Proteocephalus synodontis Woodland, 1925

Chambrier, Alain De, Scholz, Tomáš, Mahmoud, Zuheir N., Mariaux, Jean & Jirkú, Miloslav, 2011, Tapeworms (Cestoda: Proteocephalidea) of Synodontis spp. (Siluriformes) in Africa: survey of species and their redescriptions, Zootaxa 2976, pp. 1-14 : 2-10

Proteocephalus synodontis Woodland, 1925

( Figures 1–8 , 14–33 , 36–38 )

Syns.: Crepidobothrium synodontis ( Woodland, 1925) Meggitt, 1927 ; Ophiotaenia synodontis ( Woodland, 1925) Wardle and McLeod, 1952

Type host. Synodontis schall (Bloch and Schneider, 1801) ( Siluriformes : Mochokidae ).

Additional hosts. Synodontis caudovittata Boulenger, 1901 ; Synodontis euptera Boulenger, 1901 ; Synodontis frontosa Vaillant, 1895 ; Synodontis nigrita Valenciennes in Cuvier and Valenciennes, 1840; Synodontis serrata Rüppell, 1829 (all new hosts), Synodontis batensoda Rüppell, 1832 , (?) Auchenoglanis cf. acuticeps Pappenheim, 1914 ( Siluriformes : Bagridae ) (see Remarks).

Type locality. Neighbourhoods of Khartoum, Sudan (Nile River basin).

Type material. Holotype (designated as cotype) in BMNH (1961.4.10.87–102).

Geographical distribution (see Material and Methods section for coordinates): Nile River basin, Sudanlocalities Khartoum, White Nile in Kostí, Blue Nile in Sennar, Atbarah River in Khashm El-Girba; Lake Turkana, Kenya—localities El-Molo Bay (Loiyangalani area), Kalokol (Longech village) and Omo River Delta (Todonyang) (except for Khartoum, all new geographical records).

Redescription. Based on recently collected specimens from Kenya and Sudan; measurements of specimens from different Synodontis spp. provided in TABLE 1. Proteocephalidae, Proteocephalinae. Strobila with acraspedote proglottides, up to 84 mm ( Sudan) and 94 mm (Turkana) long and 2.38 mm ( Sudan) and 2.19 mm ( Kenya) wide, consisting of 138–290 proglottides: 95–148 immature (up to appearance of spermatozoa in vas deferens), only 5–10 mature (up to appearance of eggs in uterus), 25–36 pregravid (up to appearance of hooks in oncospheres) and 44–99 gravid. Proglottides variable in shape, from much wider than long ( Figs. 24 , 29, 32 ), almost rectangular ( Figs. 21 , 30 ), to much longer than wide in some gravid proglottides ( Fig. 31 ).

Longitudinal internal musculature extraordinarily well developed, forming wide band of dense bundles of muscle fibres, occupying about one half of proglottides in cross sections ( Figs. 23 , 27, 28 ). Dorsoventral muscle fibres present ( Fig. 23 ).

Ventral osmoregulatory canals very wide, thin-walled, convoluted, with narrow secondary canals directed to ventral surface; canals medioventral to lateral bands of vitelline follicles and well visible in all proglottides ( Figs. 23, 24 , 30, 32 ). Dorsal osmoregulatory canals thin-walled, wide in immature proglottides, dorsal to anlagen of lateral bands of vitelline follicles ( Fig. 29 ); canals becoming indistinguishable in mature, pregravid and gravid proglottides ( Figs. 27, 28 ). Scolex with numerous anastomosed osmoregulatory canals present also in its apical part ( Fig. 26 ).

Scolex unarmed, wider than neck, pyramidal in shape (four-sided truncated cone), with four posterior lobes separated by deep longitudinal incisions ( Figs. 1–6 , 14, 16 , 25 ), 605–1,105 long and 585–1,310 wide, with longitudinal wrinkles in its posterior part ( Figs. 1, 2, 4, 5 , 14 ). Suckers uniloculate, deeply embedded ( Figs. 1–6 ), 200–530 in diameter, with well developed anterolateral circular musculature ( Fig. 26 ). Unicellular gland cells lining anterior margin of scolex ( Figs. 15–20 ). Apical organ present in all 32 specimens from Sudan, but absent in 13 of 15 worms from Kenya (present only in two immature specimens in Kenya, never in adult ones), highly variable in size (35– 140 long and 30–75 wide in specimens from Sudan, but only 25–35 × 20–30 in worms from Kenya) and shape, even in specimens of same size and from same hosts, from elongate, tear-shaped to spherical ( Figs. 15–20 ). Apical part of scolex with numerous gland cells ( Figs. 15, 16 , 25, 26 ); diameter of area with gland cells 150–260. Proliferative zone (measured from base of scolex to first segment) 1.1–1.3 mm long and 390–910 wide. Scolex and proliferative zone uniformly covered with short, dense papilliform filitriches ( Figs. 7, 8 ).

Testes medullary, spherical to oval, 50–75 long and 35–65 wide, numbering 95–133, usually in two layers in cross section ( Fig. 28 ), forming two fields separated medially ( Fig. 21 ), usually not reaching to uterine stem in premature and mature proglottides ( Figs. 22, 24 , 29, 32 ). Testes present also in gravid proglottides ( Figs. 30, 31 ). External vas deferens strongly coiled, occupying narrow field reaching, but never overlapping, midline of proglottis aporally ( Figs. 21 , 32 ).

Cirrus-sac pyriform, thick-walled, 170–290 long and 60–100 wide (length/width ratio = 2.5–4.1). RLCS = 13– 30%. Internal vas deferens thin-walled; ejaculatory duct thick-walled, long, forming several loops; cirrus unarmed, long, may occupy almost entire length of cirrus-sac ( Fig. 33 ). Genital pore irregularly alternating, almost equatorial, situated at 37–60% of proglottis length ( Figs. 21, 24 , 30–32 ). Genital atrium narrow, deep ( Fig. 33 ).

Ovary medullary, bilobed, compact or with small outgrowths on surface ( Fig. 32 ). OV = 52–66% (x = 61 ± 4%; n = 39; CV = 7%). Mehlis’ glands 55–135 (n = 29) in diameter, representing 4–13% of proglottis width. Vagina thick-walled, anterior (30–84%) or posterior (16–70%; n = 441) to cirrus-sac, with higher concentration of chromophilic cells in its distal part and feebly developed vaginal sphincter near genital pore ( Fig. 33 ). Vitelline follicles medullary, in two longitudinal bands on both sides of proglottis, occupying almost its total length ( Figs. 21, 24 , 29–32 ); bands interrupted at level of terminal genitalia on ventral side ( Figs. 24 , 32, 33 ), with few follicles on dorsal side ( Figs. 21 , 28 ).

Uterus medullary, with type 1 development according to de Chambrier et al. (2004), defined as follows: uterine stem present as thick longitudinal concentration of chromophilic cells along median line in immature proglottides ( Fig. 29 ). Lumen of uterus appears in last immature proglottides, gradually extending to form tubular structure ( Figs. 21, 24 ). Eggs appear simultaneously with formation of lateral, thick-walled diverticula lined with chromophilic cells. In gravid proglottides, lateral diverticula 4–16 in number on each side, occupy up to 75% of proglottis width; they open by two or three slit-like orifices ( Figs. 30, 31 ).

Eggs with membraneous outer envelope with paired lateral auricular projections ( Figs. 36–38 ), 48–53 long and 19–22 wide; embryophore thick, spherical to slightly subspherical, 20–21 long and 18–20 wide, containing granular, incomplete envelope ( Figs. 36–38 ). Oncospheres oval, 14–15 long and 10–11 wide, with six embryonic hooks 5.5–6.5 long ( Figs. 37, 38 ).

Remarks. Evaluation of extensive material of Proteocephalus synodontis recently collected from several species of Synodontis , including topotypic material from the type-host, has shown that this species is unique among African proteocephalidean cestodes, including P. membranacei redescribed below, in the possession of an extraordinarily developed inner longitudinal musculature forming a wide band of large, tightly grouped bundles of muscle fibres. The inner longitudinal musculature of P. synodontis resembles that of “pseudophyllidean” cestodes, i.e. some members of the orders Bothriocephalidea and Diphyllobothriidea ( Kuchta et al. 2008a, b).

In addition to a very well developed inner longitudinal musculature, P. synodontis can be differentiated from its African congeners by possessing testicular fields (the poral and aporal ones) well separated from each other, whereas those of P. membranacei and other African Proteocephalus spp. are confluent medially near the anterior margin of the proglottid. Proteocephalus synodontis can also be distinguished from all but one African proteocephalideans ( P. membranacei ) by the presence of two lateral, rounded projections on the eggs.

All specimens of P. synodontis from the Sudan (Nile River basin) possess a thin-walled, but well delimited apical organ with granular content. Examination of a large set of specimens from different hosts and localities in the Sudan has revealed a remarkable variation in shape and size of this apical organ. In tapeworms from Turkana, only two juvenile specimens possessed a very small, yet recognizable apical organ surrounded by numerous gland cells, whereas the apical organ was not observed in any of 13 adult specimens, the scolices of which contained only gland cells in their apical part.

Otherwise, the tapeworms from the Nile and Turkana basins were identical in all morphological features, including those specific for the species, i.e. extraordinarily developed inner longitudinal musculature, shape of the scolex and eggs, disappearance of dorsal osmoregulatory canals in mature and gravid proglottides, complete separation of testicular fields, etc. On the basis of this morphological similarity, all tapeworms are tentatively considered to be conspecific.

A comparative analysis of partial sequences of the 28S rRNA gene of 22 specimens from five Synodontis spp. from four localities in the Nile (n = 15) and Turkana (n = 7) basins has shown their identity in all but one nucleotide. Furthermore, partial sequences of the 5.8S /ITS2 genes of the same specimens showed a complete identity except for a slight difference in the number of repeats of a 2 bp microsatellite, separating specimens from the Nile (13/14 repeats) and Turkana (11 repeats) (Genbank JN005775 – JN005779 ). Both these slight, but invariable sequence differences seemingly correlate with the presence/absence of apical organ in adult tapeworms and may indicate ongoing allopatric speciation of geographically isolated populations after their relatively recent separation.

The morphological and molecular differences between specimens from the Nile and Turkana described above may reflect current separation of Turkana and the Omo River (its only permanent tributary), which form an endorheic basin. These two basins were connected repeatedly during the humid periods in the course of palaeoclimatic fluctuations of the Pleistocene. The last discontinuous connection was present 9,500–3,680 BC, during which the water level of Lake Turkana stood at an elevation about 80 m above its present surface level ( Harvey and Grove, 1982). The close relationship between Turkana and Nile is also evidenced by their biogeographical similarity ( Hopson 1982; Dgebuadze et al. 1994), including the occurrence of S. schall , the type host of P. synodontis , and S. frontosa in both drainages ( Froese and Pauly 2011).

It is possible that future studies using molecular markers suitable for a more detailed analysis of population structure, applied to larger samples, will provide evidence that both geographically distant populations of P. synodontis actually represent two separate, but morphologically similar (sibling) species.

The above-mentioned variability (supposedly intraspecific) in the shape, size and the presence/absence of an apical organ found in P. synodontis is unique among proteocephalidean cestodes, because a considerably lower variability in the size of the apical organ has been observed in other species (de Chambrier 1988, 1989a, b; de Chambrier & Vaucher 1999). In addition, the presence/absence of an apical organ even represents a species-specific character used for differentiation of proteocephalideans in other zoogeographical regions (de Chambrier et al. 1996; Scholz et al. 2007; de Chambrier & de Chambrier 2010).

Proteocephalus synodontis is a rather frequent parasite, which was found in as many as six Synodontis spp. in the Sudanian Nile, namely in S. schall (overall prevalence 28%; n = 88), S. caudovittata (75%; n = 4), S. euptera (25%; n = 4); S. frontosa (25%; n = 44), S. nigrita (21%; n = 19) and S. serrata (14%; n = 22), and in two fish hosts, namely S. schall (22%; n = 50), and S. frontosa (21%; n = 58), in Turkana, Kenya.

A tapeworm morphologically almost indistinguishable from those from Synodontis spp., but markedly larger and wider, was found in the bagrid catfish Auchenoglanis cf. acuticeps from the Blue Nile in Sennar. Partial sequences from both the 28S rRNA and 5.5S /ITS2 genes of this specimen were identical with those of all sequenced samples of P. synodontis from Synodontis spp. from the Sudan (data not shown). Therefore, this specimen from an atypical host is tentatively identified as P. synodontis but new material is necessary to confirm its regular occurrence in a bagrid definitive host.

Figures

FIGURES 1 – 13. Scanning electron micrographs of the scoleces of Proteocephalus spp. from Synodontis catfish: P. synodontis Woodland, 1925 from S. schall, Lake Turkana, Kenya (1 – 3, 7, 8) and from S. schall, Kostí, Sudan (4 – 6); P. membranacei Troncy, 1978 from S. membranacea, Lake Chad, Chad, syntype (MNHNP 1116 H; 9, 10); P. largoproglottis (= syn. of P. m e m - branacei), syntype (MNHNP 1115 H; 11 – 13). 1, 4, 9, 11. Dorsoventral view. 2, 5, 10, 13. Lateral view. 3, 6, 12. Apical view. 7, 8. Papilliform filitriches on the external rim and internal surface of suckers, respectively (see Fig. 1). Scale bars = 100 μm (1 – 6, 9, 11 – 13); 50 μm (10); 3 μm (7, 8).

FIGURES 14 – 24. Proteocephalus synodontis Woodland, 1925. 14, Holotype (BMNH 1961.4.10.87 – 102), Khartoum, Sudan, scolex, dorsoventral view. 15, 17 – 20. Apical organs. 15. Holotype, Khartoum. 17. From Synodontis schall, Girba, Sudan; 18. Immature tapeworm from Synodontis schall, Lake Turkana, Kenya; 19. From Synodontis schall, Kostí, Sudan; 20. From Synodontis caudovittata, Kostí, Sudan. 21, 24. Immature proglottides from S. caudovittata, Kostí, Sudan. 22. Holotype, immature proglottis (note median extent of testes not reaching to uterine stem). 23. Holotype, cross section of gravid proglottis. Abbreviations: ao—apical organ; cs—cirrus-sac; do—dorsal osmoregulatory canals; dv—dorsoventral muscle fibres; gc—gland cells; lm—longitudinal internal musculature; ov—ovary; sd—sperm duct (vas deferens); te—testes; ud—uterine diverticulum; uouterine orifice; ut—uterus; vc—vaginal canal; vi—vitelline follicles; vo—ventral osmoregulatory canals. Scale bars = 100 μm (14, 16, 21 – 24); 50 µm (15, 17 – 20).

FIGURES 25 – 35. Proteocephalus synodontis Woodland, 1925 from Synodontis schall, Lake Turkana, Kenya (25 – 33) and P. membranacei from S. membranacea, Lake Chad, Chad. 25. Scolex, dorsoventral view (note accumulation of gland cells in the apical region—gc). 26. Scolex, longitudinal section. 27, 28, 34, 35. Cross sections of pregravid proglottides at the level of ovary (27, 34), cirrus-sac (28) and testes (35). 29. Premature proglottis, dorsal view. 30, 31. Gravid proglottides of different shape, ventral view. 32. Pregravid proglottis, ventral view. 33. Terminal genitalia, ventral view (note vaginal sphincter—vs). Fig. 34 — syntype of P. membranacei (MNHNP 1116 H); Fig. 35 — syntype of P. largoproglottis (= syn. of P. membranacei; MNHNP 1115 H). Abbreviations: cm—circular musculature of suckers; cs—cirrus-sac; do—dorsal osmoregulatory canals; dv—dorsoventral muscle fibres; gc—gland cells; lm—longitudinal internal musculature; mg—Mehlis’ gland; od—oviduct; ov—ovary; sc—secondary osmoregulatory canals; sd—sperm duct (vas deferens); te—testes; ud—uterine diverticulum; uouterine orifice; ut—uterus; vd—vitelloduct; vi—vitelline follicles; vo—ventral osmoregulatory canals; vs—vaginal sphincter. Scale bars = 500 μm (25 – 32, 34, 35); 250 µm (33).

FIGURES 36 – 40. Eggs of Proteocephalus synodontis Woodland, 1925 from Synodontis schall, Lake Turkana, Kenya (36, 37) and S. schall, Khartoum, Sudan (38), and P. membranacei Troncy, 1978 from S. membranacea, Lake Chad, Chad (39, 40). Fig. 39 — syntype of P. membranacei (MNHNP 1116 H); Fig. 40 — syntype of P. largoproglottis (= syn. of P. membranacei; MNHNP 1115 H). Abbreviations: em—embryophore; oe—outer envelope; on—oncosphere. Scale bars = 20 µm.