia sp. ( Characiformes : Cichlidae ) and Hydrocynus sp. identified as Bothriocephalus sp. ( Khalil & Thurston 1973; present study), may represent incidental infection of B. acheilognathi , but species identification could not be confirmed, because the specimen from Tilapia sp. is not available and the worm from Hydrocynus sp. is without scolex.

Bothriocephalus acheilognathi is distributed throughout Africa, but its abundance is considerably lower than in newly colonized regions, especially in Europe and North America ( García-Prieto & Osorio-Sarabia 1991; Williams & Jones 1994; Salgado-Maldonado & Pineda-López 2003). The absence of records from West Africa is probably artificial, because great majority of parasitological studies on cyprinids in this region were obviously focused solely on ectoparasitic monogeneans (see Khalil & Polling 1997).

Figures

FIGURE 62. Interrelationships of 6 African bothriocephalideans and their relatives based on Bayesian inferrence analysis of partial sequences of the large subunit rDNA (lsrDNA). Rooted phylogram with node labels showing Bayesian posterior probabilities / bootstrap support values. Newly characterized sequences are marked with an asterisk.

FIGURES 1 – 11. Scanning electron micrographs of the scoleces and the body surface. 1, 2, 4, Bothriocephalus acheilognathi Yamaguti, 1934 ex Labeobarbus nedgia from Ethiopia (MHNG 55310). 1, 2, Scolex, dorsoventral and sublateral views. 4, Surface of apical region of scolex. 3, 6, 9, Ichthybothrium ichthybori Khalil, 1971 ex Ichthyborus besse from Sudan (IPCAS C- 455). 3, Scolex, dorsoventral view. 6, Surface of apical region of scolex. 9, Detail of operculum of egg. 5, 7, 8, 10, 11, Kirstenella gordoni (Woodland, 1937) ex Heterobranchus bidorsalis from Kenya (IPCAS C- 609). 5, Surface of apical region of scolex. 7, Scolex, dorsoventral view. 8, Scolex, apical view. 10, Mature segment, ventral view. 11, Detail of operculum of egg.

FIGURES 12 – 14. Line drawings. 12, Detail of genital complex of gravid segment, dorsal view, eggs not illustrated, type specimen of Bothriocephalus kivuensis Baer & Fain, 1958 (= B. acheilognathi Yamaguti, 1934) ex Barbus altianalis from Democratic Republic of the Congo (MHNG 40332). 13, 14, Ichthybothrium ichthybori Khalil, 1971 ex Ichthyborus besse from the Sudan (IPCAS C- 455). 13, Complete worm with single genital complex per segment. 14, Mature segment with double genital complexes.