Kirstenella gordoni ( Woodland, 1937 ) Kuchta

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 : 9-12

Kirstenella gordoni ( Woodland, 1937) Kuchta , n. comb.

( Figs. 7, 8, 10, 11 , 15–22 )

Syns: Polyonchobothrium gordoni Woodland, 1937 ; Polyoncobothrium gordoni ( Woodland, 1937) Yamaguti, 1959 ; Bothriocephalus prudhoei Tadros, 1967 ; Polyonchobothrium sp. of Fagbenro et al. (1993); Senga gordoni ( Woodland, 1937) Kuchta & Scholz, 2007 .

Type host: Heterobranchus bidorsalis Geoffroy Saint-Hilaire ( Siluriformes : Clariidae ).

Other definitive hosts: Clarias anguillaris (Linnaeus) ( Siluriformes : Clariidae ), Schilbe mystus (Linnaeus) ( Siluriformes : Schilbeidae ). Both species are considered accidental/atypical hosts – see the Remarks section.

Type locality: Waanje River near Pujehun, Sierra Leone.

Distribution: Gambia basin – Senegal (Lampsar River, Taoué River, Gambia River); Turkana basin – Ethiopia (lower Omo River) and Kenya (Lake Turkana – restricted to the northernmost freshwater region part of the lake; see Remarks); Upper Guinea – Sierra Leone (Moa River); Niger basin – Mali (Lake Debo), Nigeria (River Ogbase); Nile basin – the Sudan (White Nile, Kostí) and Uganda (Lake Victoria).

Prevalence and intensity of infection: Lake Turkana – Omo River delta, Todonyang, Kenya, 60%, n = 10; intensity 1–6 (present study); Ethiopia – Omo River, Omorate, 50%, n = 2, intensity 1 (present study); Nile basin – the Sudan, 20%, n = 5, intensity 1 (present study); Niger basin – Nigeria, 22%, n = 185 ( Fagbenro et al. 1993).

Type material: Syntypes (several slides with fragments of worms and their histological sections) ( BMNH 1965.2.24.36–45).

Material studied: Type material: several syntypes; holotype and paratypes of Polyonchobothrium gordoni from Waanje River , Sierra Leone ( BMNH 1965.2.24.36 –45) ; Bothriocephalus prudhoei ex Clarias anguillaris, Malakal , the Sudan ( BMNH 1998.10.15.6.7; RVC C. 1262) ; vouchers: Ptychobothriidae gen. sp. ex H. bidorsalis , Mali, Lake Dabo ( MNHNP bd10) ; P. clarias ex H. bidorsalis, Taoué River, Senegal ( RMCA 34695; D.T.F. Puylaert; 15.iii.1966); Polyonchobothrium sp. ex H. bidorsalis, Waanje River, Sierra Leone ( BMNH 1965.2.24.62–65; collected by W.N.F. Woodland) ; Polyonchobothrium sp. ex Schilbe mystus, Lake Victoria , Uganda ( BMNH 1957.12.30.34–38) ; new material: 1 specimen ex H. bidorsalis , White Nile in Kostí, the Sudan ( MHNG 49379 ; 26.iii.2006 ); 1 specimen from Omo River , Omorate, Ethiopia ( MHNG 63067 ; 15.iv.2006) ; 15 specimens from Omo River delta , Todonyang, Lake Turkana , Kenya ( MHNG 69955 ) ; 3 specimens from Niokolo-Koba National Park, River Gambia, Senegal collected by B. Koubková (2006; Sen 272-1) . The new material is deposited in BMNH (Nos. 2012.3.20.26–28), IPCAS (No. C-609), MHNG (Nos. 55339, 63254, 82036, 82038) USNPC (No. 105390) and ZMB (No. 7524).

Published records: Woodland (1937); Tadros (1968); Khalil (1973); Fagbenro et al. (1993).

Re-description (based on 10 whole mounts and 1 scolex observed by SEM; measurements from Woodland, 1937 in brackets): Bothriocephalidea , Bothriocephalidae . Strobila up to 10 [1.0–1.5] cm long; maximum width 875 [1,350]. External and internal segmentation present; segments wider than long, markedly craspedote, several ridges on surface of segments ( Figs. 10 , 15 ).

Two pairs of longitudinal osmoregulatory canals; dorsal canals narrow (diameter up to 7); ventral canals wide (diameter up to 14), connected by transverse anastomoses. Inner longitudinal musculature well developed, muscle fibres diffused ( Fig. 21 ). Surface of strobila covered with capilliform filitriches.

Scolex oval, narrow ( Figs. 7 , 15, 17 ), 926–1,480 (1,160 ± 168) [280–380] long by 224–419 (317 ± 65) [310– 516] wide (n = 15). Apical disc weakly developed, 230–300 (265 ± 18) wide by 74–102 (87 ± 10) long, armed with 40–42 (41 ± 1) [36–42] small hooks 16–88 (67 ± 19; n = 103) long. Hooks variable in size, arranged in two semicircles, smallest on periphery above each bothrium and increasing into middle of semicircle with largest hook 83– 88 (86 ± 3; 3) [64] long ( Figs. 8 , 16, 18 ). Bothria elongate, shallow, 757–1,355 (1,025 ± 230) long by 73–98 (84 ± 11) wide (n = 7) ( Figs. 7 , 17 ). Surface of scolex covered with capilliform filitriches and tumuliform globular structures (diameter around 1) ( Fig. 5 ). Neck absent, first segments appearing immediately posterior to scolex ( Figs. 7 , 15, 17 ).

Immature segments 112–257 (191 ± 43) long by 217–531 (340 ± 101) wide; segment length/width ratio 0.27– 0.94: 1 (n = 15) ( Fig. 15 ). Mature segments wider than long, 134–371 (242 ± 74) long by 283–998 (667 ± 201) wide; segment length/width ratio 0.23–0.66: 1 (n = 24) ( Fig. 22 ). Gravid segments wider than long, 188–573 (326 ± 97) long by 704–1,104 (869 ± 114) wide; segment length/width ratio 0.24–0.79: 1 (n = 20) ( Fig. 15 ).

Testes medullary, oval, 70–133 (86 ± 20; 10) [under 30] in number per segment, 23–51 (35 ± 9) long by 26–45 (36 ± 6) wide [69 × 44 in sections] (n = 10) in diameter, forming 2 narrow longitudinal bands, 34–72 (47 ± 11) testes per band, confluent between segments, absent medially and near lateral margins ( Fig. 22 ). Cirrus-sac large, thick-walled (thickness of sac wall 7–14), spherical, 92–161 (121 ± 21) long by 91–171 (132 ± 20) wide, length/ width ratio 0.66–1.15: 1 (n = 24), pre-equatorial to postequatorial (at 30–69% of length of mature segment from anterior margin; n = 10). Internal seminal vesicle present, Vas deferens forms numerous loops posterolateral to cirrus-sac; internal sperm ducts strongly coiled, cirrus unarmed, opening into genital atrium ( Figs. 19, 21, 22 ). Genital pore dorsal, median, pre-equatorial ( Fig. 22 ).

Ovary asymmetrical, compact, bilobed, 44–95 (70 ± 16) long by 224–455 (332 ± 7) wide (n = 16) ( Figs. 19, 22 ). Vagina a straight, thin-walled tube, 22–52 in diameter, opens posterior to cirrus-sac into genital atrium; vaginal sphincter absent ( Fig. 19 ). Vitelline follicles numerous, small, spherical, 11–17 (14 ± 2; 8) [51 × 22] in diameter, cortical, form 2 wide longitudinal bands confluent between segments, separated medially, rarely connected by several follicles in postovarian region ( Fig. 22 ).

Uterine duct forms numerous tightly coiled loops, filled with eggs, enlarged in gravid segments ( Fig. 15 ). Uterus thick-walled, median, spherical, enlarged in gravid segments, occupies 4–30% of segment surface ( Fig. 15 ). Uterine pore thick-walled, opens slightly posterior to midlength of uterus ( Figs. 19, 22 ). Eggs oval, thin-walled, operculate, unembryonated, with abopercular knob, 30–43 (38 ± 4) lo ng by 21–33 (28 ± 4) wide [47 × 31] (n = 11) ( Figs. 11 , 20 ).

Remarks: Polyonchobothrium gordoni Woodland, 1937 was described from Heterobranchus bidorsalis from Sierra Leone. Woodland (1937) mentioned similarity of his new species with Tetracampos ciliotheca Wedl, 1861 in the shape of the body (“great part of strobila tightly coiled”) and differentiated both taxa by the number and size of apical hooks.

Tadros (1967) described a new species Bothriocephalus prudhoei Tadros, 1967 based on material collected by K.N. Soliman from Clarias anguillaris in the Sudan in 1958. Only one complete specimen with several pieces of strobila was available, but the apical part of its scolex is missing. Kuchta and Scholz (2007) considered B. prudhoei to be a junior synonym of T. ciliotheca , but re-examination of the type material did not support this synonymy. In fact, strobilar morphology, including the presence of a large cirrus-sac, is identical to that of K. gordoni .

Therefore, B. prudhoei is synonymized with this species, even though B. prudhoei was not found in its type host H. bidorsalis , but in Clarias , which is considered herein to be an accidental host.

Tadros (1968) compared Polyonchobothrium gordoni with P. cylindraceum forma major Janicki, 1926 and concluded that these species were closely related and could be separated from each other by the number and size of the hooks. Kuchta & Scholz (2007) transferred P. gordoni to Senga because they considered Polyonchobothrium Diesing, 1854 to be monotypic (see Kuchta et al. 2008b). However, the present study has shown that P. gordoni differs from all species of Senga , which occur exclusively in the Indomalayan Region, in several morphological characteristics considered to be of generic importance. Therefore, the new genus, Kirstenella , is proposed to accommodate P. gordoni (see above).

No reliable record of Kirstenella gordoni has been published since the original description of the species, but new material of this tapeworm was collected by the present authors and their collaborators in Ethiopia, Kenya, Senegal and the Sudan ( Fig. 61 ). Tapeworms from H. bidorsalis from Lake Debo, Nigeria, identified as Ptychobothriidae gen. sp. (MNHNP bd10), and those from the same host from the rivers Lampsar and Taoué in Senegal (RMCA 34695), identified by Khalil (1973) as Polyonchobothrium clarias , are conspecific with K. gordoni .

Heterobranchus currently comprises 4 species and represents a sister clade to African species of the genera Clarias and Bathyclarias Jackson ( Pouyaud et al. 2009) , but only H. bidorsalis is known as the definitive host of K. gordoni . In Turkana basin, the occurrence of K. gordoni most probably reflects distribution of its host, H. bidorsalis , which is restricted to the Omo River and freshwater part of the Turkana Lake, i.e. Omo River delta and adjacent northernmost part of the lake. Interestingly, K. gordoni has not been found in any of 547 members of the genus Clarias (abundant and sympatric with H. bidorsalis ) examined in this study ( Appendix 1), further supporting the presumed narrow host specificity. Mature tapeworms morphologically indistinguishable from K. gordoni were found in the the catfish Schilbe mystus (BMNH 1957.12.30.34–38), which might represent atypical host that became infected via predation.

Figures

FIGURE 61. Distribution map of African bothriocephalideans according to existing voucher material (unconfirmed literature records not included). Ichthyological provinces are marked as follows: I. Maghreb, II. Nilo Sudan, IIa. Abyssinian subprovince, III. Upper Guinea, IV. Lower Guinea, V. Congo, VI. Quanza, VII. Zambezi, VIII. East Coast, IX. Southern province (map orig. M. Jirků; delimitation of ichthyological provinces modified from Lévêque et al. 2008).

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 15–22. Line drawings of Kirstenella gordoni (Woodland, 1937) ex Heterobranchus bidorsalis from Kenya (IPCAS C-609). 15, Complete worm. 16, Detail of hooks. 17, Scolex, dorsoventral view. 18, Complete circle of hooks. 19, Detail of genital complex of mature segment, dorsal view. 20, Egg. 21, Cross-section of gravid segment at level of cirrus-sac. 22, Mature segment, dorsal view. Abbreviations: cs, cirrus-sac; gp, genital pore; iv, internal seminal vesicle; lm, inner longitudinal muscles; ov, ovary; t, testes; up, uterine pore; ut, uterus; v, vagina; vd, vas deferens; vf, vitelline follicles; vr, viteline reservoir.