Ichthybothrium ichthybori Khalil, 1971

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 : 6-8

Ichthybothrium ichthybori Khalil, 1971

( Figs. 3, 6, 9 , 13, 14 )

Syns: “immature Bothriocephalus ” of Woodland (1936); “unidentified ptychobothriid cestode” of Khalil (1969, 1971a).

Type host: Ichthyborus besse (Joannis) ( Characiformes : Ichthyboridae ).

Other definitive host: Ichthyborus quadrilineatus (Pellegrin) (new host).

Type locality: White Nile near Khartoum, the Sudan.

Distribution: Upper Guinea – Sierra Leone (Moa River in Mano or Pujehun); Nile basin – the Sudan (Khartoum and Kostí).

Prevalence and intensity of infection: Nile, Kostí, the Sudan; 67%, n = 6, intensity 15–35 ( Khalil 1971b); 50%, n = 4, intensity 1–8 (present study).

Type material: Holotype – incomplete worm on 2 slides ( USNPC 71666 ) and 2 paratypes – 3 worms on 3 slides ( USNPC 71667) .

Material studied: Type material ( USNPC 71666, 71667); vouchers: several slides collected by W.N.F. Woodland from I. quadrilineatus in Sierra Leone ( BMNH 1977.3.28.147–179) ; new material: 9 specimens from Kostí, the Sudan ( IPCAS C-455).

Published records: Woodland (1936); Khalil (1969, 1971a, b); Kuchta et al. (2008b).

Re-description (based on 3 mature and 6 immature worms from Kostí; measurements of holotype in brackets): Bothriocephalidea , Bothriocephalidae . Strobila up to 10.0 [4.2] cm long; maximum width 3.7 [1.5] mm. External and internal segmentation weakly developed; segments variable in shape from wider than long to longer than wide, acraspedote ( Fig. 13 ). Two pairs of longitudinal osmoregulatory canals; dorsal canals narrow (diameter up to 10); ventral canals wide (diameter up to 15), connected by transverse anastomoses. Inner longitudinal musculature weakly developed, formed by few muscle fibres. Surface of strobila uniformly covered with capilliform filitriches.

Scolex oval to lanceolate, much narrower than anterior part of strobila ( Figs. 3 , 13 ), 490–630 [495] long by 340–530 wide [413]. Apical disc absent. Bothria shallow, elongate, 240–360 [360] long by 140–200 [186] wide ( Fig. 3 ). Surface of scolex covered with capilliform filitriches; tumuliform globular structures not observed ( Fig. 6 ). Neck absent, first segments appear immediately posterior to scolex ( Fig. 13 ).

Strobila with immature segments very long, representing up to 93% [58%] of total length. Mature segments, i.e. with spermatozoa in vas deferens, of two markedly different forms (morphotypes): longer than wide (486–614 by 374–529) [749–1,187 by 564–700] with one genital complex per segment or much wider than long (315–557 by 3,370–3,745) with two or three genital complexes per segment; segment length/width ratio 1.08–1.09 [1.19–1.78] or 0.08–0.16 ( Figs. 13, 14 ). Gravid segments longer than wide (736–831 by 374–523) [1,080–1,280] or wider than long (425–621 by 2,550–3,360); segment length/width ratio 1.59–1.96 [1.50–1.74] or 0.13–0.24.

Testes medullary, oval, 37–69 [48–57] in number per proglottid (110–120 testes in segments with duplicate or triplicate proglottides), 36–50 long by 22–43 wide [77–96 by 54–69], forming 2 narrow longitudinal bands (20–36 [22–29] testes per band), confluent between segments, absent medially and near lateral margins ( Fig. 14 ). Cirrussac large, thin-walled (thickness of sac wall up to 32 [35]), spherical, 107–143 in diameter [106–135]; equatorial to pre-equatorial (at 42–50% [41–48%] of length of mature segment from anterior margin). Vas deferens forms numerous loops anterolateral to cirrus-sac, cirrus unarmed, opening into genital atrium ( Fig. 14 ). Genital pore dorsal, sub-median, pre-equatorial (at 8–12% [4–10%] of length of mature segment from anterior margin), enlarging in gravid segments ( Fig. 14 ).

Ovary asymmetrical, elongated or V-shaped, lobulate, 41–143 [131–213] long by 135–394 [186–251] wide ( Fig. 14 ). Vagina a straight, thin-walled tube, with sac-like extension in proximal part, 64–83 [44–60] long by 23– 52 [26–27] wide, opens posterior to cirrus-sac into genital atrium; vaginal sphincter absent ( Fig. 14 ). Vitelline follicles numerous, small, spherical, 10–25 [30–45] long by 17–35 [25–30] wide, cortical, form 2 wide longitudinal bands confluent between segments, separated medially, rarely connected by several follicles in postovarian region ( Fig. 14 ).

Uterine duct forms numerous tightly coiled loops, filled with eggs, enlarged in gravid segments. Uterine pore thick-walled, opens slightly posterior to midlength of uterus. Eggs oval, thin-walled, operculate, unembryonated, 38–46 [45–50] long by 27–30 [32–33] wide ( Fig. 9 ).

Remarks: This tapeworm was described by Khalil (1971b) from the Sudan and placed in a newly proposed genus Ichthybothrium Khalil, 1971 . It is characterized by a lanceolate scolex, which is narrower than the anterior end of the strobila ( Figs. 3 , 13 ) and possesses shallow bothria, but no apical disc. The strobila has weakly developed segmentation and its large proportion (more than 90% in some specimens) consists of immature proglottides without genital complexes (called “pregenital region” by Khalil 1971b).

Specimens recently collected near the type locality differ markedly from the type specimens in the shape of the segments and number of genital complexes per segment, with duplication or even triplication of genital complexes (proglottides) within mature and gravid segments ( Kuchta et al. 2008b). Marked differences in the size of the worms may be influenced by crowding effect, because worms in more heavily infected hosts (intensity of infection 8–35 worms) are smaller (maximum length 6.2 cm) and consist of just a few mature and gravid segments, which are longer than wide (length/width ratio 1.08–1.96: 1) and usually contain only one genital complex ( Khalil 1971b) ( Fig. 13 ). In contrast, tapeworms from mono- or light infections are up to 10 cm long, their strobila is formed by numerous mature and gravid segments, which are much wider than long (length/width ratio 0.08–0.24: 1), and each of them contains two or even three genital complexes ( Kuchta et al. 2008b; present study) ( Fig. 14 ).

Khalil (1971b) correctly reported the cortical position of vitelline follicles in the diagnosis of I. ichthybori , but erroneously described vitelline follicles to be medullary in the diagnosis of the genus. The surface of the scolex and strobila was studied using SEM for the first time and a uniform pattern of capilliform filitriches was observed. Khalil (1971b) also reported the presence of “minute hair-like processes” on the scolex and “long hair-like processes” around the uterine pore, which may also represent capilliform filitriches ( Fig. 6 ). However, tumuliform globular structures commonly observed in many bothriocephalideans ( Kuchta et al. 2008b), including all other studied species, are missing in I. ichthybori ( Fig. 6 ).

Ichthybothrium ichthybori is a rather frequent parasite of Ichthyborus besse , with high prevalence of infection (50–67%) and a relatively high intensity of infection. However, its fish host is rare and thus only a limited number of records of this tapeworm exist in the literature. Examination of several slides with immature cestodes designated as “immature Bothriocephalus ” from Neoborus quadrilineatus (= Ichthyborus quadrilineatus ) collected by W.N.F. Woodland in Sierra Leone (BMNH 1977.3.28.147–179) ( Woodland 1936) has shown that they belong to I. ichthybori .

Figures

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.